Impact of ageing on muscle cell regeneration

Ageing Research Reviews

Volumn 10, Issue 1, 2011, Pages 35-42

  Carosio, Silvia ^a   Berardinelli, Maria Grazia ^a   Aucello, Michela ^a   Musarò, Antonio ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b EDITH COWAN UNIVERSITY   (Australia)

Author keywords

Aging; Growth factors; Muscle regeneration; Satellite cells; Stem cells; Tissue niche

Indexed keywords

AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; HUMAN; INFLAMMATION; MOLECULAR DYNAMICS; MUSCLE CELL REGENERATION; MUSCLE INJURY; MUSCLE REGENERATION; NONHUMAN; REVIEW; SKELETAL MUSCLE SATELLITE CELL; STEM CELL; STEM CELL NICHE;

AGING; ANIMALS; HUMANS; INFLAMMATION; MUSCLE CELLS; MUSCLE, SKELETAL; MUSCLES; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 78650239733     PISSN: 15681637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.arr.2009.08.001     Document Type: Review

References (119)

1. Allen R.E., Boxhorn L.K. 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. 1989, 138:311-315.
2. Angelini C., Fanin M., Menegazzo E., Freda M.P., Duggan D.J., Hoffman E.P. Homozygous alpha-sarcoglycan mutation in two siblings: one asymptomatic and one steroid-responsive mild limb-girdle muscular dystrophy patient. Muscle Nerve 1998, 21:769-775.
3. 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, 204:1057-1069.
4. Asakura A., Seale P., Girgis-Gabardo A., Rudnicki M.A. Myogenic specification of side population cells in skeletal muscle. J. Cell Biol. 2002, 159:123-134.
5. Barton-Davis E.R., Shoturma D.I., Musarò A., Rosenthal N., Sweeney H.L. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15603-15607.
6. Beauchamp J.R., Morgan J.E., Pagel C.N., Partridge T.A. Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J. Cell Biol. 1999, 144:1113-1122.
7. Beauchamp J.R., Heslop L., Yu D.S., Tajbakhsh S., Kelly R.G., Wernig A., Buckingham M.E., Partridge T.A., Zammit P.S. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 2000, 151:1221-1234.
8. Belcastro A.N., Arthur G.D., Albisser T.A., Raj D.A. Heart, liver, and skeletal muscle myeloperoxidase activity during exercise. J. Appl. Physiol. 1996, 80:1331-1335.
9. Bischoff R. The satellite cell and muscle regeneration. Myology 1994, 97-118. McGraw-Hill, New York. A.G. Engel, C. Franzini-Armstrong (Eds.).
10. Bodensteiner J.B., Engel A.G. Intracellular calcium accumulation in Duchenne dystrophy and other myopathies: a study of 567,000 muscle fibers in 114 biopsies. Neurology 1978, 28:439-446.
11. Brack A.S., Bildsoe H., Hughes S.M. 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, 118:4813-4821.
12. Brack A.S., Conboy M.J., Roy S., Lee M., Kuo C.J., Keller C., Rando T.A. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007, 317:807-810.
13. Brack A.S., Rando T.A. Age-dependent changes in skeletal muscle regeneration. Skeletal Muscle Repair and Regeneration (Advances in Muscle Research) 2008, 359-374. Springer-Verlag, The Netherlands. S. Schiaffino, T. Partridge (Eds.).
14. Brack A.S., Conboy I.M., Conboy M.J., Shen J., Rando T.A. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008, 2:50-59.
15. Bucala R., Spiegel L.A., Chesney J., Hogan M., Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol. Med. 1994, 1:71-81.
16. Buckingham M. Skeletal muscle progenitor cells and the role of Pax genes. C. R. Biol. 2007, 330:530-533.
17. Calandra T., Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 2003, 3:791-800.
18. Cantini M., Carraro U. Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J. Neuropathol. Exp. Neurol. 1995, 54:121-128.
19. Cantini M., Massimino M.L., Bruson A., Catani C., Dalla Libera L., Carraro U. Macrophages regulate proliferation and differentiation of satellite cells. Biochem. Biophys. Res. Commun. 1994, 202:1688-1696.
20. Carlson B.M., Faulkner J.A. Muscle transplantation between young and old rats: age of host determines recovery. Am. J. Physiol. 1989, 256:C1262-C1266.
