Mechanistic Aspects of COX-2 Expression in Colorectal Neoplasia

Part of the Recent Results in Cancer Research book series (RECENTCANCER, volume 191)

Abstract

The cyclooxygenase-2 (COX-2) enzyme catalyzes the rate-limiting step of prostaglandin formation in pathogenic states and a large amount of evidence has demonstrated constitutive COX-2 expression to be a contributing factor promoting colorectal cancer (CRC). Various genetic, epigenetic, and inflammatory pathways have been identified to be involved in the etiology and development of CRC. Alteration in these pathways can influence COX-2 expression at multiple stages of colon carcinogenesis allowing for elevated prostanoid biosynthesis to occur in the tumor microenvironment. In normal cells, COX-2 expression levels are potently regulated at the post-transcriptional level through various RNA sequence elements present within the mRNA 3′ untranslated region (3′UTR). A conserved AU-rich element (ARE) functions to target COX-2 mRNA for rapid decay and translational inhibition through association with various RNA-binding proteins to influence the fate of COX-2 mRNA. Specific microRNAs (miRNAs) bind regions within the COX-2 3′UTR and control COX-2 expression. In this chapter, we discuss novel insights in the mechanisms of altered post-transcriptional regulation of COX-2 in CRC and how this knowledge may be used to develop novel strategies for cancer prevention and treatment.

Keywords

Adenomatous Polyposis Coli Lynch Syndrome Colon Tumorigenesis T8473C Single Nucleotide Polymorphism Cytoplasmic Stress Granule 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

CRC

Colorectal cancer

CV

Cardiovascular

CIN

Chromosomal instability

APC

Adenomatous polyposis coli

FAP

Familial adenomatous polyposis

EGF

Epidermal growth factor

TGF

Transforming growth factor

COX

Cyclooxygenase

PG

Prostaglandin

(TX)A2

Thromboxane

PGI2

Prostacyclin

GI

Gastrointestinal

NSAIDs

Nonsteroidal anti-inflammatory drugs

mPGES

Microsomal Prostaglandin E Synthase

15-PGDH

15-hydroxyprostaglandin dehydrogenase

PPAR

Peroxisome proliferator-activated receptor

AU

Rich elements (AREs)

miRNAs

MicroRNAs

HuR

Hu antigen R

TIA-1

T cell intracellular antigen 1

RBM3

RNA-binding motif protein 3

Notes

Acknowledgments

This work was supported by the National Institutes of Health (R01 CA134609 to D.A. Dixon) and American Cancer Society (RSG-06-122-01-CNE to D.A. Dixon). We apologize to our colleagues for not being able to reference all primary work due to space limitations.

