Tumor suppression by miR-31 in esophageal carcinoma is p21- dependent

Genes and Cancer

Volumn 5, Issue 11-12, 2014, Pages 436-444

  Ning, Zhifeng ^a,b,c   Zhu, Hua ^d   Li, Feifei ^b,c   Liu, Qing ^b,c   Liu, Gefei ^c   Tan, Tao ^d   Zhang, Bo ^d   Chen, Shaobin ^b   Li, Guanwu ^c   Huang, Dongyang ^c   Meltzer, Stephen J ^e   Zhang, Hao ^b,c  

^a HUBEI UNIVERSITY   (China)

^b CANCER HOSPITAL OF SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^c SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^d OHIO STATE UNIVERSITY   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Esophageal squamous cell cancer; MicroRNA; MiR 31; P21; Personalized medicine

Indexed keywords

MICRORNA 31; PROTEIN P21; PROTEIN P53; SHORT HAIRPIN RNA; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL INVASION ASSAY; CLINICAL ARTICLE; COLONY FORMATION; CONTROLLED STUDY; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MTT ASSAY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SQUAMOUS CELL CARCINOMA CELL LINE; WESTERN BLOTTING;

EID: 84943592502     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. S. B. Umar, D. E. Fleischer, Esophageal cancer: epidemiology, pathogenesis and prevention. Nature Clinical Practice Gastroenterology & Hepatology 5, 517 (2008).
2. A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, D. Forman, Global cancer statistics. CA: a cancer journal for clinicians 61, 69 (2011).
3. Y. Feng, C. Ke, Q. Tang, H. Dong, X. Zheng, W. Lin et al., Metformin promotes autophagy and apoptosis in esophageal squamous cell carcinoma by downregulating Stat3 signaling. Cell Death Dis 5, e1088 (2014).
4. P. C. Enzinger, R. J. Mayer, Esophageal cancer. New England Journal of Medicine 349, 2241 (2003).
5. T. Lerut, W. Coosemans, G. Decker, P. De Leyn, P. Nafteux, D. Van Raemdonck, Cancer of the esophagus and gastroesophageal junction: potentially curative therapies. Surgical oncology 10, 113 (2001).
6. H. Zhang, W. Lin, K. Kannan, L. Luo, J. Li, P. W. Chao et al., Aberrant chimeric RNA GOLM1-MAK10 encoding a secreted fusion protein as a molecular signature for human esophageal squamous cell carcinoma. Oncotarget 4, 2135 (2013).
7. Z. Guohong, S. Min, W. DuenMei, H. Songnian, L. Min, L. Jinsong et al., Genetic heterogeneity of oesophageal cancer in high-incidence areas of southern and northern China. PloS one 5, e9668 (2010).
8. Y.-J. You, Y.-P. Chen, X.-X. Zheng, S. J. Meltzer, H. Zhang, Aberrant methylation of the PTPRO gene in peripheral blood as a potential biomarker in esophageal squamous cell carcinoma patients. Cancer Lett 315, 138 (2012).
9. Q. Tang, G. Li, X. Wei, J. Zhang, J. F. Chiu, D. Hasenmayer et al., Resveratrol-induced apoptosis is enhanced by inhibition of autophagy in esophageal squamous cell carcinoma. Cancer Lett 336, 325 (2013).
10. Y. Hu, A. M. Correa, A. Hoque, B. Guan, F. Ye, J. Huang et al., Prognostic significance of differentially expressed miRNAs in esophageal cancer. International journal of cancer 128, 132 (2011).
11. C. J. Creighton, M. D. Fountain, Z. Yu, A. K. Nagaraja, H. Zhu, M. Khan et al., Molecular profiling uncovers a p53-associated role for microRNA-31 in inhibiting the proliferation of serous ovarian carcinomas and other cancers. Cancer research 70, 1906 (2010).
12. S. Valastyan, A. Chang, N. Benaich, F. Reinhardt, R. A. Weinberg, Activation of miR-31 function in alreadyestablished metastases elicits metastatic regression. Genes & development 25, 646 (2011).
13. O. Aprelikova, X. Yu, J. Palla, B.-R. Wei, S. John, M. Yi et al., The role of miR-31 and its target gene SATB2 in cancerassociated fibroblasts. Cell Cycle 9, 4387 (2010).
