Molecular chaperones and their roles in neural cell differentiation

Developmental Neuroscience

Volumn 24, Issue 1, 2002, Pages 1-13

  Calabrese, Vittorio ^b   Scapagnini, G ^c   Ravagna, A ^c   Giuffrida Stella, A M ^c   Butterfield, D A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF CATANIA   (Italy)

^c NONE

Author keywords

Antioxidants; Cell differentiation; Heat shock proteins; Neuronal pattern; Protein folding disease

Indexed keywords

AMPHETAMINE DERIVATIVE; ANSAMYCIN DERIVATIVE; BETA TUBULIN; CHAPERONE; GELDANAMYCIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE REGULATED PROTEIN; HEAT SHOCK FACTOR 1; HEAT SHOCK FACTOR 2; HEAT SHOCK FACTOR 2ALPHA; HEAT SHOCK FACTOR 2BETA; HEAT SHOCK FACTOR 4; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 100; HEAT SHOCK PROTEIN 20; HEAT SHOCK PROTEIN 32; HEAT SHOCK PROTEIN 47; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90ALPHA; HEAT SHOCK PROTEIN 90BETA; HELIX LOOP HELIX PROTEIN; HERBIMYCIN; LYSERGIDE; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; RAF PROTEIN; STEROID RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; APOPTOSIS; BRAIN INJURY; BRAIN ISCHEMIA; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROTECTION; CELL STRAIN K 562; CELL SURVIVAL; CREUTZFELDT JAKOB DISEASE; DEGENERATIVE DISEASE; DNA BINDING; DNA TRANSCRIPTION; EMBRYO DEVELOPMENT; EMBRYO INDUCTION; GENE DISRUPTION; GENE EXPRESSION; GENETIC CODE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HYPERTHERMIA; IMMUNOCYTOCHEMISTRY; MAMMAL CELL; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; PURKINJE CELL; REVIEW; SEIZURE; TEMPERATURE SENSITIVITY; WESTERN BLOTTING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HUMANS; MAMMALS; MOLECULAR CHAPERONES; NERVE TISSUE PROTEINS; NEURONS; OXIDATIVE STRESS; STRESS;

EID: 0036969748     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000064941     Document Type: Review

References (95)

