Aberrant promoter methylation and loss of Suppressor of Cytokine Signalling-1 gene expression in the development of uterine cervical carcinogenesis

Cellular Oncology

Volumn 34, Issue 6, 2011, Pages 533-543

  Sobti, R C ^a   Singh, Neha ^a   Hussain, Showket ^b   Suri, Vanita ^c   Nijhawan, Raje ^c   Bharti, A C ^b   Bharadwaj, Mausumi ^b   Das, B C ^d  

^a PANJAB UNIVERSITY   (India)

^b Institute of Cytology and Preventive Oncology ICMR   (India)

^c POSTGRADUATE INSTITUTE OF MEDICAL EDUCATION AND RESEARCH   (India)

^d UNIVERSITY OF DELHI   (India)

Author keywords

Cervical cancer; HPV; Promoter methylation; SOCS 1

Indexed keywords

JANUS KINASE; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SOCS1 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING;

ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR BIOPSY; UTERINE CERVIX BIOPSY; UTERINE CERVIX CANCER; DNA METHYLATION; GENETIC PREDISPOSITION; GENETICS; IN VITRO STUDY; ISOLATION AND PURIFICATION; METABOLISM; PAPILLOMA VIRUS; PROMOTER REGION; UTERINE CERVIX TUMOR; VIROLOGY;

DNA METHYLATION; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; PAPILLOMAVIRIDAE; PROMOTER REGIONS, GENETIC; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UTERINE CERVICAL NEOPLASMS;

EID: 84861498667     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-011-0056-2     Document Type: Article

References (58)

