CXCL1 induced by prostaglandin E2 promotes angiogenesis in colorectal cancer

Journal of Experimental Medicine

Volumn 203, Issue 4, 2006, Pages 941-951

  Wang, Dingzhi ^a   Wang, Haibin ^a   Brown, Joanne ^a   Daikoku, Takiko ^a   Ning, Wei ^a   Shi, Qiong ^a   Richmond, Ann ^b   Strieter, Robert ^d   Dey, Sudhansu K ^a,b,c   DuBois, Raymond N ^a,b,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; PROSTAGLANDIN E2;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CANCER CELL; CARCINOMA CELL; CELL MIGRATION; COLORECTAL CANCER; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MEDIATOR RELEASE; MICROVASCULATURE; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; TISSUE LEVEL; TUMOR GROWTH;

ADENOMA; ANIMALS; CACO-2 CELLS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINES, CXC; COLORECTAL NEOPLASMS; DINOPROSTONE; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; MICE, SCID; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; NEOVASCULARIZATION, PATHOLOGIC; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INTERLEUKIN-8B;

EID: 33645850713     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052124     Document Type: Article

References (64)

1. Kuper, H., H.O. Adami, and D. Trichopoulos. 2000. Infections as a major preventable cause of human cancer. J. Intern. Med. 248:171-183.
2. DuBois, R.N., S.B. Abramson, L. Crofford, R.A. Gupta, L.S. Simon, L.B. Van De Putte, and P.E. Lipsky. 1998.Cyclooxygenase in biology and disease. FASEB J. 12:1063-1073.
3. Hoffmann, E., O. Dittrich-Breiholz, H. Holtmann, and M. Kracht. 2002. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 72:847-855.
4. Anisowicz, A., M. Messineo, S.W. Lee, and R. Sager. 1991. An NF-kappa B-like transcription factor mediates IL-1/TNF-alpha induction of gro in human fibroblasts. J. Immunol. 147:520-527.
5. Pugh, S., and G.A. Thomas. 1994. Patients with adenomatous polyps and carcinomas have increased colonic mucosal prostaglandin E 2. Gut. 35:675-678.
6. Rigas, B., I.S. Goldman, and L. Levine. 1993. Altered eicosanoid levels in human colon cancer. J. Lab. Clin. Med. 122:518-523.
7. Mahmoud, N.N., A.J. Dannenberg, R.T. Bilinski, J.R. Mestre, A. Chadburn, M. Churchill, C. Martucci, and M.M. Bertagnolli. 1999. Administration of an unconjugated bile acid increases duodenal tumors in a murine model of familial adenomatous polyposis. Carcinogenesis. 20:299-303.
8. Giardiello, F.M., R.A. Casero Jr., S.R. Hamilton, L.M. Hylind, J.D. Trimbath, D.E. Geiman, K.R. Judge, W. Hubbard, G.J. Offerhaus, and V.W. Yang. 2004. Prostanoids, ornithine decarboxylase, and polyamines in primary chemoprevention of familial adenomatous polyposis. Gastroenterology. 126:425-431.
9. Wang, D., H. Wang, Q. Shi, S. Katkuri, W. Walhi, B. Desvergne, S.K. Das, S.K. Dey, and R.N. DuBois. 2004. Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta. Cancer Cell. 6:285-295.
10. Jones, M.K., H. Wang, B.M. Peskar, E. Levin, R.M. Itani, I.J. Sarfeh, and A.S. Tarnawski. 1999. Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing. Nat. Med. 5:1418-1423.
11. Hammond, M.E., V. Shyamala, M.A. Siani, C.A. Gallegos, P.H. Feucht, J. Abbott, G.R. Lapointe, M. Moghadam, H. Khoja, J. Zakel, and P. Tekamp-Olson. 1996. Receptor recognition and specificity of interleukin-8 is determined by residues that cluster near a surface-accessible hydrophobic pocket. J. Biol. Chem. 271:8228-8235.
