DNA methylation reactivates GAD1 expression in cancer by preventing CTCF-mediated polycomb repressive complex 2 recruitment

Oncogene

Volumn 35, Issue 30, 2016, Pages 3995-4008

  Yan, H ^a   Tang, G ^b   Wang, H ^a   Hao, L ^a   He, T ^a   Sun, X ^a   Ting, A H ^c   Deng, A ^a   Sun, S ^b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID DECARBOXYLASE 1; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; CCCTC-BINDING FACTOR; GLUTAMATE DECARBOXYLASE 1; MESSENGER RNA; REPRESSOR PROTEIN; SUZ12 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; BINDING SITE; CANCER CELL; CANCER GROWTH; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; EPITHELIUM CELL; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; GENETIC TRANSCRIPTION; HCT116 CELL LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LIVER CANCER CELL LINE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SEQUENCE ANALYSIS; SMMC7721 CANCER CELL LINE; SW480 CANCER CELL LINE; THLE 3 CANCER CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; DNA METHYLATION; GLUTAMATE DECARBOXYLASE; HUMANS; NEOPLASMS; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; RNA, MESSENGER;

EID: 84980004961     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.423     Document Type: Article

References (50)

1. Joh TH, Baetge EE, Ross ME, Lai CY, Docherty M, Bradford H et al. Genes for neurotransmitter synthesis, storage, and uptake. Fed Proc 1985; 44: 2773-2779.
2. Matuszek M, Jesipowicz M, Kleinrok Z. GABA content and GAD activity in gastric cancer. Med Sci Monit 2001; 7: 377-381.
3. Kimura R, Kasamatsu A, Koyama T, Fukumoto C, Kouzu Y, Higo M et al. Glutamate acid decarboxylase 1 promotes metastasis of human oral cancer by beta-catenin translocation and MMP7 activation. BMC Cancer 2013; 13: 555.
4. Maemura K, Yamauchi H, Hayasaki H, Kanbara K, Tamayama T, Hirata I et al. Gamma-amino-butyric acid immunoreactivity in intramucosal colonic tumors. J Gastroenterol Hepatol 2003; 18: 1089-1094.
5. Azuma H, Inamoto T, Sakamoto T, Kiyama S, Ubai T, Shinohara Y et al. Gammaaminobutyric acid as a promoting factor of cancer metastasis; induction of matrix metalloproteinase production is potentially its underlying mechanism. Cancer Res 2003; 63: 8090-8096.
6. Jaraj SJ, Augsten M, Haggarth L, Wester K, Ponten F, Ostman A et al. GAD1 is a biomarker for benign and malignant prostatic tissue. Scand J Urol Nephrol 2011; 45: 39-45.
7. Li CM, Kim CE, Margolin AA, Guo M, Zhu J, Mason JM et al. CTNNB1 mutations and overexpression of Wnt/beta-catenin target genes in WT1-mutant Wilms' tumors. Am J Pathol 2004; 165: 1943-1953.
8. Jorissen RN, Lipton L, Gibbs P, Chapman M, Desai J, Jones IT et al. DNA copynumber alterations underlie gene expression differences between microsatellite stable and unstable colorectal cancers. Clin Cancer Res 2008; 14: 8061-8069.
9. Andang M, Hjerling-Leffler J, Moliner A, Lundgren TK, Castelo-Branco G, Nanou E et al. Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation. Nature 2008; 451: 460-464.
10. Huerta S, Harris DM, Jazirehi A, Bonavida B, Elashoff D, Livingston EH et al. Gene expression profile of metastatic colon cancer cells resistant to cisplatin-induced apoptosis. Int J Oncol 2003; 22: 663-670.
11. Xu Y, Hu B, Choi AJ, Gopalan B, Lee BH, Kalady MF et al. Unique DNA methylome profiles in CpG island methylator phenotype colon cancers. Genome Res 2012; 22: 283-291.
12. Razin A, Riggs AD. DNA methylation and gene function. Science 1980; 210: 604-610.
13. Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science 1975; 187: 226-232.
14. Bird A. Perceptions of epigenetics. Nature 2007; 447: 396-398.
15. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 2006; 38: 1378-1385.
16. Gius D, Cui H, Bradbury CM, Cook J, Smart DK, Zhao S et al. Distinct effects on gene expression of chemical and genetic manipulation of the cancer epigenome revealed by a multimodality approach. Cancer Cell 2004; 6: 361-371.
17. Lai AY, Fatemi M, Dhasarathy A, Malone C, Sobol SE, Geigerman C et al. DNA methylation prevents CTCF-mediated silencing of the oncogene BCL6 in B cell lymphomas. J Exp Med 2010; 207: 1939-1950.
18. Renaud S, Loukinov D, Abdullaev Z, Guilleret I, Bosman FT, Lobanenkov V et al. Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene. Nucleic Acids Res 2007; 35: 1245-1256.
19. Huang HS, Akbarian S. GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with schizophrenia. PloS One 2007; 2: e809.
20. Ha M, Ng DW, Li WH, Chen ZJ. Coordinated histone modifications are associated with gene expression variation within and between species. Genome Res 2011; 21: 590-598.
