Cloning, characterization, and heat stress-induced redistribution of a protein homologous to human hsp27 in the zebrafish Danio rerio

Experimental Cell Research

Volumn 306, Issue 1, 2005, Pages 230-241

  Mao, Li ^a   Bryantsev, Anton L ^a   Chechenova, Maria B ^a   Shelden, Eric A ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Actin; Cytoskeleton; Epithelial; Heart; Hsp27; Hyperthermia; Injury; Muscle; Stress; Zebrafish

Indexed keywords

ACTIN; ANISOMYCIN; HEAT SHOCK PROTEIN 27; HYBRID PROTEIN; MESSENGER RNA; ZEBRAFISH PROTEIN;

ACTIN FILAMENT; ACTIN MYOSIN INTERACTION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EMBRYO DEVELOPMENT; FIBROBLAST; GENE CONTROL; GENE FUNCTION; GENE SEQUENCE; GENETIC CONSERVATION; HEAT STRESS; MAMMAL CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; TELEOST; UPREGULATION; ZEBRA FISH;

ANIMALIA; DANIO RERIO; MAMMALIA; TELEOSTEI;

EID: 18844378922     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.02.007     Document Type: Article

References (68)

1. J.M. Fontaine, J.S. Rest, M.J. Welsh, and R. Benndorf The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins Cell Stress Chaperones 8 2003 62 69
2. C. Liu, and M.J. Welsh Identification of a site of Hsp27 binding with Hsp27 and alpha B-crystallin as indicated by the yeast two-hybrid system Biochem. Biophys. Res. Commun. 255 1999 256 261
3. X. Sun, J.M. Fontaine, J.S. Rest, E.A. Shelden, M.J. Welsh, and R. Benndorf Interaction of human HSP22 (HSPB8) with other small heat shock proteins J. Biol. Chem. 279 2004 2394 2402 (Electronic publication 2003 Oct 31)
4. S.H. Baek, J.N. Min, E.M. Park, M.Y. Han, Y.S. Lee, Y.J. Lee, and Y.M. Park Role of small heat shock protein HSP25 in radioresistance and glutathione-redox cycle J. Cell. Physiol. 183 2000 100 107
5. A. Komatsuda, H. Wakui, Y. Oyama, H. Imai, A.B. Miura, H. Itoh, and Y. Tashima Overexpression of the human 72 kDa heat shock protein in renal tubular cells confers resistance against oxidative injury and cisplatin toxicity Nephrol. Dial. Transplant. 14 1999 1385 1390
6. J. Huot, F. Houle, D.R. Spitz, and J. Landry HSP27 phosphorylation- mediated resistance against actin fragmentation and cell death induced by oxidative stress Cancer Res. 56 1996 273 279
7. P. Mehlen, C. Kretz-Remy, J. Briolay, P. Fostan, M.E. Mirault, and A.P. Arrigo Intracellular reactive oxygen species as apparent modulators of heat-shock protein 27 (hsp27) structural organization and phosphorylation in basal and tumour necrosis factor alpha-treated T47D human carcinoma cells Biochem. J. 312 1995 367 375
8. A.P. Arrigo Hsp27: novel regulator of intracellular redox state IUBMB Life 52 2001 303 307
9. I. Dalle-Donne, R. Rossi, A. Milzani, P. Di Simplicio, and R. Colombo The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself Free Radical Biol. Med. 31 2001 1624 1632
10. J. Escobedo, A.M. Pucci, and T.J. Koh HSP25 protects skeletal muscle cells against oxidative stress Free Radical Biol. Med. 37 2004 1455 1462
11. R.T. Bonham, M.R. Fine, F.M. Pollock, and E.A. Shelden Hsp27, Hsp70, and metallothionein in MDCK and LLC-PK1 renal epithelial cells: effects of prolonged exposure to cadmium Toxicol. Appl. Pharmacol. 191 2003 63 73
12. S. Somji, D.A. Sens, S.H. Garrett, M.A. Sens, and J.H. Todd Heat shock protein 27 expression in human proximal tubule cells exposed to lethal and sublethal concentrations of CdCl2 Environ. Health Perspect. 107 1999 545 552
13. R.B. Leal, F.M. Cordova, L. Herd, L. Bobrovskaya, and P.R. Dunkley Lead-stimulated p38MAPK-dependent Hsp27 phosphorylation Toxicol. Appl. Pharmacol. 178 2002 44 51
