Sodium arsenite and cadmium chloride induction of proteasomal inhibition and HSP accumulation in Xenopus laevis A6 kidney epithelial cells

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 155, Issue 2, 2012, Pages 307-317

  Brunt, Jara J ^a   Khan, Saad ^a   Heikkila, John J ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Amphibian; Frog; Heat shock proteins; Molecular chaperone; Proteasomal inhibition; Ubiquitin

Indexed keywords

ACTIN; ARSENITE SODIUM; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CADMIUM CHLORIDE; CELASTROL; CHYMOTRYPSIN; HEAT SHOCK PROTEIN 30; HEAT SHOCK PROTEIN 70; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITINATED PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; KIDNEY TUBULE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; UBIQUITINATION; XENOPUS LAEVIS;

AMPHIBIA; ANURA; VERTEBRATA; XENOPUS LAEVIS;

EID: 84655170290     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2011.09.011     Document Type: Article

References (72)

1. R. Abdulle, A. Mohindra, P. Fernando, and J.J. Heikkila Xenopus small heat shock proteins, HSP30C and HSP30D, maintain heat- and chemically denatured luciferase in a folding-competent state Cell Stress Chaperones 7 2002 6 16 (Pubitemid 36138899)
2. N. Awasthi, and B.J. Wagner Upregulation of heat shock protein expression by proteasome inhibition: an antiapoptotic mechanism in the lens Invest. Opthalmolog. Vis. Sci. 46 2005 2082 2091
3. S.R. Blechinger, R.C. Kusch, K. Haugo, C. Matz, D.P. Chivers, and P.H. Krone Brief embryonic cadmium exposure induces a stress response and cell death in the developing olfactory system followed by long-term olfactory deficits in juvenile zebrafish Toxicol. Appl. Pharmacol. 224 2007 72 80 (Pubitemid 47404621)
4. A.M. Bode, and Z. Dong The paradox of arsenic: molecular mechanisms of cell transformation and chemotherapeutic effects Crit. Rev. Oncol. Hematol. 42 2002 5 24 (Pubitemid 34229146)
5. B.A. Buckley, M.-E. Owen, and G.E. Hofmann Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history J. Exp. Biol. 204 2001 3571 3579 (Pubitemid 34861335)
6. K.T. Bush, A.L. Goldberg, and S.K. Nigam Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance J. Biol. Chem. 272 1997 9086 9092 (Pubitemid 27154911)
7. S. Chora, B. McDonagh, D. Sheehan, M. Starita-Geribaldi, M. Romeo, and M.J. Bebianno Ubiquitination and carbonylation as markers of oxidative-stress in Ruditapes decussatus Mar. Environ. Res. 66 2008 95 97
8. A.M. Chow, and I.R. Brown Induction of heat shock proteins in differentiated human and rodent neurons by celastrol Cell Stress Chaperones 12 2007 237 244 (Pubitemid 351199386)
9. S. Darasch, D.D. Mosser, N.C. Bols, and J.J. Heikkila Heat shock gene expression in Xenopus laevis A6 cells in response to heat shock and sodium arsenite treatments Biochem. Cell Biol. 66 1988 862 868
10. L.M. Del Razo, B. Quintanilla-Vega, E. Brambila-Colombres, E.S. Calderon-Aranda, M. Manno, and A. Albores Stress proteins induced by arsenic Toxicol. Appl. Pharmacol. 177 2001 132 148 (Pubitemid 34033047)
11. C.A. Downs, G. Shigenaka, J.E. Fauth, C.E. Robinson, and A. Huang Cellular physiological assessment of bivalves after chronic exposure to spilled Exxon Valdez crude oil using a novel molecular diagnostic biotechnology Environ. Sci. Technol. 36 2002 2987 2993 (Pubitemid 34747298)
12. C. Esser, S. Alberti, and J. Hohfeld Cooperation of molecular chaperones with the ubiquitin/proteasome system Biochim. Biophys. Acta 1695 2004 171 188 (Pubitemid 39574972)
13. U. Feige, R.I. Morimoto, I. Yahara, and B.S. Polla Stress-inducible cellular responses 1996 Birkhauser Verlag., Basel Switzerland
14. P. Fernando, and J.J. Heikkila Functional characterization of Xenopus small heat shock protein, Hsp30C: the carboxyl end is required for stability and chaperone activity Cell Stress Chaperones 5 2000 148 159
15. 2-induced neuronal oxidative stress Mol. Biol. Rep. 26 1999 65 69 (Pubitemid 29223253)
