Regenerative function of immune system: Modulation of muscle stem cells

Ageing Research Reviews

Volumn 27, Issue , 2016, Pages 67-76

  Saini, Jasdeep ^a   McPhee, Jamie S ^a   Al Dabbagh, Sarah ^a   Stewart, Claire E ^b   Al Shanti, Nasser ^a  

^a MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^b LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

Immune system; Muscle treg; Regeneration; Skeletal muscle

Indexed keywords

CHEMOKINE; CYTOKINE; GROWTH FACTOR;

ADAPTIVE IMMUNITY; AVULSION INJURY; CELL ACTIVATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTUSION; HUMAN; IMMUNE SYSTEM; INNATE IMMUNITY; MACROPHAGE; MICROENVIRONMENT; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE REGENERATION; MUSCLE STEM CELL; MUSCLE WEAKNESS; NEUTROPHIL; REGULATORY T LYMPHOCYTE; REVIEW; SATELLITE CELL; SKELETAL MUSCLE; AGING; CELL AGING; IMMUNOLOGY; PHYSIOLOGY; REGENERATION; SARCOPENIA; SKELETAL MUSCLE SATELLITE CELL;

AGING; CELL AGING; HUMANS; MUSCLE, SKELETAL; REGENERATION; SARCOPENIA; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84962376432     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2016.03.006     Document Type: Review

References (124)

1. Abbadie C., Lindia J.A., Cumiskey A.M., Peterson L.B., Mudgett J.S., Bayne E.K., DeMartino J.A., MacIntyre D.E., Forrest M.J. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(June (13)):7947-7952.
2. Adams G.R. Satellite cell proliferation and skeletal muscle hypertrophy. Appl. Physiol. Nutr. Metab. 2006, 31(December (6)):782-790.
3. Al-Dabbagh S., McPhee J.S., Murgatroyd C., Butler-Browne G., Stewart C.E., Al-Shanti N. The lymphocyte secretome from young adults enhances skeletal muscle proliferation and migration, but effects are attenuated in the secretome of older adults. Physiol. Rep. 2015, 3(November (11)).
4. Al-Shanti N., Durcan P., Al-Dabbagh S., Dimchev G.A., Stewart C.E. Activated lymphocytes secretome inhibits differentiation and induces proliferation of C2C12 myoblasts. Cell. Physiol. Biochem. 2014, 33(1):117-128.
5. Arango Duque G., Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front. Immunol. 2014, 5:491.
6. Arnold L., Henry A., Poron F., Baba-Amer Y., van Rooijen N., Plonquet A., Gherardi R.K., Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 2007, 204(May (5)):1057-1069.
7. Barberi L., Scicchitano B.M., De Rossi M., Bigot A., Duguez S., Wielgosik A., Stewart C., McPhee J., Conte M., Narici M., Franceschi C., Mouly V., Butler-Browne G., Musarò A. Age-dependent alteration in muscle regeneration: the critical role of tissue niche. Biogerontology 2013, 14(June (3)):273-292.
8. Bentzinger C.F., Wang Y.X., Rudnicki M.A. Building muscle: molecular regulation of myogenesis. Cold Spring Harb. Perspect. Biol. 2012, 4(February (2)).
9. Blotnick S., Peoples G.E., Freeman M.R., Eberlein T.J., Klagsbrun M. T lymphocytes synthesize and export heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor mitogens for vascular cells and fibroblasts: differential production and release by CD4+ and CD8+ T cells. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(April (8)):2890-2894.
10. Bosurgi L., Corna G., Vezzoli M., Touvier T., Cossu G., Manfredi A.A., Brunelli S., Rovere-Querini P. Transplanted mesoangioblasts require macrophage IL-10 for survival in a mouse model of muscle injury. J. Immunol. 2012, 188(June (12)):6267-6277.