1. Calabrese V, Bates TE, Stella AM: NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: The role of oxidant/antioxidant balance. Neurochem Res 2000;25:1315-1341.
2. Hightower LE: Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 1991;66: 1-20.
3. Le Douarin NM, Smith J: Development of the peripheral nervous system from the neural crest. Annu Rev Cell Biol 1988;4:375-404.
4. Puelles L, Rubenstein JL: Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 1993;16:472-479.
5. Loones MT, Chang Y, Morange M: The distribution of heat shock proteins in the nervous system of the unstressed mouse embryo suggests a role in neuronal and non-neuronal differentiation. Cell Stress Chaperones 2000;5: 291-305.
6. Nornes HO, Das GD: Temporal pattern of neurogenesis in spinal cord of rat: An autoradiographic study-time and sites of origin and migration and settling patterns of neuroblasts. Brain Res 1974;73:121-138.
7. Easter SS, Ross LS, Frankfurter A: Initial tract formation in the mouse brain. J Neurosci 1993; 13:285-299.
8. Raff MC, Miller RH, Noble M: A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 1983;303:390-396.
9. Oppenheim RW: Cell death during development of the nervous system. Annu Rev Neurosci 1991;14:453-501.
10. Walsh D, Li Z, Wu Y, Nagata K: Heat shock and the role of the HSPs during neural plate induction in early mammalian CNS and brain development. Cell Mol Life Sci 1997;53:198-211.
11. Morimoto RI, Santoro MG: Stress-inducible response and heat shock proteins: New pharmacologic targets for cytoprotection. Nat Biotechnol 1998;16:833-838.
12. Santoro MG: Heat shock and the control of the stress response. Biochem Pharmacol 2000;59: 55-63.
13. Morimoto RI, Kline MP, Bimston DN, Cotto JJ: The heat shock response: Regulation and function of heat shock proteins and molecular chaperones. Essays Biochem 1997;32:17-29.
14. Minami Y, Hohfeld J, Ohtsuka K, Hartl FU: Regulation of the heat shock protein 70 reaction cycle by the mammalian DnaJ homolog Hsp40. J Biol Chem 1996;271:19617-19624.
15. Morrison AJ, Rush SJ, Brown IR: Heat shock transcription factors and the hsp70 induction response in brain and kidney of the hyperthermic rat during postnatal development. J Neurochem 2000;75:363-372.
16. Goodson ML, Park-Sarge OK, Sarge KD: Tissue-dependent expression of heat shock factor 2 isoforms with distinct transcriptional activities. Mol Cell Biol 1995;15:5288-5293.
17. Xia W, Voellmy R: Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers. J Biol Chem 1997;272:4094-4102.
18. McMillan DR, Xiao X, Shao L, Graves K, Benjamin IJ: Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J Biol Chem 1998;273:7523-7528.
19. Xiao X, Zuo X, Davis AA, McMillan DR, Curry, BB, Richardson JA, Benjamin IJ: HSF1 is required for extra-embryonic development postnatal growth and protection during inflammatory responses in mice. EMBO J 1999;18: 5943-5952.
20. Sistonen L, Sarge KD, Morimoto R: Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription. Mol Cell Biol 1994;14: 2087-2099.
21. Sistonen L, Sarge KD, Phillips B, Abravaya K, Morimoto RI: Activation of heat shock factor 2 during hemin-induced differentiation of human erythroleukemia cells. Mol Cell Biol 1992; 12:4104-4111.
22. Eriksson M, Jokinen E, Sistonen L, Leppa S: Heat shock factor 2 is activated during mouse heart development. Int J Dev Biol 2000;44: 471-477.
23. Rallu M, Loones M, Lallemand Y, Morimoto R, Morange M, Mezger V: Function and regulation of heat shock factor 2 during mouse embryogenesis. Proc Natl Acad Sci USA 1997; 94:2392-2397.
24. Mathew A, Mathur SK, Morimoto RI: Heat shock response and protein degradation: Regulation of HSF2 by the ubiquitin-proteasome pathway. Mol Cell Biol 1998;18:5091-5098.
25. Hong Y, Sarge KD: Regulation of protein phosphatase 2A activity by heat shock transcription factor 2. J Biol Chem 1999;274:12967-12970.
26. Cohen BR, Sladek CD: Expression of floor plate in dispersed mesencephalic cultures: Role in differentiation of tyrosine hydroxylase neurons. Exp Neurol 1997;147:525-531.