14. P.-C. Lin, Y.-L. Chiu, S. Banerjee, K. Park, J. M. Mosquera, E. Giannopoulou et al., Epigenetic repression of miR-31 disrupts androgen receptor homeostasis and contributes to prostate cancer progression. Cancer research 73, 1232 (2013).
15. D. Sun, F. Yu, Y. Ma, R. Zhao, X. Chen, J. Zhu et al., MicroRNA-31 activates the Ras pathway and functions as an oncogenic microRNA in human colorectal cancer by repressing RAS p21 GTPase activating protein 1 (RASA1). Journal of Biological Chemistry 288, 9508 (2013).
16. Y.-H. Tsai, M.-F. Wu, Y.-H. Wu, S.-J. Chang, S.-F. Lin, T. V. Sharp et al., The M type K15 protein of Kaposi’s sarcomaassociated herpesvirus regulates microRNA expression via its SH2-binding motif to induce cell migration and invasion. Journal of virology 83, 622 (2009).
17. S. G. Liu, X. G. Qin, B. S. Zhao, B. Qi, W. J. Yao, T. Y. Wang et al., Differential expression of miRNAs in esophageal cancer tissue. Oncol Lett 5, 1639 (2013).
18. T. Zhang, Q. Wang, D. Zhao, Y. Cui, B. Cao, L. Guo et al., The oncogenetic role of microRNA-31 as a potential biomarker in oesophageal squamous cell carcinoma. Clin Sci (Lond) 121, 437 (2011).
19. N. Lynam-Lennon, J. V. Reynolds, L. Marignol, O. M. Sheils, G. P. Pidgeon, S. G. Maher, MicroRNA-31 modulates tumour sensitivity to radiation in oesophageal adenocarcinoma. J Mol Med (Berl) 90, 1449 (2012).
20. B. S. Zhao, S. G. Liu, T. Y. Wang, Y. H. Ji, B. Qi, Y. P. Tao et al., Screening of microRNA in patients with esophageal cancer at same tumor node metastasis stage with different prognoses. Asian Pac J Cancer Prev 14, 139 (2013).
21. Y. Yang, R. S. Tarapore, M. H. Jarmel, M.-P. Tetreault, J. P. Katz, p53 mutation alters the effect of the esophageal tumor suppressor KLF5 on keratinocyte proliferation. Cell Cycle 11, 4033 (2012).
22. S. Komatsu, I. Imoto, H. Tsuda, K. I. Kozaki, T. Muramatsu, Y. Shimada et al., Overexpression of SMYD2 relates to tumor cell proliferation and malignant outcome of esophageal squamous cell carcinoma. Carcinogenesis 30, 1139 (2009).
23. C. Barnas, G. Martel-Planche, Y. Furukawa, M. Hollstein, R. Montesano, P. Hainaut, Inactivation of the p53 protein in cell lines derived from human esophageal cancers. International journal of cancer 71, 79 (1997).
24. N. Xu, F. Meisgen, L. M. Butler, G. Han, X.-J. Wang, C. Söderberg-Nauclér et al., MicroRNA-31 Is overexpressed in psoriasis and modulates inflammatory cytokine and chemokine production in keratinocytes via targeting serine/ threonine kinase 40. The Journal of Immunology 190, 678 (2013).
25. S. Valastyan, F. Reinhardt, N. Benaich, D. Calogrias, A. M. Szász, Z. C. Wang et al., A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137, 1032 (2009).
26. B. P. Zhou, Y. Liao, W. Xia, B. Spohn, M.-H. Lee, M.-C. Hung, Cytoplasmic localization of p21Cip1/WAF1 by Aktinduced phosphorylation in HER-2/neu-overexpressing cells. Nat Cell Biol 3, 245 (2001).
27. B.-D. Chang, K. Watanabe, E. V. Broude, J. Fang, J. C. Poole, T. V. Kalinichenko et al., Effects of p21Waf1/ Cip1/Sdi1 on cellular gene expression: implications for carcinogenesis, senescence, and age-related diseases. Proceedings of the National Academy of Sciences 97, 4291 (2000).
28. Y. Cang, J. Zhang, S. A. Nicholas, A. L. Kim, P. Zhou, S. P. Goff, DDB1 is essential for genomic stability in developing epidermis. Proceedings of the National Academy of Sciences 104, 2733 (2007).
29. T. Abbas, A. Dutta, p21 in cancer: intricate ne tworks and multiple activities.Nat Rev Cancer 9, 400 (2009).
