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“Proteotoxicity” of ATP Depletion: Disruption of the Cytoskeleton, Protein Aggregation and Involvement of Molecular Chaperones

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Heat Shock Proteins and Cytoprotection

Abstract

The majority of cell-stressing exposures affect proteins. Typical “proteotoxic” exposures such as heating, ultra-violet irradiation, de crease in pH and treatment with oxidants or heavy metals are able to damage various proteins both in vitro (in a solution) and in vivo (in a cell). Lack of ATP in artificially prepared protein solutions does not seem to be very critical for the stability of the soluted proteins; in contrast, the depletion of intracellular ATP destroys the cytoskeletal framework and evokes aggregation (or insolubility) of many cellular proteins including HSPs. Although this proteotoxic component is only one of the many harmful effects of ATP depletion on mammalian cells, we consider it the most crucial event coupling the mechanisms of cell injury and cell adaptation under metabolic (or ischemic) stress. That is why this phenomenon is considered substantially here.

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References

  1. Ganote C, Armstrong S. Ischaemia and the myocyte cytoskeleton: review and specula tion. Cardiovasc Res 1993; 27: 1387–1403.

    Article  Google Scholar 

  2. Cooper JA. The role of actin polymeriza tion in cell motility. Annu Rev Physiol 1991; 53: 585–605.

    Article  Google Scholar 

  3. Condeelis J. Life at the leading edge: The formation of cell protrusions. Annu Rev Cell Biol 1993;9: 411–444.

    Article  Google Scholar 

  4. Janmey PA, Hvidt S, Oster GF et al. Effect of ATP on actin filament stiffness. Nature 1990; 347: 44-49-

    Google Scholar 

  5. Pollard TD, Goldberg I, Schwartz WH. Nucleotide exchange, structure, and molecu lar properties of filaments assembled from ATP-actin and ADP-actin. J Biol Chem 1992; 267: 20339–20345.

    Google Scholar 

  6. Orlova A, Egelman EH. Structural basis for the destabilization of F-actin by phosphate release following ATP hydrolysis. J Mol Biol 1992; 227: 1043–1053.

    Article  Google Scholar 

  7. Pantaloni D, Carlier M-F. How profilin promotes actin filament assembly in the presence of thymosin β4. Cell 1993; 75: 1007–1014.

    Article  Google Scholar 

  8. Carlier M-F, Jean C, Rieger KJ et al. Modu lation of the interaction between G-actin and thymosin β4 by the ATP/ADP ratio: Possible implication in the regulation of actin dynamics. Proc Natl Acad Sci USA 1993; 90: 5034–5038.

    Article  Google Scholar 

  9. Safer D, Nachmias VT. Beta thymosins as actin binding peptides. BioEsseys 1994; 16: 473–479.

    Article  Google Scholar 

  10. Ikeuchi Y, Iwamura K, Machi T et al. In stability of F-actin of ATP: A small amount of myosin destabilizes F-actin. J Biochem 1992; 111: 606–613.

    Google Scholar 

  11. Laham LE, Way M, Yin HL, Janmey PA. Identification of two sites in gelsolin with different sensitivities to adenine nucleotides. Eur J Biochem 1995; 234: 1–7.

    Article  Google Scholar 

  12. Bershadsky AD, Gelfand VI, Svitkina TM, Tint IS. Destruction of microfilament bundles in mouse embryo fibroblasts treated with inhibitors of energy metabolism. Exp Cell Res 1980; 127: 421–429.

    Article  Google Scholar 

  13. Sanger JW, Sanger JM, Jockusch BM. Dif ferential response of three types of actin filament bundles to depletion of cellular ATP level. Eur J Cell Biol 1983; 31: 197–204.

    Google Scholar 

  14. Bershadsky AD, Gelfand VI. Role of ATP in the regulation of stability of cytoskeletal structures. Cell Biol Int Rep 1983; 7: 173–187.

    Article  Google Scholar 

  15. Wang YL. Reorganization of α-actinin and vinculin in living cells following ATP deple tion and replenishment. Exp Cell Res 1986; 167: 16–28.