References

  1. Abdelmohsen K, Gorospe M (2010) Post-transcriptional regulation of cancer traits by HuR. Wiley Interdisc Rev RNA 1:214–229Google Scholar
  2. Ahnen DJ (2011) The American college of gastroenterology emily couric lecture–the adenoma-carcinoma sequence revisited: Has the era of genetic tailoring finally arrived? Am J Gastroenterol 106:190–198PubMedGoogle Scholar
  3. Akao Y, Nakagawa Y, Naoe T (2006) MicroRNAs 143 and 145 are possible common onco-microRNAs in human cancers. Oncol Rep 16:845–850PubMedGoogle Scholar
  4. Akao Y, Nakagawa Y, Naoe T (2007) MicroRNA-143 and -145 in colon cancer. DNA Cell Biol 26:311–320PubMedGoogle Scholar
  5. Ali IU, Luke BT, Dean M et al (2005) Allellic variants in regulatory regions of cyclooxygenase-2: association with advanced colorectal adenoma. Br J Cancer 93:953–959PubMedGoogle Scholar
  6. Anant S, Houchen CW, Pawar V et al (2010) Role of RNA-binding proteins in colorectal carcinogenesis. Curr Colorectal Cancer Rep 6:68–73PubMedGoogle Scholar
  7. Anderson P, Kedersha N (2008) Stress granules: the tao of RNA triage. Trends Biochem Sci 33:141–150PubMedGoogle Scholar
  8. Araki Y, Okamura S, Hussain SP et al (2003) Regulation of cyclooxygenase-2 expression by the wnt and ras pathways. Cancer Res 63:728–734PubMedGoogle Scholar
  9. Atkin WS, Edwards R, Kralj-Hans I et al (2010) Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 375:1624–1633PubMedGoogle Scholar
  10. Backlund MG, Mann JR, Holla VR et al (2005) 15-hydroxyprostaglandin dehydrogenase is down-regulated in colorectal cancer. J Biol Chem 280:3217–3223PubMedGoogle Scholar
  11. Bakheet T, Williams BR, Khabar KS (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34:D111–D114PubMedGoogle Scholar
  12. Bandres E, Cubedo E, Agirre X et al (2006) Identification by real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer 5:29PubMedGoogle Scholar
  13. Barreau C, Paillard L, Osborne HB (2005) AU-rich elements and associated factors: Are there unifying principles? Nucleic Acids Res 33:7138–7150PubMedGoogle Scholar
  14. Bazan NG, Lukiw WJ (2002) Cyclooxygenase-2 and presenilin-1 gene expression induced by interleukin-1beta and amyloid beta 42 peptide is potentiated by hypoxia in primary human neural cells. J Biol Chem 277:30359–30367PubMedGoogle Scholar
  15. Bertagnolli MM, Eagle CJ, Zauber AG et al (2006) Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med 355:873–884PubMedGoogle Scholar
  16. Brennan CM, Steitz JA (2001) HuR and mRNA stability. Cell Mol Life Sci 58:266–277PubMedGoogle Scholar
  17. Briata P, Ilengo C, Corte G et al (2003) The wnt/beta-catenin → pitx2 pathway controls the turnover of pitx2 and other unstable mrnas. Mol Cell 12:1201–1211PubMedGoogle Scholar
  18. Bruno A, Di Francesco L, Coletta I et al (2010) Effects of af3442 [n-(9-ethyl-9 h-carbazol-3-yl)-2-(trifluoromethyl)benzamide], a novel inhibitor of human microsomal prostaglandin e synthase-1, on prostanoid biosynthesis in human monocytes in vitro. Biochem Pharmacol 79:974–981PubMedGoogle Scholar
  19. Buchanan FG, DuBois RN (2006) Connecting COX-2 and wnt in cancer. Cancer Cell 9:6–8PubMedGoogle Scholar
  20. Buchanan FG, Holla V, Katkuri S et al (2007) Targeting cyclooxygenase-2 and the epidermal growth factor receptor for the prevention and treatment of intestinal cancer. Cancer Res 67:9380–9388PubMedGoogle Scholar
  21. Burn J, Bishop DT, Chapman PD et al (2011) A randomized placebo-controlled prevention trial of aspirin and/or resistant starch in young people with familial adenomatous polyposis. Cancer Prev Res 4:655–665Google Scholar
  22. Calin GA, Dumitru CD, Shimizu M et al (2002) Frequent deletions and down-regulation of micro-RNA genes mir15 and mir16 at 13q14 in chronic lymphocytic leukemia. Proc Nat Acad Sci USA 99:15524–15529PubMedGoogle Scholar
  23. Campa D, Zienolddiny S, Maggini V et al (2004) Association of a common polymorphism in the cyclooxygenase 2 gene with risk of non-small cell lung cancer. Carcinogenesis 25:229–235PubMedGoogle Scholar
  24. Cao Y, Prescott SM (2002) Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J Cell Physiol 90:279–286Google Scholar
  25. Carballo E, Lai WS, Blackshear PJ (1998) Feedback inhibition of macrophage tumor necrosis factor-a production by tristetraprolin. Science 281:1001–1005PubMedGoogle Scholar