12. Anisowicz, A., L. Bardwell, and R. Sager. 1987. Constitutive overexpression of a growth-regulated gene in transformed Chinese hamster and human cells. Proc. Natl. Acad. Sci. USA. 84:7188-7192.
13. Richmond, A., D.H. Lawson, D.W. Nixon, and R.K. Chawla. 1985. Characterization of autostimulatory and transforming growth factors from human melanoma cells. Cancer Res. 45:6390-6394.
14. Richmond, A., and H.G. Thomas. 1986. Purification of melanoma growth stimulatory activity. J. Cell. Physiol. 129:375-384.
15. Cochran, B.H., A.C. Reffel, and C.D. Stiles. 1983. Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell. 33:939-947.
16. Tekamp-Olson, P., C. Gallegos, D. Bauer, J. McClain, B. Sherry, M. Fabre, S. van Deventer, and A. Cerami. 1990. Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J. Exp. Med. 172:911-919.
17. Luan, J., R. Shattuck-Brandt, H. Haghnegahdar, J.D. Owen, R. Strieter, M. Burdick, C. Nirodi, D. Beauchamp, K.N. Johnson, and A. Richmond. 1997. Mechanism and biological significance of constitutive expression of MGSA/GRO chemokines in malignant melanoma tumor progression. J. Leukoc. Biol. 62:588-597.
18. Balentien, E., B.E. Mufson, R.L. Shattuck, R. Derynck, and A. Richmond. 1991. Effects of MGSA/GRO alpha on melanocyte transformation. Oncogene. 6:1115-1124.
19. Strieter, R.M., P.J. Polverini, S.L. Kunkel, D.A. Arenberg, M.D. Burdick, J. Kasper, J. Dzuiba, J. Van Damme, A. Walz, D. Marriott, et al. 1995. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem. 270:27348-27357.
20. Lane, B.R., J. Liu, P.J. Bock, D. Schols, M.J. Coffey, R.M. Strieter, P.J. Polverini, and D.M. Markovitz. 2002. Interleukin-8 and growth-regulated oncogene alpha mediate angiogenesis in Kaposi's sarcoma. J. Virol. 76:11570-11583.
21. Arenberg, D.A., P.J. Polverini, S.L. Kunkel, A. Shanafelt, J. Hesselgesser, R. Horuk, and R.M. Strieter. 1997. The role of CXC chemokines in the regulation of angiogenesis in non-small cell lung cancer. J. Leukoc. Biol. 62:554-562.
22. Kettunen, H.L., A.S. Kettunen, and N.E. Rautonen. 2003. Intestinal immune responses in wild-type and Apcmin/+ mouse, a model for colon cancer. Cancer Res. 63:5136-5142.
23. Buchanan, F.G., D. Wang, F. Bargiacchi, and R.N. DuBois. 2003. Prostaglandin E2 regulates cell migration via the intracellular activation of the epidermal growth factor receptor. J. Biol. Chem. 278:35451-35457.
24. Sheng, H., J. Shao, M.K. Washington, and R.N. DuBois. 2001. Prostaglandin E2 increases growth and motility of colorectal carcinoma cells. J. Biol. Chem. 276:18075-18081.
25. Tsujii, M., S. Kawano, S. Tsuji, H. Sawaoka, M. Hori, and R.N. DuBois. 1998. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell. 93:705-716.
26. Eberhart, C.E., R.J. Coffey, A. Radhika, F.M. Giardiello, S. Ferrenbach, and R.N. DuBois. 1994. Up-regulation of cyclooxygenase-2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology. 107:1183-1188.
27. Marnett, L.J., and R.N. DuBois. 2002. COX-2: a target for colon cancer prevention. Annu. Rev. Pharmacol. Toxicol. 42:55-80.
