Heat stress: A risk factor for skin carcinogenesis

Cancer Letters

Volumn 337, Issue 1, 2013, Pages 35-40

  Calapre, Leslie ^a   Gray, Elin S ^a   Ziman, Mel ^a,b  

^a EDITH COWAN UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Heat shock proteins; Heat shock response; Heat stress; HSP72; HSP90; Skin cancer

Indexed keywords

EID: 84880040865     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.05.039     Document Type: Review

References (91)

1. Solomon S., Qin D., Manning M., Chen Z., Marquis M., Averyt K., Tignor M., Miller H. Climate change 2007: the physical science basis, Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, Cambridge University Press, United Kingdom, New York.
2. Climate Data Online, Australian Bureau of Meteorology, 2013.
3. Bernabo P., Rebecchi L., Jousson O., Martinez-Guitarte J.L., Lencioni V. Thermotolerance and hsp70 heat shock response in the cold-stenothermal chironomid Pseudodiamesa branickii (NE Italy). Cell Stress Chaperones 2011, 16:403-410.
4. Chinnathambi S., Tomanek-Chalkley A., Bickenbach J.R. HSP70 and EndoG modulate cell death by heat in human skin keratinocytes in vitro. Cells Tissues Organs 2008, 187:131-140.
5. Kim S.A., Yoon J.H., Lee S.H., Ahn S.G. Polo-like kinase 1 phosphorylates heat shock transcription factor 1 and mediates its nuclear translocation during heat stress. J. Biol. Chem. 2005, 280:12653-12657.
6. Kregel K.C. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 2002, 92:2177-2186.
7. Sonna L.A., Fujita J., Gaffin S.L., Lilly C.M. Invited review: effects of heat and cold stress on mammalian gene expression. J. Appl. Physiol. 2002, 92:1725-1742.
8. Jonak C., Klosner G., Trautinger F. Heat shock proteins in the skin. Int. J. Cosmet. Sci. 2006, 28:233-241.
9. Arnold A.W., Itin P.H. Laptop computer-induced erythema ab igne in a child and review of the literature. Pediatrics 2010, 126:e1227-e1230.
10. Cavallari V., Cicciarello R., Torre V., Gagliardi M.E., Albiero F., Palazzo R., Siragusa M., Schipis C. Chronic heat-induced skin lesions (erythema ab Igne): ultrastructural studies. Ultrastruct. Pathol. 2001, 25:93-97.
11. Bivik C., Rosdahl I., Ollinger K. Hsp70 protects against UVB induced apoptosis by preventing release of cathepsins and cytochrome c in human melanocytes. Carcinogenesis 2007, 28:537-544.
12. Soti C., Nagy E., Giricz Z., Vigh L., Csermely P., Ferdinandy P. Heat shock proteins as emerging therapeutic targets. Br. J. Pharmacol. 2005, 146:769-780.
13. Ciocca D.R., Calderwood S.K. Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 2005, 10:86-103.
14. Volloch V., Rits S. A natural extracellular factor that induces Hsp72, inhibits apoptosis, and restores stress resistance in aged human cells. Exp. Cell Res. 1999, 253:483-492.
15. Lee J.S., Lee J.J., Seo J.S. HSP70 deficiency results in activation of c-Jun N-terminal Kinase, extracellular signal-regulated kinase, and caspase-3 in hyperosmolarity-induced apoptosis. J. Biol. Chem. 2005, 280:6634-6641.
16. Park H.G., Han S.I., Oh S.Y., Kang H.S. Cellular responses to mild heat stress. Cell Mol. Life Sci. 2005, 62:10-23.
17. Brash D.E. Roles of the transcription factor p53 in keratinocyte carcinomas. Br. J. Dermatol. 2006, 154(Suppl. 1):8-10.
