通过使用幼年小鼠粪便进行粪便菌群移植使老龄小鼠的皮肤再生

Shoujuan Yu, Ziyang Li, Xiaoxu Zhang, Qi Zhang, Liwei Zhang, Liang Zhao, Ping Liu, Jie Guo, Juan Chen, Chengying Zhang, Xinjuan Liu, Mengyang Yu, Dekui Jin, Xiaofeng Wang, Guang Li, Yan Cao, Fazheng Ren, Ran Wang

工程(英文) ›› 2024, Vol. 42 ›› Issue (11) : 26-38.

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工程(英文) ›› 2024, Vol. 42 ›› Issue (11) : 26-38. DOI: 10.1016/j.eng.2024.08.005
研究论文

通过使用幼年小鼠粪便进行粪便菌群移植使老龄小鼠的皮肤再生

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Skin Rejuvenation in Aged Mice by Fecal Transplantation Microbiota from Young Mice Feces

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Abstract

Skin aging is an increasingly prominent topic in the context of healthy aging. During the aging process, the skin’s barrier function diminishes, its water content decreases, wrinkles begin to form, and changes occur in the gut microbiota composition. However, the relationship between gut microbiota and skin aging remains unclear. In this study, we explored skin rejuvenation in aged mice through fecal microbiota transplantation (FMT) using feces from young mice. The results demonstrated enhanced water retention, thickened stratum corneum, increased collagen content, and improved epithelial cell differentiation in aged mice following FMT. Notably, FMT particularly increased the abundance of Lactobacillus and Lactococcus in aged mice, which were nearly undetectable in untreated aged mice. Non-targeted and targeted metabolomics analyses indicated that FMT significantly elevated levels of tryptophan (Trp) and its microbiota metabolites (e.g., indole-3-lactic acid (ILA)) in the feces and serum of aged mice. Both Trp and ILA appeared to rejuvenate aged skin by activating the aryl hydrocarbon receptor (AhR) to promote epidermal cell differentiation. In conclusion, FMT from young mice rejuvenated aged skin via Trp-metabolizing bacteria (Lactobacillus and Lactococcus) and Trp-derived metabolites, suggesting that interventions targeting Trp metabolites may effectively improve skin aging.

Keywords

Skin aging / FMT / Tryptophan / Indole-3-lactic acid / AhR / Epidermal differentiation

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Shoujuan Yu, Ziyang Li, Xiaoxu Zhang. 通过使用幼年小鼠粪便进行粪便菌群移植使老龄小鼠的皮肤再生. Engineering. 2024, 42(11): 26-38 https://doi.org/10.1016/j.eng.2024.08.005

