Age-related impairment of t cell-induced skeletal muscle precursor cell function

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 6, 2011, Pages

  Dumke, Breanna R ^b   Lees, Simon J ^a,b  

^a NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Immune cell; Migration; Proliferation; Regeneration; Satellite cell

Indexed keywords

INTERLEUKIN 2;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL REGENERATION; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; IMMUNOCOMPETENT CELL; MALE; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MUSCLE MASS; MUSCLE PRECURSOR CELL; MUSCLE STRENGTH; NONHUMAN; PRIORITY JOURNAL; RAT; SATELLITE CELL; SKELETAL MUSCLE; STEM CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; HUMANS; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; PRECURSOR CELLS, T-LYMPHOID; RATS; RATS, INBRED F344; T-LYMPHOCYTES;

ANIMALIA;

EID: 79957633640     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00354.2010     Document Type: Article

References (73)

1. Adams GR, Caiozzo VJ, Haddad F, Baldwin KM. Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J Physiol Cell Physiol 283: C1182-C1195, 2002.
2. Allen RE, Boxhorn LK. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138: 311-315, 1989.
3. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165: 307-312, 1995.
4. Almekinders LC, Gilbert JA. Healing of experimental muscle strains and the effects of nonsteroidal antiinflammatory medication. Am J Sports Med 14: 303-308, 1986.
5. Alway SE, Degens H, Krishnamurthy G, Smith CA. Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am J Physiol Cell Physiol 283: C66-C76, 2002.
6. Barani AE, Durieux AC, Sabido O, Freyssenet D. Age-related changes in the mitotic and metabolic characteristics of muscle-derived cells. J Appl Physiol 95: 2089-2098, 2003.
7. Barlow Y, Willoughby J. Pathophysiology of soft tissue repair. Br Med Bull 48: 698-711, 1992.
8. Bischoff R. Proliferation of muscle satellite cells on intact myofibers in culture. Dev Biol 115: 129-139, 1986.
9. Bischoff R. A satellite cell mitogen from crushed adult muscle. Dev Biol 115: 140-147, 1986.
10. Bischoff R, Heintz C. Enhancement of skeletal muscle regeneration. Dev Dyn 201: 41-54, 1994.
11. Blotnick S, Peoples GE, Freeman MR, Eberlein TJ, 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 USA 91: 2890-2894, 1994.
12. Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317: 807-810, 2007.
13. Braun T, Buschhausen-Denker G, Bober E, Tannich E, Arnold HH. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J 8: 701-709, 1989.
14. Brooks SV, Faulkner JA. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am J Physiol Cell Physiol 258: C436-C442, 1990.
15. Chakravarthy MV, Davis BS, Booth FW. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle. J Appl Physiol 89: 1365-1379, 2000.
16. Cheng M, Nguyen MH, Fantuzzi G, Koh TJ. Endogenous interferongamma is required for efficient skeletal muscle regeneration. Am J Physiol Cell Physiol 294: C1183-C1191, 2008.
17. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 302: 1575-1577, 2003.
18. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433: 760-764, 2005.
19. Conboy IM, Rando TA. Aging, stem cells and tissue regeneration: lessons from muscle. Cell Cycle 4: 407-410, 2005.
20. Cook DR, Doumit ME, Merkel RA. Transforming growth factor-beta, basic fibroblast growth factor, and platelet-derived growth factor-BB interact to affect proliferation of clonally derived porcine satellite cells. J Cell Physiol 157: 307-312, 1993.
21. Cornelison DD. Context matters: in vivo and in vitro influences on muscle satellite cell activity. J Cell Biochem 105: 663-669, 2008.
22. Cornelison DD, Wold BJ. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191: 270-283, 1997.
23. Corsetti G, Pasini E, D'Antona G, Nisoli E, Flati V, Assanelli D, Dioguardi FS, Bianchi R. Morphometric changes induced by amino acid supplementation in skeletal and cardiac muscles of old mice. Am J Cardiol 101: 26E-34E, 2008.
24. De Rosa SC, Lu FX, Yu J, Perfetto SP, Falloon J, Moser S, Evans TG, Koup R, Miller CJ, Roederer M. Vaccination in humans generates broad T cell cytokine responses. J Immunol 173: 5372-5380, 2004.
