Preoperative low dose NSAID treatment influences the genes for stemness, growth, invasion and metastasis in colorectal cancer

International Journal of Oncology

Volumn 45, Issue 6, 2014, Pages 2208-2220

  Lönnroth, Christina ^a   Andersson, Marianne ^a   Asting, Annika G ^a   Nordgren, Svante ^a   Lundholm, Kent ^a  

^a SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Clinical trial; Colorectal cancer; NSAIDs; Stemness markers; Tumor suppressors

Indexed keywords

CELECOXIB; INDOMETACIN; MICRORNA; NONSTEROID ANTIINFLAMMATORY AGENT; OCTAMER TRANSCRIPTION FACTOR 4; POU5F1 PROTEIN, HUMAN; PYRAZOLE DERIVATIVE; SOX2 PROTEIN, HUMAN; SULFONAMIDE; TRANSCRIPTION FACTOR SOX; TUMOR MARKER;

BIOSYNTHESIS; COLORECTAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METASTASIS; PATHOLOGY; PROGNOSIS;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; COLORECTAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOMETHACIN; MALE; MICRORNAS; NEOPLASM METASTASIS; OCTAMER TRANSCRIPTION FACTOR-3; PROGNOSIS; PYRAZOLES; SOXB1 TRANSCRIPTION FACTORS; SULFONAMIDES; TUMOR MARKERS, BIOLOGICAL;

EID: 84907691104     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2686     Document Type: Article

References (89)

1. Flossmann E, Rothwell PM; British Doctors Aspirin Trial and the UK-TIA Aspirin Trial: Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies. Lancet 369:1603-1613, 2007.
2. Din FV, Theodoratou E, Farrington SM, Tenesa A, Barnetson RA, Cetnarskyj R, Stark L, Porteous ME, Campbell H and Dunlop MG: Effect of aspirin and NSAIDs on risk and survival from colorectal cancer. Gut 59:1670-1679, 2010.
3. Bastiaannet E, Sampieri K, Dekkers OM, de Craen AJ, van Herk-Sukel MP, Lemmens V, van den Broek CB, Coebergh JW, Herings RM, van de Velde CJ, et al: Use of aspirin postdiagnosis improves survival for colon cancer patients. Br J Cancer 106:1564-1570, 2012.
4. Chan AT, Ogino S and Fuchs CS: Aspirin use and survival after diagnosis of colorectal cancer. JAMA 302:649-658, 2009.
5. Lundholm K, Gelin J, Hyltander A, Lonnroth C, Sandstrom R, Svaninger G, et al: Anti-inflammatory treatment may prolong survival in undernourished patients with metastatic solid tumors. Cancer Res 54:5602-5606, 1994.
6. Reimers MS, Bastiaannet E, Langley RE, van Eijk R, van Vlierberghe RL, Lemmens VE, van Herk-Sukel MP, van Wezel T, Fodde R, Kuppen PJ, et al: Expression of HLA class-I antigen, aspirin use, and survival after a diagnosis of colon cancer. JAMA Intern Med 174:732-739, 2014.
7. Lonnroth C, Andersson M, Arvidsson A, Nordgren S, Brevinge H, Lagerstedt K and Lundholm K: Preoperative treatment with a non-steroidal anti-inflammatory drug (NSAID) increases tumor tissue infiltration of seemingly activated immune cells in colorectal cancer. Cancer Immun 8:5, 2008.
8. Lonnroth C, Andersson M, Nordgren S and Lundholm K: Downregulation of Prominin 1/CD133 expression in colorectal cancer by NSAIDs following short-term preoperative treatment. Int J Oncol 41:15-23, 2012.
9. Blanco Calvo M, Bolos Fernandez V, Medina Villaamil V, Aparicio Gallego G, Diaz Prado S and Grande Pulido E: Biology of BMP signalling and cancer. Clin Transl Oncol 11:126-137, 2009.
