Biological significance and therapeutic implication of resveratrolinhibited Wnt, notch and STAT3 signaling in cervical cancer cells

Genes and Cancer

Volumn 5, Issue 5-6, 2014, Pages 154-164

  Zhang, Peng ^a   Li, Hong ^a   Yang, Bin ^b   Yang, Fan ^b   Zhang, Lin Lin ^a   Kong, Qing You ^a   Chen, Xiao Yan ^a   Wu, Mo Li ^a   Liu, Jia ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Cervical cancers; Molecular target; Resveratrol; Signal transduction pathways; STAT3 signaling

Indexed keywords

BETA CATENIN; NOTCH RECEPTOR; RESVERATROL; STAT3 PROTEIN; WNT PROTEIN;

ADENOCARCINOMA; APOPTOSIS; ARTICLE; CAUSE OF DEATH; CELL GROWTH; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; FLOW CYTOMETRY; GENE REPRESSION; GENE TRANSLOCATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TISSUE MICROARRAY; UPREGULATION; UTERINE CERVIX CANCER; WESTERN BLOTTING;

EID: 84907953697     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Schiller JT, Davies P. Delivering on the promise: HPV vaccines and cervical cancer. Nat Rev Microbiol. 2004; 2(4):343-347.
2. Ojesina AI, Lichtenstein L, Freeman SS, Pedamallu CS, Imaz-Rosshandler I, Pugh TJ, Cherniack AD, Ambrogio L, Cibulskis K, Bertelsen B, Romero-Cordoba S, Treviño V, Vazquez-Santillan K, Guadarrama AS, Wright AA, Rosenberg MW, et al. Landscape of genomic alterations in cervical carcinomas. Nature. 2014; 506(7488):371-375.
3. Hirschowitz L, Nucci M and Zaino RJ. Problematic issues in the staging of endometrial, cervical and vulval carcinomas. Histopathology. 2013; 62(1):176-202.
4. Touboul C, Uzan C, Mauguen A, Gouy S, Rey A, Pautier P, Lhommé C, Duvillard P, Haie-Meder C and Morice P. Prognostic factors and morbidities after completion surgery in patients undergoing initial chemoradiation therapy for locally advanced cervical cancer. Oncologist. 2010; 15(4):405-415.
5. Liu SY and Zheng PS. High aldehyde dehydrogenase activity identifies cancer stem cells in human cervical cancer. Oncotarget. 2013; 4(12):2462-2475.
6. Kumar S, Rana ML, Verma K, Singh N, Sharma AK, Mar iaAK, Dhaliwal GS, Khaira HK and Saini S. PrediQt-Cx: post treatment health related quality of life prediction model for cervical cancer patients. PLoS One. 2014; 9(2):e89851.
7. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006; 444(7117):337-342.
8. Leone S, Basso E, Polticelli F and Cozzi R. Resveratrol acts as a topoisomerase II poison in human glioma cells. Int J Cancer. 2012; 131(3):173-178.
9. Aires V, Limagne E, Cotte AK, Latruffe N, Resveratrol metabolites inhibit human metastatic colon cancer cells progression and synergize with chemotherapeutic drugs to induce cell death. Mol Nutr Food Res. 2013; 57(7):1170-1181.
10. Tang Q, Li G, Wei X, Zhang J, Chiu JF, Hasenmayer D, Zhang D and Zhang H. Resveratrol-induced apoptosis is enhanced by inhibition of autophagy in esophageal squamous cell carcinoma. Cancer Lett. 2013; 336(2):325-337.
11. Wang Q, Li H, Wang XW, Wu DC, Chen XY and Liu J. Resveratrol promotes differentiation and induces Fasindependent apoptosis of human medulloblastoma cells. Neurosci Lett. 2003; 351(2):83-86.
12. Wu ML, Li H, Yu LJ, Chen XY, Kong QY, Song X, Shu XH and Liu J. Short-term resveratrol exposure causes in vitro and in vivo growth inhibition and apoptosis of bladder cancer cells. PLoS One. 2014; 9(2):e89806.
13. Shu XH, Li H, Sun XX, Wang Q, Sun Z, Wu ML, Chen XY, Li C, Kong QY and Liu J. Metabolic patterns and biotransformation activities of resveratrol in human glioblastoma cells: relevance with therapeutic efficacies. PLoS One. 2011; 6(11):e27484.