21. Kim BN, Yamamoto H, Ikeda K, Damdinsuren B, Sugita Y, Ngan CY et al. Methylation and expression of p16INK4 tumor suppressor gene in primary colorectal cancer tissues. Int J Oncol 2005; 26: 1217-1226.
22. Zhang J, Tsoi H, Li X, Wang H, Gao J, Wang K et al. Carbonic anhydrase IV inhibits colon cancer development by inhibiting the Wnt signalling pathway through targeting the WTAP-WT1-TBL1 axis. Gut 2015; e-pub ahead of print 12 June 2015; doi:10.1136/gutjnl-2014-308614.
23. Bell AC, Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000; 405: 482-485.
24. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000; 405: 486-489.
25. Euskirchen GM, Rozowsky JS, Wei CL, Lee WH, Zhang ZD, Hartman S et al. Mapping of transcription factor binding regions in mammalian cells by ChIP: comparison of array-and sequencing-based technologies. Genome Res 2007; 17: 898-909.
26. Rago C, Vogelstein B, Bunz F. Genetic knockouts and knockins in human somatic cells. Nat Protoc 2007; 2: 2734-2746.
27. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007; 128: 735-745.
28. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 2004; 23: 4061-4071.
29. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S et al. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Mol Cell Biol 2008; 28: 6473-6482.
30. Kobayashi T, Ebihara S, Ishii K, Kobayashi T, Nishijima M, Endo S et al. Structural and functional characterization of mouse glutamate decarboxylase 67 gene promoter. Biochim Biophys Acta 2003; 1628: 156-168.
31. Catalano V, Loupakis F, Graziano F, Torresi U, Bisonni R, Mari D et al. Mucinous histology predicts for poor response rate and overall survival of patients with colorectal cancer and treated with first-line oxaliplatin-and/or irinotecan-based chemotherapy. Br J Cancer 2009; 100: 881-887.
32. Cotter PD, Gahan CG, Hill C. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol Microbiol 2001; 40: 465-475.
33. Labrador M, Corces VG. Setting the boundaries of chromatin domains and nuclear organization. Cell 2002; 111: 151-154.
34. West AG, Huang S, Gaszner M, Litt MD, Felsenfeld G. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol Cell 2004; 16: 453-463.
35. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 2009; 137: 1194-1211.
36. Ren L, Wang Y, Shi M, Wang X, Yang Z, Zhao Z. CTCF mediates the cell-type specific spatial organization of the Kcnq5 locus and the local gene regulation. PloS One 2012; 7: e31416.
37. Rodriguez C, Borgel J, Court F, Cathala G, Forne T, Piette J. CTCF is a DNA methylation-sensitive positive regulator of the INK/ARF locus. Biochem Biophys Res Commun 2010; 392: 129-134.
38. Nozoe T, Anai H, Nasu S, Sugimachi K. Clinicopathological characteristics of mucinous carcinoma of the colon and rectum. J Surg Oncol 2000; 75: 103-107.
39. Du W, Mah JT, Lee J, Sankila R, Sankaranarayanan R, Chia KS. Incidence and survival of mucinous adenocarcinoma of the colorectum: a population-based study from an Asian country. Dis Colon Rectum 2004; 47: 78-85.
40. Negri FV, Wotherspoon A, Cunningham D, Norman AR, Chong G, Ross PJ. Mucinous histology predicts for reduced fluorouracil responsiveness and survival in advanced colorectal cancer. Ann Oncol 2005; 16: 1305-1310.
41. Maisano R, Azzarello D, Maisano M, Mafodda A, Bottari M, Egitto G et al. Mucinous histology of colon cancer predicts poor outcomes with FOLFOX regimen in metastatic colon cancer. J Chemother 2012; 24: 212-216.
42. Xiang YY, Wang S, Liu M, Hirota JA, Li J, Ju W et al. A GABAergic system in airway epithelium is essential for mucus overproduction in asthma. Nat Med 2007; 13: 862-867.
43. Fu XW, Wood K, Spindel ER. Prenatal nicotine exposure increases GABA signaling and mucin expression in airway epithelium. Am J Respir Cell Mol Biol 2011; 44: 222-229.
44. Leopoldo S, Lorena B, Cinzia A, Gabriella DC, Angela Luciana B, Renato C et al. Two subtypes of mucinous adenocarcinoma of the colorectum: clinicopathological and genetic features. Ann Surg Ocol 2008; 15: 1429-1439.
45. Gatenby RA, Gawlinski ET, Gmitro AF, Kaylor B, Gillies RJ. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 2006; 66: 5216-5223.
46. Hernandez A. Proton dynamics in cancer. Curr Pharm Des 2012; 18: 1317-1318.
47. Stuhmer T, Puelles L, Ekker M, Rubenstein JL. Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 2002; 12: 75-85.
48. Yan HL, Xue G, Mei Q, Wang YZ, Ding FX, Liu MF et al. Repression of the miR-17-92 cluster by p53 has an important function in hypoxia-induced apoptosis. EMBO J 2009; 28: 2719-2732.
49. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science 2002; 295: 1306-1311.
50. Wang Z. Epitope tagging of endogenous proteins for genome-wide chromatin immunoprecipitation analysis. Methods Mol Biol 2009; 567: 87-98.