25. DiMario J, Buffinger N, Yamada S, Strohman RC. Fibroblast growth factor in the extracellular matrix of dystrophic (mdx) mouse muscle. Science 244: 688-690, 1989.
26. Farini A, Meregalli M, Belicchi M, Battistelli M, Parolini D, D'Antona G, Gavina M, Ottoboni L, Constantin G, Bottinelli R, Torrente Y. T and B lymphocyte depletion has a marked effect on the fibrosis of dystrophic skeletal muscles in the scid/mdx mouse. J Pathol 213: 229-238, 2007.
27. Fasth AE, Dastmalchi M, Rahbar A, Salomonsson S, Pandya JM, Lindroos E, Nennesmo I, Malmberg KJ, Soderberg-Naucler C, Trollmo C, Lundberg IE, Malmstrom V. T cell infiltrates in the muscles of patients with dermatomyositis and polymyositis are dominated by CD28null T cells. J Immunol 183: 4792-4799, 2009.
28. Fava RA, Olsen NJ, Postlethwaite AE, Broadley KN, Davidson JM, Nanney LB, Lucas C, Townes AS. Transforming growth factor beta 1 (TGF-beta 1) induced neutrophil recruitment to synovial tissues: implications for TGF-beta-driven synovial inflammation and hyperplasia. J Exp Med 173: 1121-1132, 1991.
29. Florini JR, Ewton DZ, Magri KA. Hormones, growth factors, and myogenic differentiation. Annu Rev Physiol 53: 201-216, 1991.
30. Fritsch RD, Shen X, Sims GP, Hathcock KS, Hodes RJ, Lipsky PE. Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J Immunol 175: 6489-6497, 2005.
31. Goldspink G, Fernandes K, Williams PE, Wells DJ. Age-related changes in collagen gene expression in the muscles of mdx dystrophic and normal mice. Neuromuscul Disord 4: 183-191, 1994.
32. Griffiths RD. Muscle mass, survival, and the elderly ICU patient. Nutrition 12: 456-458, 1996.
33. Hathaway MR, Pampusch MS, Hembree JR, Dayton WR. Transforming growth factor beta-1 facilitates establishing clonal populations of ovine muscle satellite cells. J Anim Sci 72: 2001-2007, 1994.
34. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551, 2001.
35. Hidestrand M, Richards-Malcolm S, Gurley CM, Nolen G, Grimes B, Waterstrat A, Zant GV, Peterson CA. Sca-1-expressing nonmyogenic cells contribute to fibrosis in aged skeletal muscle. J Gerontol A Biol Sci Med Sci 63: 566-579, 2008.
36. Jump SS, Childs TE, Zwetsloot KA, Booth FW, Lees SJ. Fibroblast growth factor 2-stimulated proliferation is lower in muscle precursor cells from old rats. Exp Physiol 94: 739-748, 2009.
37. Krug N, Madden J, Redington AE, Lackie P, Djukanovic R, Schauer U, Holgate ST, Frew AJ, Howarth PH. T-cell cytokine profile evaluated at the single cell level in BAL and blood in allergic asthma. Am J Respir Cell Mol Biol 14: 319-326, 1996.
38. Lees SJ, Childs TE, Booth FW. Age-dependent FOXO regulation of p27Kip1 expression via a conserved binding motif in rat muscle precursor cells. Am J Physiol Cell Physiol 295: C1238-C1246, 2008.
39. Lees SJ, Childs TE, Booth FW. p21(Cip1) expression is increased in ambient oxygen, compared to estimated physiological (5%) levels in rat muscle precursor cell culture. Cell Prolif 41: 193-207, 2008.
40. Lees SJ, Rathbone CR, Booth FW. Age-associated decrease in muscle precursor cell differentiation. Am J Physiol Cell Physiol 290: C609-C615, 2006.
41. Lees SJ, Zwetsloot KA, Booth FW. Muscle precursor cells isolated from aged rats exhibit an increased tumor necrosis factor- alpha response. Aging Cell 8: 26-35, 2009.
42. Lefaucheur JP, Sebille A. Basic fibroblast growth factor promotes in vivo muscle regeneration in murine muscular dystrophy. Neurosci Lett 202: 121-124, 1995.
43. Levings MK, Bacchetta R, Schulz U, Roncarolo MG. The role of IL-10 and TGF-beta in the differentiation and effector function of T regulatory cells. Int Arch Allergy Immunol 129: 263-276, 2002.
44. Levings MK, Sangregorio R, Sartirana C, Moschin AL, Battaglia M, Orban PC, Roncarolo MG. Human CD25+CD4+ T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. J Exp Med 196: 1335-1346, 2002.
45. Lorenzon P, Bandi E, de Guarrini F, Pietrangelo T, Schafer R, Zweyer M, Wernig A, Ruzzier F. Ageing affects the differentiation potential of human myoblasts. Exp Gerontol 39: 1545-1554, 2004.
46. Machida S, Booth FW. Increased nuclear proteins in muscle satellite cells in aged animals as compared to young growing animals. Exp Gerontol 39: 1521-1525, 2004.