21. Carnac G., Ricaud S., Vernus B., Bonnieu A. Myostatin: biology and clinical relevance. Mini Rev. Med. Chem. 2006, 6:765-770.
22. Chilosi M., Poletti V., Zamò A., Lestani M., Montagna L., Piccoli P., Pedron S., Bertaso M., Scarpa A., Murer B., Cancellieri A., Maestro R., Semenzato G., Dogliosi C. Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am. J. Pathol. 2003, 162:1495-1502.
23. Conboy I.M., Rando T.A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 2002, 3:397-409.
24. Conboy I.M., Conboy M.J., Smythe G.M., Rando T.A. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003, 302:1575-1577.
25. 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, 433:760-764.
26. Connolly A.M., Pestronk A., Mehta S., Al-Lozi M. Primary alpha-sarcoglycan deficiency responsive to immunosuppression over three years. Muscle Nerve 1998, 21:1549-1553.
27. Cornelison D.D., Filla M.S., Stanley H.M., Rapraeger A.C., Olwin B.B. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 2001, 239:79-94.
28. Creuzet S., Lescaudron L., Li Z., Fontaine-Pérus J. MyoD, myogenin, and desmin-nls-lacZ transgene emphasize the distinct patterns of satellite cell activation in growth and regeneration. Exp. Cell Res. 1998, 243:241-253.
29. Crisco J.J., Jokl P., Heinen G.T., Connell M.D., Panjabi M.M. A muscle contusion injury model. Biomechanics, physiology, and histology. Am. J. Sports Med. 1994, 22:702-710.
30. De Angelis L., Berghella L., Coletta M., Lattanzi L., Zanchi M., Cusella-De Angelis M.G., Ponzetto C., Cossu G. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J. Cell Biol. 1999, 147:869-878.
31. Dominique J.E., Gerard C. Myostatin regulation of muscle development: molecular basis, natural mutations, physiopathological aspects. Exp. Cell Res. 2006, 312:2401-2414.
32. Douglas M.R., Morrison K.E., Salmon M., Buckley C.D. Why does inflammation persist: a dominant role for the stromal microenvironment?. Exp. Rev. Mol. Med. 2002, 4:1-18.
33. Engert J.C., Berglund E.B., Rosenthal N. Proliferation precedes differentiation in IGF-I-stimulated myogenesis. J. Cell Biol. 1996, 135:431-440.
34. Fan Y., Maley M., Beilharz M., Grounds M. Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve 1996, 19:853-860.
35. Fielding R.A., Manfredi T.J., Ding W., Fiatarone M.A., Evans W.J., Cannon J.G. Acute phase response in exercise. III. Neutrophil and IL-1β accumulation in skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1993, 265:R166-R172.
36. Garry D.J., Yang Q., Bassel-Duby R., Williams R.S. Persistent expression of MNF identifies myogenic stem cells in postnatal muscles. Dev. Biol. 1997, 188:280-294.
37. Gayraud-Morel B., Chrétien F., Tajbakhsh S. Skeletal muscle as a paradigm for regenerative biology and medicine. Regen. Med. 2009, 4:293-319.
38. Gibson M.C., Schultz E. Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve 1983, 6:574-580.
39. Goetsch S.C., Hawke T.J., Gallardo T.D., Richardson J.A., Garry D.J. Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol. Genomics 2003, 14:261-271.
40. Grounds M.D. Phagocytosis of necrotic muscle in muscle isografts is influenced by the strain, age, and sex of host mice. J. Pathol. 1987, 153:71-82.
41. Grounds M.D., McGeachie J.K. A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis. Cell Tissue Res. 1987, 250:563-569.
42. Gussoni E., Soneoka Y., Strickland C.D., Buzney E.A., Khan M.K., Flint A.F., Kunkel L.M., Mulligan R.C. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 1999, 401:390-394.
43. Hawke T.J., Garry D.J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 2001, 91:534-551.
44. Horber F.F., Haymond M.W. Human growth hormone prevents the protein catabolic side effects of prednisone in humans. J. Clin. Invest. 1990, 86:265-272.
45. Irintchev A., Zeschnigk M., Starzinski-Powitz A., Wernig A. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 1994, 199:326-337.
