Potential role of vitexin in alleviating heat stress-induced cytotoxicity: Regulatory effect of Hsp90 on ER stress-mediated autophagy

Life Sciences

Volumn 142, Issue , 2015, Pages 36-48

  Bhardwaj, Monika ^a   Paul, Souren ^a   Jakhar, Rekha ^a   Kang, Sun Chul ^a  

^a Daegu University   (South Korea)

Author keywords

Antioxidant activity; Autophagy; ER stress; Heat stress; Hsp90; Vitexin

Indexed keywords

ACRIDINE ORANGE; ANTIOXIDANT; CHAPERONE; CYCLOHEXIMIDE; DACTINOMYCIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK TRANSCRIPTION FACTOR 1; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; RADICICOL; VITEXIN; APIGENIN; CYTOTOXIN; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR;

A549 CELL LINE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BINDING AFFINITY; CELL PROTECTION; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; CYTOTOXICITY ASSAY; DRUG EFFICACY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; FLUORESCENCE IMAGING; GEL MOBILITY SHIFT ASSAY; HEAT STRESS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LACTATE DEHYDROGENASE ASSAY; MONOTHERAPY; MTT ASSAY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAINING; UPREGULATION; DRUG EFFECTS; HEAT SHOCK RESPONSE; METABOLISM; TUMOR CELL LINE;

APIGENIN; AUTOPHAGY; CELL LINE, TUMOR; CYTOTOXINS; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEAT-SHOCK RESPONSE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; TRANSCRIPTION FACTORS;

EID: 84944790085     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2015.10.012     Document Type: Article

References (68)