11. Brack A.S., Rando T.A. Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 2007, 3(Fall (3)):226-237.
12. Brack A.S., Munoz-Canoves P. The ins and outs of muscle stem cell aging. Skelet. Muscle 2015, 6:1.
13. Brun Caroline E., Rudnicki Michael A. GDF11 and the mythical fountain of youth. Cell Metab. 2015, 22(1):54-56.
14. Bruunsgaard H., Andersen-Ranberg K., Hjelmborg J., Pedersen B.K., Jeune B. Elevated levels of tumor necrosis factor alpha and mortality in centenarians. Am. J. Med. 2003, 115(September (4)):278-283.
15. Burzyn D., Benoist C., Mathis D. Regulatory T cells in nonlymphoid tissues. Nat. Immunol. 2013, 14(October (10)):1007-1013.
16. Burzyn D., Kuswanto W., Kolodin D., Shadrach Jennifer L., Cerletti M., Jang Y., Sefik E., Tan Tze G., Wagers Amy J., Benoist C., Mathis D. A special population of regulatory T cells potentiates muscle repair. Cell 2013, 155(6):1282-1295. (12/5/).
17. Carlson B.M., Faulkner J.A. Muscle transplantation between young and old rats: age of host determines recovery. Am. J. Physiol. 1989, 256(June (6 Pt. 1)):C1262-C1266.
18. Carlson M.E., Hsu M., Conboy I.M. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008, 454(7203):528-532. 07/24/print.
19. Carlson M.E., Suetta C., Conboy M.J., Aagaard P., Mackey A., Kjaer M., Conboy I. Molecular aging and rejuvenation of human muscle stem cells. EMBO Mol. Med. 2009, 1(November (8-9)):381-391.
20. Cassatella M.A. Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 1999, 73:369-509.
21. Castiglioni A., Corna G., Rigamonti E., Basso V., Vezzoli M., Monno A., Almada A.E., Mondino A., Wagers A.J., Manfredi A.A., Rovere-Querini P. FOXP3+ T cells recruited to sites of sterile skeletal muscle injury regulate the fate of satellite cells and guide effective tissue regeneration. PLoS One 2015, 10(6):e0128094.
22. Cerletti M., Shadrach J.L., Jurga S., Sherwood R., Wagers A.J. Regulation and function of skeletal muscle stem cells. Cold Spring Harb. Symp. Quant. Biol. 2008, 73:317-322.
23. Chakkalakal J.V., Jones K.M., Basson M.A., Brack A.S. The aged niche disrupts muscle stem cell quiescence. Nature 2012, 490(October (7420)):355-360.
24. Chakravarthy M.V., Abraha T.W., Schwartz R.J., Fiorotto M.L., Booth F.W. Insulin-like growth factor-i extends in vitro replicative life span of skeletal muscle satellite cells by enhancing G1/S cell cycle progression via the activation of phosphatidylinositol 3'-kinase/Akt signaling pathway. J. Biol. Chem. 2000, 275(November (46)):35942-35952.
25. Chen S.E., Gerken E., Zhang Y., Zhan M., Mohan R.K., Li A.S., Reid M.B., Li Y.P. Role of TNF-alpha signaling in regeneration of cardiotoxin-injured muscle. Am. J. Physiol. Cell Physiol. 2005, 289(November (5)):C1179-1187.
26. Cheng M., Nguyen M.H., Fantuzzi G., Koh T.J. Endogenous interferon-gamma is required for efficient skeletal muscle regeneration. Am. J. Physiol. Cell Physiol. 2008, 294(May (5)):C1183-1191.
27. Conboy I.M., Conboy M.J., Wagers A.J., Girma E.R., Weissman I.L., Rando T.A. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433(7027):760-764. (02/17/print).
28. Cosgrove B.D., Gilbert P.M., Porpiglia E., Mourkioti F., Lee S.P., Corbel S.Y., Llewellyn M.E., Delp S.L., Blau H.M. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat. Med. 2014, 20(3):255-264. 03//print.
29. Crameri R.M., Aagaard P., Qvortrup K., Langberg H., Olesen J., Kjaer M. Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J. Physiol. 2007, 583(August (Pt. 1)):365-380.
30. Cruz-Jentoft A.J., Baeyens J.P., Bauer J.M., Boirie Y., Cederholm T., Landi F., Martin F.C., Michel J.P., Rolland Y., Schneider S.M., Topinkova E., Vandewoude M., Zamboni M. Sarcopenia: european consensus on definition and diagnosis: report of the european working group on sarcopenia in older people. Age Ageing 2010, 39(July (4)):412-423.
