IGF-1 induces human myotube hypertrophy by increasing cell recruitment

Experimental Cell Research

Volumn 299, Issue 1, 2004, Pages 148-158

  Jacquemin, V ^a   Furling, D ^a   Bigot, A ^a   Butler Browne, G S ^a   Mouly, V ^a  

^a CNRS   (France)

Author keywords

5 bromo 2 deoxyuridine; BrdU; differentiation medium; DM; FBS; FDA; fetal bovine serum; fluorescein diacetate; Hypertrophy; IGF 1; IGF binding proteins; IGFBPs; insulin like growth factor 1; MPD; Proliferation; Satellite cell; Skeletal muscle

Indexed keywords

MYOSIN HEAVY CHAIN; SOMATOMEDIN C;

ADOLESCENT; ADULT; ARTICLE; CELL CULTURE; CELL DIVISION; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; MUSCLE HYPERTROPHY; MYOBLAST; MYOTUBE; NEWBORN; PRIORITY JOURNAL; PROTEIN CONTENT; SATELLITE CELL;

BOVINAE; RODENTIA;

EID: 4043061445     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.05.023     Document Type: Article

References (62)

1. Adams G.R., Haddad F. The relationships among IGF-1, DNA content, and protein accumulation during skeletal muscle hypertrophy. J. Appl. Physiol. 81:1996;2509-2516
2. Adams G.R., McCue S.A. Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J. Appl. Physiol. 84:1998;1716-1722
3. Baroffio A., Bochaton-Piallat M.L., Gabbiani G., Bader C.R. Heterogeneity in the progeny of single human muscle satellite cells. Differentiation. 59:1995;259-268
4. Barton-Davis E.R., Shoturma D.I., Musaro 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. 95:1998;15603-15607
5. Barton-Davis E.R., Shoturma D.I., Sweeney H.L. Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiol. Scand. 167:1999;301-305
6. Bischoff R., Heintz C. Enhancement of skeletal muscle regeneration. Dev. Dyn. 201:1994;41-54
7. Blau H.M., Webster C., Pavlath G.K. Defective myoblasts identified in Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U. S. A. 80:1983;4856-4860
8. Brooks S.V., Faulkner J.A. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am. J. Physiol. 258:1990;C436-C442
9. 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. 275:2000;35942-35952
10. Chakravarthy M.V., Booth F.W., Spangenburg E.E. The molecular responses of skeletal muscle satellite cells to continuous expression of IGF-1: implications for the rescue of induced muscular atrophy in aged rats. Int. J. Sport Nutr. Exerc. Metab. 11 Suppl.:2001;S44-S48
11. Chakravarthy M.V., Davis B.S., Booth F.W. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle. J. Appl. Physiol. 89:2000;1365-1379
12. Coleman M.E., DeMayo F., Yin K.C., Lee H.M., Geske R., Montgomery C., Schwartz R.J. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J. Biol. Chem. 270:1995;12109-12116
13. Coolican S.A., Samuel D.S., Ewton D.Z., McWade F.J., Florini J.R. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J. Biol. Chem. 272:1997;6653-6662
14. Cooper R.N., Tajbakhsh S., Mouly V., Cossu G., Buckingham M., Butler-Browne G.S. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell Sci. 112:1999;2895-2901
15. Cristofalo V.J. Cellular biomarkers of aging. Exp. Gerontol. 23:1988;297-307
16. Decary S., Hamida C.B., Mouly V., Barbet J.P., Hentati F., Butler-Browne G.S. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscular Disord. 10:2000;113-120
17. Decary S., Mouly V., Butler-Browne G.S. Telomere length as a tool to monitor satellite cell amplification for cell-mediated gene therapy. Hum. Gene Ther. 7:1996;1347-1350
18. Decary S., Mouly V., Hamida C.B., Sautet A., Barbet J.P., Butler-Browne G.S. Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum. Gene Ther. 8:1997;1429-1438
19. Dupont-Versteegden E.E., Murphy R.J., Houle J.D., Gurley C.M., Peterson C.A. Mechanisms leading to restoration of muscle size with exercise and transplantation after spinal cord injury. Am. J. Physiol.: Cell Physiol. 279:2000;C1677-C1684
