Covalent Modification of CDK2 by 4-Hydroxynonenal as a Mechanism of Inhibition of Cell Cycle Progression

Chemical Research in Toxicology

Volumn 29, Issue 3, 2016, Pages 323-332

  Camarillo, Jeannie M ^a   Rose, Kristie L ^a   Galligan, James J ^a   Xu, Shu ^a   Marnett, Lawrence J ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; CYCLIN DEPENDENT KINASE 2; CYCLIN E; PROTEIN P21; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RECOMBINANT CYCLIN DEPENDENT KINASE 2; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; 4-HYDROXY-2-NONENAL; ALDEHYDE; CDK2 PROTEIN, HUMAN;

ADDUCTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CARCINOMA CELL; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CHEMICAL MODIFICATION; CLICK CHEMISTRY; COLORECTAL CANCER CELL LINE; COLORECTAL CARCINOMA; CONTROLLED STUDY; DNA DAMAGE; ENZYME INACTIVATION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; MOLECULAR MODEL; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE;

ALDEHYDES; CELL CYCLE CHECKPOINTS; CYCLIN-DEPENDENT KINASE 2; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MODELS, MOLECULAR; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

EID: 84961753023     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/acs.chemrestox.5b00485     Document Type: Article

References (41)

1. Sayre, L. M., Zelasko, D. A., Harris, P. L., Perry, G., Salomon, R. G., and Smith, M. A. (1997) 4-hydroxynonenal-derived advanced lipid peroxidation end products are increased in alzheimer's disease J. Neurochem. 68, 2092-2097 10.1046/j.1471-4159.1997.68052092.x
2. Yoritaka, A., Hattori, N., Uchida, K., Tanaka, M., Stadtman, E. R., and Mizuno, Y. (1996) Immunohistochemical detection of 4-hydroxynonenal protein adducts in parkinson disease Proc. Natl. Acad. Sci. U. S. A. 93, 2696-2701 10.1073/pnas.93.7.2696
3. Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R., and Milzani, A. (2003) Protein carbonylation in human diseases Trends Mol. Med. 9, 169-176 10.1016/S1471-4914(03)00031-5
4. Hussain, S. P., Hofseth, L. J., and Harris, C. C. (2003) Radical causes of cancer Nat. Rev. Cancer 3, 276-285 10.1038/nrc1046
5. Marnett, L. J., Riggins, J. N., and West, J. D. (2003) Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein J. Clin. Invest. 111, 583-593 10.1172/JCI200318022
6. Yin, H., Xu, L., and Porter, N. A. (2011) Free radical lipid peroxidation: Mechanisms and analysis Chem. Rev. 111, 5944-5972 10.1021/cr200084z
7. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radical Biol. Med. 11, 81-128 10.1016/0891-5849(91)90192-6
8. Ullery, J. C. and Marnett, L. J. (2012) Protein modification by oxidized phospholipids and hydrolytically released lipid electrophiles: Investigating cellular responses Biochim. Biophys. Acta, Biomembr. 1818, 2424-2435 10.1016/j.bbamem.2012.04.014
9. Ekholm, S. V. and Reed, S. I. (2000) Regulation of g(1) cyclin-dependent kinases in the mammalian cell cycle Curr. Opin. Cell Biol. 12, 676-684 10.1016/S0955-0674(00)00151-4
10. Lees, E., Faha, B., Dulic, V., Reed, S. I., and Harlow, E. (1992) Cyclin e/cdk2 and cyclin a/cdk2 kinases associate with p107 and e2f in a temporally distinct manner Genes Dev. 6, 1874-1885 10.1101/gad.6.10.1874
11. Harbour, J. W., Luo, R. X., Dei Santi, A., Postigo, A. A., and Dean, D. C. (1999) CDK phosphorylation triggers sequential intramolecular interactions that progressively block rb functions as cells move through G1 Cell 98, 859-869 10.1016/S0092-8674(00)81519-6
