Nanotechnology: A New Strategy for Lung Cancer Treatment Targeting Pro-Tumor Neutrophils

Jian Zhang, Shasha Jiang, Shilin Li, Jipeng Jiang, Jie Mei, Yandong Chen, Yongfu Ma, Yang Liu, Ying Liu

Engineering ›› 2023, Vol. 27 ›› Issue (8) : 106-126.

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Engineering ›› 2023, Vol. 27 ›› Issue (8) : 106-126. DOI: 10.1016/j.eng.2022.11.006
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Nanotechnology: A New Strategy for Lung Cancer Treatment Targeting Pro-Tumor Neutrophils

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Abstract

Primary and metastatic lung cancers are malignant lung tumors each with of which has a different pathogenesis, although both threaten patient lives. Tumor development and progression involve communication between tumor cells and the host microenvironment. Neutrophils are the most abundant immune cells in the tumor microenvironment (TME); they participate in the generation of an inflammatory milieu and influence patient survival through their anti- and pro-tumor abilities. Neutrophils can be classified into various categories according to different criteria; frequent categories include N1 antitumor neutrophils and N2 immunosuppressive neutrophils. The antitumor effects of neutrophils are reported to be mediated through a combination of reactive oxygen species, tumor necrosis factor-related apoptosis-inducing ligand, and receptor for advanced glycation end-products-cathepsin G association, as well as the regulation of the activities of other immune cells. There have also been reports that neutrophils can function as tumor promoters that contribute to lung cancer progression and metastasis by influencing processes including carcinogenesis, angiogenesis, cancer cell proliferation, and invasion ability, as well as having similar roles in the lung metastasis of other cancers. The rapid development of nanotechnology has provided new strategies for cancer treatment targeting neutrophils.

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Keywords

Lung cancer / Metastasis / Neutrophils / Tumor microenvironment / Nanotechnology

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Jian Zhang, Shasha Jiang, Shilin Li, Jipeng Jiang, Jie Mei, Yandong Chen, Yongfu Ma, Yang Liu, Ying Liu. Nanotechnology: A New Strategy for Lung Cancer Treatment Targeting Pro-Tumor Neutrophils. Engineering, 2023, 27(8): 106‒126 https://doi.org/10.1016/j.eng.2022.11.006

References

[1]
J. Jiang, J. Mei, S. Yi, C. Feng, Y. Ma, Y. Liu, et al. Tumor associated macrophage and microbe: the potential targets of tumor vaccine delivery. Adv Drug Deliv Rev, 180 (2022), Article 114046.
[2]
J. Liu, X. Feng, Z. Chen, X. Yang, Z. Shen, M. Guo, et al. The adjuvant effect of C60(OH)22 nanoparticles promoting both humoral and cellular immune responses to HCV recombinant proteins. Mater Sci Eng C Mater Biol Appl, 97 (2019), pp. 753-759.
[3]
N. Qiu, G. Wang, J. Wang, Q. Zhou, M. Guo, Y. Wang, et al. Tumor-associated macrophage and tumor-cell dually transfecting polyplexes for efficient interleukin-12 cancer gene therapy. Adv Mater, 33 (2) (2021), p. e2006189
[4]
J. Tang, Z. Chen, B. Sun, J. Dong, J. Liu, H. Zhou, et al. Polyhydroxylated fullerenols regulate macrophage for cancer adoptive immunotherapy and greatly inhibit the tumor metastasis. Nanomedicine, 12 (4) (2016), pp. 945-954.
[5]
M. Oudkerk, S. Liu, M.A. Heuvelmans, J.E. Walter, J.K. Field. Lung cancer LDCT screening and mortality reduction—evidence, pitfalls and future perspectives. Nat Rev Clin Oncol, 18 (3) (2021), pp. 135-151. DOI: 10.1038/s41571-020-00432-6
[6]
Z. Chen, Y. Liu, B. Sun, H. Li, J. Dong, L. Zhang, et al. Polyhydroxylated metallofullerenols stimulate IL-1β secretion of macrophage through TLRs/MyD88/NF-κB pathway and NLRP3 inflammasome activation. Small, 10 (12) (2014), pp. 2362-2372. DOI: 10.1002/smll.201302825
[7]
J. Giron, A. Lacout, P.Y. Marcy. Dealing with lung cancer TNM classification. J Thorac Oncol, 11 (6) (2016), pp. e77-e78.
[8]
W.D. Travis, E. Brambilla, M. Noguchi, A.G. Nicholson, K. Geisinger, Y. Yatabe, et al. Diagnosis of lung adenocarcinoma in resected specimens: implications of the 2011 International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification. Arch Pathol Lab Med, 137 (5) (2013), pp. 685-705.
[9]
T. Kirby. Young non-smoker diagnosed with lung cancer. Lancet Respir Med, 8 (2) (2020), pp. 141-142.
[10]
G.K. Aulakh. Neutrophils in the lung: “the first responders”. Cell Tissue Res, 371 (3) (2018), pp. 577-588. DOI: 10.1007/s00441-017-2748-z
[11]
S. Diem, S. Schmid, M. Krapf, L. Flatz, D. Born, W. Jochum, et al. Neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte ratio (PLR) as prognostic markers in patients with non-small cell lung cancer (NSCLC) treated with Nivolumab. Lung Cancer, 111 (2017), pp. 176-181.
[12]
L. Mezquita, E. Auclin, R. Ferrara, M. Charrier, J. Remon, D. Planchard, et al. Association of the lung immune prognostic index with immune checkpoint inhibitor outcomes in patients with advanced non-small cell lung cancer. JAMA Oncol, 4 (3) (2018), pp. 351-357. DOI: 10.1001/jamaoncol.2017.4771
[13]
G. Kichenadasse, J.O. Miners, A.A. Mangoni, A. Rowland, A.M. Hopkins, M.J. Sorich. Multiorgan immune-related adverse events during treatment with atezolizumab. J Natl Compr Canc Netw, 18 (9) (2020), pp. 1191-1199. DOI: 10.6004/jnccn.2020.7567
[14]
A.J. Wisdom, C.S. Hong, A.J. Lin, Y. Xiang, D.E. Cooper, J. Zhang, et al. Neutrophils promote tumor resistance to radiation therapy. Proc Natl Acad Sci USA, 116 (37) (2019), pp. 18584-18589. DOI: 10.1073/pnas.1901562116
[15]
Dinh HQ, Eggert T, Meyer MA, Zhu YP, Olingy CE, Llewellyn R, et al. Coexpression of CD71 and CD 117 identifies an early unipotent neutrophil progenitor population in human bone marrow. Immunity 2020 ;53(2):319-34.
[16]
Zilionis R, Engblom C, Pfirschke C, Savova V, Zemmour D, Saatcioglu HD, et al. Single-cell transcriptomics of human and mouse lung cancers reveals conserved myeloid populations across individuals and species. Immunity 2019 ;50(5):1317-34.
[17]
S. Xiong, L. Dong, L. Cheng. Neutrophils in cancer carcinogenesis and metastasis. J Hematol Oncol, 14 (1) (2021), p. 173.
[18]
W. Liang, Q. Li, N. Ferrara. Metastatic growth instructed by neutrophil-derived transferrin. Proc Natl Acad Sci USA, 115 (43) (2018), pp. 11060-11065. DOI: 10.1073/pnas.1811717115
[19]
O.E. Sørensen, N. Borregaard. Neutrophil extracellular traps—the dark side of neutrophils. J Clin Invest, 126 (5) (2016), pp. 1612-1620.
[20]
H. Huang, H. Zhang, A.E. Onuma, A. Tsung. Neutrophil elastase and neutrophil extracellular traps in the tumor microenvironment. Adv Experimental Medicine Biol, 1263 (2020), pp. 13-23
[21]
C. Jackaman, F. Tomay, L. Duong, N.B. Abdol Razak, F.J. Pixley, P. Metharom, et al. Aging and cancer: the role of macrophages and neutrophils. Ageing Res Rev, 36 (2017), pp. 105-116.
[22]
Y. Wang, R. Cai, C. Chen. The nano-bio interactions of nanomedicines: understanding the biochemical driving forces and redox reactions. Acc Chem Res, 52 (6) (2019), pp. 1507-1518. DOI: 10.1021/acs.accounts.9b00126
[23]
H. Zhou, M. Guo, J. Li, F. Qin, Y. Wang, T. Liu, et al. Hypoxia-triggered self-assembly of ultrasmall iron oxide nanoparticles to amplify the imaging signal of a tumor. J Am Chem Soc, 143 (4) (2021), pp. 1846-1853. DOI: 10.1021/jacs.0c10245
[24]
S.M. Davidson, T. Papagiannakopoulos, B.A. Olenchock, J.E. Heyman, M.A. Keibler, A. Luengo, et al. Environment impacts the metabolic dependencies of Ras-driven non-small cell lung cancer. Cell Metab, 23 (3) (2016), pp. 517-528.
[25]
S. Li, S. Xu, X. Liang, Y. Xue, J. Mei, Y. Ma, et al. Nanotechnology: breaking the current treatment limits of lung cancer. Adv Healthc Mater, 10 (12) (2021), p. e2100078
[26]
Y. Liu, C. Chen. Role of nanotechnology in HIV/AIDS vaccine development. Adv Drug Deliv Rev, 103 (2016), pp. 76-89. DOI: 10.5539/ijps.v8n2p76
[27]
Y. Liu, C. Chen, P. Qian, X. Lu, B. Sun, X. Zhang, et al. Gd-metallofullerenol nanomaterial as non-toxic breast cancer stem cell-specific inhibitor. Nat Commun, 6 (2015), p. 5988.