16. M. Galazyn-Sidorczuk, M.M. Brzoska, M. Jurczuk, and J. Moniuszko-Jakoniuk Oxidative damage to proteins and DNA in rats exposed to cadmium and/or ethanol Chem. Biol. Interact. 180 2009 31 38
17. J. Gauley, and J.J. Heikkila Examination of the expression of the heat shock protein, hsp110, in Xenopus laevis cultured cells and embryos Comp. Biochem. Physiol. A Mol. Integr. Physiol. 145 2006 225 234 (Pubitemid 44380392)
18. J. Gauley, J.T.F. Young, and J.J. Heikkila Intracellular localization of the heat shock protein, HSP110, in Xenopus laevis A6 kidney epithelial cells Comp. Biochem. Physiol. A Mol. Integr. Physiol. 151 2008 133 138
19. M. Gellalchew, and J.J. Heikkila Intracellular localization of Xenopus small heat shock protein, hsp30, in A6 kidney epithelial cells Cell Biol. Int. 29 2005 221 227 (Pubitemid 40726409)
20. S. Gordon, S. Bharadwaj, A. Hnatov, A. Ali, and N. Ovsenek Distinct stress-inducible and developmentally regulated heat shock transcription factors in Xenopus oocytes Dev. Biol. 181 1997 47 63 (Pubitemid 27079634)
21. J.J. Heikkila Heat shock protein gene expression and function in amphibian model systems Comp. Biochem. Physiol. A Mol. Integr. Physiol. 156 2010 19 33
22. G.E. Hofmann, and G.N. Somero Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus J. Exp. Biol. 198 1995 1509 1518
23. S.M. Kelly, J.K. VanSlyke, and L.S. Musil Regulation of ubiquitin-proteasome system-mediated degradation by cytosolic stress Mol. Biol. Cell 18 2007 4279 4291 (Pubitemid 350060158)
24. S. Khan, and J.J. Heikkila Curcumin-induced inhibition of proteasomal activity, enhanced HSP accumulation and the acquisition of thermotolerance in Xenopus laevis A6 cells Comp. Biochem. Physiol. A Mol. Integr. Physiol. 158 2011 566 576
25. D.S. Kirkpatrick, K.V. Dale, J.M. Catania, and A.J. Gandolfi Low-level arsenite causes accumulation of ubiquitinated proteins in rabbit renal cortical slices and HEK293 cells Toxicol. Appl. Pharmacol. 186 2003 101 109 (Pubitemid 36298619)
26. P.H. Krone, A. Snow, A. Ali, J.J. Pasternak, and J.J. Heikkila Comparison of regulatory and structural regions of the Xenopus laevis small heat-shock protein-encoding gene family Gene 110 1992 159 166
27. L. Lang, D. Miskovic, P. Fernando, and J.J. Heikkila Spatial pattern of constitutive and heat shock-induced expression of the small heat shock protein gene family, hsp30, in Xenopus laevis tailbud embryos Dev. Genet. 25 1999 365 374
28. P. Le Goff, Y. Le Drean, C. Le Person, C. Le Jossic-Corcos, A. Ainouche, and D. Michel Intracellular trafficking of heat shock factor 2 Exp. Cell Res. 294 2004 480 493 (Pubitemid 38326746)
29. D.H. Lee, and A.L. Goldberg Proteasome inhibitors: valuable new tools for cell biologists Trends Cell Biol. 8 1998 397 403 (Pubitemid 28458705)
30. N.L. Lehman The ubiquitin proteasome system in neuropathology Acta Neuropathol. 118 2009 329 347
31. L. Li, H. Yang, D. Chen, C. Cui, and Q.P. Dou Disulfiram promotes the conversion of carcinogenic cadmium to a proteasome inhibitor with pro-apoptotic activity in human cancer cells Toxicol. Appl. Pharmacol. 229 2008 206 214
32. W. Liao, X. Li, M. Mancini, and L. Chan Proteasome inhibition induces differential heat shock protein response but not unfolded protein response in HepG2 cells J. Cell. Biochem. 99 2006 1085 1095 (Pubitemid 44673966)
33. J. Liu, M.B. Kadiiska, Y. Liu, T. Lu, W. Qu, and M.P. Waalkes Stress-related gene expression in mice treated with inorganic arsenicals Toxicol. Sci. 61 2001 314 320 (Pubitemid 32499399)
34. J. Lundgren, P. Masson, Z. Mirzaei, and P. Young Identification and characterization of a Drosophila proteasome regulatory network Mol. Cell. Biol. 25 2005 4662 4675 (Pubitemid 40705769)
35. B. Malik, L. Schlanger, O. Al-Khalili, H.F. Bao, G. Yue, S.R. Price, W.E. Mitch, and D.C. Eaton Enac degradation in A6 cells by the ubiquitin-proteosome proteolytic pathway J. Biol. Chem. 276 2001 12903 12910