31. De Rosa S.C., Lu F.X., Yu J., Perfetto S.P., Falloon J., Moser S., Evans T.G., Koup R., Miller C.J., Roederer M. Vaccination in humans generates broad T cell cytokine responses. J. Immunol. 2004, 173(November (9)):5372-5380.
32. Degens H. The role of systemic inflammation in age-related muscle weakness and wasting. Scand. J. Med. Sci. Sports 2010, 20(February (1)):28-38.
33. Deng B., Wehling-Henricks M., Villalta S.A., Wang Y., Tidball J.G. IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration. J. Immunol. 2012, 189(October (7)):3669-3680.
34. Dumke B.R., Lees S.J. Age-related impairment of T cell-induced skeletal muscle precursor cell function. Am. J. Physiol. Cell Physiol. 2011, 300(June (6)):C1226-1233.
35. Dumont N., Bouchard P., Frenette J. Neutrophil-induced skeletal muscle damage: a calculated and controlled response following hindlimb unloading and reloading. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295(December (6)):R1831-R1838.
36. Egan B., Zierath J.R. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013, 17(February (2)):162-184.
37. Elabd C., Cousin W., Upadhyayula P., Chen R.Y., Chooljian M.S., Li J., Kung S., Jiang K.P., Conboy I.M. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat. Commun. 2014, 5. 06/10/online.
38. English K.L., Paddon-Jones D. Protecting muscle mass and function in older adults during bed rest. Curr. Opin. Clin. Nutr. Metab. Care 2010, 13(January (1)):34-39.
39. Ershler W.B., Keller E.T. Age-associated increased interleukin-6 gene expression, late-life diseases and frailty. Annu. Rev. Med. 2000, 51:245-270.
40. Farup J., Madaro L., Puri P.L., Mikkelsen U.R. Interactions between muscle stem cells, mesenchymal-derived cells and immune cells in muscle homeostasis, regeneration and disease. Cell Death Dis. 2015, 6:e1830.
41. Forbes S.J., Rosenthal N. Preparing the ground for tissue regeneration: from mechanism to therapy. Nat. Med. 2014, 20(August (8)):857-869.
42. Franceschi C., Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69(June (Suppl. 1)):S4-S9.
43. Franceschi C., Bonafe M., Valensin S., Olivieri F., De Luca M., Ottaviani E., De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 2000, 908(June):244-254.
44. Fried L.P., Tangen C.M., Walston J., Newman A.B., Hirsch C., Gottdiener J., Seeman T., Tracy R., Kop W.J., Burke G., McBurnie M.A. Frailty in older adults: evidence for a phenotype. J. Gerontol. A Biol. Sci. Med. Sci. 2001, 56(March (3)):M146-M156.
45. Fry C.S., Lee J.D., Mula J., Kirby T.J., Jackson J.R., Liu F., Yang L., Mendias C.L., Dupont-Versteegden E.E., McCarthy J.J., Peterson C.A. Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat. Med. 2015, 21(1):76-80. 01//print.
46. Fujishima S., Hoffman A.R., Vu T., Kim K.J., Zheng H., Daniel D., Kim Y., Wallace E.F., Larrick J.W., Raffin T.A. Regulation of neutrophil interleukin 8 gene expression and protein secretion by LPS, TNF-alpha, and IL-1 beta. J. Cell. Physiol. 1993, 154(March (3)):478-485.
47. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19(July (1)):71-82.
48. Glass D., Roubenoff R. Recent advances in the biology and therapy of muscle wasting. Ann. N. Y. Acad. Sci. 2010, 1211(November):25-36.
49. Glass D.J. Molecular mechanisms modulating muscle mass. Trends Mol. Med. 2003, 9(August (8)):344-350.
50. Huey K.A., Meador B.M., Krzyszton C.P., Johnson R.W. Effects of IL-10 and age on IL-6 IL-1 beta, and TNF alpha responses to an acute inflammatory insult in mouse skeletal muscle. Faseb J. 2008, 22(April):p1.
