Fibro-adipogenic progenitor cells in skeletal muscle unloading: metabolic and functional impairments

Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC, Locksley RM, et al. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell. 2013;153:376–88.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Joe AWB, Yi L, Natarajan A, Le Grand F, So L, Wang J, et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol. 2010;12:153–63.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol. 2010;12:143–52.

Article  CAS  PubMed  Google Scholar 

Wosczyna MN, Rando TA, A Muscle Stem Cell Support Group.: Coordinated Cellular Responses in Muscle Regeneration. Dev Cell [Internet]. 2018;46:135–43. https://doi.org/10.1016/j.devcel.2018.06.018

Lemos DR, Babaeijandaghi F, Low M, Chang C-K, Lee ST, Fiore D, et al. Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nat Med. 2015;21:786–94.

Article  CAS  PubMed  Google Scholar 

Wosczyna MN, Konishi CT, Perez Carbajal EE, Wang TT, Walsh RA, Gan Q, et al. Mesenchymal stromal cells are required for regeneration and Homeostatic Maintenance of Skeletal Muscle. Cell Rep. 2019;27:2029–e20355.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Fiore D, Judson RN, Low M, Lee S, Zhang E, Hopkins C, et al. Pharmacological blockage of fibro/adipogenic progenitor expansion and suppression of regenerative fibrogenesis is associated with impaired skeletal muscle regeneration. Stem Cell Res. 2016;17:161–9.

Article  CAS  PubMed  Google Scholar 

Uezumi A, Ikemoto-Uezumi M, Zhou H, Kurosawa T, Yoshimoto Y, Nakatani M et al. Mesenchymal Bmp3b expression maintains skeletal muscle integrity and decreases in age-related Sarcopenia. J Clin Invest. 2021;131.

Malecova B, Gatto S, Etxaniz U, Passafaro M, Cortez A, Nicoletti C et al. Dynamics of cellular states of fibro-adipogenic progenitors during myogenesis and muscular dystrophy. Nat Commun [Internet]. 2018;9:3670. https://doi.org/10.1038/s41467-018-06068-6

Boppart MD, De Lisio M, Zou K, Huntsman HD. Defining a role for non-satellite stem cells in the regulation of muscle repair following exercise. Front Physiol. 2013;4:310.

Article  PubMed  PubMed Central  Google Scholar 

Collao N, Farup J, De Lisio M. Role of metabolic stress and Exercise in regulating Fibro/Adipogenic progenitors. Front cell Dev Biol. 2020;8:9.

Article  PubMed  PubMed Central  Google Scholar 

Farup J, De Lisio M, Rahbek SK, Bjerre J, Vendelbo MH, Boppart MD, et al. Pericyte response to contraction mode-specific resistance exercise training in human skeletal muscle. J Appl Physiol. 2015;119:1053–63.

Article  CAS  PubMed  Google Scholar 

Valero MC, Huntsman HD, Liu J, Zou K, Boppart MD. Eccentric Exercise Facilitates Mesenchymal Stem Cell Appearance in Skeletal Muscle. PLoS One [Internet]. 2012;7:e29760. https://doi.org/10.1371/journal.pone.0029760

Yaseen W, Kraft-Sheleg O, Zaffryar-Eilot S, Melamed S, Sun C, Millay DP et al. Fibroblast fusion to the muscle fiber regulates myotendinous junction formation. Nat Commun [Internet]. 2021;12:3852. https://doi.org/10.1038/s41467-021-24159-9

Wei X, Nicoletti C, Puri PL. Fibro-Adipogenic progenitors: versatile keepers of skeletal muscle homeostasis, beyond the response to myotrauma. Semin Cell Dev Biol. 2021;119:23–31.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Farup J, Just J, de Paoli F, Lin L, Jensen JB, Billeskov T, et al. Human skeletal muscle CD90 + fibro-adipogenic progenitors are associated with muscle degeneration in type 2 diabetic patients. Cell Metab. 2021;33:2201–e221410.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yao L, Tichy ED, Zhong L, Mohanty S, Wang L, Ai E, et al. Gli1 defines a subset of Fibro-adipogenic progenitors that promote skeletal muscle regeneration with less Fat Accumulation. J bone Min Res off J Am Soc Bone Min Res. 2021;36:1159–73.

