Cultured human skeletal muscle satellite cells exhibit characteristics of mesenchymal stem cells and play anti-inflammatory roles through prostaglandin E2 and hepatocyte growth factors.
Adipose Tissue
/ metabolism
Anti-Inflammatory Agents
/ metabolism
Biomarkers
/ metabolism
Cell Differentiation
/ physiology
Cells, Cultured
Cyclooxygenase 2
/ metabolism
Dinoprostone
/ metabolism
Hepatocyte Growth Factor
/ metabolism
Hepatocytes
/ metabolism
Humans
Interleukin-1beta
/ metabolism
Macrophages
/ metabolism
Mesenchymal Stem Cells
/ metabolism
Satellite Cells, Skeletal Muscle
/ metabolism
THP-1 Cells
/ metabolism
hepatocyte growth factor
interleukin-1β
macrophages
prostaglandin E2
skeletal muscle satellite cells
Journal
Cell biology international
ISSN: 1095-8355
Titre abrégé: Cell Biol Int
Pays: England
ID NLM: 9307129
Informations de publication
Date de publication:
Dec 2021
Dec 2021
Historique:
revised:
06
07
2021
received:
22
04
2021
accepted:
07
08
2021
pubmed:
11
8
2021
medline:
3
3
2022
entrez:
10
8
2021
Statut:
ppublish
Résumé
Skeletal muscle satellite cells (SkMSCs) play crucial roles in muscle fiber maintenance, repair, and remodeling; however, it remains unknown if these properties are preserved in cultured SkMSCs. In this study, we investigated the characteristics of cultured SkMSCs and their ability to regulate the activity of M1 macrophages. SkMSCs grew well with an average population doubling time of 26.26 ± 6.85 h during 10 passages (P). At P5, Pax7, MyoD, cluster of differentiation (CD)34, and CD56 were not expressed in SkMSCs, but the MSC markers CD73, CD105, and CD90 were expressed and the cells were differentiated into adipocytes and osteoblasts. When SkMSCs were cocultured with macrophages, interleukin (IL)-1β secretion was decreased, prostaglandin (PG)E2 was produced in coculture, and cyclooxygenase-2 protein was induced in an SkMSC-dependent manner. Hepatocyte growth factor (HGF) was highly secreted by monocultured SkMSCs; interferon-γ and lipopolysaccharide reduced its expression level. However, HGF expression recovered when SkMSCs and macrophages were cocultured. Although exogenous PGE2 upregulated macrophage pro-IL-1β expression, it suppressed the secretion of cleaved IL-1β. In contrast, HGF decreased active IL-1β secretion without affecting pro-IL-1β expression. Co-treatment of macrophages with HGF and PGE2 reduced pro-IL-1β expression level and active IL-1β secretion. Our results suggest that SkMSCs lose their satellite cell properties during serial passaging but acquire mesenchymal stem cell properties including the ability to exert an anti-inflammatory response for macrophages through PGE2 and HGF.
Substances chimiques
Anti-Inflammatory Agents
0
Biomarkers
0
HGF protein, human
0
Interleukin-1beta
0
Hepatocyte Growth Factor
67256-21-7
Cyclooxygenase 2
EC 1.14.99.1
Dinoprostone
K7Q1JQR04M
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2443-2451Subventions
Organisme : Research Grant of Yonsei University Wonju College of Medicine
ID : YUWCM-2018-96
Organisme : National Research Foundation of Korea
ID : NRF-2017R1D1A1A02019212
Informations de copyright
© 2021 International Federation for Cell Biology.
Références
Aggarwal, S., & Pittenger, M. F. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 105(4), 1815-1822. https://doi.org/10.1182/blood-2004-04-1559
Choi, W., Lee, J., Lee, J., Lee, S. H., & Kim, S. (2019). Hepatocyte growth factor regulates macrophage transition to the M2 phenotype and promotes murine skeletal muscle regeneration. Frontiers in Physiology, 10, 914. https://doi.org/10.3389/fphys.2019.00914
Eom, Y. W., Oh, J. E., Lee, J. I., Baik, S. K., Rhee, K. J., Shin, H. C., Kim, Y. M., Ahn, C. M., Kong, J. H., Kim, H. S., & Shim, K. Y. (2014). The role of growth factors in maintenance of stemness in bone marrow-derived mesenchymal stem cells. Biochemical and Biophysical Research Communications, 445(1), 16-22. https://doi.org/10.1016/j.bbrc.2014.01.084
Fibbi, G., D'Alessio, S., Pucci, M., Cerletti, M., & Del Rosso, M. (2002). Growth factor-dependent proliferation and invasion of muscle satellite cells require the cell-associated fibrinolytic system. Biological Chemistry, 383(1), 127-136. https://doi.org/10.1515/BC.2002.013
Heredia, J. E., Mukundan, L., Chen, F. M., Mueller, A. A., Deo, R. C., Locksley, R. M., Rando, T. A., & Chawla, A. (2013). Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell, 153(2), 376-388. https://doi.org/10.1016/j.cell.2013.02.053
Huh, C. G., Factor, V. M., Sanchez, A., Uchida, K., Conner, E. A., & Thorgeirsson, S. S. (2004). Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proceedings of the National Academy of Sciences of the United States of America, 101(13), 4477-4482. https://doi.org/10.1073/pnas.0306068101
Jennische, E., Ekberg, S., & Matejka, G. L. (1993). Expression of hepatocyte growth factor in growing and regenerating rat skeletal muscle. The American Journal of Physiology, 265(1 Pt 1), C122-C128. https://doi.org/10.1152/ajpcell.1993.265.1.C122