[28]
M. Cao, R. Cai, L. Zhao, M. Guo, L. Wang, Y. Wang, et al. Molybdenum derived from nanomaterials incorporates into molybdenum enzymes and affects their activities in vivo. Nat Nanotechnol, 16 (6) (2021), pp. 708-716. DOI: 10.1038/s41565-021-00856-w
[29]
X. Lu, Y. Zhu, R. Bai, Z. Wu, W. Qian, L. Yang, et al. Long-term pulmonary exposure to multi-walled carbon nanotubes promotes breast cancer metastatic cascades. Nat Nanotechnol, 14 (7) (2019), pp. 719-727. DOI: 10.1038/s41565-019-0472-4
[30]
H. Hosseinalizadeh, M. Mahmoodpour, Z. Razaghi Bahabadi, M.R. Hamblin, H. Mirzaei. Neutrophil mediated drug delivery for targeted glioblastoma therapy: a comprehensive review. Biomed Pharmacother, 156 (2022), Article 113841.
[31]
Y. Chen, H. Hu, S. Tan, Q. Dong, X. Fan, Y. Wang, et al. The role of neutrophil extracellular traps in cancer progression, metastasis and therapy. Exp Hematol Oncol, 11 (1) (2022), p. 99
[32]
H. Meng, W. Leong, K.W. Leong, C. Chen, Y. Zhao. Walking the line: the fate of nanomaterials at biological barriers. Biomaterials, 174 (2018), pp. 41-53.
[33]
X. Wang, M. Wang, R. Lei, S.F. Zhu, Y. Zhao, C. Chen. Chiral surface of nanoparticles determines the orientation of adsorbed transferrin and its interaction with receptors. ACS Nano, 11 (5) (2017), pp. 4606-4616. DOI: 10.1021/acsnano.7b00200
[34]
X. Lu, T. Zhu, C. Chen, Y. Liu. Right or left: the role of nanoparticles in pulmonary diseases. Int J Mol Sci, 15 (10) (2014), pp. 17577-17600. DOI: 10.3390/ijms151017577
[35]
J. Pan, Y. Xue, S. Li, L. Wang, J. Mei, D. Ni, et al. PM2.5 induces the distant metastasis of lung adenocarcinoma via promoting the stem cell properties of cancer cells. Environ Pollut, 296 (2022), Article 118718.
[36]
P. Wu, D. Yin, J. Liu, H. Zhou, M. Guo, J. Liu, et al. Cell membrane based biomimetic nanocomposites for targeted therapy of drug resistant EGFR-mutated lung cancer. Nanoscale, 11 (41) (2019), pp. 19520-19528. DOI: 10.1039/c9nr05791a
[37]
Y. Li, Y. Liu, Y. Fu, T. Wei, L. Le Guyader, G. Gao, et al. The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-β signaling pathways. Biomaterials, 33 (2) (2012), pp. 402-411. DOI: 10.1504/IJNVO.2012.046460
[38]
Y. Liu, F. Jiao, Y. Qiu, W. Li, F. Lao, G. Zhou, et al. The effect of Gd@C82(OH)22 nanoparticles on the release of Th1/Th 2 cytokines and induction of TNF-α mediated cellular immunity. Biomaterials, 30 (23-24) (2009), pp. 3934-3945.
[39]
Y. Liu, F. Jiao, Y. Qiu, W. Li, Y. Qu, C. Tian, et al. Immunostimulatory properties and enhanced TNF-α mediated cellular immunity for tumor therapy by C60(OH)20 nanoparticles. Nanotechnology, 20 (41) (2009), Article 415102. DOI: 10.1088/0957-4484/20/41/415102
[40]
M.H. Kang, S.I. Go, H.N. Song, A. Lee, S.H. Kim, J.H. Kang, et al. The prognostic impact of the neutrophil-to-lymphocyte ratio in patients with small-cell lung cancer. Br J Cancer, 111 (3) (2014), pp. 452-460. DOI: 10.1038/bjc.2014.317
[41]
J. Yee, M.D. Sadar, D.D. Sin, M. Kuzyk, L. Xing, J. Kondra, et al. Connective tissue-activating peptide III: a novel blood biomarker for early lung cancer detection. J Clin Oncol, 27 (17) (2009), pp. 2787-2792.
[42]
M. Duruisseaux, A. Martínez-Cardús, M.E. Calleja-Cervantes, S. Moran, M. Castro de Moura, V. Davalos, et al. Epigenetic prediction of response to anti-PD-1 treatment in non-small-cell lung cancer: a multicentre, retrospective analysis. Lancet. Respir Med, 6 (10) (2018), pp. 771-781.
[43]
K. Kadota, J.I. Nitadori, H. Ujiie, D.H. Buitrago, K.M. Woo, C.S. Sima, et al. Prognostic impact of immune microenvironment in lung squamous cell carcinoma: tumor-infiltrating CD10+ neutrophil/CD20+ lymphocyte ratio as an independent prognostic factor. J Thorac Oncol, 10 (9) (2015), pp. 1301-1310. DOI: 10.1097/JTO.0000000000000617
[44]
D. Xie, R. Marks, M. Zhang, G. Jiang, A. Jatoi, Y.I. Garces, et al. Nomograms predict overall survival for patients with small-cell lung cancer incorporating pretreatment peripheral blood markers. J Thorac Oncol, 10 (8) (2015), pp. 1213-1220. DOI: 10.1097/JTO.0000000000000585
[45]
M.E. Shaul, Z.G. Fridlender. Tumour-associated neutrophils in patients with cancer. Nat Rev Clin Oncol, 16 (10) (2019), pp. 601-620. DOI: 10.1038/s41571-019-0222-4
[46]
N.A. Cannon, J. Meyer, P. Iyengar, C. Ahn, K.D. Westover, H. Choy, et al. Neutrophil-lymphocyte and platelet-lymphocyte ratios as prognostic factors after stereotactic radiation therapy for early-stage non-small-cell lung cancer. J Thorac Oncol, 10 (2) (2015), pp. 280-285. DOI: 10.1097/JTO.0000000000000399
[47]
A.M. Hopkins, G. Kichenadasse, E. Garrett-Mayer, C.S. Karapetis, A. Rowland, M.J. Sorich. Development and validation of a prognostic model for patients with advanced lung cancer treated with the immune checkpoint inhibitor atezolizumab. Clin Cancer Res, 26 (13) (2020), pp. 3280-3286. DOI: 10.1158/1078-0432.ccr-19-2968
[48]
M. Jiang, W. Peng, X. Pu, B. Chen, J. Li, F. Xu, et al. Peripheral blood biomarkers associated with outcome in non-small cell lung cancer patients treated with nivolumab and durvalumab monotherapy. Front Oncol, 10 (2020), p. 913.
[49]
D. Kazandjian, Y. Gong, P. Keegan, R. Pazdur, G.M. Blumenthal. Prognostic value of the lung immune prognostic index for patients treated for metastatic non-small cell lung cancer. JAMA Oncol, 5 (10) (2019), pp. 1481-1485. DOI: 10.1001/jamaoncol.2019.1747
[50]
Y. Yao, D. Yuan, H. Liu, X. Gu, Y. Song. Pretreatment neutrophil to lymphocyte ratio is associated with response to therapy and prognosis of advanced non-small cell lung cancer patients treated with first-line platinum-based chemotherapy. Cancer Immunol Immunother, 62 (3) (2013), pp. 471-479. DOI: 10.1007/s00262-012-1347-9
[51]
B. Sun, E.D. Brooks, R. Komaki, Z. Liao, M. Jeter, M. McAleer, et al. Long-term outcomes of salvage stereotactic ablative radiotherapy for isolated lung recurrence of non-small cell lung cancer: a phase II clinical trial. J Thorac Oncol, 12 (6) (2017), pp. 983-992.
[52]
Y. Kim, C.H. Kim, H.Y. Lee, S.H. Lee, H.S. Kim, S. Lee, et al. Comprehensive clinical and genetic characterization of hyperprogression based on volumetry in advanced non-small cell lung cancer treated with immune checkpoint inhibitor. J Thorac Oncol, 14 (9) (2019), pp. 1608-1618.
[53]
A. Castello, S. Rossi, E. Mazziotti, L. Toschi, E. Lopci. Hyperprogressive disease in patients with non-small cell lung cancer treated with checkpoint inhibitors: the role of 18F-FDG PET/CT. J Nucl Med, 61 (6) (2020), pp. 821-826. DOI: 10.2967/jnumed.119.237768
[54]
S. Teramukai, T. Kitano, Y. Kishida, M. Kawahara, K. Kubota, K. Komuta, et al. Pretreatment neutrophil count as an independent prognostic factor in advanced non-small-cell lung cancer: an analysis of Japan Multinational Trial Organisation LC00-03. Eur J Cancer, 45 (11) (2009), pp. 1950-1958.
[55]
B. Li, Y. Cui, M. Diehn, R. Li. Development and validation of an individualized immune prognostic signature in early-stage nonsquamous non-small cell lung cancer. JAMA Oncol, 3 (11) (2017), pp. 1529-1537. DOI: 10.1001/jamaoncol.2017.1609
[56]
N. Pore, S. Wu, N. Standifer, M. Jure-Kunkel, R.M. de Los, Y. Shrestha, et al. Resistance to durvalumab and durvalumab plus tremelimumab is associated with functional STK11 mutations in patients with non-small cell lung cancer and is reversed by STAT3 knockdown. Cancer Discov, 11 (11) (2021), pp. 2828-2845. DOI: 10.1158/2159-8290.cd-20-1543
[57]
J. Tanizaki, K. Haratani, H. Hayashi, Y. Chiba, Y. Nakamura, K. Yonesaka, et al. Peripheral blood biomarkers associated with clinical outcome in non-small cell lung cancer patients treated with Nivolumab. J Thorac Oncol, 13 (1) (2018), pp. 97-105.
