Meflin/ISLR is a marker of adipose stem and progenitor cells in mice and humans that suppresses white adipose tissue remodeling and fibrosis.
Islr
Meflin
adipose stem and progenitor cells
adipose stem cells
fibrosis
glucose tolerance
immunoglobulin superfamily containing leucine‐rich repeat
mesenchymal stem cell
metabolic syndrome
Journal
Genes to cells : devoted to molecular & cellular mechanisms
ISSN: 1365-2443
Titre abrégé: Genes Cells
Pays: England
ID NLM: 9607379
Informations de publication
Date de publication:
13 Aug 2024
13 Aug 2024
Historique:
revised:
25
07
2024
received:
07
05
2024
accepted:
30
07
2024
medline:
13
8
2024
pubmed:
13
8
2024
entrez:
13
8
2024
Statut:
aheadofprint
Résumé
Identifying specific markers of adipose stem and progenitor cells (ASPCs) in vivo is crucial for understanding the biology of white adipose tissues (WAT). PDGFRα-positive perivascular stromal cells represent the best candidates for ASPCs. This cell lineage differentiates into myofibroblasts that contribute to the impairment of WAT function. However, ASPC marker protein(s) that are functionally crucial for maintaining WAT homeostasis are unknown. We previously identified Meflin as a marker of mesenchymal stem cells (MSCs) in bone marrow and tissue-resident perivascular fibroblasts in various tissues. We also demonstrated that Meflin maintains the undifferentiated status of MSCs/fibroblasts. Here, we show that Meflin is expressed in WAT ASPCs. A lineage-tracing experiment showed that Meflin
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Japan Agency for Medical Research and Development
ID : 22ck0106779h0001
Organisme : Japan Agency for Medical Research and Development
ID : 23gm1210009s0105
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 20H03467
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 22H02848
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 22K18390
Informations de copyright
© 2024 The Author(s). Genes to Cells published by Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd.
Références
Ando, R., Shiraki, Y., Miyai, Y., Shimizu, H., Furuhashi, K., Minatoguchi, S., Kato, K., Kato, A., Iida, T., Mizutani, Y., Ito, K., Asai, N., Mii, S., Esaki, N., Takahashi, M., & Enomoto, A. (2024). Meflin is a marker of pancreatic stellate cells involved in fibrosis and epithelial regeneration in the pancreas. The Journal of Pathology, 262(1), 61–75. https://doi.org/10.1002/path.6211
Barrett, R. L., & Puré, E. (2020). Cancer‐associated fibroblasts and their influence on tumor immunity and immunotherapy. eLife, 9, e57243. https://doi.org/10.7554/eLife.57243
Berry, R., & Rodeheffer, M. S. (2013). Characterization of the adipocyte cellular lineage in vivo. Nature Cell Biology, 15(3), 302–308. https://doi.org/10.1038/ncb2696
Buechler, M. B., Pradhan, R. N., Krishnamurty, A. T., Cox, C., Calviello, A. K., Wang, A. W., Yang, Y. A., Tam, L., Caothien, R., Roose‐Girma, M., Modrusan, Z., Arron, J. R., Bourgon, R., Müller, S., & Turley, S. J. (2021). Cross‐tissue organization of the fibroblast lineage. Nature, 593(7860), 575–579. https://doi.org/10.1038/s41586-021-03549-5
Cattaneo, P., Mukherjee, D., Spinozzi, S., Zhang, L., Larcher, V., Stallcup, W. B., Kataoka, H., Chen, J., Dimmeler, S., Evans, S. M., & Guimarães‐Camboa, N. (2020). Parallel lineage‐tracing studies establish fibroblasts as the prevailing in vivo adipocyte progenitor. Cell Reports, 30(2), 571–582.e2. https://doi.org/10.1016/j.celrep.2019.12.046
Cinti, S., Mitchell, G., Barbatelli, G., Murano, I., Ceresi, E., Faloia, E., Wang, S., Fortier, M., Greenberg, A. S., & Obin, M. S. (2005). Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. Journal of Lipid Research, 46(11), 2347–2355. https://doi.org/10.1194/jlr.M500294-JLR200
