Nitric oxide induces cell death by regulating anti-apoptotic BCL-2 family members

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Snyder, Colleen M ^a   Shroff, Emelyn H ^a   Liu, Jing ^a   Chandel, Navdeep S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; CYTOCHROME C; DIETHYLENETRIAMINE; LACTATE DEHYDROGENASE; NITRIC OXIDE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; APOPTOSIS SIGNAL REGULATING KINASE 1; BAK1 PROTEIN, MOUSE; BAX PROTEIN, MOUSE; MAP3K5 PROTEIN, MOUSE; MULTIENZYME COMPLEX; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE 1;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL TRANSPORT; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME RELEASE; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN DEFICIENCY; WILD TYPE; ANIMAL; APOPTOSIS; FIBROBLAST; GENE EXPRESSION REGULATION; METABOLISM; MULTIGENE FAMILY;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CASPASE 9; CYTOCHROMES C; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; FIBROBLASTS; GENE EXPRESSION REGULATION; MAP KINASE KINASE KINASE 5; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 8; MULTIGENE FAMILY; NITRIC OXIDE; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES;

EID: 70349509861     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007059     Document Type: Article

References (51)

1. Brown GC, Cooper CE (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356: 295-298.
2. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 345: 50-54.
3. Bolanos JP, Peuchen S, Heales SJ, Land JM, Clark JB (1994) Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochem 63: 910-916.
4. Clementi E, Brown GC, Feelisch M, Moncada S (1998) Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci U S A 95: 7631-7636.
5. Moncada S, Erusalimsky JD (2002) Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 3: 214-220.
6. Go YM, Patel RP, Maland MC, Park H, Beckman JS, et al. (1999) Evidence for peroxynitrite as a signaling molecule in flow-dependent activation of c-Jun NH(2)-terminal kinase. Am J Physiol 277: H1647-1653.
7. Shacka JJ, Sahawneh MA, Gonzalez JD, Ye YZ, D'Alessandro TL, et al. (2006) Two distinct signaling pathways regulate peroxynitrite-induced apoptosis in PC12 cells. Cell Death Differ 13: 1506-1514.
8. Schieke SM, Briviba K, Klotz LO, Sies H (1999) Activation pattern of mitogen-activated protein kinases elicited by peroxynitrite: attenuation by selenite supplementation. FEBS Lett 448: 301-303.
9. Hsu YT, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci U S A 94: 3668-3672.
10. Antonsson B, Montessuit S, Sanchez B, Martinou JC (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276: 11615-11623.
11. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
12. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, et al. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
13. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157.
14. Willis SN, Chen L, Dewson G, Wei A, Naik E, et al. (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19: 1294-1305.
15. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, et al. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192.
16. Messmer UK, Reed UK, Brune B (1996) Bcl-2 protects macrophages from nitric oxide-induced apoptosis. J Biol Chem 271: 20192-20197.
17. Okada S, Zhang H, Hatano M, Tokuhisa T (1998) A physiologic role of Bcl-xL induced in activated macrophages. J Immunol 160: 2590-2596.
18. Ing DJ, Zang J, Dzau VJ, Webster KA, Bishopric NH (1999) Modulation of cytokine-induced cardiac myocyte apoptosis by nitric oxide, Bak, and Bcl-x. Circ Res 84: 21-33.
19. Lee VY, McClintock DS, Santore MT, Budinger GR, Chandel NS (2002) Hypoxia sensitizes cells to nitric oxide-induced apoptosis. J Biol Chem 277: 16067-16074.
20. Brunelle JK, Shroff EH, Perlman H, Strasser A, Moraes CT, et al. (2007) Loss of Mcl-1 protein and inhibition of electron transport chain together induce anoxic cell death. Mol Cell Biol 27: 1222-1235.
21. Liu J, Minemoto Y, Lin A (2004) c-Jun N-terminal protein kinase 1 (JNK1), but not JNK2, is essential for tumor necrosis factor alpha-induced c-Jun kinase activation and apoptosis. Mol Cell Biol 24: 10844-10856.
22. Emerling BM, Platanias LC, Black E, Nebreda AR, Davis RJ, et al. (2005) Mitochondrial reactive oxygen species activation of p38 mitogen-activated protein kinase is required for hypoxia signaling. Mol Cell Biol 25: 4853-4862.