参考文献

[1]
J.M. Waller, H.I. Maibach. Age and skin structure and function, a quantitative approach (I): blood flow, pH, thickness, and ultrasound echogenicity. Skin Res Technol, 11 (4) (2005), pp. 221-235
[2]
C. López-Otín, M.A. Blasco, L. Partridge, M. Serrano, G. Kroemer. The hallmarks of aging. Cell, 153 (6) (2013), pp. 1194-1217
[3]
A.J. McLean, D.G. Le Couteur. Aging biology and geriatric clinical pharmacology. Pharmacol Rev, 56 (2) (2004), pp. 163-184
[4]
T. Gracia-Cazaña, S. González, C. Parrado, Á. Juarranz, Y. Gilaberte. Influence of the exposome on skin cancer. Actas Dermosifiliogr, 111 (6) (2020), pp. 460-470
[5]
N. Liu, H. Matsumura, T. Kato, S. Ichinose, A. Takada, T. Namiki, et al. Stem cell competition orchestrates skin homeostasis and ageing. Nature, 568 (7752) (2019), pp. 344-350
[6]
J. Koester, Y.A. Miroshnikova, S. Ghatak, C.A. Chacón-Martínez, J. Morgner, X. Li, et al. Niche stiffening compromises hair follicle stem cell potential during ageing by reducing bivalent promoter accessibility. Nat Cell Biol, 23 (7) (2021), pp. 771-781
[7]
S. Mahmoudi, E. Mancini, L. Xu, A. Moore, F. Jahanbani, K. Hebestreit, et al. Heterogeneity in old fibroblasts is linked to variability in reprogramming and wound healing. Nature, 574 (7779) (2019), pp. 553-558
[8]
A. Giangreco, M. Qin, J.E. Pintar, F.M. Watt. Epidermal stem cells are retained in vivo throughout skin aging. Aging Cell, 7 (2) (2008), pp. 250-259
[9]
J. Doles, M. Storer, L. Cozzuto, G. Roma, W.M. Keyes. Age-associated inflammation inhibits epidermal stem cell function. Genes Dev, 26 (19) (2012), pp. 2144-2153
[10]
S.A. Benitah, P.S. Welz. Circadian regulation of adult stem cell homeostasis and aging. Cell Stem Cell, 26 (6) (2020), pp. 817-831
[11]
E.H. Choi. Aging of the skin barrier. Clin Dermatol, 37 (4) (2019), pp. 336-345
[12]
H.L. Zhang, H. Sun, Y.F. Yang, Y.M. Li. Skin substitutes comprised of recombinant human collagen hydrogel promote full-thickness skin defect reconstruction. Burns, 48 (6) (2022), pp. 1523-1524
[13]
W.H. Truswell. Prescription skin care products and skin rejuvenation. Facial Plast Surg Clin North Am, 28 (1) (2020), pp. 59-65
[14]
H. Murad, M.P. Tabibian. The effect of an oral supplement containing glucosamine, amino acids, minerals, and antioxidants on cutaneous aging: a preliminary study. J Dermatolog Treat, 12 (1) (2001), pp. 47-51
[15]
S. Zhang, E. Duan. Fighting against skin aging: the way from bench to bedside. Cell Transplant, 27 (5) (2018), pp. 729-738
[16]
J.Y. Jwo, Y.T. Chang, Y.C. Huang. Effects of probiotics supplementation on skin photoaging and skin barrier function: a systematic review and meta-analysis. Photodermatol Photoimmunol Photomed, 39 (2) (2023), pp. 122-131
[17]
B. De Pessemier, L. Grine, M. Debaere, A. Maes, B. Paetzold, C. Callewaert. Gut-skin axis: current knowledge of the interrelationship between microbial dysbiosis and skin conditions. Microorganisms, 9 (2) (2021), p. 353
[18]
L. Chen, J. Li, W. Zhu, Y. Kuang, T. Liu, W. Zhang, et al. Skin and gut microbiome in psoriasis: gaining insight into the pathophysiology of it and finding novel therapeutic strategies. Front Microbiol, 11 (2020), Article 589726
[19]
Z. Fang, T. Pan, L. Li, H. Wang, J. Zhu, H. Zhang, et al. Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis. Gut Microbes, 14 (1) (2022), Article 2044723
[20]
Y. Yu, W. Wang, F. Zhang. The next generation fecal microbiota transplantation: to transplant bacteria or virome. Adv Sci, 10 (35) (2023), Article 2301097
[21]
H. Junca, D.H. Pieper, E. Medina. The emerging potential of microbiome transplantation on human health interventions. Comput Struct Biotechnol J, 20 (2022), pp. 615-627
[22]