Corselli, M., Chen, C. W., Sun, B., Yap, S., Rubin, J. P., & Péault, B. (2012). The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells and Development, 21(8), 1299–1308. https://doi.org/10.1089/scd.2011.0200
Crisan, M., Chen, C. W., Corselli, M., Andriolo, G., Lazzari, L., & Péault, B. (2009). Perivascular multipotent progenitor cells in human organs. Annals of the New York Academy of Sciences, 1176, 118–123. https://doi.org/10.1111/j.1749-6632.2009.04967.x
Crisan, M., Yap, S., Casteilla, L., Chen, C. W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., Norotte, C., Teng, P. N., Traas, J., Schugar, R., Deasy, B. M., Badylak, S., Buhring, H. J., Giacobino, J. P., Lazzari, L., … Péault, B. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 3(3), 301–313. https://doi.org/10.1016/j.stem.2008.07.003
Czerwiec, K., Zawrzykraj, M., Deptuła, M., Skoniecka, A., Tymińska, A., Zieliński, J., Kosiński, A., & Pikuła, M. (2023). Adipose‐derived mesenchymal stromal cells in basic research and clinical applications. International Journal of Molecular Sciences, 24(4), 3888. https://doi.org/10.3390/ijms24043888
Emont, M. P., Jacobs, C., Essene, A. L., Pant, D., Tenen, D., Colleluori, G., Di Vincenzo, A., Jørgensen, A. M., Dashti, H., Stefek, A., McGonagle, E., Strobel, S., Laber, S., Agrawal, S., Westcott, G. P., Kar, A., Veregge, M. L., Gulko, A., Srinivasan, H., … Rosen, E. D. (2022). A single‐cell atlas of human and mouse white adipose tissue. Nature, 603(7903), 926–933. https://doi.org/10.1038/s41586-022-04518-2
Guimarães‐Camboa, N., Cattaneo, P., Sun, Y., Moore‐Morris, T., Gu, Y., Dalton, N. D., Rockenstein, E., Masliah, E., Peterson, K. L., Stallcup, W. B., Chen, J., & Evans, S. M. (2017). Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell, 20(3), 345–359.e5. https://doi.org/10.1016/j.stem.2016.12.006
Han, X., Zhang, Z., He, L., Zhu, H., Li, Y., Pu, W., Han, M., Zhao, H., Liu, K., Li, Y., Huang, X., Zhang, M., Jin, H., Lv, Z., Tang, J., Wang, J., Sun, R., Fei, J., Tian, X., … Zhou, B. (2021). A suite of new dre recombinase drivers markedly expands the ability to perform intersectional genetic targeting. Cell Stem Cell, 28(6), 1160–1176.e7. https://doi.org/10.1016/j.stem.2021.01.007
Hara, A., Kato, K., Ishihara, T., Kobayashi, H., Asai, N., Mii, S., Shiraki, Y., Miyai, Y., Ando, R., Mizutani, Y., Iida, T., Takefuji, M., Murohara, T., Takahashi, M., & Enomoto, A. (2021). Meflin defines mesenchymal stem cells and/or their early progenitors with multilineage differentiation capacity. Genes Cells, 26(7), 495–512. https://doi.org/10.1111/gtc.12855
Hara, A., Kobayashi, H., Asai, N., Saito, S., Higuchi, T., Kato, K., Okumura, T., Bando, Y. K., Takefuji, M., Mizutani, Y., Miyai, Y., Saito, S., Maruyama, S., Maeda, K., Ouchi, N., Nagasaka, A., Miyata, T., Mii, S., Kioka, N., … Enomoto, A. (2019). Roles of the mesenchymal stromal/stem cell marker Meflin in cardiac tissue repair and the development of diastolic dysfunction. Circulation Research, 125(4), 414–430. https://doi.org/10.1161/CIRCRESAHA.119.314806
Hirata, Y., Furuhashi, K., Ishii, H., Li, H. W., Pinho, S., Ding, L., Robson, S. C., Frenette, P. S., & Fujisaki, J. (2018). CD150high bone marrow Tregs maintain hematopoietic stem cell quiescence and immune privilege via adenosine. Cell Stem Cell, 22(3), 445–453.e5. https://doi.org/10.1016/j.stem.2018.01.017
Ichioka, M., Suganami, T., Tsuda, N., Shirakawa, I., Hirata, Y., Satoh‐Asahara, N., Shimoda, Y., Tanaka, M., Kim‐Saijo, M., Miyamoto, Y., Kamei, Y., Sata, M., & Ogawa, Y. (2011). Increased expression of macrophage‐inducible C‐type lectin in adipose tissue of obese mice and humans. Diabetes, 60(3), 819–826. https://doi.org/10.2337/db10-0864
