Role of sustained overexpression of central nervous system IGF-I in the age-dependent decline of mouse excitation-contraction coupling

Journal of Membrane Biology

Volumn 212, Issue 3, 2006, Pages 147-161

  Moreno, Ramón Jiménez ^a   Messi, María Laura ^a   Zheng, Zhenlin ^a   Wang, Zhong Min ^a   Ye, Ping ^b   D'Ercole, Joseph A ^b   Delbono, Osvaldo ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Calcium channel; Insulin like growth factor I; Skeletal muscle

Indexed keywords

1,4 DIHYDROPYRIDINE RECEPTOR; CALCIUM CHANNEL; CALCIUM ION; RECEPTOR SUBUNIT; SOMATOMEDIN C;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; GENE OVEREXPRESSION; GROUPS BY AGE; IN VITRO STUDY; MOUSE; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE EXCITATION; MUSCLE FORCE; MUSCLE INNERVATION; MUSCLE MASS; MUSCLE STRENGTH; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SKELETAL MUSCLE; SOLEUS MUSCLE; TRANSGENIC MOUSE; WILD TYPE;

AGING; ANIMALS; CALCIUM SIGNALING; CENTRAL NERVOUS SYSTEM; ELECTROPHYSIOLOGY; GENE EXPRESSION; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE STRENGTH; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; SPINAL CORD;

MUS;

EID: 33947141368     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-006-0044-z     Document Type: Article

References (62)

