Cancer Letters
Volume 243, Issue 2 , Pages 255-263 , 18 November 2006

Cytoplasmic phospholipase A2 expression in human colon adenocarcinoma is correlated with cyclooxygenase-2 expression and contributes to prostaglandin E2 production

  • Valentine Panel

      Affiliations

    • INSERM, UMR S538, Paris, F-75012 France
    • ,
  • Pierre-Yves Boëlle

      Affiliations

    • INSERM, UMR S707, Paris, F-75012 France
    • ,
  • Jesus Ayala-Sanmartin

      Affiliations

    • INSERM, UMR S538, Paris, F-75012 France
    • ,
  • Anne-Marie Jouniaux

      Affiliations

    • INSERM, UMR S538, Paris, F-75012 France
    • ,
  • Richard Hamelin

      Affiliations

    • INSERM, UMR S762, Paris, F-75010 France
    • ,
  • Joëlle Masliah

      Affiliations

    • INSERM, UMR S538, Paris, F-75012 France
    • Université Pierre et Marie Curie-Paris6, Paris, France
    • ,
  • Germain Trugnan

      Affiliations

    • INSERM, UMR S538, Paris, F-75012 France
    • Université Pierre et Marie Curie-Paris6, Paris, France
    • ,
  • Jean-François Fléjou

      Affiliations

    • INSERM, UMR S762, Paris, F-75010 France
    • Université Pierre et Marie Curie-Paris6, Paris, France
    • AP-HP, Hôpital St Antoine, Department of Pathology, Paris, F-75012 France
    • ,
  • Dominique Wendum

      Affiliations

    • INSERM, UMR S538, Paris, F-75012 France
    • Université Pierre et Marie Curie-Paris6, Paris, France
    • AP-HP, Hôpital St Antoine, Department of Pathology, Paris, F-75012 France
    • Corresponding Author InformationCorresponding author. Address: Department of Pathology, Hopital Saint-Antoine, AP-HP, 184 rue du Faubourg Saint-Antoine, 75571 Paris Cedex 12, France. Fax: +33 1 49 28 28 78.

Received 17 August 2005 ,Revised 31 October 2005 ,Accepted 27 November 2005.