Iida, T., Mizutani, Y., Esaki, N., Ponik, S. M., Burkel, B. M., Weng, L., Kuwata, K., Masamune, A., Ishihara, S., Haga, H., Kataoka, K., Mii, S., Shiraki, Y., Ishikawa, T., Ohno, E., Kawashima, H., Hirooka, Y., Fujishiro, M., Takahashi, M., & Enomoto, A. (2022). Pharmacologic conversion of cancer‐associated fibroblasts from a protumor phenotype to an antitumor phenotype improves the sensitivity of pancreatic cancer to chemotherapeutics. Oncogene, 41(19), 2764–2777. https://doi.org/10.1038/s41388-022-02288-9
Joe, A. W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M. A., & Rossi, F. M. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nature Cell Biology, 12(2), 153–163. https://doi.org/10.1038/ncb2015
Kobayashi, H., Gieniec, K. A., Lannagan, T. R. M., Wang, T., Asai, N., Mizutani, Y., Iida, T., Ando, R., Thomas, E. M., Sakai, A., Suzuki, N., Ichinose, M., Wright, J. A., Vrbanac, L., Ng, J. Q., Goyne, J., Radford, G., Lawrence, M. J., Sammour, T., … Worthley, D. L. (2022). The origin and contribution of cancer‐associated fibroblasts in colorectal carcinogenesis. Gastroenterology, 162(3), 890–906. https://doi.org/10.1053/j.gastro.2021.11.037
Kobayashi, H., Gieniec, K. A., Wright, J. A., Wang, T., Asai, N., Mizutani, Y., Lida, T., Ando, R., Suzuki, N., Lannagan, T. R. M., Ng, J. Q., Hara, A., Shiraki, Y., Mii, S., Ichinose, M., Vrbanac, L., Lawrence, M. J., Sammour, T., Uehara, K., … Woods, S. L. (2021). The balance of stromal BMP signaling mediated by GREM1 and ISLR drives colorectal carcinogenesis. Gastroenterology, 160(4), 1224–1239.e30. https://doi.org/10.1053/j.gastro.2020.11.011
Kuwano, T., Izumi, H., Aslam, M. R., Igarashi, Y., Bilal, M., Nishimura, A., Watanabe, Y., Nawaz, A., Kado, T., Ikuta, K., Yamamoto, S., Sasahara, M., Fujisaka, S., Yagi, K., Mori, H., & Tobe, K. (2021). Generation and characterization of a Meflin‐CreERT2 transgenic line for lineage tracing in white adipose tissue. PLoS One, 16(3), e0248267. https://doi.org/10.1371/journal.pone.0248267
Maeda, K., Enomoto, A., Hara, A., Asai, N., Kobayashi, T., Horinouchi, A., Maruyama, S., Ishikawa, Y., Nishiyama, T., Kiyoi, H., Kato, T., Ando, K., Weng, L., Mii, S., Asai, M., Mizutani, Y., Watanabe, O., Hirooka, Y., Goto, H., & Takahashi, M. (2016). Identification of Meflin as a potential marker for mesenchymal stromal cells. Scientific Reports, 6, 22288. https://doi.org/10.1038/srep22288
Marcelin, G., Gautier, E. L., & Clément, K. (2022). Adipose tissue fibrosis in obesity: Etiology and challenges. Annual Review of Physiology, 84, 135–155. https://doi.org/10.1146/annurev-physiol-060721-092930
Marcelin, G., Silveira, A. L. M., Martins, L. B., Ferreira, A. V., & Clément, K. (2019). Deciphering the cellular interplays underlying obesity‐induced adipose tissue fibrosis. The Journal of Clinical Investigation, 129(10), 4032–4040. https://doi.org/10.1172/JCI129192
Matsumoto, K., Mitani, T. T., Horiguchi, S. A., Kaneshiro, J., Murakami, T. C., Mano, T., Fujishima, H., Konno, A., Watanabe, T. M., Hirai, H., & Ueda, H. R. (2019). Advanced CUBIC tissue clearing for whole‐organ cell profiling. Nature Protocols, 14(12), 3506–3537. https://doi.org/10.1038/s41596-019-0240-9
Mazini, L., Rochette, L., Amine, M., & Malka, G. (2019). Regenerative capacity of adipose derived stem cells (ADSCs), comparison with mesenchymal stem cells (MSCs). International Journal of Molecular Sciences, 20(10), 2523. https://doi.org/10.3390/ijms20102523
Minatoguchi, S., Saito, S., Furuhashi, K., Sawa, Y., Okazaki, M., Shimamura, Y., Kaihan, A. B., Hashimoto, Y., Yasuda, Y., Hara, A., Mizutani, Y., Ando, R., Kato, N., Ishimoto, T., Tsuboi, N., Esaki, N., Matsuyama, M., Shiraki, Y., Kobayashi, H., … Maruyama, S. (2022). A novel renal perivascular mesenchymal cell subset gives rise to fibroblasts distinct from classic myofibroblasts. Scientific Reports, 12(1), 5389. https://doi.org/10.1038/s41598-022-09331-5