51. Janssen I. The epidemiology of sarcopenia. Clin. Geriatr. Med. 2011, 27(August (3)):355.
52. Janssen I., Heymsfield S.B., Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J. Am. Geriatr. Soc. 2002, 50(May (5)):889-896.
53. Jetten N., Verbruggen S., Gijbels M.J., Post M.J., De Winther M.P.J., Donners M. Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 2014, 17(January (1)):109-118.
54. Joanisse S., Gillen J.B., Bellamy L.M., McKay B.R., Tarnopolsky M.A., Gibala M.J., Parise G. Evidence for the contribution of muscle stem cells to nonhypertrophic skeletal muscle remodeling in humans. FASEB J. 2013, 27(November (11)):4596-4605.
55. Josefowicz S.Z., Lu L.F., Rudensky A.Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 2012, 30:531-564.
56. Kim K.D., Zhao J., Auh S., Yang X.M., Du P.S., Tang H., Fu Y.X. Adaptive immune cells temper initial innate responses. Nat. Med. 2007, 13(October (10)):1248-1252.
57. Kuang S., Kuroda K., Le Grand F., Rudnicki M.A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007, 129(June (5)):999-1010.
58. Langen R.C., Van Der Velden J.L., Schols A.M., Kelders M.C., Wouters E.F., Janssen-Heininger Y.M. Tumor necrosis factor-alpha inhibits myogenic differentiation through MyoD protein destabilization. FASEB J. 2004, 18(February (2)):227-237.
59. Lepper C., Partridge T.A., Fan C.M. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 2011, 138(September (17)):3639-3646.
60. Leto D., Saltiel A.R. Regulation of glucose transport by insulin: traffic control of GLUT4. Nat. Rev. Mol. Cell Biol. 2012, 13(June (6)):383-396.
61. Levings M.K., Bacchetta R., Schulz U., Roncarolo M.G. The role of IL-10 and TGF-beta in the differentiation and effector function of T regulatory cells. Int. Arch. Allergy Immunol. 2002, 129(December (4)):263-276.
62. Lexell J. Human aging, muscle mass and fiber-type composition. J. Gerontol. A Biol. Sci. Med. Sci. 1995, 50(November):11-16.
63. Lexell J., Taylor C.C., Sjostrom M. What is the cause of the aging atrophy-total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15-year-old to 83-year-old men. J. Neurol. Sci. 1988, 84(April (2-3)):275-294.
64. Liu Q.C., Zha X.H., Faralli H., Yin H., Louis-Jeune C., Perdiguero E., Pranckeviciene E., Munoz-Canoves P., Rudnicki M.A., Brand M., Perez-Iratxeta C., Dilworth F.J. Comparative expression profiling identifies differential roles for Myogenin and p38 alpha MAPK signaling in myogenesis. J. Mol. Cell Biol. 2012, 4(December (6)):386-397.
65. Lu H., Huang D., Ransohoff R.M., Zhou L. Acute skeletal muscle injury: CCL2 expression by both monocytes and injured muscle is required for repair. FASEB J. 2011, 25(October (10)):3344-3355.
66. Lu H., Huang D., Saederup N., Charo I.F., Ransohoff R.M., Zhou L. Macrophages recruited via CCR2 produce insulin-like growth factor-1 to repair acute skeletal muscle injury. FASEB J. 2011, 25(January (1)):358-369.
67. Mackey A.L., Bojsen-Moller J., Qvortrup K., Langberg H., Suetta C., Kalliokoski K.K., Kjaer M., Magnusson S.P. Evidence of skeletal muscle damage following electrically stimulated isometric muscle contractions in humans. J. Appl. Physiol. (1985) 2008, 105(November (5)):1620-1627.
68. Madaro L., Bouche M. From innate to adaptive immune response in muscular dystrophies and skeletal muscle regeneration: the role of lymphocytes. Biomed. Res. Int. 2014, 2014:438675.
69. Maden-Wilkinson T.M., McPhee J.S., Rittweger J., Jones D.A., Degens H. Thigh muscle volume in relation to age, sex and femur volume age, sex and femur volume. Age (Dordr) 2014, 36(February (1)):383-393.
70. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25(December (12)):677-686.