28. Sheehan, K.M., K. Sheahan, D.P. O'Donoghue, F. MacSweeney, R.M. Conroy, D.J. Fitzgerald, and F.E. Murray. 1999. The relationship between cyclooxygenase-2 expression and colorectal cancer. JAMA. 282:1254-1257.
29. Khuri, F.R., H. Wu, J.J. Lee, B.L. Kemp, R. Lotan, S.M. Lippman, L. Feng, W.K. Hong, and X.C. Xu. 2001. Cyclooxygenase-2 overexpression is a marker of poor prognosis in stage I non-small cell lung cancer. Clin. Cancer Res. 7:861-867.
30. Ristimaki, A., A. Sivula, J. Lundin, M. Lundin, T. Salminen, C. Haglund, H. Joensuu, and J. Isola. 2002. Prognostic significance of elevated cyclooxygenase-2 expression in breast cancer. Cancer Res. 62:632-635.
31. Gaffney, D.K., J. Holden, M. Davis, K. Zempolich, K.J. Murphy, and M. Dodson. 2001. Elevated cyclooxygenase-2 expression correlates with diminished survival in carcinoma of the cervix treated with radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 49:1213-1217.
32. Buskens, C.J., B.P. Van Rees, A. Sivula, J.B. Reitsma, C. Haglund, P.J. Bosma, G.J. Offerhaus, J.J. Van Lanschot, and A. Ristimaki. 2002. Prognostic significance of elevated cyclooxygenase 2 expression in patients with adenocarcinoma of the esophagus. Gastroenterology. 122:1800-1807.
33. Gupta, R.A., and R.N. Dubois. 2001. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat. Rev. Cancer. 1:11-21.
34. Chulada, P.C., M.B. Thompson, J.F. Mahler, C.M. Doyle, B.W. Gaul, C. Lee, H.F. Tiano, S.G. Morham, O. Smithies, and R. Langenbach. 2000. Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res. 60:4705-4708.
35. Williams, C.S., M. Tsujii, J. Reese, S.K. Dey, and R.N. DuBois. 2000. Host cyclooxygenase-2 modulates carcinoma growth. J. Clin. Invest. 105:1589-1594.
36. Δ716 knockout mice by inhibition of prostaglandin endoperoxide synthase-2 (COX-2). Cell. 87:803-809.
37. Folkman, J. 1995. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1:27-31.
38. Folkman, J. 1971. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285:1182-1186.
39. Zetter, B.R. 1998. Angiogenesis and tumor metastasis. Annu. Rev. Med. 49:407-424.
40. Hanahan, D., and J. Folkman. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:353-364.
41. Arenberg, D.A., S.L. Kunkel, P.J. Polverini, M. Glass, M.D. Burdick, and R.M. Strieter. 1996. Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice. J. Clin. Invest. 97:2792-2802.
42. Risau, W. 1997. Mechanisms of angiogenesis. Nature. 386:671-674.
43. Korpelainen, E.I., and K. Alitalo. 1998. Signaling angiogenesis and lymphangiogenesis. Curr. Opin. Cell Biol. 10:159-164.
44. Neufeld, G., T. Cohen, S. Gengrinovitch, and Z. Poltorak. 1999. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13:9-22.
45. Hurwitz, H., L. Fehrenbacher, W. Novotny, T. Cartwright, J. Hainsworth, W. Heim, J. Berlin, A. Baron, S. Griffing, E. Holmgren, et al. 2004. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350:2335-2342.
46. Franson, P.J., and D.V. Lapka. 2005. Antivascular endothelial growth factor monoclonal antibody therapy: a promising paradigm in colorectal cancer. Clin. J. Oncol. Nurs. 9:55-60.
47. Balkwill, F. 2004. Cancer and the chemokine network. Nat. Rev. Cancer. 4:540-550.
48. Balkwill, F. 2004. The significance of cancer cell expression of the chemokine receptor CXCR 4. Semin. Cancer Biol. 14:171-179.