12. Giacinti, C. and Giordano, A. (2006) Rb and cell cycle progression Oncogene 25, 5220-5227 10.1038/sj.onc.1209615
13. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. (1993) The p21 cdk-interacting protein cip1 is a potent inhibitor of g1 cyclin-dependent kinases Cell 75, 805-816 10.1016/0092-8674(93)90499-G
14. Wang, Y., Fisher, J. C., Mathew, R., Ou, L., Otieno, S., Sublet, J., Xiao, L., Chen, J., Roussel, M. F., and Kriwacki, R. W. (2011) Intrinsic disorder mediates the diverse regulatory functions of the cdk inhibitor p21 Nat. Chem. Biol. 7, 214-221 10.1038/nchembio.536
15. Barrera, G., Pizzimenti, S., and Dianzani, M. U. (2004) 4-hydroxynonenal and regulation of cell cycle: Effects on the prb/e2f pathway Free Radical Biol. Med. 37, 597-606 10.1016/j.freeradbiomed.2004.05.023
16. Wonisch, W., Kohlwein, S. D., Schaur, J., Tatzber, F., Guttenberger, H., Zarkovic, N., Winkler, R., and Esterbauer, H. (1998) Treatment of the budding yeast saccharomyces cerevisiae with the lipid peroxidation product 4-hne provokes a temporary cell cycle arrest in g1 phase Free Radical Biol. Med. 25, 682-687 10.1016/S0891-5849(98)00110-5
17. Barrera, G., Pizzimenti, S., Muraca, R., Barbiero, G., Bonelli, G., Baccino, F. M., Fazio, V. M., and Dianzani, M. U. (1996) Effect of 4-hydroxynonenal on cell cycle progression and expression of differentiation-associated antigens in hl-60 cells Free Radical Biol. Med. 20, 455-462 10.1016/0891-5849(95)02049-7
18. Laurora, S., Tamagno, E., Briatore, F., Bardini, P., Pizzimenti, S., Toaldo, C., Reffo, P., Costelli, P., Dianzani, M. U., Danni, O., and Barrera, G. (2005) 4-hydroxynonenal modulation of p53 family gene expression in the sk-n-be neuroblastoma cell line Free Radical Biol. Med. 38, 215-225 10.1016/j.freeradbiomed.2004.10.014
19. Codreanu, S. G., Zhang, B., Sobecki, S. M., Billheimer, D. D., and Liebler, D. C. (2009) Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal Mol. Cell. Proteomics 8, 670-680 10.1074/mcp.M800070-MCP200
20. Vila, A., Tallman, K. A., Jacobs, A. T., Liebler, D. C., Porter, N. A., and Marnett, L. J. (2008) Identification of protein targets of 4-hydroxynonenal using click chemistry for ex vivo biotinylation of azido and alkynyl derivatives Chem. Res. Toxicol. 21, 432-444 10.1021/tx700347w
21. Codreanu, S. G., Ullery, J. C., Zhu, J., Tallman, K. A., Beavers, W. N., Porter, N. A., Marnett, L. J., Zhang, B., and Liebler, D. C. (2014) Alkylation damage by lipid electrophiles targets functional protein systems Mol. Cell. Proteomics 13, 849-859 10.1074/mcp.M113.032953
22. Zhang, B., Shi, Z., Duncan, D. T., Prodduturi, N., Marnett, L. J., and Liebler, D. C. (2011) Relating protein adduction to gene expression changes: A systems approach Mol. BioSyst. 7, 2118-2127 10.1039/c1mb05014a
23. McGrath, C. E., Tallman, K. A., Porter, N. A., and Marnett, L. J. (2011) Structure-activity analysis of diffusible lipid electrophiles associated with phospholipid peroxidation: 4-hydroxynonenal and 4-oxononenal analogues Chem. Res. Toxicol. 24, 357-370 10.1021/tx100323m
24. van den Heuvel, S. and Harlow, E. (1993) Distinct roles for cyclin-dependent kinases in cell cycle control Science 262, 2050-2054 10.1126/science.8266103
25. Schonthal, A. H. (2004) Measuring cyclin-dependent kinase activity Methods Mol. Biol. 281, 105-124 10.1385/1-59259-811-0:105