27. Fink AL, Goto Y: Molecular chaperones: Clamps for the Clps? Curr Biol 1998;8:R464-R467.
28. Welch WJ: Mammalian stress response: Cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 1992;72:1063-1081.
29. Quraishi H, Brown IR: Expression of heat shock protein 90 (Hsp90) in neural and non-neural tissues of the control and hyperthermic rabbit. Exp Cell Res 1995;219:358-363.
30. Acquino DA, Klipfel AA, Brosnan CF, Norton WT: The 70-kDa heat shock cognate protein (HSC70) is a major constituent of the central nervous system and is up-regulated only at the mRNA level in acute experimental autoimmune encephalomyelitis. J Neurosci 1993;61: 1340-1348.
31. Brown IR, Rush SJ: Expression of heat shock genes (hsp70) in the mammalian brain: Distinguishing constitutively expressed and hyperthermia-inducible mRNA species. J Neurosci Res 1990;25:14-19.
32. Brown IR: Induction of heat shock genes in the mammalian brain by hyperthermia and tissue injury; in Mayer RJ, Brown IR (eds): Heat Shock Proteins in the Nervous System. London, Academic Press, 1994, pp 31-53.
33. Mayer Plumier J-CL, Armstrong JN, Landry J, Babity JM, Robertson HA, Currie RW: Expression of the 27,000 mol. wt. heat shock protein following kainic acid-induced status epilepticus in the rat. Neuroscience 1996;75:849-856.
34. Kato S, Hirano A, Umahara T, Kato M, Herz F, Ohama E: Comparative immunohistochemical study on the expression of alpha B crystallin, ubiquitin and stress-response protein 27 in ballooned neurons in various disorders. Neuropathol Appl Neurobiol 1992;18:335-340.
35. Hartl FU: Molecular chaperones in cellular protein folding. Nature 1996;381:571-579.
36. Nathan DF, Harju-Vos M, Lindquist S: In vivo functions of Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 1997;94: 12949-12956.
37. Rutherford SL, Linquist S: Hsp90 as a capacitor for morphological evolution. Nature 1998; 396:336-342.
38. Picard D, Kursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR: Reduced levels of Hsp90 compromise steroid receptor action in vivo. Nature 1990;348:166-168.
39. Shaknovitch R, Shue G, Kotz S: Conformational activation of abasic helix-loop-helix protein (MyoD1) by the C-terminal region of murine Hsp90 (Hsp84). Cell Biol 1992;12:5059-5068.
40. McGuire J, Coumailleau P, Withelaw ML, Gustafsson JA, Poellingher L: The basic loop-helix/PAS factor Sim is associated with Hsp90: Implication for regulations by interaction with partner factors. J Biol Chem 1996;270:31353-31357.
41. Kageyama R, Nakanishi S: Helix-loop-helix in growth and differentiation of the vertebrate nervous system. Curr Genet Dev 1997;7:659-665.
42. Yi SJ, Master JN, Baram TZ: Glucocorticoid receptor mRNA ontogeny in the fetal and post-natal rat forebrain. Mol Cell Neurosci 1994;5: 385-393.
43. Olazabal UE, Pfaff DW, Mobbs CV: Estrogenic regulation of heat shock protein 90 kDa in the rat ventromedial hypothalamus and uterus. Mol Cell Endocrinol 1992;84:175-183.
44. D'Souza SM, Brown IR: Constitutive expression of heat shock proteins Hsp90, Hsc70, Hsp70 and Hsp60 in neural and non-neural tissues of the rat during postnatal development. Cell Stress Chaperones 1998;3:188-199.
45. Takeda A, Perry G, Abraham NG, Dwyer BE, Kutty RK: Laitinen JT, Petersen RB, Smith MA: Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau. J Biol Chem 2000;275:5395-5399.
46. Yenay MA, Giffard R, Sapolsky RM, Steinberg GK: The neuroprotective potential of heat shock protein (Hsp70). Mol Med Today 1999; 51:525-531.
47. Yenari MA, Fink SL, Sun GH, Chang LK, Patel MK, Kunis DM, Onley D, Ho DY, Sapolsky RM, Steinberg GK: Gene therapy with Hsp72 is neuroprotective in rat models of stroke and epilepsy. Am Neurol 1998;44:584-591.
48. Hata R, Gass P, Mies G, Wiessner C, Hossmann KA: Attenuated c-fos mRNA induction after middle cerebral artery occlusion in CREB knockout mice does not modulate focal ischemic injury. J Cereb Blood Flow Metab 1998; 18:1325-1335.
