Impairment of IGF-I expression and anabolic signaling following ischemia/reperfusion in skeletal muscle of old mice

Experimental Gerontology

Volumn 46, Issue 4, 2011, Pages 265-272

  Hammers, David W ^a   Matheny, Ronald W ^b   Sell, Christian ^c   Adamo, Martin L ^b   Walters, Thomas J ^d   Estep, J Scot ^d   Farrar, Roger P ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

Author keywords

FoxO; MTOR; Muscle regeneration; Sarcopenia; Tourniquet

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHRL1;

AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HINDLIMB; INTRACELLULAR SIGNALING; MALE; MOUSE; MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION; SKELETAL MUSCLE;

AGING; ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; DNA PRIMERS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; PROTO-ONCOGENE PROTEINS C-AKT; REPERFUSION INJURY; RNA, MESSENGER; SARCOPENIA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

MUS;

EID: 79952708482     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2010.11.002     Document Type: Article

References (66)

1. Adamo M.L., Farrar R.P. Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res. Rev. 2006, 5:310-331.
2. Adams G.R. Autocrine and/or paracrine insulin-like growth factor-I activity in skeletal muscle. Clin. Orthop. Relat. Res. 2002, S188-S196.
3. Adams G.R., McCue S.A. Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J. Appl. Physiol. 1998, 84:1716-1722.
4. Barton E.R. The ABCs of IGF-I isoforms: impact on muscle hypertrophy and implications for repair. Appl. Physiol. Nutr. Metab. 2006, 31:791-797.
5. 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. USA 1998, 95:15603-15607.
6. Blaisdell F.W. The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc. Surg. 2002, 10:620-630.
7. Bodine S.C. mTOR signaling and the molecular adaptation to resistance exercise. Med. Sci. Sports Exerc. 2006, 38:1950-1957.
8. Bodine S.C., Stitt T.N., Gonzalez M., Kline W.O., Stover G.L., Bauerlein R., Zlotchenko E., Scrimgeour A., Lawrence J.C., Glass D.J., Yancopoulos G.D. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001, 3:1014-1019.
9. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
10. Brooks S.V., Faulkner J.A. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am. J. Physiol. 1990, 258:C436-C442.
11. Brooks S.V., Faulkner J.A. The magnitude of the initial injury induced by stretches of maximally activated muscle fibres of mice and rats increases in old age. J. Physiol. 1996, 497(Pt 2):573-580.
12. Burnett P.E., Barrow R.K., Cohen N.A., Snyder S.H., Sabatini D.M. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl Acad. Sci. USA 1998, 95:1432-1437.
13. 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.
14. Chakravarthy M.V., Davis B.S., Booth F.W. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle. J. Appl. Physiol. 2000, 89:1365-1379.
15. Charge S.B., Rudnicki M.A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 2004, 84:209-238.
16. Conboy I.M., Rando T.A. Aging, stem cells and tissue regeneration: lessons from muscle. Cell Cycle 2005, 4:407-410.
17. 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.
18. 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. 1997, 272:6653-6662.
19. D'Ercole A.J., Stiles A.D., Underwood L.E. Tissue concentrations of somatomedin C: further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms of action. Proc. Natl Acad. Sci. USA 1984, 81:935-939.
20. Dluzniewska J., Sarnowska A., Beresewicz M., Johnson I., Srai S.K., Ramesh B., Goldspink G., Gorecki D.C., Zablocka B. A strong neuroprotective effect of the autonomous C-terminal peptide of IGF-1 Ec (MGF) in brain ischemia. Faseb J. 2005, 19:1896-1898.