  26. Carballo E, Lai WS, Blackshear PJ (2000) Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 95:1891–1899PubMedGoogle Scholar
  27. Castells A, Paya A, Alenda C et al (2006) Cyclooxygenase 2 expression in colorectal cancer with DNA mismatch repair deficiency. Clin Cancer Res 12:1686–1692PubMedGoogle Scholar
  28. Cha YI, DuBois RN (2007) NSAIDs and cancer prevention: targets downstream of COX-2. Annu Rev Med 58:239–252PubMedGoogle Scholar
  29. Chakrabarty A, Tranguch S, Daikoku T et al (2007) MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc Nat Acad Sci USA 104:15144–15149PubMedGoogle Scholar
  30. Chan AT, Ogino S, Fuchs CS (2007) Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med 356:2131–2142PubMedGoogle Scholar
  31. Cheadle C, Fan J, Cho-Chung YS et al (2005) Control of gene expression during t cell activation: alternate regulation of mRNA transcription and mRNA stability. BMC Genomics 6:75PubMedGoogle Scholar
  32. Chen X, Guo X, Zhang H et al (2009) Role of miR-143 targeting kras in colorectal tumorigenesis. Oncogene 28:1385–1392PubMedGoogle Scholar
  33. Chulada PC, Thompson MB, Mahler JF et al (2000) Genetic disruption of ptgs-1, as well as ptgs-2, reduces intestinal tumorigenesis in min mice. Cancer Res 60:4705–4708PubMedGoogle Scholar
  34. Cimmino A, Calin GA, Fabbri M et al (2005) MiR-15 and miR-16 induce apoptosis by targeting bcl2. Proc Nat Acad Sci USA 102:13944–13949PubMedGoogle Scholar
  35. Cok SJ, Morrison AR (2001) The 3′-untranslated region of murine cyclooxygenase-2 contains multiple regulatory elements that alter message stability and translational efficiency. J Biol Chem 276:23179–23185PubMedGoogle Scholar
  36. Cordes KR, Sheehy NT, White MP et al (2009) MiR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460:705–710PubMedGoogle Scholar
  37. Croce CM (2009) Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10:704–714PubMedGoogle Scholar
  38. Cummins JM, He Y, Leary RJ et al (2006) The colorectal micrornaome. Proc Nat Acad Sci USA 103:3687–3692PubMedGoogle Scholar
  39. Dai Y, Wang WH (2010) Peroxisome proliferator-activated receptor gamma and colorectal cancer. World J Gastrointest Oncol 2:159–164PubMedGoogle Scholar
  40. Dimberg J, Hugander A, Sirsjo A et al (2001) Enhanced expression of cyclooxygenase-2 and nuclear beta-catenin are related to mutations in the APC gene in human colorectal cancer. Anticancer Res 21:911–915PubMedGoogle Scholar
  41. Dixon DA (2003) Regulation of COX-2 expression in human cancer. Prog Exp Tumor Res 37:52–71PubMedGoogle Scholar
  42. Dixon DA, Balch GC, Kedersha N et al (2003) Regulation of cyclooxygenase-2 expression by the translational silencer TIA-1. J Exp Med 198:475–481PubMedGoogle Scholar
  43. Dixon DA, Kaplan CD, McIntyre TM et al (2000) Post-transcriptional control of cyclooxygenase-2 gene expression. The role of the 3′-untranslated region. J Biol Chem 275:11750–11757PubMedGoogle Scholar
  44. Dixon DA, Tolley ND, King PH et al (2001) Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest 108:1657–1665PubMedGoogle Scholar
  45. Dixon DA, Tolley ND, Bemis-Standoli K et al (2006) Expression of COX-2 in platelet-monocyte interactions occurs via combinatorial regulation involving adhesion and cytokine signaling. J Clin Invest 116:2727–2738PubMedGoogle Scholar
  46. Dohner H, Stilgenbauer S, Benner A et al (2000) Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med 343:1910–1916PubMedGoogle Scholar
  47. Dresios J, Aschrafi A, Owens GC et al (2005) Cold stress-induced protein RBM3 binds 60s ribosomal subunits, alters microRNA levels, and enhances global protein synthesis. Proc Nat Acad Sci USA 102:1865–1870PubMedGoogle Scholar
  48. Duval A, Hamelin R (2002) Mutations at coding repeat sequences in mismatch repair-deficient human cancers: toward a new concept of target genes for instability. Cancer Res 62:2447–2454PubMedGoogle Scholar
  49. Eberhart CE, Coffey RJ, Radhika A et al (1994) Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 107:1183–1188PubMedGoogle Scholar
  50. Elander N, Ungerback J, Olsson H et al (2008) Genetic deletion of mPGES-1 accelerates intestinal tumorigenesis in apc(min/+) mice. Biochem Biophys Res Commun 372:249–253PubMedGoogle Scholar
  51. Eulalio A, Behm-Ansmant I, Izaurralde E (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 8:9–22PubMedGoogle Scholar
