Epigenetics override pro-inflammatory PTGS transcriptomic signature towards selective hyperactivation of PGE2 in colorectal cancer

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Cebola, Inês ^a,e   Custodio, Joaquin ^a,f   Muñoz, Mar ^a   Díez Villanueva, Anna ^a   Paré, Laia ^b   Prieto, Patricia ^c   Aussó, Susanna ^b   Coll Mulet, Llorenç ^a   Boscá, Lisardo ^c   Moreno, Victor ^b,d   Peinado, Miguel A ^a  

^a Institute of Predictive and Personalized Medicine of Cancer (IMPPC)   (Spain)

^b CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^c INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

COX pathway; DNA methylation; Gene expression; Inflammation; Prostaglandins; Prostanoids

Indexed keywords

BISULFITE; DNA; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; PROSTANOID; PROSTANOID RECEPTOR;

ADULT; AGED; AKR1B1 GENE; ARTICLE; CANCER CELL; COLON MUCOSA; COLORECTAL ADENOMA; COLORECTAL CANCER; COLORECTAL CARCINOMA; CONTROLLED STUDY; DISSOCIATION; DNA METHYLATION; EPIGENETICS; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PTGER3 GENE; PTGFR GENE; PTGIS GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; TUMOR MICROENVIRONMENT;

EID: 84937865655     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0110-4     Document Type: Article

References (59)

1. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.
2. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis. 2009;30:1073–81.
3. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140:883–99.
4. Aggarwal BB, Vijayalekshmi RV, Sung B. Targeting inflammatory pathways for prevention and therapy of cancer: short-term friend, long-term foe. Clin Cancer Res. 2009;15:425–30.
5. Cathcart MC, Lysaght J, Pidgeon GP. Eicosanoid signalling pathways in the development and progression of colorectal cancer: novel approaches for prevention/intervention. Cancer Metastasis Rev. 2011;30:363–85.
6. Greenhough A, Smartt HJM, Moore AE, Roberts HR, Williams AC, Paraskeva C, et al. The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis. 2009;30:377–86.
7. Wang D, Dubois RN. The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene. 2010;29:781–8.
8. Coghill AE, Newcomb PA, Poole EM, Hutter CM, Makar KW, Duggan D, et al. Genetic variation in inflammatory pathways is related to colorectal cancer survival. Clin Cancer Res. 2011;17:7139–47.
9. Resler AJ, Makar KW, Heath L, Whitton J, Potter JD, Poole EM, et al. Genetic variation in prostaglandin synthesis and related pathways, NSAID use and colorectal cancer risk in the Colon Cancer Family Registry. Carcinogenesis. 2014;35(9):2121-6.
10. Poole EM, Hsu L, Xiao L, Kulmacz RJ, Carlson CS, Rabinovitch PS, et al. Genetic variation in prostaglandin E2 synthesis and signaling, prostaglandin dehydrogenase, and the risk of colorectal adenoma. Cancer Epidemiol Biomarkers Prev. 2010;19:547–57.
11. Cox DG, Pontes C, Guino E, Navarro M, Osorio A, Canzian F, et al. Polymorphisms in prostaglandin synthase 2/cyclooxygenase 2 (PTGS2/COX2) and risk of colorectal cancer. Br J Cancer. 2004;91:339–43.
12. Rigas B, Goldman IS, Levine L. Altered eicosanoid levels in human colon cancer. J Lab Clin Med. 1993;122:518–23.
13. Pugh S, Thomas GA. Patients with adenomatous polyps and carcinomas have increased colonic mucosal prostaglandin E2. Gut. 1994;35:675–8.
14. Ogino S, Kirkner GJ, Nosho K, Irahara N, Kure S, Shima K, et al. Cyclooxygenase-2 expression is an independent predictor of poor prognosis in colon cancer. Clin Cancer Res. 2008;14:8221–7.
15. Tsujii M, Kawano S, DuBois RN. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc Natl Acad Sci U S A. 1997;94:3336–40.
16. Kunzmann AT, Murray LJ, Cardwell CR, McShane CM, McMenamin UC, Cantwell MM. PTGS2 (Cyclooxygenase-2) expression and survival among colorectal cancer patients: a systematic review. Cancer Epidemiol Biomarkers Prev. 2013;22:1490–7.
17. Kurtova AV, Xiao J, Mo Q, Pazhanisamy S, Krasnow R, Lerner SP et al. Blocking PGE-induced tumour repopulation abrogates bladder cancer chemoresistance. Nature. 2014;517:209–13.
18. Tougeron D, Sha D, Manthravadi S, Sinicrope FA. Aspirin and colorectal cancer: back to the future. Clin Cancer Res. 2014;20:1087–94.
19. Sahin IH, Hassan MM, Garrett CR. Impact of non-steroidal anti-inflammatory drugs on gastrointestinal cancers: current state-of-the science. Cancer Lett. 2014;345:249–57.
20. Thun MJ, Jacobs EJ, Patrono C. The role of aspirin in cancer prevention. Nat Rev Clin Oncol. 2012;9:259–67.
21. Liao X, Lochhead P, Nishihara R, Morikawa T, Kuchiba A, Yamauchi M, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2012;367:1596–606.
22. Ulrich CM, Bigler J, Potter JD. Non-steroidal anti-inflammatory drugs for cancer prevention: promise, perils and pharmacogenetics. Nat Rev Cancer. 2006;6:130–40.
23. Ng K, Meyerhardt JA, Chan AT, Sato K, Chan JA, Niedzwiecki D, et al. Aspirin and COX-2 inhibitor use in patients with stage III colon cancer. J Natl Cancer Inst. 2015;107:345.
24. Din FV, Theodoratou E, Farrington SM, Tenesa A, Barnetson RA, Cetnarskyj R, et al. Effect of aspirin and NSAIDs on risk and survival from colorectal cancer. Gut. 2010;59:1670–9.
25. Patrignani P, Capone ML, Tacconelli S. NSAIDs and cardiovascular disease. Heart. 2008;94:395–7.
26. Colussi D, Brandi G, Bazzoli F, Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci. 2013;14:16365–85.
27. Carmona FJ, Esteller M. Epigenomics of human colon cancer. Mutat Res. 2010;693:53–60.
28. Bardhan K, Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers (Basel). 2013;5:676–713.
29. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8:286–98.
30. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128:683–92.
31. Cebola I, Peinado MA. Epigenetic deregulation of the COX pathway in cancer. Prog Lipid Res. 2012;51:301–13.
32. Harris RE. Cyclooxygenase-2 (cox-2) and the inflammogenesis of cancer. Subcell Biochem. 2007;42:93–126.
