Membrane depolarization induces calcium-dependent upregulation of Hsp70 and Hmox-1 in skeletal muscle cells

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 3, 2009, Pages

  Jorquera, Gonzalo ^a   Juretić, Nevenka ^a   Jaimovich, Enrique ^a   Riveros, Nora ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

Excitation transcription; Heat shock proteins; Inositol 1,4,5 trisphophate receptors; Muscle gene expression; Myotubes

Indexed keywords

ACTIN; CALCIUM; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; INOSITOL 1,4,5 TRISPHOSPHATE; MESSENGER RNA; PROTEIN KINASE C;

ADAPTATION; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CELL STRESS; CONTROLLED STUDY; FETUS; GENE EXPRESSION REGULATION; GENE INDUCTION; MUSCLE REGENERATION; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; UPREGULATION;

ANIMALS; CALCIUM; CELLS, CULTURED; ELECTRIC STIMULATION; HEME OXYGENASE (DECYCLIZING); HSP70 HEAT-SHOCK PROTEINS; MEMBRANE POTENTIALS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; UP-REGULATION;

EID: 70349238662     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00167.2009     Document Type: Article

References (64)

1. Adams GR, Haddad F, Baldwin KM. Time course of changes in markers of myogenesis in overloaded rat skeletal muscles. J Appl Physiol 87: 1705-1712, 1999.
2. Araya R, Liberona JL, Cárdenas JC, Riveros N, Estrada M, Powell JA, Carrasco MA, Jaimovich E. Dihydropyridine receptors as voltage sensors for a depolarization-evoked, IP3R-mediated, slow calcium signal in skeletal muscle cells. J Gen Physiol 121: 3-16, 2003. (Pubitemid 36133933)
3. 2-terminal kinase pathway in rat skeletal muscle. J Biol Chem 272: 25636-25640, 1997.
4. Borger DR, Essig DA. Induction of HSP 32 gene in hipoxic cardiomyocytes is attenuated by treatment with N-acetyl-L-cysteine. Am J Physiol Heart Circ Physiol 274: H965-H973, 1998. (Pubitemid 28158293)
5. Broquet AH, Thomas G, Masliah J, Trugnan G, Bachelet M. Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J Biol Chem 278: 21601-21606, 2003. (Pubitemid 36792559)
6. 2+ transients and modulate cAMP response element binding protein phosphorylation. J Cell Sci 118: 3131-3140, 2005.
7. Carrasco MA, Riveros N, Ríos J, Müller M, Torres F, Pineda J, Lantadilla S, Jaimovich E. Depolarization-induced slow calcium transients activate early genes in skeletal muscle cells. Am J Physiol Cell Physiol 284: C1438-C1447, 2003. (Pubitemid 36583385)
8. Carson JA, Nettleton D, Reecy JM. Differential gene expression in the rat soleus muscle during early work overload-induced hypertrophy. FASEB J 16: 207-209, 2002.
9. Choi AM, Tucker RW, Carlson SG, Weigand G, Holbrook NJ. Calcium mediates expression of stress-response genes in prostaglandin A2-induced growth arrest. FASEB J 8: 1048-1054, 1994. (Pubitemid 24979537)
10. Craig EA, Weissman JS, Horwich AL. Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78: 365-372, 1994. (Pubitemid 24250802)
11. i. J Investig Med 44: 144-153, 1996.
12. 2+ signals through a Gbetagamma/phosphatidylinositol 3-kinase gamma pathway in skeletal myotubes. J Biol Chem 281: 12143-12154, 2006.
13. Eltit JM, Hidalgo J, Liberona JL, Jaimovich E. Slow calcium signals after tetanic stimulation in skeletal myotubes. Biophys J 86: 3042-3051, 2004. (Pubitemid 38552706)
14. Essig DA, Borger DR, Jackson DA. Induction of heme oxygenase-1 (HSP32) mRNA in skeletal muscle following contractions. Am J Physiol Cell Physiol 272: C59-C67, 1997. (Pubitemid 27073904)
15. Estrada M, Cárdenas C, Liberona JL, Carrasco MA, Mignery GA, Allen PD, Jaimovich E. Calcium transients in 1B5 myotubes lacking ryanodine receptors are related to inositol trisphosphate receptors. J Biol Chem 276: 22868-22874, 2001. (Pubitemid 37410975)
16. 2+ stimulates ERK, CREB, early genes. J Cell Physiol 209: 379-388, 2006.
