Interaction between Hsp70 and the SR Ca2+ pump: A potential mechanism for cytoprotection in heart and skeletal muscle

Applied Physiology, Nutrition and Metabolism

Volumn 33, Issue 5, 2008, Pages 1023-1032

  Tupling, A Russell ^a   Bombardier, Eric ^a   Vigna, Chris ^a   Quadrilatero, Joe ^a   Fu, Minghua ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Apoptosis; Ca2+ overload; Oxidative stress; Preconditioning

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); HEAT SHOCK PROTEIN 70;

ANIMAL; CONFERENCE PAPER; ENZYMOLOGY; HEART; HEART INFARCTION PREVENTION; HEART MUSCLE; HUMAN; PATHOLOGY; PHYSIOLOGY; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ANIMALS; CALCIUM-TRANSPORTING ATPASES; HEART; HSP70 HEAT-SHOCK PROTEINS; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MUSCLE, SKELETAL; MYOCARDIUM; SARCOPLASMIC RETICULUM;

EID: 53649108812     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H08-067     Document Type: Conference Paper

References (102)

1. Badhwar, A., Bihari, A., Dungey, A.A., Scott, J.R., Albion, C.D., Forbes, T.L., et al. 2004. Protective mechanisms during ischemic tolerance in skeletal muscle. Free Radic. Biol. Med. 36: 371-379. doi:10.1016/j.freeradbiomed. 2003.11.015. PMID:15036356.
2. Barnes, K.A., Samson, S.E., and Grover, A.K. 2000. Sarco/endoplasmic reticulum Ca2+-pump isoform SERCA3a is more resistant to superoxide damage than SERCA2b. Mol. Cell. Biochem. 203: 17-21. doi:10.1023/A:1007053802481. PMID:10724328.
3. Beckman, K.B., and Ames, B.N. 1998. The free radical theory of aging matures. Physiol. Rev. 78: 547-581. PMID:9562038.
4. Beere, H.M. 2005. Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J. Clin. Invest. 115: 2633-2639. doi:10.1172/JCI26471. PMID:16200196.
5. Beere, H.M., and Green, D.R. 2001. Stress management - heat shock protein-70 and the regulation of apoptosis. Trends Cell Biol. 11: 6-10. doi:10.1016/S0962-8924(00)01874-2. PMID:11146277.
6. Beere, H.M., Wolf, B.B., Cain, K., Mosser, D.D., Mahboubi, A., Kuwana, T., et al. 2000. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2: 469-475. doi:10.1038/35019501. PMID:10934466.
7. Bolli, R. 2000. The late phase of preconditioning. Circ. Res. 87: 972-983. PMID:11090541.
8. Bolli, R. 2007. Preconditioning: a paradigm shift in the biology of myocardial ischemia. Am. J. Physiol. Heart Circ. Physiol. 292: H19-H27. doi:10.1152/ajpheart.00712.2006.
9. Bolli, R., and Marban, E. 1999. Molecular and cellular mechanisms of myocardial stunning. Physiol. Rev. 79: 609-634. PMID:10221990.
10. Broome, C.S., Kayani, A.C., Palomero, J., Dillmann, W.H., Mestril, R., Jackson, M.J., et al. 2006. Effect of lifelong overexpression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after nondamaging contractile activity. FASEB J. 20: 1549-1551. doi:10.1096/fj.05-4935fje. PMID:16723383.
11. Bruskov, V.I., Malakhova, L.V., Masalimov, Z.K., and Chernikov, A.V. 2002. Heat-induced formation of reactive oxygen species and 8-oxoguanine, a biomarker of damage to DNA. Nucleic Acids Res. 30: 1354-1363. doi:10.1093/nar/30.6.1354. PMID:11884633.
12. Carroll, C.M., Carroll, S.M., Overgoor, M.L., Tobin, G., and Barker, J.H. 1997. Acute ischemic preconditioning of skeletal muscle prior to flap elevation augments muscle-flap survival. Plast. Reconstr. Surg. 100: 58-65. doi:10.1097/00006534-199707000-00010. PMID:9207659.
13. Chipuk, J.E., Kuwana, T., Bouchier-Hayes, L., Droin, N.M., Newmeyer, D.D., Schuler, M., et al. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science, 303: 1010-1014. doi:10.1126/science.1092734. PMID:14963330.
14. Chipuk, J.E., Bouchier-Hayes, L., and Green, D.R. 2006. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13: 1396-1402. doi:10.1038/sj.cdd.4401963. PMID:16710362.