36. L.A. Manwell, and J.J. Heikkila Examination of KNK437- and quercetin-mediated inhibition of heat shock-induced heat shock protein gene expression in Xenopus laevis cultured cells Comp. Biochem. Physiol. A Mol. Integr. Physiol. 148 2007 521 530 (Pubitemid 47484224)
37. B. McDonagh Detection of ubiquitination in 2DE Methods Mol. Biol. 519 2009 377 381
38. B. McDonagh, and D. Sheehan redox proteomics in the blue mussel Mytilus edulis: carbonylation is not a pre-requisite for ubiquitination in acute free radical-mediated oxidative stress Aquat. Toxicol. 79 2006 325 333 (Pubitemid 44374763)
39. G.C. Meacham, C. Patterson, W. Zhang, J.M. Younger, and D.M. Cyr The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation Nat. Cell Biol. 3 2001 100 105 (Pubitemid 32114840)
40. III, modify CYP3A4, PXR and RXR alpha expression in the small intestine of CYP3A4 transgenic mice Toxicol. Appl. Pharmacol. 239 2009 162 168
41. M. Mendez-Armenta, and C. Rios Cadmium neurotoxicity Environ. Toxicol. Pharmacol. 23 2007 350 358
42. E.G. Mimnaugh, H.Y. Chen, J.R. Davie, J.E. Celis, and L. Neckers Rapid deubiquitination of nucleosomal histones in hyman tumour cells caused by proteasome inhibitors and stress response inducers: effects on replication, transcription, translation, and the cellular stress response Biochemistry 36 1997 14418 14429 (Pubitemid 27509934)
43. R.I. Morimoto Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators Genes Dev. 12 1998 3788 3796 (Pubitemid 29024840)
44. R.I. Morimoto Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging Genes Dev. 22 2008 1427 1438 (Pubitemid 351793077)
45. F. Mouchet, L. Gauthier, M. Baudrimont, P. Gonzalez, C. Mailhes, V. Ferrier, and A. Devaux Comparative evaluation of the toxicity and genotoxicity of cadmium in amphibian larvae (Xenopus laevis and Pleurodeles waltl) using the comet assay and the micronucleus test Environ. Toxicol. 22 2007 422 435 (Pubitemid 47121923)
46. S. Murata, Y. Minami, M. Minami, T. Chiba, and K. Tanaka CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein EMBO Rep. 2 2001 1133 1138 (Pubitemid 34055961)
47. E.J. Noonan, R.F. Place, C. Giardina, and L.E. Hightower Hsp70B' regulation and function Cell Stress Chaperones 12 2007 242 253
48. K. Ohnishi, A. Takahashi, S. Yokota, and T. Ohnishi Effects of a heat shock protein inhibitor KNK437 on heat sensitivity and heat tolerance in human squamous cell carcinoma cell lines differing in p53 status Int. J. Radiat. Biol. 80 2004 607 614 (Pubitemid 39287046)
49. S. Othumpangat, M. Kashon, and P. Joseph Eukaryotic translation initiation factor 4E is a cellular target for toxicity and death due to exposure to cadmium chloride J. Biol. Chem. 280 2005 25162 25169 (Pubitemid 40934608)
50. A. Parcellier, E. Schmitt, S. Gurbuxani, D. Seigneurin-Berny, A. Pance, A. Chantome, S. Plenchette, S. Khochbin, E. Solary, and C. Garrido HSP27 is a ubiquitin-binding protein involved in I-kBa proteasomal degradation Mol. Cell. Biol. 23 2003 5790 5802 (Pubitemid 36951341)
51. H.M. Peng, Y. Morishima, G.J. Jenkins, A.Y. Dunbar, M. Lau, C. Patterson, W.B. Pratt, and Y. Osawa Ubiquitination of neuronal nitric-oxide synthase by CHIP, a chaperone-dependent E3 ligase J. Biol. Chem. 279 2004 52970 52977 (Pubitemid 40051795)
52. W.B. Pratt, Y. Morishima, H.M. Peng, and Y. Osawa Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergoes oxidative and toxic damage Exp. Biol. Med. (Maywood) 235 2010 278 289
53. T.A. Pritts, E.S. Hungness, D.D. Hershko, B.W. Robb, X. Sun, G.J. Luo, J.E. Fischer, H.R. Wong, and P.O. Hasselgren Proteasome inhibitors induce heat shock response and increase IL-6 expression in human intestinal epithelial cells Am. J. Physiol. Regul. Integr. Comp. Physiol. 282 2002 1016 1026
54. M.A. Rea, J.P. Gregg, Q. Quin, M.A. Phillips, and R.H. Rice Global alteration of gene expression human keratinocytes by inorganic arsenic Carcinogenesis 24 2003 747 756 (Pubitemid 36592410)
55. C.A. Ross, and C.M. Pickart The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases Trends Cell Biol. 14 2004 703 711 (Pubitemid 39572556)
