SUMOylation and SENP3 regulate STAT3 activation in head and neck cancer

Oncogene

Volumn 35, Issue 45, 2016, Pages 5826-5838

  Zhou, Z ^a,b   Wang, M ^a   Li, J ^b   Xiao, M ^a   Chin, Y E ^a   Cheng, J ^a   Yeh, E T H ^c   Yang, J ^a   Yi, J ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ALCOHOL; INTERLEUKIN 6; REACTIVE OXYGEN METABOLITE; SENP3 PROTEIN; STAT3 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; TRANSCRIPTION FACTOR; TUBULIN; UNCLASSIFIED DRUG; 4-(N-METHYL-N-NITROSAMINO)-1-(3-PYRIDYL)-1-BUTANONE; CYSTEINE PROTEINASE; NITROSAMINE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 2; SENP3 PROTEIN, HUMAN; SUMO PROTEIN; SUMO2 PROTEIN, HUMAN; SUMO3 PROTEIN, HUMAN; UBIQUITIN;

ALCOHOL CONSUMPTION; ARTICLE; CANCER STAGING; FEMALE; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; HUMAN TISSUE; LARYNX CARCINOMA; MAJOR CLINICAL STUDY; MALE; OXIDATIVE STRESS; PHARYNX CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SMOKING; SUMOYLATION; ADVERSE EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HEAD AND NECK NEOPLASMS; LARYNGEAL NEOPLASMS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; CYSTEINE ENDOPEPTIDASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; INTERLEUKIN-6; LARYNGEAL NEOPLASMS; MALE; NEOPLASM STAGING; NITROSAMINES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 2; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SMOKING; STAT3 TRANSCRIPTION FACTOR; SUMOYLATION; TRANSCRIPTION, GENETIC; UBIQUITINS;

EID: 84968649977     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.124     Document Type: Article

References (85)

1. Zhong Z, Wen Z, Darnell JE Jr. STAT3: A STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 1994; 264: 95-98.
2. Levy DE, Darnell JE. Signalling: Stats: Transcriptional control and biological impact. Nat Rev Mol Cell Biol 2002; 3: 651-662.
3. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454: 436-444.
4. Becker C, Fantini MC, Schramm C, Lehr HA, Wirtz S, Nikolaev A et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004; 21: 491-501.
5. Berishaj M, Gao SP, Ahmed S, Leslie K, Al-Ahmadie H, Gerald WL et al. STAT3 is tyrosine-phosphorylated through the interleukin-6/glycoprotein 130/Janus kinase pathway in breast cancer. Breast Cancer Res 2007; 9: R32.
6. Morikawa T, Baba Y, Yamauchi M, Kuchiba A, Nosho K, Shima K et al. STAT3 expression, molecular features, inflammation patterns, and prognosis in a database of 724 colorectal cancers. Clin Cancer Res 2011; 17: 1452-1462.
7. Kim D-Y, Cha S-T, Ahn D-H, Kang H-Y, Kwon C-I, Ko K-H et al. STAT3 expression in gastric cancer indicates a poor prognosis. J Gastroenterol Hepatol 2009; 24: 646-651.
8. Lou W, Ni Z, Dyer K, Tweardy DJ, Gao AC. Interleukin-6 induces prostate cancer cell growth accompanied by activation of STAT3 signaling pathway. Prostate 2000; 42: 239-242.
9. Masuda M, Suzui M, Yasumatu R, Nakashima T, Kuratomi Y, Azuma K et al. Constitutive activation of signal transducers and activators of transcription 3 correlates with Cyclin D1 overexpression and may provide a novel prognostic marker in head and neck squamous cell carcinoma. Cancer Res 2002; 62: 3351-3355.
10. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: A leading role for STAT3. Nat Rev Cancer 2009; 9: 798-809.
11. Bromberg J, Wang TC. Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell 2009; 15: 79-80.
12. Li N, Grivennikov SI, Karin M. The Unholy Trinity: inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell 2011; 19: 429-431.
