SWIR Fluorescence Imaging In Vivo Monitoring and Evaluating Implanted M2 Macrophages in Skeletal Muscle Regeneration

Mo Chen, Yuzhou Chen, Sijia Feng, Shixian Dong, Luyi Sun, Huizhu Li, Fuchun Chen, Nguyen Thi Kim Thanh, Yunxia Li, Shiyi Chen, You Wang, Jun Chen

Engineering ›› 2024, Vol. 33 ›› Issue (2) : 283-294.

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Engineering ›› 2024, Vol. 33 ›› Issue (2) : 283-294. DOI: 10.1016/j.eng.2023.05.010
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SWIR Fluorescence Imaging In Vivo Monitoring and Evaluating Implanted M2 Macrophages in Skeletal Muscle Regeneration

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Abstract

Skeletal muscle has a robust regeneration ability that is impaired by severe injury, disease, and aging, resulting in a decline in skeletal muscle function. Therefore, improving skeletal muscle regeneration is a key challenge in treating skeletal muscle-related disorders. Owing to their significant role in tissue regeneration, implantation of M2 macrophages (M2Mø) has great potential for improving skeletal muscle regeneration. Here, we present a short-wave infrared (SWIR) fluorescence imaging technique to obtain more in vivo information for an in-depth evaluation of the skeletal muscle regeneration effect after M2Mø transplantation. SWIR fluorescence imaging was employed to track implanted M2Mø in the injured skeletal muscle of mouse models. It is found that the implanted M2Mø accumulated at the injury site for two weeks. Then, SWIR fluorescence imaging of blood vessels showed that M2Mø implantation could improve the relative perfusion ratio on day 5 (1.09 ± 0.09 vs 0.85 ± 0.05; p = 0.01) and day 9 (1.38 ± 0.16 vs 0.95 ± 0.03; p = 0.01) post-injury, as well as augment the degree of skeletal muscle regeneration on day 13 post-injury. Finally, multiple linear regression analyses determined that post-injury time and relative perfusion ratio could be used as predictive indicators to evaluate skeletal muscle regeneration. These results provide more in vivo details about M2Mø in skeletal muscle regeneration and confirm that M2Mø could promote angiogenesis and improve the degree of skeletal muscle repair, which will guide the research and development of M2Mø implantation to improve skeletal muscle regeneration.

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In vivo / Short-wave infrared / Skeletal muscle / Macrophage / Regeneration

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Mo Chen, Yuzhou Chen, Sijia Feng, Shixian Dong, Luyi Sun, Huizhu Li, Fuchun Chen, Nguyen Thi Kim Thanh, Yunxia Li, Shiyi Chen, You Wang, Jun Chen. SWIR Fluorescence Imaging In Vivo Monitoring and Evaluating Implanted M2 Macrophages in Skeletal Muscle Regeneration. Engineering, 2024, 33(2): 283‒294 https://doi.org/10.1016/j.eng.2023.05.010

