P27 suppresses cyclooxygenase-2 expression by inhibiting p38β and p38δ-mediated CREB phosphorylation upon arsenite exposure

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 9, 2013, Pages 2083-2091

  Che, Xun ^a   Liu, Jinyi ^a   Huang, Haishan ^a,b   Mi, Xiaoyi ^a   Xia, Qing ^a   Li, Jingxia ^a   Zhang, Dongyun ^a   Ke, Qingdong ^b   Gao, Jimin ^b   Huang, Chuanshu ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Arsenite; Cox 2; Creb; P27; P38

Indexed keywords

ARSENIC TRIOXIDE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P38BETA; PROTEIN P38DELTA; SYNAPTOPHYSIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; PROTEIN C JUN; PROTEIN P27; SYNAPTOPHYSIN BETA; SYNAPTOPHYSIN DELTA; ARSENOUS ACID DERIVATIVE; CDKN1B PROTEIN, MOUSE; CREB1 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE 11; MITOGEN ACTIVATED PROTEIN KINASE 13; PTGS2 PROTEIN, MOUSE; TERATOGENIC AGENT;

ANIMAL CELL; ARSENITE EXPOSURE; ARTICLE; BINDING SITE; CANCER INHIBITION; CELL CYCLE G0 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; CYTOSOLIC FRACTION; DNA SEQUENCE; ENVIRONMENTAL EXPOSURE; ENZYME INDUCTION; GENE INACTIVATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; LONG TERM EXPOSURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; CYTOTOXICITY; PROTEIN FUNCTION; ANIMAL; BIOSYNTHESIS; CELL LINE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION;

ANIMALS; ARSENITES; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLOOXYGENASE 2; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 11; MITOGEN-ACTIVATED PROTEIN KINASE 13; PHOSPHORYLATION; TERATOGENS; TRANSCRIPTION, GENETIC;

EID: 84883080123     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.04.012     Document Type: Article

References (68)

