Activation of ER stress and apoptosis by hydrogen peroxide in HeLa cells: Protective role of mild heat preconditioning at 40°C

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 12, 2011, Pages 1987-1999

  Pallepati, Pragathi ^a   Averill Bates, Diana A ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Apoptosis; Calpain; Caspase; Endoplasmic reticulum; H2O2; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CALPAIN; CASPASE 12; CASPASE 4; CASPASE 7; CASPASE 9; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HYDROGEN PEROXIDE; INITIATION FACTOR 2ALPHA; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL KILLING; CELL PROTECTION; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; HEAT TOLERANCE; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; ROOM TEMPERATURE; UNFOLDED PROTEIN RESPONSE;

APOPTOSIS; CELL SURVIVAL; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HELA CELLS; HOT TEMPERATURE; HUMANS; HYDROGEN PEROXIDE; IMMUNOENZYME TECHNIQUES; OXIDANTS; PHOSPHORYLATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 80053371703     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.07.021     Document Type: Article

References (62)

1. Circu M.L., Aw T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48:749-762.
2. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12:913-922.
3. Fulda S., Gorman A.M., Hori O., Samali A. Cellular stress responses: cell survival and cell death. Int. J. Cell. Biol. 2010, 214074.
4. Faitova J., Krekac D., Hrstka R., Vojtesek B. Endoplasmic reticulum stress and apoptosis. Cell. Mol. Biol. Lett. 2006, 11:488-505.
5. Schröder M., Kaufman R.J. ER stress and the unfolded protein response. Mutat. Res. 2005, 569:29-63.
6. Breckenridge D.G., Germain M., Mathai J.P., Nguyen M., Shore G.C. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003, 22:8608-8618.
7. Malhotra J.D., Kaufman R.J. The endoplasmic reticulum and unfold protein response. Semin. Cell Dev. Biol. 2007, 18:716-731.
8. Rasheva V.I., Domingos P.M. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 2009, 14:996-1007.
9. Portt L., Norman G., Clapp C., Greenwood M., Greenwood M.T. Anti-apoptosis and cell survival: a review. Biochim. Biophys. Acta 2010, 1813:238-259.
10. Przybytkowski E., Bates J.H., Bates D.A., Mackillop W.J. Thermal adaptation in CHO cells at 40degrees C: the influence of growth conditions and the role of heat shock proteins. Radiat. Res. 1986, 107:317-331.
11. Wiese A.G., Pacifici R.E., Davies K.J. Transient adaptation of oxidative stress in mammalian cells. Arch. Biochem. Biophys. 1995, 318:231-240.
12. Kregel K.C. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 2002, 92:2177-2186.
13. Bettaieb A., Averill-Bates D.A. Thermotolerance induced at a mild temperature of 40 degrees C protects cells against heat shock-induced apoptosis. J. Cell. Physiol. 2005, 205:47-57.
14. Holsapple M.P., Wallace K.B. Dose response considerations in risk assessment-an overview of recent ILSI activities. Toxicol. Lett. 2008, 180:85-92.
15. Landry J., Bernier D., Chrétien P., Nicole L.M., Tanguay R.M., Marceau N. Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res. 1982, 42:2457-2461.
16. Martindale J.L., Holbrook N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 2002, 192:1-15.
17. Richter K., Haslbeck M., Buchner J. The heat shock response: life on the verge of death. Mol. Cell 2010, 40:253-266.
18. Landry J., Chrétien P., Lambert H., Hickey E., Weber L.A. Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J. Cell Biol. 1989, 109:7-15.
19. Pallepati P., Averill-Bates D.A. Mild thermotolerance induced at 40degrees C increases antioxidants and protects HeLa cells against mitochondrial apoptosis induced by hydrogen peroxide: role of p53. Arch. Biochem. Biophys. 2010, 495:97-111.
20. Bettaieb A., Averill-Bates D.A. Thermotolerance induced at a fever temperature of 40 degrees C protects cells against hyperthermia-induced apoptosis mediated by death receptor signalling. Biochem. Cell Biol. 2008, 86:521-538.
21. Lord-Fontaine S., Averill D.A. Enhancement of cytotoxicity of hydrogen peroxide by hyperthermia in Chinese hamster ovary cells: role of antioxidant defenses. Arch. Biochem. Biophys. 1999, 363:283-295.
22. Tanel A., Averill-Bates D.A. The aldehyde acrolein induces apoptosis via activation of the mitochondrial pathway. Biochim. Biophys. Acta 2005, 1743:255-267.
23. Samali A., Cai J., Zhivotovsky B., Jones D.P., Orrenius S. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of Jurkat cells. EMBO J. 1999, 18:2040-2048.
24. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
25. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
26. Harding H.P., Zhang Y., Bertolotti A., Zeng H., Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 2000, 5:897-904.
27. Nakagawa T., Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 2000, 150:887-894.
28. Tan Y., Dourdin N., Wu C., De Veyra T., Elce J.S., Greer P.A. Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J. Biol. Chem. 2006, 281:16016-16024.
29. Boyce M., Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 2006, 13:363-373.
30. Fan T.J., Han L.H., Cong R.S., Liang J. Caspase family proteases and apoptosis. Acta Biochim. Biophys. Sin. 2005, 37:719-727.
31. Morishima N., Nakanishi K., Takenouchi H., Shibata T., Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 2002, 277:34287-34294.