21. Edwall D., Schalling M., Jennische E., Norstedt G. Induction of insulin-like growth factor I messenger ribonucleic acid during regeneration of rat skeletal muscle. Endocrinology 1989, 124:820-825.
22. Foster A.H., Carlson B.M. Myotoxicity of local anesthetics and regeneration of the damaged muscle fibers. Anesth. Analg. 1980, 59:727-736.
23. Garcia-Fernandez M., Castilla-Cortazar I., Diaz-Sanchez M., Navarro I., Puche J.E., Castilla A., Casares A.D., Clavijo E., Gonzalez-Baron S. Antioxidant effects of insulin-like growth factor-I (IGF-I) in rats with advanced liver cirrhosis. BMC Gastroenterol. 2005, 5:7.
24. Hammers D.W., Merritt E.K., Matheny W., Adamo M.L., Walters T.J., Estep J.S., Farrar R.P. Functional deficits and insulin-like growth factor-I gene expression following tourniquet-induced injury of skeletal muscle in young and old rats. J. Appl. Physiol. 2008, 105:1274-1281.
25. Hayashi S., Aso H., Watanabe K., Nara H., Rose M.T., Ohwada S., Yamaguchi T. Sequence of IGF-I, IGF-II, and HGF expression in regenerating skeletal muscle. Histochem. Cell Biol. 2004, 122:427-434.
26. Heron-Milhavet L., Mamaeva D., LeRoith D., Lamb N.J., Fernandez A. Impaired muscle regeneration and myoblast differentiation in mice with a muscle-specific KO of IGF-IR. J. Cell. Physiol. 2010, 225:1-6.
27. 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. 2003, 549:409-418.
28. Hill M., Wernig A., Goldspink G. Muscle satellite (stem) cell activation during local tissue injury and repair. J. Anat. 2003, 203:89-99.
29. Huang H., Tindall D.J. Dynamic FoxO transcription factors. J. Cell Sci. 2007, 120:2479-2487.
30. Hwee D.T., Bodine S.C. Age-related deficit in load-induced skeletal muscle growth. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64:618-628.
31. Jallali N., Ridha H., Thrasivoulou C., Butler P., Cowen T. Modulation of intracellular reactive oxygen species level in chondrocytes by IGF-1, FGF, and TGF-beta1. Connect. Tissue Res. 2007, 48:149-158.
32. Jennische E., Hansson H.A. Regenerating skeletal muscle cells express insulin-like growth factor I. Acta Physiol. Scand. 1987, 130:327-332.
33. Jennische E., Skottner A., Hansson H.A. Satellite cells express the trophic factor IGF-I in regenerating skeletal muscle. Acta Physiol. Scand. 1987, 129:9-15.
34. Joulia-Ekaza D., Cabello G. The myostatin gene: physiology and pharmacological relevance. Curr. Opin. Pharmacol. 2007, 7:310-315.
35. Kooijman R. Regulation of apoptosis by insulin-like growth factor (IGF)-I. Cytokine Growth Factor Rev. 2006, 17:305-323.
36. Kravchenko I.V., Furalyov V.A., Khotchenkov V.P., Popov V.O. Monoclonal antibodies to mechano-growth factor. Hybridoma (Larchmt) 2006, 25:300-305.
37. Latres E., Amini A.R., Amini A.A., Griffiths J., Martin F.J., Wei Y., Lin H.C., Yancopoulos G.D., Glass D.J. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J. Biol. Chem. 2005, 280:2737-2744.
38. Lee S., Barton E.R., Sweeney H.L., Farrar R.P. Viral expression of insulin-like growth factor-I enhances muscle hypertrophy in resistance-trained rats. J. Appl. Physiol. 2004, 96:1097-1104.
39. Machida S., Spangenburg E.E., Booth F.W. Forkhead transcription factor FoxO1 transduces insulin-like growth factor's signal to p27Kip1 in primary skeletal muscle satellite cells. J. Cell. Physiol. 2003, 196:523-531.
40. Mammucari C., Milan G., Romanello V., Masiero E., Rudolf R., Del Piccolo P., Burden S.J., Di Lisi R., Sandri C., Zhao J., Goldberg A.L., Schiaffino S., Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007, 6:458-471.
41. Matheny R.W., Adamo M.L. Role of Akt isoforms in IGF-I-mediated signaling and survival in myoblasts. Biochem. Biophys. Res. Commun. 2009, 389:117-121.
42. Matheny R.W., Nindl B.C., Adamo M.L. Minireview: mechano-growth factor: a putative product of IGF-I gene expression involved in tissue repair and regeneration. Endocrinology 2010, 151:865-875.
