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. 2002 Mar;82(3):1338–1344. doi: 10.1016/S0006-3495(02)75489-1

Sustained overexpression of IGF-1 prevents age-dependent decrease in charge movement and intracellular Ca(2+) in mouse skeletal muscle.

Zhong-Min Wang 1, María Laura Messi 1, Osvaldo Delbono 1
PMCID: PMC1301936  PMID: 11867450

Abstract

In this work we tested the hypothesis that transgenic sustained overexpression of IGF-1 prevents age-dependent decreases in charge movement and intracellular Ca(2+) in skeletal muscle fibers. To this end, short flexor digitorum brevis (FDB) muscle fibers from 5-7- and 21-24-month-old FVB (wild-type) and S1S2 (IGF-1 transgenic) mice were studied. Fibers were voltage-clamped in the whole-cell configuration of the patch-clamp technique according to described procedures (Wang, Z. M., M. L. Messi, and O. Delbono. 1999. Biophys. J. 77:2709-2716). Charge movement and intracellular Ca(2+) concentration were recorded simultaneously. The maximum charge movement (Q(max)) recorded in young wild-type and transgenic mice was (mean +/- SEM, in nC microF(-1)): 52 +/- 2.1 (n = 46) and 54 +/- 1.9 (n = 38) (non-significant, ns), respectively, whereas in old wild-type and old transgenic mice the values were 36 +/- 2.1 (n = 32) and 49 +/- 2.3 (n = 35), respectively (p < 0.01). The peak intracellular calcium [Ca(2+)](i) recorded in young wild-type and transgenic mice was (in muM): 14.5 +/- 0.9 and 16 +/- 2.1 (ns), whereas in old wild-type and transgenic mice the values were 9.9 +/- 0.1 and 14 +/- 1.1 (p < 0.01), respectively. No significant changes in the voltage distribution or steepness of the Q-V or [Ca(2+)]-V relationship were found. These data support the concept that overexpression of IGF-1 in skeletal muscle prevents age-dependent reduction in charge movement and peak [Ca(2+)](i).