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
B.K. Pedersen, M.A. Febbraio. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol, 8 (8) (2012), pp. 457-465
[2]
M. Samandari, J. Quint, A. Rodríguez-Delarosa, I. Sinha, O. Pourquié, A. Tamayol. Bioinks and bioprinting strategies for skeletal muscle tissue engineering. Adv Mater, 34 (12) (2022), Article e2105883
[3]
N.A. Dumont, C.F. Bentzinger, M.C. Sincennes, M.A. Rudnicki. Satellite cells and skeletal muscle regeneration. Compr Physiol, 5 (3) (2015), pp. 1027-1059
[4]
B.K. Pedersen. Muscle as a secretory organ. Compr Physiol, 3 (3) (2013), pp. 1337-1362
[5]
S. Palermi, B. Massa, M. Vecchiato, F. Mazza, P. De Blasiis, A.M. Romano, et al.. Indirect structural muscle injuries of lower limb: rehabilitation and therapeutic exercise. J Funct Morphol Kinesiol, 6 (3) (2021), p. 75
[6]
T.A. Järvinen, T.L. Järvinen, M. Kääriäinen, V. Aärimaa, S. Vaittinen, H. Kalimo, et al.. Muscle injuries: optimising recovery. Best Pract Res Clin Rheumatol, 21 (2) (2007), pp. 317-331
[7]
G.J. Haas, A.J. Dunn, M. Marcinczyk, M. Talovic, M. Schwartz, R. Scheidt, et al.. Biomimetic sponges for regeneration of skeletal muscle following trauma. J Biomed Mater Res A, 107 (1) (2019), pp. 92-103
[8]
T. Namsrai, A. Parkinson, A. Chalmers, C. Lowe, M. Cook, C. Phillips, et al.. Diagnostic delay of myositis: an integrated systematic review. Orphanet J Rare Dis, 17 (1) (2022), p. 420
[9]
G. Zhang, M. Tang, X. Zhang, S. Zhou, C. Wu, J. Zhao, et al.. Effects of conventional rehabilitative and aerobic training in patients with idiopathic inflammatory myopathy. Rheumatol Immunol Res, 3 (1) (2022), pp. 23-30
[10]
D. Zhou, E.H. King, S. Rothwell, O. Krystufkova, A. Notarnicola, S. Coss, et al.. Low copy numbers of complement C4 and C4A deficiency are risk factors for myositis, its subgroups and autoantibodies. Ann Rheum Dis, 82 (2) (2022), pp. 235-245
[11]
E. Porpiglia, T. Mai, P. Kraft, C.A. Holbrook, A. de Morree, V.D. Gonzalez, et al.. Elevated CD 47 is a hallmark of dysfunctional aged muscle stem cells that can be targeted to augment regeneration. Cell Stem Cell, 29 (12) (2022), pp. 1653-1658
[12]
J.O. Brett, M. Arjona, M. Ikeda, M. Quarta, A. de Morrée, I.M. Egner, et al.. Exercise rejuvenates quiescent skeletal muscle stem cells in old mice through restoration of cyclin D1. Nat Metab, 2 (4) (2020), pp. 307-317
[13]
A.J. Cruz-Jentoft, A.A. Sayer. Sarcopenia. Lancet, 393 (10191) (2019), pp. 2636-2646
[14]
M.A. Ruehle, M.A. Li, A. Cheng, L. Krishnan, N.J. Willett, R.E. Guldberg. Decorin-supplemented collagen hydrogels for the co-delivery of bone morphogenetic protein-2 and microvascular fragments to a composite bone-muscle injury model with impaired vascularization. Acta Biomater, 93 (2019), pp. 210-221
[15]
M. Baumann, C. Gumpold, W. Mueller-Felber, B. Schoser, C. Haberler, W.N. Loescher, et al.. Pattern of myogenesis and vascular repair in early and advanced lesions of juvenile dermatomyositis. Neuromuscul Disord, 28 (12) (2018), pp. 973-985
[16]
A. Das, G.X. Huang, M.S. Bonkowski, A. Longchamp, C. Li, M.B. Schultz, et al.. Impairment of an endothelial NAD+-H2S signaling network is a reversible cause of vascular aging. Cell, 173 (1) (2018), pp. 74-89.e20
[17]
T.A. Wynn, A. Chawla, J.W. Pollard. Macrophage biology in development, homeostasis and disease. Nature, 496 (7446) (2013), pp. 445-455
[18]
M. Shang, F. Cappellesso, R. Amorim, J. Serneels, F. Virga, G. Eelen, et al.. Macrophage-derived glutamine boosts satellite cells and muscle regeneration. Nature, 587 (7835) (2020), pp. 626-631
[19]
D. Ratnayake, P.D. Nguyen, F.J. Rossello, V.C. Wimmer, J.L. Tan, L.A. Galvis, et al.. Macrophages provide a transient muscle stem cell niche via NAMPT secretion. Nature, 591 (7849) (2021), pp. 281-287
[20]
Z. Luo, B. Qi, Y. Sun, Y. Chen, J. Lin, H. Qin, et al.. Engineering bioactive M2 macrophage-polarized, anti-inflammatory, miRNA-based liposomes for functional muscle repair: from exosomal mechanisms to biomaterials. Small, 18 (34) (2022), Article e2201957
[21]