47. Mendias CL, Tatsumi R, Allen RE. Role of cyclooxygenase-1 and -2 in satellite cell proliferation, differentiation, and fusion. Muscle Nerve 30: 497-500, 2004.
48. Merrick MA. Secondary injury after musculoskeletal trauma: a review and update. J Athl Train 37: 209-217, 2002.
49. Mezzogiorno A, Coletta M, Zani BM, Cossu G, Molinaro M. Paracrine stimulation of senescent satellite cell proliferation by factors released by muscle or myotubes from young mice. Mech Ageing Dev 70: 35-44, 1993.
50. Michalopoulos GK, Zarnegav R. Hepatocyte growth factor. Hepatology 15: 149-155, 1992.
51. Mikkelsen UR, Langberg H, Helmark IC, Skovgaard D, Andersen LL, Kjaer M, Mackey AL. Local NSAID infusion inhibits satellite cell proliferation in human skeletal muscle after eccentric exercise. J Appl Physiol 107: 1600-1611, 2009.
52. Miner JH, Wold B. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci USA 87: 1089-1093, 1990.
53. Mishra DK, Friden J, Schmitz MC, Lieber RL. Anti-inflammatory medication after muscle injury. A treatment resulting in short-term improvement but subsequent loss of muscle function. J Bone Joint Surg Am 77: 1510-1519, 1995.
54. Morgan JE, Partridge TA. Muscle satellite cells. Int J Biochem Cell Biol 35: 1151-1156, 2003.
55. Morrison J, Lu QL, Pastoret C, Partridge T, Bou-Gharios G. T-celldependent fibrosis in the mdx dystrophic mouse. Lab Invest 80: 881-891, 2000.
56. Morrison J, Partridge T, Bou-Gharios G. Nude mutation influences limb skeletal muscle development. Matrix Biol 23: 535-542, 2005.
57. Muir AR, Kanji AH, Allbrook D. The structure of the satellite cells in skeletal muscle. J Anat 99: 435-444, 1965.
58. Muraguchi A, Hirano T, Tang B, Matsuda T, Horii Y, Nakajima K, Kishimoto T. The essential role of B cell stimulatory factor 2 (BSF-2/IL-6) for the terminal differentiation of B cells. J Exp Med 167: 332-344, 1988.
59. Pinney DF, Pearson-White SH, Konieczny SF, Latham KE, Emerson CP Jr. Myogenic lineage determination and differentiation: evidence for a regulatory gene pathway. Cell 53: 781-793, 1988.
60. Rantanen J, Hurme T, Lukka R, Heino J, Kalimo H. Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab Invest 72: 341-347, 1995.
61. Rhodes SJ, Konieczny SF. Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev 3: 2050-2061, 1989.
62. Rudnicki MA, Le Grand F, McKinnell I, Kuang S. The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73: 323-331, 2008.
63. Schaerli P, Britschgi M, Keller M, Steiner UC, Steinmann LS, Moser B, Pichler WJ. Characterization of human T cells that regulate neutrophilic skin inflammation. J Immunol 173: 2151-2158, 2004.
64. Schultz E, Jaryszak DL, Valliere CR. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8: 217-222, 1985.
65. Sheehan SM, Tatsumi R, Temm-Grove CJ, Allen RE. HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 23: 239-245, 2000.
66. Smith C, Kruger MJ, Smith RM, Myburgh KH. The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med 38: 947-969, 2008.
67. Spencer MJ, Montecino-Rodriguez E, Dorshkind K, Tidball JG. Helper (CD4(+)) and cytotoxic (CD8(+)) T cells promote the pathology of dystrophin-deficient muscle. Clin Immunol 98: 235-243, 2001.
68. Spencer MJ, Tidball JG. Do immune cells promote the pathology of dystrophin-deficient myopathies? Neuromuscul Disord 11: 556-564, 2001.
69. Tatsumi R, Liu X, Pulido A, Morales M, Sakata T, Dial S, Hattori A, Ikeuchi Y, Allen RE. Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. Am J Physiol Cell Physiol 290: C1487-C1494, 2006.
70. Tidball JG. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288: R345-R353, 2005.
71. Tidball JG, Villalta SA. Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integr Comp Physiol 298: R1173-R1187, 2010.
72. Vetrone SA, Montecino-Rodriguez E, Kudryashova E, Kramerova I, Hoffman EP, Liu SD, Miceli MC, Spencer MJ. Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J Clin Invest 119: 1583-1594, 2009.
73. Zanin-Zhorov A, Cahalon L, Tal G, Margalit R, Lider O, Cohen IR. Heat shock protein 60 enhances CD4+ CD25+ regulatory T cell function via innate TLR2 signaling. J Clin Invest 116: 2022-2032, 2006.