15. Currie, R.W., Karmazyn, M., Kloc, M., and Mailer, K. 1988. Heatshock response is associated with enhanced postischemic ventricular recovery. Circ. Res. 63: 543-549. PMID:3409486.
16. Currie, R.W., Tanguay, R.M., and Kingma, J.G. 1993. Heat-shock response and limitation of tissue necrosis during occlusion/reperfusion in rabbit hearts. Circulation, 87: 963-971. PMID:8443915.
17. Das, D.K., and Maulik, N. 2006. Cardiac genomic response following preconditioning stimulus. Cardiovasc. Res. 70: 254-263. doi:10.1016/j.cardiores.2006.02.023. PMID:16566910.
18. 2+-ATPase of sarcoplasmic reticulum as revealed by thapsigargin stabilization. Biochim. Biophys. Acta, 1289: 187-194. PMID:8600972.
19. Davies, K.J., Lin, S.W., and Pacifici, R.E. 1987a. Protein damage and degradation by oxygen radicals. IV. Degradation of denatured protein. J. Biol. Chem. 262: 9914-9920. PMID:3036878.
20. Davies, K.J.A., Delsignore, M.E., and Lin, S.W. 1987b. Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J. Biol. Chem. 262: 9902-9907. PMID:3036876.
21. Donnelly, T.J., Sievers, R.E., Vissern, J.L.J., Welch, W.J., and Wolfe, C.L. 1992. Heat shock protein induction in rat hearts. A role for improved myocardial salvage after ischemia and reperfusion? Circulation, 85: 769-778. PMID:1735169.
22. Dröge, W. 2002. Free radicals in the physiological control of cell function. Physiol. Rev. 82: 47-95. PMID:11773609.
23. Ermak, G., and Davies, K.J.A. 2002. Calcium and oxidative stress: from cell signaling to cell death. Mol. Immunol. 38: 713-721. doi:10.1016/S0161-5890(01)00108-0. PMID:11841831.
24. 2+-ATPase from skeletal muscle sarcoplasmic reticulum. J. Appl. Physiol. 84: 425-430. PMID:9475847.
25. Flanagan, S.W., Moseley, P.L., and Buettner, G.R. 1998. Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping. FEBS Lett. 431: 285-286.
26. Fu, M., and Tupling, A.R. 2007. Hsp70 provides functional protection to the cardiac Ca2+ pump (SERCA2a) against heat stress. Appl. Physiol. Nutr. Metab. 32(S1): S32.
27. Gabai, V.L., Mabuchi, K., Mosser, D.D., and Sherman, M.Y. 2002. Hsp72 and stress kinase c-jun N-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor-induced apoptosis. Mol. Cell. Biol. 22: 3415-3424. doi:10.1128/MCB.22.10.3415-3424.2002. PMID:11971973.
28. Garramone, R.R., Winters, R.M., Das, D.P., and Deckers, P.J. 1992. Reduction of skeletal muscle injury through stress conditioning using the heat shock response. Plast. Reconstr. Surg. 93: 1242-1247.
29. Goldberg, A.L. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature, 426: 895-899. doi:10.1038/nature02263. PMID:14685250.
30. Green, D.R., and Kroemer, G. 2004. The pathophysiology of mitochondrial cell death. Science, 305: 626-629. doi:10.1126/science.1099320. PMID:15286356.
31. Grover, A.K., Kwan, C.Y., and Samson, S.E. 2003. Effects of peroxynitrite on sarco/endoplasmic reticulum Ca2+ pump isoforms SERCA2b and SERCA3a. Am. J. Physiol. Cell Physiol. 285: C1537-C1543. PMID:14600079.
32. Gurbuxani, S., Schmitt, E., Cande, C., Parcellier, A., Hammann, A., Daugas, E., et al. 2003. Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor. Oncogene, 22: 6669-6678. doi:10.1038/sj.onc.1206794. PMID:14555980.
33. Gutierrez-Martin, Y., Martin-Romero, F.J., Inesta-Vaquera, F.A., Gutierrez-Merino, C., and Henao, F. 2004. Modulation of sarcoplasmic reticulum Ca2+-ATPase by chronic and acute exposure to peroxynitrite. Eur. J. Biochem. 271: 2647-2657. doi:10.1111/j.1432-1033.2004.04193.x. PMID:15206930.
