Altered Gene Expression of Muscle Satellite Cells Contributes to Agerelated Sarcopenia in Mice

Author(s): Zsofia Budai, Laszlo Balogh, Zsolt Sarang*.

Journal Name: Current Aging Science

Volume 11 , Issue 3 , 2018

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Abstract:

Background: During aging, muscle tissue undergoes profound changes which lead to a decline in its functional and regenerative capacity. We utilized global gene expression analysis and gene set enrichment analysis to characterize gene expression changes in aging muscle satellite cells.

Method: Gene expression data; obtained from Affymetrix Mouse Genome 430 2.0 Array, for 14 mouse muscle satellite cell samples (5 young, 4 middle-aged, and 5 aged), were retrieved from public Gene Expression Omnibus repository. List of differentially expressed genes was generated based on 0.05 multiple-testing-adjusted p-value and 2-fold FC cut-off values. Functional profiling of genes was carried out using PANTHER Classification System.

Results: We have found several differentially expressed genes in satellite cells derived from aged mice compared to young ones. The gene expression changes increased progressively with time, and the majority of the differentially expressed genes were upregulated during aging. While the downregulated genes could not be correlated with specific biological processes the upregulated ones could be associated with muscle differentiation-, inflammation- or fibrosis-related processes. The latter two processes encompass the senescence-associated secretory phenotype for satellite cells which alters the tissue microenvironment and contributes to inflammation and fibrosis observed in aging muscle.

Conclusion: Our analysis reveals that by altering gene expression pattern and expressing inflammatory mediators and extracellular matrix components, these cells can directly contribute to muscle wasting in aged mice.

Keywords: Satellite cell, aging, senescence-associated secretory phenotype, fibrosis, muscle, inflammation.