    Article  Google Scholar 

  16. Glascott PA Jr, NcSorley KM, Mittal B et al. Stress fiber reformation after ATP deple tion. Cell Motil Cytoskeleton 1987; 8: 118–129.

    Article  Google Scholar 

  17. Hinshaw DB, Armstrong BC, Beals TF, Hyslop PA. A cellular model of endothelial cell ischemia. J Surg Res 1988; 44: 527–537.

    Article  Google Scholar 

  18. Hinshaw DB, Armstrong BC, Burger JM et al. ATP and microfilaments in cellular oxidant injury. Am J Pathol 1988; 132: 479–488.

    Google Scholar 

  19. Kuhne W, Besselmann M, Noll T et al. Disintegration of cytoskeletal structure of actin filaments in energy-depleted cells. Am J Physiol 1993; 264: H1599–H1608.

    Google Scholar 

  20. Hinshaw DB, Burger JM, Miller MT et al. ATP depletion induces an increase in the assembly of a labile pool of polymerized actin in endothelial cells. Am J Physiol 1993; 264: C1171–C1179.

    Google Scholar 

  21. Bacallao R, Gafinkel A, Monke S et al. ATP depletion: a novel method to study junc-tional properties in epithelial tissues. I. Rearrangement of the actin cytoskeleton. J Cell Sci 1994; 107: 3301–3313.

    Google Scholar 

  22. Golenhofen N, Doctor RB, Bacallao R, Mandel LJ. Actin and villin compart-mentation during ATP depletion and re covery in renal cultured cells. Kidney Int 1996; 48: 1837–1845.

    Article  Google Scholar 

  23. Molitoris BA, Geerdes A, Mclntoch JR. Dissociation and redistribution of Na+,K+−ATPase from its surface membrane actin cytoskeletal complex during cellular ATP depletion. J Clin Invest 1991; 88: 462–469.

    Article  Google Scholar 

  24. Gabai VL, Kabakov AE, Mosin AF. Ass ciation of blebbing with assembly of cytoskeletal proteins in ATP-depleted EL-4 ascites tumour cells. Tissue Cell 1992; 24: 171–177.

    Article  Google Scholar 

  25. Gabai VL, Kabakov AE. Tumor cell resis tance to energy deprivation and hyper-thermia can be determined by the actin skeleton stability. Cancer Lett 1993; 52: 3648–3654.

    Google Scholar 

  26. Kabakov AE, Gabai VL. Protein aggrega tion as primary and characteristic cell reac tion to various stresses. Experientia 1993; 49: 706–710.

    Article  Google Scholar 

  27. Gabai VL, Kabakov AE. Rise in heat-shock protein level confers tolerance to energy deprivation. FEBS Lett 1993; 327: 247–250.

    Article  Google Scholar 

  28. Kabakov AE, Gabai VL. Stress-induced in solubility of certain proteins in ascites tu mor cells. Arch Biochem Biophys 1994; 309: 247–253.

    Article  Google Scholar 

  29. Kabakov AE, Gabai VL. Heat shock-induced accumulation of 70-kDa stress protein (HSP70) can protect ATP-depleted tumor cells from necrosis. Exp Cell Res 1995; 217: 15–21.

    Article  Google Scholar 

  30. Kabakov AE, Molotkov AO, Budagova KR et al. Adaptation of Ehrlich ascites carci noma cells to energy deprivation in vivo can be associated with heat shock protein accumulation. J Cell Physiol 1995; 165: 1–6.

    Article  Google Scholar 

  31. Piper HM. Metabolic processes leading to myocardial cell death. Meth Achiev Exp Pathol 1988; 13: 144–180.

    Google Scholar 

  32. Steenbergen CJ, Hill ML, Jennings RB. Cytoskeletal damage during myocardial ischemia: changes in vinculin immunofluo rescence staining during total in vitro ischemia in canine heart. Circ Res 1987; 60: 478–486.