18. Dai C., Whitesell L., Rogers A.B., Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007, 130:1005-1018.
19. Tan S., Bertucci V. Erythema ab igne: an old condition new again. CMAJ 2000, 162:77-78.
20. Donoghue A.M. Occupational health hazards in mining: an overview. Occup. Med. (Lond) 2004, 54:283-289.
21. Fortes C. Nonsolar occupational risk factors for cutaneous melanoma. Int. Soc. Dermatol. 2008, 47:319-328.
22. De Maio A. Heat shock proteins: facts, thoughts, and dreams. Shock 1999, 11:1-12.
23. Joly A.L., Wettstein G., Mignot G., Ghiringhelli F., Garrido C. Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J. Innate Immun. 2010, 2:238-247.
24. Jolly C., Metz A., Govin J., Vigneron M., Turner B.M., Khochbin S., Vourc'h C. Stress-induced transcription of satellite III repeats. J. Cell Biol. 2004, 164:25-33.
25. King F.W., Wawrzynow A., Hohfeld J., Zylicz M. Co-chaperones Bag-1, Hop and Hsp40 regulate Hsc70 and Hsp90 interactions with wild-type or mutant p53. EMBO J. 2001, 20:6297-6305.
26. Morimoto R.I. Dynamic remodeling of transcription complexes by molecular chaperones. Cell 2002, 110:281-284.
27. Amin J., Ananthan J., Voellmy R. Key features of heat shock regulatory elements. Mol. Cell Biol. 1988, 8:3761-3769.
28. Guo S., Wharton W., Moseley P., Shi H. Heat shock protein 70 regulates cellular redox status by modulating glutathione-related enzyme activities. Cell Stress Chaperones 2007, 12:245-254.
29. De Maio A. Extracellular heat shock proteins, cellular export vesicles, and the Stress Observation System: a form of communication during injury, infection, and cell damage. It is never known how far a controversial finding will go! Dedicated to Ferruccio Ritossa. Cell Stress Chaperones 2011, 16:235-249.
30. Yaglom J.A., Gabai V.L., Sherman M.Y. High levels of heat shock protein Hsp72 in cancer cells suppress default senescence pathways. Cancer Res. 2007, 67:2373-2381.
31. Shellman Y.G., Howe W.R., Miller L.A., Goldstein N.B., Pacheco T.R., Mahajan R.L., LaRue S.M., Norris D.A. Hyperthermia induces endoplasmic reticulum-mediated apoptosis in melanoma and non-melanoma skin cancer cells. J. Invest. Dermatol. 2008, 128:949-956.
32. Roti Roti J.L. Cellular responses to hyperthermia (40-46°C): cell killing and molecular events. Int. J. Hyperther. 2008, 24:3-15.
33. Roti Roti J.L. Heat-induced alterations of nuclear protein associations and their effects on DNA repair and replication. Int. J. Hyperther. 2007, 23:3-15.
34. Wong R.S., Kapp L.N., Krishnaswamy G., Dewey W.C. Critical steps for induction of chromosomal aberrations in CHO cells heated in S phase. Radiat. Res. 1993, 133:52-59.
35. Hunt C.R., Pandita R.K., Laszlo A., Higashikubo R., Agarwal M., Kitamura T., Gupta A., Rief N., Horikoshi N., Baskaran R., Lee J.H., Lobrich M., Paull T.T., Roti Roti J.L., Pandita T.K. Hyperthermia activates a subset of ataxia-telangiectasia mutated effectors independent of DNA strand breaks and heat shock protein 70 status. Cancer Res. 2007, 67:3010-3017.
36. Takahashi A., Matsumoto H., Nagayama K., Kitano M., Hirose S., Tanaka H., Mori E., Yamakawa N., Yasumoto J., Yuki K., Ohnishi K., Ohnishi T. Evidence for the involvement of double-strand breaks in heat-induced cell killing. Cancer Res. 2004, 64:8839-8845.
37. Daugaard M., Kirkegaard-Sorensen T., Ostenfeld M.S., Aaboe M., Hoyer-Hansen M., Orntoft T.F., Rohde M., Jaattela M. Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res. 2007, 67:2559-2567.