34. Hampton, C.R., Shimamoto, A., Rothnie, C.L., Griscavage-Ennis, J., Chong, A., Dix, D., et al. 2003. HSP70.1 and -70.3 are required for late-phase protection induced by ischemic preconditioning of mouse hearts. Am. J. Physiol. Heart Circ. Physiol. 285: H866-H874. PMID:12714332.
35. Hoshida, S., Yamashita, N., Otsu, K., and Hori, M. 2002a. The importance of manganese superoxide dismutase in delayed preconditioning: involvement of reactive oxygen species and cytokines. Cardiovasc. Res. 55: 495-505. doi:10.1016/S0008-6363(02)00337-1. PMID:12160946.
36. Hoshida, S., Yamashita, N., Otsu, K., and Hori, M. 2002b. Repeated physiologic stresses provide persistent cardioprotection against ischemia-reperfusion injury in rats. J. Am. Coll. Cardiol. 40: 826-831. doi:10.1016/S0735-1097(02)02001-6. PMID:12204517.
37. Hutter, J.J., Mestril, R., Tam, E.K., Sievers, R.E., Dillmann, W.H., and Wolfe, C.L. 1996. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation, 94: 1408-1411. PMID:8823000.
38. Hutter, M.M., Sievers, R.E., Barbosa, V., and Wolfe, C.L. 1994. Heat-shock protein induction in rat hearts: a direct correlation between the amount of heat-shock protein induced and the degree of myocardial protection. Circulation, 89: 355-360. PMID:8281669.
39. Kampinga, H.H. 1993. Thermotolerance in mammalian cells: protein denaturation and aggregation, and stress proteins. J. Cell Sci. 104: 11-17. PMID:8449990.
40. Kanyani, A.C., Morton, J.P., and McArdle, A. 2008. The exercise-induced stress response in skeletal muscle: failure during aging. Appl. Physiol. Nutr. Metab. 33(5): this issue.
41. Kim, Y.K., Suarez, J., Hu, Y., McDonough, P.M., Boer, C., Dix, D.J., et al. 2006. Deletion of the inducible 70-kDa heat shock protein genes in mice impairs cardiac contractile function and calcium handling associated with hypertrophy. Circulation, 113: 2589-2597. doi:10.1161/CIRCULATIONAHA.105. 598409. PMID:16735677.
42. Knowlton, A. 1997. An overview of the heat shock proteins, their regulation, and function. In Heat shock proteins and the cardiovascular system. Edited by A. Knowlton. KIuwer Academic Publishers, Boston, Mass. pp. 1-24.
43. Latchman, D.S. 2001. Heat shock proteins and cardiac protection. Cardiovasc. Res. 51: 637-646. doi:10.1016/S0008-6363(01)00354-6. PMID:11530097.
44. Lee, C., Liu, X., and Zweier, J.L. 2000. Regulation of xanthine oxidase by nitric oxide and peroxynitrite. J. Biol. Chem. 275: 9369-9376. doi:10.1074/jbc.275.13.9369. PMID:10734080.
45. 2+-ATPase of sarcoplasmic reticulum reveals two thermodynamically independent domains. Biochemistry, 29: 681-689. doi:10.1021/bi00455a013. PMID:2140054.
46. Lepore, D.A., and Morrison, W.A. 2000. Ischemic preconditioning: lack of delayed protection against skeletal muscle ischemia-reperfusion. Microsurgery, 20: 350-355. doi:10.1002/1098-2752(2000)20:7〈350::AID-MICR7〉3. 0. CO;2-9. PMID:11119291.
47. Lepore, D.A., Hurley, J.V., Stewart, A.G., Morrison, W.A., and Anderson, R.L. 2000. Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo. Muscle Nerve, 23: 1847-1855. doi:10.1002/1097- 4598(200012)23:12〈1847::AIDMUS8〉3.0.CO;2-U. PMID:11102908.
48. Lille, S., Su, C.Y., Schoeller, T., Suchy, H., Lyons, S., Russell, R.C., et al. 1999. Induction of heat-shock protein 72 in rat skeletal muscle does not increase tolerance to ischemia-reperfusion injury. Muscle Nerve, 22: 390-393. doi:10.1002/(SICI)1097-4598(199903) 22:3〈390::AID-MUS12〉3.0. CO;2-1. PMID:10086900.
49. Lindquist, S. 1986. The heat-shock response. Annu. Rev. Biochem. 55: 1151-1191. doi:10.1146/annurev.bi.55.070186.005443. PMID:2427013.