23. Mandic A, Viktorsson K, Molin M, Akusjarvi G, Eguchi H, et al. (2001) Cisplatin induces the proapoptotic conformation of Bak in a deltaMEKK1-dependent manner. Mol Cell Biol 21: 3684-3691.
24. Pervin S, Singh R, Chaudhuri G (2001) 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 U S A 98: 3583-3588.
25. Pervin S, Singh R, Gau CL, Edamatsu H, Tamanoi F, et al. (2001) Potentiation of nitric oxide-induced apoptosis of MDA-MB-468 cells by farnesyltransferase inhibitor: implications in breast cancer. Cancer Res 61: 4701-4706.
26. Pfeilschifter J, Huwiler A (1996) Nitric oxide stimulates stress-activated protein kinases in glomerular endothelial and mesangial cells. FEBS Lett 396: 67-70.
27. Callsen D, Brune B (1999) Role of mitogen-activated protein kinases in S-nitrosoglutathione-induced macrophage apoptosis. Biochemistry 38: 2279-2286.
28. Lei K, Davis RJ (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci U S A 100: 2432-2437.
29. Putcha GV, Le S, Frank S, Besirli CG, Clark K, et al. (2003) JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron 38: 899-914.
30. Harris CA, Johnson EM, Jr. (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J Biol Chem 276: 37754-37760.
31. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
32. Sarker KP, Biswas KK, Rosales JL, Yamaji K, Hashiguchi T, et al. (2003) Ebselen inhibits NO-induced apoptosis of differentiated PC12 cells via inhibition of ASK1-p38 MAPK-p53 and JNK signaling and activation of p44/ 42 MAPK and Bcl-2. J Neurochem 87: 1345-1353.
33. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, et al. (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/ JNK and p38 signaling pathways. Science 275: 90-94.
34. Cuconati A, Mukherjee C, Perez D, White E (2003) DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells. Genes Dev 17: 2922-2932.
35. Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, et al. (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev 17: 1475-1486.
36. Czabotar PE, Lee EF, van Delft MF, Day CL, Smith BJ, et al. (2007) Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci U S A 104: 6217-6222.
37. Zhong Q, Gao W, Du F, Wang X (2005) Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121: 1085-1095.
38. Gotoh Y, Cooper JA (1998) Reactive oxygen species- and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction. J Biol Chem 273: 17477-17482.
39. Mendelson KG, Contois LR, Tevosian SG, Davis RJ, Paulson KE (1996) Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc Natl Acad Sci U S A 93: 12908-12913.
40. Clerk A, Fuller SJ, Michael A, Sugden PH (1998) Stimulation of "stress-regulated" mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J Biol Chem 273: 7228-7234.
41. Poderoso JJ, Carreras MC, Lisdero C, Riobo N, Schopfer F, et al. (1996) Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch Biochem Biophys 328: 85-92.
42. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, et al. (2006) Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10: 241-252.
43. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, et al. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859.
44. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, et al. (2006) Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8: 1348-1358.
45. Song L, Li Y, Sun Y, Shen B (2002) Mcl-1 mediates cytokine deprivation induced apoptosis of human myeloma cell line XG-7. Chin Med J (Engl) 115: 1241-1243.
46. Jourdan M, Veyrune JL, De Vos J, Redal N, Couderc G, et al. (2003) A major role for Mcl-1 antiapoptotic protein in the IL-6-induced survival of human myeloma cells. Oncogene 22: 2950-2959.
47. Deng Y, Ren X, Yang L, Lin Y, Wu X (2003) A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 115: 61-70.
48. Inoshita S, Takeda K, Hatai T, Terada Y, Sano M, et al. (2002) Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 277: 43730-43734.
49. Kobayashi S, Lee SH, Meng XW, Mott JL, Bronk SF, et al. (2007) Serine 64 phosphorylation enhances the antiapoptotic function of Mcl-1. J Biol Chem 282: 18407-18417.
50. Lander HM, Jacovina AT, Davis RJ, Tauras JM (1996) Differential activation of mitogen-activated protein kinases by nitric oxide-related species. J Biol Chem 271: 19705-19709.
51. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, et al. (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. Embo J 17: 2596-2606.