1. Barton-Davis, E.R., Shoturma, D.I., Musaro, A., Rosenthal, N., Sweeney, H.L. 1998. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muslce function. Proc. Natl. Acad. Sci. USA 95:15603-15607
2. Brooks, S.V., Faulkner, J.A. 1988. Contractile properties of skeletal muscles from young, adult and aged mice. J. Physiol. 404:71-82
3. Buller, A.J., Eccles, J. C., Eccles, R.M. 1960a. Differentiation of fast and slow muscles in the cat hind limb. J. Physiol. 150:399-416
4. Buller, A.J., Eccles, J. C., Eccles, R.M. 1960b. Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J. Physiol. 150:417-439
5. Caroni, P., Grandes, P. 1990. Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin like growth factors. J. Cell Biol. 110:1307-1317
6. Coleman, M.E., DeMayo, F., Yin, K.C., Lee, H.M., Geske, R., Montgomery, C., Schwartz, R.J. 1995. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J. Biol. Chem. 270:12109-12116
7. Dai, Z., Takahashi, S.I., Wyk, J.J., D'Ercole, A.J. 1992. Creation of an autocrine model of insulin-like growth factor-I action in transfected FRTL-5 cells. Endocrinology 130:3175-3183
8. Delbono, O. 2003. Neural control of aging skeletal muscle. Aging Cell 2:21-29
9. D'Ercole, A.J., Ye, P., O'Kusky, J.R. 2002. Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 36:209-220
10. Dobrowolny, G., Giacinti, C., Pelosi, L., Nicoletti, C., Winn, N., Barberi, L., Molinaro, M., Rosenthal, N., Musaro, A. 2005. Muscle expression of a local IGF-I isoform protects motor neurons in an ALS mouse model. J. Cell Biol. 168:193-199
11. Eddinger, T.J., Cassens, R.G., Moss, R.L. 1986. Mechanical and histochemical characterization of skeletal muscles from senescent rats. Am. J. Physiol. 251:C421-C430
12. Einsiedel, L.J., Luff, A.R. 1992. Effect of partial denervation on motor units in the ageing rat medial gastrocnemius. J. Neurol. Sci. 112:178-184
13. Fervenza, F.C., Tsao, T., Hsu, F., Rabkin, R. 1999. Intrarenal insulin-like growth factor-1 axis after unilateral nephrectomy in rat. J. Am. Soc. Nephrol. 10:43-50
14. Fitts, R.H., Troup, J.P., Witzmann, F.A., Holloszy, J.O. 1984. The effect of ageing and exercise on skeletal muscle function. Mech. Ageing Dev. 27:161-172
15. Florini, J.R., Ewton, D.Z., Coolican, S.A. 1996. Growth hormone and insulin growth factor system in myogenesis. Endocr. Rev. 17:481-517
16. Giulian, G.G., Moss, R.L., Greaser, M. 1983. Improved methodology for analysis and quantitation of proteins on one dimensional silver-stained slab gels. Anal. Biochem. 129:277-287
17. Gonzalez, E., Messi, M.L., Delbono, O. 2000. The specific force of single intact extensor digitorum longus and soleus mouse muscle fibers declines with aging. J. Membr. Biol. 178:175-183
18. 2+ in single intact muscle fibres from transgenic mice. J. Physiol. 552:833-844
19. Greensmith, L., Vrbova, G. 1996. Motoneurone survival: A functional approach. Trends Neurosci. 19:450-455
20. Hashizume, K., Kanda, K., Burke, R. 1988. Medial gastrocnemius motor nucleus in the rat: Age-related changes in the number and size of motoneurons. J. Comp. Neurol. 269:425-430
21. Kadhiresan, V.A., Hassett, C.A., Faulkner, J.A. 1996. Properties of single motor units in medial gastrocnemius muscles of adult and old rats. J. Physiol. 493:543-552
22. Kanda, K., Hashizume, K. 1989. Changes in properties of the medial gastrocnemius motor units in aging rats. J. Neurophysiol. 1989:737-746
23. Kanje, M., Skottner, A., Sjoberg, J., Lundborg, G. 1989. Insulin-like growth factor I (IGF-I) stimulates regeneration of the rat sciatic nerve. Brain Res. 486:396-398
24. Knudson, C.M., Chaudhari, N., Sharp, A.H., Powell, J.A., Beam, K.G., Campbell, K.P. 1989. Specific absence of the alpha 1 subunit of the dihydropyridine receptor in mice with muscular dysgenesis. J. Biol. Chem. 264:1345-1348
25. Lang, C.H., Frost, R.A., Svanberg, E., Vary, T.C. 2004. IGF-I/IGFBP-3 ameliorates alterations in protein synthesis, eIF4E availability, and myostatin in alcohol-fed rats. Am. J. Physiol. 286:E916-E926
26. Larsson, L., Ansved, T. 1995. Effects of ageing on the motor unit. Prog. Neurobiol. 45:397-458
27. 2+ channel from rabbit skeletal muscle. Evidence for two distinct high molecular weight subunits. J. Biol. Chem. 262:7943-7946
28. Lexell, J. 1995. Human aging, muscle mass, and fiber type composition. J. Gerontol. A Biol. Sci. Med. Sci. 50:11-16
29. +-pump stimulation by IGF-I in VSMC. Am. J. Physiol. 276:H2109-H2116
30. Li, J.B., Wang, C.Y., Chen, J.W., Feng, Z.Q., Ma, H.T. 2004. Expression of liver insulin-like growth factor 1 gene and its serum level in patients with diabetes. World J. Gastroenterol. 10:255-259
31. Li, X., Oppenheim, R.W., Lei, M., Houenou, L.J. 1994. Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J. Neurobiol. 25:759-766
32. Messi, M.L., Delbono, O. 2003. Target-derived trophic effect on skeletal muscle innervation in senescent mice. J. Neurosci. 23:1351-1359