50. 2+ homeostasis in rat ventricular myocytes subjected to simulated ischemia. Am. J. Physiol. Cell Physiol. 290: C583-C591. doi:10.1152/ajpcell.00145.2005. PMID:16207797.
51. Liu, Y., Gampert, L., Nething, K., and Steinacker, J.M. 2006b. Response and function of skeletal muscle heat shock protein 70. Front. Biosci. 11: 2802-2827. doi:10.2741/2011. PMID:16720354.
52. Locke, M., Tanguay, R.M., Klabunde, R.E., and Ianuzzo, C.D. 1995. Enhanced postischemic myocardial recovery following exercise induction of HSP72. Am. J. Physiol. 269: H320-H325. PMID:7631864.
53. Marber, M.S., Latchman, D.S., Walker, J.M., and Yellon, D.M. 1993. Cardiac stress protein elevation 24 hours after brief ischaemia or heat stress is associated with resistance to myocardial infarction. Circ. Res. 88: 1264-1272.
54. Marber, M.S., Walker, J.M., Latchman, D.S., and Yellon, D.M. 1994. Myocardial protection after whole body stress in the rabbit is dependent on metabolic substrate and is related to the amount of the inducible 70-kD heat stress protein. J. Clin. Invest. 93: 1087-1094. doi:10.1172/JCI117059. PMID:8132747.
55. Marber, M.S., Mestril, R., Chi, S.H., Sayen, M.R., Yellon, D.M., and Dillmann, W.H. 1995. Overexpression of the rat inducible 70-kD heat stgress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J. Clin. Invest. 95: 1446-1456. doi:10.1172/JCI117815. PMID:7706448.
56. McArdle, A., Dillmann, W.H., Mestril, R., Faulkner, J.A., and Jackson, M.J. 2004. Overexpression of HSP70 in mouse skeletal muscle protects against muscle damage and age-related muscle dysfunction. FASEB J. 18: 355-357. PMID:14688209.
57. McCord, J.M. 2000. The evolution of free radicals and oxidative stress. Am. J. Med. 108: 652-659. doi:10.1016/S0002-9343(00) 00412-5. PMID:10856414.
58. Mestril, R. 2005. The use of transgenic mice to study cytoprotection by the stress proteins. Methods, 35: 165-169. doi:10.1016/j.ymeth.2004.08. 007. PMID:15649843.
59. Miyabara, E.H., Martin, J.L., Griffin, T.M., Moriscot, A.S., and Mestril, R. 2006. Overexpression of inducible 70-kDa heat shock protein in mouse attenuates skeletal muscle damage induced by cryolesioning. Am. J. Physiol. Cell Physiol. 290: C1128-C1138. doi:10.1152/ajpcell.00399.2005. PMID:16291818.
60. 2+-pump dysfunction in rat cardiomyocytes briefly exposed to hydroxyl radicals. Free Radic. Biol. Med. 22: 37-47. doi:10.1016/S0891-5849(96) 00238-9. PMID:8958128.
61. Mosser, D.D., Caron, A.W., Bourget, L., Meriin, A.B., Sherman, M.Y., Morimoto, R.I., et al. 2000. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol. Cell. Biol. 20: 7146-7159. doi:10.1128/MCB.20.19.7146-7159.2000. PMID:10982831.
62. Mubagwa, K. 1995. Sarcoplasmic reticulum function during myocardial ischemia and reperfusion. Cardiovasc. Res. 30: 166-175. doi:10.1016/0008-6363(95)00066-6. PMID:7585801.
63. Noble, E.G., Milne, K.J., and Melling, C.W.J. 2008. Heat shock proteins and exercise: a primer. Appl. Physiol. Nutr. Metab. 33(5): this issue.
64. 2+-channel activation by ischemia/reperfusion. Mol. Cell. Biochem. 173: 135-143. doi:10.1023/A:1006840013439. PMID:9278264.
65. Orrenius, S., Zhivotovsky, B., and Nicotera, P. 2003. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4: 552-565. doi:10.1038/nrm1150. PMID:12838338.
66. Park, H.S., Cho, S.G., Kim, C.K., Hwang, H.S., Noh, K.T., Kim, M.S., et al. 2002. Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol. Cell. Biol. 22: 7721-7730. doi:10.1128/MCB.22.22.7721-7730.2002. PMID:12391142.