  52. Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379PubMedGoogle Scholar
  53. Ferguson HR, Wild CP, Anderson LA et al (2008) Cyclooxygenase-2 and inducible nitric oxide synthase gene polymorphisms and risk of reflux esophagitis, barrett’s esophagus, and esophageal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 17:727–731PubMedGoogle Scholar
  54. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9:102–114PubMedGoogle Scholar
  55. Franks TM, Lykke-Andersen J (2007) TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev 21:719–735PubMedGoogle Scholar
  56. Friedman RC, Farh KK, Burge CB et al (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92–105PubMedGoogle Scholar
  57. Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875PubMedGoogle Scholar
  58. Garcia Rodriguez LA, Tacconelli S, Patrignani P (2008) Role of dose potency in the prediction of risk of myocardial infarction associated with nonsteroidal anti-inflammatory drugs in the general population. J Am Coll Cardiol 52:1628–1636PubMedGoogle Scholar
  59. Garneau NL, Wilusz J, Wilusz CJ (2007) The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8:113–126PubMedGoogle Scholar
  60. Giardiello FM, Casero RA Jr, Hamilton SR et al (2004) Prostanoids, ornithine decarboxylase, and polyamines in primary chemoprevention of familial adenomatous polyposis. Gastroenterology 126:425–431PubMedGoogle Scholar
  61. Gong Z, Bostick RM, Xie D et al (2009) Genetic polymorphisms in the cyclooxygenase-1 and cyclooxygenase-2 genes and risk of colorectal adenoma. Int J Colorectal Dis 24:647–654PubMedGoogle Scholar
  62. Grady WM, Carethers JM (2008) Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology 135:1079–1099PubMedGoogle Scholar
  63. Grosser T, Fries S, FitzGerald GA (2006) Biological basis for the cardiovascular consequences of COX-2 inhibition: therapeutic challenges and opportunities. J Clin Invest 116:4–15PubMedGoogle Scholar
  64. Gruber AR, Fallmann J, Kratochvill F et al (2010) Aresite: a database for the comprehensive investigation of AU-rich elements. Nucleic Acids Res 39:D66–D69PubMedGoogle Scholar
  65. Guo H, Ingolia NT, Weissman JS et al (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835–840PubMedGoogle Scholar
  66. Hall-Pogar T, Zhang H, Tian B et al (2005) Alternative polyadenylation of cyclooxygenase-2. Nucleic Acids Res 33:2565–2579PubMedGoogle Scholar
  67. Hao Y, Gu X, Zhao Y et al (2011) Enforced expression of miR-101 inhibits prostate cancer cell growth by modulating the COX-2 pathway in vivo. Cancer Prev Res (Phila) 4:1073–1083Google Scholar
  68. Harper KA, Tyson-Capper AJ (2008) Complexity of COX-2 gene regulation. Biochem Soc Trans 36:543–545PubMedGoogle Scholar
  69. Hernandez GL, Volpert OV, Iniguez MA et al (2001) Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin a: roles of the nuclear factor of activated t cells and cyclooxygenase 2. J Exp Med 193:607–620PubMedGoogle Scholar
  70. Holla VR, Backlund MG, Yang P et al (2008) Regulation of prostaglandin transporters in colorectal neoplasia. Cancer Prev Res 1:93–99Google Scholar
  71. Howe LR, Subbaramaiah K, Chung WJ et al (1999) Transcriptional activation of cyclooxygenase-2 in wnt-1-transformed mouse mammary epithelial cells. Cancer Res 59:1572–1577PubMedGoogle Scholar
  72. Issa JP (2004) CpG island methylator phenotype in cancer. Nat Rev Cancer 4:988–993PubMedGoogle Scholar
  73. Jakobsson PJ, Thoren S, Morgenstern R et al (1999) Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc Nat Acad Sci USA 96:7220–7225PubMedGoogle Scholar
  74. Jemal A, Bray F, Center MM et al (2011) Global cancer statistics. CA Cancer J Clin 61:69–90PubMedGoogle Scholar
  75. Jing Q, Huang S, Guth S et al (2005) Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120:623–634PubMedGoogle Scholar
  76. Kaidi A, Qualtrough D, Williams AC et al (2006) Direct transcriptional up-regulation of cyclooxygenase-2 by hypoxia-inducible factor (HIF)-1 promotes colorectal tumor cell survival and enhances HIF-1 transcriptional activity during hypoxia. Cancer Res 66:6683–6691PubMedGoogle Scholar
  77. Kanies CL, Smith JJ, Kis C et al (2008) Oncogenic ras and transforming growth factor-beta synergistically regulate AU-rich element-containing mRNAs during epithelial to mesenchymal transition. Mol Cancer Res 6:1124–1136PubMedGoogle Scholar