20. Edom F., Mouly V., Barbet J.P., Fiszman M.Y., Butler-Browne G.S. Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. Dev. Biol. 164:1994;219-229
21. Edom-Vovard F., Mouly V., Barbet J.P., Butler-Browne G.S. The four populations of myoblasts involved in human limb muscle formation are present from the onset of primary myotube formation. J. Cell Sci. 112(Pt 2):1999;191-199
22. Fiorotto M.L., Schwartz R.J., Delaughter M.C. Persistent IGF-I overexpression in skeletal muscle transiently enhances DNA accretion and growth. FASEB J. 17:2003;59-60
23. Florini J.R., Ewton D.Z., Coolican S.A. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr. Rev. 17:1996;481-517
24. Florini J.R., Ewton D.Z., Roof S.L. Insulin-like growth factor-I stimulates terminal myogenic differentiation by induction of myogenin gene expression. Mol. Endocrinol. 5:1991;718-724
25. Furmanczyk P.S., Quinn L.S. Interleukin-15 increases myosin accretion in human skeletal myogenic cultures. Cell Biol. Int. 27:2003;845-851
26. Gambke B., Rubinstein N.A. A monoclonal antibody to the embryonic myosin heavy chain of rat skeletal muscle. J. Biol. Chem. 259:1984;12092-12100
27. Grounds M.D. Reasons for the degeneration of ageing skeletal muscle: a central role for IGF-1 signalling. Biogerontology. 3:2002;19-24
28. Haugk K.L., Wilson H.M., Swisshelm K., Quinn L.S. Insulin-like growth factor (IGF)-binding protein-related protein-1: an autocrine/paracrine factor that inhibits skeletal myoblast differentiation but permits proliferation in response to IGF. Endocrinology. 141:2000;100-110
29. Hayashi T., Ogawa T., Sato M., Tsuchida N., Fotovati A., Iwamoto H., Ikeuchi Y., Cassens R.G., Ito T. S-myotrophin promotes the hypertrophy of myotube as insulin-like growth factor-I does. Int. J. Biochem. Cell Biol. 33:2001;831-838
30. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37:1965;614-636
31. Hill M., Goldspink G. Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J. Physiol. 549:2003;409-418
32. Hyatt J.P., Roy R.R., Baldwin K.M., Edgerton V.R. Nerve activity-independent regulation of skeletal muscle atrophy: role of MyoD and myogenin in satellite cells and myonuclei. Am. J. Physiol.: Cell Physiol. 285:2003;C1161-C1173
33. Kadi F., Eriksson A., Holmner S., Butler-Browne G.S., Thornell L.E. Cellular adaptation of the trapezius muscle in strength-trained athletes. Histochem. Cell Biol. 111:1999;189-195
34. Karey K.P., Sirbasku D.A. Differential responsiveness of human breast cancer cell lines MCF-7 and T47D to growth factors and 17 beta-estradiol. Cancer Res. 48:1988;4083-4092
35. Kipling D. Telomere structure and telomerase expression during mouse development and tumorigenesis. Eur. J. Cancer. 33:1997;792-800
36. Lawlor M.A., Feng X., Everding D.R., Sieger K., Stewart C.E., Rotwein P. Dual control of muscle cell survival by distinct growth factor-regulated signaling pathways. Mol. Cell. Biol. 20:2000;3256-3265
37. Lawlor M.A., Rotwein P. Coordinate control of muscle cell survival by distinct insulin-like growth factor activated signaling pathways. J. Cell Biol. 151:2000;1131-1140
38. Li X., Eastman E.M., Schwartz R.J., Draghia-Akli R. Synthetic muscle promoters: activities exceeding naturally occurring regulatory sequences. Nat. Biotechnol. 17:1999;241-245
39. Liu J.P., Baker J., Perkins A.S., Robertson E.J., Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 75:1993;59-72
40. Marsh D.R., Hinds L.R., Lester W.S., Reinking B.E., Booth F.W. The force-frequency relationship is altered in regenerating and senescent rat skeletal muscle. Muscle Nerve. 21:1998;1265-1274
41. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9:1961;493-495
