Mitochondrial c-Jun NH2-terminal kinase prevents the accumulation of reactive oxygen species and reduces necrotic damage in neural tumor cells that lack trophic support

Molecular Cancer Research

Volumn 5, Issue 1, 2007, Pages 47-60

  López Sánchez, Noelia ^a   Rodríguez, José Rodrigo ^a   Frade, José María ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; REACTIVE OXYGEN METABOLITE; SCAVENGER; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CELL CYCLE PROGRESSION; CELL DEATH; CELL MEMBRANE POTENTIAL; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RELEASE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MITOCHONDRION; NERVE CELL; NEURILEMOMA; NEUROBLASTOMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; TROPHIC CASCADE; TUMOR CELL;

ANIMALS; CELL DEATH; CULTURE MEDIA, SERUM-FREE; CYTOCHROMES C; ENZYME INHIBITORS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; NECROSIS; NEURILEMMOMA; NEUROBLASTOMA; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED;

EID: 33846986842     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-06-0233     Document Type: Article

References (74)

1. Green DR, Evan GI. A matter of life and death. Cancer Cell 2002;1:19-30.
2. Leist M, Jäättelä M. Four deaths and a funeral: from caspases to alternative mechanisms. Nature Rev Mol Cell Biol 2001;2:1-10.
3. Hibi M, Lin A, Smeal T, Minden A, Karin M. Identification of an oncoprotein-and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 1993;7:2135-48.
4. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000;103:239-52.
5. Maundrell K, Antonsson B, Magnenat E, et al. Bcl-2 undergoes phosphorylation by c-Jun N-terminal kinase/stress-activated protein kinases in the presence of the constitutively active GTP-binding protein Rac1. J Biol Chem 1997;272:25238-42.
6. Morrison DK, Davis RJ. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 2003;19:91-118.
7. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001;81:807-69.
8. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 2001;410:37-40.
9. Bost F, McKay R, Dean N, Mercola D. The JUN kinase/stress-activated protein kinase pathway is required for epidermal growth factor stimulation of growth of human A549 lung carcinoma cells. J Biol Chem 1997;272:33422-9.
10. Bost F, McKay R, Bost M, Potapova O, Dean NM, Mercola D. The Jun kinase 2 isoform is preferentially required for epidermal growth factor-induced transformation of human A549 lung carcinoma cells. Mol Cell Biol 1999;19:1938-49.
11. Yang YM, Bost F, Charbono W, et al. C-Jun NH(2)-terminal kinase mediates proliferation and tumor growth of human prostate carcinoma. Clin Cancer Res 2003;9:391-401.
12. Venugopal R, Jaiswal AK. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 1998;17:3145-56.
13. Wang MC, Bohmann D, Jasper H. JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 2003;5:811-6.
14. Karbowski M, Youle RJ. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 2003;10:870-80.
15. Bossy-Wetzel E, Barsoum MJ, Godzik A, Schwarzenbacher R, Lipton SA. Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr Opin Cell Biol 2003;15:706-16.
16. Sesaki H, Jensen RE. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol 1999;147:699-706.
17. Nunnari J, Marshall W, Straight A, Murray A, Sedat J, Walter P. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol Biol Cell 1997;8:1233-42.
18. Frank S, Gaume B, Bergmann-Leitner ES, et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 2001;1:515-25.
19. Pfeiffer SE, Wechsler W. Biochemically differentiated neoplastic clone of Schwann cells. Proc Natl Acad Sci U S A 1972;69:2885-9.
20. Gentry JJ, Casaccia-Bonnefil P, Carter BD. Nerve growth factor activation of nuclear factor κB through its p75 receptor is an anti-apoptotic signal in RN22 schwannoma cells. J Biol Chem 2000;275:7558-65.
21. Frade JM. Nuclear translocation of the p75 neurotrophin receptor cytoplasmic domain in response to neurotrophin binding. J Neurosci 2005;25:1407-11.
22. Susen K, Blochl A. Low concentrations of aggregated β-amyloid induce neunte formation via the neurotrophin receptor p75. J Mol Med 2005;83:720-35.