14. Sun Z, Li H, Shu XH, Shi H, Chen XY, Kong QY, Wu ML and Liu J. Distinct sulfonation activities in resveratrolsensitive and resveratrol-insensitive human glioblastoma cells. FEBS J. 2012; 279(13):2381-2392.
15. Chung TK, Cheung TH, Lo WK, Yim SF, Yu MY, Krajewski S, Reed JC and Wong YF. Expression of apoptotic regulators and their significance in cervical cancer. Cancer Lett. 2002; 180(1):63-68.
16. Zhang P, Li H, Wu ML, Chen XY, Kong QY, Wang XW, Sun Y, Wen S and Liu J. c-Myc downregulation: a critical molecular event in resveratrol-induced cell cycle arrest and apoptosis of human medulloblastoma cells. J Neuro-oncol. 2006; 80(2):123-131.
17. Wang Q, Li H, Liu N, Chen XY, Wu ML, Zhang KL, Kong QY and Liu J. Correlative analyses of notch signaling with resveratrol-induced differentiation and apoptosis of human medulloblastoma cells. Neurosci Lett. 2008; 438(2):168-173.
18. Wen S, Li H, Wu ML, Fan SH, Wang Q, Shu XH, Kong QY, Chen XY and Liu J. Inhibition of NF-kB signaling commits resveratrol-treated medulloblastoma cells to apoptosis without neuronal differentiation. J Neuro-oncol. 2011; 104(1):169-177.
19. Plascak J, Llanos A, Pennell M, Weier R and Paskett E. Neighborhood and geographic factors associated with diagnostic resolution after an abnormal breast or cervical cancer screening test among women enrolled in a patient navigator program. Cancer Epidemiol Biomarkers Prev. 2014; 23(3):569.
20. Beller U, Quinn MA, Benedet JL, Creasman WT, Ngan HY, Maisonneuve P, Pecorelli S, Odicino F and Heintz AP. Carcinoma of the vulva. FIGO 26th annual report on the results of treatment in gynecological cancer. Int J Gynaecol Obstet. 2006; 95 Suppl 1:S7-27.
21. Kim DY, Shim SH, Kim SO, Lee SW, Park JY, Suh DS, Kim JH, Kim YM, Kim YT and Nam JH. Preoperative nomogram for the identification of lymph node metastasis in early cervical cancer. Br J Cancer. 2014; 110(1):34-41.
22. Kim HS, Kim T, Lee ES, Kim HJ, Chung HH, Kim JW, Song YS and Park NH. Impact of chemoradiation on prognosis in stage IVB cervical cancer with distant lymphatic metastasis. Cancer Res Treat. 2013; 45(3):193-201.
23. Schefter T, Winter K, Kwon JS, Stuhr K, Balaraj K, Yaremko BP, Small W, Sause W and Gaffney D. RTOG 0417: efficacy of bevacizumab in combination with definitive radiation therapy and cisplatin chemotherapy in untreated patients with locally advanced cervical carcinoma. Int J Radiat Oncol Biol Phys. 2014; 88(1):101-105.
24. Disilvestro PA, Ali S, Craighead PS, Lucci JA, Lee YC, Cohn DE, Spirtos NM, Tewari KS, Muller C, Gajewski WH, Steinhoff MM and Monk BJ. Phase III randomized trial of weekly cisplatin and irradiation versus cisplatin and tirapazamine and irradiation in stages IB2, IIA, IIB, IIIB, and IVA cervical carcinoma limited to the pelvis: a gynecologic oncology group study. J Clin Oncol. 2014; 32(5):458-464.
25. Schlumbrecht MP, Sun CC, Huang MS, Zandstra FandBodurka DC. Lifestyle modification in cervical cancer survivors: an ongoing need. Int J Gynecol Cancer. 2014; 24(3):570-575.
26. Fruscio R, Villa A, Chiari S, Vergani P, Ceppi L, Dell’Orto F, Dell’Anna T, Chiappa V, Bonazzi CM, Milani R, Mangioni C and Locatelli A. Delivery delay wit hneoadjuvant chemotherapy for cervical cancer patients during pregnancy: a series of nine cases and literature review. Gynecol Oncol. 2012; 126(2):192-197.
27. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC and Pezzuto JM. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 1997; 275(5297):218-220.