33. Meyer, O.A., Tilson, H.A., Byrd, W.C., Riley, M.T. 1979. A method for the routine assessment of fore- and hindlimb grip strength of rats and mice. Neurobehav. Toxicol. 1:233-236
34. Mourkioti, F., Rosenthal, N. 2005. IGF-I, inflammation and stem cells: Interactions during muscle regeneration. Trends Immunol. 26:535-542
35. Murray, B.E., Ohlendieck, K. 1997. Cross-linking analysis of the ryanodine receptor and alpha1-dihydropyridine receptor in rabbit skeletal muscle triads. Biochem. J. 324:689-696
36. Musaro, A., McCullagh, K.J., Paul, A., Houghton, L., Dobrowolny, G., Molinaro, M., Barton-Davis, E.R., Sweeney, H.L., Rosenthal, N. 2001. Localized IGF-I transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27:195-200
37. Neff, N.T., Prevette, D.M., Houenou, L.J., Lewis, M.E., Glicksman, M.A., Yin, Q.-W., Oppenheim, R.W. 1993. Insulin-like growth factors: Putative muscle-derived trophic agents that promote motoneuron survival. J. Neurobiol. 24:1578-1588
38. O'Kusky, J.R., Ye, P., D'Ercole, J. 2000. Insulin-Like growth factor-1 promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 15:8435-8442
39. Ogura, H., Aruga, J., Mikoshiba, K. 2001. Behavioral abnormalities of Zic1 and Zic2 mutant mice: Implications as models for human neurological disorders. Behav. Genet. 31:317-324
40. Oppenheim, R.W. 1996. Neurotrophic survival molecules for motoneurons: An embarrassment of riches. Neuron 17:195-197
41. Payne A.M., Delbono O. 2004. Neurogenesis of excitation-contraction uncoupling in aging skeletal musule. Exerc Sport Sci Rev. 32:36-40
42. Payne, A.M., Zheng, Z., Messi, M.L., Milligan, C.E., Gonzalez, E., Delbono, O. 2006. Motor neurone targeting of IGF-I prevents specific force decline in ageing mouse muscle. J. Physiol. 570:283-294
43. Pestronk, A., Drachman, D.B. 1978. A new stain for quantitative measurement of sprouting at neuromuscular junctions. Muscle Nerve 1:70-74
44. Pette, D., Staron, R.S. 2001. Transitions of muscle fiber phenotypic profiles. Histochem. Cell Biol. 115:359-372
45. Popken, G.J., Hodge, R.D., Ye, P., Zhang, J., Ng, W., O'Kusky, J.R., D'Ercole, A.J. 2004. In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur. J. Neurosci. 19:2056-2068
46. Rabinovsky, E.D., Gelir, E., Gelir, S., Lui, H., Kattash, M., DeMayo, F.J., Shenaq, S.M., Schwartz, R.J. 2003. Targeted expression of IGF-I transgene to skeletal muscle accelerates muscle and motor neuron regeneration. FASEB J. 17:53-55
47. Renganathan, M., Messi, M.L., Delbono, O. 1998. Overexpression of IGF-I exclusively in skeletal muscle prevents age-related decline in the number of dihydropyridine receptors. J. Biol. Chem. 273:28845-28851
48. Sacco, A., Regis, D., LaBarge, M.A., Hammer, M.M., Kraft, P., Blau, H.M. 2005. IGF-I increases bone marrow contribution to adult skeletal muscle and enhances the fusion of myelomonocytic precursors. J. Cell Biol. 171:483-492
49. Segal, S.S., Faulkner, J.A. 1985. Temperature-dependent physiological stability of rat skeletal muscle in vitro. Am. J. Physiol. 248:C265-C270
50. Serrano, A.L., Petrie, J.L., Rivero, J.L.L., Hermanson, J.W. 1996. Myosin isoforms and muscle fiber characteristics in equine gluteus medius muscle. Anat. Rec. 244:444-451
51. Sonntag, W.E., Ramsey, M., Carter, C.S. 2005. Growth hormone and insulin-like growth factor-1 (IGF-I) and their influence on cognitive aging. Ageing Res. Rev. 4:195-212
52. Stanfield, B.B., Cowan, W.M. 1979. The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185:393-422
53. Su, J.L., Stimpson, S., Edwards, C., Arnold, J., Burgess, S., Lin, P. 1997. Neutralizing IGF-I monoclonal antibody with cross-species reactivity. Hybridoma 16:513-518
54. 2+ with quin2: Practical aspects. Methods Enzymol. 172:230-262
55. 2+ in skeletal muscle fibers from aging mice. Biophys. J. 78:1947-1954
56. Wang, Z.-M., Messi, M.L., Delbono, O. 2002. Sustained overexpression of IGF-I prevents age-dependent decrease in charge movement and intracellular calcium in mouse skeletal muscle. Biophys. J. 82:1338-1344
57. 2+ transients in adult skeletal muscle fibers. Biophys. J. 77:2709-2716
58. Ye, P., Li, L., Richards, R.G., DiAugustine, R.P., D'Ercole, A.J. 2002. Myelination is altered in insulin-like growth factor-I null mutant mice. J. Neurosci. 22:6041-6051
59. Ye, P., Xing, Y., Dai, Z., D'Ercole, J. 1996. In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: Evidence that IGF-I increases proliferation of granule cells progenitors. Dev. Brain Res. 95:44-54
60. Zhang, C., Goto, N., Suzuki, M., Ke, M. 1996. Age-related reductions in number and size of anterior horn cells at C6 level of the human spinal cord. Okajimas Folia Anat. Jpn. 73:171-177
61. 1S transcriptional activity by acting on the cAMP-response element-binding protein element of the promoter region. J. Biol. Chem. 277:50535-50542
62. 1S transcription. J. Membr. Biol. 197:101-112