23. Ito Y, Mishra NC, Yoshida K, Kharbanda S, Saxena S, Kufe D. Mitochondrial targeting of JNK/SAPK in the phorbol ester response of myeloid leukemia cells. Cell Death Differ 2001;8:794-800.
24. Kharbanda S, Saxena S, Yoshida K, et al. Translocation of SAPK/JNK to mitochondria and interaction with Bcl-x(L) in response to DNA damage. J Biol Chem 2000;275:322-7.
25. Brichese L, Cazettes G, Valette A. JNK is associated with Bcl-2 and PP1 in mitochondria: paclitaxel induces its activation and its association with the phosphorylated form of Bcl-2. Cell Cycle 2004;3:1312-9.
26. Hollinshead M, Sanderson J, Vaux DJ. Anti-biotin antibodies offer superior organelle-specific labeling of mitochondria over avidin or streptavidin. J Histol Cytochem 1997;45:1053-7.
27. Potapova O, Gorospe M, Bost F, et al. c-Jun N-terminal kinase is essential for growth of human T98G glioblastoma cells. J Biol Chem 2000;275:24767-75.
28. Dougherty CJ, Kubasiak LA, Prentice H, Andreka P, Bishopric NH, Webster KA. Activation of c-Jun N-terminal kinase promotes survival of cardiac myocytes after oxidative stress. Biochem J 2002;362:561-71.
29. Yu C, Minemoto Y, Zhang J, et al. JNK suppresses apoptosis via phosphorylation of the proapoptotic Bcl-2 family protein BAD. Mol Cell 2004;13:329-40.
30. Bennett BL, Sasaki DT, Murray BW, et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 2001;98:13681-6.
31. 2-terminal protein kinase inhibitor with neuroprotective properties. J Pharmacol Exp Ther 2004;310:25-32.
32. Holzberg D, Knight CG, Dittrich-Breiholz O, et al. Disruption of the c-JUN-JNK complex by a cell-permeable peptide containing the c-JUN δ domain induces apoptosis and affects a distinct set of interleukin-1-induced inflammatory genes. J Biol Chem 2003;278:40213-23.
33. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999;397:441-6.
34. Lockshin RA, Zakeri Z. Apoptosis, autophagy, and more. Int J Biochem Cell Biol 2004;36:2405-19.
35. Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004;23:2891-906.
36. Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000;19:5720-8.
37. Boya P, González-Polo R-A, Casares N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005;25:1025-40.
38. Johnson LV, Walsh ML, Chen LB. Localization of mitochondria in living cells with rhodamine 123. Proc Natl Acad Sci U S A 1980;77:990-4.
39. Darzynkiewicz Z, Staiano-Coico L, Melamed MR. Increased mitochondrial uptake of rhodamine 123 during lymphocyte stimulation. Proc Natl Acad Sci U S A 1981;78:2383-7.
40. Darzynkiewicz Z, Traganos F, Staiano-Coico L, Kapuscinski J, Melamed MR. Interactions of rhodamine 123 with living cells studied by flow cytometry. Cancer Res 1982;42:799-806.
41. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997;416:15-8.
42. Liu SS. Cooperation of a "reactive oxygen cycle" with the Q cycle and the proton cycle in the respiratory chain - superoxide generating and cycling mechanisms in mitochondria. J Bioenerg Biomemb 1999;31:367-76.
43. Halliwell B, Gutteridge JMC. Free radicals in biology and medicine, 3rd ed. Oxford: Oxford University Press; 2003.
44. Patel M, Day BJ. Metalloporphyrin class of therapeutic catalytic antioxidants. Trends Pharmacol Sci 1999;20:359-64.
45. Wu AS, Kiaei M, Aguirre N, et al. Iron porphyrin treatment extends survival in a transgenic animal model of amyotrophic lateral sclerosis. J Neurochem 2003;85:142-50.
46. Yu T, Robotham JL, Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci U S A 2006;103:2653-8.
47. Funk RH, Nagel F, Wonka F, Krinke HE, Gölfert F, Hofer A. Effects of heat shock on the functional morphology of cell organelles observed by video-enhanced microscopy. Anat Rec 1999;255:458-64.
48. Roue G, Bitton N, Yuste VJ, et al. Mitochondrial dysfunction in CD47-mediated caspase-independent cell death: ROS production in the absence of cytochrome c and AIF release. Biochimie 2003;85:741-6.
49. Guerrieri F, Pellecchia G, Lopriore B, et al. Changes in ultrastructure and the occurrence of permeability transition in mitochondria during rat liver regeneration. Eur J Biochem 2002;269:3304-12.
50. Lim ML, Minamikawa T, Nagley P. The protonophore CCCP induces mitochondrial permeability transition without cytochrome c release in human osteosarcoma cells. FEBS Lett 2001;503:69-74.