14. J.M. Hollander, J.L. Martin, D.D. Belke, B.T. Scott, E. Swanson, V. Krishnamoorthy, and W.H. Dillmann Overexpression of wild-type heat shock protein 27 and a nonphosphorylatable heat shock protein 27 mutant protects against ischemia/reperfusion injury in a transgenic mouse model Circulation 29 2004 29
15. L.P. Reynolds, and G.V. Allen A review of heat shock protein induction following cerebellar injury Cerebellum 2 2003 171 177
16. R.S. Vander Heide Increased expression of HSP27 protects canine myocytes from simulated ischemia-reperfusion injury Am. J. Physiol.: Heart Circ. Physiol. 282 2002 H935 H941
17. E.A. Shelden, M.J. Borrelli, F.M. Pollock, and R. Bonham Heat shock protein 27 associates with basolateral cell boundaries in heat-shocked and ATP-depleted epithelial cells J. Am. Soc. Nephrol. 13 2002 332 341
18. D.R. Ciocca, and L.M. Vargas-Roig Hsp27 as a prognostic and predictive factor in cancer Prog. Mol. Subcell. Biol. 28 2002 205 218
19. D.R. Ciocca, S. Oesterreich, G.C. Chamness, W.L. McGuire, and S.A. Fuqua Biological and clinical implications of heat shock protein 27,000 (Hsp27): a review J. Natl. Cancer Inst. 85 1993 1558 1570
20. C. Scheler, X.P. Li, J. Salnikow, M.J. Dunn, and P.R. Jungblut Comparison of two-dimensional electrophoresis patterns of heat shock protein Hsp27 species in normal and cardiomyopathic hearts Electrophoresis 20 1999 3623 3628
21. A.A. Knowlton, S. Kapadia, G. Torre-Amione, J.B. Durand, R. Bies, J. Young, and D.L. Mann Differential expression of heat shock proteins in normal and failing human hearts J. Mol. Cell. Cardiol. 30 1998 811 818
22. R. Benndorf, and M.J. Welsh Shocking degeneration Nat. Genet. 36 2004 547 548
23. I.J. Benjamin, J. Shelton, D.J. Garry, and J.A. Richardson Temporospatial expression of the small HSP/alpha B-crystallin in cardiac and skeletal muscle during mouse development Dev. Dyn. 208 1997 75 84
24. H. Ito, K. Kamei, I. Iwamoto, Y. Inaguma, and K. Kato Regulation of the levels of small heat-shock proteins during differentiation of C2C12 cells Exp. Cell Res. 266 2001 213 221
25. S.M. Davidson, and M. Morange Hsp25 and the p38 MAPK pathway are involved in differentiation of cardiomyocytes Dev. Biol. 218 2000 146 160
26. T. Wakayama, and S. Iseki Specific expression of the mRNA for 25 kDA heat-shock protein in the spermatocytes of mouse seminiferous tubules Anat. Embryol. (Berl) 199 1999 419 425
27. O.V. Evgrafov, I. Mersiyanova, J. Irobi, L. Van Den Bosch, I. Dierick, C.L. Leung, O. Schagina, N. Verpoorten, K. Van Impe, V. Fedotov, E. Dadali, M. Auer-Grumbach, C. Windpassinger, K. Wagner, Z. Mitrovic, D. Hilton-Jones, K. Talbot, J.J. Martin, N. Vasserman, S. Tverskaya, A. Polyakov, R.K. Liem, J. Gettemans, W. Robberecht, P. De, and V. Jonghe Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy Nat. Genet. 36 2004 602 606 (Electronic publication 2004 May 02)
28. J.P. Brady, D.L. Garland, D.E. Green, E.R. Tamm, F.J. Giblin, and E.F. Wawrousek AlphaB-crystallin in lens development and muscle integrity: a gene knockout approach Invest. Ophthalmol. Visual Sci. 42 2001 2924 2934
29. U. Jakob, M. Gaestel, K. Engel, and J. Buchner Small heat shock proteins are molecular chaperones J. Biol. Chem. 268 1993 1517 1520
30. C. Paul, F. Manero, S. Gonin, C. Kretz-Remy, S. Virot, and A.P. Arrigo Hsp27 as a negative regulator of cytochrome C release Mol. Cell. Biol. 22 2002 816 834
31. J.M. Bruey, C. Ducasse, P. Bonniaud, L. Ravagnan, S.A. Susin, C. Diaz-Latoud, S. Gurbuxani, A.P. Arrigo, G. Kroemer, E. Solary, and C. Garrido Hsp27 negatively regulates cell death by interacting with cytochrome c Nat. Cell Biol. 2 2000 645 652
32. N. Mounier, and A. Arrigo Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperone 7 2002 167 176