26. Weerapana, E., Wang, C., Simon, G. M., Richter, F., Khare, S., Dillon, M. B., Bachovchin, D. A., Mowen, K., Baker, D., and Cravatt, B. F. (2010) Quantitative reactivity profiling predicts functional cysteines in proteomes Nature 468, 790-795 10.1038/nature09472
27. Xu, M., Sheppard, K. A., Peng, C. Y., Yee, A. S., and Piwnica-Worms, H. (1994) Cyclin a/cdk2 binds directly to e2f-1 and inhibits the DNA-binding activity of e2f-1/dp-1 by phosphorylation Mol. Cell. Biol. 14, 8420-8431 10.1128/MCB.14.12.8420
28. Sheaff, R. J., Groudine, M., Gordon, M., Roberts, J. M., and Clurman, B. E. (1997) Cyclin e-cdk2 is a regulator of p27kip1 Genes Dev. 11, 1464-1478 10.1101/gad.11.11.1464
29. Akiyama, T., Ohuchi, T., Sumida, S., Matsumoto, K., and Toyoshima, K. (1992) Phosphorylation of the retinoblastoma protein by cdk2 Proc. Natl. Acad. Sci. U. S. A. 89, 7900-7904 10.1073/pnas.89.17.7900
30. Sampey, B. P., Carbone, D. L., Doorn, J. A., Drechsel, D. A., and Petersen, D. R. (2007) 4-hydroxy-2-nonenal adduction of extracellular signal-regulated kinase (erk) and the inhibition of hepatocyte erk-est-like protein-1-activating protein-1 signal transduction Mol. Pharmacol. 71, 871-883 10.1124/mol.106.029686
31. Barrera, G., Pizzimenti, S., Laurora, S., Moroni, E., Giglioni, B., and Dianzani, M. U. (2002) 4-hydroxynonenal affects prb/e2f pathway in hl-60 human leukemic cells Biochem. Biophys. Res. Commun. 295, 267-275 10.1016/S0006-291X(02)00649-6
32. Sharma, A., Sharma, R., Chaudhary, P., Vatsyayan, R., Pearce, V., Jeyabal, P. V., Zimniak, P., Awasthi, S., and Awasthi, Y. C. (2008) 4-hydroxynonenal induces p53-mediated apoptosis in retinal pigment epithelial cells Arch. Biochem. Biophys. 480, 85-94 10.1016/j.abb.2008.09.016
33. Gu, Y., Rosenblatt, J., and Morgan, D. O. (1992) Cell cycle regulation of cdk2 activity by phosphorylation of thr160 and tyr15 EMBO J. 11, 3995-4005
34. Ji, C., Amarnath, V., Pietenpol, J. A., and Marnett, L. J. (2001) 4-hydroxynonenal induces apoptosis via caspase-3 activation and cytochrome c release Chem. Res. Toxicol. 14, 1090-1096 10.1021/tx000186f
35. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B., and Jacks, T. (1995) P53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage Genes Dev. 9, 935-944 10.1101/gad.9.8.935
36. Sayre, L. M., Lin, D., Yuan, Q., Zhu, X., and Tang, X. (2006) Protein adducts generated from products of lipid oxidation: Focus on hne and one Drug Metab. Rev. 38, 651-675 10.1080/03602530600959508
37. Russo, A. A., Jeffrey, P. D., and Pavletich, N. P. (1996) Structural basis of cyclin-dependent kinase activation by phosphorylation Nat. Struct. Biol. 3, 696-700 10.1038/nsb0896-696
38. Honda, R., Lowe, E. D., Dubinina, E., Skamnaki, V., Cook, A., Brown, N. R., and Johnson, L. N. (2005) The structure of cyclin e1/cdk2: Implications for cdk2 activation and cdk2-independent roles EMBO J. 24, 452-463 10.1038/sj.emboj.7600554
39. Fisher, R. P. and Morgan, D. O. (1994) A novel cyclin associates with mo15/cdk7 to form the cdk-activating kinase Cell 78, 713-724 10.1016/0092-8674(94)90535-5
40. Chi, Y., Welcker, M., Hizli, A. A., Posakony, J. J., Aebersold, R., and Clurman, B. E. (2008) Identification of cdk2 substrates in human cell lysates Genome Biol. 9, R149 10.1186/gb-2008-9-10-r149
41. Grafstrom, R. H., Pan, W., and Hoess, R. H. (1999) Defining the substrate specificity of cdk4 kinase-cyclin d1 complex Carcinogenesis 20, 193-198 10.1093/carcin/20.2.193