Miyai, Y., Esaki, N., Takahashi, M., & Enomoto, A. (2020). Cancer‐associated fibroblasts that restrain cancer progression: Hypotheses and perspectives. Cancer Science, 111(4), 1047–1057. https://doi.org/10.1111/cas.14346
Miyai, Y., Sugiyama, D., Hase, T., Asai, N., Taki, T., Nishida, K., Fukui, T., Chen‐Yoshikawa, T. F., Kobayashi, H., Mii, S., Shiraki, Y., Hasegawa, Y., Nishikawa, H., Ando, Y., Takahashi, M., & Enomoto, A. (2022). Meflin‐positive cancer‐associated fibroblasts enhance tumor response to immune checkpoint blockade. Life Science Alliance, 5(6), e202101230. https://doi.org/10.26508/lsa.202101230
Mizutani, Y., Kobayashi, H., Iida, T., Asai, N., Masamune, A., Hara, A., Esaki, N., Ushida, K., Mii, S., Shiraki, Y., Ando, K., Weng, L., Ishihara, S., Ponik, S. M., Conklin, M. W., Haga, H., Nagasaka, A., Miyata, T., Matsuyama, M., … Takahashi, M. (2019). Meflin‐positive cancer‐associated fibroblasts inhibit pancreatic carcinogenesis. Cancer Research, 79(20), 5367–5381. https://doi.org/10.1158/0008-5472.CAN-19-0454
Murano, I., Barbatelli, G., Parisani, V., Latini, C., Muzzonigro, G., Castellucci, M., & Cinti, S. (2008). Dead adipocytes, detected as crown‐like structures, are prevalent in visceral fat depots of genetically obese mice. Journal of Lipid Research, 49(7), 1562–1568. https://doi.org/10.1194/jlr.M800019-JLR200
Nakahara, Y., Hashimoto, N., Sakamoto, K., Enomoto, A., Adams, T. S., Yokoi, T., Omote, N., Poli, S., Ando, A., Wakahara, K., Suzuki, A., Inoue, M., Hara, A., Mizutani, Y., Imaizumi, K., Kawabe, T., Rosas, I. O., Takahashi, M., Kaminski, N., & Hasegawa, Y. (2021). Fibroblasts positive for meflin have anti‐fibrotic properties in pulmonary fibrosis. The European Respiratory Journal, 58(6), 2003397. https://doi.org/10.1183/13993003.03397-2020
Owaki, T., Iida, T., Miyai, Y., Kato, K., Hase, T., Ishii, M., Ando, R., Hinohara, K., Akashi, T., Mizutani, Y., Ishikawa, T., Mii, S., Shiraki, Y., Esaki, N., Yamamoto, M., Tsukamoto, T., Nomura, S., Murakami, T., Takahashi, M., … Enomoto, A. (2024). Synthetic retinoid‐mediated preconditioning of cancer‐associated fibroblasts and macrophages improves cancer response to immune checkpoint blockade. British Journal of Cancer, 131(2), 372–386. https://doi.org/10.1038/s41416-024-02734-3
Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., & Marshak, D. R. (1999). Multilineage potential of adult human mesenchymal stem cells. Science, 284(5411), 143–147. https://doi.org/10.1126/science.284.5411.143
Rodeheffer, M. S., Birsoy, K., & Friedman, J. M. (2008). Identification of white adipocyte progenitor cells in vivo. Cell, 135(2), 240–249. https://doi.org/10.1016/j.cell.2008.09.036
Rosen, E. D., & Spiegelman, B. M. (2014). What we talk about when we talk about fat. Cell, 156(1–2), 20–44. https://doi.org/10.1016/j.cell.2013.12.012
Sakers, A., De Siqueira, M. K., Seale, P., & Villanueva, C. J. (2022). Adipose‐tissue plasticity in health and disease. Cell, 185(3), 419–446. https://doi.org/10.1016/j.cell.2021.12.016
Saltiel, A. R., & Olefsky, J. M. (2017). Inflammatory mechanisms linking obesity and metabolic disease. The Journal of Clinical Investigation, 127(1), 1–4. https://doi.org/10.1172/JCI92035
Shimizu, Y., Kondo, K., Hayashida, R., Sasaki, K. I., Ohtsuka, M., Fukumoto, Y., Takashima, S., Inoue, O., Usui, S., Takamura, M., Sakuma, M., Inoue, T., Nagata, T., Akashi, Y. J., Yamada, Y., Kato, T., Kuwahara, K., Tateno, K., Kobayashi, Y., … TACT‐ADRC multicenter trial Group. (2022). Therapeutic angiogenesis for patients with no‐option critical limb ischemia by adipose‐derived regenerative cells: TACT‐ADRC multicenter trial Group. Angiogenesis, 25(4), 535–546. https://doi.org/10.1007/s10456-022-09844-7