71. Martinez C.O., McHale M.J., Wells J.T., Ochoa O., Michalek J.E., McManus L.M., Shireman P.K. Regulation of skeletal muscle regeneration by CCR2-activating chemokines is directly related to macrophage recruitment. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299(September (3)):R832-842.
72. McCarthy J.J., Mula J., Miyazaki M., Erfani R., Garrison K., Farooqui A.B., Srikuea R., Lawson B.A., Grimes B., Keller C., Van Zant G., Campbell K.S., Esser K.A., Dupont-Versteegden E.E., Peterson C.A. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 2011, 138(September (17)):3657-3666.
73. Merly F., Lescaudron L., Rouaud T., Crossin F., Gardahaut M.F. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 1999, 22(June (6)):724-732.
74. Mildner M., Hacker S., Haider T., Gschwandtner M., Werba G., Barresi C., Zimmermann M., Golabi B., Tschachler E., Ankersmit H.J. Secretome of peripheral blood mononuclear cells enhances wound healing. PLoS One 2013, 8(3):e60103.
75. Moore D.R. Keeping older muscle young through dietary protein and physical activity12. Adv. Nutr. 2014, 5(September (5)):599s-607s.
76. Morley J.E., Baumgartner R.N., Roubenoff R., Mayer J., Nair K.S. Sarcopenia. J. Lab. Clin. Med. 2001, 137(April (4)):231-243.
77. Morrison J., Partridge T., Bou-Gharios G. Nude mutation influences limb skeletal muscle development. Matrix Biol. 2005, 23(January (8)):535-542.
78. Mourkioti F., Rosenthal N. IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol. 2005, 26(October (10)):535-542.
79. Naito A.T., Sumida T., Nomura S., Liu M.L., Higo T., Nakagawa A., Okada K., Sakai T., Hashimoto A., Hara Y., Shimizu I., Zhu W., Toko H., Katada A., Akazawa H., Oka T., Lee J.K., Minamino T., Nagai T., Walsh K., Kikuchi A., Matsumoto M., Botto M., Shiojima I., Komuro I. Complement C1q activates canonical Wnt signaling and promotes aging-related phenotypes. Cell 2012, 149(June (6)):1298-1313.
80. Narici M.V., Maffulli N. Sarcopenia: characteristics mechanisms and functional significance. Br. Med. Bull. 2010, 95:139-159.
81. Nosaka K., Aldayel A., Jubeau M., Chen T.C. Muscle damage induced by electrical stimulation. Eur. J. Appl. Physiol. 2011, 111(October (10)):2427-2437.
82. Novak M.L., Weinheimer-Haus E.M., Koh T.J. Macrophage activation and skeletal muscle healing following traumatic injury. J. Pathol. 2014, 232(February (3)):344-355.
83. O'Mahony L., Holland J., Jackson J., Feighery C., Hennessy T.P., Mealy K. Quantitative intracellular cytokine measurement: age-related changes in proinflammatory cytokine production. Clin. Exp. Immunol. 1998, 113(August (2)):213-219.
84. Paliwal P., Pishesha N., Wijaya D., Conboy I.M. Age dependent increase in the levels of osteopontin inhibits skeletal muscle regeneration. Aging (Albany NY) 2012, 4(August (8)):553-566.
85. Paulsen G., Mikkelsen U.R., Raastad T., Peake J.M. Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise. Exerc. Immunol. Rev. 2012, 18:42-97.
86. Paulsen G., Crameri R., Benestad H.B., Fjeld J.G., Morkrid L., Hallen J., Raastad T. Time course of leukocyte accumulation in human muscle after eccentric exercise. Med. Sci. Sports Exerc. 2010, 42(January (1)):75-85.
87. Peake J., Della Gatta P., Cameron-Smith D. Aging and its effects on inflammation in skeletal muscle at rest and following exercise-induced muscle injury. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298(June (6)):R1485-R1495.
88. Pedersen B.K. Muscles and their myokines. J. Exp. Biol. 2011, 214(January (Pt. 2)):337-346.
89. Pelosi M., De Rossi M., Barberi L., Musarò A. IL-6 impairs myogenic differentiation by downmodulation of p90RSK/eEF2 and mTOR/p70S6K axes without affecting AKT activity. BioMed. Res. Int. 2014, 12.