67. Paroo, Z., Haist, J.V., Karmazyn, M., and Noble, E.G. 2002. Exercise improves postischemic cardiac function in males but not females: consequences of a novel sex-specific heat shock protein 70 response. Circ. Res. 90: 911-917. doi:10.1161/01.RES.0000016963.43856.B1. PMID:11988493.
68. 2+-ATPase labelled selectively with fluorescein. Biochim. Biophys. Acta, 626: 255-261. PMID:6450619.
69. Plumier, J.C., and Currie, R.W. 1996. Heat shock-induced myocardial protection against ischemic injury: a role for Hsp70? Cell Stress Chaperones, 1: 13-17. doi:10.1379/1466-1268(1996) 001〈0013:HSIMPA〉2.3.CO;2. PMID:9222583.
70. Plumier, J.C., Ross, B., Currie, R., Angelidis, C., Kazlaris, H., Kollias, G., et al. 1995. Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J. Clin. Invest. 95: 1854-1860. doi:10.1172/JCI117865. PMID:7706492.
71. Pudupakkam, S., Harris, K.A., Jamieson, W.G., DeRose, G., Scott, J.A., Carson, M.W., et al. 1998. Ischemic tolerance in skeletal muscle: role of nitric oxide. Am. J. Physiol. 275: 94-99.
72. Qian, Y.Z., Shipley, J.B., Levasseur, J.E., and Kukreja, R.C. 1998. Dissociation of heat shock proteins expression with ischemic tolerance by whole body hyperthermia in rat heart. J. Mol. Cell. Cardiol. 30: 1163-1172. doi:10.1006/jmcc.1998.0680. PMID:9689590.
73. Quan, E.E., Ramirez, S., Tecimer, T., Grossi, F.V., Barker, J.H., and Maldonado, C. 2004. Late-phase ischemic preconditioning in sksletal muscle: is the phenomenon protective? Microsurgery, 24: 151-156. doi:10.1002/micr.20008. PMID:15038023.
74. Quindry, J.C., Hamilton, K.L., French, J.P., Lee, Y., Murlasits, Z., Tumer, N., et al. 2007. Exercise-induced HSP-72 elevation and cardioprotection against infarct and apoptosis. J. Appl. Physiol. 103: 1056-1062. doi:10.1152/japplphysiol.00263.2007. PMID:17569768.
75. Radford, N.B., Fina, M., Benjamin, I.J., Moreadith, R.W., Graves, K.H., Zhao, P., et al. 1996. Cardioprotective effects of 70-kDa heat shock protein in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 93: 2339-2342. doi:10.1073/pnas.93.6.2339. PMID:8637874.
76. Reid, M.B. 2001. Invited review: redox modulation of skeletal muscle contraction: what we know and what we don't. J. Appl. Physiol. 90: 724-731. doi:10.1063/1.1381002. PMID:11160074.
77. Rubin, B.B., Romaschin, A., Walker, P.M., Gute, D.C., and Korthuis, R.T. 1996. Mechanisms of postischemic injury in skeletal muscle: intervention strategies. J. Appl. Physiol. 80: 369-387. PMID:8929572.
78. Ruchalski, K., Mao, H., Singh, S.K., Wang, Y., Mosser, D.D., Li, F., et al. 2003. HSP72 inhibits apoptosis-inducing factor release in ATP-depleted renal epithelial cells. Am. J. Physiol. Cell Physiol. 285: C1483-C1493. PMID:12930708.
79. Saleh, A., Srinivasula, S.M., Balkir, L., Robbins, P.D., and Alnemri, E.S. 2000. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol. 2: 476-483. doi:10.1038/35019510. PMID:10934467.
80. 2+-ATPase function. Am. J. Physiol. Endocrinol. Metab. 283: E722-E728. PMID:12217889.
81. 2+-ATPase of sarcoplasmic reticulum by thiol-specific, heat shock inducers results in thermal denaturation at 37 degrees C. Biochemistry, 36: 11002-11011. doi:10.1021/bi9711590. PMID:9283092.
82. Squier, T.C., and Bigelow, D.J. 2000. Protein oxidation and age-dependent alterations in calcium homeostasis. Front. Biosci. 5: d504-d526. doi:10.2741/Squier. PMID:10799358.
83. Stadtman, E.R. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62: 797-821. doi:10.1146/annurev.bi.62.070193.004053. PMID:8352601.
84. Stamler, J.S., and Meissner, G. 2001. Physiology of nitric oxide in skeletal muscle. Physiol. Rev. 81: 209-237. PMID:11152758.