10. Mizrak D, Brittan M and Alison M: CD133: molecule of the moment. J Pathol 214:3-9, 2008.
11. Rizzino A: Sox2 and Oct-3/4: a versatile pair of master regulators that orchestrate the self-renewal and pluripotency of embryonic stem cells. Wiley Interdiscip Rev Syst Biol Med 1:228-236, 2009.
12. Hu T, Liu S, Breiter DR, Wang F, Tang Y and Sun S: Octamer 4 small interfering RNA results in cancer stem cell-like cell apoptosis. Cancer Res 68:6533-6540, 2008.
13. Friedman JM and Jones PA: MicroRNAs: critical mediators of differentiation, development and disease. Swiss Med Wkly 139:466-472, 2009.
14. Slaby O, Svoboda M, Michalek J and Vyzula R: MicroRNAs in colorectal cancer: translation of molecular biology into clinical application. Mol Cancer 8:102, 2009.
15. Gustafsson A, Hansson E, Kressner U, Nordgren S, Andersson M, Wang W, Lonnroth C and Lundholm K: EP1-4 subtype, COX and PPAR gamma receptor expression in colorectal cancer in prediction of disease-specific mortality. Int J Cancer 121:232-240, 2007.
16. Cahlin C, Lonnroth C, Arvidsson A, Nordgren S and Lundholm K: Growth associated proteins in tumor cells and stroma related to disease progression of colon cancer accounting for tumor tissue PGE2 content. Int J Oncol 32:909-918, 2008.
17. Chen S, Song X, Chen Z, Li X, Li M, Liu H and Li J: CD133 expression and the prognosis of colorectal cancer: a systematic review and meta-analysis. PLoS One 8: e56380, 2013.
18. He A, Qi W, Huang Y, Feng T, Chen J, Sun Y, Shen Z and Yao Y: CD133 expression predicts lung metastasis and poor prognosis in osteosarcoma patients: A clinical and experimental study. Exp Ther Med 4:435-441, 2012.
19. Hashimoto K, Aoyagi K, Isobe T, Kouhuji K and Shirouzu K: Expression of CD133 in the cytoplasm is associated with cancer progression and poor prognosis in gastric cancer. Gastric Cancer 17:97-106, 2014.
20. Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, Hoek M, Zeilstra J, Pals ST, Mehmet H, Stassi G and Medema JP: The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 70:719-729, 2010.
21. Mak AB, Blakely KM, Williams RA, Penttila PA, Shukalyuk AI, Osman KT, Kasimer D, Ketela T and Moffat J: CD133 protein N-glycosylation processing contributes to cell surface recognition of the primitive cell marker AC133 epitope. J Biol Chem 286:41046-41056, 2011.
22. Liu A, Yu X and Liu S: Pluripotency transcription factors and cancer stem cells: small genes make a big difference. Chin J Cancer 32:483-487, 2013.
23. Wang X and Dai J: Concise review: isoforms of OCT4 contribute to the confusing diversity in stem cell biology. Stem Cells 28:885-893, 2010.
24. Atlasi Y, Mowla SJ, Ziaee SA, Gokhale PJ and Andrews PW: OCT4 spliced variants are differentially expressed in human pluripotent and nonpluripotent cells. Stem Cells 26:3068-3074, 2008.
25. Gao Y, Wang X, Han J, Xiao Z, Chen B, Su G and Dai J: The novel OCT4 spliced variant OCT4B1 can generate three protein isoforms by alternative splicing into OCT4B. J Genet Genomics 37:461-465, 2010.
26. Gazouli M, Roubelakis MG, Theodoropoulos GE, Papailiou J, Vaiopoulou A, Pappa KI, Nikiteas N and Anagnou NP: OCT4 spliced variant OCT4B1 is expressed in human colorectal cancer. Mol Carcinog 51:165-173, 2012.
27. Fang X, Yu W, Li L, Shao J, Zhao N, Chen Q, Ye Z, Lin SC, Zheng S and Lin B: ChIP-seq and functional analysis of the SOX2 gene in colorectal cancers. OMICS 14:369-384, 2010.