References 

  1. Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E, et al. Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell. 1996;87:803–809
  2. Chulada PC, Thompson MB, Mahler JF, Doyle CM, Gaul BW, Lee C, et al. Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res. 2000;60:4705–4708
  3. Eberhart CE, Coffey RJ, Radhika A, Giardiello FM, Ferrenbach S, DuBois RN. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology. 1994;107:1183–1188
  4. Hao X, Bishop AE, Wallace M, Wang H, Willcocks TC, Maclouf J, et al. Early expression of cyclo-oxygenase-2 during sporadic colorectal carcinogenesis. J. Pathol. 1999;187:295–301
  5. Sheng H, Shao J, Morrow JD, Beauchamp RD, DuBois RN. Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Res. 1998;58:362–366
  6. Sheng H, Shao J, Washington MK, DuBois RN. Prostaglandin E2 increases growth and motility of colorectal carcinoma cells. J. Biol. Chem. 2001;276:18075–18081
  7. Hansen-Petrik MB, McEntee MF, Jull B, Shi H, Zemel MB, Whelan J. Prostaglandin E(2) protects intestinal tumors from nonsteroidal anti-inflammatory drug-induced regression in Apc(Min/+) mice. Cancer Res. 2002;62:403–408
  8. Seno H, Oshima M, Ishikawa TO, Oshima H, Takaku K, Chiba T, et al. Cyclooxygenase 2- and prostaglandin E(2) receptor EP(2)-dependent angiogenesis in Apc(Delta716) mouse intestinal polyps. Cancer Res. 2002;62:506–511
  9. Balsinde J, Balboa MA, Insel PA, Dennis EA. Regulation and inhibition of phospholipase A2. Annu. Rev. Pharmacol. Toxicol. 1999;39:175–189
  10. Bonventre JV, Huang Z, Taheri MR, O'Leary E, Li E, Moskowitz MA, et al. Reduced fertility and postischaemic brain injury in mice deficient in cytosolic phospholipase A2. Nature. 1997;390:622–625
  11. Uozumi N, Kume K, Nagase T, Nakatani N, Ishii S, Tashiro F, et al. Role of cytosolic phospholipase A2 in allergic response and parturition. Nature. 1997;390:618–622
  12. Murakami M, Shimbara S, Kambe T, Kuwata H, Winstead MV, Tischfield JA, et al. The functions of five distinct mammalian phospholipase A2S in regulating arachidonic acid release. Type IIa and type V secretory phospholipase A2S are functionally redundant and act in concert with cytosolic phospholipase A2. J. Biol. Chem. 1998;273:14411–14423
  13. Fujishima H, Sanchez Mejia RO, Bingham CO, Lam BK, Sapirstein A, Bonventre JV, et al. Cytosolic phospholipase A2 is essential for both the immediate and the delayed phases of eicosanoid generation in mouse bone marrow-derived mast cells. Proc. Natl Acad. Sci. USA. 1999;96:4803–4807
  14. Takaku K, Sonoshita M, Sasaki N, Uozumi N, Doi Y, Shimizu T, et al. Suppression of intestinal polyposis in Apc(delta 716) knockout mice by an additional mutation in the cytosolic phospholipase A(2) gene. J. Biol. Chem. 2000;275:34013–34016
  15. Hong KH, Bonventre JC, O'Leary E, Bonventre JV, Lander ES. Deletion of cytosolic phospholipase A(2) suppresses Apc(Min)-induced tumorigenesis. Proc. Natl Acad. Sci. USA. 2001;98:3935–3939
  16. Dong M, Guda K, Nambiar PR, Rezaie A, Belinsky GS, Lambeau G, et al. Inverse association between phospholipase A2 and COX-2 expression during mouse colon tumorigenesis. Carcinogenesis. 2003;24:307–315
  17. Ilsley JN, Nakanishi M, Flynn C, Belinsky GS, De Guise S, Adib JN, et al. Cytoplasmic phospholipase A2 deletion enhances colon tumorigenesis. Cancer Res. 2005;65:2636–2643
  18. Soydan AS, Tavares IA, Weech PK, Temblay NM, Bennett A. High molecular weight phospholipase A2 and fatty acids in human colon tumours and associated normal tissue. Eur. J. Cancer. 1996;32A:1781–1787
  19. Dimberg J, Samuelsson A, Hugander A, Soderkvist P. Gene expression of cyclooxygenase-2, group II and cytosolic phospholipase A2 in human colorectal cancer. Anticancer Res. 1998;18:3283–3287
  20. Morioka Y, Ikeda M, Saiga A, Fujii N, Ishimoto Y, Arita H, et al. Potential role of group X secretory phospholipase A(2) in cyclooxygenase-2-dependent PGE(2) formation during colon tumorigenesis. Fed. Eur. Biochem. Soc. Lett. 2000;487:262–266
  21. Osterstrom A, Dimberg J, Fransen K, Soderkvist P. Expression of cytosolic and group X secretory phospholipase A(2) genes in human colorectal adenocarcinomas. Cancer Lett. 2002;182:175–182
  22. Wendum D, Svrcek M, Rigau V, Boelle PY, Sebbagh N, Parc R, et al. Inflammatory secreted PLA2, and cytoplasmic PLA2 protein expression in small bowel adenocarcinomas compared with colorectal adenocarcinomas. Mod. Pathol. 2003;16:130–136
  23. Dong M, Johnson M, Rezaie A, Ilsley JN, Nakanishi M, Sanders MM, et al. Cytoplasmic phospholipase A2 levels correlate with apoptosis in human colon tumorigenesis. Clin. Cancer Res. 2005;11:2265–2271
  24. S.R. Hamilton, L.A. Aaltonen (Eds.), World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Digestive System, IARC Press, Lyon, 2000.
  25. Rigau V, Sebbagh N, Olschwang S, Paraf F, Mourra N, Parc Y, et al. Microsatellite instability in colorectal carcinoma. The comparison of immunohistochemistry and molecular biology suggests a role for hMSH6 [correction of hMLH6] immunostaining. Arch. Pathol. Lab. Med. 2003;127:694–700