33. J.W. Wong, B. Shi, B. Farboud, M. McClaren, T. Shibamoto, C.E. Cross, and R.R. Isseroff Ultraviolet B-mediated phosphorylation of the small heat shock protein HSP27 in human keratinocytes J. Invest. Dermatol. 115 2000 427 434
34. A. Samali, J.D. Robertson, E. Peterson, F. Manero, L. van Zeijl, C. Paul, I.A. Cotgreave, A.P. Arrigo, and S. Orrenius Hsp27 protects mitochondria of thermotolerant cells against apoptotic stimuli Cell Stress Chaperones 6 2001 49 58
35. A.S. Adhikari, K. Sridhar Rao, N. Rangaraj, V.K. Parnaik, and C. Mohan Rao Heat stress-induced localization of small heat shock proteins in mouse myoblasts: intranuclear lamin A/C speckles as target for alphaB-crystallin and Hsp25 Exp. Cell Res. 299 2004 393 403
36. A.L. Bryantsev, S.A. Loktionova, O.P. Ilyinskaya, E.M. Tararak, H.H. Kampinga, and A.E. Kabakov Distribution, phosphorylation, and activities of Hsp25 in heat-stressed H9c2 myoblasts: a functional link to cytoprotection Cell Stress Chaperones 7 2002 146 155
37. S.A. Loktionova, O.P. Ilyinskaya, V.L. Gabai, and A.E. Kabakov Distinct effects of heat shock and ATP depletion on distribution and isoform patterns of human Hsp27 in endothelial cells FEBS Lett. 392 1996 100 104
38. F.A. van de Klundert, M.L. Gijsen, I.P.R. van den, L.H. Snoeckx, and W.W. de Jong alpha B-crystallin and hsp25 in neonatal cardiac cells-differences in cellular localization under stress conditions Eur. J. Cell Biol. 75 1998 38 45
39. C.J. Neumann Vertebrate development: a view from the zebrafish Semin. Cell Dev. Biol. 13 2002 469
40. E.T. Keller, and J.M. Murtha The use of mature zebrafish (Danio rerio) as a model for human aging and disease Comp. Biochem. Physiol., C Toxicol. Pharmacol. 138 2004 335 341
41. B. Key, and C.A. Devine Zebrafish as an experimental model: strategies for developmental and molecular neurobiology studies Methods Cell Sci. 25 2003 1 6
42. C.E. Norris, M.A. Brown, E. Hickey, L.A. Weber, and L.E. Hightower Low-molecular-weight heat shock proteins in a desert fish (Poeciliopsis lucida): homologs of human Hsp27 and Xenopus Hsp30 Mol. Biol. Evol. 14 1997 1050 1061
43. M. Wieske, R. Benndorf, J. Behlke, R. Dolling, G. Grelle, H. Bielka, and G. Lutsch Defined sequence segments of the small heat shock proteins HSP25 and alphaB-crystallin inhibit actin polymerization Eur. J. Biochem. 268 2001 2083 2090
44. T. Wakayama, and S. Iseki Expression and cellular localization of the mRNA for the 25-kDa heat-shock protein in the mouse Cell Biol. Int. 22 1998 295 304
45. U. Warrior, X.G. Chiou, M.P. Sheets, R.J. Sciotti, J.M. Parry, R.L. Simmer, B.W. Surber, D.J. Burns, B.A. Beutel, K.W. Mollison, S.W. Djuric, and J.M. Trevillyan Development of a p38 kinase binding assay for high throughput screening J. Biomol. Screen 4 1999 129 135
46. C.L. Manthey, S.W. Wang, S.D. Kinney, and Z. Yao SB202190, a selective inhibitor of p38 mitogen-activated protein kinase, is a powerful regulator of LPS-induced mRNAs in monocytes J. Leukocyte Biol. 64 1998 409 417
47. S. Nemoto, J. Xiang, S. Huang, and A. Lin Induction of apoptosis by SB202190 through inhibition of p38beta mitogen-activated protein kinase J. Biol. Chem. 273 1998 16415 16420
48. M. Barancik, P. Htun, and W. Schaper Okadaic acid and anisomycin are protective and stimulate the SAPK/JNK pathway J. Cardiovasc. Pharmacol. 34 1999 182 190
49. L.F. Barros, M. Young, J. Saklatvala, and S.A. Baldwin Evidence of two mechanisms for the activation of the glucose transporter GLUT1 by anisomycin: p38(MAP kinase) activation and protein synthesis inhibition in mammalian cells J. Physiol. 504 1997 517 525
50. E. Cano, Y.N. Doza, R. Ben-Levy, P. Cohen, and L.C. Mahadevan Identification of anisomycin-activated kinases p45 and p55 in murine cells as MAPKAP kinase-2 Oncogene 12 1996 805 812