    Article  Google Scholar 

  33. Armstrong SC, Ganote CE. Flow cytometric analysis of isolated adult cardiomyocytes: vinculin and tubulin fluorescence during metabolic inhibition and ischemia. J Mol Cell Cardiol 1992;24: 149–162.

    Article  Google Scholar 

  34. VanWinkle WB, Snuggs M, Buja LM. Hypoxia-induced alterations in cytoskeleton coincide with collagenase expression in cultured neonatal rat cardio-myocytes. J Mol Cell Cardiol 1995; 27: 2531–2542.

    Article  Google Scholar 

  35. Ganote CE, Vander Heide RS. Cytoskeletal lesions in anoxic myocardial injury: a conventional and high voltage electron microscopic and immunofluorescence study. Am J Pathol 1987; 129: 327–344.

    Google Scholar 

  36. Barry WH, Hamilton CA, Knowlton KU. Regulated expression of a contractile protein gene correlates with recovery of contractile function after reversible metabolic inhibition in cultured myocytes. J Mol Cell Cardiol 1995; 27: 551–561.

    Article  Google Scholar 

  37. Kellerman PS, Bogusky RT. Microfilament disruption occurs very early in ischemic proximal tubule cell injury. Kidney Int 1992, 42: 896–902.

    Article  Google Scholar 

  38. Leiser J, Molitoris BA. Disease processes in epithelia: the role of the actin cytoskeleton and altered surface membrane polarity. Biochim Biophys Acta 1993; 1225: 1–13.

    Article  Google Scholar 

  39. Kellerman PS, Norenberg S, Guse N. Ex ogenous adenosine triphosphate (ATP) pre serves proximal tubule microfilament struc ture and function in vivo in a maleic acid model of ATP depletion. J Clin Invest 1993; 92: 1940–1949.

    Article  Google Scholar 

  40. Maro B, Bornens M. Reorganization of HeLa cell cytoskeleton induced by an uncoupler of oxidative phosphorylation. Nature 1982; 295: 334–336.

    Article  Google Scholar 

  41. Nover L. Heat Shock Response. Boca Raton: CRC Press, 1991.

    Google Scholar 

  42. Wiegant FAC, Van Bergen en Henegouwen PMP, Van Dongen G, Linnemans WAM. Stress-induced thermotolerance of the cytoskeleton of mouse neuroblastoma N2A cells and rat Reuber H35 hepatoma cells. Cancer Res 1987; 47: 1674–1680.

    Google Scholar 

  43. Bellomo G, Mirabelli F, Vairetti M, Malormi W. Cytoskeleton as a target in menadione-induced oxidative stress in cultured mammalian cells: biochemical and immunocytochemical features. J Cell Physiol 1990; 143: 118–128.

    Article  Google Scholar 

  44. Kabakov AE, Gabai VL. Heat shock pro teins maintain the viability of ATP-de prived cells: what is the mechanism? Trends Cell Biol 1994; 4: 193–196.

    Article  Google Scholar 

  45. Steenbergen C, Hill ML, Jennings RB. Vol ume regulation and plasma membrane injury in aerobic, anaerobic, and ischemic myocar dium in vitro. Circ Res 1985; 57: 864–875.

    Article  Google Scholar 

  46. Mandel LJ, Doctor RB, Bacallao R. ATP depletion: a novel method to study junc-tional properties in epithelial tissues. II. Internalization of Na+,K+-ATPase and E-cadherin. J Cell Sci 1994; 107: 3315–3324.

    Google Scholar 

  47. Atsma DE, Bastiaanse EML, Jerzewski A et al. Role of calcium-activated neutral protease (calpain) in cell death in cultured neonatal rat cardiomyocytes during meta bolic inhibition. Circ Res 1995; 76: 1071–1078.

    Article  Google Scholar 

  48. Sun FF, Fleming WE, Taylor BM. Degradation of membrane phospholipids in the cul tured human astroglial cell line UC-11MG during ATP depletion. Biochem Pharmacol 1993; 45: 1149–1155.