33. Karnes Jr WE, Shattuck-Brandt R, Burgart LJ, DuBois RN, Tester DJ, Cunningham JM, et al. Reduced COX-2 protein in colorectal cancer with defective mismatch repair. Cancer Res. 1998;58:5473–7.
34. Sinicrope FA, Lemoine M, Xi L, Lynch PM, Cleary KR, Shen Y, et al. Reduced expression of cyclooxygenase 2 proteins in hereditary nonpolyposis colorectal cancers relative to sporadic cancers. Gastroenterology. 1999;117:350–8.
35. Frigola J, Muñoz M, Clark SJ, Moreno V, Capella G, Peinado MA. Hypermethylation of the prostacyclin synthase (PTGIS) promoter is a frequent event in colorectal cancer and associated with aneuploidy. Oncogene. 2005;24:7320–6.
36. Luo Y, Wong CJ, Kaz AM, Dzieciatkowski S, Carter KT, Morris SM, et al. Differences in DNA methylation signatures reveal multiple pathways of progression from adenoma to colorectal cancer. Gastroenterology. 2014;147:418–29. e8.
37. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature. 2002;416:552–6.
38. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med. 2004;10:789–99.
39. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.
40. Toyota M, Shen L, Ohe-Toyota M, Hamilton SR, Sinicrope FA, Issa JP. Aberrant methylation of the cyclooxygenase 2 CpG island in colorectal tumors. Cancer Res. 2000;60:4044–8.
41. de Maat MFG, van de Velde CJH, Umetani N, de Heer P, Putter H, van Hoesel AQ, et al. Epigenetic silencing of cyclooxygenase-2 affects clinical outcome in gastric cancer. J Clin Oncol. 2007;25:4887–94.
42. Shoji Y, Takahashi M, Kitamura T, Watanabe K, Kawamori T, Maruyama T, et al. Downregulation of prostaglandin E receptor subtype EP3 during colon cancer development. Gut. 2004;53:1151–8.
43. Gustafsson A, Hansson E, Kressner U, Nordgren S, Andersson M, Lonnroth C, et al. Prostanoid receptor expression in colorectal cancer related to tumor stage, differentiation and progression. Acta Oncol. 2007;46:1107–12.
44. Kropotova ES, Tychko RA, Zinov'eva OL, Zyrianova AF, Khankin SL, Cherkes VL, et al. Downregulation of AKR1B10 gene expression in colorectal cancer. Mol Biol (Mosk). 2010;44:243–50.
45. 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;38:149–53.
46. Tsujii M. Cyclooxygenase, cancer stem cells and DNA methylation play important roles in colorectal carcinogenesis. Digestion. 2013;87:12–6.
47. Xia D, Wang D, Kim SH, Katoh H, DuBois RN. Prostaglandin E2 promotes intestinal tumor growth via DNA methylation. Nat Med. 2012;18:224–6.
48. Nakanishi M, Perret C, Meuillet EJ, Rosenberg DW. Non-cell autonomous effects of targeting inducible PGE2 synthesis during inflammation-associated colon carcinogenesis. Carcinogenesis. 2015;36:478–86.
49. Wang D, DuBois RN. Cyclooxygenase 2-derived prostaglandin E2 regulates the angiogenic switch. Proc Natl Acad Sci U S A. 2004;101:415–6.
50. Zuo X, Shureiqi I. Eicosanoid profiling in colon cancer: emergence of a pattern. Prostaglandins Other Lipid Mediat. 2013;104-105:139–43.
51. Chandramouli A, Onyeagucha BC, Mercado-Pimentel ME, Stankova L, Shahin NA, LaFleur BJ, et al. MicroRNA-101 (miR-101) post-transcriptionally regulates the expression of EP4 receptor in colon cancers. Cancer Biol Ther. 2012;13:175–83.
52. Katoh H, Hosono K, Ito Y, Suzuki T, Ogawa Y, Kubo H, et al. COX-2 and prostaglandin EP3/EP4 signaling regulate the tumor stromal proangiogenic microenvironment via CXCL12-CXCR4 chemokine systems. Am J Pathol. 2010;176:1469–83.
53. Kubo H, Hosono K, Suzuki T, Ogawa Y, Kato H, Kamata H, et al. Host prostaglandin EP3 receptor signaling relevant to tumor-associated lymphangiogenesis. Biomed Pharmacother. 2010;64:101–6.
54. Bishehsari F, Mahdavinia M, Vacca M, Malekzadeh R, Mariani-Costantini R. Epidemiological transition of colorectal cancer in developing countries: environmental factors, molecular pathways, and opportunities for prevention. World J Gastroenterol. 2014;20:6055–72.
55. Barrow TM, Michels KB. Epigenetic epidemiology of cancer. Biochem Biophys Res Commun. 2014;455:70–83.
56. Coppede F. The role of epigenetics in colorectal cancer. Expert Rev Gastroenterol Hepatol. 2014;8:935–48.
57. Ogino S, Lochhead P, Chan AT, Nishihara R, Cho E, Wolpin BM, et al. Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Mod Pathol. 2013;26:465–84.
58. Sanz-Pamplona R, Berenguer A, Cordero D, Mollevi DG, Crous-Bou M, Sole X, et al. Aberrant gene expression in mucosa adjacent to tumor reveals a molecular crosstalk in colon cancer. Mol Cancer. 2014;13:46.
59. Worm J, Aggerholm A, Guldberg P. In-tube DNA methylation profiling by fluorescence melting curve analysis. Clin Chem. 2001;47:1183–9.