Cdk2 nitrosylation and loss of mitochondrial potential mediate NO-dependent biphasic effect on HL-60 cell cycle

Free Radical Biology and Medicine

Volumn 48, Issue 6, 2010, Pages 851-861

  Kumar, Sachin ^a   Barthwal, Manoj Kumar ^a   Dikshit, Madhu ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

Cell cycle; Free radicals; HL 60; Nitric oxide; Nitrosylation; Proliferation

Indexed keywords

CASPASE 3; CYCLIN B; CYCLIN DEPENDENT KINASE 2; CYCLIN E; NITRIC OXIDE; ROSCOVITINE;

APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL LOSS; CELL PROLIFERATION; CELL STRAIN HL 60; CONCENTRATION PROCESS; CONTROLLED STUDY; CYTOSTASIS; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; NITROSYLATION; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 2; HL-60 CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE DONORS; OXIDATION-REDUCTION; PURINES; TRIAZENES;

EID: 76049118697     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.01.004     Document Type: Article

References (48)

1. Bredt D.S., and Snyder S.H. Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63 (1994) 175-195
2. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell, 78 (1994) 931-936
3. Li C.Q., and Wogan G.N. Nitric oxide as a modulator of apoptosis. Cancer Lett. 226 (2005) 1-15
4. Villalobo A. Nitric oxide and cell proliferation. FEBS J 273 (2006) 2329-2344
5. Lu Q., Jourd'Heuil F.L., and Jourd'Heuil D. Redox control of G(1)/S cell cycle regulators during nitric oxide-mediated cell cycle arrest. J. Cell Physiol. 212 (2007) 827-839
6. Brookes P.S., Salinas E.P., Darley-Usmar K., Eiserich J.P., Freeman B.A., Darley-Usmar V.M., and Anderson P.G. Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J. Biol. Chem 275 (2000) 20474-20479
7. Pervin S., Singh R., and Chaudhuri G. Nitric oxide-induced cytostasis and cell cycle arrest of a human breast cancer cell line (MDA-MB-231): potential role of cyclin D1. Proc. Natl. Acad. Sci. USA 98 (2001) 3583-3588
8. Heller R., Polack T., Grabner R., and Till U. Nitric oxide inhibits proliferation of human endothelial cells via a mechanism independent of cGMP. Atherosclerosis 144 (1999) 49-57
9. Wang X., Sun H., and Li C. Nitric oxide induces promyelocytic cell growth arrest and apoptosis through deactivation of Akt pathway. Leuk. Res. 31 (2007) 653-660
10. Jea J.C., Liu T.C., Wang S.Y., and Sung Y.J. Nitric oxide enhances the growth of U937 human leukemic cells through a cyclooxygenase-mediated pathway. J. Leukocyte Biol. 64 (1998) 451-458
11. Hajri A., Metzger E., Vallat F., Coffy S., Flatter E., Evrard S., Marescaux J., and Aprahamian M. Role of nitric oxide in pancreatic tumour growth: in vivo and in vitro studies. Br. J. Cancer 78 (1998) 841-849
12. Liu Q., Chan S.T., and Mahendran R. Nitric oxide induces cyclooxygenase expression and inhibits cell growth in colon cancer cell lines. Carcinogenesis, 24 (2003) 637-642
13. Kim Y.M., Kim T.H., Seol D.W., Talanian R.V., and Billiar T.R. Nitric oxide suppression of apoptosis occurs in association with an inhibition of Bcl-2 cleavage and cytochrome c release. J. Biol. Chem. 273 (1998) 31437-31441
14. Liu L., and Stamler J.S. NO: an inhibitor of cell death. Cell Death Differ. 6 (1999) 937-942
15. Azad N., Vallyathan V., Wang L., Tantishaiyakul V., Stehlik C., Leonard S.S., and Rojanasakul Y. S-nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation: a novel antiapoptotic mechanism that suppresses apoptosis. J. Biol. Chem. 281 (2006) 34124-34134