    Article  Google Scholar 

  49. Trump BF, Berezesky IK. The role of calcium in cell injury and repair: a hypothesis. Surv Synth Pathol Res 1985; 97: 248–256.

    Google Scholar 

  50. Steenbergen C, Murphy E, Watts JA, London RE. Correlation between cytosolic free calcium, contracture, ATP, and irreversible ischemic injury in perfused rat heart. Circ Res 1990; 66: 135–146.

    Article  Google Scholar 

  51. Niemenen A-L, Gores GJ, Wray BE et al. Calcium dependence of bleb formation and cell death in hepatocytes. Cell Calcium 1988; 9: 237–246.

    Article  Google Scholar 

  52. Jurkowitz-Alexander MS, Altschuld RA, Haun SE et al. Protection of ROC-1 hybrid glial cells by polyethylene glycol following ATP depletion. J Neurochem 1993; 61: 1581–1584.

    Article  Google Scholar 

  53. Cantiello HF. Actin filaments stimulate the Na+-K+ATPase. Am J Physiol (Renal Fluid and Electrolyte Physiology) 1995; 38: F637–F643.

    Google Scholar 

  54. Nguyen VT, Morange M, Bensaude O. Protein denaturation during heat shock and related stress. J Biol Chem 1989; 264: 10487–10492.

    Google Scholar 

  55. Bensaude O, Pinto MP, Dubois M-F et al. Protein denaturation during heat shock and related stress. In: Schlesinger MJ and Santoro G, eds. Stress Proteins. Induction and Function. Berlin: Springer Verlag, 1990: 89–99.

    Google Scholar 

  56. Dubois M-F, Hovanessian AG, Bensaude O. Heat shock-induced denaturation of proteins. Characterization of the insolubility of the interferon-induced p68 kinase. J Biol Chem 1991; 266: 9707–9711.

    Google Scholar 

  57. Bensaude O, Dubois M-F, Legagneux V et al. Early effects of heat shock on enzymes: heat denaturation of reporter proteins and activation of a protein kinase which phospho-rylates the C-terminal domain of RNA poly-merase II. In: Maresca B, Lindquist S, eds. Heat Shock. Berlin: Springer Verlag, 1991:97–103.

    Chapter  Google Scholar 

  58. Pinto M, Morange M, Bensaude O. Dena turation of proteins during heat shock. J Biol Chem 1991; 266: 13941–13946.

    Google Scholar 

  59. Nguyen VT, Bensaude O. Increased ther mal protein aggregation in ATP-depleted mammalian cells. Eur J Biochem 1994; 220: 239–246.

    Article  Google Scholar 

  60. Gabai VL, Kabakov AE. Induction of heat-shock protein synthesis and thermo-toler-ance in EL-4 ascites tumor cells by transient ATP depletion after ischemic stress. Exp Mol Pathol 1994; 60: 88–99.

    Article  Google Scholar 

  61. Gabai VL, Mosina VA, Budagova KR, Kabakov AE. Spontaneous over-expression of heat-shock proteins in Ehrlich ascites carcinoma cells during in vivo growth. Biochem Mol Biol Int 1995; 35: 95–102.

    Google Scholar 

  62. Musters RJP, Post JA, Verkleij AJ. The isolated neonatal rat-cardiomyocyte used in an in vitro model for “ischemia”. I: a mor phological study. Biochim Biophys Acta 1991; 1091: 270–277.

    Article  Google Scholar 

  63. Schneijdenberg CTWM, Verkleij AJ, Post JA. Aggregation of myocardial sarcolemmal transmembrane proteins is not hindered by an interaction with the cyto-skeleton. Possible implications for ischemia and reper-fusion. J Mol Cell Cardiol 1995; 27: 2337–2345.

    Article  Google Scholar 

  64. Hayashi T, Takada K, Matsuda M. Subcel-lular distribution of ubiquitin-protein conjugates in the hippocampus following tran sient ischemia. J Neurosci Res 1992; 31: 561–564.

    Article  Google Scholar 

  65. Hayashi T, Takada K, Matsuda M. Post-transient ischemia increase in ubiquitin conjugates in the early reperfusion. Neuro report 1992; 3: 519–520.