  78. Karnes WE, Shattuck-Brandt R, Burgart LJ et al (1998) Reduced COX-2 protein in colorectal cancer with defective mismatch repair. Cancer Res 58:5473–5477PubMedGoogle Scholar
  79. Kedersha N, Stoecklin G, Ayodele M et al (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169:871–884PubMedGoogle Scholar
  80. Keene J (1999) Why is Hu where? Shuttling of early-response messenger RNA subsets. Proc Nat Acad Sci USA 96:5–7PubMedGoogle Scholar
  81. Kim Y, Fischer SM (1998) Transcriptional regulation of cyclooxygenase-2 in mouse skin carcinoma cells. Regulatory role of ccaat/enhancer-binding proteins in the differential expression of cyclooxygenase-2 in normal and neoplastic tissues. J Biol Chem 273:27686–27694PubMedGoogle Scholar
  82. Kojima M, Morisaki T, Izuhara K et al (2000) Lipopolysaccharide increases cyclo-oxygenase-2 expression in a colon carcinoma cell line through nuclear factor-kappa B activation. Oncogene 19:1225–1231PubMedGoogle Scholar
  83. Kondo Y, Issa JP (2004) Epigenetic changes in colorectal cancer. Cancer Metastasis Rev 23:29–39PubMedGoogle Scholar
  84. Kudo I, Murakami M (2005) Prostaglandin e synthase, a terminal enzyme for prostaglandin E2 biosynthesis. J Biochem Mol Biol 38:633–638PubMedGoogle Scholar
  85. Kulendran M, Stebbing JF, Marks CG et al (2011) Predictive and prognostic factors in colorectal cancer: a personalized approach. Cancers 3:1622–1638Google Scholar
  86. Kutchera W, Jones DA, Matsunami N et al (1996) Prostaglandin synthase 2 is abnormally expressed in human colon cancer: evidence for a transcriptional effect. Proc Nat Acad Sci USA 93:4816–4820PubMedGoogle Scholar
  87. Lai WS, Carballo E, Strum JR et al (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19:4311–4323PubMedGoogle Scholar
  88. Langsenlehner U, Yazdani-Biuki B, Eder T et al (2006) The cyclooxygenase-2 (PTGS2) 8473T > C polymorphism is associated with breast cancer risk. Clin Cancer Res 12:1392–1394PubMedGoogle Scholar
  89. Liu Q, Fu H, Sun F et al (2008) Mir-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res 36:5391–5404PubMedGoogle Scholar
  90. Lopez de Silanes I, Galban S, Martindale JL et al (2005a) Identification and functional outcome of mRNAs associated with RNA-binding protein tia-1. Mol Cell Biol 25:9520–9531PubMedGoogle Scholar
  91. Lopez de Silanes I, Lal A, Gorospe M (2005b) HuR: post-transcriptional paths to malignancy. RNA Biol 2:11–13PubMedGoogle Scholar
  92. Lopez de Silanes I, Quesada MP, Esteller M (2007) Aberrant regulation of messenger RNA 3′-untranslated region in human cancer. Cell Oncol 29:1–17PubMedGoogle Scholar
  93. Markowitz SD, Bertagnolli MM (2009) Molecular origins of cancer: molecular basis of colorectal cancer. N Engl J Med 361:2449–2460PubMedGoogle Scholar
  94. Markowitz S, Wang J, Myeroff L et al (1995) Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 268:1336–1338PubMedGoogle Scholar
  95. Masso Gonzalez EL, Patrignani P, Tacconelli S et al (2010) Variability among nonsteroidal antiinflammatory drugs in risk of upper gastrointestinal bleeding. Arthritis Rheum 62:1592–1601PubMedGoogle Scholar
  96. Mayr C, Bartel DP (2009) Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138:673–684PubMedGoogle Scholar
  97. Meade EA, McIntyre TM, Zimmerman GA et al (1999) Peroxisome proliferators enhance cyclooxygenase-2 expression in epithelial cells. J Biol Chem 274:8328–8334PubMedGoogle Scholar
  98. Mei JM, Hord NG, Winterstein DF et al (1999) Differential expression of prostaglandin endoperoxide H synthase-2 and formation of activated beta-catenin-lef-1 transcription complex in mouse colonic epithelial cells contrasting in APC. Carcinogenesis 20:737–740PubMedGoogle Scholar
  99. Meisner NC, Hintersteiner M, Mueller K et al (2007) Identification and mechanistic characterization of low-molecular-weight inhibitors for HuR. Nat Chem Biol 3:508–515PubMedGoogle Scholar
  100. Michael MZ, OC SM, van Holst Pellekaan NG et al (2003) Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 1:882–891PubMedGoogle Scholar
  101. Miller C, Zhang M, He Y et al (1998) Transcriptional induction of cyclooxygenase-2 gene by okadaic acid inhibition of phosphatase activity in human chondrocytes: co-stimulation of AP-1 and cre nuclear binding proteins. J Cell Biochem 69:392–413PubMedGoogle Scholar