51. Gadd ME, Broekemeier KM, Crouser ED, Kumar J, Graff G, Pfeiffer DR. Mitochondrial iPLA2 activity modulates the release of cytochrome c from mitochondria and influences the permeability transition. J Biol Chem 2006;281:6931-9.
52. Morkuniene R, Jekabsone A, Borutaite V. Estrogens prevent calcium-induced release of cytochrome c from heart mitochondria. FEBS Lett 2002;521:53-6.
53. Antonyak MA, Kenyon LC, Godwin AK, et al. Elevated JNK activation contributes to the pathogenesis of human brain tumors. Oncogene 2002;21:5038-46.
54. Wiltshire C, Matsushita M, Tsukada S, Gillespie DA, May GH. A new c-Jun N-terminal kinase (JNK)-interacting protein, Sab (SH3BP5),associates with mitochondria. Biochem J 2002;367:577-85.
55. Wiltshire C, Gillespie DA, May GH. Sab (SH3BP5), a novel mitochondria-localized JNK-interacting protein. Biochem Soc Trans 2004;32:1075-7.
56. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 1999;22:667-76.
57. Sabapathy K, Jochum W, Hochedlinger K, Chang L, Karin M, Wagner EF. Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 1999;89:115-24.
58. Khaled AR, Reynolds DA, Young HA, Thompson CB, Muegge K, Durum SK. Interleukin-3 withdrawal induces an early increase in mitochondrial membrane potential unrelated to Bcl-2 family. Roles of intracellular pH, ADP transport, and F(0)F(1)-ATPase. J Biol Chem 2001;276:6453-62.
59. Kowaltowski AJ, Cosso RG, Campos CB, Fiskum G. Effect of Bcl-2 overexpression on mitochondrial structure and function. J Biol Chem 2002;277:42802-7.
60. 2 and modulates the growth arrest response to scavenging of H2O2 by catalase. Exp Cell Res 2003;285:146-58.
61. Zou X, Tsutsui T, Ray D, et al. The cell cycle-regulatory CDC25A phosphatase inhibits apoptosis signal-regulating kinase 1. Mol Cell Biol 2001;21:4818-28.
62. Chen K, Vita JA, Berk BC, Keaney JF, Jr. c-Jun N-terminal kinase activation by hydrogen peroxide in endothelial cells involves SRC-dependent epidermal growth factor receptor transactivation. J Biol Chem 2001;276:16045-50.
63. Dougherty CJ, Kubasiak LA, Li DP, et al. Mitochondrial signals initiate the activation of c-Jun N-terminal kinase (JNK) by hypoxia-reoxygenation. FASEB J 2004;18:1060-70.
64. Chen YR, Shrivastava A, Tan TH. Down-regulation of the c-Jun N-terminal kinase (JNK) phosphatase M3/6 and activation of JNK by hydrogen peroxide and pyrrolidine dithiocarbamate. Oncogene 2001;20:367-74.
65. Chen R, Fearnley IM, Peak-Chew SY, Walker JE. The phosphorylation of subunits of complex I from bovine heart mitochondria. J Biol Chem 2004;279:26036-45.
66. Schulenberg B, Goodman TN, Aggeler R, Capaldi RA, Patton WF. Characterization of dynamic and steady-state protein phosphorylation using a fluorescent phosphoprotein gel stain and mass spectrometry. Electrophoresis 2004;25:2526-32.
67. Thomson M. Evidence of undiscovered cell regulatory mechanisms: phosphoproteins and protein kinases in mitochondria. Cell Mol Life Sci 2002;59:213-9.
68. Raha S, Myint AT, Johnstone L, Robinson BH. Control of oxygen free radical formation from mitochondrial complex I: roles for protein kinase A and pyruvate dehydrogenase kinase. Free Radic Biol Med 2002;32:421-30.
69. Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol 2000;20:7311-8.
70. 2+ homeostasis of mitochondria in endothelial cells. J Cardiovasc Pharmacol 2004;44:423-36.
71. Cripe LD, Gelfanov VM, Smith EA, et al. Role for c-jun N-terminal kinase in treatment-refractory acute myeloid leukemia (AML): signaling to multidrug-efflux and hyperproliferation. Leukemia 2002;16:799-812.
72. Hayakawa J, Depatie C, Ohmichi M, Mercola D. The activation of c-Jun NH2-terminal kinase (JNK) by DNA-damaging agents serves to promote drug resistance via activating transcription factor 2 (ATF2)-dependent enhanced DNA repair. J Biol Chem 2003;278:20582-92.
73. Ruiz F, Alvarez G, Ramos M, Hernandez M, Bogonez E, Satrustegui J. Cyclosporin A targets involved in protection against glutamate excitotoxicity. Eur J Pharmacol 2000;404:29-39.
74. Martinou I, Desagher S, Eskes R, et al. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J Cell Biol 1999;144:883-9.