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Selected References

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  1. Adams B. A., Tanabe T., Mikami A., Numa S., Beam K. G. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature. 1990 Aug 9;346(6284):569–572. doi: 10.1038/346569a0. [DOI] [PubMed] [Google Scholar]
  2. Angel P., Hattori K., Smeal T., Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 1988 Dec 2;55(5):875–885. doi: 10.1016/0092-8674(88)90143-2. [DOI] [PubMed] [Google Scholar]
  3. Ashley C. C., Mulligan I. P., Lea T. J. Ca2+ and activation mechanisms in skeletal muscle. Q Rev Biophys. 1991 Feb;24(1):1–73. doi: 10.1017/s0033583500003267. [DOI] [PubMed] [Google Scholar]
  4. Baumgartner R. N., Koehler K. M., Gallagher D., Romero L., Heymsfield S. B., Ross R. R., Garry P. J., Lindeman R. D. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998 Apr 15;147(8):755–763. doi: 10.1093/oxfordjournals.aje.a009520. [DOI] [PubMed] [Google Scholar]
  5. Beam K. G., Franzini-Armstrong C. Functional and structural approaches to the study of excitation-contraction coupling. Methods Cell Biol. 1997;52:283–306. doi: 10.1016/s0091-679x(08)60384-2. [DOI] [PubMed] [Google Scholar]
  6. Brooks S. V., Faulkner J. A. Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol. 1988 Oct;404:71–82. doi: 10.1113/jphysiol.1988.sp017279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brooks S. V., Faulkner J. A. Isometric, shortening, and lengthening contractions of muscle fiber segments from adult and old mice. Am J Physiol. 1994 Aug;267(2 Pt 1):C507–C513. doi: 10.1152/ajpcell.1994.267.2.C507. [DOI] [PubMed] [Google Scholar]
  8. 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. 1995 May 19;270(20):12109–12116. doi: 10.1074/jbc.270.20.12109. [DOI] [PubMed] [Google Scholar]
  9. Delbono O. Calcium current activation and charge movement in denervated mammalian skeletal muscle fibres. J Physiol. 1992;451:187–203. doi: 10.1113/jphysiol.1992.sp019160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Delbono O., Meissner G. Sarcoplasmic reticulum Ca2+ release in rat slow- and fast-twitch muscles. J Membr Biol. 1996 May;151(2):123–130. doi: 10.1007/s002329900063. [DOI] [PubMed] [Google Scholar]
  11. Delbono O., O'Rourke K. S., Ettinger W. H. Excitation-calcium release uncoupling in aged single human skeletal muscle fibers. J Membr Biol. 1995 Dec;148(3):211–222. doi: 10.1007/BF00235039. [DOI] [PubMed] [Google Scholar]
  12. Delbono O., Renganathan M., Messi M. L. Excitation-Ca2+ release-contraction coupling in single aged human skeletal muscle fiber. Muscle Nerve Suppl. 1997;5:S88–S92. doi: 10.1002/(sici)1097-4598(1997)5+<88::aid-mus21>3.0.co;2-u. [DOI] [PubMed] [Google Scholar]
  13. Delbono O., Renganathan M., Messi M. L. Regulation of mouse skeletal muscle L-type Ca2+ channel by activation of the insulin-like growth factor-1 receptor. J Neurosci. 1997 Sep 15;17(18):6918–6928. doi: 10.1523/JNEUROSCI.17-18-06918.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Delbono O., Stefani E. Calcium transients in single mammalian skeletal muscle fibres. J Physiol. 1993 Apr;463:689–707. doi: 10.1113/jphysiol.1993.sp019617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Florini J. R., Ewton D. Z., Coolican S. A. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev. 1996 Oct;17(5):481–517. doi: 10.1210/edrv-17-5-481. [DOI] [PubMed] [Google Scholar]
  16. Florini J. R., Ewton D. Z., Magri K. A., Mangiacapra F. J. IGFs and muscle differentiation. Adv Exp Med Biol. 1993;343:319–326. doi: 10.1007/978-1-4615-2988-0_31. [DOI] [PubMed] [Google Scholar]
  17. Garcia J., Schneider M. F. Calcium transients and calcium release in rat fast-twitch skeletal muscle fibres. J Physiol. 1993 Apr;463:709–728. doi: 10.1113/jphysiol.1993.sp019618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. González E., Delbono O. Age-dependent fatigue in single intact fast- and slow fibers from mouse EDL and soleus skeletal muscles. Mech Ageing Dev. 2001 Jul 31;122(10):1019–1032. doi: 10.1016/s0047-6374(01)00229-9. [DOI] [PubMed] [Google Scholar]
  19. González E., Delbono O. Recovery from fatigue in fast and slow single intact skeletal muscle fibers from aging mouse. Muscle Nerve. 2001 Sep;24(9):1219–1224. doi: 10.1002/mus.1135. [DOI] [PubMed] [Google Scholar]
  20. González E., Messi M. L., Delbono O. The specific force of single intact extensor digitorum longus and soleus mouse muscle fibers declines with aging. J Membr Biol. 2000 Dec 1;178(3):175–183. doi: 10.1007/s002320010025. [DOI] [PubMed] [Google Scholar]
  21. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  22. Kabbara A. A., Allen D. G. The use of the indicator fluo-5N to measure sarcoplasmic reticulum calcium in single muscle fibres of the cane toad. J Physiol. 2001 Jul 1;534(Pt 1):87–97. doi: 10.1111/j.1469-7793.2001.00087.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Melzer W., Herrmann-Frank A., Lüttgau H. C. The role of Ca2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim Biophys Acta. 1995 May 8;1241(1):59–116. doi: 10.1016/0304-4157(94)00014-5. [DOI] [PubMed] [Google Scholar]
  24. Moore D. H., 2nd A study of age group track and field records to relate age and running speed. Nature. 1975 Jan 24;253(5489):264–265. doi: 10.1038/253264a0. [DOI] [PubMed] [Google Scholar]
  25. Renganathan M., Messi M. L., Delbono O. Dihydropyridine receptor-ryanodine receptor uncoupling in aged skeletal muscle. J Membr Biol. 1997 Jun 1;157(3):247–253. doi: 10.1007/s002329900233. [DOI] [PubMed] [Google Scholar]
  26. Renganathan M., Messi M. L., Delbono O. Overexpression of IGF-1 exclusively in skeletal muscle prevents age-related decline in the number of dihydropyridine receptors. J Biol Chem. 1998 Oct 30;273(44):28845–28851. doi: 10.1074/jbc.273.44.28845. [DOI] [PubMed] [Google Scholar]
  27. Renganathan M., Messi M. L., Schwartz R., Delbono O. Overexpression of hIGF-1 exclusively in skeletal muscle increases the number of dihydropyridine receptors in adult transgenic mice. FEBS Lett. 1997 Nov 3;417(1):13–16. doi: 10.1016/s0014-5793(97)01225-8. [DOI] [PubMed] [Google Scholar]
  28. Renganathan M., Sonntag W. E., Delbono O. L-type Ca2+ channel-insulin-like growth factor-1 receptor signaling impairment in aging rat skeletal muscle. Biochem Biophys Res Commun. 1997 Jun 27;235(3):784–789. doi: 10.1006/bbrc.1997.6881. [DOI] [PubMed] [Google Scholar]
  29. Roubenoff R., Hughes V. A. Sarcopenia: current concepts. J Gerontol A Biol Sci Med Sci. 2000 Dec;55(12):M716–M724. doi: 10.1093/gerona/55.12.m716. [DOI] [PubMed] [Google Scholar]
  30. Tsien R., Pozzan T. Measurement of cytosolic free Ca2+ with quin2. Methods Enzymol. 1989;172:230–262. doi: 10.1016/s0076-6879(89)72017-6. [DOI] [PubMed] [Google Scholar]
  31. Wang Z. M., Messi M. L., Delbono O. L-Type Ca(2+) channel charge movement and intracellular Ca(2+) in skeletal muscle fibers from aging mice. Biophys J. 2000 Apr;78(4):1947–1954. doi: 10.1016/S0006-3495(00)76742-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wang Z. M., Messi M. L., Delbono O. Patch-clamp recording of charge movement, Ca2+ current, and Ca2+ transients in adult skeletal muscle fibers. Biophys J. 1999 Nov;77(5):2709–2716. doi: 10.1016/s0006-3495(99)77104-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wang Z. M., Messi M. L., Renganathan M., Delbono O. Insulin-like growth factor-1 enhances rat skeletal muscle charge movement and L-type Ca2+ channel gene expression. J Physiol. 1999 Apr 15;516(Pt 2):331–341. doi: 10.1111/j.1469-7793.1999.0331v.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zheng Z., Messi M. L., Delbono O. Age-dependent IGF-1 regulation of gene transcription of Ca2+ channels in skeletal muscle. Mech Ageing Dev. 2001 Apr 15;122(4):373–384. doi: 10.1016/s0047-6374(00)00236-0. [DOI] [PubMed] [Google Scholar]

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