1. W.R. Chappell, B.D. Beck, K.G. Brown, R. Chaney, R. Cothern, C.R. Cothern, K.J. Irgolic, D.W. North, I. Thornton, T.A. Tsongas, Inorganic arsenic: a need and an opportunity to improve risk assessment, Environ. Health Perspect. 105 (1997) 1060-1067.
2. F.C. Knowles, A.A. Benson, The mode of action of arsenical herbicides and drugs, Z. Gesamte Hyg. 30 (1984) 407-408.
3. S.A. Lerman, T.W. Clarkson, R.J. Gerson, Arsenic uptake andmetabolismby liver cells is dependent on arsenic oxidation state, Chem. Biol. Interact. 45 (1983) 401-406.
4. D.R. Germolec, J. Spalding, H.S. Yu, G.S. Chen, P.P. Simeonova, M.C. Humble, A. Bruccoleri, G.A. Boorman, J.F. Foley, T. Yoshida, M.I. Luster, Arsenic enhancement of skin neoplasia by chronic stimulation of growth factors, Am. J. Pathol. 153 (1998) 1775-1785.
5. M. Ding, X. Shi, V. Castranova, V. Vallyathan, Predisposing factors in occupational lung cancer: inorganic minerals and chromium, J. Environ. Pathol. Toxicol. Oncol. 19 (2000) 129-138.
6. C. Huang, Q. Ke, M. Costa, X. Shi, Molecular mechanisms of arsenic carcinogenesis, Mol. Cell. Biochem. 255 (2004) 57-66.
7. J. Liu, D. Zhang, X. Mi, Q. Xia, Y. Yu, Z. Zuo, W. Guo, X. Zhao, J. Cao, Q. Yang, A. Zhu, W. Yang, X. Shi, J. Li, C. Huang, p27 suppresses arsenite-induced Hsp27/Hsp70 expression through inhibiting JNK2/c-Jun- and HSF-1-dependent pathways, J. Biol. Chem. 285 (2010) 26058-26065.
8. W. Ouyang, Q.Ma, J. Li, D. Zhang, Z.G. Liu, A.K. Rustgi, C. Huang, Cyclin D1 induction through IkappaB kinase beta/nuclear factor-kappaB pathway is responsible for arsenite-induced increased cell cycle G1-S phase transition in human keratinocytes, Cancer Res. 65 (2005) 9287-9293.
9. D. Zhang, L. Song, J. Li, K. Wu, C. Huang, Coordination of JNK1 and JNK2 is critical for GADD45alpha induction and its mediated cell apoptosis in arsenite responses, J. Biol. Chem. 281 (2006) 34113-34123.
10. W.L. Smith, D.L. DeWitt, R.M. Garavito, Cyclooxygenases: structural, cellular, and molecular biology, Annu. Rev. Biochem. 69 (2000) 145-182.
11. K. Subbaramaiah, A.J. Dannenberg, Cyclooxygenase 2: a molecular target for cancer prevention and treatment, Trends Pharmacol. Sci. 24 (2003) 96-102.
12. R.N. Dubois, S.B. Abramson, L. Crofford, R.A. Gupta, L.S. Simon, L.B. Van De Putte, P.E. Lipsky, Cyclooxygenase in biology and disease, FASEB J. 12 (1998) 1063-1073.
13. J. Ding, J. Li, C. Xue, K.Wu,W. Ouyang, D. Zhang, Y. Yan, C. Huang, Cyclooxygenase-2 induction by arsenite is through a nuclear factor of activated T-cell-dependent pathway and plays an antiapoptotic role in Beas-2B cells, J. Biol. Chem. 281 (2006) 24405-24413.
14. H. Toyoshima, T. Hunter, p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21, Cell 78 (1994) 67-74.
15. K. Polyak, J.Y. Kato, M.J. Solomon, C.J. Sherr, J. Massague, J.M. Roberts, A. Koff, p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest, Genes Dev. 8 (1994) 9-22.
16. N. Kawamata, R. Morosetti, C.W. Miller, D. Park, K.S. Spirin, T. Nakamaki, S. Takeuchi, Y. Hatta, J. Simpson, S. Wilcyznski, et al., Molecular analysis of the cyclin-dependent kinase inhibitor gene p27/Kip1 in human malignancies, Cancer Res. 55 (1995) 2266-2269.
17. M.L. Fero, M. Rivkin, M. Tasch, P. Porter, C.E. Carow, E. Firpo, K. Polyak, L.H. Tsai, V. Broudy, R.M. Perlmutter, K. Kaushansky, J.M. Roberts, A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice, Cell 85 (1996) 733-744.