30. Waf1/Cip1/Sdi1: association with cell senescence and tumour-promoting activities of stromal fibroblasts. Cancer Lett 179, 1 (2002).
31. A. L. Gartel, Is p21 an oncogene? Mol Cancer Ther 5, 1385 (2006).
32. G. Baretton, U. Klenk, J. Diebold, N. Schmeller, U. Löhrs, Proliferation-and apoptosis-associated factors in advanced prostatic carcinomas before and after androgen deprivation therapy: prognostic significance of p21/WAF1/CIP1 expression. Br J Cancer 80, 546 (1999).
33. S. Aaltomaa, P. Lipponen, M. Eskelinen, M. Ala-Opas, V. Kosma, Prognostic value and expression of p21 (waf1/cip1) protein in prostate cancer. Prostate 39, 8 (1999).
34. G. Ferrandina, A. Stoler, A. Fagotti, F. Fanfani, R. Sacco, A. De Pasqua et al., p21WAF1/CIP1 protein expression in primary ovarian cancer. Int J Oncol 17, 1231 (2000).
35. T. H. Cheung, K. W. Lo, M. M. Yu, S. F. Yim, C. S. Poon, T. K. Chung et al., Aberrant expression of p21(WAF1/CIP1) and p27(KIP1) in cervical carcinoma. Cancer Lett 172, 93 (2001).
36. C. Ceccarelli, D. Santini, P. Chieco, C. Lanciotti, M. Taffurelli, G. Paladini et al., Quantitative p21WAF - 1/p53 immunohistochemical analysis defines groups of primary invasive breast carcinomas with different prognostic indicators. International journal of cancer 95, 128 (2001).
37. M. Sarbia, H. E. Gabbert, Modern pathology: prognostic parameters in squamous cell carcinoma of the esophagus. Recent Results Cancer Res 155, 15 (2000).
38. J. M. Jung, J. M. Bruner, S. Ruan, L. A. Langford, A. P. Kyritsis, T. Kobayashi et al., Increased levels of p21WAF1/ Cip1 in human brain tumors. Oncogene 11, 2021 (1995).
39. Q. Qi, H. Zhang, W. Xu, Z. Chen, L. Wang, X. Dong et al., p21 Waf1/Cip1 polymorphisms and risk of esophageal cancer. Ann Surg Oncol 17, 1453 (2010).
40. M. Noushin Taghavi, M. Masoud Sotoudeh, N. Taghavi, F. Biramijamal, M. R. Abbaszadegan, H. Khademi et al., P21 (waf1/cip1) gene polymorphisms and possible interaction with cigarette smoking in esophageal squamous cell carcinoma in northeastern Iran: a preliminary study. Arch Iran Med 13, 235 (2010).
41. M. Shiohara, W. S. el-Deiry, M. Wada, T. Nakamaki, S. Takeuchi, R. Yang et al., Absence of WAF1 mutations in a variety of human malignancies. Blood 84, 3781 (1994).
42. M. J. Garnett, E. J. Edelman, S. J. Heidorn, C. D. Greenman, A. Dastur, K. W. Lau et al., Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 483, 570 (2012).
43. N. Hu, C. Wang, D. Ng, R. Clifford, H. H. Yang, Z. Z. Tang et al., Genomic characterization of esophageal squamous cell carcinoma from a high-risk population in China. Cancer Res 69, 5908 (2009).
44. J. Barretina, G. Caponigro, N. Stransky, K. Venkatesan, A. A. Margolin, S. Kim et al., The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603 (2012).
45. D.-Q. Li, S. B. Pakala, S. D. N. Reddy, K. Ohshiro, S.-H. Peng, Y. Lian et al., Revelation of p53-independent Function of MTA1 in DNA Damage Response via Modulation of the p21WAF1-Proliferating Cell Nuclear Antigen Pathway. Journal of Biological Chemistry 285, 10044 (2010).
46. A. L. Gartel, F. Najmabadi, E. Goufman, A. L. Tyner, A role for E2F1 in Ras activation of p21 (WAF1/CIP1) transcription. Oncogene 19, 961 (2000).
47. A. L. Gartel, A. L. Tyner, Transcriptional regulation of the p21((WAF1/CIP1)) gene. Exp Cell Res 246, 280 (1999).
48. H. Dong, H. Guo, L. Xie, G. Wang, X. Zhong, T. Khoury et al., The metastasis-associated gene MTA3, a component of the Mi-2/NuRD transcriptional repression complex, predicts prognosis of gastroesophageal junction adenocarcinoma. PloS one 8, e62986 (2013).