32. Davies K.J. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 2000, 50:279-289.
33. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7:880-885.
34. Cullinan S.B., Zhang D., Hannink M., Arvisais E., Kaufman R.J., Diehl J.A. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol. Cell. Biol. 2003, 23:7198-7209.
35. Venugopal R., Jaiswal A.K. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 1998, 17:3145-3156.
36. Wild A.C., Moinova H.R., Mulcahy R.T. Regulation of gamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 1999, 274:33627-33636.
37. He C.H., Gong P., Hu B., Stewart D., Choi M.E., Choi A.M., Alam J. Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J. Biol. Chem. 2001, 276:20858-20865.
38. Nguyen T., Sherratt P.J., Nioi P., Yang C.S., Pickett C.B. Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J. Biol. Chem. 2005, 280:32485-32492.
39. Min S.K., Lee S.K., Park J.S., Lee J., Paeng J.Y., Lee S.I., Lee H.J., Kim Y., Pae H.O., Lee S.K., Kim E.C. Endoplasmic reticulum stress is involved in hydrogen peroxide induced apoptosis in immortalized and malignant human oral keratinocytes. J. Oral Pathol. Med. 2008, 37:490-498.
40. Wei H., Li Z., Hu S., Chen X., Cong X. Apoptosis of mesenchymal stem cells induced by hydrogen peroxide concerns both endoplasmic reticulum stress and mitochondrial death pathway through regulation of caspases, p38 and JNK. J. Cell. Biochem. 2010, 111:967-978.
41. Haidara K., Marion M., Gascon-Barré M., Denizeau F., Averill-Bates D.A. Implication of caspases and subcellular compartments in tert-butylhydroperoxide induced apoptosis. Toxicol. Appl. Pharmcol. 2008, 229:65-76.
42. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
43. Fischer H., Koenig U., Eckhart L., Tschachler E. Human caspase 12 has acquired deleterious mutations. Biochem. Biophys. Res. Commun. 2002, 293:722-726.
44. Luthra S., Fardin B., Dong J., Hertzog D., Kamjoo S., Gebremariam S., Butani V., Narayanan R., Mungcal J.K., Kuppermann B.D., Kenney M.C. Activation of caspase-8 and caspase-12 pathways by 7-ketocholesterol in human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 2006, 47:5569-5575.
45. Bitko V., Barik S. An endoplasmic reticulum-specific stress-activated caspase (caspase-12) is implicated in the apoptosis of A549 epithelial cells by respiratory syncytial virus. J. Cell. Biochem. 2001, 80:441-454.
46. Kerbiriou M., Teng L., Benz N., Trouvé P., Férec C. The calpain, caspase 12, caspase 3 cascade leading to apoptosis is altered in F508del-CFTR expressing cells. PLoS One 2009, 4:e8436.
47. Yoneda T., Imaizumi K., Oono K., Yui D., Gomi F., Katayama T., Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 2001, 276:13935-13940.
48. Won S.J., Ki Y.S., Chung K.S., Choi J.H., Bae K.H., Lee K.T. 3alpha,23-isopropylidenedioxyolean-12-en-27-oic acid, a triterpene isolated from Aceriphyllum rossii, induces apoptosis in human cervical cancer HeLa cells through mitochondrial dysfunction and endoplasmic reticulum stress. Biol. Pharm. Bull. 2010, 33:1620-1626.
49. 2+ oscillation. J. Biochem. Mol. Biol. 2005, 38:709-716.
50. Rao R.V., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ. 2004, 11:372-380.
51. Hitomi J., Katayama T., Eguchi Y., Kudo T., Taniguchi M., Koyama Y., Manabe T., Yamagishi S., Bando Y., Imaizumi K., Tsujimoto Y., Tohyama M. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J. Cell Biol. 2004, 165:347-356.
52. Kim S.J., Zhang Z., Hitomi E., Lee Y.C., Mukherjee A.B. Endoplasmic reticulum stress-induced caspase-4 activation mediates apoptosis and neurodegeneration in INCL. Hum. Mol. Genet. 2006, 15:1826-1834.
53. 2+ homeostasis under the ER stress. NeuroChem. Int. 2010, 56:352-356.
54. Agard N.J., Maltby D., Wells J.A. Inflammatory stimuli regulate caspase substrate profiles. Mol. Cell. Proteomics 2010, 9:880-893.
55. Yukioka F., Matsuzaki S., Kawamoto K., Koyama Y., Hitomi J., Katayama T., Tohyama M. Presenilin-1 mutation activates the signaling pathway of caspase-4 in endoplasmic reticulum stress-induced apoptosis. Neurochem. Int. 2008, 52:683-687.
56. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 2001, 21:1249-1259.
57. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., Hughes P.D., Michalak E.M., McKimm-Breschkin J., Motoyama N., Gotoh T., Akira S., Bouillet P., Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349.
58. Beere H.M. "The stress of dying": the role of heat shock proteins in the regulation of apoptosis. J. Cell Sci. 2004, 117:2641-2651.
59. Gupta S., Deepti A., Deegan S., Lisbona F., Hetz C., Samali A. HSP72 protects cells from ER stress-induced apoptosis via enhancement of IRE1alpha-XBP1 signaling through a physical interaction. PLoS Biol. 2010, 8:e1000410.
60. Arrigo A.P., Virot S., Chaufour S., Firdaus W., Kretz-Remy C., Diaz-Latoud C. Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid. Redox Signal. 2005, 7:414-422.
61. Wyttenbach A., Sauvageot O., Carmichael J., Diaz-Latoud C., Arrigo A.P., Rubinsztein D.C. Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum. Mol. Genet. 2002, 11:1137-1151.
62. Préville X., Salvemini F., Giraud S., Chaufour S., Paul C., Stepien G., Ursini M.V., Arrigo A.P. Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp. Cell Res. 1999, 247:61-78.