13. Groner B, Lucks P, Borghouts C. The function of STAT3 in tumor cells and their microenvironment. Semin Cell Dev Biol 2008; 19: 341-350.
14. Pilati C, Amessou M, Bihl MP, Balabaud C, Van Nhieu JT, Paradis V et al. Somatic mutations activating STAT3 in human inflammatory hepatocellular adenomas. J Exp Med 2011; 208: 1359-1366.
15. Rokavec M, Öner MG, Li H, Jackstadt R, Jiang L, Lodygin D et al. IL-6 R/STAT3/ miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest 2014; 124: 1853-1867.
16. Yuan Z-L, Guan Y-J, Chatterjee D, Chin YE. STAT3 dimerization regulated by reversible acetylation of a single lysine residue. Science 2005; 307: 269-273.
17. Yang J, Huang J, Dasgupta M, Sears N, Miyagi M, Wang B et al. Reversible methylation of promoter-bound STAT3 by histone-modifying enzymes. Proc Natl Acad Sci USA 2010; 107: 21499-21504.
18. Chen X, Ying Z, Lin X, Lin H, Wu J, Li M et al. Acylglycerol kinase augments JAK2/STAT3 signaling in esophageal squamous cells. J Clin Invest 2013; 123: 2576-2589.
19. Zhang P, Zhao Y, Zhu X, Sedwick D, Zhang X, Wang Z. Cross-talk between phospho-STAT3 and PLC1 plays a critical role in colorectal tumorigenesis. Mol Cancer Res 2011; 9: 1418-1428.
20. He Q-Y, Yi H-M, Yi H, Xiao T, Qu J-Q, Yuan L et al. Reduction of RKIP expression promotes nasopharyngeal carcinoma invasion and metastasis by activating STAT3 signaling. Oncotarget 2015; 6: 16422-16436.
21. Song JI, Grandis JR. STAT signaling in head and neck cancer. Oncogene 2000; 19: 2489-2495.
22. Nagpal JK, Mishra R, Das BR. Activation of Stat-3 as one of the early events in tobacco chewing-mediated oral carcinogenesis. Cancer 2002; 94: 2393-2400.
23. Masuda M, Wakasaki T, Suzui M, Toh S, Joe AK, Weinstein IB. STAT3 orchestrates tumor development and progression: The Achilles' heel of head and neck cancers? Curr Cancer Drug Targets 2010; 10: 117-126.
24. Leeman RJ, Lui VWY, Grandis JR. STAT3 as a therapeutic target in head and neck cancer. Expert Opin Biol Ther 2006; 6: 231-241.
25. Liu T, Peng H, Zhang M, Deng Y, Wu Z. Cucurbitacin B, a small molecule inhibitor of the STAT3 signaling pathway, enhances the chemosensitivity of laryngeal squamous cell carcinoma cells to cisplatin. Eur J Pharmacol 2010; 641: 15-22.
26. Gao LF, Wen LJ, Yu H, Zhang L, Meng Y, Shao YT et al. Knockdown of STAT3 expression using RNAi inhibits growth of laryngeal tumors in vivo. Acta Pharmacol Sin 2006; 27: 347-352.
27. Gao LF, Xu DQ, Wen LJ, Zhang XY, Shao YT, Zhao XJ. Inhibition of STAT3 expression by siRNA suppresses growth and induces apoptosis in laryngeal cancer cells. Acta Pharmacol Sin 2005; 26: 377-383.
28. Xi S, Gooding WE, Grandis JR. In vivo antitumor efficacy of STAT3 blockade using a transcription factor decoy approach: implications for cancer therapy. Oncogene 2004; 24: 970-979.
29. Grandis JR, Drenning SD, Chakraborty A, Zhou MY, Zeng Q, Pitt AS et al. Requirement of STAT3 but not Stat1 activation for epidermal growth factor receptor-mediated cell growth In vitro. J Clin Invest 1998; 102: 1385-1392.