38. G. Pockley, Heat shock proteins as regulators of the immune response, The Lancet, 2003.
39. Mosser D.D., Morimoto R.I. Molecular chaperones and the stress of oncogenesis. Oncogene 2004, 23:2907-2918.
40. Quenneville L.A., Trotter M.J., Maeda T., Tron V.A. P53-dependent regulation of heat shock protein 72. Br. J. Dermatol. 2002, 146:786-791.
41. Maloney A., Workman P. HSP90 as a new therapeutic target for cancer therapy: the story unfolds. Expert Opin. Biol. Ther. 2002, 2:3-24.
42. Cornford P.A., Dodson A.R., Parsons K.F., Desmond A.D., Woolfenden A., Fordham M., Neoptolemos J.P., Ke Y., Foster C.S. Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res. 2000, 60:7099-7105.
43. Gabai V.L., Yaglom J.A., Waldman T., Sherman M.Y. Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells. Mol. Cell Biol. 2009, 29:559-569.
44. Phillips P.A., Dudeja V., McCarroll J.A., Borja-Cacho D., Dawra R.K., Grizzle W.E., Vickers S.M., Saluja A.K. Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer Res. 2007, 67:9407-9416.
45. Sun B., Zhang S., Zhang D., Li Y., Zhao X., Luo Y., Guo Y. Identification of metastasis-related proteins and their clinical relevance to triple-negative human breast cancer. Clin. Cancer Res. 2008, 14:7050-7059.
46. Zylicz M., King F.W., Wawrzynow A. Hsp70 interactions with the p53 tumour suppressor protein. EMBO J. 2001, 20:4634-4638.
47. Park H.S., Lee J.S., Huh S.H., Seo J.S., Choi E.J. Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J. 2001, 20:446-456.
48. Weston C.R., Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 2007, 19:142-149.
49. Karin M., Gallagher E. From JNK to pay dirt: jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 2005, 57:283-295.
50. Wagner E.F., Nebreda A.R. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer 2009, 9:537-549.
51. Chen N., Nomura M., She Q.B., Ma W.Y., Bode A.M., Wang L., Flavell R.A., Dong Z. Suppression of skin tumorigenesis in c-Jun NH(2)-terminal kinase-2-deficient mice. Cancer Res. 2001, 61:3908-3912.
52. She Q.B., Chen N., Bode A.M., Flavell R.A., Dong Z. Deficiency of c-Jun-NH(2)-terminal kinase-1 in mice enhances skin tumor development by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res. 2002, 62:1343-1348.
53. Merienne K., Helmlinger D., Perkin G.R., Devys D., Trottier Y. Polyglutamine expansion induces a protein-damaging stress connecting heat shock protein 70 to the JNK pathway. J. Biol. Chem. 2003, 278:16957-16967.
54. Beere H.M., Wolf B.B., Cain K., Mosser D.D., Mahboubi A., Kuwana T., Tailor P., Morimoto R.I., Cohen G.M., Green D.R. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2000, 2:469-475.
55. Kayama M., Nakazawa T., Thanos A., Morizane Y., Murakami Y., Theodoropoulou S., Abe T., Vavvas D., Miller J.W. Heat shock protein 70 (HSP70) is critical for the photoreceptor stress response after retinal detachment via modulating anti-apoptotic Akt kinase. Am. J. Pathol. 2011, 178:1080-1091.
56. Liu M., Aneja R., Liu C., Sun L., Gao J., Wang H., Dong J.T., Sarli V., Giannis A., Joshi H.C., Zhou J. Inhibition of the mitotic kinesin Eg5 up-regulates Hsp70 through the phosphatidylinositol 3-kinase/Akt pathway in multiple myeloma cells. J. Biol. Chem. 2006, 281:18090-18097.