  26. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, et al. A national cancer institute workshop on microsatellite instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res. 1998;58:5248–5257
  27. Umar A, Boland CR, Terdiman JP, Syngal S, de la Chapelle A, Ruschoff J, et al. Revised bethesda guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J. Natl Cancer Inst. 2004;96:261–268
  28. Marcus VA, Madlensky L, Gryfe R, Kim H, So K, Millar A, et al. Immunohistochemistry for hMLH1 and hMSH2: a practical test for DNA mismatch repair-deficient tumors. Am. J. Surg. Pathol. 1999;23:1248–1255
  29. Soydan AS, Tavares IA, Weech PK, Tremblay NM, Bennett A. High molecular weight phospholipase A2: its occurrence and quantification in human colon cancer and normal mucosa. Adv. Exp. Med. Biol. 1997;400A:31–37
  30. Kashiwagi M, Friess H, Uhl W, Berberat P, Abou-Shady M, Martignoni M, et al. Group II and IV phospholipase A(2) are produced in human pancreatic cancer cells and influence prognosis. Gut. 1999;45:605–612
  31. Zhi H, Zhang J, Hu G, Lu J, Wang X, Zhou C, et al. The deregulation of arachidonic acid metabolism-related genes in human esophageal squamous cell carcinoma. Int. J. Cancer. 2003;106:327–333
  32. Maxwell AP, Goldberg HJ, Tay AH, Li ZG, Arbus GS, Skorecki KL. Epidermal growth factor and phorbol myristate acetate increase expression of the mRNA for cytosolic phospholipase A2 in glomerular mesangial cells. Biochem. J. 1993;295:763–766
  33. Wu T, Ikezono T, Angus CW, Shelhamer JH. Tumor necrosis factor-alpha induces the 85-kDa cytosolic phospholipase A2 gene expression in human bronchial epithelial cells. Biochim. Biophys. Acta. 1996;1310:175–184
  34. Guthridge CJ, Stampfer MR, Clark MA, Steiner MR. Phospholipases A2 in ras-transformed and immortalized human mammary epithelial cells. Cancer Lett. 1994;86:11–21
  35. Heasley LE, Thaler S, Nicks M, Price B, Skorecki K, Nemenoff RA. Induction of cytosolic phospholipase A2 by oncogenic Ras in human non-small cell lung cancer. J. Biol. Chem. 1997;272:14501–14504
  36. Six DA, Dennis EA. The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim. Biophys. Acta. 2000;1488:1–19
  37. Kennedy BP, Soravia C, Moffat J, Xia L, Hiruki T, Collins S. Overexpression of the nonpancreatic secretory group II PLA2 messenger RNA and protein in colorectal adenomas from familial adenomatous polyposis patients. Cancer Res. 1998;58:500–503
  38. Murakami M, Yoshihara K, Shimbara S, Sawada M, Inagaki N, Nagai H, et al. Group IID heparin-binding secretory phospholipase A(2) is expressed in human colon carcinoma cells and human mast cells and up-regulated in mouse inflammatory tissues. Eur. J. Biochem. 2002;269:2698–2707
  39. Murakami M, Kudo I. Recent advances in molecular biology and physiology of the prostaglandin E2-biosynthetic pathway. Prog. Lipid Res. 2004;43:3–35
  40. Murakami M, Kambe T, Shimbara S, Kudo I. Functional coupling between various phospholipase A2s and cyclooxygenases in immediate and delayed prostanoid biosynthetic pathways. J. Biol. Chem. 1999;274:3103–3115
  41. Bailleux A, Wendum D, Audubert F, Jouniaux AM, Koumanov K, Trugnan G, et al. Cytosolic phospholipase A2-p11 interaction controls arachidonic acid release as a function of epithelial cell confluence. Biochem. J. 2004;378:307–315
  42. Meyer AM, Dwyer-Nield LD, Hurteau GJ, Keith RL, O'Leary E, You M, et al. Decreased lung tumorigenesis in mice genetically deficient in cytosolic phospholipase A2. Carcinogenesis. 2004;25:1517–1524(Epub 2004 Mar 1519)
  43. Laye JP, Gill JH. Phospholipase A2 expression in tumours: a target for therapeutic intervention?. Drug Discov. Today. 2003;8:710–716
  44. Karnes 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;58:5473–5477
  45. 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;117:350–358
  46. Wendum D, Boelle PY, Rigau V, Sebbagh N, Olschwang S, Mourra N, et al. Mucinous colon carcinomas with microsatellite instability have a lower microvessel density and lower vascular endothelial growth factor expression. Virch. Arch. 2003;442:111–117
  47. Sheehan KM, Sheahan K, O'Donoghue DP, MacSweeney F, Conroy RM, Fitzgerald DJ, et al. The relationship between cyclooxygenase-2 expression and colorectal cancer. Jama. 1999;282:1254–1257
  48. Zhang H, Sun XF. Overexpression of cyclooxygenase-2 correlates with advanced stages of colorectal cancer. Am. J. Gastroenterol. 2002;97:1037–1041
  49. Jayadev S, Hayter HL, Andrieu N, Gamard CJ, Liu B, Balu R, et al. Phospholipase A2 is necessary for tumor necrosis factor alpha-induced ceramide generation in L929 cells. J. Biol. Chem. 1997;272:17196–17203
  50. Selzner M, Bielawska A, Morse MA, Rudiger HA, Sindram D, Hannun YA, et al. Induction of apoptotic cell death and prevention of tumor growth by ceramide analogues in metastatic human colon cancer. Cancer Res. 2001;61:1233–1240

PII: S0304-3835(05)01037-2

doi: 10.1016/j.canlet.2005.11.045

Cancer Letters
Volume 243, Issue 2 , Pages 255-263 , 18 November 2006

Article Tools

* Image Usage & Resolution