Production of chemokine CXCL1/KC by okadaic acid through the nuclear factor-κB pathway

Carcinogenesis

Volumn 27, Issue 1, 2006, Pages 43-52

  Feng, Gong ^a   Ohmori, Yoshihiro ^b   Chang, Pi Ling ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b MEIKAI UNIVERSITY SCHOOL OF DENTISTRY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CXCL1 CHEMOKINE; DIMER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUCIFERASE; MESSENGER RNA; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN P50; PROTEIN SUBUNIT; SERINE DERIVATIVE; SYNAPTOTAGMIN; TRANSCRIPTION FACTOR REL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL LINE; CELL NUCLEUS; CELL STIMULATION; COMPLEX FORMATION; CONTROLLED STUDY; EPIDERMIS CELL; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUSION; GENE MUTATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA SYNTHESIS; TRANSACTIVATION; TUMOR PROMOTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CARCINOGENS; CELL NUCLEUS; CELLS, CULTURED; CHEMOKINE CXCL1; CHEMOKINES, CXC; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPIDERMIS; GENE EXPRESSION REGULATION; LUCIFERASES; MICE; NF-KAPPA B; OKADAIC ACID; PROMOTER REGIONS (GENETICS); PROMOTER REGIONS, GENETIC; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 29744464706     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgi174     Document Type: Article

References (59)

1. U.S. Food and Drug Administration (2001) Fish and fishery products hazards and controls guidance. In Natural Toxin. 3rd edn, Chapter 6, pp. 73-82.
2. Tachibana,K., Scheuer,P.J., Tsukitani,Y., Kikuchi,H., Van Engen,D., Clardy,J., Gopichand,Y. and Schmitz,F.J. (1981) Okadaic acid, a cytotoxic polyether from two marine sponges of the genus Halichondria. J. Am. Chem. Soc., 103, 2469-2471.
3. Suganuma,M., Fujiki,H., Okabe,S., Nishiwaki,S., Brautigan,D., Ingebritsen,T.S. and Rosner,M.R. (1992) Structurally different members of the okadaic acid class selectively inhibit protein serine/threonine but not tyrosine phosphatase activity. Toxicon., 30, 873-878.
4. Hescheler,J., Mieskes,G., Ruegg,J.C., Takai,A. and Trautwein,W. (1988) Effects of a protein phosphatase inhibitor, okadaic acid, on membrane currents of isolated guinea-pig cardiac myocytes. Pflugers Arch., 412, 248-252.
5. Maynes,J.T., Bateman,K.S., Cherney,M.M., Das,A.K., Luu,H.A., Holmes,C.F. and James,M.N. (2001) Crystal structure of the tumor-promoter okadaic acid bound to protein phosphatase-1. J. Biol. Chem., 276, 44078-44082.
6. Gupta,V., Ogawa,A.K., Du,X., Houk,K.N. and Armstrong,R.W. (1997) A model for binding of structurally diverse natural product inhibitors of protein phosphatases PP1 and PP2A. J. Med. Chem., 40, 3199-3206.
7. Bialojan,C. and Takai,A. (1988) Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem. J., 256, 283-290.
8. Suganuma,M., Fujiki,H., Suguri,H., Yoshizawa,S., Hirota,M., Nakayasu,M., Ojika,M., Wakamatsu,K., Yamada,K. and Sugimura,T. (1988) Okadaic acid: an additional non-phorbol-12-tetradecanoate-13-acetate-type tumor promoter. Proc. Natl Acad. Sci. USA, 85, 1768-1771.
9. Herschman,H.R., Lim,R.W., Brankow,D.W. and Fujiki,H. (1989) The tumor promoters 12-O-tetradecanoylphorbol-13-acetate and okadaic acid differ in toxicity, mitogenic activity and induction of gene expression. Carcinogenesis, 10, 1495-1498.
10. Fujiki,H., Suganuma,M., Yoshizawa,S., Kanazawa,H., Sugimura,T., Manam,S., Kahn,S.M., Jiang,W., Hoshina,S. and Weinstein, I.B. (1989) Codon 61 mutations in the c-Harvey-ras gene in mouse skin tumors induced by 7,12-dimethylbenz[a]anthracene plus okadaic acid class tumor promoters. Mol. Carcinog., 2, 184-187.