28. Wang Q, He W, Lu C, Wang Z, Wang J, Giercksky KE, Nesland JM and Suo Z: Oct3/4 and Sox2 are significantly associated with an unfavorable clinical outcome in human esophageal squamous cell carcinoma. Anticancer Res 29:1233-1241, 2009.
29. Otsubo T, Akiyama Y, Yanagihara K and Yuasa Y: SOX2 is frequently downregulated in gastric cancers and inhibits cell growth through cell-cycle arrest and apoptosis. Br J Cancer 98:824-831, 2008.
30. Wong OG, Huo Z, Siu MK, Zhang H, Jiang L, Wong ES and Cheung AN: Hypermethylation of SOX2 promoter in endometrial carcinogenesis. Obstet Gynecol Int 2010:682504, 2010.
31. Cox JL, Wilder PJ, Desler M and Rizzino A: Elevating SOX2 levels deleteriously affects the growth of medulloblastoma and glioblastoma cells. PLoS One 7: e44087, 2012.
32. Niwa H, Miyazaki J and Smith AG: Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372-376, 2000.
33. Boer B, Kopp J, Mallanna S, Desler M, Chakravarthy H, Wilder PJ, Bernadt C and Rizzino A: Elevating the levels of Sox2 in embryonal carcinoma cells and embryonic stem cells inhibits the expression of Sox2:Oct-3/4 target genes. Nucleic Acids Res 35:1773-1786, 2007.
34. Saunders A, Faiola F and Wang J: Concise review: pursuing self-renewal and pluripotency with the stem cell factor Nanog. Stem Cells 31:1227-1236, 2013.
35. Qiu W, Wang X, Leibowitz B, Liu H, Barker N, Okada H, Oue N, Yasui W, Clevers H, Schoen RE, et al: Chemoprevention by nonsteroidal anti-inflammatory drugs eliminates oncogenic intestinal stem cells via SMAC-dependent apoptosis. Proc Natl Acad Sci USA 107:20027-20032, 2010.
36. Motoyama K, Tanaka F, Kosaka Y, Mimori K, Uetake H, Inoue H, Sugihara K and Mori M. Clinical significance of BMP7 in human colorectal cancer: Ann Surg Oncol 15:1530-1537, 2008.
37. Chen J, Ye L, Xie F, Yang Y, Zhang L and Jiang WG: Expression of bone morphogenetic protein 7 in lung cancer and its biological impact on lung cancer cells. Anticancer Res 30:1113-1120, 2010.
38. Li W, Cai HX, Ge XM, Li K, Xu WD and Shi WH: Prognostic significance of BMP7 as an oncogene in hepatocellular carcinoma. Tumour Biol 34:669-674, 2013.
39. Megumi K, Ishigami S, Uchikado Y, Kita Y, Okumura H, Matsumoto M, Uenosono Y, Arigami T, Kijima Y, Kitazono M, et al: Clinicopathological significance of BMP7 expression in esophageal squamous cell carcinoma. Ann Surg Onco 19:2066-2071, 2012.
40. Yamashita S, Tsujino Y, Moriguchi K, Tatematsu M and Ushijima T: Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5.aza-2'.deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 97:64-71, 2006.
41. Della Vittoria Scarpati G, Falcetta F, Carlomagno C, Ubezio P, Marchini S, De Stefano A, Singh VK, D'Incalci M, De Placido S and Pepe S: A specific miRNA signature correlates with complete pathological response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Int J Radiat Oncol Biol Phys 83:1113-1119, 2012.
42. Farhana L, Dawson MI, Murshed F, Das JK, Rishi AK and Fontana JA: Upregulation of miR-150∗ and miR-630 induces apoptosis in pancreatic cancer cells by targeting IGF-1R. PLoS One 8: e61015, 2013.
43. Corcoran C, Rani S, Breslin S, Gogarty M, Ghobrial IM, Crown J and O'Driscoll L: miR-630 targets IGF1R to regulate response to HER-targeting drugs and overall cancer cell progression in HER2 over-expressing breast cancer. Mol Cancer 13:71, 2014.