30. Grandis JR, Drenning SD, Zeng Q, Watkins SC, Melhem MF, Endo S et al. Constitutive activation of STAT3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc Natl Acad Sci USA 2000; 97: 4227-4232.
31. Lee TL. Epigenetic modification of SOCS-1 differentially regulates STAT3 activation in response to interleukin-6 receptor and epidermal growth factor receptor signaling through JAK and/or MEK in head and neck squamous cell carcinomas. Mol Cancer Ther 2006; 5: 8-19.
32. Sriuranpong V, Park JI, Amornphimoltham P, Patel V, Nelkin BD, Gutkind JS. Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system. Cancer Res 2003; 63: 2948-2956.
33. Squarize CH, Castilho RM, Sriuranpong V, Pinto Jr DS, Gutkind JS. Molecular cross-talk between the NFkappaB and STAT3 signaling pathways in head and neck squamous cell carcinoma. Neoplasia 2006; 8: 733-746.
34. Hashibe M, Brennan P, Benhamou S, Castellsague X, Chen C, Curado MP et al. Alcohol drinking in never users of tobacco, cigarette smoking in never drinkers, and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. J Natl Cancer Inst 2007; 99: 777-789.
35. Lewin F, Norell SE, Johansson H, Gustavsson P, Wennerberg J, Biörklund A et al. Smoking tobacco, oral snuff, and alcohol in the etiology of squamous cell carcinoma of the head and neck. Cancer 1998; 82: 1367-1375.
36. Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S et al. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Res 1988; 48: 3282-3287.
37. Macha MA, Matta A, Chauhan SS, Siu KWM, Ralhan R. Guggulsterone (GS) inhibits smokeless tobacco and nicotine-induced NF-kB and STAT3 pathways in head and neck cancer cells. Carcinogenesis 2011; 32: 368-380.
38. Liu X. STAT3 activation inhibits human bronchial epithelial cell apoptosis in response to cigarette smoke exposure. Biochem Biophys Res Commun 2007; 353: 121-126.
39. Chen RJ, Ho YS, Guo HR, Wang YJ. Rapid activation of STAT3 and ERK1/2 by nicotine modulates cell proliferation in human bladder cancer cells. Toxicol Sci 2007; 104: 283-293.
40. Csiszar A, Podlutsky A, Wolin MS, Losonczy G, Pacher P, Ungvari Z. Oxidative stress and accelerated vascular aging: implications for cigarette smoking. Front Biosci (Landmark Ed) 2009; 14: 3128-3144.
41. Pryor WA, Prier DG, Church DF. Electron-spin resonance study of mainstream and sidestream cigarette smoke: nature of the free radicals in gas-phase smoke and in cigarette tar. Environ Health Perspect 1983; 47: 345-355.
42. Zang LY, Stone K, Pryor WA. Detection of free radicals in aqueous extracts of cigarette tar by electron spin resonance. Free Radic Biol Med 1995; 19: 161-167.
43. Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann NY Acad Sci 1993; 686: 12-27.
44. Ng IHW, Yeap YYC, Ong LSR, Jans DA, Bogoyevitch MA. Oxidative stress impairs multiple regulatory events to drive persistent cytokine-stimulated STAT3 phosphorylation. Biochim Biophys Acta 2014; 1843: 483-494.
45. Qu Y, Oyan AM, Liu R, Hua Y, Zhang J, Hovland R et al. Generation of prostate tumor-initiating cells is associated with elevation of reactive oxygen species and IL-6/STAT3 signaling. Cancer Res 2013; 73: 7090-7100.
46. Bito T, Sumita N, Masaki T, Shirakawa T, Ueda M, Yoshiki R et al. Ultraviolet light induces STAT3 activation in human keratinocytes and fibroblasts through reactive oxygen species and DNA damage. Exp Dermatol 2010; 19: 654-660.
47. Huang C, Han Y, Wang Y, Sun X, Yan S, Yeh ETH et al. SENP3 is responsible for HIF-1 transactivation under mild oxidative stress via p300 de-SUMOylation. EMBO J 2009; 28: 2748-2762.