49. Nishimura RN, Dwyer BE: Pharmacological induction of heat shock protein 68 synthesis in cultured rat astrocytes. J Biol Chem 1995;270: 29967-29970.
50. Fink SL, Chang LK, Ho DY, Sapolsky RM: Defective herpes simplex virus vectors expressing the rat brain stress-inducible heat shock protein 72 protect cultured neurons from severe heat shock. J Neurochem 1997;68:961-969.
51. Huot J, Houle F, Marceau F, Landry J: Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 1997;80:383-392.
52. Takayama S, Bimston DN, Matsuzawa S, Freeman BC, Aime-Sempe C, Xie Z, Morimoto RI, Reed JC: BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J 1997;16: 4887-4896.
53. Calabrese, V, Copani A, Testa D, Ravagna A, Spadaro F, Tendi E, Nicoletti VG, Giuffrida Stella AM: Nitric oxide synthase induction in astroglial cell cultures: Effect on heat shock protein 70 synthesis and oxidant/antioxidant balance. J Neurosci 2000;60:613-622.
54. Calabrese V, Testa D, Ravagna A, Bates TE, Giuffrida Stella AM: Hsp70 induction in the brain following ethanol administration in the rat: Regulation by glutathione redox state. Biochem Biophys Res Commun 2000;269:397-400.
55. Kato M, Mizuguchi M, Takashima S: Developmental changes of heat shock protein 73 in human brain. Brain Res Dev Brain Res 1995; 86:180-186.
56. Sharp FR, Massa S, Swanson RA: Heat shock protein protection. TINS 1999;22:97-99.
57. Goldbaum O, Richter-Landsberg C: Stress proteins in oligodendrocytes: Differential effects of heat shock and oxidative stress. J Neurochem 2001;78:1233-1242.
58. Maines MD: The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517-554.
59. Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, Green CJ: Endothelial heme oxygenase-1 induction by hypoxia: Modulation by inducible nitric oxide synthase (iNOS) and S-nitrosothiols. J Biol Chem 2000;275:13613-13620.
60. Morano KA, Thiele DJ: Heat shock factor function and regulation in response to cellular stress, growth and differentiation signals. Gene Expr 1999;7:271-282.
61. Panahian N, Yoshiura M, Maines MD: Over-expression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 1999;72:1187-1203.
62. Butterfield DA, Drake J, Pocernich C, Castegna A: Evidence of oxidative damage in Alzheimer's disease brain: Central role for amyloid β-peptide. Trends Mol 2001;7:548-554.
63. Schipper HM, Cissè S, Stopa EG: Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann Neurol 1995;37: 758-768.
64. Schipper HM, Liberman A, Stopa EG: Neural heme oxygenase-1 expression in idiopathic Parkinson's disease. Exp Neurol 1998;150:60-68.
65. Turner CP, Bergeron M, Matz P, Zegna A, Noble LJ, Panter SS, Sharp FR: Heme oxygenase-1 is induced in glia throughout brain by subarachnoid hemoglobin. J Cereb Blood Flow Metab 1998;18:257-273.
66. Nath KA, Haggard JJ, Croatt AJ, Grande JP, Poss KD, Alam J: The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am J Pathol 2000;156:1527-1535.
67. Klemenz R, Frohli E, Steiger RH, Schafer R, Aoyama A: Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci USA 1991; 88:3652-3656.
68. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J: Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 1995;15:505-516.
69. Saklatvala J, Kaur P, Guesdon F: Phosphorylation 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.
70. Imura T, Shimohama S, Sato M, Nishikawa H, Madono K, Akaike A, Kimura J: Differential expression of small heat shock proteins in reactive astrocytes after focal ischemia: Possible role of beta-adrenergic receptor. J Neurosci 1999;19:9768-9779.
71. Arrigo AP: Expression of stress genes during development. Neuropathol Appl Neurobiol 1995;21:488-491.
72. Zhang WL, Tsuneishi S, Nakamura H: Induction of heat shock proteins and its effects on glial differentiation in rat C6 glioblastoma cells. Kobe J Med Sci 2001;47:77-95.
73. Mehlen P, Schulze-Osthoff K, Arrigo AP: Small stress proteins as novel regulators of apoptosis: Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 1996;271:16510-16514.