11. Kim,H.J., Lee,M.H., Shin,H.I., Choi,J.Y. and Ryoo,H.M. (2002) Okadaic acid stimulates osteopontin expression through de novo induction of AP-1. J. Cell. Biochem., 87, 93-102.
12. Yang,J., Fan,G.H., Wadzinski,B.E., Sakurai,H. and Richmond,A. (2001) Protein phosphatase 2A interacts with and directly dephosphorylates RelA. J. Biol. Chem., 276, 47828-47833.
13. Hsu,T.C., Nair,R., Tulsian,P., Camalier,C.E., Hegamyer,G.A., Young,M.R. and Colbum,N.H. (2001) Transformation nonresponsive cells owe their resistance to lack of p65/nuclear factor-kappaB activation. Cancer Res., 61, 4160-4168.
14. Dong,Z., Birrer,M.J., Watts,R.G., Matrisian,L.M. and Colburn,N.H. (1994) Blocking of tumor promoter-induced AP-1 activity inhibits induced transformation in JB6 mouse epidermal cells. Proc. Natl Acad. Sci. USA, 91, 609-613.
15. Budunova,I.V., Kowalczyk,D., Perez,P., Yao,Y.J., Jorcano,J.L. and Slaga,T.J. (2003) Glucocorticoid receptor functions as a potent suppressor of mouse skin carcinogenesis. Oncogene, 22, 3279-3287.
16. Young,M.R., Li,J.J., Rincon,M., Flavell,R.A., Sathyanarayana,B.K., Hunziker,R. and Colbum,N. (1999) Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc. Natl Acad. Sci. USA, 96, 9827-9832.
17. Martin-Oliva,D., O'Valle,F., Munoz-Gamez,J.A., Valenzuela,M.T., Nunez,M.I., Aguilar,M., Ruiz de Almodovar,J.M., Garcia del Moral,R. and Oliver,F.J. (2004) Crosstalk between PARP-1 and NF-kappaB modulates the promotion of skin neoplasia. Oncogene, 23, 5275-5283.
18. Hermann,R., Hensel,F., Muller,E.C., Keppler,M., Souto-Carneiro,M., Brandlein,S., Muller-Hermelink,H.K. and Vollmers,H.P. (2001) Deactivation of regulatory proteins hnRNP A1 and A2 during SC-1 induced apoptosis. Hum. Antibodies, 10, 83-90.
19. Moore,R.J., Owens,D.M., Stamp,G., Arnott,C., Burke,F., East,N., Holdsworth,H., Turner,L., Rollins,B., Pasparakis,M., Kollias,G. and Balkwill,F. (1999) Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med., 5, 828-831.
20. Suganuma,M., Okabe,S., Marino,M.W., Sakai,A., Sueoka,E. and Fujiki,H. (1999) Essential role of tumor necrosis factor alpha (TNF-alpha) in tumor promotion as revealed by TNF-alpha-deficient mice. Cancer Res., 59, 4516-4518.
21. Suganuma,M., Okabe,S., Kurusu,M., Iida,N., Ohshima,S., Saeki,Y., Kishimoto,T. and Fujiki,H. (2002) Discrete roles of cytokines, TNF-alpha, IL-1, IL-6 in tumor promotion and cell transformation. Int. J. Oncol., 20, 131-136.
22. Zlotnik,A. and Yoshie,O. (2000) Chemokines: A new classification system and their role in immunity. Immunity, 12, 121-127.
23. Bozic,C.R., Gerard,N.P., von Uexkull-Guldenband,C., Kolakowski,L.F.Jr, Conklyn,M.J., Breslow,R., Showell, H.J. and Gerard,C. (1994) The murine interleukin 8 type B receptor homologue and its ligands. Expression and biological characterization. J. Biol. Chem., 269, 29355-19358.
24. Lee,J., Cacalano,G., Camerato,T., Toy,K., Moore,M.W. and Wood,W.I. (1995) Chemokine binding and activities mediated by the mouse IL-8 receptor. J. Immunol., 155, 2158-2164.
25. Heinrich,J.N. and Bravo,R. (1995) The orphan mouse receptor imerleukin (IL)-8R beta binds N51. Structure-function analysis using N51/IL-8 chimeric molecules. J. Biol. Chem., 270, 4987-4989.