1. D.M. Parkin, F. Bray, J. Ferlay, P. Pisani, Global cancer statistics 2002. CA Canc. J. Clin. 55, 74-108 (2005)
2. B.C. Das, S. Hussain, V. Nasare, M. Bharadwaj, Prospects and prejudices of human papillomavirus vaccines in India. Vaccine 26, 2669-2679 (2008)
3. H. zur Hausen, Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Canc. 2, 342-350 (2002)
4. R.C. Sobti, S. Kaur, P. Kaur, J. Singh, I. Gupta, V. Jain et al., Interaction of passive smoking with GST (GSTM1, GSTT1, and GSTP1) genotypes in the risk of cervical cancer in India. Canc. Genet. Cytogenet. 166, 17-23 (2006)
5. C.M. Wheeler, Advances in primary and secondary interventions for cervical cancer: human papillomavirus prophylactic vaccines and testing. Nat. Clin. Pract. Oncol. 4, 224-235 (2007) (Pubitemid 46510532)
6. A. Ferenczy, E. Franco, Persistent human papillomavirus infection and cervical neoplasia. Lancet Oncol. 3, 11-16 (2002) (Pubitemid 34121141)
7. M. Kamio, T. Yoshida, H. Ogata, T. Douchi, Y. Nagata, M. Inoue, M. Hasegawa, Y. Yonemitsu, A. Yoshimura, SOCS1 [corrected] inhibits HPV-E7-mediated transformation by inducing degradation of E7 protein. Oncogene 23, 3107-3115 (2004) (Pubitemid 38648201)
8. R.C. Sobti, N. Singh, S. Hussain, V. Suri, A.C. Bharti, B.C. Das, Overexpression of STAT-3 in HPV-mediated cervical cancer in a North Indian population. Mol. Cell. Biochem. 330, 193-199 (2009)
9. T.A. Endo, M. Masuhara, M. Yokouchi, R. Suzuki, H. Sakamoto, K. Mitsui et al., A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387, 921-924 (1997) (Pubitemid 27289595)
10. R. Starr, T.A. Willson, E.M. Viney, L.J. Murray, J.R. Rayner, B.J. Jenkins, T.J. Gonda et al., A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921 (1997) (Pubitemid 27289594)
11. A. Duenas-Gonzalez, M. Lizano, M. Candelaria, L. Cetina, C. Arce, E. Cervera, Epigenetics of cervical cancer. An overview and therapeutic perspectives. Mol. Canc. 4, 38 (2005)
12. M.K. Neyaz, R.S. Kumar, S. Hussain, S.H. Naqvi, I. Kohaar, N. Thakur et al., Effect of aberrant promoter methylation of FHITand RASSF1A genes on susceptibility to cervical cancer in a North Indian population. Biomarkers 13, 597-606 (2008)
13. I. Kuzmin, L. Liu, R. Dammann, L. Geil, E.J. Stanbridge, S.P. Wilczynski et al., Inactivation of RAS association domain family 1A gene in cervical carcinomas and the role of human papillomavirus infection. Canc. Res. 63, 1888-1893 (2003) (Pubitemid 36460854)
14. G. Narayan, H. Arias-Pulido, S. Koul, H. Vargas, F.F. Zhang, J. Villella et al., Frequent promoter methylation of CDH1, DAPK, RARB, and HIC1 genes in carcinoma of cervix uteri: its relationship to clinical outcome. Mol. Canc. 2, 24 (2003)
15. M. Esteller, J.G. Herman, Cancer as an epigenetic disease: DNA methylation and chromatin alterations in human tumours. J. Pathol. 196, 1-7 (2002)
16. S.B. Baylin, M. Esteller, M.R. Rountree, K.E. Bachman, K. Schuebel, J.G. Herman, Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet. 10, 687-692 (2001) (Pubitemid 32331576)
17. S.B. Baylin, J.G. Herman, DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends. Genet. 16, 168-174 (2000) (Pubitemid 30169152)
18. Y. Cohen, E. Merhavi-Shoham, R.B. Avraham, S. Frenkel, J. Pe'er, N. Goldenberg-Cohen, Hypermethylation of CpG island loci of multiple tumor suppressor genes in retinoblastoma. Exp. Eye. Res. 86, 201-206 (2008)
19. H. Yoshikawa, K. Matsubara, G.S. Qian, P. Jackson, J.D. Groopman, J.E. Manning et al., SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat. Genet. 28, 29-35 (2008)
20. O. Galm, H. Yoshikawa, M. Esteller, R. Osieka, J.G. Herman, SOCS-1, a negative regulator of cytokine signaling, is frequently silenced by methylation in multiple myeloma. Blood 101, 2784-2788 (2003) (Pubitemid 36857644)