    Google Scholar 

  66. Hayashi T, Tanaka J, Kamikubo T et al. Increase in ubiquitin conjugates dependent on ischemic damage. Brain Res 1993; 620: 171–173.

    Article  Google Scholar 

  67. Andres J, Sharma HS, Knoll R et al. Ex pression of heat shock proteins in the nor mal and stunned porcine myocardium. Cardiovasc Res 1993; 27: 1421–1429.

    Article  Google Scholar 

  68. Jungbluth A, Eckerskorn C, Gerisch G et al. Stress-induced tyrosine phos-phorylation of actin in Dictyostelium cells and localiza tion of the phosphorylation site to tyrosine-53 adjacent to the DNase I binding loop. FEBS Lett 1996; 375: 87–90.

    Article  Google Scholar 

  69. Palleros DR, Welch WJ, Fink AL. Interac tion of hsp70 with unfolded proteins: Effects of temperature and nucleotides on the kinet ics of binding. Proc Natl Acad Sci USA 1991; 88: 5719–5723.

    Article  Google Scholar 

  70. Palleros DR, Reid KL, Shi L et al. ATP-induced protein-Hsp70 complex dissociation requires K+ but not ATP hydrolysis. Na ture 1993; 365: 664–666.

    Google Scholar 

  71. Palleros DR, Shi L, Reid KL, Fink AL. Hsp70-protein complexes; complex stability and conformation of bound substrate pro tein. J Biol Chem 1994; 269: 13107–13114.

    Google Scholar 

  72. Barbato R, Menabo R, Dainese P et al. Binding of cytosolic proteins to myofibrils in ischemic rat hearts. Circ Res 1996; 78: 821–828.

    Article  Google Scholar 

  73. Michels AA, Nguyen VT, Konings AWT et al. Thermostability of a nuclear targeted luciferase expressed in mammalian cells. Destabilizing influence of the intranuclear microenvironment. Eur J Biochem 1995; 234: 382–389.

    Article  Google Scholar 

  74. Imamoto N, Matsuoka Y, Kurihara T et al. Antibodies against 70-kD heat shock cog nate protein inhibit mediated nuclear im port of karyophilic proteins. J Cell Biol 1992; 119: 1047–1061.

    Article  Google Scholar 

  75. Gronostajski RM, Pardee AB, Goldberg AL. The ATP dependence of the degradation of short and long lived proteins in growing fibroblasts. J Biol Chem 1985; 260: 3344–3349.

    Google Scholar 

  76. Orino E, Tanaka K, Tamura T et al. ATP-dependent reversible association of pro-teasomes with multiple protein components to form 26S complexes that degrade ubiquitinated proteins in human HL-60 cells. FEBS Lett 1991; 284: 206–210.

    Article  Google Scholar 

  77. Gabai VL, Kabakov AE, Makarova YuM et al. DNA fragmentation in Ehrlich ascites carcinoma under exposures causing cyto-skeletal protein aggregation. Biochemistry (Moscow, engl transi) 1994; 59: 399–404.

    Google Scholar 

  78. Gabai VL, Zamulaeva IV, Mosin AF et al. Resistance of Ehrlich tumor cells to apoptosis can be due to accumulation of heat shock proteins. FEBS Lett 1995; 375: 21–26.

    Article  Google Scholar 

  79. Ucker DS, Obermiller PS, Eckhart W et al. Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol Cell Biol 1992; 12: 3060–3069.

    Google Scholar 

  80. Peitsch MC, Polzar B, Stephan H et al. Characterization of the endogenous deox-yribonuclease involved in nuclear DNA egradation during apoptosis (programmed cell death). EMBO J 1993; 12: 371–377.

    Google Scholar 

  81. Kim D, Lee YJ, Corry PM. Constitutive HSP70: Oligomerization and its dependence on ATP binding. J Cell Physiol 1992; 153: 353–361.