48. Han Y, Huang C, Sun X, Xiang B, Wang M, Yeh ETH et al. SENP3-mediated de-conjugation of SUMO2/3 from promyelocytic leukemia is correlated with accelerated cell proliferation under mild oxidative stress. J Biol Chem 2010; 285: 12906-12915.
49. Yan S, Sun X, Xiang B, Cang H, Kang X, Chen Y et al. Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J 2010; 29: 3773-3786.
50. Ren Y, Liu K, Wang M, Yu Y, Yang K, Chen Q et al. De-SUMOylation of FOXC2 by SENP3 promotes the epithelial-mesenchymal transition in gastric cancer cells. Oncotarget 2014; 5: 7093-7104.
51. Hecht SS. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat Rev Cancer 2003; 3: 733-744.
52. Schindler C, Darnell JE. Transcriptional responses to polypeptide ligands: The JAK-STAT pathway. Annu Rev Biochem 1995; 64: 621-651.
53. Wen Z, Zhong Z, Darnell JE Jr. Maximal activation of transcription by statl and STAT3 requires both tyrosine and serine phosphorylation. Cell 1995; 82: 241-250.
54. Pryor WA, Stone K, Zang LY, Bermúdez E. Fractionation of aqueous cigarette tar extracts: Fractions that contain the tar radical cause DNA damage. Chem Res Toxicol 1998; 11: 441-448.
55. Yeh E. SUMOylation and De-SUMOylation: wrestling with life's processes. J Biol Chem 2009; 284: 8223-8227.
56. Chen W, Daines MO, Khurana Hershey GK. Turning off signal transducer and activator of transcription (STAT): The negative regulation of STAT signaling. J Allergy Clin Immunol 2004; 114: 476-489.
57. Yamamoto T, Sekine Y, Kashima K, Kubota A, Sato N, Aoki N et al. The nuclear isoform of protein-tyrosine phosphatase TC-PTP regulates interleukin-6-mediated signaling pathway through STAT3 dephosphorylation. Biochem Biophys Res Commun 2002; 297: 811-817.
58. Johnston PA, Grandis JR. STAT3 signaling: Anticancer strategies and challenges. Mol Interv 2011; 11: 18-26.
59. Wilkinson KA, Henley JM. Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 2010; 428: 133-145.
60. Ulane CM, Rodriguez JJ, Parisien JP, Horvath CM. STAT3 ubiquitylation and degradation by mumps virus suppress cytokine and oncogene signaling. J Virol 2003; 77: 6385-6393.
61. Perry E, Tsruya R, Levitsky P, Pomp O, Taller M, Weisberg S et al. TMF/ARA160 is a BC-box-containing protein that mediates the degradation of STAT3. Oncogene 2004; 23: 8908-8919.
62. Geiss-Friedlander R, Melchior F. Concepts in sumoylation: A decade on. Nat Rev Mol Cell Biol 2007; 8: 947-956.
63. Yeh ET, Gong L, Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene 2000; 248: 1-14.
64. Gill G. Something about SUMO inhibits transcription. Curr Opin Genet Dev 2005; 15: 536-541.
65. Girdwood DWH, Tatham MH, Hay RT. SUMO and transcriptional regulation. Semin Cell Dev Biol 2004; 15: 201-210.
66. Droescher M, Begitt A, Marg A, Zacharias M, Vinkemeier U. Cytokine-induced paracrystals prolong the activity of signal transducers and activators of transcription (STAT) and provide a model for the regulation of protein solubility by Small Ubiquitin-like Modifier (SUMO). J Biol Chem 2011; 286: 18731-18746.
67. Hunter KD, Parkinson EK, Harrison PR. Profiling early head and neck cancer. Nat Rev Cancer 2005; 5: 127-135.
68. Quon H, Liu FF, Cummings BJ. Potential molecular prognostic markers in head and neck squamous cell carcinomas. Head Neck 2001; 23: 147-159.