18. C. Spruck, H. Strohmaier, M. Watson, A.P. Smith, A. Ryan, T.W. Krek, S.I. Reed, A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1, Mol. Cell 7 (2001) 639-650.
19. A. Besson, H.C. Hwang, S. Cicero, S.L. Donovan, M. Gurian-West, D. Johnson, B.E. Clurman, M.A. Dyer, J.M. Roberts, Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype, Genes Dev. 21 (2007) 1731-1746.
20. S.Y. Wang, Q.B. Huang, X.H. Guo, U.T. Brunk, J.H. Han, K.S. Zhao, M. Zhao, The P38 alpha and P38 deltaMAP kinasesmay be gene therapy targets in the future treatment of severe burns, Shock 34 (2010) 176-182.
21. H. Enslen, J. Raingeaud, R.J. Davis, Selective activation of p38 mitogen-activated protein (MAP) kinase isoforms by the MAP kinase kinases MKK3 and MKK6, J. Biol. Chem. 273 (1998) 1741-1748.
22. K. Subbaramaiah, P. Bulic, Y. Lin, A.J.Dannenberg, D.S. Pasco, Development and use of a gene promoter-based screen to identify novel inhibitors of cyclooxygenase-2 transcription, J. Biomol. Screen. 6 (2001) 101-110.
23. D. Zhang, J. Li, M. Costa, J. Gao, C. Huang, JNK1 mediates degradation HIF-1alpha by a VHL-independent mechanism that involves the chaperones Hsp90/Hsp70, Cancer Res. 70 (2010) 813-823.
24. L. Song, J. Li, D. Zhang, Z.G. Liu, J. Ye, Q. Zhan, H.M. Shen, M. Whiteman, C. Huang, IKKbeta programs to turn on the GADD45alpha-MKK4-JNK apoptotic cascade specifically via p50 NF-kappaB in arsenite response, J. Cell Biol. 175 (2006) 607-617.
25. K.S. Chun, Y.J. Surh, Signal transduction pathways regulating cyclooxygenase-2 expression: potential molecular targets for chemoprevention, Biochem. Pharmacol. 68 (2004) 1089-1100.
26. S. Nakao, Y. Ogata, E. Shimizu-Sasaki, M. Yamazaki, S. Furuyama, H. Sugiya, Activation of NFkappaB is necessary for IL-1beta-induced cyclooxygenase-2 (COX-2) expression in human gingival fibroblasts, Mol. Cell. Biochem. 209 (2000) 113-118.
27. J.L. Jimenez, M.A. Iniguez, M.A. Munoz-Fernandez, M. Fresno, Effect of phosphodiesterase 4 inhibitors on NFAT-dependent cyclooxygenase-2 expression in human T lymphocytes, Cell. Signal. 16 (2004) 1363-1373.
28. C. Miller, M. Zhang, Y. He, J. Zhao, J.P. Pelletier, J. Martel-Pelletier, J.A. Di Battista, 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 (1998) 392-413.
29. W.H. Cao, K.W. Daniel, J. Robidoux, P. Puigserver, A.V. Medvedev, X. Bai, L.M. Floering, B.M. Spiegelman, S. Collins, p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene, Mol. Cell. Biol. 24 (2004) 3057-3067.
30. R. Pramanik, X. Qi, S. Borowicz, D. Choubey, R.M. Schultz, J. Han, G. Chen, p38 isoforms have opposite effects on AP-1-dependent transcription through regulation of c-Jun. The determinant roles of the isoforms in the p38 MAPK signal specificity, J. Biol. Chem. 278 (2003) 4831-4839.
31. T. Cai, X. Li, J. Ding, W. Luo, J. Li, C. Huang, A cross-talk between NFAT and NF-kappa B pathways is crucial for nickel-induced COX-2 expression in Beas-2B cells, Curr. Cancer Drug Targets 11 (2011) 548-559.
32. Z.H. Zuo, T.J. Cai, J.X. Li, D.Y. Zhang, Y.H. Yu, C.S. Huang, Hexavalent chromium Cr(VI) up-regulates COX-2 expression through an NF kappa B/c-Jun/AP-1-dependent pathway, Environ. Health Perspect. 120 (2012) 547-553.
33. K. Nakayama,N. Ishida, M. Shirane, A. Inomata, T. Inoue,N. Shishido, I.Horii, D.Y. Loh, Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors, Cell 85 (1996) 707-720.