[58]
J.B. Cowland, N. Borregaard. Granulopoiesis and granules of human neutrophils. Immunol Rev, 273 (1) (2016), pp. 11-28. DOI: 10.1111/imr.12440
[59]
S.J. Galli, N. Borregaard, T.A. Wynn. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol, 12 (11) (2011), pp. 1035-1044. DOI: 10.1038/ni.2109
[60]
S.M. Lawrence, R. Corriden, V. Nizet. The ontogeny of a neutrophil: mechanisms of granulopoiesis and homeostasis. Microbiol Mol Biol Rev, 82 (1) (2018), pp. e00057-117
[61]
C. Yin, B. Heit. Armed for destruction: formation, function and trafficking of neutrophil granules. Cell Tissue Res, 371 (3) (2018), pp. 455-471. DOI: 10.1007/s00441-017-2731-8
[62]
A. Othman, M. Sekheri, J.G. Filep. Roles of neutrophil granule proteins in orchestrating inflammation and immunity. FEBS J, 289 (14) (2022), pp. 3932-3953. DOI: 10.1111/febs.15803
[63]
S. Rørvig, O. Østergaard, N.H. Heegaard, N. Borregaard. Proteome profiling of human neutrophil granule subsets, secretory vesicles, and cell membrane: correlation with transcriptome profiling of neutrophil precursors. J Leukoc Biol, 94 (4) (2013), pp. 711-721. DOI: 10.1189/jlb.1212619
[64]
S. Vols, R.V. Sionov, Z. Granot. Always look on the bright side: anti-tumor functions of neutrophils. Curr Pharm Des, 23 (32) (2017), pp. 4862-4892. DOI: 10.2174/1381612823666170704125420
[65]
N. Antonio, M.L. Bønnelykke-Behrndtz, L.C. Ward, J. Collin, I.J. Christensen, T. Steiniche, et al. The wound inflammatory response exacerbates growth of pre-neoplastic cells and progression to cancer. EMBO J, 34 (17) (2015), pp. 2219-2236. DOI: 10.15252/embj.201490147
[66]
M.G. García-Mendoza, D.R. Inman, S.M. Ponik, J.J. Jeffery, D.S. Sheerar, R.R. van Doorn, et al. Neutrophils drive accelerated tumor progression in the collagen-dense mammary tumor microenvironment. Breast Cancer Res, 18 (1) (2016), p. 49.
[67]
M. Janiszewska, D.P. Tabassum, Z. Castaño, S. Cristea, K.N. Yamamoto, N.L. Kingston, et al. Subclonal cooperation drives metastasis by modulating local and systemic immune microenvironments. Nat Cell Biol, 21 (7) (2019), pp. 879-888. DOI: 10.1038/s41556-019-0346-x
[68]
S. Khou, A. Popa, C. Luci, F. Bihl, A. Meghraoui-Kheddar, P. Bourdely, et al. Tumor-associated neutrophils dampen adaptive immunity and promote cutaneous squamous cell carcinoma development. Cancers, 12 (7) (2020), p. 1860. DOI: 10.3390/cancers12071860
[69]
J. Jablonska, S. Leschner, K. Westphal, S. Lienenklaus, S. Weiss. Neutrophils responsive to endogenous IFN-β regulate tumor angiogenesis and growth in a mouse tumor model. J Clin Invest, 120 (4) (2010), pp. 1151-1164.
[70]
J.D. Spicer, B. McDonald, J.J. Cools-Lartigue, S.C. Chow, B. Giannias, P. Kubes, et al. Neutrophils promote liver metastasis via Mac-1-mediated interactions with circulating tumor cells. Cancer Res, 72 (16) (2012), pp. 3919-3927.
[71]
S.K. Wculek, I. Malanchi. Neutrophils support lung colonization of metastasis-initiating breast cancer cells. Nature, 528 (7582) (2015), pp. 413-417. DOI: 10.1038/nature16140
[72]
A. Tyagi, S. Sharma, K. Wu, S.Y. Wu, F. Xing, Y. Liu, et al. Nicotine promotes breast cancer metastasis by stimulating N2 neutrophils and generating pre-metastatic niche in lung. Nat Commun, 12 (1) (2021), p. 474.
[73]
Xiao Y, Cong M, Li J, He D, Wu Q, Tian P, et al. Cathepsin C promotes breast cancer lung metastasis by modulating neutrophil infiltration and neutrophil extracellular trap formation. Cancer Cell 2021 ;39(3):423-37.
[74]
T. El Rayes, R. Catena, S. Lee, M. Stawowczyk, N. Joshi, C. Fischbach, et al. Lung inflammation promotes metastasis through neutrophil protease-mediated degradation of TSP-1. Proc Natl Acad Sci USA, 112 (52) (2015), pp. 16000-16005. DOI: 10.1073/pnas.1507294112
[75]
J. Faget, S. Groeneveld, G. Boivin, M. Sankar, N. Zangger, M. Garcia, et al. Neutrophils and snail orchestrate the establishment of a pro-tumor microenvironment in lung cancer. Cell Rep, 21 (11) (2017), pp. 3190-3204.
[76]
T. Jamieson, M. Clarke, C.W. Steele, M.S. Samuel, J. Neumann, A. Jung, et al. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest, 122 (9) (2012), pp. 3127-3144.
[77]
M. Kowanetz, X. Wu, J. Lee, M. Tan, T. Hagenbeek, X. Qu, et al. Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes. Proc Natl Acad Sci USA, 107 (50) (2010), pp. 21248-21255. DOI: 10.1073/pnas.1015855107
[78]
A.N. Gordon-Weeks, S.Y. Lim, A.E. Yuzhalin, K. Jones, B. Markelc, K.J. Kim, et al. Neutrophils promote hepatic metastasis growth through fibroblast growth factor 2-dependent angiogenesis in mice. Hepatology, 65 (6) (2017), pp. 1920-1935. DOI: 10.1002/hep.29088
[79]
S.B. Coffelt, K. Kersten, C.W. Doornebal, J. Weiden, K. Vrijland, C.S. Hau, et al. IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis. Nature, 522 (7556) (2015), pp. 345-348. DOI: 10.1038/nature14282
[80]
S. Tabariès, V. Ouellet, B.E. Hsu, M.G. Annis, A.A. Rose, L. Meunier, et al. Granulocytic immune infiltrates are essential for the efficient formation of breast cancer liver metastases. Breast Cancer Res, 17 (1) (2015), p. 45.
[81]
A. Forsthuber, K. Lipp, L. Andersen, S. Ebersberger, E.W. Graña-Castro, et al. CXCL 5 as regulator of neutrophil function in cutaneous melanoma. J Invest Dermatol, 139 (1) (2019), pp. 186-194.
[82]
Z. Granot, E. Henke, E.A. Comen, T.A. King, L. Norton, R. Benezra. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell, 20 (3) (2011), pp. 300-314.
[83]
M.A. López-Lago, S. Posner, V.J. Thodima, A.M. Molina, R.J. Motzer, R.S. Chaganti. Neutrophil chemokines secreted by tumor cells mount a lung antimetastatic response during renal cell carcinoma progression. Oncogene, 32 (14) (2013), pp. 1752-1760. DOI: 10.1038/onc.2012.201
[84]
Z.G. Fridlender, J. Sun, S. Kim, V. Kapoor, G. Cheng, L. Ling, et al. Polarization of tumor-associated neutrophil phenotype by TGF-β: “N1” versus “N2” TAN. Cancer Cell, 16 (3) (2009), pp. 183-194
[85]
M. Gershkovitz, Y. Caspi, T. Fainsod-Levi, B. Katz, J. Michaeli, S. Khawaled, et al. TRPM2 mediates neutrophil killing of disseminated tumor cells. Cancer Res, 78 (10) (2018), pp. 2680-2690. DOI: 10.1158/0008-5472.can-17-3614
[86]
M.A. Sanford, Y. Yan, S.E. Canfield, W. Hassan, W.A. Selleck, G. Atkinson, et al. Independent contributions of GR-1+ leukocytes and Fas/FasL interactions to induce apoptosis following interleukin-12 gene therapy in a metastatic model of prostate cancer. Hum Gene Ther, 12 (12) (2001), pp. 1485-1498. DOI: 10.1089/10430340152480221
[87]
H. Schaider, M. Oka, T. Bogenrieder, M. Nesbit, K. Satyamoorthy, C. Berking, et al. Differential response of primary and metastatic melanomas to neutrophils attracted by IL-8. Int J Cancer, 103 (3) (2003), pp. 335-343.
[88]
P. Li, M. Lu, J. Shi, L. Hua, Z. Gong, Q. Li, et al. Dual roles of neutrophils in metastatic colonization are governed by the host NK cell status. Nat Commun, 11 (1) (2020), p. 4387.
[89]
H. Läubli, O.M. Pearce, F. Schwarz, S.S. Siddiqui, L. Deng, M.A. Stanczak, et al. Engagement of myelomonocytic Siglecs by tumor-associated ligands modulates the innate immune response to cancer. Proc Natl Acad Sci USA, 111 (39) (2014), pp. 14211-14216. DOI: 10.1073/pnas.1409580111
[90]
B. Uyanik, A.R. Goloudina, A. Akbarali, B.B. Grigorash, A.V. Petukhov, S. Singhal, et al. Inhibition of the DNA damage response phosphatase PPM1D reprograms neutrophils to enhance anti-tumor immune responses. Nat Commun, 12 (1) (2021), p. 3622.