21. N. Fukushima, N. Sato, F. Sahin, G.H. Su, R.H. Hruban, M. Goggins, Aberrant methylation of suppressor of cytokine signalling-1 (SOCS-1) gene in pancreatic ductal neoplasms. Br. J. Canc. 89, 338-343 (2003) (Pubitemid 36980626)
22. F.J. Huang, P.S. Steeg, J.E. Price, W.T. Chiu, P.C. Chou, K. Xie et al., Molecular basis for the critical role of suppressor of cytokine signaling-1 in melanoma brain metastasis. Canc. Res. 68, 9634-9642 (2008)
23. R. Rottapel, S. Ilangumaran, C. Neale, J. La Rose, J.M. Ho, M.H. Nguyen et al., The tumor suppressor activity of SOCS-1. Oncogene 21, 4351-62 (2002) (Pubitemid 34774838)
24. P. De Sepulveda, S. Ilangumaran, R. Rottapel, Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation. J. Biol. Chem. 275, 14005-14008 (2000) (Pubitemid 30339671)
25. K. Munger, P.M. Howley, Human papillomavirus immortalization and transformation functions. Virus. Res. 89, 213-228 (2002) (Pubitemid 35351540)
26. J. Elliott, M.B. Hookham, J.A. Johnston, The suppressors of cytokine signalling E3 ligases behave as tumour suppressors. Biochem. Soc. Trans. 36, 464-468 (2008) (Pubitemid 351839356)
27. B.C. Das, J.K. Sharma, V. Gopalakrishna, U.K. Luthra, Analysis by polymerase chain reaction of the physical state of human papillomavirus type 16 DNA in cervical preneoplastic and neoplastic lesions. J. Gen. Virol. 73, 2327-2336 (1992)
28. U. Kailash, C.C. Soundararajan, R. Lakshmy, R. Arora, S. Vivekanandhan, B.C. Das, Telomerase activity as an adjunct to high-risk human papillomavirus types 16 and 18 and cytology screening in cervical cancer. Br. J. Canc. 95, 1250-1257 (2006) (Pubitemid 44658491)
29. J. de Wilde, J. De-Castro Arce, P.J. Snijders, C.J. Meijer, F. Rosl, R.D. Steenbergen, Alterations in AP-1 and AP-1 regulatory genes during HPV-induced carcinogenesis. Cell. Oncol. 30, 77-87 (2008) (Pubitemid 351161039)
30. R.C. Sobti, N. Singh, S. Hussain, V. Suri, M. Bharadwaj, B.C. Das, Deregulation of STAT-5 isoforms in the development of HPVmediated cervical carcinogenesis. J. Recept. Signal. Transduct. Res. 30, 178-188 (2010)
31. J.D. Dignam, Preparation of extracts from higher eukaryotes. Meth. Enzymol. 182, 194-203 (1990)
32. S. Hussain, A.C. Bharti, I. Salam, M.A. Bhat, M.M. Mir, S. Hedau et al., Transcription factor AP-1 in esophageal squamous cell carcinoma: alterations in activity and expression during human Papillomavirus infection. BMC Canc. 9, 329 (2009)
33. H. Yu, M. Kortylewski, D. Pardoll, Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 7, 41-51 (2007) (Pubitemid 46020826)
34. H. Yu, R. Jove, The STATs of cancer-new molecular targets come of age. Nat. Rev. Canc. 4, 97-105 (2004) (Pubitemid 38198738)
35. J.J. Schuringa, A.T. Wierenga, W. Kruijer, E. Vellenga, Constitutive Stat3, Tyr705, and Ser727 phosphorylation in acute myeloid leukemia cells caused by the autocrine secretion of interleukin-6. Blood 95, 3765-3770 (2000) (Pubitemid 30412848)
36. T.S. Lin, S. Mahajan, D.A. Frank, STAT signaling in the pathogenesis and treatment of leukemias. Oncogene 19, 2496-2504 (2000) (Pubitemid 30339205)
37. L. Li, P.E. Shaw, Autocrine-mediated activation of STAT3 correlates with cell proliferation in breast carcinoma lines. J. Biol. Chem. 277, 17397-17405 (2002) (Pubitemid 34967539)
38. T. Komazaki, H. Nagai, M. Emi, Y. Terada, A. Yabe, E. Jin et al., Hypermethylation-associated inactivation of the SOCS-1 gene, a JAK/STAT inhibitor, in human pancreatic cancers. Jpn. J. Clin. Oncol. 34, 191-194 (2004) (Pubitemid 43102896)
39. Y. Oshimo, K. Kuraoka, H. Nakayama, Y. Kitadai, K. Yoshida, K. Chayama et al., Epigenetic inactivation of SOCS-1 by CpG island hypermethylation in human gastric carcinoma. Int. J. Canc. 112, 1003-1009 (2004) (Pubitemid 39507006)
40. A.K. Virmani, C. Muller, A. Rathi, S. Zoechbauer-Mueller, M. Mathis, A.F. Gazdar, Aberrant methylation during cervical carcinogenesis. Clin. Canc. Res. 7, 584-589 (2001) (Pubitemid 32707982)