17. Febbraio MA, Steensberg A, Walsh R, Koukoulas I, van Hall G, Saltin B, Pedersen BK. Reduced glycogen availability is associated with an elevation in HSP72 in contracting human skeletal muscle. J Physiol 538: 911-917, 2002. (Pubitemid 35190081)
18. Flück M, Hoppeler H. Molecular basis of skeletal muscle plasticity- from gene to form and function. Rev Physiol Biochem Pharmacol 146: 159-216, 2003. (Pubitemid 36084147)
19. Flück M. Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209: 2239-2248, 2006. (Pubitemid 44065519)
20. Georgopoulos C, Welch WJ. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol 9: 601-634, 1993. (Pubitemid 2021168)
21. Goldspink G. Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 194: 323-334, 1999. (Pubitemid 29241484)
22. Hildebrandt AL, Pilegaard H, Neufer PD. Differential transcriptional activation of select metabolic genes in response to variations in exercise intensity and duration. Am J Physiol Endocrinol Metab 285: E1021-E1027, 2003. (Pubitemid 37296323)
23. Hodd DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209: 2265-2275, 2006. (Pubitemid 44065521)
24. Holmberg CI, Roos PM, Lord JM, Eriksson JE, Sistonen L. Conventional and novel PKC isoenzymes modify the heat-induced stress response but are not activated by heat shock. J Cell Sci 111: 3357-3365, 1998. (Pubitemid 28563038)
25. Holmberg CI, Tran SE, Eriksson JE, Sistonen L. Multisite phosphorylation provides sophisticated regulation of transcription factors. Trends Biochem Sci 27: 619-627, 2002. (Pubitemid 35435311)
26. Jackson MJ. Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise. Philos Trans R Soc Lond B Biol Sci 360: 2285-2291, 2005. (Pubitemid 46682147)
27. + and tetracaine in cultured rat myotubes. Cell Calcium 15: 356-368, 1994.
28. 2+ signals in cultured skeletal muscle. Am J Physiol Cell Physiol 278: C998-C1010, 2000.
29. 2+ transients stimulate transcription of IL-6 gene in skeletal muscle cells. Am J Physiol Cell Physiol 290: C1428-C1436, 2006.
30. Juretić N, Urzúa U, Munroe DJ, Jaimovich E, Riveros N. Differential gene expression in skeletal muscle cells after membrane depolarization. J Cell Physiol 210: 819-830, 2007. (Pubitemid 46185051)
31. Khanna A, Aten RF, Behrman HR. Physiological and pharmacological inhibitors of luteinizing hormone-dependent steroidogenesis induce heat shock protein-70 in rat luteal cells. Endocrinology 136: 1775-1781, 1995.
32. Khassaf M, Child RB, McArdle A, Brodie DA, Esanu C, Jackson MJ. Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J Appl Physiol 90: 1031-1035, 2001. (Pubitemid 32171391)
33. Kiang JG, Tsokos GC. Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80: 183-201, 1998. (Pubitemid 28498227)
34. i or activation of G proteins but not pHi or cAMP. Am J Physiol Cell Physiol 267: C104-C114, 1994.
35. 2+, PKC, and PKA in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 282: G415-G423, 2002.
36. Kroeger PE, Sarge KD, Morimoto RI. Mouse heat shock transcription factors 1 and 2 prefer a trimeric binding site but interact differently with the HSP70 heat shock element. Mol Cell Biol 13: 3370-3383, 1993. (Pubitemid 23157274)
37. Linden T, Doutheil J, Paschen W. Role of calcium in the activation of erp72 and heme oxygenase-1 expression on depletion of endoplasmic reticulum calcium stores in rat neuronal cell culture. Neurosci Lett 247: 103-106, 1998. (Pubitemid 28240107)
38. Liu Y, Gampert L, Nething K, Steinacker JM. Response and function of skeletal muscle heat shock protein 70. Front Biosci 11: 2802-2827, 2006. (Pubitemid 43800377)
39. Liu Y, Lormes W, Wang L, Reissnecker S, Steinacker JM. Different skeletal muscle HSP70 responses to high-intensity strength training and low-intensity endurance training. Eur J Appl Physiol 91: 330-335, 2004. (Pubitemid 38325013)
40. Liu Y, Mayr S, Opitz-Gress A, Zeller C, Lormes W, Baur S, Lehmann M, Steinacker JM. Human skeletal muscle HSP70 response to training in highly trained rowers. J Appl Physiol 86: 101-104, 1999. (Pubitemid 29046946)