[91]
Y. Liu, C.E. O’Leary, L.S. Wang, T.R. Bhatti, N. Dai, V. Kapoor, et al. CD11b+Ly6G+ cells inhibit tumor growth by suppressing IL-17 production at early stages of tumorigenesis. Oncoimmunology, 5 (1) (2015), p. e1061175
[92]
C. Hagerling, H. Gonzalez, K. Salari, C.Y. Wang, C. Lin, I. Robles, et al. Immune effector monocyte-neutrophil cooperation induced by the primary tumor prevents metastatic progression of breast cancer. Proc Natl Acad Sci USA, 116 (43) (2019), pp. 21704-21714. DOI: 10.1073/pnas.1907660116
[93]
M. Desbois, C. Béal, M. Charrier, B. Besse, G. Meurice, N. Cagnard, et al. IL-15 superagonist RLI has potent immunostimulatory properties on NK cells: implications for antimetastatic treatment. J Immunother Cancer, 8 (1) (2020), p. e000632. DOI: 10.1136/jitc-2020-000632
[94]
S. Singhal, P.S. Bhojnagarwala, S. O’Brien, E.K. Moon, A.L. Garfall, A.S. Rao, et al. Origin and role of a subset of tumor-associated neutrophils with antigen-presenting cell features in early-stage human lung cancer. Cancer Cell, 30 (1) (2016), pp. 120-135.
[95]
D.L. Costanzo-Garvey, T. Keeley, A.J. Case, G.F. Watson, M. Alsamraae, Y. Yu, et al. Neutrophils are mediators of metastatic prostate cancer progression in bone. Cancer Immunol Immunother, 69 (6) (2020), pp. 1113-1130. DOI: 10.1007/s00262-020-02527-6
[96]
S. Raftopoulou, P. Valadez-Cosmes, Z.N. Mihalic, R. Schicho, J. Kargl.Tumor-mediated neutrophil polarization and therapeutic implications. Int J Mol Sci, 23 (6) (2022), p. 3218. DOI: 10.3390/ijms23063218
[97]
R.V. Sionov. Leveling up the controversial role of neutrophils in cancer: when the complexity becomes entangled. Cells, 10 (9) (2021), p. 2486. DOI: 10.3390/cells10092486
[98]
C.A. Dumitru, K. Moses, S. Trellakis, S. Lang, S. Brandau. Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology. Cancer Immunol Immunother, 61 (8) (2012), pp. 1155-1167. DOI: 10.1007/s00262-012-1294-5
[99]
F. Wu, J. Fan, Y. He, A. Xiong, J. Yu, Y. Li, et al. Single-cell profiling of tumor heterogeneity and the microenvironment in advanced non-small cell lung cancer. Nat Commun, 12 (1) (2021), p. 2540.
[100]
M.E. Shaul, L. Levy, J. Sun, I. Mishalian, S. Singhal, V. Kapoor, et al. Tumor-associated neutrophils display a distinct N1 profile following TGF-β modulation: a transcriptomics analysis of pro- vs. antitumor TANs. Oncoimmunology, 5 (11) (2016), p. e1232221.
[101]
I. Mishalian, R. Bayuh, L. Levy, L. Zolotarov, J. Michaeli, Z.G. Fridlender. Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol Immunother, 62 (11) (2013), pp. 1745-1756. DOI: 10.1007/s00262-013-1476-9
[102]
H. Piccard, R.J. Muschel, G. Opdenakker. On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit Rev Oncol Hematol, 82 (3) (2012), pp. 296-309.
[103]
C. Carmona-Rivera, M.J. Kaplan. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin Immunopathol, 35 (4) (2013), pp. 455-463. DOI: 10.1007/s00281-013-0375-7
[104]
Fu J, Tobin MC, Thomas LL. Neutrophil-like low-density granulocytes are elevated in patients with moderate to severe persistent asthma. Ann Allergy Asthma Immunol 2014 ;113(6):635-40.
[105]
J.Y. Sagiv, S. Voels, Z. Granot.Isolation and characterization of low- vs. high-density neutrophils in cancer. Methods Mol Biol, 1458 (2016), pp. 179-193. DOI: 10.1007/978-1-4939-3801-8_13
[106]
R. Grecian, M.K.B. Whyte, S.R. Walmsley. The role of neutrophils in cancer. Br Med Bull, 128 (1) (2018), pp. 5-14. DOI: 10.1093/bmb/ldy029
[107]
M.E. Shaul, O. Eyal, S. Guglietta, P. Aloni, A. Zlotnik, E. Forkosh, et al. Circulating neutrophil subsets in advanced lung cancer patients exhibit unique immune signature and relate to prognosis. FASEB J, 34 (3) (2020), pp. 4204-4218. DOI: 10.1096/fj.201902467r
[108]
A. Ui Mhaonaigh, A.M. Coughlan, A. Dwivedi, J. Hartnett, J. Cabral, B. Moran, et al. Low density granulocytes in ANCA vasculitis are heterogenous and hypo-responsive to anti-myeloperoxidase antibodies. Front Immunol, 10 (2019), p. 2603.
[109]
M. Hassani, P. Hellebrekers, N. Chen, C. van Aalst, S. Bongers, F. Hietbrink, et al. On the origin of low-density neutrophils. J Leukoc Biol, 107 (5) (2020), pp. 809-818. DOI: 10.1002/jlb.5hr0120-459r
[110]
J.M. Pitt, A. Marabelle, A. Eggermont, J.C. Soria, G. Kroemer, L. Zitvogel. Targeting the tumor microenvironment: removing obstruction to anticancer immune responses and immunotherapy. Ann Oncol, 27 (8) (2016), pp. 1482-1492. DOI: 10.1093/annonc/mdw168
[111]
R. Remark, C. Becker, J.E. Gomez, D. Damotte, M.C. Dieu-Nosjean, C. Sautès-Fridman, et al. The non-small cell lung cancer immune contexture. A major determinant of tumor characteristics and patient outcome. Am J Respir Crit Care Med, 191 (4) (2015), pp. 377-390.
[112]
S.H. Tay, T. Celhar, A.M. Fairhurst. Low-density neutrophils in systemic lupus erythematosus. Arthritis Rheumatol, 72 (10) (2020), pp. 1587-1595. DOI: 10.1002/art.41395
[113]
P. Valadez-Cosmes, K. Maitz, O. Kindler, S. Raftopoulou, M. Kienzl, A. Santiso, et al. Identification of novel low-density neutrophil markers through unbiased high-dimensional flow cytometry screening in non-small cell lung cancer patients. Front Immunol, 12 (2021), Article 703846.
[114]
T. Condamine, J. Mastio, D.I. Gabrilovich. Transcriptional regulation of myeloid-derived suppressor cells. J Leukoc Biol, 98 (6) (2015), pp. 913-922.
[115]
M. Dysthe, R. Parihar. Myeloid-derived suppressor cells in the tumor microenvironment. Adv Experimental Med Biol, 1224 (2020), pp. 117-140. DOI: 10.1007/978-3-030-35723-8_8
[116]
D.I. Gabrilovich. Myeloid-derived suppressor cells. Cancer Immunol Res, 5 (1) (2017), pp. 3-8.
[117]
A. Grover, E. Sanseviero, E. Timosenko, D.I. Gabrilovich. Myeloid-derived suppressor cells: a propitious road to clinic. Cancer Discov, 11 (11) (2021), pp. 2693-2706. DOI: 10.1158/2159-8290.cd-21-0764
[118]
V. Kumar, S. Patel, E. Tcyganov, D.I. Gabrilovich. The nature of myeloid-derived suppressor cells in the tumor microenvironment. Trends Immunol, 37 (3) (2016), pp. 208-220.
[119]
A.M.K. Law, F. Valdes-Mora, D. Gallego-Ortega. Myeloid-derived suppressor cells as a therapeutic target for cancer. Cells, 9 (3) (2020), p. 561. DOI: 10.3390/cells9030561
[120]
K. Movahedi, M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, A. Beschin, et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood, 111 (8) (2008), pp. 4233-4244. DOI: 10.1182/blood-2007-07-099226
[121]
S. Ostrand-Rosenberg, P. Sinha. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol, 182 (8) (2009), pp. 4499-4506. DOI: 10.4049/jimmunol.0802740
[122]
J. Pillay, T. Tak, V.M. Kamp, L. Koenderman. Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell Mol Life Sci, 70 (20) (2013), pp. 3813-3827. DOI: 10.1007/s00018-013-1286-4
[123]
F. Veglia, A. Hashimoto, H. Dweep, E. Sanseviero, A. De Leo, E. Tcyganov, et al. Analysis of classical neutrophils and polymorphonuclear myeloid-derived suppressor cells in cancer patients and tumor-bearing mice. J Exp Med, 218 (4) (2021), p. e20201803.