1. P.A. Baeuerle Inducible gene expression. Vol. I. Environmental stresses and nutrients Vol. II. Hormonal Signals 1995 Birkhauser Boston Cambridge, MA
2. C.H. Park, M.J. Lee, J. Ahn, S. Kim, H.H. Kim, K.H. Kim, H.C. Eun, and J.H. Chung Heat shock-induced matrix metalloproteinase MMP-1 and MMP-3 are mediated through ERK and JNK activation and via an autocrine interleukin-6 loop J. Investig. Dermatol. 123 2004 1012 1019
3. S. Matsuki, Y. Iuchi, Y. Ikeda, I. Sasagawa, Y. Tomita, and J. Fujii Suppression of cytochrome c release and apoptosis in testes with heat stress by minocycline Biochem. Biophys. Res. Commun. 312 2003 843 849
4. D. Nowak, A. Antczak, T. Pietras, P. Bialasiewicz, and M. Krol Protective effect of ambroxol against heat- and hydrogen peroxide-induced damage to lung lipids in mice Eur. Respir. J. 7 1994 1629 1634
5. J.F. Davidson, and R.H. Schiest Cytotoxic and genotoxic consequences of heat stress are dependent on the presence of oxygen in Saccharomyces cerevisiae J. Bacteriol. 183 2001 4580 4587
6. D.M. Toivola, P. Strnad, A. Habtezion, and M.B. Omary Intermediate filaments take the heat as stress proteins Trends Cell Biol. 20 2010 79 91
7. W.J. Welch, and J.P. Suhan Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment J. Cell Biol. 101 1985 1198 1211
8. S. Boulon, B.J. Westman, S. Hutten, F.M. Boisvert, and A.I. Lamond The nucleolus under stress Mol. Cell 40 2010 216 227
9. I.S. Kim, H.Y. Moon, H.S. Yun, and I. Jin Heat shock causes oxidative stress and induces a variety of cell rescue proteins in Saccharomyces cerevisiae KNU5377 J. Microbiol. 44 2006 492 501
10. K.C. Kregel Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance J. Appl. Physiol. 92 1985, 2002 2177 2186
11. X. Xu, S. Gupta, W. Hu, B.C. McGrath, and D.R. Cavener Hyperthermia induces the ER stress pathway PLoS One 6 2011 e23740 10.1371/journal.pone.0023740
12. S. Fulda, A.M. Gorman, O. Hori, and A. Samali Cellular stress responses: cell survival and cell death Int. J. Cell Biol. 2010 2010 1 22
13. O. Hori, M. Miyazaki, T. Tamatani, K. Ozawa, K. Takano, M. Okabe, M. Ikawa, E. Hartmann, P. Mai, D.M. Stern, Y. Kitao, and S. Ogawa Deletion of SERP1/RAMP4, a component of the endoplasmic reticulum (ER) translocation sites, leads to ER stress Mol. Cell. Biol. 26 2006 4257 4267
14. D.C. Rubinsztein, P. Codogno, and B. Levine Autophagy modulation as a potential therapeutic target for diverse diseases Nat. Rev. Drug Discov. 11 2012 709 730
15. E.H. Baehrecke Autophagy: dual roles in life and death? Nat. Rev. Mol. Cell Biol. 6 2005 505 510
16. Y. Cheng, and J.M. Yang Survival and death of endoplasmic-reticulum-stressed cells: role of autophagy World J. Biol. Chem. 2 2011 226 231
17. S.J. Lee, J.H. Lee, H.H. Lee, S. Lee, S. Kim, T. Chun, and J.Y. Imm Effect of mung bean ethanol extract on pro-inflammatory cytokines in LPS stimulated macrophages Food Sci. Biotechnol. 20 2011 519 524
18. E. Farsi, A. Shafaei, S.Y. Hor, M.B.K. Ahamed, M.F. Yam, I.H. Attitala, M.Z. Asmawi, and Z. Ismail Correlation between enzymes inhibitory effects and antioxidant activities of standardized fractions of methanolic extract obtained from Ficus deltoidea leaves Afr. J. Biotechnol. 10 2011 15184 15194
19. J. Kim, I. Lee, J. Seo, M. Jung, Y. Kim, and N. Yim Vitexin, orientin and other flavonoids from Spirodela polyrhiza inhibit adipogenesis in 3T3-L1 cells Phytother. Res. 10 2010 1543 1548
20. E. Gaitan, R.C. Cooksey, J. Legan, and R.H. Lindsay Antithyroid effects in vivo and in vitro of vitexin: a C-glucosylflavone in millet J. Clin. Endocrinol. Metab. 80 1995 1144 1147
21. Z. Tan, Y. Zhang, J. Deng, G. Zeng, and Y. Zhang Purified vitexin compound 1 suppresses tumor growth and induces cell apoptosis in a mouse model of human choriocarcinoma Int. J. Gynecol. Cancer 22 2012 360 366
22. D. Cao, H. Li, J. Yi, J. Zhang, H. Che, J. Cao, L. Yang, C. Zhu, and W. Jiang Antioxidant properties of the mung bean flavonoids on alleviating heat stress PLoS One 6 2011 e21071 10.1371/journal.pone.0021071
23. J.F. Pittet, L.N. Lu, T. Geiser, H. Lee, M.A. Matthay, and W.J. Welch Stress preconditioning attenuates oxidative injury to the alveolar epithelium of the lung following haemorrhage in rats J. Physiol. 538 Pt 2 2002 583 597
24. S.H. Weng, M.S. Tsai, Y.F. Chiu, Y.H. Kuo, H.J. Chen, and Y.W. Lin Enhancement of mitomycin C-induced cytotoxicity by curcumin results from down-regulation of MKK1/2-ERK1/2-mediated thymidine phosphorylase expression Basic Clin. Pharmacol. Toxicol. 110 2012 298 306