16. Sato J., Nair K., Hiddinga J., Eberhardt N.L., Fitzpatrick L.A., Katusic Z.S., and O'Brien T. eNOS gene transfer to vascular smooth muscle cells inhibits cell proliferation via upregulation of p27 and p21 and not apoptosis. Cardiovasc. Res. 47 (2000) 697-706
17. Guo K., Andres V., and Walsh K. Nitric oxide-induced downregulation of Cdk2 activity and cyclin A gene transcription in vascular smooth muscle cells. Circulation, 97 (1998) 2066-2072
18. Tanner F.C., Meier P., Greutert H., Champion C., Nabel E.G., and Luscher T.F. Nitric oxide modulates expression of cell cycle regulatory proteins: a cytostatic strategy for inhibition of human vascular smooth muscle cell proliferation. Circulation, 101 (2000) 1982-1989
19. Takagi K., Isobe Y., Yasukawa K., Okouchi E., and Suketa Y. Nitric oxide blocks the cell cycle of mouse macrophage-like cells in the early G2+M phase. FEBS Lett. 340 (1994) 159-162
20. Maejima Y., Adachi S., Ito H., Nobori K., Tamamori-Adachi M., and Isobe M. Nitric oxide inhibits ischemia/reperfusion-induced myocardial apoptosis by modulating cyclin A-associated kinase activity. Cardiovasc. Res. 59 (2003) 308-320
21. Magrinat G., Mason S.N., Shami P.J., and Weinberg J.B. Nitric oxide modulation of human leukemia cell differentiation and gene expression. Blood, 80 (1992) 1880-1884
22. Shami P.J., and Weinberg J.B. Differential effects of nitric oxide on erythroid and myeloid colony growth from CD34+human bone marrow cells. Blood, 87 (1996) 977-982
23. Ulibarri J.A., Mozdziak P.E., Schultz E., Cook C., and Best T.M. Nitric oxide donors, sodium nitroprusside and S-nitroso-N-acetylpenicillamine, stimulate myoblast proliferation in vitro. In Vitro Cell Dev. Biol. Anim. 35 (1999) 215-218
24. Du M., Islam M.M., Lin L., Ohmura Y., Moriyama Y., and Fujimura S. Promotion of proliferation of murine BALB/C3T3 fibroblasts mediated by nitric oxide at lower concentrations. Biochem. Mol. Biol. Int. 41 (1997) 625-631
25. Gordge M.P., Hothersall J.S., and Noronha-Dutra A.A. Evidence for a cyclic GMP-independent mechanism in the anti-platelet action of S-nitrosoglutathione. Br. J. Pharmacol. 124 (1998) 141-148
26. Miller M.R., and Megson I.L. Recent developments in nitric oxide donor drugs. Br. J. Pharmacol. 151 (2007) 305-321
27. Saini R., Patel S., Saluja R., Sahasrabuddhe A.A., Singh M.P., Habib S., Bajpai V.K., and Dikshit M. Nitric oxide synthase localization in the rat neutrophils: immunocytochemical, molecular, and biochemical studies. J. Leukocyte Biol. 79 (2006) 519-528
28. Krishan A. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J. Cell Biol. 66 (1975) 188-193
29. Lugli E., Troiano L., Ferraresi R., Roat E., Prada N., Nasi M., Pinti M., Cooper E.L., and Cossarizza A. Characterization of cells with different mitochondrial membrane potential during apoptosis. Cytometry A 68 (2005) 28-35
30. Cid C., Alvarez-Cermeno J.C., Regidor I., Plaza J., Salinas M., and Alcazar A. Caspase inhibitors protect against neuronal apoptosis induced by cerebrospinal fluid from multiple sclerosis patients. J. Neuroimmunol. 136 (2003) 119-124
31. Akiyama T., Ohuchi T., Sumida S., Matsumoto K., and Toyoshima K. Phosphorylation of the retinoblastoma protein by cdk2. Proc. Natl. Acad. Sci. USA 89 (1992) 7900-7904