[124]
L. Barrera, E. Montes-Servín, J.M. Hernandez-Martinez, M. Orozco-Morales, E. Montes-Servín, D. Michel-Tello, et al. Levels of peripheral blood polymorphonuclear myeloid-derived suppressor cells and selected cytokines are potentially prognostic of disease progression for patients with non-small cell lung cancer. Cancer Immunol Immunother, 67 (9) (2018), pp. 1393-1406. DOI: 10.1007/s00262-018-2196-y
[125]
S. Solito, I. Marigo, L. Pinton, V. Damuzzo, S. Mandruzzato, V. Bronte. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann N Y Acad Sci, 1319 (2014), pp. 47-65. DOI: 10.1111/nyas.12469
[126]
J.E. Talmadge, D.I. Gabrilovich. History of myeloid-derived suppressor cells. Nat Rev Cancer, 13 (10) (2013), pp. 739-752. DOI: 10.1038/nrc3581
[127]
O. Marini, S. Costa, D. Bevilacqua, F. Calzetti, N. Tamassia, C. Spina, et al. Mature CD10+ and immature CD10- neutrophils present in G-CSF-treated donors display opposite effects on T cells. Blood, 129 (10) (2017), pp. 1343-1356. DOI: 10.1182/blood-2016-04-713206
[128]
Z. Peng, C. Liu, A.R. Victor, D.Y. Cao, L.C. Veiras, E.A. Bernstein, et al. Tumors exploit CXCR4hiCD62Llo aged neutrophils to facilitate metastatic spread. Oncoimmunology, 10 (1) (2021), p. 1870811.
[129]
C. Yang, Z. Wang, L. Li, Z. Zhang, X. Jin, P. Wu, et al. Aged neutrophils form mitochondria-dependent vital NETs to promote breast cancer lung metastasis. J Immunother Cancer, 9 (10) (2021), p. e002875. DOI: 10.1136/jitc-2021-002875
[130]
C.R. Millrud, Å. Kågedal, S. Kumlien Georén, O. Winqvist, R. Uddman, R. Razavi, et al. NET-producing CD16high CD62Ldim neutrophils migrate to tumor sites and predict improved survival in patients with HNSCC. Int J Cancer, 140 (11) (2017), pp. 2557-2567. DOI: 10.1002/ijc.30671
[131]
A. Schroeter, M.J. Roesel, T. Matsunaga, Y. Xiao, H. Zhou, S.G. Tullius. Aging affects the role of myeloid-derived suppressor cells in alloimmunity. Front Immunol, 13 (2022), Article 917972.
[132]
E. Tcyganov, J. Mastio, E. Chen, D.I. Gabrilovich. Plasticity of myeloid-derived suppressor cells in cancer. Curr Opin Immunol, 51 (2018), pp. 76-82.
[133]
S. Hegde, A.M. Leader, M. Merad. MDSC: markers, development, states, and unaddressed complexity. Immunity, 54 (5) (2021), pp. 875-884.
[134]
C. Rosales. Neutrophil: a cell with many roles in inflammation or several cell types?. Front Physiol, 9 (2018), p. 113.
[135]
J. Favaloro, T. Liyadipitiya, R. Brown, S. Yang, H. Suen, N. Woodland, et al. Myeloid derived suppressor cells are numerically, functionally and phenotypically different in patients with multiple myeloma. Leuk Lymphoma, 55 (12) (2014), pp. 2893-2900. DOI: 10.3109/10428194.2014.904511
[136]
L. Cassetta, E.S. Baekkevold, S. Brandau, A. Bujko, M.A. Cassatella, A. Dorhoi, et al. Deciphering myeloid-derived suppressor cells: isolation and markers in humans, mice and non-human primates. Cancer Immunol Immunother, 68 (4) (2019), pp. 687-697. DOI: 10.1007/s00262-019-02302-2
[137]
S.A. Kusmartsev, Y. Li, S.H. Chen.Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J Immunol, 165 (2) (2000), pp. 779-785. DOI: 10.4049/jimmunol.165.2.779
[138]
A.A. Keskinov, M.R. Shurin. Myeloid regulatory cells in tumor spreading and metastasis. Immunobiology, 220 (2) (2015), pp. 236-242.
[139]
A. Blaisdell, A. Crequer, D. Columbus, T. Daikoku, K. Mittal, S.K. Dey, et al. Neutrophils oppose uterine epithelial carcinogenesis via debridement of hypoxic tumor cells. Cancer Cell, 28 (6) (2015), pp. 785-799.
[140]
R.V. Sionov, Z.G. Fridlender, Z. Granot. The multifaceted roles neutrophils play in the tumor microenvironment. Cancer Microenviron, 8 (3) (2015), pp. 125-158. DOI: 10.1007/s12307-014-0147-5
[141]
L. Andzinski, N. Kasnitz, S. Stahnke, C.F. Wu, M. Gereke, M. von Köckritz-Blickwede, et al. Type I IFNs induce anti-tumor polarization of tumor associated neutrophils in mice and human. Int J Cancer, 138 (8) (2016), pp. 1982-1993. DOI: 10.1002/ijc.29945
[142]
B. Yan, J.J. Wei, Y. Yuan, R. Sun, D. Li, J. Luo, et al. IL-6 cooperates with G-CSF to induce protumor function of neutrophils in bone marrow by enhancing STAT3 activation. J Immunol, 190 (11) (2013), pp. 5882-5893. DOI: 10.4049/jimmunol.1201881
[143]
A. Spiegel, M.W. Brooks, S. Houshyar, F. Reinhardt, M. Ardolino, E. Fessler, et al. Neutrophils suppress intraluminal NK cell-mediated tumor cell clearance and enhance extravasation of disseminated carcinoma cells. Cancer Discov, 6 (6) (2016), pp. 630-649.
[144]
S. Hadjigol, B.A. Shah, N.M. O’Brien-Simpson. The ‘danse macabre’—neutrophils the interactive partner affecting oral cancer outcomes. Front Immunol, 13 (2022), Article 894021.
[145]
I. Mishalian, R. Bayuh, E. Eruslanov, J. Michaeli, L. Levy, L. Zolotarov, et al. Neutrophils recruit regulatory T-cells into tumors via secretion of CCL17—a new mechanism of impaired antitumor immunity. Int J Cancer, 135 (5) (2014), pp. 1178-1186. DOI: 10.1002/ijc.28770
[146]
J.M. Zou, J. Qin, Y.C. Li, Y. Wang, D. Li, Y. Shu, et al. IL-35 induces N2 phenotype of neutrophils to promote tumor growth. Oncotarget, 8 (20) (2017), pp. 33501-33514. DOI: 10.18632/oncotarget.16819
[147]
A. Schernberg, P. Blanchard, C. Chargari, E. Deutsch. Neutrophils, a candidate biomarker and target for radiation therapy?. Acta Oncol, 56 (11) (2017), pp. 1522-1530.
[148]
C. Jungnickel, L.H. Schmidt, L. Bittigkoffer, L. Wolf, A. Wolf, F. Ritzmann, et al. IL-17C mediates the recruitment of tumor-associated neutrophils and lung tumor growth. Oncogene, 36 (29) (2017), pp. 4182-4190. DOI: 10.1038/onc.2017.28
[149]
Y. Tie, F. Tang, Y.Q. Wei, X.W. Wei. Immunosuppressive cells in cancer: mechanisms and potential therapeutic targets. J Hematol Oncol, 15 (1) (2022), p. 61.
[150]
X. Yu, W. Liu, S. Chen, X. Cheng, P.A. Paez, T. Sun, et al. Immunologically programming the tumor microenvironment induces the pattern recognition receptor NLRC4-dependent antitumor immunity. J Immunother Cancer, 9 (1) (2021), p. e001595. DOI: 10.1136/jitc-2020-001595
[151]
P.H. Lizotte, A.M. Wen, M.R. Sheen, J. Fields, P. Rojanasopondist, N.F. Steinmetz, et al. In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat Nanotechnol, 11 (3) (2016), pp. 295-303. DOI: 10.1038/nnano.2015.292
[152]
R.E. Davis, S. Sharma, J. Conceição, P. Carneiro, F. Novais, P. Scott, et al. Phenotypic and functional characteristics of HLA-DR+ neutrophils in Brazilians with cutaneous leishmaniasis. J Leukoc Biol, 101 (3) (2017), pp. 739-749.
[153]
M.R. Galdiero, G. Varricchi, S. Loffredo, A. Mantovani, G. Marone. Roles of neutrophils in cancer growth and progression. J Leukoc Biol, 103 (3) (2018), pp. 457-464. DOI: 10.1002/jlb.3mr0717-292r
[154]
J.Y. Sagiv, J. Michaeli, S. Assi, I. Mishalian, H. Kisos, L. Levy, et al. Phenotypic diversity and plasticity in circulating neutrophil subpopulations in cancer. Cell Rep, 10 (4) (2015), pp. 562-573.
[155]
J. Kargl, S.E. Busch, G.H. Yang, K.H. Kim, M.L. Hanke, H.E. Metz, et al. Neutrophils dominate the immune cell composition in non-small cell lung cancer. Nat Commun, 8 (2017), p. 14381.
[156]
S. Rakoff-Nahoum. Why cancer and inflammation?. Yale J Biol Med, 79 (3-4) (2006), pp. 123-130.
[157]
A. Rojas, I. GonzÁlez, P. Araya. RAGE in cancer lung: the end of a long and winding road is in sight. Chin J Lung Cancer, 21 (9) (2018), pp. 655-657. [Chinese].
[158]
L.M. Coussens, C.L. Tinkle, D. Hanahan, Z. Werb. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell, 103 (3) (2000), pp. 481-490.
[159]
G. Bergers, R. Brekken, G. McMahon, T.H. Vu, T. Itoh, K. Tamaki, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol, 2 (10) (2000), pp. 737-744.
[160]
D. Liao, Z. Liu, W.J. Wrasidlo, Y. Luo, G. Nguyen, T. Chen, et al. Targeted therapeutic remodeling of the tumor microenvironment improves an HER-2 DNA vaccine and prevents recurrence in a murine breast cancer model. Cancer Res, 71 (17) (2011), pp. 5688-5696.
