Lineage-specific RUNX3 hypomethylation marks the preneoplastic immune component of gastric cancer

Oncogene

Volumn 34, Issue 22, 2015, Pages 2856-2866

  Kurklu, B ^a,b   Whitehead, R H ^b   Ong, E K ^a   Minamoto, T ^c   Fox, J G ^d   Mann, J R ^a,b   Judd, L M ^a,b   Giraud, A S ^a,b   Menheniott, T R ^a,b  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c KANAZAWA UNIVERSITY   (Japan)

^d Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR RUNX3; RUNX3 PROTEIN, HUMAN;

AMPLICON; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BYSTANDER EFFECT; CD8+ T LYMPHOCYTE; CELL IMMORTALIZATION; CELL SELECTION; CONTROLLED STUDY; CPG ISLAND; DENDRITIC CELL; DNA METHYLATION; EPIGENETICS; EXON; GASTRITIS; GENE MAPPING; GENETIC CONSERVATION; GENETIC MODEL; GENETIC REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTESTINE METAPLASIA; INTRON; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; ONCOGENE; PRECANCER; PRIORITY JOURNAL; PROMOTER REGION; RUNX3 GENE; SPLEEN CELL; STOMACH CANCER; STOMACH CARCINOGENESIS; STOMACH EPITHELIUM; TUMOR MICROENVIRONMENT; ANIMAL; ANTIBODY SPECIFICITY; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CELL LINEAGE; CELL TRANSFORMATION; GASTRIC MUCOSA; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; STOMACH TUMOR; TRANSGENIC MOUSE;

ANIMALS; CELL LINEAGE; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 3 SUBUNIT; CPG ISLANDS; DNA METHYLATION; GASTRIC MUCOSA; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN SPECIFICITY; PRECANCEROUS CONDITIONS; PROMOTER REGIONS, GENETIC; STOMACH NEOPLASMS;

EID: 84922209347     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.233     Document Type: Article

References (53)

1. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. International Agency for Research on Cancer: Lyon, France, 2013.
2. Yeoh KG. How do we improve outcomes for gastric cancer? J Gastroenterol Hepatol 2007; 22: 970-972.
3. Correa P, Haenszel W, Cuello C, Tannenbaum S, Archer M. A model for gastric cancer epidemiology. Lancet 1975; 2: 58-60.
4. Schier S, Wright NA. Stem cell relationships and the origin of gastrointestinal cancer. Oncology 2005; 69(Suppl 1): 9-13.
5. Hoffmann W. Self-renewal of the gastric epithelium from stem and progenitor cells. Front Biosci (Schol Ed) 2013; 5: 720-731.
6. Peterson AJ, Menheniott TR, O'Connor L, Walduck AK, Fox JG, Kawakami K et al. Helicobacter pylori infection promotes methylation and silencing of trefoil factor 2, leading to gastric tumor development in mice and humans. Gastroenterology 2010; 139: 2005-2017.
7. Schmid CA, Muller A. FoxD3 is a novel, epigenetically regulated tumor suppressor in gastric carcinogenesis. Gastroenterology 2013; 144: 22-25.
8. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21: 5400-5413.
9. Clark SJ, Melki J. DNA methylation and gene silencing in cancer: which is the guilty party? Oncogene 2002; 21: 5380-5387.
10. Sproul D, Nestor C, Culley J, Dickson JH, Dixon JM, Harrison DJ et al. Transcriptionally repressed genes become aberrantly methylated and distinguish tumors of different lineages in breast cancer. Proc Natl Acad Sci USA 2011; 108: 4364-4369.
11. Dedeurwaerder S, Fuks F. DNA methylation markers for breast cancer prognosis: unmasking the immune component. Oncoimmunology 2012; 1: 962-964.
12. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007; 39: 457-466.
13. Schmidl C, Klug M, Boeld TJ, Andreesen R, Hoffmann P, Edinger M et al. Lineagespecific DNA methylation in T cells correlates with histone methylation and enhancer activity. Genome Res 2009; 19: 1165-1174.
14. Dedeurwaerder S, Desmedt C, Calonne E, Singhal SK, Haibe-Kains B, Defrance M et al. DNA methylation profiling reveals a predominant immune component in breast cancers. EMBO Mol Med 2011; 3: 726-741.
15. Hu M, Yao J, Cai L, Bachman KE, van den Brule F, Velculescu V et al. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 2005; 37: 899-905.
16. Westendorf JJ, Hiebert SW. Mammalian runt-domain proteins and their roles in hematopoiesis, osteogenesis, and leukemia. J Cell Biochem 1999; (Suppl 32-33): 51-58.
17. Lian JB, Javed A, Zaidi SK, Lengner C, Montecino M, van Wijnen AJ et al. Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors. Crit Rev Eukaryot Gene Expr 2004; 14: 1-41.
18. Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R et al. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 2002; 21: 3454-3463.
19. Woolf E, Xiao C, Fainaru O, Lotem J, Rosen D, Negreanu V et al. Runx3 and Runx1 are required for CD8 T cell development during thymopoiesis. Proc Natl Acad Sci USA 2003; 100: 7731-7736.
20. Taniuchi I, Osato M, Egawa T, Sunshine MJ, Bae SC, Komori T et al. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 2002; 111: 621-633.
21. Fainaru O, Woolf E, Lotem J, Yarmus M, Brenner O, Goldenberg D et al. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J 2004; 23: 969-979.
22. Lai CB, Mager DL. Role of runt-related transcription factor 3 (RUNX3) in transcription regulation of natural cytotoxicity receptor 1 (NCR1/NKp46), an activating natural killer (NK) cell receptor. J Biol Chem 2012; 287: 7324-7334.
23. Levanon D, Negreanu V, Lotem J, Bone KR, Brenner O, Leshkowitz D et al. Runx3 regulates interleukin-15 dependent natural killer cell activation. Mol Cell Biol 2014; 34: 1158-1169.
24. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ et al. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 2002; 109: 113-124.
25. Fan XY, Hu XL, Han TM, Wang NN, Zhu YM, Hu W et al. Association between RUNX3 promoter methylation and gastric cancer: a meta-analysis. BMC Gastroenterol 2011; 11: 92.
26. Subramaniam MM, Chan JY, Yeoh KG, Quek T, Ito K, Salto-Tellez M. Molecular pathology of RUNX3 in human carcinogenesis. Biochim Biophys Acta 2009; 1796: 315-331.
27. Levanon D, Bernstein Y, Negreanu V, Bone KR, Pozner A, Eilam R et al. Absence of Runx3 expression in normal gastrointestinal epithelium calls into question its tumour suppressor function. EMBO Mol Med 2011; 3: 593-604.
28. Salto-Tellez M, Peh BK, Ito K, Tan SH, Chong PY, Han HC et al. RUNX3 protein is overexpressed in human basal cell carcinomas. Oncogene 2006; 25: 7646-7649.