[1]
Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961; 9: 493-5.
[2]
Jankowski RJ, Deasy BM, Huard J. Muscle-derived stem cells. Gene Ther 2002; 9(10): 642-7.
[3]
Sherwood RI, Christensen JL, Conboy IM, et al. Isolation of adult mouse myogenic progenitors: Functional heterogeneity of cells within and engrafting skeletal muscle. Cell 2004; 119(4): 543-54.
[4]
Bazgir B, Fathi R, Rezazadeh VM, et al. Satellite cells contribution to exercise mediated muscle hypertrophy and repair. Cell J 2017; 18(4): 473-84.
[5]
Terzi MY, Izmirli M, Gogebakan B. The cell fate: Senescence or quiescence. Mol Biol Rep 2016; 43(11): 1213-20.
[6]
Sousa-Victor P, Gutarra S, García-Prat L, et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 2014; 506(7488): 316-21.
[7]
Coppé JP, Patil CK, Rodier F, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008; 6(12): 2853-68.
[8]
Freund A, Orjalo AV, Desprez PY, et al. Inflammatory networks during cellular senescence: Causes and consequences. Trends Mol Med 2010; 16(5): 238-46.
[9]
Brack AS, Bildsoe H, Hughes SM. Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy. J Cell Sci 2005; 118(Pt 20): 4813-21.
[10]
Day K, Shefer G, Shearer A, et al. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol 2010; 340(2): 330-43.
[11]
Leiter JR, Anderson JE. Satellite cells are increasingly refractory to activation by nitric oxide and stretch in aged mouse-muscle cultures. Int J Biochem Cell Biol 2010; 42(1): 132-6.
[12]
Grimble RF. Inflammatory response in the elderly. Curr Opin Clin Nutr Metab Care 2003; 6(1): 21-9.
[13]
Singh T, Newman AB. Inflammatory markers in population studies of aging. Ageing Res Rev 2011; 10(3): 319-29.
[14]
Arnold L, Henry A, Poron F, et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 2007; 204(5): 1057-69.
[15]
Costamagna D, Costelli P, Sampaolesi M, et al. Role of inflammation in muscle homeostasis and myogenesis. Mediators Inflamm 2015; 2015: 805172.
[16]
Bruunsgaard H, Pedersen M, Pedersen BK. Aging and proinflammatory cytokines. Curr Opin Hematol 2001; 8(3): 131-6.
[17]
Dreyer HC, Blanco CE, Sattler FR, et al. Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve 2006; 33(2): 242-53.
[18]
Sinha M, Jang YC, Oh J, et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 2014; 344(6184): 649-52.
[19]
Chakkalakal JV, Jones KM, Basson MA, et al. The aged niche disrupts muscle stem cell quiescence. Nature 2012; 490(7420): 355-60.
[20]
Oh J, Sinha I, Tan KY, et al. Age-associated NF-κB signaling in myofibers alters the satellite cell niche and re-strains muscle stem cell function. Aging (Albany NY) 2016; 8(11): 2871-96.
[21]
Lucero HA, Kagan HM. Lysyl oxidase: An oxidative enzyme and effector of cell function. Cell Mol Life Sci 2006; 63(19-20): 2304-16.
[22]
Lazarus HM, Cruikshank WW, Narasimhan N, et al. Induction of human monocyte motility by lysyl oxidase. Matrix Biol 1995; 14(9): 727-31.
[23]
Shi GP, Sukhova GK, Grubb A, et al. Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J Clin Invest 1999; 104(9): 1191-7.
[24]
Ogasawara S, Cheng XW, Inoue A, et al. Cathepsin K activity controls cardiotoxin-induced skeletal muscle repair in mice. J Cachexia Sarcopenia Muscle 2018; 9(1): 160-75.
[25]
Choi YC, Kim TS, Kim SY. Increase in transglutaminase 2 in idiopathic inflammatory myopathies. Eur Neurol 2004; 51(1): 10-4.
[26]
Lee J, Kim YS, Choi DH, et al. Transglutaminase 2 induces nuclear factor-kappaB activation via a novel pathway in BV-2 microglia. J Biol Chem 2004; 279(51): 53725-35.
[27]
Mann CJ, Perdiguero E, Kharraz Y, et al. Aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 2011; 1(1): 21.
[28]
Sun YB, Qu X, Caruana G, et al. The origin of renal fibroblasts/myofibroblasts and the signals that trigger fibrosis. Differentiation 2016; 92(3): 102-7.
[29]
Saika S, Yamanaka O, Okada Y, et al. TGF beta in fibroproliferative diseases in the eye. Front Biosci (Schol Ed) 2009; 1: 376-90.
[30]
Yen JH, Lin LC, Chen MC, et al. The metastatic tumor antigen 1-transglutaminase-2 pathway is involved in self-limitation of monosodium urate crystal-induced inflammation by upregulating TGF-β1. Arthritis Res Ther 2015; 17: 65.
[31]
Nunes I, Gleizes PE, Metz CN, et al. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J Cell Biol 1997; 136(5): 1151-63.
[32]
Alexakis C, Partridge T, Bou-Gharios G. Implication of the satellite cell in dystrophic muscle fibrosis: A self-perpetuating mechanism of collagen overproduction. Am J Physiol Cell Physiol 2007; 293(2): C661-9.
[33]
Stearns-Reider KM, D’Amore A, Beezhold K, et al. Aging of the skeletal muscle extracellular matrix drives a stem cell fibrogenic conversion. Aging Cell 2017; 16(3): 518-28.
[34]
Bains W. Transglutaminase 2 and EGGL, the protein cross-link formed by transglutaminase 2, as therapeutic targets for disabilities of old age. Rejuvenation Res 2013; 16(6): 495-517.
[35]
Schelling JR. Tissue transglutaminase inhibition as treatment for diabetic glomerular scarring: It’s good to be glueless. Kidney Int 2009; 76(4): 363-5.
[36]
Johnson TS, Fisher M, Haylor JL, et al. Transglutaminase inhibition reduces fibrosis and preserves function in experimental chronic kidney disease. J Am Soc Nephrol 2007; 18(12): 3078-88.
[37]
Gilpin D, Coleman S, Hall S, et al. Injectable collagenase Clostridium histolyticum: A new nonsurgical treatment for Dupuytren’s disease. J Hand Surg Am 2010; 35(12): 2027-38.


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Article Details

VOLUME: 11
ISSUE: 3
Year: 2018
Page: [165 - 172]
Pages: 8
DOI: 10.2174/1874609811666180925104241

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