90. Piasecki M., Ireland A., Stashuk D., Hamilton-Wright A., Jones D.A., McPhee J.S. Age-related neuromuscular changes affecting human vastus lateralis. J. Physiol. 2015, 1-12. 10.1113/JP271087.
91. Plackett T.P., Boehmer E.D., Faunce D.E., Kovacs E.J. Aging and innate immune cells. J. Leukoc. Biol. 2004, 76(August (2)):291-299.
92. Relaix F., Zammit P.S. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 2012, 139(August (16)):2845-2856.
93. Rodriguez-Prados J.C., Traves P.G., Cuenca J., Rico D., Aragones J., Martin-Sanz P., Cascante M., Bosca L. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation trate fate in activated macrophages. J. Immunol. 2010, 185(July (1)):605-614.
94. Saclier M., Cuvellier S., Magnan M., Mounier R., Chazaud B. Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J. 2013, 280(September (17)):4118-4130.
95. Serrano A.L., Baeza-Raja B., Perdiguero E., Jardi M., Munoz-Canoves P. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 2008, 7(January (1)):33-44.
96. Shavlakadze T., McGeachie J., Grounds M.D. Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology 2010, 11(June (3)):363-376.
97. Siegel A.L., Kuhlmann P.K., Cornelison D.D. Muscle satellite cell proliferation and association: new insights from myofiber time-lapse imaging le satellite cell proliferation and association: new insights from myofiber time-lapse imaging. Skelet. Muscle 2011, 1(1):7.
98. Siegel A.L., Atchison K., Fisher K.E., Davis G.E., Cornelison D.D. 3D timelapse analysis of muscle satellite cell motility. Stem Cells 2009, 27(October (10)):2527-2538.
99. Sinha M., Jang Y.C., Oh J., Khong D., Wu E.Y., Manohar R., Miller C., Regalado S.G., Loffredo F.S., Pancoast J.R., Hirshman M.F., Lebowitz J., Shadrach J.L., Cerletti M., Kim M.J., Serwold T., Goodyear L.J., Rosner B., Lee R.T., Wagers A.J. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 2014, 344(May (6184)):649-652.
100. Smith C., Kruger M.J., Smith R.M., Myburgh K.H. The inflammatory response to skeletal muscle injury. Sports Med. 2008, 38(11):947-969.
101. Smythe G.M., Shavlakadze T., Roberts P., Davies M.J., McGeachie J.K., Grounds M.D. Age influences the early events of skeletal muscle regeneration: studies of whole muscle grafts transplanted between young (8 weeks) and old (13-21 months) mice. Exp. Gerontol. 2008, 43(June (6)):550-562.
102. Sousa-Victor P., Gutarra S., Garcia-Prat L., Rodriguez-Ubreva J., Ortet L., Ruiz-Bonilla V., Jardi M., Ballestar E., Gonzalez S., Serrano A.L., Perdiguero E., Munoz-Canoves P. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 2014, 506(February (7488)):316-321.
103. Steensberg A., Keller C., Starkie R.L., Osada T., Febbraio M.A., Pedersen B.K. IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2002, 283(December (6)):E1272-E1278.
104. Sun D., Martinez C.O., Ochoa O., Ruiz-Willhite L., Bonilla J.R., Centonze V.E., Waite L.L., Michalek J.E., McManus L.M., Shireman P.K. Bone marrow-derived cell regulation of skeletal muscle regeneration. FASEB J. 2009, 23(February (2)):382-395.
105. Tedesco F.S., Dellavalle A., Diaz-Manera J., Messina G., Cossu G. Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J. Clin. Invest. 2010, 120(January (1)):11-19.
106. Tidball J.G. Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288(February (2)):R345-R353.
107. Tidball J.G., Welc S.S. Macrophage-derived IGF-1 is a potent coordinator of myogenesis and inflammation in regenerating muscle. Mol. Ther. 2015, 23(7):1134-1135. 07//print.
