Inactivation of miR-34a by aberrant CpG methylation in Kazakh patients with esophageal carcinoma

Journal of Experimental and Clinical Cancer Research

Volumn 33, Issue 1, 2014, Pages

  Cui, Xiaobin ^a,b   Zhao, Zhimin ^a   Liu, Dong ^a   Guo, Tao ^a   Li, Su ^a   Hu, Jianming ^a   Liu, Chunxia ^a   Yang, Lan ^a   Cao, Yuwen ^a   Jiang, Jinfang ^a   Liang, Weihua ^a   Liu, Wei ^a   Li, Shugang ^a   Wang, Lianghai ^a   Wang, Lidong ^c   Gu, Wenyi ^d   Wu, Chuanyue ^a,e   Chen, Yunzhao ^a   Li, Feng ^a,b  

^a SHIHEZI UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c ZHENGZHOU UNIVERSITY   (China)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Esophageal squamous cell carcinoma; Kazakh; Methylation; MiR 34a

Indexed keywords

MICRORNA 34A; PROTEIN P53;

ADULT; ADVANCED CANCER; ARTICLE; CANCER PATIENT; CANCER STAGING; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; GENE EXPRESSION; GENE INACTIVATION; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; KAZAKHSTAN; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MIDDLE AGED; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION;

CARCINOMA, SQUAMOUS CELL; CASE-CONTROL STUDIES; CPG ISLANDS; DNA METHYLATION; ESOPHAGEAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENETIC ASSOCIATION STUDIES; HUMANS; KAZAKHSTAN; LYMPHATIC METASTASIS; MALE; MICRORNAS; MIDDLE AGED; PROMOTER REGIONS, GENETIC;

EID: 84896716496     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-33-20     Document Type: Article

References (45)