41. Maglara AA, Vasilaki A, Jackson MJ, McArdle A. Damage to developing mouse skeletal muscle myotubes in culture: protective effect of heat shock proteins. J Physiol 548.3: 837-846, 2003. (Pubitemid 36592777)
42. Maines MD, Mayer RD, Ewing JF, McCoubrey WK Jr. Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/repefrusion: possible role of heme as both promotor of tissue damage and regulator of HSP32. J Pharmacol Exp Ther 264: 457-462, 1993.
43. McArdle A, Pattwell D, Vasilaki A, Griffiths RD, Jackson MJ. Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol Cell Physiol 280: C621-C627, 2001. (Pubitemid 32466825)
44. McArdle F, Spiers S, Aldemir H, Vasilaki A, Beaver A, Iwanejko L, McArdle A, Jackson MJ. Preconditioning of skeletal muscle against contraction-induced damage: the role of adaptations to oxidants in mice. J Physiol 561:233-244, 2004. (Pubitemid 39549479)
45. 2+-dependent transcription. Curr Opin Neurobiol 11: 312-319, 2001.
46. Pilegaard H, Ordway GA, Saltin B, Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000. (Pubitemid 30951407)
47. Powell J, Petherbridge L, Flucher B. Formation of triads without the dihydropyridine receptor alpha subunits in cell lines from dysgenic skeletal muscle. J Cell Biol 134: 375-387, 1996. (Pubitemid 26250706)
48. +2 signaling pathway in skeletal muscle. J Cell Sci 114: 3673-3683, 2001.
49. 2+ is essential for multistep activation of the heat shock factor in permeabilized cells. Mol Cell Biol 11: 3365-3368, 1991.
50. Puntschart A, Vogt M, Widmer HR, Hoppeler H, Billeter R. Hsp70 expression in human skeletal muscle after exercise. Acta Physiol Scand 157: 411-417, 1996. (Pubitemid 26258980)
51. Reid MB, Durham WJ. Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: potential impact on aging. Ann NY Acad Sci 959: 108-116, 2002.
52. Sakamoto K, Goodyear LJ. Invited review: intracellular signaling in contracting skeletal muscle. J Appl Physiol 93: 369-383, 2002. (Pubitemid 34686234)
53. Schiaffino S, Serrano A. Calcineurin signaling and neural control of skeletal muscle fiber type and size. Trends Pharmacol Sci 23: 569-575, 2002. (Pubitemid 35375802)
54. Silomon M, Bauer I, Bauer M, Nolting J, Paxian M, Rensing H. Induction of heme oxygenase-1 and heat shock protein 70 in rat hepatocytes: the role of calcium signaling. Cell Mol Biol Lett 12: 25-38, 2007. (Pubitemid 46786639)
55. 2+, and phospholipase A2 in endothelial cells. Am J Physiol Heart Circ Physiol 276: H1493-H1501, 1999.
56. Thompson HS, Maynard EB, Morales ER, Scordilis SP. Exercise-induced HSP27, HSP70 and MAPK responses in human skeletal muscle. Acta Physiol Scand 178: 61-72, 2003.
57. Vissing K, Andersen JL, Schjerling P. Are exercise-induced genes induced by exercise? FASEB J 19: 94-96, 2005. (Pubitemid 40069929)
58. Walsh RC, Koukoulas I, Garnham A, Moseley PL, Hargreaves M, Febbraio MA. Exercise increases serum Hsp72 in humans. Cell Stress Chaperones 6: 386-393, 2001. (Pubitemid 33123492)
59. Welch WJ. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72: 1063-1081, 1992.
60. Williams RS, Neufer PD. Regulation of gene expression in skeletal muscle by contractile activity. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 25, p. 1124-1150.
61. Wittwer M, Billeter R, Hoppeler H, Fluck M. Regulatory gene expression in skeletal muscle of highly endurance-trained humans. Acta Physiol Scand 180: 217-227, 2004. (Pubitemid 38241389)
62. 2+ and protein kinases in the induction of the hsp70 gene. Kidney Int 45: 1093-1104, 1994.
63. Yang RC, Jao HC, Huang LJ, Wang SJ, Hsu C. The essential role of PKC-alpha in the protective effect of heat-shock pretreatment on TNF-alpha induced apoptosis in hepatic epithelial cell line. Exp Cell Res 296: 276-284, 2004. (Pubitemid 38624648)
64. Zambon AC, Mc Dearmon EL, Salomonis N, Vranizan KM, Johansen KL, Adey D, Takahashi JS, Schambelan M, Conklin BR. Time- and exercised-dependent gene regulation in human skeletal muscle. Genome Biol 4: R61.1-R61.12, 2003.