34. F. Bullrich, T.K. MacLachlan, N. Sang, T. Druck, M.L. Veronese, S.L. Allen, N. Chiorazzi, A. Koff, K. Heubner, C.M. Croce, et al., Chromosomal mapping of members of the cdc2 family of protein kinases, cdk3, cdk6, PISSLRE, and PITALRE, and a cdk inhibitor, p27Kip1, to regions involved in human cancer, Cancer Res. 55 (1995) 1199-1205.
35. I. Reynisdottir, J. Massague, The subcellular locations of p15(Ink4b) and p27(Kip1) coordinate their inhibitory interactions with cdk4 and cdk2, Genes Dev. 11 (1997) 492-503.
36. A.A. Russo, P.D. Jeffrey, A.K. Patten, J. Massague, N.P. Pavletich, Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex, Nature 382 (1996) 325-331.
37. J. Font de Mora, A. Uren, M. Heidaran, E. Santos, Biological activity of p27kip1 and its amino- and carboxy-terminal domains in G2/M transition of Xenopus oocytes, Oncogene 15 (1997) 2541-2551.
38. G. Viglietto, M.L. Motti, P. Bruni, R.M. Melillo, A. D'Alessio, D. Califano, F. Vinci, G. Chiappetta, P. Tsichlis, A. Bellacosa, A. Fusco, M. Santoro, Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Aktmediated phosphorylation in breast cancer, Nat. Med. 8 (2002) 1136-1144.
39. C. Denicourt, C.C. Saenz, B. Datnow, X.S. Cui, S.F. Dowdy, Relocalized p27Kip1 tumor suppressor functions as a cytoplasmic metastatic oncogene in melanoma, Cancer Res. 67 (2007) 9238-9243.
40. M.D. Larrea, S.A. Wander, J.M. Slingerland, p27 as Jekyll and Hyde: regulation of cell cycle and cell motility, Cell Cycle 8 (2009) 3455-3461.
41. J.R. Vane, Y.S. Bakhle, R.M. Botting, Cyclooxygenases 1 and 2, Annu. Rev. Pharmacol. Toxicol. 38 (1998) 97-120.
42. K. Muller-Decker, G. Furstenberger, M. Neumann, M. Schnolzer, Differential protein expression in the epidermis of wild-type and COX-2 transgenic mice, Skin Pharmacol. Physiol. 19 (2006) 89-94.
43. C.S. Williams, R.L. Shattuck-Brandt, R.N. DuBois, The role of COX-2 in intestinal cancer, Expert Opin. Investig. Drugs 8 (1999) 1-12.
44. J. Ding, X. Zhang, J. Li, L. Song, W. Ouyang, D. Zhang, C. Xue, M. Costa, J.A. Melendez, C. Huang, Nickel compounds render anti-apoptotic effect to human bronchial epithelial Beas-2B cells by induction of cyclooxygenase-2 through an IKKbeta/p65-dependent and IKKalpha- and p50-independent pathway, J. Biol. Chem. 281 (2006) 39022-39032.
45. A. Kaidi, D. Qualtrough, A.C. Williams, C. Paraskeva, 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 (2006) 6683-6691.
46. P. Rockwell, J.Martinez, L. Papa, E. Gomes, Redox regulates COX-2 upregulation and cell death in the neuronal response to cadmium, Cell. Signal. 16 (2004) 343-353.
47. K.M. Lee, M.K. Hwang, D.E. Lee, K.W. Lee, H.J. Lee, Protective effect of quercetin against arsenite-induced COX-2 expression by targeting PI3K in rat liver epithelial cells, J. Agric. Food Chem. 58 (2010) 5815-5820.
48. N. Kuzushita, B.I. Aswad,M.J. Park, S.F.Moss, Deficiency of p27 leads to increased gastric epithelial and inflammatory responses to Helicobacter pylori, Gastroenterology 124 (2003) A5-A6.
49. T. Hussain, S. Gupta, H. Mukhtar, Cyclooxygenase-2 and prostate carcinogenesis, Cancer Lett. 191 (2003) 125-135.
50. C. Szabo, C. Thiemermann, C.C. Wu, M. Perretti, J.R. Vane, Attenuation of the induction of nitric-oxide synthase by endogenous glucocorticoids accounts for endotoxin tolerance in-vivo, Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 271-275.
51. H.Wolff, K. Saukkonen, S. Anttila, A. Karjalainen, H. Vainio, A. Ristimaki, Expression of cyclooxygenase-2 in human lung carcinoma, Cancer Res. 58 (1998) 4997-5001.