85. Stankiewicz, A.R., Lachapelle, G., Foo, C.P., Radicioni, S.M., and Mosser, D.D. 2005. Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J. Biol. Chem. 280: 38729-38739. doi:10.1074/jbc.M509497200. PMID:16172114.
86. Sun, J.Z., Tang, X.L., Knowlton, A.A., Park, S.W., Qiu, Y., and Bolli, R. 1995. Late preconditioning against myocardial stunning. An endogenous protective mechanism that confers resistance to postischemic dysfunctin 24 h after brief ischemia in conscious pigs. J. Clin. Invest. 95: 388-403. doi:10.1172/JCI117667. PMID:7814639.
87. Suzuki, K., Murtuza, B., Sammut, I.A., Latif, N., Jayakumar, J., Smolenski, R.T., et al. 2002. Heat shock protein 72 enhances manganese superoxide dismutase activity during myocardial ischemia-reperfusion injury, associated with mitochondrial protection and apoptosis reduction. Circulation, 106: 270-276.
88. Taegtmeyer, H., Roberts, A.F., and Raine, A.E. 1985. Energy metabolism in reperfused heart muscle: metabolic correlates to return of function. J. Am. Coll. Cardiol. 6: 864-870. PMID:4031301.
89. Taylor, R.P., Harris, M.B., and Starnes, J.W. 1999. Acute exercise can improve cardioprotection without increasing heat shock protein content. Am. J. Physiol. 276: H1098-H1102. PMID:10070097.
90. Thompson, C.B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science, 267: 1456-1462. doi:10.1126/science.7878464. PMID:7878464.
91. Toyoshima, C., Nakasako, M., Nomura, H., and Ogawa, H. 2000. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature, 405: 647-655. doi:10.1038/35015017. PMID:10864315.
92. Trost, S.U., Omens, J.H., Karlon, W.J., Meyer, M., Mestril, R., Covell, J.W., et al. 1998. Protection against myocardial dysfunction after a brief ischemic period in transgenic mice expressing inducible heat shock protein 70. J. Clin. Invest. 101: 855-862. doi:10.1172/JCI265. PMID:9466981.
93. Tupling, A.R. 2004. The sarcoplasmic reticulum in muscle fatigue and disease: role of the sarco(endo)plasmic reticulum Ca2+-ATPase. Can. J. Appl. Physiol. 29: 308-329. PMID:15199229.
94. Tupling, A.R., Gramolini, A.O., Duhamel, T.A., Kondo, H., Asahi, M., Tsuchiya, S.C., et al. 2004. HSP70 binds to the fast-twitch skeletal muscle Sarco (endo)plasmic reticulum Ca2+-ATPase (SERCA1a) and prevents thermal inactivation. J. Biol. Chem. 279: 52382-52389. doi:10.1074/jbc. M409336200. PMID:15371420.
95. Tupling, R., Green, H., Senisterra, G., Lepock, J., and McKee, N. 2001. Ischemia-induced structural change in SR Ca2+-ATPase is associated with reduced enzyme activity in rat muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281: R1681-R1688. PMID:11641141.
96. van Loo, G., Saelens, X., van Gurp, M., MacFarlane, M., Martin, S.J., and Vandenabeele, P. 2002. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9: 1031-1042. doi:10.1038/sj.cdd.4401088. PMID:12232790.
97. 2+-ATPase. Biochemistry, 36: 7706-7716. doi:10.1021/bi970058z. PMID:9201911.
98. Viner, R.I., Williams, T.D., and Schöneich, C. 1999. Peroxynitrite modification of protein thiols: oxidation, nitrosylation, and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry, 38: 12408-12415. doi:10.1021/bi9909445. PMID:10493809.
99. Welch, W.J. 1992. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72: 1063-1081. PMID:1438579.
100. 2+-ATPase function by direct attack on the ATP binding site. Circ. Res. 80: 76-81. PMID:8978325.
101. Yamagishi, N., Ishihara, K., Saito, Y., and Hatayama, T. 2003. Hsp105 but not Hsp70 family proteins suppress the aggregation of heat-denatured protein in the presence of ADP. FEBS Lett. 555: 390-396. doi:10.1016/S0014-5793(03) 01292-4. PMID:14644449.
102. Yamamoto, K., Ichijo, H., and Korsmeyer, S.J. 1999. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19: 8469-8478.