44. John B, Enright AJ, Aravin A, Tuschl T, Sander C and Marks DS: Human MicroRNA targets. PLoS Biol 2: e363, 2004.
45. Kanaan Z, Rai SN, Eichenberger MR, Roberts H, Keskey B, Pan J and Galandiuk S: Plasma miR-21: a potential diagnostic marker of colorectal cancer. Ann Surg 256:544-551, 2012.
46. Caruso SI, Bazan V, Rolfo C, Insalaco L, Fanale D, Bronte G, Corsini LR, Rizzo S, Cicero G and Russo A: MicroRNAs in colorectal cancer stem cells: new regulators of cancer stemness? Oncogenesis 1: e32, 2012.
47. Chen WS, Leung CM, Pan HW, Hu LY, Li SC, Ho MR and Tsai K W: Silencing of miR-1-1 and miR-133a-2 cluster expression by DNA hypermethylation in colorectal cancer. Oncol Rep 28:1069-1076, 2012.
48. Nasser MW, Datta J, Nuovo G, Kutay H, Motiwala T, Majumder S, Wang B, Suster S, Jacob ST and Ghoshal K: Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J Biol Chem 283:33394-33405, 2008.
49. Hudson RS, Yi M, Esposito D, Watkins SK, Hurwitz AA, Yfantis HG, Lee DH, Borin JF, Naslund MJ, Alexander RB, et al: MicroRNA-1 is a candidate tumor suppressor and prognostic marker in human prostate cancer. Nucleic Acids Res 40:3689-3703, 2012.
50. Yamasaki T, Yoshino H, Enokida H, Hidaka H, Chiyomaru T, Nohata N, Kinoshita T, Fuse M, Seki N and Nakagawa M: Novel molecular targets regulated by tumor suppressors microRNA-1 and microRNA-133a in bladder cancer. Int J Oncol 40:1821-1830, 2012.
51. Nohata N, Hanazawa T, Enokida H and Seki N: microRNA-1/133a and microRNA-206/133b clusters: dysregulation and functional roles in human cancers. Oncotarget 3:9-21, 2012.
52. Chen WC, Lin MS, Ye YL, Gao HJ, Song ZY and Shen XY: microRNA expression pattern and its alteration following celecoxib intervention in human colorectal cancer. Exp Ther Med 3:1039-1048, 2012.
53. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA, Khodiyar VK, Lush MJ, Povey S, Talbot CC Jr, Wright MW, et al: Gene map of the extended human MHC. Nat Rev Genet 5:889-899, 2004.
54. Mak AB, Nixon AM, Kittanakom S, Stewart JM, Chen GI, Curak J, Gingras AC, Mazitschek R, Neel BG, Stagljar I and Moffat J: Regulation of CD133 by HDAC6 promotes β.catenin signaling to suppress cancer cell differentiation. Cell Rep 2:951-963, 2012.
55. Brandão RD, Veeck J, Van de Vijver KK, Lindsey P, de Vries B, van Elssen CH, Blok MJ, Keymeulen K, Ayoubi T, Smeets HJ, et al: A randomised controlled phase II trial of pre-operative celecoxib treatment reveals anti-tumour transcriptional response in primary breast cancer. Breast Cancer Res 15: R29, 2013.
56. Zhou Y, Cho KJ, Plowman SJ and Hancock JF: Nonsteroidal anti-inflammatory drugs alter the spatiotemporal organization of Ras proteins on the plasma membrane. J Biol Chem 287:16586-16595, 2012.
57. Kim MS, Lee EJ, Kim HR and Moon A: p38 kinase is a key signaling molecule for H-Ras-induced cell motility and invasive phenotype in human breast epithelial cells. Cancer Res 63:5454-5461, 2003.