    Article  Google Scholar 

  82. Brown CR, Martin RL, Hansen WJ et al. The constitutive and stress-inducible forms of hsp70 exhibit functional similarities and interact with one another in an ATP-depen-dent fashion. J Cell Biol 1993; 120: 1101–1112.

    Article  Google Scholar 

  83. Beckmann RP, Mizzen LA, Welch WJ. Interaction of hsp70 with newly synthesized proteins: implications for protein folding and assembly. Science 1990; 248: 850–854.

    Article  Google Scholar 

  84. Beckmann RP, Lovett M, Welch WJ. Examining the function and regulation of hsp70 in cells subjected to metabolic stress. J Cell Biol 1992; 117: 1137–1150.

    Article  Google Scholar 

  85. Hightower LE, Sadis SE. Interaction of ver tebrate hsc70 and hsp70 with unfolded proteins and peptides. In: Morimoto RI, Tissieres A, Georgopoulos C, eds. The Biology of Heat Shock Proteins and Molecu lar Chaperones. New York: Cold Spring Harbor Laboratory Press, 1994: 179–207.

    Google Scholar 

  86. Margulis BA, Welsh M. Analysis of protein binding to heat shock protein 70 in pancre atic islet cells exposed to elevated tempera ture or interleukin lβ. J Biol Chem 1991; 266: 9295–9298.

    Google Scholar 

  87. Haus U, Trommler P, Fisher PR et al. The heat shock cognate protein from Dictyostelium affects actin polymerization through inter action with the actin-binding protein cap32/ 34. EMBO J 1993; 12: 3763–3771.

    Google Scholar 

  88. Liao J, Lowthert LA, Ghori N, Omary MB. The 70-kDa heat shock proteins associate with glandular intermediate filaments in an ATP-dependent manner. J Biol Chem 1995; 270: 915–922.

    Article  Google Scholar 

  89. Sadis S, Hightower LE. Unfolded proteins stimulate molecular chaperone Hsc70 AT-Pase by accelerating ADP/ATP exchange. Biochemistry 1992; 31: 9406–9412.

    Article  Google Scholar 

  90. Hesketh JE, Pryme IF. Interaction between mRNA, ribosomes and the cytoskeleton (a review). Biochem J 1991; 277:1-10.

    Google Scholar 

  91. Flaherty KM, DeLuca-Flaherty C, McKay DB. Three dimensional structure of the ATPase fragment of a 7OK heat-shock cog nate protein. Nature 1990; 346: 623–628.

    Article  Google Scholar 

  92. Kampinga HH. Thermotolerance in mam malian cells. Protein denaturation and ag gregation, and stress proteins. J Cell Sci 1993; 104: 11–17.

    Google Scholar 

  93. Tuijl MJM, van Bergen en Henegouwen PMP, van Wijk R et al. The isolated neo natal rat-cardiomyocyte used in an in vitro model for ‘ischemia’. II. Induction of the 68 kDa heat shock protein. Biochim Biophys Acta 1991; 1091: 278–284.

    Article  Google Scholar 

  94. Hohfeld J, Minami Y, Hartl F-U. Hip, a novel cochaperone involved in the eukary-otic Hsc70/Hsp40 reaction cycle. Cell 1995; 83: 589–598.

    Article  Google Scholar 

  95. Longoni S, Lattonen S, Bullock G et al. Cardiac alpha-crystallin. II. Intra-cellular local ization. Mol Cell Biochem 1990; 97: 121–128.

    Article  Google Scholar 

  96. Chiesi M, Longoni S, Limbruno U. Cardiac alpha-crystallin. III. Involvement during heart ischemia. Mol Cell Biochem 1990; 97: 129–136.

    Article  Google Scholar 

  97. Bennardini F, Wrzosek A, Chiesi M. αB-crystallin in cardiac tissue. Association with actin and desmin filaments. Circulation Res 1992; 71: 288–294.

    Article  Google Scholar 

  98. Loktionova SA, Ilyinskaya OP, Gabai VL, Kabakov AE. Distinct effects of heat shock and ATP depletion on distribution and isoform patterns of human Hsp27 in endo-thelial cells. FEBS Lett 1996; 392: 100–104.