Article  CAS  Google Scholar 

Madaro L, Passafaro M, Sala D, Etxaniz U, Lugarini F, Proietti D et al. Denervation-activated STAT3–IL-6 signalling in fibro-adipogenic progenitors promotes myofibres atrophy and fibrosis. Nat Cell Biol [Internet]. 2018;20:917–27. https://doi.org/10.1038/s41556-018-0151-y

Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol. 2002;92:1367–77.

Article  PubMed  Google Scholar 

Smolina N, Kostareva A, Bruton J, Karpushev A, Sjoberg G, Sejersen T. Primary murine myotubes as a model for investigating muscular dystrophy. Biomed Res Int. 2015;2015.

Richler C, Yaffe D. The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev Biol. 1970;23:1–22.

Article  CAS  PubMed  Google Scholar 

Dmitrieva RI, Minullina R, Bilibina AA, Tarasova OV, Anisimov SV, Zaritskey AY. Bone marrow- and subcutaneous adipose tissue-derived mesenchymal stem cells: differences and similarities. Cell Cycle. 2012;11:377–83.

Article  CAS  PubMed  Google Scholar 

Divakaruni AS, Paradyse A, Ferrick DA, Murphy AN, Jastroch M. Analysis and interpretation of microplate-based oxygen consumption and pH data [Internet]. 1st ed. Methods Enzymol. Elsevier Inc.; 2014. https://doi.org/10.1016/B978-0-12-801415-8.00016-3

Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–30.

Article  CAS  PubMed  Google Scholar 

Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause DS et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006.

Boxall SA, Jones E. Markers for characterization of bone marrow multipotential stromal cells. Stem Cells Int. 2012;2012.

Arrighi N, Moratal C, Clément N, Giorgetti-Peraldi S, Peraldi P, Loubat A, et al. Characterization of adipocytes derived from fibro/adipogenic progenitors resident in human skeletal muscle. 2015; Available from: www.nature.com/cddis

Contreras O, Rossi FMV, Theret M. Origins, potency, and heterogeneity of skeletal muscle fibro-adipogenic progenitors—time for new definitions. Skelet Muscle [Internet]. 2021;11:16. https://doi.org/10.1186/s13395-021-00265-6

Contreras O, Cruz-Soca M, Theret M, Soliman H, Tung LW, Groppa E et al. Cross-talk between TGF-β and PDGFRα signaling pathways regulates the fate of stromal fibro-adipogenic progenitors. J Cell Sci. 2019;132.

Dammone G, Karaz S, Lukjanenko L, Winkler C, Sizzano F, Jacot G et al. PPARγ Controls Ectopic Adipogenesis and Cross-Talks with Myogenesis During Skeletal Muscle Regeneration. Int J Mol Sci [Internet]. 2018;19. https://www.mdpi.com/1422-0067/19/7/2044

Pagano AF, Brioche T, Arc-Chagnaud C, Demangel R, Chopard A, Py G. Short-term disuse promotes fatty acid infiltration into skeletal muscle. J Cachexia Sarcopenia Muscle. 2018;9:335–47.

Article  PubMed  Google Scholar 

Buras ED, Converso-Baran K, Davis CS, Akama T, Hikage F, Michele DE et al. Fibro-Adipogenic Remodeling of the Diaphragm in Obesity-Associated Respiratory Dysfunction. Diabetes [Internet]. 2018;68:45–56. https://doi.org/10.2337/db18-0209

Ahmadian M, Suh JM, Hah N, Liddle C, Atkins AR, Downes M et al. PPARγ signaling and metabolism: the good, the bad and the future. Nat Med [Internet]. 2013;19:557–66. https://doi.org/10.1038/nm.3159

Rosen ED, Sarraf P, Troy AE, Bradwin G, Moore K, Milstone DS, et al. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell. 1999;4:611–7.