58. Fang JY and Richardson BC: The MAPK signalling pathways and colorectal cancer. Lancet Oncol 6:322-327, 2005.
59. Alesutan I, Sopjani M, Dermaku-Sopjani M, Munoz C, Voelkl J and Lang F: Upregulation of Na-coupled glucose transporter SGLT1 by Tau tubulin kinase 2. Cell Physiol Biochem 30:458-465, 2012.
60. Sarkar R, Hunter IA, Rajaganeshan R, Perry SL, Guillou P and Jayne DG: Expression of cyclin D2 is an independent predictor of the development of hepatic metastasis in colorectal cancer. Colorectal Dis 12:316-323, 2010.
61. Van Erk MJ, Teuling E, Staal YC, Huybers S, Van Bladeren PJ, Aarts JM and Van Ommen B: Time- and dose-dependent effects of curcumin on gene expression in human colon cancer cells. J Carcinog 3:8, 2004.
62. Sato T, Oshima T, Yoshihara K, Yamamoto N, Yamada R, Nagano Y, Fujii S, Kunisaki C, Shiozawa M, Akaike M, et al: Overexpression of the fibroblast growth factor receptor-1 gene correlates with liver metastasis in colorectal cancer. Oncol Rep 21:211-216, 2009.
63. Lee JH, Kang MJ, Han HY, Lee MG, Jeong SI, Ryu BK, Ha TK, Her NG, Han J, Park SJ, et al: Epigenetic alteration of PRKCDBP in colorectal cancers and its implication in tumor cell resistance to TNF α.induced apoptosis. Clin Cancer Res 17:7551-7562, 2011.
64. Kim E, Chen F, Wang CC and Harrison LE: CDK5 is a novel regulatory protein in PPARgamma ligand-induced antiproliferation. Int J Oncol 28:191-194, 2006.
65. Eggers JP, Grandgenett PM, Collisson EC, Lewallen ME, Tremayne J, Singh PK, Swanson BJ, Andersen JM, Caffrey TC, High RR, et al: Cyclin-dependent kinase 5 is amplified and overexpressed in pancreatic cancer and activated by mutant K-Ras. Clin Cancer Res 17:6140-6150, 2011.
66. Blumenthal RD, Leon E, Hansen HJ and Goldenberg DM: Expression patterns of CEACAM5 and CEACAM6 in primary and metastatic cancers. BMC Cancer 7:2, 2007.
67. Jantscheff P, Terracciano L, Lowy A, Glatz-Krieger K, Grunert F, Micheel B, Brummer J, Laffer U, Metzger U, Herrmann R and Rochlitz C: Expression of CEACAM6 in resectable colorectal cancer: a factor of independent prognostic significance. J Clin Oncol 21:3638-3646, 2003.
68. Beauchemin N and Arabzadeh A: Carcinoembryonic antigen-related cell adhesion molecules (CEACAMs) in cancer progression and metastasis. Cancer Metastasis Rev 32:643-671, 2013.
69. Hirakawa M, Takimoto R, Tamura F, Yoshida M, Ono M, Murase K, Sato Y, Osuga T, Sato T, Iyama S, et al: Fucosylated TGF. β receptors transduces a signal for epithelial-mesenchymal transition in colorectal cancer cells. Br J Cancer 110:156-163, 2014.
70. Zhou F, Mu YD, Liang J, Liu ZX, Chen HS and Zhang JF: Expression and prognostic value of tumor stem cell markers ALDH1 and CD133 in colorectal carcinoma. Oncol Lett 7:507-512, 2014.
71. Aoi J, Endo M, Kadomatsu T, Miyata K, Ogata A, Horiguchi H, Odagiri H, Masuda T, Fukushima S, Jinnin M, et al: Angiopoietin-like protein 2 accelerates carcinogenesis by activating chronic inflammation and oxidative stress. Mol Cancer Res 12:239-249, 2014.
72. Fanali C, Lucchetti D, Farina M, Corbi M, Cufino V, Cittadini A and Sgambato A: Cancer stem cells in colorectal cancer from pathogenesis to therapy: controversies and perspectives. World J Gastroenterol 20:923-942, 2014.