32. Adams P.D., Li X., Sellers W.R., Baker K.B., Leng X., Harper J.W., Taya Y., and Kaelin Jr. W.G. Retinoblastoma protein contains a C-terminal motif that targets it for phosphorylation by cyclin-cdk complexes. Mol. Cell. Biol. 19 (1999) 1068-1080
33. Hedley D.W., and Chow S. Evaluation of methods for measuring cellular glutathione content using flow cytometry. Cytometry 15 (1994) 349-358
34. Gooch K.J., Dangler C.A., and Frangos J.A. Exogenous, basal, and flow-induced nitric oxide production and endothelial cell proliferation. J. Cell. Physiol. 171 (1997) 252-258
35. Rosenberg P.A., Li Y., Ali S., Altiok N., Back S.A., and Volpe J.J. Intracellular redox state determines whether nitric oxide is toxic or protective to rat oligodendrocytes in culture. J. Neurochem. 73 (1999) 476-484
36. Jaffrey S.R., Erdjument-Bromage H., Ferris C.D., Tempst P., and Snyder S.H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3 (2001) 193-197
37. Selemidis S., Dusting G.J., Peshavariya H., Kemp-Harper B.K., and Drummond G.R. Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc. Res. 75 (2007) 349-358
38. Moellering D., Mc Andrew J., Patel R.P., Forman H.J., Mulcahy R.T., Jo H., and Darley-Usmar V.M. The induction of GSH synthesis by nanomolar concentrations of NO in endothelial cells: a role for gamma-glutamylcysteine synthetase and gamma-glutamyl transpeptidase. FEBS Lett. 448 (1999) 292-296
39. Johnson D.G., and Walker C.L. Cyclins and cell cycle checkpoints. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 295-312
40. Ishimura N., Bronk S.F., and Gores G.J. Inducible nitric oxide synthase upregulates cyclooxygenase-2 in mouse cholangiocytes promoting cell growth. Am. J. Physiol. Gastrointest. Liver Physiol 287 (2004) G88-95
41. Gow A.J., Chen Q., Hess D.T., Day B.J., Ischiropoulos H., and Stamler J.S. Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem 277 (2002) 9637-9640
42. 1-protease inhibitor after S-nitrosylation: inhibition of cysteine protease and antibacterial activity. Biochem. Biophys. Res. Commun. 267 (2000) 918-923
43. Lander H.M., Hajjar D.P., Hempstead B.L., Mirza U.A., Chait B.T., Campbell S., and Quilliam L.A. A molecular redox switch on p21(ras): structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem. 272 (1997) 4323-4326
44. Alessi F., Quarta S., Savio M., Riva F., Rossi L., Stivala L.A., Scovassi A.I., Meijer L., and Prosperi E. The cyclin-dependent kinase inhibitors olomoucine and roscovitine arrest human fibroblasts in G1 phase by specific inhibition of CDK2 kinase activity. Exp. Cell Res. 245 (1998) 8-18
45. Wesierska-Gadek J., Gueorguieva M., Wojciechowski J., and Horky M. Cell cycle arrest induced in human breast cancer cells by cyclin-dependent kinase inhibitors: a comparison of the effects exerted by roscovitine and olomoucine. Pol. J. Pharmacol. 56 (2004) 635-641
46. Edamatsu H., Gau C.L., Nemoto T., Guo L., and Tamanoi F. Cdk inhibitors, roscovitine and olomoucine, synergize with farnesyltransferase inhibitor (FTI) to induce efficient apoptosis of human cancer cell lines. Oncogene, 19 (2000) 3059-3068
47. Lala P.K., and Chakraborty C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2 (2001) 149-156
48. Jenkins D.C., Charles I.G., Thomsen L.L., Moss D.W., Holmes L.S., Baylis S.A., Rhodes P., Westmore K., Emson P.C., and Moncada S. Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA 92 (1995) 4392-4396