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
Lemos, D. R., Babaeijandaghi, F., Low, M., Chang, C. K., Lee, S. T., Fiore, D., Zhang, R. H., Natarajan, A., Nedospasov, S. A., & Rossi, F. M. (2015). Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nature Medicine, 21(7), 786-794. https://doi.org/10.1038/nm.3869
Lukjanenko, L., Karaz, S., Stuelsatz, P., Gurriaran-Rodriguez, U., Michaud, J., Dammone, G., Sizzano, F., Mashinchian, O., Ancel, S., Migliavacca, E., Liot, S., Jacot, G., Metairon, S., Raymond, F., Descombes, P., Palini, A., Chazaud, B., Rudnicki, M. A., Bentzinger, C. F., & Feige, J. N. (2019). Aging disrupts muscle stem cell function by impairing matricellular WISP1 secretion from fibro-adipogenic progenitors. Cell Stem Cell, 24(3), 433-446. https://doi.org/10.1016/j.stem.2018.12.014
Meisel, R., Zibert, A., Laryea, M., Gobel, U., Daubener, W., & Dilloo, D. (2004). Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood, 103(12), 4619-4621. https://doi.org/10.1182/blood-2003-11-3909
Melief, S. M., Schrama, E., Brugman, M. H., Tiemessen, M. M., Hoogduijn, M. J., Fibbe, W. E., & Roelofs, H. (2013). Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes toward anti-inflammatory macrophages. Stem Cells, 31(9), 1980-1991. https://doi.org/10.1002/stem.1432
Mosser, D. M., & Edwards, J. P. (2008). Exploring the full spectrum of macrophage activation. Nature Reviews Immunology, 8(12), 958-969. https://doi.org/10.1038/nri2448
Nakamura, T., & Mizuno, S. (2010). The discovery of hepatocyte growth factor (HGF) and its significance for cell biology, life sciences and clinical medicine. Proceedings of the Japan Academy Series B-Physical and Biological Sciences, 86(6), 588-610. https://doi.org/10.2183/pjab.86.588
Otis, J. S., Niccoli, S., Hawdon, N., Sarvas, J. L., Frye, M. A., Chicco, A. J., & Lees, S. J. (2014). Pro-inflammatory mediation of myoblast proliferation. PLOS One, 9(3), e92363. https://doi.org/10.1371/journal.pone.0092363
Palacios, D., Mozzetta, C., Consalvi, S., Caretti, G., Saccone, V., Proserpio, V., Marquez, V. E., Valente, S., Mai, A., Forcales, S. V., Sartorelli, V., & Puri, P. L. (2010). TNF/p38ɑ/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell, 7(4), 455-469. https://doi.org/10.1016/j.stem.2010.08.013
Park, H. J., Kim, J., Saima, F. T., Rhee, K. J., Hwang, S., Kim, M. Y., Baik, S. K., Eom, Y. W., & Kim, H. S. (2018). Adipose-derived stem cells ameliorate colitis by suppression of inflammasome formation and regulation of M1-macrophage population through prostaglandin E2. Biochemical and Biophysical Research Communications, 498(4), 988-995. https://doi.org/10.1016/j.bbrc.2018.03.096
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
Saldana, L., Bensiamar, F., Valles, G., Mancebo, F. J., Garcia-Rey, E., & Vilaboa, N. (2019). Immunoregulatory potential of mesenchymal stem cells following activation by macrophage-derived soluble factors. Stem Cell Research and Therapy, 10(1), 58. https://doi.org/10.1186/s13287-019-1156-6
Schneider, B. S., & Tiidus, P. M. (2007). Neutrophil infiltration in exercise-injured skeletal muscle: How do we resolve the controversy? Sports Medicine, 37(10), 837-856. https://doi.org/10.2165/00007256-200737100-00002
Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scime, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., Tempst, P., Rudnicki, M. A., Beier, D. R., & Spiegelman, B. M. (2008). PRDM16 controls a brown fat/skeletal muscle switch. Nature, 454(7207), 961-967. https://doi.org/10.1038/nature07182
Shefer, G., Wleklinski-Lee, M., & Yablonka-Reuveni, Z. (2004). Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. Journal of Cell Science, 117(Pt 22), 5393-5404. https://doi.org/10.1242/jcs.01419
Sisson, T. H., Nguyen, M. H., Yu, B., Novak, M. L., Simon, R. H., & Koh, T. J. (2009). Urokinase-type plasminogen activator increases hepatocyte growth factor activity required for skeletal muscle regeneration. Blood, 114(24), 5052-5061. https://doi.org/10.1182/blood-2008-12-196212
Tatsumi, R., Anderson, J. E., Nevoret, C. J., Halevy, O., & Allen, R. E. (1998). HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Developmental Biology, 194(1), 114-128. https://doi.org/10.1006/dbio.1997.8803
Tatsumi, R., Sankoda, Y., Anderson, J. E., Sato, Y., Mizunoya, W., Shimizu, N., Suzuki, T., Yamada, M., Rhoads, R. P. Jr., Ikeuchi, Y., & Allen, R. E. (2009). Possible implication of satellite cells in regenerative motoneuritogenesis: HGF upregulates neural chemorepellent Sema3A during myogenic differentiation. American Journal of Physiology-Cell Physiology, 297(2), C238-C252. https://doi.org/10.1152/ajpcell.00161.2009
Tidball, J. G. (2017). Regulation of muscle growth and regeneration by the immune system. Nature Reviews Immunology, 17(3), 165-178. https://doi.org/10.1038/nri.2016.150