25. W.R. Fields, J.G. Desiderio, K.P. Putnam, D.W. Bombick, and D.J. Doolittle Quantification of changes in c-myc mRNA levels in normal human bronchial epithelial (NHBE) and lung adenocarcinoma (A549) cells following chemical treatment Toxicol. Sci. 63 2001 107 114
26. K. Kato, H. Ito, K. Kamei, and I. Iwamoto Stimulation of the stress-induced expression of stress proteins by curcumin in cultured cells and in rat tissues in vivo Cell Stress Chaperones 3 1998 152 160
27. B.K. Brar, J. Railson, A. Stephanou, R.A. Knight, and D.S. Latchman Urocortin increases the expression of heat shock protein 90 in rat cardiac myocytes in a MEK1/2-dependent manner J. Endocrinol. 172 2002 283 293
28. M. Ogata, S. Hino, A. Saito, K. Morikawa, S. Kondo, and S. Kanemoto Autophagy is activated for cell survival after endoplasmic reticulum stress Mol. Cell. Biol. 26 2006 9220 9231
29. F. Urano, X. Wang, A. Bertolotti, Y. Zhang, P. Chung, and H.P. Harding Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666
30. H. Aoki, Y. Takada, S. Kondo, R. Sawaya, B.B. Aggarwal, and Y. Kondo Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: role of Akt and extracellular signal-regulated kinase signaling pathways Mol. Pharmacol. 72 2007 29 39
31. P. Pallepati, and D.A. Averill-Bates Mild thermotolerance induced at 40 °C protects HeLa cells against activation of death receptor-mediated apoptosis by hydrogen peroxide Free Radic. Biol. Med. 50 2011 667 679
32. B. Hildebrandt, P. Wust, O. Ahlers, A. Dieing, G. Sreenivasa, T. Kerner, R. Felix, and H. Riess The cellular and molecular basis of hyperthermia Crit. Rev. Oncol. Hematol. 43 2002 33 56
33. V.R. Khan, and I.R. Brown The effect of hyperthermia on the induction of cell death in brain, testis, and thymus of the adult and developing rat Cell Stress Chaperones 7 2002 73 90
34. T.J. Standiford, S.L. Kunkel, M.A. Basha, S.W. Chensue, J.P. Lynch III, G.B. Toews, J. Westwick, and R.M. Strieter Interleukin-8 gene expression by a pulmonary epithelial cell line a model for cytokine networks in the lung J. Clin. Invest. 86 1990 1945 1953
35. K. Aoshiba, and A. Nagai Oxidative stress, cell death, and other damage to alveolar epithelial cells induced by cigarette smoke Tob. Induc. Dis. 1 2003 219 226
36. A. Ugusman, Z. Zakaria, C.K. Hui, N.A.M.M. Nordin, and Z.A. Mahdy Flavonoids of Piper sarmentosum and its cyto-protective effects against oxidative stress EXCLI J. 11 2012 705 714
37. S.M. Mustafi, P.K. Chakraborty, R.S. Dey, and S. Raha Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt Cell Stress Chaperones 14 2009 579 589
38. R. Ahmed, and R.F. Duncan Translational regulation of HSP90 mRNA AUG-proximal 5-untranslated region elements essential for preferential heat shock translation J. Biol. Chem. 279 2004 49919 49930
39. C. Mitchell, M.A. Park, G. Zhang, S.I. Han, H. Harada, R.A. Franklin, A. Yacoub, P.L. Li, P.B. Hylemon, S. Grant, and P. Dent 17-Allylamino-17-demethoxygeldanamycin enhances the lethality of deoxycholic acid in primary rodent hepatocytes and established cell lines Mol. Cancer Ther. 6 2007 618 632
40. D. Greenbaum, C. Colangelo, K. Williams, and M. Gerestein Comparing protein abundance and mRNA expression levels on a genomic scale Genome Biol. 4 2003 117 (Epub Review. PubMed PMID: 12952525; PubMed Central PMCID: PMC193646)
41. Á. Putics, E.M. Végh, P. Csermely, and C. Soti Resveratrol induces the heat-shock response and protects human cells from severe heat stress Antioxid. Redox Signal. 10 2008 65 75
42. N. Hosokawa, K. Hirayoshi, H. Kudo, H. Takechi, A. Aoike, K. Kawai, and K. Nagata Inhibition of the activation of heat shock factor in vivo and in vitro by flavonoids Mol. Cell. Biol. 12 1992 3490 3498
43. A.T. Hoang, J. Huang, N.R. Ganguly, J. Zheng, W.C. Powell, S.K. Rabindran, C. Wu, and P. Roy-Burman A novel association between the human heat shock transcription factor 1 (HSF1) and prostate adenocarcinoma Am. J. Pathol. 156 2000 857 864
44. S.C. Nair, E.J. Toran, R.A. Rimerman, S. Hjermstad, T.E. Smithgall, and D.F. Smith A pathway of multi-chaperone interactions common to diverse regulatory proteins: estrogen receptor, Fes tyrosine kinase, heat shock transcription factor HSF1, and the aryl hydrocarbon receptor Cell Stress Chaperones 1 1996 237 250
45. 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. Phys. A 158 2011 566 576
46. M.G. Marcu, M. Doyle, A. Bertolotti, D. Ron, L. Hendershot, and L. Neckers Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha Mol. Cell. Biol. 22 2002 8506 8513