74. 2 in an oxidative stress-resistant cell line. J Cell Physiol 1998;177:606-617.
75. Nicholl ID, Quinlan RA: Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J 1994;13:945-953.
76. Armstrong CL, Krueger-Naug AM, Currie RW, Hawkes R: Constitutive expression of heat shock protein Hsp25 in the central nervous system of the developing and adult mouse. J Comp Neurol 2001;434:262-274.
77. Calabrese V, Scapagnini G, Giuffrida Stella AM, Bates TE, Clark JB: Mitochondrial involvement in brain function and dysfunction: Relevance to aging, neurodegenerative disorders and longevity. Neurochem Res 2001;26: 739-764.
78. Kaneko M, Abe K, Kogure K, Saito H, Matsuki N: Correlation between electroconvulsive seizure and Hsc70 mRNA induction in mice brain. Neurosci Lett 1993;157:195-198.
79. Nedivi E, Evroni D, Naot D, Israeli D, Citri Y: Numerous candidate plasticity genes revealed by differential cDNA cloning. Nature 1993; 363:718-722.
80. Liang P, McRae TH: Molecular chaperones and the cytoskeleton. J Cell Sci 1997;110: 1431-1440.
81. Mairesse N, Horman S, Mosselmans R, Galand P: Antisense inhibition of the 27 kDa heat shock protein production affects growth rate and cytoskeleton organization in MCF-7 cells. Cell Biol Int 1996;20:205-212.
82. Djabali K, De Nechaud B, Landon F, Portier FF: Alpha-β-crystallin interacts with intermediate filaments in response to stress. J Cell Sci 1997;110:2759-2769.
83. Blak MM, Chestnut MH, Pleasure JT, Keen JH: Stable clathrin: Uncoating protein (Hsc70) complexes in intact neurons and their axonal transport. J Neurosci 1991;11:1163-1172.
84. Tsang TC: New model for 70 kDa heat shock protein, potential mechanism of function. FEBS Lett 1993;323:1-3.
85. Lomax P: Implications of drugs for heat and exercise tolerance; in Hales JRS, Richards DAB (eds): Heat Stress: Physical Exertion and Environment. Amsterdam, Experta Medica, Elsevier Science, 1987, pp 399-418.
86. Milunsky A, Ulcicas M, Rothman KJ, Willett W, Jick S, Jick H: Maternal heat exposure and neural tube defects. JAMA 1992;268:882-885.
87. Edwards MJ, Shiota K, Smith MS, Wealsh DA: Hyperthermia and birth defects. Reprod Toxicol 1995;9:411-425.
88. Kedzireska S, Jezierski G, Taylor A: DnaK/ DnaJ chaperone system reactivates endogenous E. coli thermostable FBP aldolase in vivo and in vitro: The effect is enhanced by GroE heat shock proteins. Cell Stress Chaperones 2001;6:29-37.
89. Calabrese V, Renis M, Calderone A, Russo A, Barcellona ML, Rizza V: Stress proteins and SH-groups in oxidant-induced cell damage after acute ethanol administration in rat. Free Radic Biol Med 1996;20:391-397.
90. Calabrese V, Renis M, Calderone A, Russo A, Reale S, Barcellona ML, Rizza V: Stress proteins and SH-groups in oxidant-induced cell injury after chronic ethanol administration in rat. Free Radic Biol Med 1998:24:1159-1167.
91. Calabrese V, Scapagnini G, Catalano C, Bates TE, Geraci D, Pennisi G, Giuffrida Stella AM: Induction of heat shock protein synthesis in human skin fibroblasts in response to oxidative stress. Regulation by vitamin E. Int J Tissue React 2001;23:91-99.
92. Calabrese V, Scapagnini G, Catalano C, Bates TE, Dinotta F, Micali G, Giuffrida Stella AM: Induction of heat shock protein synthesis in human skin fibroblasts in response to oxidative stress: Regulation by a natural antioxidant from rosemary extract. Int J Tissue React 2001; 23:121-128.
93. Stephanou A, Isenberg DA, Nakajima K, Latchman DS: Signal transducer and activator of transcription-1 and heat shock factor-1 interact and activate the transcription of the HSP70 and HS90beta gene promoters. J Biol Chem 1999;274:1723-1728.
94. He H, Chen C, Xie Y, Asea A, Calderwood SK: Hsp70 and heat shock factor 1 cooperate to repress Ras-induced transcriptional activation of the c-fos gene. Cell Stress Chaperones 2000; 5:406-411.
95. Asea A, Kabingu E, Stevenson MA, Calderwood SK: Hsp70 peptide-bearing and peptide-negative preparations act as chaperokines. Cell Stress Chaperones 2000;5:425-431.