41. J.E. Flatley, K. McNeir, L. Balasubramani, J. Tidy, E.L. Stuart, T. A. Young et al., Folate status and aberrant DNA methylation are associated with HPV infection and cervical pathogenesis. Canc. Epidemiol. Biomarkers. Prev. 18, 2782-2789 (2009)
42. A. Tanemura, A.M. Terando, M.S. Sim, A.Q. van Hoesel, M.F. de Maat, D.L. Morton et al., CpG island methylator phenotype predicts progression of malignant melanoma. Clin. Canc. Res. 15, 1801-1807 (2009)
43. O. Hatirnaz, U. Ure, C. Ar, C. Akyerli, T. Soysal, B. Ferhanoglu et al., The SOCS-1 gene methylation in chronic myeloid leukemia patients. Am. J. Hematol. 82, 729-730 (2007) (Pubitemid 47221655)
44. R. Buslei, J. Kreutzer, B. Hofmann, V. Schmidt, F. Siebzehnrubl, E. Hahnen et al., Abundant hypermethylation of SOCS-1 in clinically silent pituitary adenomas. Acta Neuropathol. 111, 264-271 (2006)
45. I. Tischoff, U.R. Hengge, M. Vieth, C. Ell, M. Stolte, A. Weber et al., Methylation of SOCS-3 and SOCS-1 in the carcinogenesis of Barrett's adenocarcinoma. Gut 56, 1047-1053 (2007) (Pubitemid 47123231)
46. J.F. Costello, M.C. Fruhwald, D.J. Smiraglia, L.J. Rush, G.P. Robertson, X. Gao et al., Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat. Genet. 24, 132-138 (2000) (Pubitemid 30094712)
47. M. Scheffner, B.A. Werness, J.M. Huibregtse, A.J. Levine, P.M. Howley, The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129-1136 (1990) (Pubitemid 120035062)
48. S.N. Boyer, D.E. Wazer, V. Band, E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Canc. Res. 56, 4620-4624 (1996) (Pubitemid 26338060)
49. B. Yang, M. Guo, J.G. Herman, D.P. Clark, Aberrant promoter methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am. J. Pathol. 163, 1101-1107 (2003) (Pubitemid 37040145)
50. H. Miyoshi, H. Fujie, Y. Shintani, T. Tsutsumi, S. Shinzawa, M. Makuuchi et al., Hepatitis C virus core protein exerts an inhibitory effect on suppressor of cytokine signaling (SOCS)-1 gene expression. J. Hepatol. 43, 757-763 (2005) (Pubitemid 41414500)
51. H. Zhou, R. Miki, M. Eeva, F.M. Fike, D. Seligson, L. Yang et al., Reciprocal regulation of SOCS 1 and SOCS3 enhances resistance to ionizing radiation in glioblastoma multiforme. Clin. Canc. Res. 13, 2344-2353 (2007) (Pubitemid 46698583)
52. T.L. Lee, J. Yeh, C. Van Waes, Z. Chen, 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. Canc. Therapeut. 5, 8-19 (2006)
53. O. Okochi, K. Hibi, M. Sakai, S. Inoue, S. Takeda, T. Kaneko, A. Nakao, Methylation-mediated silencing of SOCS-1 gene in hepatocellular carcinoma derived from cirrhosis. Clin. Canc. Res. 9, 5295-5298 (2003) (Pubitemid 37413582)
54. H. Miyoshi, H. Fujie, K. Moriya, Y. Shintani, T. Tsutsumi, M. Makuuchi et al., Methylation status of suppressor of cytokine signaling-1 gene in hepatocellular carcinoma. J. Gastroenterol. 39, 563-569 (2004) (Pubitemid 38996899)
55. S. Fujitake, K. Hibi, O. Okochi, Y. Kodera, K. Ito, S. Akiyama et al., Aberrant methylation of SOCS-1 was observed in younger colorectal cancer patients. J. Gastroenterol. 39, 120-124 (2004) (Pubitemid 38325187)
56. H. Nagai, T. Naka, Y. Terada, T. Komazaki, A. Yabe, E. Jin et al., Hypermethylation associated with inactivation of the SOCS-1 gene, a JAK/STAT inhibitor, in human hepatoblastomas. J. Hum. Genet. 48, 65-69 (2003) (Pubitemid 36305857)
57. S.Nomoto, T. Kinoshita, K. Kato,S.Otani,H.Kasuya, S. Takeda et al., Hypermethylation of multiple genes as clonal markers in multicentric hepatocellular carcinoma. Br. J. Canc. 97, 1260-1265 (2007) (Pubitemid 350035807)
58. K. Brakensiek, F. Langer, B. Schlegelberger, H. Kreipe, U. Lehmann, Hypermethylation of the suppressor of cytokine signalling-1 (SOCS-1) in myelodysplastic syndrome. Br. J. Haematol. 130, 209-217 (2005) (Pubitemid 41602521)