D.L. Suskind, M.J. Brittnacher, G. Wahbeh, M.L. Shaffer, H.S. Hayden, X. Qin, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis, 21 (3) (2015), pp. 556-563
[23]
T. Vongsavath, R. Rahmani, K.M. Tun, V. Manne. The use of fecal microbiota transplant in overcoming and modulating resistance to anti-pd-1 therapy in patients with skin cancer. Cancers, 16 (3) (2024), p. 499
[24]
X. Jiang, Z. Liu, Y. Ma, L. Miao, K. Zhao, D. Wang, et al. Fecal microbiota transplantation affects the recovery of AD-skin lesions and enhances gut microbiota homeostasis. Int Immunopharmacol, 118 (2023), Article 110005
[25]
Y. Mou, Y. Du, L. Zhou, J. Yue, X. Hu, Y. Liu, et al. Gut microbiota interact with the brain through systemic chronic inflammation: implications on neuroinflammation, neurodegeneration, and aging. Front Immunol, 13 (2022), Article 796288
[26]
A. Parker, S. Romano, R. Ansorge, A. Aboelnour, G. Le Gall, G.M. Savva, et al. Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain. Microbiome, 10 (1) (2022), p. 68
[27]
J. Shin, J.R. Noh, D. Choe, N. Lee, Y. Song, S. Cho, et al. Ageing and rejuvenation models reveal changes in key microbial communities associated with healthy ageing. Microbiome, 9 (1) (2021), p. 240
[28]
M. Boehme, K.E. Guzzetta, T.F.S. Bastiaanssen, M. van de Wouw, G.M. Moloney, A. Gual-Grau, et al. Microbiota from young mice counteracts selective age-associated behavioral deficits. Nat Aging, 1 (8) (2021), pp. 666-676
[29]
J. Lee, J. d’Aigle, L. Atadja, V. Quaicoe, P. Honarpisheh, B.P. Ganesh, et al. Gut microbiota-derived short-chain fatty acids promote poststroke recovery in aged mice. Circ Res, 127 (4) (2020), pp. 453-465
[30]
K.H. Kim, Y. Chung, J.W. Huh, D.J. Park, Y. Cho, Y. Oh, et al. Gut microbiota of the young ameliorates physical fitness of the aged in mice. Microbiome, 10 (1) (2022), p. 238
[31]
W. Wei, C.C. Wong, Z. Jia, W. Liu, C. Liu, F. Ji, et al.. Parabacteroides distasonis uses dietary inulin to suppress NASH via its metabolite pentadecanoic acid. Nat Microbiol, 8 (8) (2023), pp. 1534-1548
[32]
Q. Li, H. Chan, W.X. Liu, C.A. Liu, Y. Zhou, D. Huang, et al. Carnobacterium maltaromaticum boosts intestinal vitamin D production to suppress colorectal cancer in female mice. Cancer Cell, 41 (8) (2023), pp. 1450-1465
[33]
X. Shen, R. Wang, X. Xiong, Y. Yin, Y. Cai, Z. Ma, et al. Metabolic reaction network-based recursive metabolite annotation for untargeted metabolomics. Nat Commun, 10 (1) (2019), p. 1516
[34]
J. Yu, Y. Luo, Z. Zhu, Y. Zhou, L. Sun, J. Gao, et al. A tryptophan metabolite of the skin microbiota attenuates inflammation in patients with atopic dermatitis through the aryl hydrocarbon receptor. J Allergy Clin Immunol, 143 (6) (2019), pp. 2108-2119
[35]
T. Wang, Y. Qin, J. Qiao, Y. Liu, L. Wang, X. Zhang. Overexpression of SIRT6 regulates NRF2/HO-1 and NF-κB signaling pathways to alleviate UVA-induced photoaging in skin fibroblasts. J Photochem Photobiol B, 249 (2023), Article 112801
[36]
Y. Jing, Y. Yu, F. Bai, L. Wang, D. Yang, C. Zhang, et al. Effect of fecal microbiota transplantation on neurological restoration in a spinal cord injury mouse model: involvement of brain-gut axis. Microbiome, 9 (1) (2021), p. 59
[37]
W. Li, Z. Wang, J. Cao, Y. Dong, Y. Chen. Melatonin improves skin barrier damage caused by sleep restriction through gut microbiota. J Pineal Res, 75 (1) (2023), p. 12874
[38]
Q. Zhang, G. Li, W. Zhao, X. Wang, J. He, L. Zhou, et al. Efficacy of bifidobacterium animalis subsp. lactis BL-99 in the treatment of functional dyspepsia: a randomized placebo-controlled clinical trial. Nat Commun, 15 (1) (2024), p. 227
[39]
D.H. Stones, A.M. Krachler. Against the tide: the role of bacterial adhesion in host colonization. Biochem Soc Trans, 44 (6) (2016), pp. 1571-1580