[161]
M. De Palma, D. Biziato, T.V. Petrova. Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer, 17 (8) (2017), pp. 457-474. DOI: 10.1038/nrc.2017.51
[162]
H.B. Acuff, K.J. Carter, B. Fingleton, D.L. Gorden, L.M. Matrisian. Matrix metalloproteinase-9 from bone marrow-derived cells contributes to survival but not growth of tumor cells in the lung microenvironment. Cancer Res, 66 (1) (2006), pp. 259-266.
[163]
K. Taniguchi, P. Yang, J. Jett, E. Bass, R. Meyer, Y. Wang, et al. Polymorphisms in the promoter region of the neutrophil elastase gene are associated with lung cancer development. Clin Cancer Res, 8 (4) (2002), pp. 1115-1120.
[164]
A.M. Houghton, D.M. Rzymkiewicz, H. Ji, A.D. Gregory, E.E. Egea, H.E. Metz, et al. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med, 16 (2) (2010), pp. 219-223. DOI: 10.1038/nm.2084
[165]
A.D. Saleh, H. Cheng, S.E. Martin, H. Si, P. Ormanoglu, S. Carlson, et al. Integrated genomic and functional microRNA analysis identifies miR-30-5p as a tumor suppressor and potential therapeutic nanomedicine in head and neck cancer. Clin Cancer Res, 25 (9) (2019), pp. 2860-2873. DOI: 10.1158/1078-0432.ccr-18-0716
[166]
N.K. Verma, E. Dempsey, A. Long, A. Davies, S.P. Barry, P.G. Fallon, et al. Leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction induces a novel genetic signature resulting in T-cells refractory to transforming growth factor-β signaling. J Biol Chem, 287 (32) (2012), pp. 27204-27216. DOI: 10.1074/jbc.M112.376616
[167]
M. Wislez, M. Antoine, N. Rabbe, V. Gounant, V. Poulot, A. Lavolé, et al. Neutrophils promote aerogenous spread of lung adenocarcinoma with bronchioloalveolar carcinoma features. Clin Cancer Res, 13 (12) (2007), pp. 3518-3527.
[168]
M. Wislez, N. Rabbe, J. Marchal, B. Milleron, B. Crestani, C. Mayaud, et al. Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma: role in tumor progression and death. Cancer Res, 63 (6) (2003), pp. 1405-1412.
[169]
P.A. Stewart, E.A. Welsh, R.J.C. Slebos, B. Fang, V. Izumi, M. Chambers, et al. Proteogenomic landscape of squamous cell lung cancer. Nat Commun, 10 (1) (2019), p. 3578.
[170]
J. Shen, J. Hao, Y. Chen, H. Liu, J. Wu, B. Hu, et al. Neutrophil-mediated clinical nanodrug for treatment of residual tumor after focused ultrasound ablation. J Nanobiotechnology, 19 (1) (2021), p. 345.
[171]
E.A. Akbay, S. Koyama, Y. Liu, R. Dries, L.E. Bufe, M. Silkes, et al. Interleukin-17A promotes lung tumor progression through neutrophil attraction to tumor sites and mediating resistance to PD-1 blockade. J Thorac Oncol, 12 (8) (2017), pp. 1268-1279.
[172]
Gillette MA, Satpathy S, Cao S, Dhanasekaran SM, Vasaikar SV, Krug K, et al.; CPTAC. Proteogenomic characterization reveals therapeutic vulnerabilities in lung adenocarcinoma. Cell 2020 ;182(1):200-25.
[173]
M. Perego, V.A. Tyurin, Y.Y. Tyurina, J. Yellets, T. Nacarelli, C. Lin, et al. Reactivation of dormant tumor cells by modified lipids derived from stress-activated neutrophils. Sci Transl Med, 12 (572) (2020)eabb5817
[174]
J. Chen, S. Hou, Q. Liang, W. He, R. Li, H. Wang, et al. Localized degradation of neutrophil extracellular traps by photoregulated enzyme delivery for cancer immunotherapy and metastasis suppression. ACS Nano, 16 (2) (2022), pp. 2585-2597. DOI: 10.1021/acsnano.1c09318
[175]
J. Albrengues, M.A. Shields, D. Ng, C.G. Park, A. Ambrico, M.E. Poindexter, et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science, 361 (6409) (2018)eaao4227
[176]
B.G. Zeiher, A. Artigas, J.L. Vincent, A. Dmitrienko, K. Jackson, B.T. Thompson, et al. STRIVE Study Group. Neutrophil elastase inhibition in acute lung injury: results of the STRIVE study. Crit Care Med, 32 (8) (2004), pp. 1695-1702.
[177]
E.B. Okeke, C. Louttit, C. Fry, A.H. Najafabadi, K. Han, J. Nemzek, et al. Inhibition of neutrophil elastase prevents neutrophil extracellular trap formation and rescues mice from endotoxic shock. Biomaterials, 238 (2020), Article 119836.
[178]
M. Gershkovitz, T. Fainsod-Levi, S. Khawaled, M.E. Shaul, R.V. Sionov, L. Cohen-Daniel, et al. Microenvironmental cues determine tumor cell susceptibility to neutrophil cytotoxicity. Cancer Res, 78 (17) (2018), pp. 5050-5059. DOI: 10.1158/0008-5472.can-18-0540
[179]
Y. Koga, A. Matsuzaki, A. Suminoe, H. Hattori, T. Hara. Neutrophil-derived TNF-related apoptosis-inducing ligand (TRAIL): a novel mechanism of antitumor effect by neutrophils. Cancer Res, 64 (3) (2004), pp. 1037-1043.
[180]
J.L. Markman, R.A. Porritt, D. Wakita, M.E. Lane, D. Martinon, M. Noval Rivas, et al. Loss of testosterone impairs anti-tumor neutrophil function. Nat Commun, 11 (1) (2020), p. 1613.
[181]
R.V. Sionov, T. Fainsod-Levi, T. Zelter, L. Polyansky, C.T. Pham, Z. Granot. Neutrophil cathepsin G and tumor cell RAGE facilitate neutrophil anti-tumor cytotoxicity. Oncoimmunology, 8 (9) (2019), p. e1624129. DOI: 10.1080/2162402x.2019.1624129
[182]
R.V. Sionov, C. Lamagna, Z. Granot. Recognition of tumor nidogen-1 by neutrophil C-type lectin receptors. Biomedicines, 10 (4) (2022), p. 908. DOI: 10.3390/biomedicines10040908
[183]
A. Gutiérrez-Fernández, A. Fueyo, A.R. Folgueras, C. Garabaya, C.J. Pennington, S. Pilgrim, et al. Matrix metalloproteinase-8 functions as a metastasis suppressor through modulation of tumor cell adhesion and invasion. Cancer Res, 68 (8) (2008), pp. 2755-2763.
[184]
E.B. Eruslanov, P.S. Bhojnagarwala, J.G. Quatromoni, T.L. Stephen, A. Ranganathan, C. Deshpande, et al. Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J Clin Invest, 124 (12) (2014), pp. 5466-5480.
[185]
Q. Wu, Z. He, X. Wang, Q. Zhang, Q. Wei, S. Ma, et al. Cascade enzymes within self-assembled hybrid nanogel mimicked neutrophil lysosomes for singlet oxygen elevated cancer therapy. Nat Commun, 10 (1) (2019), p. 240
[186]
H. Läubli, L. Borsig. Selectins promote tumor metastasis. Semin Cancer Biol, 20 (3) (2010), pp. 169-177.
[187]
Z. Mi, L. Guo, P. Liu, Y. Qi, Z. Feng, J. Liu, et al. “Trojan Horse” Salmonella enabling tumor homing of silver nanoparticles via neutrophil infiltration for synergistic tumor therapy and enhanced biosafety. Nano Lett, 21 (1) (2021), pp. 414-423. DOI: 10.1021/acs.nanolett.0c03811
[188]
X. Dong, D. Chu, Z. Wang. Neutrophil-mediated delivery of nanotherapeutics across blood vessel barrier. Ther Deliv, 9 (1) (2018), pp. 29-35. DOI: 10.4155/tde-2017-0081
[189]
B. McDonald, J. Spicer, B. Giannais, L. Fallavollita, P. Brodt, L.E. Ferri. Systemic inflammation increases cancer cell adhesion to hepatic sinusoids by neutrophil mediated mechanisms. Int J Cancer, 125 (6) (2009), pp. 1298-1305. DOI: 10.1002/ijc.24409
[190]
T. Kang, Q. Zhu, D. Wei, J. Feng, J. Yao, T. Jiang, et al. Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis. ACS Nano, 11 (2) (2017), pp. 1397-1411. DOI: 10.1021/acsnano.6b06477
[191]
Y. Li, Y. Yang, T. Gan, J. Zhou, F. Hu, N. Hao, et al. Extracellular RNAs from lung cancer cells activate epithelial cells and induce neutrophil extracellular traps. Int J Oncol, 55 (1) (2019), pp. 69-80. DOI: 10.3390/pr7020069
[192]
J. Lee, D. Lee, S. Lawler, Y. Kim.Role of neutrophil extracellular traps in regulation of lung cancer invasion and metastasis: structural insights from a computational model. PLoS Comput Biol, 17 (2) (2021), p. e1008257. DOI: 10.1371/journal.pcbi.1008257
[193]
J. Cools-Lartigue, J. Spicer, B. McDonald, S. Gowing, S. Chow, B. Giannias, et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest, 123 (8) (2013), pp. 3446-3458.
[194]
J. Xue, Z. Zhao, L. Zhang, L. Xue, S. Shen, Y. Wen, et al. Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat Nanotechnol, 12 (7) (2017), pp. 692-700. DOI: 10.1038/nnano.2017.54
[195]
J.E. De Larco, B.R. Wuertz, L.T. Furcht.The potential role of neutrophils in promoting the metastatic phenotype of tumors releasing interleukin-8. Clin Cancer Res, 10 (15) (2004), pp. 4895-4900.