56. F.A. Salomons, K. Acs, and N.P. Dantuma Illuminating the ubiquitin/proteasome system Exp. Cell Res. 316 2010 1289 1295
57. S. Samuel, R. Kathirvel, T. Jayavelu, and P. Chinnakkannu Protein oxidative damage in arsenic induced rat brain: influence of DL-lipoic acid Toxicol. Lett. 155 2005 27 34 (Pubitemid 39600733)
58. X. Song, Z. Chen, C. Wu, and S. Zhao Abrogating HSP response augments cell death induced by As2O3 in glioma cell lines Can. J. Neurol. Sci. 37 2010 504 511
59. K. Stangl, C. Gunther, T. Frank, M. Lorenz, S. Meiners, T. Ropke, L. Stelter, M. Moobed, G. Baumann, P.M. Kloetzel, and V. Stangl Inhibition of the ubiquitin-proteasome pathway induces differential heat-shock protein response in cardiomyocytes and renders early cardiac protection Biochem. Biophys. Res. Commun. 291 2002 542 549 (Pubitemid 34687378)
60. P.-F. Su, Y.-J. Hu, I.-C. Ho, Y.-M. Cheng, and T.C. Lee Distinct gene expression profiles in immortalized human urothelial cells exposed to inorganic arsenite and its methylated trivalent metabolites Environ. Health Perspect. 114 2006 394 403 (Pubitemid 43338265)
61. +-ATPase through proteasomal and endo-/lysosomal proteolytic pathways FASEB J. 13 1999 1751 1761 (Pubitemid 29473337)
62. T.-C. Tsou, F.-Y. Tsai, Y.-W. Hsieh, L.-A. Li, S.C. Yeh, and L.W. Chang Arsenite induces endothelial cytotoxicity by down-regulation of vascular endothelial nitric oxide synthase Toxicol. Appl. Pharmacol. 208 2005 277 284 (Pubitemid 41457229)
63. R. Voellmy On mechanisms that control heat shock transcription factor activity in metazoan cells Cell Stress Chaperones 9 2004 122 133 (Pubitemid 39013809)
64. J. Voyer, and J.J. Heikkila Comparison of the effect of heat shock factor inhibitor, KNK437, on heat shock- and chemical stress-induced hsp30 gene expression in Xenopus laevis A6 cells Comp. Biochem. Physiol. A Mol. Integr. Physiol. 151 2008 253 261
65. M. Waisberg, J. Pius, B. Hale, and D. Beyersmann Molecular and cellular mechanisms of cadmium carcinogenesis Toxicology 192 2003 95 117 (Pubitemid 37311405)
66. S.E. Walcott, and J.J. Heikkila Celastrol can inhibit proteasome activity and upregulate the expression of heat shock protein genes, hsp30 and hsp70, in Xenopus laevis A6 cells Comp. Biochem. Physiol. A Mol. Integr. Physiol. 156 2010 285 293
67. J.P. Woolfson, and J.J. Heikkila Examination of cadmium-induced expression of the small heat shock protein gene, hsp30, in Xenopus laevis A6 kidney epithelial cells Comp. Biochem. Physiol. A Mol. Integr. Physiol. 152 2009 91 99
68. J.T. Young, and J.J. Heikkila Proteasome inhibition induces hsp30 and hsp70 gene expression as well as the acquisition of thermotolerance in Xenopus laevis A6 cells Cell Stress Chaperones 15 2010 323 334
69. J.T. Young, J. Gauley, and J.J. Heikkila Simultaneous exposure of Xenopus A6 kidney epithelial cells to concurrent mild sodium arsenite and heat stress results in enhanced hsp30 and hsp70 gene expression and the acquisition of thermotolerance Comp. Biochem. Physiol. A Mol. Integr. Physiol. 153 2009 417 424
70. X. Yu, S. Hong, and E.M. Faustman Cadmium-induced activation of stress signaling pathways, disruption of ubiquitin-dependent protein degradation and apoptosis in primary rat sertoli cell-gonocyte cocultures Toxicol. Sci. 104 2008 385 396 (Pubitemid 352038260)
71. X. Yu, J.F. Robinson, J.S. Sidhu, S. Hong, and E.M. Faustman A system-based comparison of gene expression reveals alterations in oxidative stress, disruption of ubiquitin-proteasome system and altered cell cycle regulation after exposure to cadmium and methylmercury in mouse embryonic fibroblast Toxicol. Sci. 114 2010 356 377
72. X. Yu, J.S. Sidhu, S. Hong, J.F. Robinson, R.A. Ponce, and E.M. Faustman Cadmium induced p53-dependent activation of stress signaling, accumulation of ubiquitinated proteins, and apoptosis in mouse embryonic fibroblast cells Toxicol. Sci. 120 2011 403 412