29. Li J, Kleeff J, Guweidhi A, Esposito I, Berberat PO, Giese T et al. RUNX3 expression in primary and metastatic pancreatic cancer. J Clin Pathol 2004; 57: 294-299.
30. Kudo Y, Tsunematsu T, Takata T. Oncogenic role of RUNX3 in head and neck cancer. J Cell Biochem 2011; 112: 387-393.
31. Hu SL, Huang DB, Sun YB, Wu L, Xu WP, Yin S et al. Pathobiologic implications of methylation and expression status of Runx3 and CHFR genes in gastric cancer. Med Oncol 2011; 28: 447-454.
32. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987; 196: 261-282.
33. Han H, Cortez CC, Yang X, Nichols PW, Jones PA, Liang G. DNA methylation directly silences genes with non-CpG island promoters and establishes a nucleosome occupied promoter. Hum Mol Genet 2011; 20: 4299-4310.
34. Jackson CB, Judd LM, Menheniott TR, Kronborg I, Dow C, Yeomans ND et al. Augmented gp130-mediated cytokine signalling accompanies human gastric cancer progression. J Pathol 2007; 213: 140-151.
35. Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ. Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res 2007; 35: e119.
36. Biondo M, Nasa Z, Marshall A, Toh BH, Alderuccio F. Local transgenic expression of granulocyte macrophage-colony stimulating factor initiates autoimmunity. J Immunol 2001; 166: 2090-2099.
37. Judd LM, Alderman BM, Howlett M, Shulkes A, Dow C, Moverley J et al. Gastric cancer development in mice lacking the SHP2 binding site on the IL-6 family coreceptor gp130. Gastroenterology 2004; 126: 196-207.
38. Keshet I, Schlesinger Y, Farkash S, Rand E, Hecht M, Segal E et al. Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat Genet 2006; 38: 149-153.
39. Smiraglia DJ, Rush LJ, Fruhwald MC, Dai Z, Held WA, Costello JF et al. Excessive CpG island hypermethylation in cancer cell lines versus primary human malignancies. Hum Mol Genet 2001; 10: 1413-1419.
40. Landan G, Cohen NM, Mukamel Z, Bar A, Molchadsky A, Brosh R et al. Epigenetic polymorphism and the stochastic formation of differentially methylated regions in normal and cancerous tissues. Nat Genet 2012; 44: 1207-1214.
41. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39: 232-236.
42. Fujii S, Ito K, Ito Y, Ochiai A. Enhancer of zeste homologue 2 (EZH2) downregulates RUNX3 by increasing histone H3 methylation. J Biol Chem 2008; 283: 17324-17332.
43. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL et al. Chromosomewide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 2005; 37: 853-862.
44. Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res 2001; 61: 3225-3229.
45. So K, Tamura G, Honda T, Homma N, Endoh M, Togawa N et al. Quantitative assessment of RUNX3 methylation in neoplastic and non-neoplastic gastric epithelia using a DNA microarray. Pathol Int 2006; 56: 571-575.
46. Brenner O, Levanon D, Negreanu V, Golubkov O, Fainaru O, Woolf E et al. Loss of Runx3 function in leukocytes is associated with spontaneously developed colitis and gastric mucosal hyperplasia. Proc Natl Acad Sci USA 2004; 101: 16016-16021.
47. Sugai M, Aoki K, Osato M, Nambu Y, Ito K, Taketo MM et al. Runx3 is required for full activation of regulatory T cells to prevent colitis-associated tumor formation. J Immunol 2011; 186: 6515-6520.
48. Whitehead RH. Establishment of cell lines from colon carcinoma. In: Freshney IR (ed). Culture of Human Tumor Cells. John Wiley and Sons: New York, NY, USA, 2003, pp 68-80.
49. Huber M, Helgason CD, Damen JE, Liu L, Humphries RK, Krystal G. The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation. Proc Natl Acad Sci USA 1998; 95: 11330-11335.
50. Kalesnikoff J, Galli SJ. Antiinflammatory and immunosuppressive functions of mast cells. Methods Mol Biol 2011; 677: 207-220.
51. Menheniott TR, Peterson AJ, O'Connor L, Lee KS, Kalantzis A, Kondova I et al. A novel gastrokine, Gkn3, marks gastric atrophy and shows evidence of adaptive gene loss in humans. Gastroenterology 2010; 138: 1823-1835.
52. Levanon D, Brenner O, Negreanu V, Bettoun D, Woolf E, Eilam R et al. Spatial and temporal expression pattern of Runx3 (Aml2) and Runx1 (Aml1) indicates nonredundant functions during mouse embryogenesis. Mech Dev 2001; 109: 413-417.
53. Lee KS, Kalantzis A, Jackson CB, O'Connor L, Murata-Kamiya N, Hatakeyama M et al. Helicobacter pylori CagA triggers expression of the bactericidal lectin REG3gamma via gastric STAT3 activation. PLoS ONE 2012; 7: e30786.