Q. Ma, N. Zhang, Y. You, J. Zhu, Z. Yu, H. Chen, et al.. CXCR4 blockade in macrophage promotes angiogenesis in ischemic hindlimb by modulating autophagy. J Mol Cell Cardiol, 169 (2022), pp. 57-70
[22]
K. Welsher, Z. Liu, S.P. Sherlock, J.T. Robinson, Z. Chen, D. Daranciang, et al.. A route to brightly fluorescent carbon nanotubes for near-infrared imaging in mice. Nat Nanotechnol, 4 (11) (2009), pp. 773-780
[23]
A.M. Smith, M.C. Mancini, S. Nie. Bioimaging: second window for in vivo imaging. Nat Nanotechnol, 4 (11) (2009), pp. 710-711
[24]
Y. Yang, J. Chen, X. Shang, Z. Feng, C. Chen, J. Lu, et al.. Visualizing the fate of intra-articular injected mesenchymal stem cells in vivo in the second near-infrared window for the effective treatment of supraspinatus tendon tears. Adv Sci, 6 (19) (2019), Article 1901018
[25]
M. Chen, S. Feng, Y. Yang, Y. Li, J. Zhang, S. Chen, et al.. Tracking the in vivo spatio-temporal patterns of neovascularization via NIR-II fluorescence imaging. Nano Res, 13 (11) (2020), pp. 3123-3129
[26]
W. Ying, P.S. Cheruku, F.W. Bazer, S.H. Safe, B. Zhou. Investigation of macrophage polarization using bone marrow derived macrophages. J Vis Exp, 76 (2013), Article 50323
[27]
Y. Kong, J. Chen, H. Fang, G. Heath, Y. Wo, W. Wang, et al.. Highly fluorescent ribonuclease-a-encapsulated lead sulfide quantum dots for ultrasensitive fluorescence in vivo imaging in the second near-infrared window. Chem Mater, 28 (9) (2016), pp. 3041-3050
[28]
M.J. Myers, D.L. Shepherd, A.J. Durr, D.S. Stanton, J.S. Mohamed, J.M. Hollander, et al.. The role of SIRT 1 in skeletal muscle function and repair of older mice. J Cachexia Sarcopenia Muscle, 10 (4) (2019), pp. 929-949
[29]
Z. Ma, M. Zhang, J. Yue, C. Alcazar, Y. Zhong, T.C. Doyle, et al.. Near-infrared IIb fluorescence imaging of vascular regeneration with dynamic tissue perfusion measurement and high spatial resolution. Adv Funct Mater, 28 (36) (2018), Article 1803417
[30]
A. Paschalis, B. Sheehan, R. Riisnaes, D.N. Rodrigues, B. Gurel, C. Bertan, et al.. Prostate-specific membrane antigen heterogeneity and DNA repair defects in prostate cancer. Eur Urol, 76 (4) (2019), pp. 469-478
[31]
T. Denize, S. Farah, A. Cimadamore, A. Flaifel, E. Walton, M.A. Sticco-Ivins, et al.. Biomarkers of angiogenesis and clinical outcomes to cabozantinib and everolimus in patients with metastatic renal cell carcinoma from the phase III METEOR trial. Clin Cancer Res, 28 (4) (2022), pp. 748-755
[32]
H. Bösmüller, V. Pfefferle, Z. Bittar, V. Scheble, M. Horger, B. Sipos, et al.. Microvessel density and angiogenesis in primary hepatic malignancies: differential expression of CD31 and VEGFR-2 in hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Pathol Res Pract, 214 (8) (2018), pp. 1136-1141
[33]
I.S. Park, C. Mahapatra, J.S. Park, K. Dashnyam, J.W. Kim, J.C. Ahn, et al.. Revascularization and limb salvage following critical limb ischemia by nanoceria-induced Ref-1/APE1-dependent angiogenesis. Biomaterials, 242 (2020), Article 119919
[34]
J. Lagrange, M.E. Worou, J.B. Michel, A. Raoul, M. Didelot, V. Muczynski, et al.. The VWF/LRP4/αVβ3-axis represents a novel pathway regulating proliferation of human vascular smooth muscle cells. Cardiovasc Res, 118 (2) (2022), pp. 622-637
[35]
C.C. Figueiredo, N.B. Pereira, L.X. Pereira, L.A.M. Oliveira, P.P. Campos, S.P. Andrade, et al.. Double immunofluorescence labeling for CD31 and CD 105 as a marker for polyether polyurethane-induced angiogenesis in mice. Histol Histopathol, 34 (3) (2019), pp. 257-264
[36]
M.J. Van Amerongen, G. Molema, J. Plantinga, H. Moorlag, M.J. van Luyn. Neovascularization and vascular markers in a foreign body reaction to subcutaneously implanted degradable biomaterial in mice. Angiogenesis, 5 (3) (2002), pp. 173-180
[37]
X. He, Y. Zhang. Protective effect of amino acids on the muscle injury of aerobics athletes after endurance exercise based on CT images. J Healthc Eng, 2022 (2022), Article 5961267
[38]
M. Kumaravel, P. Bawa, N. Murai. Magnetic resonance imaging of muscle injury in elite American football players: predictors for return to play and performance. Eur J Radiol, 108 (2018), pp. 155-164
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