Article  CAS  PubMed  Google Scholar 

Prentice KJ, Saksi J, Hotamisligil GS. Adipokine FABP4 integrates energy stores and counterregulatory metabolic responses. J Lipid Res. 2019;60:734–40.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ojha S, Budge H, Symonds ME. Adipocytes in Normal Tissue Biology. In: McManus LM, Mitchell RNBT-P of HD, editors. San Diego: Academic Press; 2014. pp. 2003–13. https://www.sciencedirect.com/science/article/pii/B9780123864567044087

Nielsen TS, Møller N. Adipose triglyceride lipase and G0/G1 switch gene 2: approaching proof of concept. Diabetes. 2014;63:847–9.

Article  CAS  PubMed  Google Scholar 

Olofsson LE, Orho-Melander M, William-Olsson L, Sjöholm K, Sjöström L, Groop L, et al. CCAAT/enhancer binding protein alpha (C/EBPalpha) in adipose tissue regulates genes in lipid and glucose metabolism and a genetic variation in C/EBPalpha is associated with serum levels of triglycerides. J Clin Endocrinol Metab. 2008;93:4880–6.

Article  CAS  PubMed  Google Scholar 

Rosen ED, Hsu C-H, Wang X, Sakai S, Freeman MW, Gonzalez FJ, et al. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev. 2002;16:22–6.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Takahashi Y, Shinoda A, Kamada H, Shimizu M, Inoue J, Sato R. Perilipin2 plays a positive role in adipocytes during lipolysis by escaping proteasomal degradation. Sci Rep [Internet]. 2016;6:20975. https://doi.org/10.1038/srep20975

Huang P-I, Chou Y-C, Chang Y-L, Chien Y, Chen K-H, Song W-S et al. Enhanced differentiation of three-gene-reprogrammed Induced Pluripotent Stem cells into adipocytes via adenoviral-mediated PGC-1α overexpression. Int J Mol Sci. 2011. pp. 7554–68.

Abou-Samra M, Selvais CM, Dubuisson N, Brichard SM. Adiponectin and Its Mimics on Skeletal Muscle: Insulin Sensitizers, Fat Burners, Exercise Mimickers, Muscling Pills … or Everything Together? Int. J. Mol. Sci. 2020.

Biferali B, Proietti D, Mozzetta C, Madaro L. Fibro–adipogenic progenitors cross-talk in skeletal muscle: the Social Network. Front. Physiol. Frontiers Media S.A.; 2019.

Nicholls DG. Spare respiratory capacity, oxidative stress and excitotoxicity. Biochem Soc Trans. 2009;37:1385–8.

Article  CAS  PubMed  Google Scholar 

Masuda S, Tanaka M, Inoue T, Ohue-Kitano R, Yamakage H, Muranaka K et al. Chemokine (C-X-C motif) ligand 1 is a myokine induced by palmitate and is required for myogenesis in mouse satellite cells. Acta Physiol (Oxf). 2018;222.

Waldemer-Streyer RJ, Reyes-Ordoñez A, Kim D, Zhang R, Singh N, Chen J. Cxcl14 depletion accelerates skeletal myogenesis by promoting cell cycle withdrawal. npj Regen Med [Internet]. 2017;2:16017. https://doi.org/10.1038/npjregenmed.2016.17

Yahiaoui L, Gvozdic D, Danialou G, Mack M, Petrof BJ. CC family chemokines directly regulate myoblast responses to skeletal muscle injury. J Physiol [Internet]. 2008;586:3991–4004. https://physoc.onlinelibrary.wiley.com/doi/abs/https://doi.org/10.1113/jphysiol.2008.152090

Kusuyama J, Komorizono A, Bandow K, Ohnishi T, Matsuguchi T. CXCL3 positively regulates adipogenic differentiation. J Lipid Res [Internet]. 2016;57:1806–20. https://www.sciencedirect.com/science/article/pii/S0022227520353906

Scheler M, Irmler M, Lehr S, Hartwig S, Staiger H, Al-Hasani H, et al. Cytokine response of primary human myotubes in an in vitro exercise model. Am J Physiol Cell Physiol. 2013;305:C877–86.

Comments (0)

No login
gif