57. Marquette A., Bagot M., Bensussan A., Dumaz N. Recent discoveries in the genetics of melanoma and their therapeutic implications. Arch. Immunol. Ther. Exp. 2007, 55:363-372.
58. A.L. Rerole, A.L. Joly, D. Thuringer, C. Garrido, HSP70 and HSP27: Emerging Targets in Cancer Therapy, Apoptosome, 2010, pp. 169-202.
59. Hubner A., Mulholland D.J., Standen C.L., Karasarides M., Cavanagh-Kyros J., Barrett T., Chi H., Greiner D.L., Tournier C., Sawyers C.L., Flavell R.A., Wu H., Davis R.J. JNK and PTEN cooperatively control the development of invasive adenocarcinoma of the prostate. Proc. Natl. Acad. Sci. USA 2012, 109:12046-12051.
60. Paraiso K.H., Xiang Y., Rebecca V.W., Abel E.V., Chen Y.A., Munko A.C., Wood E., Fedorenko I.V., Sondak V.K., Anderson A.R., Ribas A., Palma M.D., Nathanson K.L., Koomen J.M., Messina J.L., Smalley K.S. PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res. 2011, 71:2750-2760.
61. Bennett D. Familial Melanoma Genes, Melanocyte Immortalisation, and Melanoma Initiation. From Melanocyte to Melanoma: The progression to Malignancy 2005, 183-196. Humana Press inc., NJ. V. Hearing, S. Leong (Eds.).
62. Vivanco I., Palaskas N., Tran C., Finn S.P., Getz G., Kennedy N.J., Jiao J., Rose J., Xie W., Loda M., Golub T., Mellinghoff I.K., Davis R.J., Wu H., Sawyers C.L. Identification of the JNK signaling pathway as a functional target of the tumor suppressor PTEN. Cancer Cell 2007, 11:555-569.
63. Wang S., Gao J., Lei Q., Rozengurt N., Pritchard C., Jiao J., Thomas G.V., Li G., Roy-Burman P., Nelson P.S., Liu X., Wu H. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003, 4:209-221.
64. Sumimoto H., Imabayashi F., Iwata T., Kawakami Y. The BRAK-MAPK signalling pathway is essential for cancer-immune evasion in human melanoma cells. J. Exp. Med. 2006, 203:1651-1656.
65. Wellbrock C. Melanoma development and pigment cell transformation. From Melanocytes to Melanoma: The Progression to Malignancy 2005, 247-261. Humana Press Inc., NJ. V. Hearing, S. Leong (Eds.).
66. Zhang H., Burrows F. Targeting multiple signal transduction pathways through inhibition of Hsp90. J. Mol. Med. (Berl) 2004, 82:488-499.
67. Banerji U., Affolter A., Judson I., Marais R., Workman P. BRAF and NRAS mutations in melanoma: potential relationships to clinical response to HSP90 inhibitors. Mol. Cancer Ther. 2008, 7:737-739.
68. Tronov V., Artamonov D., Gorbacheva L.B. Genetic markers of melanoma. Russ. J. Genet. 2010, 46:146-156.
69. Benjamin C.L., Ullrich S.E., Kripke M.L., Ananthaswamy H.N. P53 tumor suppressor gene: a critical molecular target for UV induction and prevention of skin cancer. Photochem. Photobiol. 2008, 84:55-62.
70. Harris S.L., Levine A.J. The p53 pathway: positive and negative feedback loops. Oncogene 2005, 24:2899-2908.
71. Harrison M.K., Adon A.M., Saavedra H.I. The G1 phase Cdks regulate the centrosome cycle and mediate oncogene-dependent centrosome amplification. Cell Div. 2011, 6:2.
72. Terzian T., Torchia E., Dai D., Robinson S., Murao K., Steigman R., Gonzalez V., Boyle G., Powell M., Pollock P., Lozano G., Robinson W., Roop D., Box N. P53 prevents progression of nevi to melanoma predominantly through cell cycle regulation. Pig. Cell Melanoma Res. 2010, 23:781-794.