  102. Ming XF, Stoecklin G, Lu M et al (2001) Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol Cell Biol 21:5778–5789PubMedGoogle Scholar
  103. Moore AE, Young LE, Dixon DA (2011) A common single-nucleotide polymorphism in cyclooxygenase-2 disrupts microRNA-mediated regulation. Oncogene (in press)Google Scholar
  104. Moran AE, Hunt DH, Javid SH et al (2004) APC deficiency is associated with increased EGFR activity in the intestinal enterocytes and adenomas of C57Bl/6j-Min/+ mice. J Biol Chem 279:43261–43272PubMedGoogle Scholar
  105. Moser AR, Luongo C, Gould KA et al (1995) APCmin: a mouse model for intestinal and mammary tumorigenesis. Eur J Cancer 31A:1061–1064PubMedGoogle Scholar
  106. Mukhopadhyay D, Houchen CW, Kennedy S et al (2003) Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol Cell 11:113–126PubMedGoogle Scholar
  107. Murakami M, Naraba H, Tanioka T et al (2000) Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2. J Biol Chem 275:32783–32792PubMedGoogle Scholar
  108. Murmu N, Jung J, Mukhopadhyay D et al (2004) Dynamic antagonism between RNA-binding protein cugbp2 and cyclooxygenase-2-mediated prostaglandin E2 in radiation damage. Proc Nat Acad Sci USA 101:13873–13878PubMedGoogle Scholar
  109. Myung SJ, Rerko RM, Yan M et al (2006) 15-hydroxyprostaglandin dehydrogenase is an in vivo suppressor of colon tumorigenesis. Proc Nat Acad Sci USA 103:12098–12102PubMedGoogle Scholar
  110. Nakanishi M, Gokhale V, Meuillet EJ et al (2010) mPGES-1 as a target for cancer suppression: a comprehensive invited review “phospholipase A2 and lipid mediators”. Biochimie 92:660–664PubMedGoogle Scholar
  111. Nakanishi M, Montrose DC, Clark P et al (2008) Genetic deletion of mPGES-1 suppresses intestinal tumorigenesis. Cancer Res 68:3251–3259PubMedGoogle Scholar
  112. Newbury SF, Muhlemann O, Stoecklin G (2006) Turnover in the alps: an mRNA perspective. Workshops on mechanisms and regulation of mRNA turnover. EMBO Rep 7:143–148PubMedGoogle Scholar
  113. Nomura T, Lu R, Pucci ML et al (2004) The two-step model of prostaglandin signal termination: in vitro reconstitution with the prostaglandin transporter and prostaglandin 15 dehydrogenase. Mol Pharmacol 65:973–978PubMedGoogle Scholar
  114. O’Hara SP, Mott JL, Splinter PL et al (2009) MicroRNAs: key modulators of post-transcriptional gene expression. Gastroenterology 136:17–25PubMedGoogle Scholar
  115. Oshima M, Dinchuk JE, Kargman SL et al (1996) Suppression of intestinal polyposis in APC∆716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803–809PubMedGoogle Scholar
  116. Ozhan G, Yanar TH, Ertekin C et al (2010) The effect of genetic polymorphisms of cyclooxygenase 2 on acute pancreatitis in Turkey. Pancreas 39:371–376PubMedGoogle Scholar
  117. Patrono C, Patrignani P, García Rodríguez LA (2001) Cyclooxygenase-selective inhibition of prostanoid formation: transducing biochemical selectivity into clinical read-outs. J Clin Invest 108:7–13PubMedGoogle Scholar
  118. Patrono C, Baigent C, Hirsh J et al (2008) Antiplatelet drugs: American college of chest physicians evidence-based clinical practice guidelines. Chest 133:199S–233S (8th edn)PubMedGoogle Scholar
  119. Peddareddigari VG, Wang D, Dubois RN (2011) The tumor microenvironment in colorectal carcinogenesis. Cancer Microenviron 3:149–166Google Scholar
  120. Phillips K, Kedersha N, Shen L et al (2004) Arthritis suppressor genes TIA-1 and TTP dampen the expression of tumor necrosis factor alpha, cyclooxygenase 2, and inflammatory arthritis. Proc Nat Acad Sci USA 101:2011–2016PubMedGoogle Scholar
  121. Prescott SM (2000) Is cyclooxygenase-2 the alpha and the omega in cancer? J Clin Invest 105:1511–1513PubMedGoogle Scholar
  122. Reid G, Wielinga P, Zelcer N et al (2003) The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc Nat Acad Sci USA 100:9244–9249PubMedGoogle Scholar
  123. Roberts RB, Min L, Washington MK et al (2002) Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis. Proc Nat Acad Sci USA 99:1521–1526PubMedGoogle Scholar
  124. Rothwell PM, Fowkes FG, Belch JF et al (2011) Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet 377:31–41PubMedGoogle Scholar
  125. Rothwell PM, Wilson M, Elwin CE et al (2010) Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials. Lancet 376:1741–1750PubMedGoogle Scholar