47. S. Manni, A. Brancalion, L.Q. Tubi, A. Colpo, L. Pavan, A. Cabrelle, E. Ave, F. Zaffino, G. Di Maira, M. Ruzzene, F. Adami, R. Zambello, M.R. Pitari, P. Tassone, L.A. Pinna, C. Gurrieri, G. Semenzato, and F. Piazza Protein kinase CK2 protects multiple myeloma cells from ER stress-induced apoptosis and from the cytotoxic effect of HSP90 inhibition through regulation of the unfolded protein response Clin. Cancer Res. 18 2012 1888 1900
48. Q. Jiang, Y. Wang, T. Li, K. Shi, Z. Li, and Y. Ma Heat shock protein 90-mediated inactivation of nuclear factor-κB switches autophagy to apoptosis through becn1 transcriptional inhibition in selenite-induced NB4 cells Mol. Biol. Cell 22 2011 1167 1180
49. A. Tanel, P. Pallepati, A. Bettaieb, P. Morin, and D.A. Averill-Bates Acrolein activates cell survival and apoptotic death responses involving the endoplasmic reticulum in A549 lung cells Biochim. Biophys. Acta 1843 2014 827 835
50. Y. Wang, J. Shen, N. Arenzana, W. Tirasophon, R.J. Kaufman, and R. Prywes Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response J. Biol. Chem. 275 2000 27013 27020
51. C.C. Jiang, L.H. Chen, S. Gillespie, Y.F. Wang, K.A. Kiejda, X.D. Zhang, and P. Hersey Inhibition of MEK sensitizes human melanoma cells to endoplasmic reticulum stress-induced apoptosis Cancer Res. 67 2007 9750 9761
52. H.M. Nishino, N. Fujita, T. Noda, A. Yamaguchi, T. Yoshimori, and A. Yamamoto A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation Nat. Cell Biol. 11 2009 1433 1437
53. T. Shintani, and D.J. Klionsky Autophagy in health and disease: a double-edged sword Science 306 2004 990 995
54. J. Han, X.Y. Pan, Y. Xu, Y. Xiao, Y. An, L. Tie, Y. Pan, and X.J. Li Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage Autophagy 8 2012 812 825
55. S.H. Oh, and S.C. Lim Endoplasmic reticulum stress-mediated autophagy/apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonenamide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells J. Pharmacol. Exp. Ther. 329 2009 112 122
56. J. Kim, M. Kundu, B. Viollet, and K.L. Guan AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1 Nat. Cell Biol. 13 2011 132 141
57. E.K. Kim, S. Lim, J.M. Park, J.K. Seo, J.H. Kim, K.T. Kim, S.H. Ryu, and P.G. Suh Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase J. Cell. Physiol. 227 2012 1680 1687
58. Q. Jiang, F. Li, K. Shi, P. Wu, J. An, Y. Yang, and C. Xu Involvement of p38 in signal switching from autophagy to apoptosis via the PERK/eIF2a/ATF4 axis in selenite-treated NB4 cells Cell. Death Dis. 5 2014 e1270 10.1038/cddis.2014.200
59. A. Ota, J. Zhang, P. Ping, J. Han, and Y. Wang Specific regulation of noncanonical p38 activation by HSP90-Cdc37 chaperone complex in cardiomyocyte Circ. Res. 106 2010 1404 1412
60. B. Halliwell, and J. Gutteridge Free Radicals in Biology and Medicine 1999 New York Oxford University Press 105 245
61. I. Rahman, P.S. Gilmour, L.A. Jimenez, and W. MacNee Oxidative stress and TNF-α induce histone acetylation and NF-κB/AP-1 activation in alveolar epithelial cells: potential mechanism in gene transcription in lung inflammation Mol. Cell. Biochem. 234 235 2002 239 248
62. Y. Zhang, D. Wang, L. Yang, D. Zhou, and J. Zhang Purification and characterization of flavonoids from the leaves of Zanthoxylum bungeanum and correlation between their structure and antioxidant activity PLoS ONE 9 2014 e105725 10.1371/journal.pone.0105725
63. Y.S. Tarahovsky, Y.A. Kim, E.A. Yagolnik, and E.N. Muzafarov Flavonoid-membrane interactions: involvement of flavonoid-metal complexes in raft signaling BBA-Biomembranes 1838 2014 1235 1246
64. J. Kang, Z. Li, T. Wu, G.S. Jensen, A.G. Schauss, and X. Wu Anti-oxidant capacities of flavonoid compounds isolated from acai pulp (Euterpe oleracea Mart.) Food Chem. 122 2010 610 617
65. E. Sugano, H. Isago, N. Murayama, M. Tamai, and H. Tomita Different anti-oxidant effects of thioredoxin 1 and thioredoxin 2 in retinal epithelial cells Cell Struct. Funct. 38 2013 81 88
66. T. Shimizu, H. Nojiri, S. Kawakami, S. Uchiyama, and T. Shirasawa Model mice for tissue-specific deletion of the manganese superoxide dismutase gene Geriatr. Gerontol. Int. 10 2010 S70 S79
67. E.L. Robb, M.M. Page, B.E. Wiens, and J.A. Stuart Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD Biochem. Biophys. Res. Commun. 367 2008 406 412
68. A. Rodina, M. Vilenchik, K. Moulick, J. Aguirre, J. Kim, A. Chiang, J. Litz, C.C. Clement, Y. Kang, Y. She, N. Wu, S. Felts, P. Wipf, J. Massague, X. Jiang, J.L. Brodsky, G.W. Krystal, and G. Chiosis Selective compounds define Hsp90 as a major inhibitor of apoptosis in small-cell lung cancer Nat. Chem. Biol. 8 2007 498 507