51. R.A. Lindner, J.A. Carver, M. Ehrnsperger, J. Buchner, G. Esposito, J. Behlke, G. Lutsch, A. Kotlyarov, and M. Gaestel Mouse Hsp25, a small shock protein. The role of its C-terminal extension in oligomerization and chaperone action Eur. J. Biochem. 267 2000 1923 1932
52. K. Yoshida, T. Aki, K. Harada, K.M. Shama, Y. Kamoda, A. Suzuki, and S. Ohno Translocation of HSP27 and MKBP in ischemic heart Cell Struct. Funct. 24 1999 181 185
53. K. Sakamoto, T. Urushidani, and T. Nagao Translocation of HSP27 to sarcomere induced by ischemic preconditioning in isolated rat hearts Biochem. Biophys. Res. Commun. 269 2000 137 142
54. J.P. Leger, F.M. Smith, and R.W. Currie Confocal microscopic localization of constitutive and heat shock-induced proteins HSP70 and HSP27 in the rat heart Circulation 102 2000 1703 1709
55. N. Golenhofen, M.D. Perng, R.A. Quinlan, and D. Drenckhahn Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle Histochem. Cell Biol. 122 2000 415 425 (Electronic publication 2004 Oct 12)
56. T.J. Koh, and J. Escobedo Cytoskeletal disruption and small heat shock protein translocation immediately after lengthening contractions Am. J. Physiol.: Cell Physiol. 286 2004 C713 C722 (Electronic publication 2003 Nov 19)
57. G. Lutsch, R. Vetter, U. Offhauss, M. Wieske, H.J. Grone, R. Klemenz, I. Schimke, J. Stahl, and R. Benndorf Abundance and location of the small heat shock proteins HSP25 and alphaB-crystallin in rat and human heart Circulation 96 1997 3466 3476
58. B. Hoch, G. Lutsch, W.P. Schlegel, J. Stahl, G. Wallukat, S. Bartel, E.G. Krause, R. Benndorf, and P. Karczewski HSP25 in isolated perfused rat hearts: localization and response to hyperthermia Mol. Cell. Biochem. 160-161 1996 231 239
59. W. Pipkin, J.A. Johnson, T.L. Creazzo, J. Burch, P. Komalavilas, and C. Brophy Localization, macromolecular associations, and function of the small heat shock-related protein HSP20 in rat heart Circulation 107 2003 469 476
60. K.A. Jones, and R.C. Findly Induction of heat shock proteins by canavanine in Tetrahymena. No change in ATP levels measured in vivo by NMR J. Biol. Chem. 261 1986 8703 8707
61. R.C. Findly, R.J. Gillies, and R.G. Shulman In vivo phosphorus-31 nuclear magnetic resonance reveals lowered ATP during heat shock of Tetrahymena Science 219 1983 1223 1225
62. S.K. Van Why, A.S. Mann, T. Ardito, G. Thulin, S. Ferris, M.A. Macleod, M. Kashgarian, and N.J. Siegel Hsp27 associates with actin and limits injury in energy depleted renal epithelia J. Am. Soc. Nephrol. 14 2003 98 106
63. M.J. Borrelli, L.J. Bernock, J. Landry, D.R. Spitz, L.A. Weber, E. Hickey, M.L. Freeman, and P.M. Corry Stress protection by a fluorescent Hsp27 chimera that is independent of nuclear translocation or multimeric dissociation Cell Stress Chaperones 7 2002 281 296
64. D. Walsh, J. Grantham, X.O. Zhu, J. Wei Lin, M. van Oosterum, R. Taylor, and M. Edwards The role of heat shock proteins in mammalian differentiation and development Environ. Med. 43 1999 79 87
65. R. Srikakulam, and D.A. Winkelmann Chaperone-mediated folding and assembly of myosin in striated muscle J. Cell Sci. 117 2004 641 652 (Electronic publication 2004 Jan 6)
66. M. Gernold, U. Knauf, M. Gaestel, J. Stahl, and P.M. Kloetzel Development and tissue-specific distribution of mouse small heat shock protein hsp25 Dev. Genet. 14 1993 103 111
67. J.J. Heikkila Regulation and function of small heat shock protein genes during amphibian development J. Cell. Biochem. 93 2004 672 680
68. C.B. Kimmel, W.W. Ballard, S.R. Kimmel, B. Ullmann, and T.F. Schilling Stages of embryonic development of the zebrafish Dev. Dyn. 203 1995 253 310