  126. Ryan BM, Robles AI, Harris CC (2010) Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer 10:389–402PubMedGoogle Scholar
  127. Sampey AV, Monrad S, Crofford LJ (2005) Microsomal prostaglandin E synthase-1: the inducible synthase for prostaglandin E2. Arthritis Res Ther 7:114–117PubMedGoogle Scholar
  128. Samuelsson B, Morgenstern R, Jakobsson PJ (2007) Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol Rev 59:207–224PubMedGoogle Scholar
  129. Sanchez-Beato M, Sanchez-Aguilera A, Piris MA (2003) Cell cycle deregulation in B-cell lymphomas. Blood 101:1220–1235PubMedGoogle Scholar
  130. Sanduja S, Blanco FF, Dixon DA (2010) The roles of TTP and BRF proteins in regulated mRNA decay. Wiley Interdisc Rev RNA 2:42–57Google Scholar
  131. Sawaoka H, Dixon DA, Oates JA et al (2003) Tristetrapolin binds to the 3′ untranslated region of cyclooxygenase-2 mRNA: a polyadenylation variant in a cancer cell line lacks the binding site. J Biol Chem 278:13928–13935PubMedGoogle Scholar
  132. Schmedtje JF Jr, Ji YS, Liu WL et al (1997) Hypoxia induces cyclooxygenase-2 via the NF-kappaB p65 transcription factor in human vascular endothelial cells. J Biol Chem 272:601–608PubMedGoogle Scholar
  133. Shanmugam N, Reddy MA, Natarajan R (2008) Distinct roles of heterogeneous nuclear ribonuclear protein K and microRNA-16 in cyclooxygenase-2 RNA stability induced by s100b, a ligand of the receptor for advanced glycation end products. J Biol Chem 283:36221–36233PubMedGoogle Scholar
  134. Shao J, Sheng H, Inoue H et al (2000) Regulation of constitutive cyclooxygenase-2 expression in colon carcinoma cells. J Biol Chem 275:33951–33956PubMedGoogle Scholar
  135. Shen J, Gammon MD, Terry MB et al (2006) Genetic polymorphisms in the cyclooxygenase-2 gene, use of nonsteroidal anti-inflammatory drugs, and breast cancer risk. Breast Cancer Res 8:R71–R80PubMedGoogle Scholar
  136. Sheng H, Shao J, Dixon DA et al (2000) Transforming growth factor-beta1 enhances Ha-ras-induced expression of cyclooxygenase-2 in intestinal epithelial cells via stabilization of mRNA. J Biol Chem 275:6628–6635PubMedGoogle Scholar
  137. Siezen CL, van Leeuwen AI, Kram NR et al (2005) Colorectal adenoma risk is modified by the interplay between polymorphisms in arachidonic acid pathway genes and fish consumption. Carcinogenesis 26:449–457PubMedGoogle Scholar
  138. Simmons DL, Botting RM, Hla T (2004) Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56:387–437PubMedGoogle Scholar
  139. Singer II, Kawka DW, Schloemann S et al (1998) Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 115:297–306PubMedGoogle Scholar
  140. Slaby O, Svoboda M, Fabian P et al (2007) Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology 72:397–402PubMedGoogle Scholar
  141. Song T, Zhang X, Wang C et al (2011) Expression of miR-143 reduces growth and migration of human bladder carcinoma cells by targeting cyclooxygenase-2. Asian Pac J Cancer Prev 12:929–933PubMedGoogle Scholar
  142. Steinbach G, Lynch PM, Phillips RK et al (2000) The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N Engl J Med 342:1946–1952PubMedGoogle Scholar
  143. Strillacci A, Griffoni C, Sansone P et al (2009) Mir-101 downregulation is involved in cyclooxygenase-2 overexpression in human colon cancer cells. Exp Cell Res 315:1439–1447PubMedGoogle Scholar
  144. Su H, Yang JR, Xu T et al (2009) MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 69:1135–1142PubMedGoogle Scholar
  145. Subbaramaiah K, Cole PA, Dannenberg AJ (2002a) Retinoids and carnosol suppress cyclooxygenase-2 transcription by creb-binding protein/p300-dependent and -independent mechanisms. Cancer Res 62:2522–2530PubMedGoogle Scholar
  146. Subbaramaiah K, Norton L, Gerald W et al (2002b) Cyclooxygenase-2 is overexpressed in HER-2/neu-positive breast cancer. Evidence for involvement of AP-1 and PEA3. J Biol Chem 277:18649–18657PubMedGoogle Scholar
  147. Sureban SM, Murmu N, Rodriguez P et al (2007) Functional antagonism between RNA binding proteins HuR and CUGBP2 determines the fate of COX-2 mRNA translation. Gastroenterology 132:1055–1065PubMedGoogle Scholar
  148. Sureban SM, Ramalingam S, Natarajan G et al (2008) Translation regulatory factor RBM3 is a proto-oncogene that prevents mitotic catastrophe. Oncogene 27:4544–4556PubMedGoogle Scholar