46. Jansen K.M., Pavlath G.K. Molecular control of mammalian myoblast fusion. Methods Mol. Biol. 2008, 475:115-133.
47. Jespersen J., Kjaer M., Schjerling P. The possible role of myostatin in skeletal muscle atrophy and cachexia. Scand. J. Med. Sci. Sports 2006, 16:74-82.
48. Jesse T.L., LaChance R., Iademarco M.F., Dean D.C. Interferon regulatory factor-2 is a transcriptional activator in muscle where it regulates expression of vascular cell adhesion molecule-1. J. Cell Biol. 1998, 140:1265-1276.
49. Jiang F., Parsons C.J., Stefanovic B. Gene expression profile of quiescent and activated rat hepatic stellate cells implicates Wnt signaling pathway in activation. J. Hepatol. 2006, 45:401-409.
50. Kambadur R., Sharma M., Smith T.P.L., Bass J.J. Mutations in myostatin (GDF8) in double-muscled Belgian blue and piedmontese cattle. Genome Res. 1997, 7:910-915.
51. Karpati G., Carpenter S., Prescott S. Small-caliber skeletal muscle fibers do not suffer necrosis in mdx mouse dystrophy. Muscle Nerve 1988, 11:795-803.
52. Karpati G., Molnar M.J. Muscle fibre regeneration in human skeletal muscle diseases. Skeletal Muscle Repair and Regeneration (Advances in Muscle Research) 2008, 45-64. Springer-Verlag, The Netherlands. S. Schiaffino, T. Partridge (Eds.).
53. Kjaer M., Jespersen J.G. The battle to keep or lose skeletal muscle with ageing. J. Physiol. 2009, 587:1-2.
54. Krippendorf B.B., Riley D.A. Distinguishing unloading- versus reloading-induced changes in rat soleus muscle. Muscle Nerve 1993, 16:99-108.
55. Kuang S., Chargé S.B., Seale P., Huh M., Rudnicki M.A. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 2006, 172:103-113.
56. Kuang S., Kuroda K., Le Grand F., Rudnicki M.A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007, 129:999-1010.
57. Kuhnert F., Davis C.R., Wang H.T., Chu P., Lee M., Yuan J., Nusse R., Kuo C.J. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:266-271.
58. Langley B., Thomas M., Bishop A., Sharma M., Gilmour S., Kambadur R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J. Biol. Chem. 2002, 277:49831-49840.
59. Lee H.J., Goring W., Ochs M., Muhlfeld C., Steding G., Paprotta I., Engel W., Adham I.M. Sox15 is required for skeletal muscle regeneration. Mol. Cell. Biol. 2004, 24:8428-8436.
60. Lehto M., Järvinen M., Nelimarkka O. Scar formation after skeletal muscle injury. A histological and autoradiographical study in rats. Arch. Orthop. Trauma Surg. 1986, 104:366-370.
61. Lepper C., Conway S.J., Fan C.M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 2009, 460:627-631.
62. Li Y., Foster W., Deasy B.M., Chan Y., Prisk V., Tang Y., Cummins J., Huard J. Transforming growth factor-β1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am. J. Pathol. 2004, 164:1007-1019.
63. 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, 25:677-686.
64. Manzur A.Y., Kuntzer T., Pike M., Swan A. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst. Rev. 2004, 2:CD003725.
65. Massimino M.L., Rapizzi E., Cantini M., Libera L.D., Mazzoleni F., Arslan P., Carraro U. ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochem. Biophys. Res. Commun. 1997, 235:754-759.
66. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
67. McPherron A.C., Lawler A.M., Lee S.J. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387:83-90.
68. Mechtersheimer G., Staudter M., Moller P. Expression of the natural killer (NK) cell-associated antigen CD56 (Leu-19), which is identical to the 140-kDa isoform of N-CAM, in neural and skeletal muscle cells and tumors derived therefrom. Ann. N. Y. Acad. Sci. 1992, 650:311-316.
69. Mendias C.L., Bakhurin K.I., Faulkner J.A. Tendons of myostatin-deficient mice are small, brittle, and hypocellular. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:388-393.
70. Merly F., Lescaudron L., Rouaud T., Crossin F., Gardahaut M.F. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 1999, 22:724-732.