Shiraki, Y., Mii, S., Esaki, N., & Enomoto, A. (2022). Possible disease‐protective roles of fibroblasts in cancer and fibrosis and their therapeutic application. Nagoya Journal of Medical Science, 84(3), 484–496. https://doi.org/10.18999/nagjms.84.3.484
Si, Z., Wang, X., Sun, C., Kang, Y., Xu, J., Wang, X., & Hui, Y. (2019). Adipose‐derived stem cells: Sources, potency, and implications for regenerative therapies. Biomedicine & Pharmacotherapy, 114, 108765. https://doi.org/10.1016/j.biopha.2019.108765
Sun, C., Berry, W. L., & Olson, L. E. (2017). PDGFRα controls the balance of stromal and adipogenic cells during adipose tissue organogenesis. Development, 144(1), 83–94. doi:10.1242/dev.135962
Tainaka, K., Kubota, S. I., Suyama, T. Q., Susaki, E. A., Perrin, D., Ukai‐Tadenuma, M., Ukai, H., & Ueda, H. R. (2014). Whole‐body imaging with single‐cell resolution by tissue decolorization. Cell, 159(4), 911–924. https://doi.org/10.1016/j.cell.2014.10.034
Takahashi, K., Kubota, S. I., Ehata, S., Ueda, H. R., & Miyazono, K. (2020). Protocol for imaging and analysis of mouse tumor models with CUBIC tissue clearing. STAR Protocols, 1(3), 100191. https://doi.org/10.1016/j.xpro.2020.100191
Tanaka, M., Ikeda, K., Suganami, T., Komiya, C., Ochi, K., Shirakawa, I., Hamaguchi, M., Nishimura, S., Manabe, I., Matsuda, T., Kimura, K., Inoue, H., Inagaki, Y., Aoe, S., Yamasaki, S., & Ogawa, Y. (2014). Macrophage‐inducible C‐type lectin underlies obesity‐induced adipose tissue fibrosis. Nature Communications, 5, 4982. https://doi.org/10.1038/ncomms5982
Tanaka, M., Itoh, M., Ogawa, Y., & Suganami, T. (2018). Molecular mechanism of obesity‐induced ‘metabolic’ tissue remodeling. Journal of Diabetes Investigation, 9(2), 256–261. https://doi.org/10.1111/jdi.12769
Tang, W., Zeve, D., Suh, J. M., Bosnakovski, D., Kyba, M., Hammer, R. E., Tallquist, M. D., & Graff, J. M. (2008). White fat progenitor cells reside in the adipose vasculature. Science, 322(5901), 583–586. https://doi.org/10.1126/science.1156232
Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S., & Tsuchida, K. (2010). Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nature Cell Biology, 12(2), 143–152. https://doi.org/10.1038/ncb2014
Vishvanath, L., MacPherson, K. A., Hepler, C., Wang, Q. A., Shao, M., Spurgin, S. B., Wang, M. Y., Kusminski, C. M., Morley, T. S., & Gupta, R. K. (2016). Pdgfrβ+ mural preadipocytes contribute to adipocyte hyperplasia induced by high‐fat‐diet feeding and prolonged cold exposure in adult mice. Cell Metabolism, 23(2), 350–359. https://doi.org/10.1016/j.cmet.2015.10.018
Wueest, S., Rapold, R. A., Schumann, D. M., Rytka, J. M., Schildknecht, A., Nov, O., Chervonsky, A. V., Rudich, A., Schoenle, E. J., Donath, M. Y., & Konrad, D. (2010). Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. The Journal of Clinical Investigation, 120(1), 191–202. https://doi.org/10.1172/JCI38388
Zhang, Y., Lan, M., Liu, C., Wang, T., Liu, C., Wu, S., & Meng, Q. (2023). Islr regulates insulin sensitivity by interacting with Psma4 to control insulin receptor alpha levels in obese mice. The International Journal of Biochemistry & Cell Biology, 159, 106420. https://doi.org/10.1016/j.biocel.2023.106420
Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Benhaim, P., & Hedrick, M. H. (2002). Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell, 13(12), 4279–4295. https://doi.org/10.1091/mbc.e02-02-0105
Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., & Hedrick, M. H. (2001). Multilineage cells from human adipose tissue: Implications for cell‐based therapies. Tissue Engineering, 7(2), 211–228. https://doi.org/10.1089/107632701300062859