[196]
H.C. Chen, H.C. Lin, C.Y. Liu, C.H. Wang, T. Hwang, T.T. Huang, et al. Neutrophil elastase induces IL-8 synthesis by lung epithelial cells via the mitogen-activated protein kinase pathway. J Biomed Sci, 11 (1) (2004), pp. 49-58
[197]
T. Sun, J. Gao, D. Han, H. Shi, X. Liu. Fabrication and characterization of solid lipid nano-formulation of astraxanthin against DMBA-induced breast cancer via Nrf-2-Keap1 and NF-kB and mTOR/Maf-1/PTEN pathway. Drug Deliv, 26 (1) (2019), pp. 975-988. DOI: 10.1080/10717544.2019.1667454
[198]
Z. Zheng, Y.N. Li, S. Jia, M. Zhu, L. Cao, M. Tao, et al. Lung mesenchymal stromal cells influenced by Th 2 cytokines mobilize neutrophils and facilitate metastasis by producing complement C3. Nat Commun, 12 (1) (2021), p. 6202.
[199]
H. Yin, H. Lu, Y. Xiong, L. Ye, C. Teng, X. Cao, et al. Tumor-associated neutrophil extracellular traps regulating nanocarrier-enhanced inhibition of malignant tumor growth and distant metastasis. ACS Appl Mater Interfaces, 13 (50) (2021), pp. 59683-59694. DOI: 10.1021/acsami.1c18660
[200]
N. Robichaud, S.V. del Rincon, B. Huor, T. Alain, L.A. Petruccelli, J. Hearnden, et al. Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3. Oncogene, 34 (16) (2015), pp. 2032-2042. DOI: 10.1038/onc.2014.146
[201]
L. Furic, L. Rong, O. Larsson, I.H. Koumakpayi, K. Yoshida, A. Brueschke, et al. eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc Natl Acad Sci USA, 107 (32) (2010), pp. 14134-14139. DOI: 10.1073/pnas.1005320107
[202]
J.R. Graff, B.W. Konicek, T.M. Vincent, R.L. Lynch, D. Monteith, S.N. Weir, et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest, 117 (9) (2007), pp. 2638-2648.
[203]
N. Robichaud, B.E. Hsu, R. Istomine, F. Alvarez, J. Blagih, E.H. Ma, et al. Translational control in the tumor microenvironment promotes lung metastasis: phosphorylation of eIF4E in neutrophils. Proc Natl Acad Sci USA, 115 (10) (2018), pp. E2202-E2209.
[204]
D. Chu, X. Dong, Q. Zhao, J. Gu, Z. Wang. Photosensitization priming of tumor microenvironments improves delivery of nanotherapeutics via neutrophil infiltration. Adv Mater, 29 (27) (2017), p. 1701021.
[205]
P. Li, M. Lu, J. Shi, Z. Gong, L. Hua, Q. Li, et al. Lung mesenchymal cells elicit lipid storage in neutrophils that fuel breast cancer lung metastasis. Nat Immunol, 21 (11) (2020), pp. 1444-1455. DOI: 10.1038/s41590-020-0783-5
[206]
V. Karpisheh, J. Fakkari Afjadi, M. Nabi Afjadi, M.S. Haeri, T.S. Abdpoor Sough, S. Heydarzadeh Asl, et al. Inhibition of HIF-1α/EP 4 axis by hyaluronate-trimethyl chitosan-SPION nanoparticles markedly suppresses the growth and development of cancer cells. Int J Biol Macromol, 167 ( 2021), pp. 1006-1019.
[207]
T.N. Trotter, C.W. Shuptrine, L.C. Tsao, R.D. Marek, C. Acharya, J.P. Wei, et al. IL26, a noncanonical mediator of DNA inflammatory stimulation, promotes TNBC engraftment and progression in association with neutrophils. Cancer Res, 80 (15) (2020), pp. 3088-3100. DOI: 10.1158/0008-5472.can-18-3825
[208]
A. Masjedi, A. Ahmadi, F. Atyabi, S. Farhadi, M. Irandoust, Y. Khazaei-Poul, et al. Silencing of IL-6 and STAT3 by siRNA loaded hyaluronate-N,N,N-trimethyl chitosan nanoparticles potently reduces cancer cell progression. Int J Biol Macromol, 149 (2020), pp. 487-500.
[209]
R. Jatal, S. Mendes Saraiva, C. Vázquez-Vázquez, E. Lelievre, O. Coqueret, R. López-López, et al. Sphingomyelin nanosystems decorated with TSP-1 derived peptide targeting senescent cells. Int J Pharm, 617 (2022), Article 121618.
[210]
J. Park, R.W. Wysocki, Z. Amoozgar, L. Maiorino, M.R. Fein, J. Jorns, et al. Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps. Sci Transl Med, 8 (361) (2016)361ra138
[211]
M. Demers, D.S. Krause, D. Schatzberg, K. Martinod, J.R. Voorhees, T.A. Fuchs, et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci USA, 109 (32) (2012), pp. 13076-13081. DOI: 10.1073/pnas.1200419109
[212]
J. Qin, Z. Zhang, Z. Fu, H. Ren, M. Liu, M. Qian, et al. The UDP/P2y 6 axis promotes lung metastasis of melanoma by remodeling the premetastatic niche. Cell Mol Immunol, 17 (12) (2020), pp. 1269-1271. DOI: 10.1038/s41423-020-0392-0
[213]
S.M.G. Hayat, V. Bianconi, M. Pirro, M.R. Jaafari, M. Hatamipour, A. Sahebkar. CD47: role in the immune system and application to cancer therapy. Cell Oncol, 43 (1) (2020), pp. 19-30. DOI: 10.1007/s13402-019-00469-5
[214]
S.J. Huh, S. Liang, A. Sharma, C. Dong, G.P. Robertson. Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res, 70 (14) (2010), pp. 6071-6082.
[215]
S. Muro, T. Dziubla, W. Qiu, J. Leferovich, X. Cui, E. Berk, et al. Endothelial targeting of high-affinity multivalent polymer nanocarriers directed to intercellular adhesion molecule 1. J Pharmacol Exp Ther, 317 (3) (2006), pp. 1161-1169. DOI: 10.1124/jpet.105.098970
[216]
T. Yamamoto, K. Kawada, Y. Itatani, S. Inamoto, R. Okamura, M. Iwamoto, et al. Loss of SMAD 4 promotes lung metastasis of colorectal cancer by accumulation of CCR1+ tumor-associated neutrophils through CCL15-CCR1 axis. Clin Cancer Res, 23 (3) (2017), pp. 833-844.
[217]
Y. Ito, N. Onoda, M. Kihara, A. Miya, A. Miyauchi. Prognostic significance of neutrophil-to-lymphocyte ratio in differentiated thyroid carcinoma having distant metastasis: a comparison with thyroglobulin-doubling rate and tumor volume-doubling rate. In Vivo, 35 (2) (2021), pp. 1125-1132. DOI: 10.21873/invivo.12358
[218]
D.R. Flower, A.C. North, C.E. Sansom. The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta, 1482 (1-2) (2000), pp. 9-24.
[219]
V. Volpe, Z. Raia, L. Sanguigno, D. Somma, P. Mastrovito, F. Moscato, et al. NGAL controls the metastatic potential of anaplastic thyroid carcinoma cells. J Clin Endocrinol Metab, 98 (1) (2013), pp. 228-235. DOI: 10.1210/jc.2012-2528
[220]
H.D. Jeon, Y.H. Han, J.G. Mun, D.H. Yoon, Y.G. Lee, J.Y. Kee, et al. Dehydroevodiamine inhibits lung metastasis by suppressing survival and metastatic abilities of colorectal cancer cells. Phytomedicine, 96 (2022), Article 153809.
[221]
C. Yang, W. Sun, W. Cui, X. Li, J. Yao, X. Jia, et al. Procoagulant role of neutrophil extracellular traps in patients with gastric cancer. Int J Clin Exp Pathol, 8 (11) (2015), pp. 14075-14086.
[222]
S. Bayda, M. Adeel, T. Tuccinardi, M. Cordani, F. Rizzolio. The history of nanoscience and nanotechnology: from chemical-physical applications to nanomedicine. Molecules, 25 (1) (2019), p. 112. DOI: 10.3390/molecules25010112
[223]
L. Wang, L. Yan, J. Liu, C. Chen, Y. Zhao. Quantification of nanomaterial/nanomedicine trafficking in vivo. Anal Chem, 90 (1) (2018), pp. 589-614. DOI: 10.1021/acs.analchem.7b04765
[224]
A. Ali, M. Ovais, H. Zhou, Y. Rui, C. Chen. Tailoring metal-organic frameworks-based nanozymes for bacterial theranostics. Biomaterials, 275 (2021), Article 120951.