71. Messina G., Biressi S., Cossu G. Non muscle stem cells and muscle regeneration. Skeletal Muscle Repair and Regeneration (Advances in Muscle Research) 2008, 65-84. Springer-Verlag, The Netherlands. S. Schiaffino, T. Partridge (Eds.).
72. Moss F.P., Leblond C.P. Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 1971, 170:421-435.
73. Muller S., Ronfani L., Bianchi M.E. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J. Intern. Med. 2004, 255:332-343.
74. Musarò A., Rosenthal N. Maturation of the myogenic program is induced by postmitotic expression of insulin-like growth factor I. Mol. Cell. Biol. 1999, 19:3115-3124.
75. Musarò A., McCullagh K.J., Naya F.J., Olson E.N., Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 1999, 400:581-585.
76. Musarò A., McCullagh K., Paul A., Houghton L., Dobrowolny G., Molinaro M., Barton E.R., Sweeney H.L., Rosenthal N. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 2001, 27:195-200.
77. Musarò A., Rosenthal N. The critical role of insulin-like growth factor-1 isoforms in the physiopathology of skeletal muscle. Curr. Genomics 2006, 3:19-32.
78. Mutsaers S.E., Bishop J.E., McGrouther G., Laurent G.J. Mechanisms of tissue repair: from wound healing to fibrosis. Int. J. Biochem. Cell Biol. 1997, 29:5-17.
79. Nguyen H.X., Tidball J.G. Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro. J. Physiol. 2003, 547:125-132.
80. Oberc M.A., Engel W.K. Ultrastructural localization of calcium in normal and abnormal skeletal muscle. Lab. Invest. 1977, 36:566-577.
81. Oustanina S., Hause G., Braun T. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 2004, 23:3430-3439.
82. Pelosi L., Giacinti C., Nardis C., Borsellino G., Rizzuto E., Nicoletti C., Wannenes F., Battistini L., Rosenthal N., Molinaro M., Musarò A. Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J. 2007, 21:1393-1402.
83. Polesskaya A., Seale P., Rudnicki M.A. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 2003, 113:841-852.
84. Rabinowitz S.S., Gordon S. Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli. J. Exp. Med. 1991, 174:827-836.
85. Ramprasad M.P., Fischer W., Witztum J.L., Sambrano G.R., Quehenberger O., Steinberg D. The 94-to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:9580-9584.
86. Reisz-Porszasz S., Bhasin S., Artaza J.N., Shen R., Sinha-Hikim I., Hogue A., Fielder T.J., Gonzalez-Cadavid N.F. Lower skeletal muscle mass in male transgenic mice with muscle-specific overexpression of myostatin. Am. J. Physiol. Endocrinol. Metab. 2003, 285:E876-E888.
87. Relaix F., Montarras D., Zaffran S., Gayraud-Morel B., Rocancourt D., Tajbakhsh S., Mansouri A., Cumano A., Buckingham M. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 2006, 172:91-102.
88. Rios R., Carneiro I., Arce V.M., Devesa J. Myostatin regulates cell survival during C2C12 myogenesis. Biochem. Biophys. Res. Commun. 2001, 280:561-566.
89. Rosenthal S.M., Cheng Z.-Q. Opposing early and late effects of insulin-like growth factor I on differentiation and the cell cycle regulatory retinoblastoma protein in skeletal myoblasts. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:10307-10311.
90. Sajko S., Kubinova L., Cvetko E., Kreft M., Wernig A., Erzen I. Frequency of M-cadherin-stained satellite cells declines in human muscles during aging. J. Histochem. Cytochem. 2004, 52:179-185.
91. Scicchitano B.M., Rizzuto E., Musarò A. Counteracting muscle wasting in aging and neuromuscular diseases: the critical role of IGF-1. Aging 2009, 5:1-7.
92. Schmidt K., Glaser G., Wernig A., Wegner M., Rosorius O. Sox8 is a specific marker for muscle satellite cells and inhibits myogenesis. J. Biol. Chem. 2003, 278:29769-29775.
93. Schuelke M., Wagner K.R., Stolz L.E., Hubner C., Riebel T., Komen W., Braun T., Tobin J.F., Lee S.J. Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med. 2004, 350:2682-2688.