69. Le Q-T, Giaccia AJ. Therapeutic exploitation of the physiological and molecular genetic alterations in head and neck cancer. Clin Cancer Res 2003; 9: 4287-4295.
70. Iwamoto H. An epidemiological study of laryngeal cancer in Japan. Laryngoscope 1975; 85: 1162-1172.
71. Parfenov M, Pedamallu CS, Gehlenborg N, Freeman SS, Danilova L, Bristow CA et al. Head and neck cancer [Internet]. Proc Natl Acad Sci USA 2014; 111: 15544-15549.
72. Takahashi H, Ogata H, Nishigaki R, Broide DH, Karin M. Tobacco smoke promotes lung tumorigenesis by triggering IKK-and JNK1-dependent inflammation. Cancer Cell 2010; 17: 89-97.
73. Chen R-J, Chang LW, Lin P, Wang Y-J. Epigenetic effects and molecular mechanisms of tumorigenesis induced by cigarette smoke: An overview. J Oncol 2011; 2011: 1-14.
74. Arredondo J. Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/ MEK1/ERK and JAK-2/STAT-3 pathways downstream of alpha7 nicotinic receptor in oral keratinocytes. FASEB J 2006; 20: 2093-2101.
75. Hainaut P, Pfeifer GP. Patterns of p53 GT transversions in lung cancers reflect the primary mutagenic signature of DNA-damage by tobacco smoke. Carcinogenesis 2001; 22: 367-374.
76. Pfeifer GP, Denissenko MF, Olivier M, Tretyakova N, Hecht SS, Hainaut P. Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene 2002; 21: 7435-7451.
77. Hittelman WN. Genetic instability in epithelial tissues at risk for cancer. Ann NY Acad Sci 2001; 952: 1-12.
78. Rothenberg SM, Ellisen LW. The molecular pathogenesis of head and neck squamous cell carcinoma. J Clin Invest 2012; 122: 1951-1957.
79. Huang R-Y, Li M-Y, Hsin MKY, Underwood MJ, Ma LT, Mok TSK et al. 4-Methylnitrosamino-1-3-pyridyl-1-butanone (NNK) promotes lung cancer cell survival by stimulating thromboxane A2 and its receptor. Oncogene 2010; 30: 106-116.
80. Hecht SS. Biochemistry, biology, and carcinogenicity of tobacco-specific N-nitrosamines. Chem Res Toxicol 1998; 11: 559-603.
81. Ye YN, Liu ESL, Shin VY, Wu WKK, Cho CH. The modulating role of nuclear factorkappaB in the action of alpha7-nicotinic acetylcholine receptor and cross-talk between 5-lipoxygenase and cyclooxygenase-2 in colon cancer growth induced by 4-(N-methyl-N-nitrosamino)-1-(3-pyridyl)-1-butanone. J Pharmacol Exp Ther 2004; 311: 123-130.
82. Kim PM, Wells PG. Genoprotection by UDP-glucuronosyltransferases in peroxidase-dependent, reactive oxygen species-mediated micronucleus Initiation by the carcinogens 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone and benzo[a] pyrene. Cancer Res 1996; 56: 1526-1532.
83. Khariwala SS, Hatsukami D, Hecht SS. Tobacco carcinogen metabolites and DNA adducts as biomarkers in Head and Neck cancer: Potential screening tools and prognostic indicators. Head Neck 2011; 34: 441-447.
84. Yang J, Li H, Chen Y-Y, Wang X-J, Shi G-Y, Hu Q-S et al. Anthraquinones sensitize tumor cells to arsenic cytotoxicity in vitro and in vivo via reactive oxygen species-mediated dual regulation of apoptosis. Free Radic Biol Med 2004; 37: 2027-2041.
85. Sang J, Yang K, Sun Y, Han Y, Cang H, Chen Y et al. SUMO2 and SUMO3 transcription is differentially regulated by oxidative stress in an Sp1-dependent manner. Biochem J 2011; 435: 489-498.