52. H. Cui, J. Ma, J. Ding, T. Li, G. Alam, H.F. Ding, Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentrationdependent manner, J. Biol. Chem. 281 (2006) 34696-34704.
53. M.J. Thun, NSAID use and decreased risk of gastrointestinal cancers, Gastroenterol. Clin. North Am. 25 (1996) 333-348.
54. R. Chu, Y. Lin, K.C. Reddy, J. Pan, M.S. Rao, J.K. Reddy, A.V. Yeldandi, Transformation of epithelial cells stably transfected with H2O2-generating peroxisomal urate oxidase, Cancer Res. 56 (1996) 4846-4852.
55. K.K. Wu, Transcription-based COX-2 inhibition: a therapeutic strategy, Thromb. Haemost. 96 (2006) 417-422.
56. J. Han, J.D. Lee, L. Bibbs, R.J. Ulevitch, A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells, Science 265 (1994) 808-811.
57. T. Zarubin, J. Han, Activation and signaling of the p38 MAP kinase pathway, Cell Res. 15 (2005) 11-18.
58. G.A. Keesler, J. Bray, J. Hunt, D.A. Johnson, T. Gleason, Z. Yao, S.W. Wang, C. Parker, H. Yamane, C. Cole, H.S. Lichenstein, Purification and activation of recombinant p38 isoforms alpha, beta, gamma, and delta, Protein Expr. Purif. 14 (1998) 221-228.
59. P. Sundaresan, R.W. Farndale, P38 mitogen-activated protein kinase dephosphorylation is regulated by protein phosphatase 2A in human platelets activated by collagen, FEBS Lett. 528 (2002) 139-144.
60. K. Kitatani, J. Idkowiak-Baldys, J. Bielawski, T.A. Taha, R.W. Jenkins, C.E. Senkal, B. Ogretmen, L.M. Obeid, Y.A. Hannun, Protein kinase C-induced activation of a ceramide/protein phosphatase 1 pathway leading to dephosphorylation of p38 MAPK, J. Biol. Chem. 281 (2006) 36793-36802.
61. D.M. Ouwens, N.D. de Ruiter, G.C. van der Zon, A.P. Carter, J. Schouten, C. van der Burgt, K. Kooistra, J.L. Bos, J.A. Maassen, H. van Dam, Growth factors can activate ATF2 via a two-step mechanism: phosphorylation of Thr71 through the Ras-MEKERK pathway and of Thr69 through RalGDS-Src-p38, EMBO J. 21 (2002) 3782-3793.
62. D.Y. Zhang, L. Song, J.X. Li, K.J. Wu, C.S. Huang, Coordination of JNK1 and JNK2 is critical for GADD45 alpha induction and its mediated cell apoptosis in arsenite responses, J. Biol. Chem. 281 (2006) 34113-34123.
63. A.C. Porter, G.R. Fanger, R.R. Vaillancourt, Signal transduction pathways regulated by arsenate and arsenite, Oncogene 18 (1999) 7794-7802.
64. H. Shi, X. Shi, K.J. Liu, Oxidative mechanism of arsenic toxicity and carcinogenesis, Mol. Cell. Biochem. 255 (2004) 67-78.
65. X. Wang, A.K. Mandal, H. Saito, J.F. Pulliam, E.Y. Lee, Z.J. Ke, J. Lu, S. Ding, L. Li, B.J. Shelton, T. Tucker, B.M. Evers, Z. Zhang, X. Shi, Arsenic and chromium in drinking water promote tumorigenesis in a mouse colitis-associated colorectal cancer model and the potential mechanism is ROS-mediated Wnt/beta-catenin signaling pathway, Toxicol. Appl. Pharmacol. 262 (2012) 11-21.
66. C.C. Hsieh, J. Papaconstantinou, Thioredoxin-ASK1 complex levels regulate ROS-mediated p38 MAPK pathway activity in livers of aged and long-lived Snell dwarf mice, FASEB J. 20 (2006) 259-268.
67. D. Das, G. Pintucci, A. Stern, MAPK-dependent expression of p21(WAF) and p27(kip1) in PMA-induced differentiation of HL60 cells, FEBS Lett. 472 (2000) 50-52.
68. M. Kortylewski, P.C. Heinrich, M.E. Kauffmann, M. Bohm, A. MacKiewicz, I. Behrmann, Mitogen-activated protein kinases control p27/Kip1 expression and growth of human melanoma cells, Biochem. J. 357 (2001) 297-303.