1. Global cancer statistics, 2002. Parkin DM, Bray F, Ferlay J, Pisani P, CA Cancer J Clin 2005 55 74 108 10.3322/canjclin.55.2.74 15761078 (Pubitemid 40372904)
2. Multiple polymorphisms within the PLCE1 are associated with esophageal cancer via promoting the gene expression in a Chinese Kazakh population. Cui XB, Chen YZ, Pang XL, Liu W, Hu JM, Li SG, Yang L, Zhang WJ, Liu CX, Cao YW, et al. Gene 2013 530 315 322 10.1016/j.gene.2013.08.057 23981775
3. Trends in morbidity and mortality for oesophageal cancer in Linxian County, 1959-1983. Lu JB, Yang WX, Liu JM, Li YS, Qin YM, Int J Cancer 1985 36 643 645 10.1002/ijc.2910360603 4066071 (Pubitemid 16211463)
4. Elevated expression patterns and tight correlation of the PLCE1 and NF-kappaB signaling in Kazakh patients with esophageal carcinoma. Cui XB, Pang XL, Li S, Jin J, Hu JM, Yang L, Liu CX, Li L, Wen SJ, Liang WH, et al. Med Oncol 2014 31 013 0791
5. HPV, KRAS mutations, alcohol consumption and tobacco smoking effects on esophageal squamous-cell carcinoma carcinogenesis. Radojicic J, Zaravinos A, Spandidos DA, Int J Biol Markers 2012 27 1 12 10.5301/JBM.2011.8737 22020370
6. Current implications of cyclophilins in human cancers. Lee J, Kim SS, J Exp Clin Cancer Res 2010 29 1756 9966
7. Risk factors and gene expression in esophageal cancer. Xu XC, Methods Mol Biol 2009 471 335 360 10.1007/978-1-59745-416-2-17 19109788
8. Molecular basis of esophageal cancer development and progression. Denlinger CE, Thompson RK, Surg Clin North Am 2012 92 1089 1103 10.1016/j.suc.2012.07.002 23026271
9. Loss of p53 in esophageal squamous cell carcinoma and the correlation with survival: analyses of gene mutations, protein expression, and loss of heterozygosity in Japanese patients. Egashira A, Morita M, Yoshida R, Saeki H, Oki E, Sadanaga N, Kakeji Y, Tsujitani S, Maehara Y, J Surg Oncol 2011 104 169 175 10.1002/jso.21920 21462189
10. Regulation of microRNAs by epigenetics and their interplay involved in cancer. Liu X, Chen X, Yu X, Tao Y, Bode AM, Dong Z, Cao Y, J Exp Clin Cancer Res 2013 32 96 10.1186/1756-9966-32-96 24261995
11. DNA Methylation status of Wnt antagonist SFRP5 can predict the response to the EGFR-tyrosine kinase inhibitor therapy in non-small cell lung cancer. Zhu J, Wang Y, Duan J, Bai H, Wang Z, Wei L, Zhao J, Zhuo M, Wang S, Yang L, et al. J Exp Clin Cancer Res 2012 31 1756 9966
12. Overexpression of DNA damage-induced 45 alpha gene contributes to esophageal squamous cell cancer by promoter hypomethylation. Wang BX, Yin BL, He B, Chen C, Zhao M, Wx Z, Xia ZK, Yz P, Jq T, Xm Z, et al. J Exp Clin Cancer Res 2012 31 1756 9966
13. Polymorphism of A133S and promoter hypermethylation in Ras association domain family 1A gene (RASSF1A) is associated with risk of esophageal and gastric cardia cancers in Chinese population from high incidence area in northern China. Zhou SL, Cui J, Fan ZM, Li XM, Li JL, Liu BC, Zhang DY, Liu HY, Zhao XK, Song X, et al. BMC Cancer 2013 13 1471 2407
14. Cohypermethylation of p14 in combination with CADM1 or DCC as a recurrence-related prognostic indicator in stage I esophageal squamous cell carcinoma. Lee E, Lee BB, Ko E, Kim Y, Han J, Shim YM, Park J, Kim DH, Cancer 2013 119 1752 1760 10.1002/cncr.27948 23310950
15. DNA Methylation profiles as predictors of recurrence in non muscle invasive bladder cancer: an MS-MLPA approach. Casadio V, Molinari C, Calistri D, Tebaldi M, Gunelli R, Serra L, Falcini F, Zingaretti C, Silvestrini R, Amadori D, et al. J Exp Clin Cancer Res 2013 32 94 10.1186/1756-9966-32-94 24252461
16. Candidate microRNA biomarkers of pancreatic ductal adenocarcinoma: meta-analysis, experimental validation and clinical significance. Ma MZ, Kong X, Weng MZ, Cheng K, Gong W, Quan ZW, Peng CH, J Exp Clin Cancer Res 2013 32 1756 9966
17. Oncomirs-microRNAs with a role in cancer. Esquela-Kerscher A, Slack FJ, Nat Rev Cancer 2006 6 259 269 10.1038/nrc1840 16557279
18. Altered miRNA expression is associated with differentiation, invasion, and metastasis of esophageal squamous cell carcinoma (ESCC) in patients from Huaian, China. Fu HL, de Wu P, Wang XF, Wang JG, Jiao F, Song LL, Xie H, Wen XY, Shan HS, Du YX, et al. Cell Biochem Biophys 2013 67 657 668 10.1007/s12013-013-9554-3 23516093
19. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, et al. Mol Cell 2007 26 745 752 10.1016/j.molcel.2007.05.010 17540599 (Pubitemid 46856245)
20. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H, Cell Cycle 2007 6 1586 1593 10.4161/cc.6.13.4436 17554199 (Pubitemid 47327945)
21. The miR-34 family in cancer and apoptosis. Hermeking H, Cell Death Differ 2010 17 193 199 10.1038/cdd.2009.56 19461653
22. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Korner H, Knyazev P, Diebold J, Hermeking H, Cell Cycle 2008 7 2591 2600 10.4161/cc.7.16.6533 18719384
23. Epigenetic inactivation of the miR-34a in hematological malignancies. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, Jin DY, Costello JF, Liang R, Carcinogenesis 2010 31 745 750 10.1093/carcin/bgq033 20118199
24. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Hu Y, Correa AM, Hoque A, Guan B, Ye F, Huang J, Swisher SG, Wu TT, Ajani JA, Xu XC, Int J Cancer 2011 128 132 143 10.1002/ijc.25330 20309880
25. Analysis of PTEN methylation patterns in soft tissue sarcomas by MassARRAY spectrometry. Yin L, Cai WJ, Liu CX, Chen YZ, Hu JM, Jiang JF, Li HA, Cui XB, Chang XY, Zhang WJ, et al. PLoS One 2013 8 62971 10.1371/journal.pone. 0062971 23690972
26. miR-34 miRNAs provide a barrier for somatic cell reprogramming. Choi YJ, Lin CP, Ho JJ, He X, Okada N, Bu P, Zhong Y, Kim SY, Bennett MJ, Chen C, et al. Nat Cell Biol 2011 13 1353 1360 10.1038/ncb2366 22020437
27. miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Gallardo E, Navarro A, Vinolas N, Marrades RM, Diaz T, Gel B, Quera A, Bandres E, Garcia-Foncillas J, Ramirez J, et al. Carcinogenesis 2009 30 1903 1909 10.1093/carcin/bgp219 19736307
28. Dysregulation of miR-31 and miR-21 induced by zinc deficiency promotes esophageal cancer. Alder H, Taccioli C, Chen H, Jiang Y, Smalley KJ, Fadda P, Ozer HG, Huebner K, Farber JL, Croce CM, et al. Carcinogenesis 2012 33 1736 1744 10.1093/carcin/bgs204 22689922
29. MicroRNA-1322 regulates ECRG2 allele specifically and acts as a potential biomarker in patients with esophageal squamous cell carcinoma. Zhang T, Zhao D, Wang Q, Yu X, Cui Y, Guo L, Lu SH, Mol Carcinog 2013 52 581 590 10.1002/mc.21880 22315007
30. CpG island methylation status of miRNAs in esophageal squamous cell carcinoma. Chen X, Hu H, Guan X, Xiong G, Wang Y, Wang K, Li J, Xu X, Yang K, Bai Y, Int J Cancer 2012 130 1607 1613 10.1002/ijc.26171 21547903
31. DNA methylation: a mechanism for embedding early life experiences in the genome. Szyf M, Bick J, Child Dev 2013 84 49 57 10.1111/j.1467-8624.2012.01793.x 22880724
32. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Vogt M, Munding J, Gruner M, Liffers ST, Verdoodt B, Hauk J, Steinstraesser L, Tannapfel A, Hermeking H, Virchows Arch 2011 458 313 322 10.1007/s00428-010-1030-5 21225432
33. Genetic variations in esophageal cancer risk and prognosis. Cheung WY, Liu G, Gastroenterol Clin North Am 2009 38 75 91 viii 10.1016/j.gtc.2009.01.009 19327568
34. Epidemiology of esophageal cancer: Orient to Occident. Effects of chronology, geography and ethnicity. Hongo M, Nagasaki Y, Shoji T, J Gastroenterol Hepatol 2009 24 729 735 10.1111/j.1440-1746.2009.05824.x 19646015
35. Overexpression of PLCE1 in Kazakh esophageal squamous cell carcinoma: implications in cancer metastasis and aggressiveness. Chen YZ, Cui XB, Hu JM, Zhang WJ, Li SG, Yang L, Shen XH, Liu CX, Pan QF, Yu SY, et al. APMIS 2013 121 908 918 10.1111/apm.12095 23659763
36. Heterozygote of PLCE1 rs2274223 increases susceptibility to human papillomavirus infection in patients with esophageal carcinoma among the Kazakh populations. Cui X, Chen Y, Liu L, Li L, Hu J, Yang L, Liang W, Li F, J Med Virol 2014 86 608 617 10.1002/jmv.23775 24127316
37. MicroRNA-34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1. Yang S, Li Y, Gao J, Zhang T, Li S, Luo A, Chen H, Ding F, Wang X, Liu Z, Oncogene 2013 32 4294 4303 10.1038/onc.2012.432 23001043
38. miR-34a inhibits the metastasis of osteosarcoma cells by repressing the expression of CD44. Zhao H, Ma B, Wang Y, Han T, Zheng L, Sun C, Liu T, Zhang Y, Qiu X, Fan Q, Oncol Rep 2013 29 1027 1036 23314380
39. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, Oren M, Mol Cell 2007 26 731 743 10.1016/j.molcel.2007. 05.017 17540598 (Pubitemid 46856247)
40. A microRNA component of the p53 tumour suppressor network. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, et al. Nature 2007 447 1130 1134 10.1038/nature05939 17554337 (Pubitemid 47014436)
41. miR-34a as part of the resistance network in chronic lymphocytic leukemia. Zenz T, Mohr J, Eldering E, Kater AP, Buhler A, Kienle D, Winkler D, Durig J, van Oers MH, Mertens D, et al. Blood 2009 113 3801 3808 10.1182/blood-2008-08-172254 18941118
42. Frequent downregulation of miR-34 family in human ovarian cancers. Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK, Kamat AA, Sood AK, Ellenson LH, Hermeking H, et al. Clin Cancer Res 2010 16 1119 1128 10.1158/1078-0432.CCR-09-2642 20145172
43. Reduced levels of miR-34a in neuroblastoma are not caused by mutations in the TP53 binding site. Feinberg-Gorenshtein G, Avigad S, Jeison M, Halevy-Berco G, Mardoukh J, Luria D, Ash S, Steinberg R, Weizman A, Yaniv I, Genes Chromosomes Cancer 2009 48 539 543 10.1002/gcc.20662 19373781
44. Frequent methylation and oncogenic role of microRNA-34b/c in small-cell lung cancer. Tanaka N, Toyooka S, Soh J, Kubo T, Yamamoto H, Maki Y, Muraoka T, Shien K, Furukawa M, Ueno T, et al. Lung Cancer 2012 76 32 38 10.1016/j.lungcan.2011.10.002 22047961
45. A microRNA DNA methylation signature for human cancer metastasis. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ, et al. Proc Natl Acad Sci U S A 2008 105 13556 13561 10.1073/pnas.0803055105 18768788