[225]
M. Ovais, M. Guo, C. Chen. Tailoring nanomaterials for targeting tumor-associated macrophages. Adv Mater, 31 (19) (2019), p. e1808303
[226]
H. Zhou, F. Qin, C. Chen. Designing hypoxia-responsive nanotheranostic agents for tumor imaging and therapy. Adv Healthc Mater, 10 (5) (2021), p. e2001277
[227]
M. Ovais, S.K. Nethi, S. Ullah, I. Ahmad, S. Mukherjee, C. Chen. Recent advances in the analysis of nanoparticle-protein coronas. Nanomedicine, 15 (10) (2020), pp. 1037-1061. DOI: 10.2217/nnm-2019-0381
[228]
D. Chu, X. Dong, X. Shi, C. Zhang, Z. Wang. Neutrophil-based drug delivery systems. Adv Mater, 30 (22) (2018), p. e1706245
[229]
M. Ovais, S. Mukherjee, A. Pramanik, D. Das, A. Mukherjee, A. Raza, et al. Designing stimuli-responsive upconversion nanoparticles that exploit the tumor microenvironment. Adv Mater, 32 (22) (2020), p. e2000055
[230]
D. Ni, J. Lin, N. Zhang, S. Li, Y. Xue, Z. Wang, et al. Combinational application of metal-organic frameworks-based nanozyme and nucleic acid delivery in cancer therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol, 14 (3) (2022), p. e1773.
[231]
J.W. Chen, M. Querol Sans, A. Bogdanov Jr, R. Weissleder. Imaging of myeloperoxidase in mice by using novel amplifiable paramagnetic substrates. Radiology, 240 (2) (2006), pp. 473-481. DOI: 10.1148/radiol.2402050994
[232]
L. Tang, Z. Wang, Q. Mu, Z. Yu, O. Jacobson, L. Li, et al. Targeting neutrophils for enhanced cancer theranostics. Adv Mater, 32 (33) (2020), p. e2002739
[233]
L.W. Chan, M.N. Anahtar, T.H. Ong, K.E. Hern, R.R. Kunz, S.N. Bhatia. Engineering synthetic breath biomarkers for respiratory disease. Nat Nanotechnol, 15 (9) (2020), pp. 792-800. DOI: 10.1038/s41565-020-0723-4
[234]
N. Zhang, K.P. Francis, A. Prakash, D. Ansaldi. Enhanced detection of myeloperoxidase activity in deep tissues through luminescent excitation of near-infrared nanoparticles. Nat Med, 19 (4) (2013), pp. 500-505. DOI: 10.1038/nm.3110
[235]
S.Y. Liu, A.M. Yan, W.Y. Guo, Y.Y. Fang, Q.J. Dong, R.R. Li, et al. Human neutrophil elastase activated fluorescent probe for pulmonary diseases based on fluorescence resonance energy transfer using CdSe/ZnS quantum dots. ACS Nano, 14 (4) (2020), pp. 4244-4254. DOI: 10.1021/acsnano.9b09493
[236]
Y.F. Li, C. Chen. Fate and toxicity of metallic and metal-containing nanoparticles for biomedical applications. Small, 7 (21) (2011), pp. 2965-2980. DOI: 10.1002/smll.201101059
[237]
J. Li, J. Liu, C. Chen. Remote control and modulation of cellular events by plasmonic gold nanoparticles: implications and opportunities for biomedical applications. ACS Nano, 11 (3) (2017), pp. 2403-2409. DOI: 10.1021/acsnano.7b01200
[238]
Z. Chen, R. Mao, Y. Liu. Fullerenes for cancer diagnosis and therapy: preparation, biological and clinical perspectives. Curr Drug Metab, 13 (8) (2012), pp. 1035-1045. DOI: 10.2174/138920012802850128
[239]
J. Tang, R. Zhang, M. Guo, H. Zhou, Y. Zhao, Y. Liu, et al. Gd-metallofullerenol drug delivery system mediated macrophage polarization enhances the efficiency of chemotherapy. J Control Release, 320 (2020), pp. 293-303.
[240]
B. Amulic, C. Cazalet, G.L. Hayes, K.D. Metzler, A. Zychlinsky. Neutrophil function: from mechanisms to disease. Annu Rev Immunol, 30 (2012), pp. 459-489. DOI: 10.1146/annurev-immunol-020711-074942
[241]
L. Erpenbeck, M.P. Schön. Neutrophil extracellular traps: protagonists of cancer progression?. Oncogene, 36 (18) (2017), pp. 2483-2490. DOI: 10.1038/onc.2016.406
[242]
D.R. Powell, A. Huttenlocher. Neutrophils in the tumor microenvironment. Trends Immunol, 37 (1) (2016), pp. 41-52.
[243]
L.W. Treffers, I.H. Hiemstra, T.W. Kuijpers, T.K. van den Berg, H.L. Matlung. Neutrophils in cancer. Immunol Rev, 273 (1) (2016), pp. 312-328. DOI: 10.1111/imr.12444
[244]
C. De Santo, R. Arscott, S. Booth, I. Karydis, M. Jones, R. Asher, et al. Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat Immunol, 11 (11) (2010), pp. 1039-1046. DOI: 10.1038/ni.1942
[245]
P. Scapini, O. Marini, C. Tecchio, M.A. Cassatella. Human neutrophils in the saga of cellular heterogeneity: insights and open questions. Immunol Rev, 273 (1) (2016), pp. 48-60. DOI: 10.1111/imr.12448
[246]
S. Xu, C. Wang, R. Mao, X. Liang, H. Wang, Z. Lin, et al. Surface structure change properties: auto-soft bionic fibrous membrane in reducing postoperative adhesion. Bioact Mater, 12 (2021), pp. 16-29
[247]
M. Xu, C.Y. Zhang, J. Wu, H. Zhou, R. Bai, Z. Shen, et al. PEG-detachable polymeric micelles self-assembled from amphiphilic copolymers for tumor-acidity-triggered drug delivery and controlled release. ACS Appl Mater Interfaces, 11 (6) (2019), pp. 5701-5713. DOI: 10.1021/acsami.8b13059
[248]
H. Zhou, X. Hou, Y. Liu, T. Zhao, Q. Shang, J. Tang, et al. Superstable magnetic nanoparticles in conjugation with near-infrared dye as a multimodal theranostic platform. ACS Appl Mater Interfaces, 8 (7) (2016), pp. 4424-4433. DOI: 10.1021/acsami.5b11308
[249]
Z. Wang, Z. Liu, J. Mei, S. Xu, Y. Liu. The next generation therapy for lung cancer: taking medicine by inhalation. Nanotechnology, 32 (39) (2021), p. 392002. DOI: 10.1088/1361-6528/ac0e68
[250]
D. Sun, W. Gao, P. Wu, J. Liu, S. Li, S. Li, et al. A one-pot-synthesized double-layered anticoagulant hydrogel tube. Chem Res Chin Univ, 37 (5) (2021), pp. 1085-1091. DOI: 10.1007/s40242-021-1267-3
[251]
J. Wu, Z. Zhang, J. Gu, W. Zhou, X. Liang, G. Zhou, et al. Mechanism of a long-term controlled drug release system based on simple blended electrospun fibers. J Control Release, 320 (2020), pp. 337-346.
[252]
Q. Xia, N. Zhang, J. Li, H. Wang, C. Wang, Z. Zhang, et al. Dual-functional esophageal stent coating composed of paclitaxel-loaded electrospun membrane and protective film. J Biomed Nanotechnol, 15 (10) (2019), pp. 2108-2120. DOI: 10.1166/jbn.2019.2838
[253]
J. Liu, P. Wang, X. Zhang, L. Wang, D. Wang, Z. Gu, et al. Rapid degradation and high renal clearance of Cu3BiS3 nanodots for efficient cancer diagnosis and photothermal therapy in vivo. ACS Nano, 10 (4) (2016), pp. 4587-4598. DOI: 10.1021/acsnano.6b00745
[254]
Gao S, Jiang S, Qi J, Wu T, Wang W, Liu Z, et al. Neither fluorocarbons nor silicones: hydrocarbon-based water-borne healable supramolecular elastomer with unprecedent dual resistance to water and organic solvents. CCS Chemistry. In press.
[255]
Zhang C, Bai X, Chen S, Dedkova LM, Hecht SM. Local conformational constraint of firefly luciferase can affect the energy of bioluminescence and enzyme stability. CCS Chemistry. In press.
[256]
K. Hu, H. Zhou, Y. Liu, Z. Liu, J. Liu, J. Tang, et al. Hyaluronic acid functional amphipathic and redox-responsive polymer particles for the co-delivery of doxorubicin and cyclopamine to eradicate breast cancer cells and cancer stem cells. Nanoscale, 7 (18) (2015), pp. 8607-8618.
[257]
L. Wang, Y. Liu, W. Li, X. Jiang, Y. Ji, X. Wu, et al. Selective targeting of gold nanorods at the mitochondria of cancer cells: implications for cancer therapy. Nano Lett, 11 (2) (2011), pp. 772-780. DOI: 10.1021/nl103992v
[258]
J. Saleem, L. Wang, C. Chen. Carbon-based nanomaterials for cancer therapy via targeting tumor microenvironment. Adv Healthc Mater, 7 (20) (2018), p. e1800525
[259]
J. Jin, M. Guo, J. Liu, J. Liu, H. Zhou, J. Li, et al. Graphdiyne nanosheet-based drug delivery platform for photothermal/chemotherapy combination treatment of cancer. ACS Appl Mater Interfaces, 10 (10) (2018), pp. 8436-8442. DOI: 10.1021/acsami.7b17219
[260]
X. Yan, W. Lin, H. Liu, W. Pu, J. Li, P. Wu, et al. Wavelength-tunable, long lifetime, and biocompatible luminescent nanoparticles based on a vitamin E-derived material for inflammation and tumor imaging. Small, 17 (25) (2021), p. e2100045
[261]
B. Pulli, G. Wojtkiewicz, Y. Iwamoto, M. Ali, M.W. Zeller, L. Bure, et al. Molecular MR imaging of myeloperoxidase distinguishes steatosis from steatohepatitis in nonalcoholic fatty liver disease. Radiology, 284 (2) (2017), pp. 390-400. DOI: 10.1148/radiol.2017160588
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