108. Tidball J.G., Dorshkind K., Wehling-Henricks M. Shared signaling systems in myeloid cell-mediated muscle regeneration. Development 2014, 141(March (6)):1184-1196.
109. Tonkin J., Temmerman L., Sampson R.D., Gallego-Colon E., Barberi L., Bilbao D., Schneider M.D., Musaro A., Rosenthal N. Monocyte/macrophage-derived IGF-1 orchestrates murine skeletal muscle regeneration and modulates autocrine polarization. Mol. Ther. 2015, 23(July (7)):1189-1200.
110. Torrente Y., El Fahime E., Caron N.J., Del Bo R., Belicchi M., Pisati F., Tremblay J.P., Bresolin N. Tumor necrosis factor-alpha (TNF-alpha) stimulates chemotactic response in mouse myogenic cells. Cell Transplant. 2003, 12(1):91-100.
111. Uezumi A., Ikemoto-Uezumi M., Tsuchida K. Roles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle. Front. Physiol. 2014, 5.
112. Verdijk L.B., Gleeson B.G., Jonkers R.A., Meijer K., Savelberg H.H., Dendale P., van Loon L.J. Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64(March (3)):332-339.
113. Villalta S.A., Nguyen H.X., Deng B., Gotoh T., Tidball J.G. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet. 2009, 18(February (3)):482-496.
114. Walston J., Fedarko N., Yang H., Leng S., Beamer B., Espinoza S., Lipton A., Zheng H., Becker K. The physical and biological characterization of a frail mouse model. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63(April (4)):391-398.
115. Wang H., Melton D.W., Porter L., Sarwar Z.U., McManus L.M., Shireman P.K. Altered macrophage phenotype transition impairs skeletal muscle regeneration. Am. J. Pathol. 2014, 184(4):1167-1184.
116. Warren G.L., Hulderman T., Jensen N., McKinstry M., Mishra M., Luster M.I., Simeonova P.P. Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J. 2002, 16(October (12)):1630-1632.
117. Warren G.L., O'Farrell L., Summan M., Hulderman T., Mishra D., Luster M.I., Kuziel W.A., Simeonova P.P. Role of CC chemokines in skeletal muscle functional restoration after injury. Am. J. Physiol. Cell Physiol. 2004, 286(May (5)):C1031-1036.
118. Wehling M., Spencer M.J., Tidball J.G. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 2001, 155(October (1)):123-131.
119. Wright C.R., Brown E.L., Della Gatta P.A., Fatouros I.G., Karagounis L.G., Terzis G., Mastorakos G., Michailidis Y., Mandalidis D., Spengos K., Chatzinikolaou A., Methenitis S., Draganidis D., Jamurtas A.Z., Russell A.P. Regulation of granulocyte colony-stimulating factor and its receptor in skeletal muscle is dependent upon the type of inflammatory stimulus. J. Interferon Cytokine Res. 2015, 35(September (9)):710-719.
120. Xu Q., Wu Z. The insulin-like growth factor-phosphatidylinositol 3-kinase-akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J. Biol. Chem. 2000, 275(November (47)):36750-36757.
121. Yablonkareuveni Z., Balestreri T.M., Bowenpope D.F. Regulation of proliferation and differentiation of myoblasts derived from adult-mouse skeletal-muscle by specific isoforms of PDGF. J. Cell Biol. 1990, 111(October (4)):1623-1629.
122. Yin H., Price F., Rudnicki M.A. Satellite cells and the muscle stem cell niche. Physiol. Rev. 2013, 93(January (1)):23-67.
123. Yousef H., Conboy M.J., Morgenthaler A., Schlesinger C., Bugaj L., Paliwal P., Greer C., Conboy I.M., Schaffer D. Systemic attenuation of the TGF-β pathway by a single drug simultaneously rejuvenates hippocampal neurogenesis and myogenesis in the same old mammal. Oncotarget 2015, 6(May (14)):11959-11978.
124. Zhang C., Li Y., Wu Y., Wang L., Wang X., Du J. Interleukin-6/signal transducer and activator of transcription 3 (STAT3) pathway is essential for macrophage infiltration and myoblast proliferation during muscle regeneration. J. Biol. Chem. 2013, 288(January (3)):1489-1499.