28. Zoberi I, Bradbury CM, Curry HA, Bisht KS, Goswami PC, Roti Roti JL and Gius D. Radiosensitizing and antiproliferative effects of resveratrol in two human cervical tumor cell lines. Cancer Lett. 2002; 175(2):165-173.
29. García-Zepeda SP, García-Villa E, Díaz-Chávez J, Hernández-Pando R and Gariglio P. Resveratrol induces cell death in cervical cancer cells through apoptosis and autophagy. Eur J Cancer Prev. 2013; 22(6):577-584.
30. Mémin E, Hoque M, Jain MR, Heller DS, Li H, Cracchiolo B, Hanauske-Abel HM, Pe’ery T and Mathews MB. Blocking eIF5A modification in cervical cancer cells alters the expression of cancer-related genes and suppresses cell proliferation. Cancer Res. 2014; 74(2):552-562.
31. Feng D, Wu J, Tian Y, Zhou H, Zhou Y, Hu W, Zhao W, Wei H, Ling B and Ma C. Targeting of histone deacetylases to reactivate tumour suppressor genes and its therapeutic potential in a human cervical cancer xenograft model. PLoS One. 2013; 8(11):e80657.
32. Gu W, Yeo E, McMillan N and Yu C. Silencing oncogene expression in cervical cancer stem-like cells inhibits their cell growth and self-renewal ability. Cancer Gene Ther. 2011; 18(12):897-905.
33. Iida K, Nakayama K, Rahman MT, Rahman M, Ishikawa M, Katagiri A, Yeasmin S, Otsuki Y, Kobayashi H, Nakayama S and Miyazaki K. EGFR gene amplification is related to adverse clinical outcomes in cervical squamous cell carcinoma, making the EGFR pathway a novel therapeutic target. Br J Cancer. 2011; 105(3):420-427.
34. Bajaj J, Maliekal TT, Vivien E, Pattabiraman C, Srivastava S, Krishnamurthy H, Giri V, Subramanyam D and Krishna S. Notch signaling in CD66+ cells drives the progression of human cervical cancers. Cancer Res. 2011; 71(14):4888-4897.
35. Ramachandran I, Thavathiru E, Ramalingam S, Natarajan G, Mills WK, Benbrook DM, Zuna R, Lightfoot S, Reis A, Anant and Queimado L. Wnt inhibitory factor 1 induces apoptosis and inhibits cervical cancer growth, invasion and angiogenesis in vivo. Oncogene. 2012; 31(22):2725-2737.
36. Shukla S, Shishodia G, Mahata S, Hedau S, Pandey A, Bhambhani S, Batra S, Basir SF, Das BC and Bharti AC. Aberrant expression and constitutive activation of STAT3 in cervical carcinogenesis: implications in high-risk human papillomavirus infection. Mol Cancer. 2010; 9:282.
37. Hope C, Planutis K, Planutiene M, Moyer MP, Johal KS, Woo J, Santoso C, Hanson JA and Holcombe RF. Low concentrations of resveratrol inhibit Wnt signal throughput in colon-derived cells: implications for colon cancer prevention. Mol Nutr Food Res. 2008; 52 1:S52-61.
38. Liu L, Fan Z, Tang Y and Ke Z. The resveratrol attenuates ethanol-induced hepatocyte apoptosis via inhibiting ERrelated caspase-12 activation and PDE activity in vitro. Alcohol Clin Exp Res. 2014; 38(3):683-693.
39. Zhang M, Zhou X and Zhou K. Resveratrol inhibits human nasopharyngeal carcinoma cell growth via blocking pAkt/p70S6K signaling pathways. Int J Mol Med. 2013; 31(3):621-627.
40. Yan S, Li Z and Thiele CJ. Inhibition of STAT3 with orally active JAK inhibitor, AZD1480, decreases tumor growth in neuroblastoma and pediatric sarcomas in vitro and in vivo. Oncotarget. 2013; 4(3):433-445.
41. Nelson EA, Sharma SV, Settleman J and Frank DA. A chemical biology approach to developing STAT inhibitors: molecular strategies for accelerating clinical translation. Oncotarget. 2011; 2(6):518-524.
42. Dailey DD, Anfinsen KP, Pfaff LE, Ehrhart E, Charles JB, Bønsdorff TB, Thamm DH, Powers BE, Jonasdottir TJ and Duval DL. HES1, a target of Notch signaling, is elevated in canine osteosarcoma, but reduced in the most aggressive tumors. BMC Vet Res. 2013; 9(1):130.