73. Smith M.L., Ford J.M., Hollander M.C., Bortnick R.A., Amundson S.A., Seo Y.R., Deng C.X., Hanawalt P.C., Fornace A.J. P53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol. Cell Biol. 2000, 20:3705-3714.
74. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
75. Beckerman R., Prives C. Transcriptional regulation by p53. Cold Spring Harb. Perspect Biol. 2010, 2:a000935.
76. Ozaki T., Nakagawara A. Role of p53 in cell death and human cancers. Cancers 2011, 3:994-1013.
77. Green D.R. At the gates of death. Cancer Cell 2006, 9:328-330.
78. Ming L., Wang P., Bank A., Yu J., Zhang L. PUMA dissociates Bax and Bcl-X(L) to induce apoptosis in colon cancer cells. J. Biol. Chem. 2006, 281:16034-16042.
79. Cui R., Widlund H.R., Feige E., Lin J.Y., Wilensky D.L., Igras V.E., D'Orazio J., Fung C.Y., Schanbacher C.F., Granter S.R., Fisher D.E. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 2007, 128:853-864.
80. Chakraborty A., Uechi T., Kenmochi N. Guarding the 'translation apparatus': defective ribosome biogenesis and the p53 signaling pathway. Wiley Interdiscip. Rev. RNA 2011, 2:507-522.
81. Mullerat J., Deroide F., Winslet M.C., Perrett C.W. Proliferation and p53 expression in anal cancer precursor lesions. Anticancer Res. 2003, 23:2995-2999.
82. Gaillard J.B., Chiesa J., Reboul D., Arnaud A., Brun S., Donadio D., Exbrayat C., Wickenhauser S., Bourquard P., Jourdan E., Lavabre-Bertrand T. Monosomal karyotype routinely defines a poor prognosis subgroup in acute myeloid leukemia and is frequently associated with TP53 deletion. Leuk Lymphoma 2012, 53:336-337.
83. Hussein M.R., Haemel A.K., Wood G.S. P53-related pathways and the molecular pathogenesis of melanoma. Eur. J. Cancer Prev. 2003, 12:93-100.
84. Reifenberger J., Wolter M., Knobbe C.B., Kohler B., Schonicke A., Scharwachter C., Kumar K., Blaschke B., Ruzicka T., Reifenberger G. Somatic mutations in the PTCH, SMOH, SUFUH and TP53 genes in sporadic basal cell carcinomas. Br. J. Dermatol. 2005, 152:43-51.
85. Madan V., Lear J.T., Szeimies R.M. Non-melanoma skin cancer. Lancet 2010, 375:673-685.
86. Wu X., Bayle J.H., Olson D., Levine A.J. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 1993, 7:1126-1132.
87. Wiech M., Olszewski M.B., Tracz-Gaszewska Z., Wawrzynow B., Zylicz M., Zylicz A. Molecular mechanism of mutant p53 stabilization: the role of HSP70 and MDM2. PLoS ONE 2012, 7:e51426.
88. Hagn F., Lagleder S., Retzlaff M., Rohrberg J., Demmer O., Richter K., Buchner J., Kessler H. Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53. Nat. Struct. Mol. Biol. 2011, 18:1086-1093.
89. Park S.J., Borin B., Martinez-Yamout M., Dyson H.J. The client protein p53 adopts a molten globule-like state in the presence of HSP90. Nat. Struct. Mol. Biol. 2011, 18:537-541.
90. Walerych D., Gutkowska M., Klejman M.P., Wawrzynow B., Tracz Z., Wiech M., Zylicz M., Zylicz A. ATP binding to Hsp90 is sufficient for effective chaperoning of p53 protein. J. Biol. Chem. 2010, 285:32020-32028.
91. Jeffrey K.L., Camps M., Rommel C., Mackay C.R. Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat. Rev. Drug Discov. 2007, 6:391-403.