[40]
L. Wang, N. Alammar, R. Singh, J. Nanavati, Y. Song, R. Chaudhary, et al. Gut microbial dysbiosis in the irritable bowel syndrome: a systematic review and meta-analysis of case-control studies. J Acad Nutr Diet, 120 (4) (2020), pp. 565-586
[41]
H. Gill, J. Prasad. Probiotics, immunomodulation, and health benefits. Adv Exp Med Biol, 606 (2008), pp. 423-454
[42]
M. Uccello, G. Malaguarnera, F. Basile, V. D'agata, M. Malaguarnera, G. Bertino, et al. Potential role of probiotics on colorectal cancer prevention. BMC Surg, 12 (Suppl 1) (2012), p. S35
[43]
Y. Liu, K. Chen, F. Li, Z. Gu, Q. Liu, L. He, et al. Probiotic lactobacillus rhamnosus GG prevents liver fibrosis through inhibiting hepatic bile acid synthesis and enhancing bile acid excretion in mice. Hepatology, 71 (6) (2020), pp. 2050-2066
[44]
T. Levkovich, T. Poutahidis, C. Smillie, B.J. Varian, Y.M. Ibrahim, J.R. Lakritz, et al. Probiotic bacteria induce a ‘glow of health’. PLoS One, 8 (1) (2013), p. 53867
[45]
K. Hashimoto. Emerging role of the host microbiome in neuropsychiatric disorders: overview and future directions. Mol Psychiatry, 28 (9) (2023), pp. 3625-3637
[46]
H. Shinno-Hashimoto, Y. Hashimoto, Y. Wei, L. Chang, Y. Fujita, T. Ishima, et al. Abnormal composition of microbiota in the gut and skin of imiquimod-treated mice. Sci Rep, 11 (1) (2021), p. 11265
[47]
C. Xue, G. Li, Q. Zheng, X. Gu, Q. Shi, Y. Su, et al. Tryptophan metabolism in health and disease. Cell Metab, 35 (8) (2023), pp. 1304-1326
[48]
J. Yin, B. Zhang, Z. Yu, Y. Hu, H. Lv, X. Ji, et al. Ameliorative effect of dietary tryptophan on neurodegeneration and inflammation in D-galactose-induced aging mice with the potential mechanism relying on AMPK/SIRT1/PGC-1α pathway and gut microbiota. J Agric Food Chem, 69 (16) (2021), pp. 4732-4744
[49]
L. Guenin-Macé, J.D. Morel, J.M. Doisne, A. Schiavo, L. Boulet, V. Mayau, et al. Dysregulation of tryptophan catabolism at the host-skin microbiota interface in hidradenitis suppurativa. JCI Insight, 5 (20) (2020), Article 140598
[50]
Q. Zhang, Q. Zhao, T. Li, L. Lu, F. Wang, H. Zhang, et al. Lactobacillus plantarum-derived indole-3-lactic acid ameliorates colorectal tumorigenesis via epigenetic regulation of CD8+ T cell immunity. Cell Metab, 35 (6) (2023), pp. 943-960
[51]
R. Huang, F. Wu, Q. Zhou, W. Wei, J. Yue, B. Xiao, et al. Lactobacillus and intestinal diseases: mechanisms of action and clinical applications. Microbiol Res, 260 (2022), Article 127019
[52]
S. Eyerich, K. Eyerich, C. Traidl-Hoffmann, T. Biedermann. Cutaneous barriers and skin immunity: differentiating a connected network. Trends Immunol, 39 (4) (2018), pp. 315-327
[53]
C.L. Simpson, D.M. Patel, K.J. Green. Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis. Nat Rev Mol Cell Biol, 12 (9) (2011), pp. 565-580
[54]
M. Furue, A. Hashimoto-Hachiya, G. Tsuji. Aryl hydrocarbon receptor in atopic dermatitis and psoriasis. Int J Mol Sci, 20 (21) (2019), p. 5424
[55]
P. Di Meglio, J.H. Duarte, H. Ahlfors, N.D. Owens, Y. Li, F. Villanova, et al. Activation of the aryl hydrocarbon receptor dampens the severity of inflammatory skin conditions. Immunity, 40 (6) (2014), pp. 989-1001
[56]
E.H. Van den Bogaard, J.G. Bergboer, M. Vonk-Bergers, I.M. van Vlijmen-Willems, S.V. Hato, P.G. van der Valk, et al. Coal tar induces AHR-dependent skin barrier repair in atopic dermatitis. J Clin Invest, 123 (2) (2013), pp. 917-927
[57]
T. Zelante, R.G. Iannitti, C. Cunha, A. De Luca, G. Giovannini, G. Pieraccini, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity, 39 (2) (2013), pp. 372-385
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