  149. Takagi T, Iio A, Nakagawa Y et al (2009) Decreased expression of microRNA-143 and -145 in human gastric cancers. Oncology 77:12–21PubMedGoogle Scholar
  150. Tian Q, Streuli M, Saito H et al (1991) A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Cell 67:629–639PubMedGoogle Scholar
  151. Toyota M, Shen L, Ohe-Toyota M et al (2000) Aberrant methylation of the cyclooxygenase 2 CpG island in colorectal tumors. Cancer Res 60:4044–4048PubMedGoogle Scholar
  152. Vane JR (1971) Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 231:232–523PubMedGoogle Scholar
  153. Varambally S, Cao Q, Mani RS et al (2008) Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322:1695–1699PubMedGoogle Scholar
  154. Vogel U, Christensen J, Wallin H et al (2008) Polymorphisms in genes involved in the inflammatory response and interaction with NSAID use or smoking in relation to lung cancer risk in a prospective study. Mutat Res 639:89–100PubMedGoogle Scholar
  155. Voltz R (2002) Paraneoplastic neurological syndromes: an update on diagnosis, pathogenesis, and therapy. Lancet Neurol 1:294–305PubMedGoogle Scholar
  156. Wang D, DuBois RN (2008) Pro-inflammatory prostaglandins and progression of colorectal cancer. Cancer Lett 267:197–203PubMedGoogle Scholar
  157. Wang D, Dubois RN (2010a) Eicosanoids and cancer. Nat Rev Cancer 10:181–193PubMedGoogle Scholar
  158. Wang D, Dubois RN (2010b) The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene 29:781–788PubMedGoogle Scholar
  159. Wang HJ, Ruan HJ, He XJ et al (2010) MicroRNA-101 is down-regulated in gastric cancer and involved in cell migration and invasion. Eur J Cancer 46:2295–2303PubMedGoogle Scholar
  160. Wang M, Song WL, Cheng Y et al (2008) Microsomal prostaglandin E synthase-1 inhibition in cardiovascular inflammatory disease. J Intern Med 263:500–505PubMedGoogle Scholar
  161. Wang D, Wang H, Shi Q et al (2004) Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta. Cancer Cell 6:285–295PubMedGoogle Scholar
  162. Wiemer EA (2007) The role of microRNAs in cancer: no small matter. Eur J Cancer 43:1529–1544PubMedGoogle Scholar
  163. Wiercinska-Drapalo A, Flisiak R, Prokopowicz D (1999) Effects of ulcerative colitis activity on plasma and mucosal prostaglandin E2 concentration. Prostaglandins Other Lipid Mediat 58:159–165PubMedGoogle Scholar
  164. Wu BL, Xu LY, Du ZP et al (2011) MiRNA profile in esophageal squamous cell carcinoma: downregulation of miR-143 and miR-145. World J Gastroenterol 17:79–88PubMedGoogle Scholar
  165. Wu WK, Sung JJ, Lee CW et al (2010) Cyclooxygenase-2 in tumorigenesis of gastrointestinal cancers: an update on the molecular mechanisms. Cancer Lett 295:7–16PubMedGoogle Scholar
  166. Yan M, Rerko RM, Platzer P et al (2004) 15-hydroxyprostaglandin dehydrogenase, a COX-2 oncogene antagonist, is a tgf-beta-induced suppressor of human gastrointestinal cancers. Proc Nat Acad Sci USA 101:17468–17473PubMedGoogle Scholar
  167. Yang X, Wang W, Fan J et al (2004) Prostaglandin a2-mediated stabilization of p21 mRNA through an erk-dependent pathway requiring the RNA-binding protein HuR. J Biol Chem 279:49298–49306PubMedGoogle Scholar
  168. Young LE, Dixon DA (2010) Post-transcriptional regulation of cyclooxygenase 2 expression in colorectal cancer. Curr Colorectal Cancer Rep 6:60–67PubMedGoogle Scholar
  169. Young LE, Moore AE, Sokol L et al. (2011) The mRNA stability factor HuR inhibits microRNA-16 targeting of cyclooxygenase-2. Mol Cancer Res (in press)Google Scholar
  170. Young LE, Sanduja S, Bemis-Standoli K et al (2009) The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis. Gastroenterology 136:1669–1679PubMedGoogle Scholar
  171. Zhu T, Gobeil F, Vazquez-Tello A et al (2006) Intracrine signaling through lipid mediators and their cognate nuclear G-protein-coupled receptors: a paradigm based on PGE2, PAF, and LPA1 receptors. Can J Physiol Pharmacol 84:377–391PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Cancer BiologyUniversity of Kansas Medical CenterKansasUSA
  2. 2.Center of Excellence on Aging (CeSI) and Department of Medicine and AgingG. d’Annunzio University, School of MedicineChietiItaly
  3. 3.Center of Excellence on Aging (CeSI) and Department of Neuroscience and ImagingG. d’Annunzio University, School of MedicineChietiItaly

Personalised recommendations