49. Lin, E.Y., A.V. Nguyen, R.G. Russell, and J.W. Pollard. 2001. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193:727-740.
50. Jing, H., E. Vassiliou, and D. Ganea. 2003. Prostaglandin E2 inhibits production of the inflammatory chemokines CCL3 and CCL4 in dendritic cells. J. Leukoc. Biol. 74:868-879.
51. Jing, H., J.H. Yen, and D. Ganea. 2004. A novel signaling pathway mediates the inhibition of CCL3/4 expression by prostaglandin E 2. J. Biol. Chem. 279:55176-55186.
52. Takayama, K., G. Garcia-Cardena, G.K. Sukhova, J. Comander, M.A. Gimbrone Jr., and P. Libby. 2002. Prostaglandin E2 suppresses chemokine production in human macrophages through the EP4 receptor. J. Biol. Chem. 277:44147-44154.
53. Balkwill, F., and A. Mantovani. 2001. Inflammation and cancer: back to Virchow? Lancet. 357:539-545.
54. Bottazzi, B., N. Polentarutti, R. Acero, A. Balsari, D. Boraschi, P. Ghezzi, M. Salmona, and A. Mantovani. 1983. Regulation of the macrophage content of neoplasms by chemoattractants. Science. 220:210-212.
55. Pold, M., L.X. Zhu, S. Sharma, M.D. Burdick, Y. Lin, P.P. Lee, A. Pold, J. Luo, K. Krysan, M. Dohadwala, et al. 2004. Cyclooxygenase-2-dependent expression of angiogenic CXC chemokines ENA-78/CXC Ligand (CXCL) 5 and interleukin-8/CXCL8 in human non-small cell lung cancer. Cancer Res. 64:1853-1860.
56. Heidemann, J., H. Ogawa, M.B. Dwinell, P. Rafiee, C. Maaser, H.R. Gockel, M.F. Otterson, D.M. Ota, N. Lugering, W. Domschke, and D.G. Binion. 2003. Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR 2. J. Biol. Chem. 278:8508-8515.
57. Hillyer, P., E. Mordelet, G. Flynn, and D. Male. 2003. Chemokines, chemokine receptors and adhesion molecules on different human endothelia: discriminating the tissue-specific functions that affect leucocyte migration. Clin. Exp. Immunol. 134:431-441.
58. Dormond, O., A. Foletti, C. Paroz, and C. Ruegg. 2001. NSAIDs inhibit alpha V beta 3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nat. Med. 7:1041-1047.
59. Dormond, O., M. Bezzi, A. Mariotti, and C. Ruegg. 2002. Prostaglandin E2 promotes integrin alpha Vbeta 3-dependent endothelial cell adhesion, rac-activation, and spreading through cAMP/PKA-dependent signaling. J. Biol. Chem. 277:45838-45846.
60. Wang, D., J. Sai, G. Carter, A. Sachpatzidis, E. Lolis, and A. Richmond. 2002. PAK1 kinase is required for CXCL1-induced chemotaxis. Biochemistry. 41:7100-7107.
61. DuBois, R.N., J. Awad, J. Morrow, L.J. Roberts, and P.R. Bishop. 1994. Regulation of eicosanoid production and mitogenesis in rat intestinal epithelial cells by transforming growth factor-α and phorbol ester. J. Clin. Invest. 93:493-498.
62. Nirodi, C., S. NagDas, S.P. Gygi, G. Olson, R. Aebersold, and A. Richmond. 2001. A role for poly(ADP-ribose) polymerase in the transcriptional regulation of the melanoma growth stimulatory activity (CXCL1) gene expression. J. Biol. Chem. 276:9366-9374.
63. Greenberg, L.H., and O.D. Slayden. 2004. Human endometriotic xenografts in immunodeficient RAG-2/gamma(c)KO mice. Am. J. Obstet. Gynecol. 190:1788-1795.
64. Ma, W., J. Tan, H. Matsumoto, B. Robert, D.R. Abrahamson, S.K. Das, and S.K. Dey. 2001. Adult tissue angiogenesis: evidence for negative regulation by estrogen in the uterus. Mol. Endocrinol. 15:1983-1992.