43. McEwen J.A., Inkpen K. Surgical tourniquet technology adapted for military and prehospital use. RTO-MP-HFM 2004, 109:1-12.
44. McLoughlin T.J., Smith S.M., DeLong A.D., Wang H., Unterman T.G., Esser K.A. FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am. J. Physiol. Cell Physiol. 2009, 297:C548-C555.
45. 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. 2001, 27:195-200.
46. Musaro A., Giacinti C., Borsellino G., Dobrowolny G., Pelosi L., Cairns L., Ottolenghi S., Cossu G., Bernardi G., Battistini L., Molinaro M., Rosenthal N. Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc. Natl Acad. Sci. USA 2004, 101:1206-1210.
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. 2001, 505:259-263.
48. Pelosi L., Giacinti C., Nardis C., Borsellino G., Rizzuto E., Nicoletti C., Wannenes F., Battistini L., Rosenthal N., Molinaro M., Musaro A. Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. Faseb J. 2007, 21:1393-1402.
49. Philippou A., Stavropoulou A., Sourla A., Pissimissis N., Halapas A., Maridaki M., Koutsilieris M. Characterization of a rabbit antihuman mechano growth factor (MGF) polyclonal antibody against the last 24 amino acids of the E domain. In Vivo 2008, 22:27-35.
50. Puche J.E., Garcia-Fernandez M., Muntane J., Rioja J., Gonzalez-Baron S., Castilla Cortazar I. Low doses of insulin-like growth factor-I induce mitochondrial protection in aging rats. Endocrinology 2008, 149:2620-2627.
51. Rantanen T. Muscle strength, disability and mortality. Scand. J. Med. Sci. Sports 2003, 13:3-8.
52. Rathbone C.R., Booth F.W., Lees S.J. FoxO3a preferentially induces p27Kip1 expression while impairing muscle precursor cell-cycle progression. Muscle Nerve 2008, 37:84-89.
53. 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. 2001, 3:1009-1013.
54. Sacco A., Doyonnas R., LaBarge M.A., Hammer M.M., Kraft P., Blau H.M. IGF-I increases bone marrow contribution to adult skeletal muscle and enhances the fusion of myelomonocytic precursors. J. Cell Biol. 2005, 171:483-492.
55. Sacheck J.M., Ohtsuka A., McLary S.C., Goldberg A.L. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E591-E601.
56. Sadeh M. Effects of aging on skeletal muscle regeneration. J. Neurol. Sci. 1988, 87:67-74.
57. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004, 117:399-412.
58. Senf S.M., Dodd S.L., McClung J.M., Judge A.R. Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. Faseb J. 2008, 22:3836-3845.
59. Sengupta A., Molkentin J.D., Yutzey K.E. FoxO transcription factors promote autophagy in cardiomyocytes. J. Biol. Chem. 2009, 284:28319-28331.
60. Stitt T.N., Drujan D., Clarke B.A., Panaro F., Timofeyva Y., Kline W.O., Gonzalez M., Yancopoulos G.D., Glass D.J. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 2004, 14:395-403.
61. Thaveau F., Zoll J., Bouitbir J., Ribera F., Di Marco P., Chakfe N., Kretz J.G., Piquard F., Geny B. Contralateral leg as a control during skeletal muscle ischemia-reperfusion. J. Surg. Res. 2009, 155:65-69.
62. Walters T.J., Kragh J.F., Kauvar D.S., Baer D.G. The combined influence of hemorrhage and tourniquet application on the recovery of muscle function in rats. J. Orthop. Trauma 2008, 22:47-51.
63. Walters T.J., Kragh J.F., Baer D.G. Influence of fiber-type composition on recovery from tourniquet-induced skeletal muscle ischemia-reperfusion injury. Appl. Physiol. Nutr. Metab. 2008, 33:272-281.
64. Yang S.Y., Goldspink G. Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett. 2002, 522:156-160.
65. Zerba E., Komorowski T.E., Faulkner J.A. Free radical injury to skeletal muscles of young, adult, and old mice. Am. J. Physiol. 1990, 258:C429-C435.
66. Zhao J., Brault J.J., Schild A., Cao P., Sandri M., Schiaffino S., Lecker S.H., Goldberg A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6:472-483.