26. Oquendo,P., Alberta,J., Wen,D.Z., Graycar,J.L., Derynck,R. and Stiles,C.D. (1989) The platelet-derived growth factor-inducible KC gene encodes a secretory protein related to platelet alpha-granule proteins. J. Biol. Chem., 264, 4133-4137.
27. Lira,S.A., Zalamea,P., Heinrich,J.N., Fuentes, M.E., Carrasco,D., Lewin,A.C., Barton,D.S., Durham,S. and Bravo,R. (1994) Expression of the chemokine N51/KC in the thymus and epidermis of transgenic mice results in marked infiltration of a single class of inflammatory cells. J. Exp. Med., 180, 2039-3048.
28. Ohmori,Y. and Hamilton,T.A. (1994) IFN-gamma selectively inhibits lipopolysaccharide-inducible JE/monocyte chemoattractant protein-1 and KC/GRO/melanoma growth-stimulating activity gene expression in mouse peritoneal macrophages. J. Immunol., 153, 2204-2212.
29. Ueland,J.M., Gwira,J., Liu,Z.X. and Cantley,L.G. (2004) The chemokine KC regulates HGF-stimulated epithelial cell morphogenesis. Am. J. Physiol. Renal. Physiol., 286, F581-F589.
30. Loukinova,E., Dong,G., Enamorado-Ayalya,I., Thomas,G.R., Chen,Z., Schreiber,H. and Van Waes,C. (2000) Growth regulated oncogene-alpha expression by murine squamous cell carcinoma promotes tumor growth, metastasis, leukocyte infiltration and angiogenesis by a host CXC receptor-2 dependent mechanism. Oncogene, 19, 3477-3486.
31. Dong,G., Loukinova,E., Smith,C.W., Chen,Z. and Van Waes,C. (1997) Genes differentially expressed with malignant transformation and metastatic tumor progression of murine squamous cell carcinoma. J. Cell. Biochem. Suppl., 28-29, 90-100.
32. Wen,D.Z., Rowland,A. and Derynck,R. (1989) Expression and secretion of gro/MGSA by stimulated human endothelial cells. EMBO J., 8, 1761-1766.
33. Loukinova,E., Chen,Z., Van Waes,C. and Dong,G. (2001) Expression of proangiogenic chemokine Gro 1 in low and high metastatic variants of Pam murine squamous cell carcinoma is differentially regulated by IL-1alpha, EGF and TGF-betal through NF-kappaB dependent and independent mechanisms. Int. J. Cancer, 94, 637-644.
34. Owen,J.D., Strieter,R., Burdick,M., Haghnegahdar,H., Nanney,L., Shattuck-Brandt,R. and Richmond,A. (1997) Enhanced tumor-forming capacity for immortalized melanocytes expressing melanoma growth stimulatory activity/growth-regulated cytokine beta and gamma proteins. Int. J. Cancer, 73, 94-103.
35. McGarrity,G.J., Steiner,T. and Vanaman,V. (1983) Detection of mycoplasma infection of cell cultures by DNA fluorochrome staining. In Tully,J.G. and Razin,E. (eds), Methods in Mycoplasmology. Academic Press, New York, Vol. II, pp. 155-208.
36. Chang,P.L., Tucker,M.A., Hicks,P.H. and Prince,C.W. (2002) Novel protein kinase C isoforms and mitogen-activated kinase kinase mediate phorbol ester-induced osteopontin expression. Int. J. Biochem. Cell. Biol., 34, 1142-1151.
37. Ohmori,Y., Fukumoto,S. and Hamilton,T.A. (1995) Two structurally distinct kappa B sequence motifs cooperatively control LPS-induced KC gene transcription in mouse macrophages. J. Immunol., 155, 3593-3600.
38. Chang,P.L., Lee,T.F., Garretson,K. and Prince,C.W. (1997) Calcitriol enhancement of TPA-induced tumorigenic transformation is mediated through vitamin D receptor-dependent and -independent pathways. Clin. Exp. Metastasis, 15, 580-592.
39. Dignam,J.D., Lebovitz,R.M. and Roeder,R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
40. Colburn,N.H., Former,B.F., Nelson, K.A. and Yuspa,S.H. (1979) Tumour promoter induces anchorage independence irreversibly. Nature, 281, 589-591.
41. Chang,P.L., Cao,M. and Hicks,P. (2003) Osteopontin induction is required for tumor promoter-induced transformation of pre-neoplastic mouse cells. Carcinogenesis, 24, 1749-1758.