43. Maliekal TT, Bajaj J, Giri V, Subramanyam D and Krishna S. The role of Notch signaling in human cervical cancer: implications for solid tumors. Oncogene. 2008; 27(38):5110-5114.
44. Kwan HT, Chan DW, Cai PC, Mak CS, Yung MM, Leung TH, Wong OG, Cheung AN and Ngan HY. AMPK activators suppress cervical cancer cell growth through inhibition of DVL3 mediated Wnt/β-catenin signaling activity. PLoS One. 2013; 8(1):e53597.
45. Schröer N, Pahne J, Walch B, Wickenhauser C and Smola S. Molecular pathobiology of human cervical high-grade lesions: paracrine STAT3 activation in tumor-instructed myeloid cells drives local MMP-9 expression. Cancer Res. 2011; 71(1):87-97.
46. Kamakura S, Oishi K, Yoshimatsu T, Nakafuku M, Masuyama N and Gotoh Y. Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol. 2004; 6(6):547-554.
47. Sengupta A, Banerjee D, Chandra S, Banerji SK, Ghosh R, Roy R and Banerjee S. Deregulation and cross talk among Sonic hedgehog, Wnt, Hox and Notch signaling in chronic myeloid leukemia progression. Leukemia. 2007; 21(5):949-955.
48. Liu J, Wang Q, Wu DC, Wang XW, Sun Y, Chen XY, Zhang KL and Li H. Differential regulation of CYP1A1 and CYP1B1 expression in resveratrol-treated human medulloblastoma cells. Neurosci Lett. 2004; 363(3):257-261.
49. Araki Y, Okamura S, Hussain SP, Nagashima M, He P, Shiseki M, Miura K and Harris CC. Regulation of cyclooxygenase-2 expression by the Wnt and ras pathways. Cancer Res. 2003; 63(3):728-734.
50. Chiaramonte R, Basile A, Tassi E, Calzavara E, Cecchinato V, Rossi V, Biondi A and Comi P. A wide role for NOTCH1 signaling in acute leukemia. Cancer Lett. 2005; 219(1):113-120.
51. Walsh J and Andrews PW. Expression of Wnt and Notch pathway genes in a pluripotent human embryonal carcinoma cell line and embryonic stem cell. APMIS. 2003; 111(1):197-210.
52. Scintu F, Reali C, Pillai R, Badiali M, Sanna MA, Argiolu F, Ristaldi MS and Sogos V. Differentiation of human bone marrow stem cells into cells with a neural phenotype: diverse effects of two specific treatments. BMC Neurosci. 2006; 7:14.
53. Katoh M. Frequent up-regulation of WNT2 in primary gastric cancer and colorectal cancer. Int J Oncol. 2001; 19(5):1003-1007.
54. Saitoh T, Mine T and Katoh M. Frequent up-regulation of WNT5A mRNA in primary gastric cancer. Int J Mol Med. 2002; 9(5):515-519.
55. Ebert MP, Fei G, Kahmann S, Müller O, Yu J, Sung JJ and Malfertheiner P. Increased beta-catenin mRNA levels and mutational alterations of the APC and beta-catenin gene are present in intestinal-type gastric cancer. Carcinogenesis. 2002; 23(1):87-91.
56. Yang J, Liao X, Agarwal MK, Barnes L, Auron PE and Stark GR. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFκB. Genes Dev. 2007; 21(11):1396-1408.
57. Sonnenblick A, Levy C, Razin E. Interplay between MITF, PIAS3, and STAT3 in mast cells and melanocytes. Mol Cell Biol. 2004; 24(24):10584-10592.
58. Shearman MS, Beher D, Clarke EE, Lewis HD, Harrison T, Hunt P, Nadin A, Smith AL, Stevenson G and Castro JL. L-685,458, an aspartyl protease transition state mimic, is a potent inhibitor of amyloid beta-protein precursor gammasecretase activity. Biochemistry. 2000; 39(30):8698-8704.
59. Branam AM, Davis NM, Moore RW, Schneider AJ, Vezina CM and Peterson RE. TCDD inhibition of canonical wnt signaling disrupts prostatic bud formation in mouse urogenital sinus. Toxicol Sci. 2013; 133(1):42-53.
60. Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA and Haque SJ. Inhibition of constitutively active P-STAT3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene. 2002; 21(55):8404-8413.