94. Schultz E., Lipton B.H. Skeletal muscle satellite cells: changes in proliferation potential as a function of age. Mech. Ageing Dev. 1982, 20:377-383.
95. Schultz E. Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 1996, 175:84-94.
96. Seale P., Sabourin L.A., Girgis-Gabardo A., Mansouri A., Gruss P., Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells. Cell 2000, 102:777-786.
97. Shefer G., Van de Mark D.P., Richardson J.B., Yablonka-Reuveni Z. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev. Biol. 2006, 294:50-66.
98. Shefer G., Yablonka-Reuveni Z. The ins and outs of satellite cell myogenesis: the role of the ruling growth factors. Skeletal Muscle Repair and Regeneration (Advances in Muscle Research) 2008, 107-144. Springer-Verlag, The Netherlands. S. Schiaffino, T. Partridge (Eds.).
99. Siriett V., Salerno M.S., Berry C., Nicholas G., Bower R., Kambadur R., Sharma M. Antagonism of myostatin enhances muscle regeneration during sarcopenia. Mol. Ther. 2007, 15:1463-1470.
100. Snow M.H. The effects of aging on satellite cells in skeletal muscles of mice and rats. Cell Tissue Res. 1977, 185:399-408.
101. St. Pierre B.A., Tidball J.G. Differential response of macrophage subpopulations to soleus muscle reloading following rat hindlimb suspension. J. Appl. Physiol. 1994, 77:290-297.
102. Summan M., Warren G.L., Mercer R.R., Chapman R., Hulderman T., Van Rooijen N., Simeonova P.P. Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R1488-1495.
103. Tamaki T., Akatsuka A., Ando K., Nakamura Y., Matsuzawa H., Hotta T., Roy R.R., Edgerton V.R. Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle. J. Cell Biol. 2002, 157:571-577.
104. Tatsumi R., Anderson J.E., Nevoret C.J., Halevy O., Allen R.E. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol. 1998, 194:114-128.
105. Teixeira C.F.P., Zamuner S.R., Zuliani J.P., Fernandes C.M., Cruz-Hofling M.A., Fernandes I., Chaves F., Gutierrez J.M. Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom. Muscle Nerve 2003, 28:449-459.
106. Thomas M., Langley B., Berry C., Sharma M., Kirk S., Bass J.J., Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 2000, 275:40235-40243.
107. Tidball J.G. Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R345-R353.
108. Tidball J.G., Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J. Physiol. 2007, 578:327-336.
109. Vasyutina E., Lenhard D.C., Birchmeie C. Notch function in myogenesis. Cell Cycle 2007, 6:1451-1454.
110. Velasco B., Cacicedo L., Escalada J., Lopez-Fernandez J., Sanchez-Franco F. Growth hormone gene expression and secretion in aging rats is age dependent and not age-associated weight increase related. Endocrinology 1998, 139:1314-1320.
111. 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, 18:482-496.
112. Volonte D., Liu Y., Galbiati F. The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J. 2005, 19:237-239.
113. Wagner K.R. Muscle regeneration through myostatin inhibition. Curr. Opin. Rheumatol. 2005, 17:720-724.
114. Watt F.M., Hogan B.L. Out of Eden: stem cells and their niches. Science 2000, 287:1427-1430.
115. Winn N., Paul A., Musaró A., Rosenthal N. Insulin-like growth factor isoforms in skeletal muscle aging, regeneration, and disease. Cold Spring Harb. Symp. Quant. Biol. 2002, 67:507-518.
116. Yablonka-Reuveni Z., Rivera A.J. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev. Biol. 1994, 164:588-603.
117. Yan Z., Choi S., Liu X., Zhang M., Schageman J.J., Lee S.Y., Hart R., Lin L., Thurmond F.A., Williams R.S. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 2003, 278:8826-8836.
118. Zacks S.I., Sheff M.F. Age-related impeded regeneration of mouse minced anterior tibial muscle. Muscle Nerve 1982, 5:152-161.
119. Zammit P.S. The muscle satellite cell: the story of a cell on the edge. Skeletal Muscle Repair and Regeneration (Advances in Muscle Research) 2008, 45-64. Springer-Verlag, The Netherlands. S. Schiaffino, T. Partridge (Eds.).