42. Ohmori,Y., Wyner,L., Narumi,S., Armstrong,D., Stoler,M. and Hamilton,T.A. (1993) Tumor necrosis factor-alpha induces cell type and tissue-specific expression of chemoattractant cytokines in vivo. Am. J. Pathol., 142, 861-870.
43. Baeuerle,P.A. (1998) IkappaB-NF-kappaB structures: At the interface of inflammation control. Cell, 95, 729-731.
44. Arenzana-Seisdedos,F., Thompson,J., Rodriguez,M.S., Bachelerie,F., Thomas,D. and Hay,R.T. (1995) Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNA-binding and transcriptional activities of NF-kappa B. Mol. Cell. Biol., 15, 2689-2696.
45. Zhong,H., Voll,R.E. and Ghosh,S. (1998) Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell., 1, 661-671.
46. Zhong,H., May,M.J., Jimi,E. and Ghosh,S. (2002) The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol. Cell., 9, 625-636.
47. Madrid,L.V., Mayo,M.W., Reuther,J.Y. and Baldwin,A.S.,Jr. (2001) Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J. Biol. Chem., 276, 18934-18940.
48. Jiang,X., Takahashi,N., Ando,K., Otsuka,T., Tetsuka,T. and Okamoto,T. (2003) NF-kappa B p65 transactivation domain is involved in the NF-kappa B-inducing kinase pathway. Biochem. Biophys. Res. Commun., 301, 583-590.
49. Okazaki,T., Sakon,S., Sasazuki, T., Sakurai,H., Doi,T., Yagita,H., Okumura,K. and Nakano,H. (2003) Phosphorylation of serine 276 is essential for p65 NF-kappaB subunit-dependent cellular responses. Biochem. Biophys. Res. Commun., 300, 807-812.
50. Hu,J., Nakano,H., Sakurai,H. and Colburn,N.H. (2004) Insufficient p65 phosphorylation at S536 specifically contributes to the lack of NF-kappaB activation and transformation in resistant JB6 cells. Carcinogenesis, 25, 1991-2003.
51. Budunova,I.V., Carbajal,S. and Slaga,T.J. (1996) Effect of diverse tumor promoters on the expression of gap-junctional proteins connexin (Cx)26, Cx31.1, and Cx43 in SENCAR mouse epidermis. Mol. Carcinog., 15, 202-214.
52. Schonthal,A., Tsukitani,Y. and Feramisco,J.R. (1991) Transcriptional and post-transcriptional regulation of c-fos expression by the tumor promoter okadaic acid. Oncogene, 6, 423-430.
53. Namboodiripad,A.N. and Jennings,M.L. (1996) Permeability characteristics of erythrocyte membrane to okadaic acid and calyculin A. Am. J. Physiol., 270, C449-456.
54. Yatsunami,J., Fujiki,H., Suganuma,M., Yoshizawa,S., Eriksson,J.E., Olson,M.O. and Goldman,R.D. (1991) Vimentin is hyperphosphorylated in primary human fibroblasts treated with okadaic acid. Biochem. Biophys. Res. Commun., 177, 1165-1170.
55. Sassa,T., Richter,W.W., Uda,N., Suganuma,M., Suguri,H., Yoshizawa,S., Hirota,M. and Fujiki,H. (1989) Apparent 'activation' of protein kinases by okadaic acid class tumor promoters. Biochem. Biophys. Res. Commun., 159, 939-944.
56. Cochran,B.H., Reffel,A.C. and Stiles,C.D. (1983) Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell, 33, 939-947.
57. Panwalkar,A., Verstovsek,S. and Giles,F. (2004) Nuclear factor-kappaB modulation as a therapeutic approach in hematologic malignancies. Cancer, 100, 1578-1589.
58. Sakurai,H., Suzuki,S., Kawasaki,N., Nakano,H., Okazaki,T., Chino,A., Doi,T. and Saiki,I. (2003) Tumor necrosis factor-alpha-induced IKK phosphorylation of NF-kappaB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J. Biol. Chem., 278, 36916-36923.
59. Traenckner,E.B., Pahl,H.L., Henkel,T., Schmidt,K.N., Wilk, S. and Baeuerle,P.A. (1995) Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J., 14, 2876-2883.