73. Zhao J: Coordination of DNA synthesis and histone gene expression during normal cell cycle progression and after DNA damage. Cell Cycle 3:695-697, 2004.
74. Zhang Y, Chen FQ, Sun YH, Zhou SY, Li TY and Chen R: Effects of DNMT1 silencing on malignant phenotype and methylated gene expression in cervical cancer cells. J Exp Clin Cancer Res 30:98, 2011.
75. Szyf M: The role of DNA methyltransferase 1 in growth control. Front Biosci 6: D599-D609, 2001.
76. Robert MF, Morin S, Beaulieu N, Gauthier F, Chute IC, Barsalou A and MacLeod AR: DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat Genet 33:61-65, 2003.
77. Peng DF, Kanai Y, Sawada M, Ushijima S, Hiraoka N, Kitazawa S and Hirohashi S: DNA methylation of multiple tumor-related genes in association with overexpression of DNA methyltransferase 1 (DNMT1) during multistage carcinogenesis of the pancreas. Carcinogenesis 27:1160-1168, 2006.
78. Suzuki M, Sunaga N, Shames DS, Toyooka S, Gazdar AF and Minna JD: RNA interference-mediated knockdown of DNA methyltransferase 1 leads to promoter demethylation and gene re-expression in human lung and breast cancer cells. Cancer Res 64:3137-3143, 2004.
79. Mitomi H, Fukui N, Tanaka N, Kanazawa H, Saito T, Matsuoka T and Yao T: Aberrant p16INK4a methylation is a frequent event in colorectal cancers: prognostic value and relation to mRNA expression and immunoreactivity. J Cancer Res Clin Oncol 136:323-331, 2010.
80. Licciardi PV and Karagiannis TC: Regulation of immune responses by histone deacetylase inhibitors. ISRN Hematol 2012:690901, 2012.
81. Ho AS, Turcan S and Chan TA: Epigenetic therapy: use of agents targeting deacetylation and methylation in cancer management. Onco Targets Ther 6:223-232, 2013.
82. Lee YS, Lim KH, Guo X, Kawaguchi Y, Gao Y, Barrientos T, Ordentlich P, Wang XF, Counter CM, Yao TP: The cytoplasmic deacetylase HDAC6 is required for efficient oncogenic tumorigenesis. Cancer Res 68:7561-7569, 2008.
83. Fatima N, Yi M, Ajaz S, Stephens RM, Stauffer S, Greenwald P, Munroe DJ and Ali IU: Altered gene expression profiles define pathways in colorectal cancer cell lines affected by celecoxib. Cancer Epidemiol Biomarkers Prev 17:3051-3061, 2008.
84. van Erk MJ, Roepman P, van der Lende TR, Stierum RH, Aarts JM, van Bladeren PJ and van Ommen B: I ntegrated assessment by multiple gene expression analysis of quercetin bioactivity on anticancer-related mechanisms in colon cancer cells in vitro. Eur J Nutr 44:143-156, 2005.
85. Li J and Mansmann UR: Modeling of non-steroidal anti-inflammatory drug effect within signaling pathways and mirna-regulation pathways. PLoS One 8: e72477, 2013.
86. Jeck WR, Siebold AP and Sharpless NE: Review: a meta-analysis of GWAS and age-associated diseases. Aging Cell 11:727-731, 2012.
87. Langan RC, Mullinax JE, Raiji MT, Upham T, Summers T, Stojadinovic A and Avital I: Colorectal cancer biomarkers and the potential role of cancer stem cells. J Cancer 4:241-250, 2013.
88. Tabarestani S and Ghafouri-Fard S: Cancer stem cells and response to therapy. Asian Pac J Cancer Prev 13:5951-5958, 2012.
89. Park JH, McMillan DC, Horgan PG and Roxburgh CS: The impact of anti-inflammatory agents on the outcome of patients with colorectal cancer. Cancer Treat Rev 40:68-77, 2014.