    Article  Google Scholar 

  99. Engel K, Knauf U, Gaestel M. Generation of antibodies against human hsp27 and murine hsp25 by immunization with a chimeric small heat shock protein. Biomed Biochim Acta 1991; 50: 1065–1071.

    Google Scholar 

  100. Jakob U, Gaestel M, Engel K, Buchner J. Small heat shock proteins are molecular chap-erones. J Biol Chem 1993; 268: 1517–1520.

    Google Scholar 

  101. Arrigo A-P, Landry J. Expression and function of the low-molecular-weight heat shock proteins. In: Morimoto RI, Tissieres A, Georgopoulos C, eds. The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1994: 335–373.

    Google Scholar 

  102. Kato K, Hasegawa K, Goto S, Inaguma Y. Dissociation as a result of phosphorylation of an aggregated form of the small stress protein, hsp27. J Biol Chem 1994; 269: 11274–11278.

    Google Scholar 

  103. Benndorf R, Hayeb K, Ryazantsev S et al. Phosphorylation and supra-molecular orga nization of murine small heat shock protein HSP25 abolish its actin polymerization-in hibiting activity. J Biol Chem 1994; 269: 20780–20784.

    Google Scholar 

  104. Saklatvala J, Kaur P, Guesdon F. Phospho rylation of the small heat-shock protein is regulated by interleukin 1, tumor necrosis factor, growth factors, bradykinin and ATP. Biochem J 1991; 277: 635–642.

    Google Scholar 

  105. Pombo CM, Bonventre JV, Avruch J et al. Stress-activated protein kinases are major c-jun N-terminal kinases activated by ischemia and reperfusion. J Biol Chem 1994; 269: 26546–26551.

    Google Scholar 

  106. Bogoyevitch A, Ketterman AJ, Sugden PH. Cellular stresses differentially activate c-jun N-terminal protein kinases and extracellu lar signal-regulated protein kinases in cul tured ventricular myocytes. J Biol Chem 1995; 270: 29710–29717.

    Article  Google Scholar 

  107. Seko Y, Tobe K, Ueki K et al. Hypoxia and hypoxia/reoxygenation activate Raf-1, mi togen-activated protein kinase kinase, mi togen-activated protein kinases, and S6 kinase in cultured rat cardiac myocytes. Circ Res 1996; 78: 82–90.

    Article  Google Scholar 

  108. Kato H, Chen T, Liu XH et al. Immuno-histochemical localization of ubiquitin in gerbil hippocampus with induced tolerance to ischemia. Brain Res 1993; 619: 339–343.

    Article  Google Scholar 

  109. Morimoto T, Ide T, Ihara Y et al. Transient ischemia depletes free ubiquitin in the gerbil hippocampal CA1 neurons. Am J Pathol 1996; 148: 249–257.

    Google Scholar 

  110. Kamikubo T, Hayashi T. Changes in proteasome activity following transient ischemia. Neurochem Int 1996; 28:209–212.

    Article  Google Scholar 

  111. Jentsch S. Ubiquitin-dependent protein degradation: a cellular perspective. Trends Cell Biol 1992; 2: 98–103.

    Article  Google Scholar 

  112. Molitoris BA, Dahl R, Hosford M. Cellular ATP depletion induces disruption of the spectrin cytoskeletal network. Am J Physiol (Renal Fluid Electrolyte Physiol) 1996; 40: F790–F798.

    Google Scholar 

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  1. Medical Radiology Research Center, Russian Academy of Medical Sciences, Obninsk, Russia

    Alexander E. Kabakov Ph.D & Vladimir L. Gabai Ph.D

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  1. Alexander E. Kabakov Ph.D
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Kabakov, A.E., Gabai, V.L. (1997). “Proteotoxicity” of ATP Depletion: Disruption of the Cytoskeleton, Protein Aggregation and Involvement of Molecular Chaperones. In: Heat Shock Proteins and Cytoprotection. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6007-4_3

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