42. McBride T.A., Gorin F.A., Carlsen R.C. Prolonged recovery and reduced adaptation in aged rat muscle following eccentric exercise. Mech. Ageing Dev. 83:1995;185-200
43. McCall G.E., Allen D.L., Linderman J.K., Grindeland R.E., Roy R.R., Mukku V.R., Edgerton V.R. Maintenance of myonuclear domain size in rat soleus after overload and growth hormone/IGF-I treatment. J. Appl. Physiol. 84:1998;1407-1412
44. Moss F.P., Leblond C.P. Nature of dividing nuclei in skeletal muscle of growing rats. J. Cell Biol. 44:1970;459-462
45. Moss F.P., Leblond C.P. Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 170:1971;421-435
46. Musaro 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. 27:2001;195-200
47. Owino V., Yang S.Y., Goldspink G. Age-related loss of skeletal muscle function and the inability to express the autocrine form of insulin-like growth factor-1 (MGF) in response to mechanical overload. FEBS Lett. 505:2001;259-263
48. Rabinovsky E.D., Gelir E., Gelir S., Lui H., Kattash M., DeMayo F.J., Shenaq S.M., Schwartz R.J. Targeted expression of IGF-1 transgene to skeletal muscle accelerates muscle and motor neuron regeneration. FASEB J. 1:2002;1
49. Renault V., Piron-Hamelin G., Forestier C., DiDonna S., Decary S., Hentati F., Saillant G., Butler-Browne G.S., Mouly V. Skeletal muscle regeneration and the mitotic clock. Exp. Gerontol. 35:2000;711-719
50. Renault V., Rolland E., Thornell L.E., Mouly V., Butler-Browne G. Distribution of satellite cells in the human vastus lateralis muscle during aging. Exp. Gerontol. 37:2002;1513-1514
51. Renault V., Thornell L.E., Eriksson P.O., Butler-Browne G., Mouly V., Thorne L.E. Regenerative potential of human skeletal muscle during aging. Aging Cell. 1:2002;132-139
52. Rommel C., Bodine S.C., Clarke B.A., Rossman R., Nunez L., Stitt T.N., Yancopoulos G.D., Glass D.J. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3:2001;1009-1013
53. Rosenblatt J.D., Yong D., Parry D.J. Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve. 17:1994;608-613
54. Roubenoff R., Hughes V.A. Sarcopenia: current concepts. J. Gerontol., A., Biol. Sci. Med. Sci. 55:2000;M716-M724
55. Saha N.R., Usami T., Suzuki Y. A double staining flow cytometric assay for the detection of steroid induced apoptotic leucocytes in common carp (Cyprinus carpio). Dev. Comp. Immunol. 27:2003;351-363
56. Schmalbruch H., al-Amood W.S., Lewis D.M. Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J. Physiol. 441:1991;233-241
57. Semsarian C., Sutrave P., Richmond D.R., Graham R.M. Insulin-like growth factor (IGF-I) induces myotube hypertrophy associated with an increase in anaerobic glycolysis in a clonal skeletal-muscle cell model. Biochem. J. 339:1999;443-451
58. Semsarian C., Wu M.J., Ju Y.K., Marciniec T., Yeoh T., Allen D.G., Harvey R.P., Graham R.M. Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway. Nature. 400:1999;576-581
59. Vandenburgh H.H., Karlisch P., Shansky J., Feldstein R. Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture. Am. J. Physiol. 260:1991;C475-C484
60. Vlachopapadopoulou E., Zachwieja J.J., Gertner J.M., Manzione D., Bier D.M., Matthews D.E., Slonim A.E. Metabolic and clinical response to recombinant human insulin-like growth factor I in myotonic dystrophy - A clinical research center study. J. Clin. Endocrinol. Metab. 80:1995;3715-3723
61. Welle S., Bhatt K., Shah B., Thornton C. Insulin-like growth factor-1 and myostatin mRNA expression in muscle: comparison between 62-77 and 21-31 yr old men. Exp. Gerontol. 37:2002;833-839
62. Yang S., Alnaqeeb M., Simpson H., Goldspink G. Cloning and characterization of an IGF-1 isoform expressed in skeletal muscle subjected to stretch. J. Muscle Res. Cell Motil. 17:1996;487-495