Methylpyridinium (MPP+)- and nerve growth factor-induced changes in pro- and anti-apoptotic signaling pathways in SH-SY5Y neuroblastoma cells

Brain Research

Volumn 952, Issue 1, 2002, Pages 98-110

  Halvorsen, Erik M ^a   Dennis, Jameel ^a   Keeney, Paula M ^a   Sturgill, Thomas W ^a   Tuttle, Jeremy B ^a   Bennett Jr , James P ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Akt; Apoptosis; Cell signaling; MAPK; Methylpyridinium; NGF; Parkinson's disease

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; DOPAMINE; ENZYME INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYLPYRIDINIUM; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN KINASE B; PYRIDINIUM DERIVATIVE; SB 203540; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL ASSAY; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXPOSURE; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIME;

1-METHYL-4-PHENYLPYRIDINIUM; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; CARRIER PROTEINS; DRUG INTERACTIONS; HUMANS; MAP KINASE KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE GROWTH FACTOR; NEUROBLASTOMA; NEURONS; NEUROTOXINS; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; TUMOR CELLS, CULTURED;

EID: 0037064274     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03216-X     Document Type: Article

References (68)

1. Azad B., Brunet A., West A.E., Datta S.R., Takasu M.A., Greenberg M.E. Cell survival promoted by the ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science. 286:(5443):1999;1358-1362.
2. Blum D., Torch S., Lambeng N., Nissou M., Benabid A.L., Sadoul R., Verna J.M. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog. Neurobiol. 65:2001;135-172.
3. Burgering B.M., Coffer P.J. Protein kinase B (c-Akt) in phosphatidylinositol-3-0H kinase signal transduction. Nature. 376:(6541):1995;599-602.
4. Cassarino D.S., Fall C.P., Swerdlow R.H., Smith T.S., Halvorsen E.M., Miller S.W., Parks J.P., Parker W.D. Jr., Bennett J.P. Jr. Elevated reactive oxygen species and antioxidant enzyme activities in animal and cellular models of Parkinson's disease. Biochim. Biophys. Acta. 1362:(1):1997;77-86.
5. Cassarino D.S., Bennett J.P. Jr. An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 29:1999;1-25.
6. Cassarino D.S., Halvorsen E.M., Swerdlow R.H., Abramova N., Parker W.D. Jr., Sturgill T.W., Bennett J.P. Jr. Interaction among mitochondria, mitogen-activated protein kinases, and nuclear factor-kappaB in cellular models of Parkinson's disease. J. Neurochem. 74:(4):2000;1384-1392.
7. Chang L., Karin M. Mammalian MAP kinase signaling cascades. Nature. 410:2001;37-40.
8. Chen J., Fujii K., Zhang L., Roberts T., Haian F. Raf-1 promotes cell survival by antagonizing apoptosis signal-regulating kinase 1 through a MEK-ERK independent mechanism. Proc. Natl. Acad. Sci. USA. 98:2001;7783-7788.
9. Chun H.S., Gibson G.E., DeGiorgio L.A., Zhang H., Kidd V.J., Son J.H. Dopaminergic cell death induced by MPP(+), oxidant and specific neurotoxicants shares the common molecular mechanism. J. Neurochem. 76:2001;1010-1021.
10. Cross T.G., Scheel-Toellner D., Henriquez N.V., Deacon E., Salmon M., Lord J.M. Serine/threonine protein kinases and apoptosis. Exp. Cell Res. 256:2000;34-41.
11. Datta K., Bellacosa A., Chan T.O., Tsichlis P.N. Akt is a direct target of the phosphatidylinositol 3-kinase. Activation by growth factors, v-src and v-Ha-ras, in Sf9 and mammalian cells. J. Biol. Chem. 271:(48):1996;30835-30839.
12. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 91:(2):1997;231-241.
13. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three Akts. Genes Dev. 13:(22):1999;2905-2927.
14. Datta S.R., Katsov A., Hu L., Petros A., Fesik S.W., Yaffe M.B., Greenberg M.E. 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol. Cell. 6:2000;41-51.
15. del Peso L., Gonzalez-Garcia M., Page C., Herrera R., Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science. 278:1997;687-689.
16. Deng X., Xiao L., Lang W., Gao F., Ruvulo P., May W.S. Jr. Novel role for JNK as a stress-activated Bcl2 kinase. J. Biol. Chem. 276:2001;23681-23688.
17. Downward J. How BAD phosphorylation is good for survival. Nature Cell Biol. 1:1999;E33-E35.
18. Eves E.M., Xiong W., Bellacosa A., Kennedy S.G., Tsichlis P.N., Rosner M.R., Hay N. Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol. Cell. Biol. 18:1998;2143-2152.
19. +-induced apoptosis in human SH-SY5Y neuroblastoma cells. J. Neurosci. Res. 55:1999;620-628.
20. Fang X., Yu S., Eder A., Mao M., Bast R.C. Jr., Boyd D., Mill G.B. Regulation of BAD phosphorylation at serine 112 by the Ras-mitogen-activated protein kinase pathway. Oncogene. 18:1999;6634-6635.
21. Galetic I., Andjelkovic M., Meier R., Brodbeck D., Park J., Hemmings B.A. Mechanism of protein kinase B activation by insulin/insulin-like growth factor-1 revealed by specific inhibitors of phosphoinositide 3-kinase - significance for diabetes and cancer. Pharmacol. Ther. 82:1999;409-425.
22. Ghatan S., Larner S., Kinoshita Y., Hetman M., Patel L., Xia Z., Youle R.J., Morrison R.S. p38 Map kinase mediates Bax translocation in nitric oxide-induced apoptosis in neurons. J. Cell Biol. 150:2000;335-347.
23. Ghoda L., Lin X., Greene W.C. The 90-kDa ribosomal S6 kinase (pp90rsk) phosphorylates the N-terminal regulatory domain of IkappaBalpha and stimulates its degradation in vitro. J. Biol. Chem. 272:1997;21281-21288.
24. Gomez C., Reiriz J., Pique M., Gil J., Ferrer I., Ambrosio S. Low concentrations of 1-methyl-4-phenylpyridinium ion induce caspase-mediated apoptosis in human SH-SY5Y neuroblastoma cells. J. Neurosci. Res. 63:2001;421-428.
25. Hamanoue M., Middleton G., Wyatt S., Jaffray E., Hay R.T., Davies A.M. p75-Mediated NF-KB activation enhances the survival response of developing sensory neurons to nerve growth factor. Mol. Cell. Neurosci. 14:1999;28-40.
26. Harada H., Becknell B., Wilm M., Mann M., Huang L.J., Taylor S.S., Scott J.D., Korsmeyer S.J. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell. 3:1999;413-422.
27. Hartmann A., Hunot S., Michel P.P., Muriel M.P., Vyas S., Faucheux B.A., Mouatt-Prigent A., Turmel H., Srinivasan A., Ruberg M., Evan G.I., Agid Y., Hirsch E.C. Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc. Natl. Acad. Sci. USA. 97:2000;2875-2880.
28. Hetman M., Kanning K., Cavanaugh J.E., Xia Z. Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. J. Biol. Chem. 274:1999;22569-22580.
29. Heumann R., Goemans C., Bartsch D., Lingenhohl K., Waldmeier P.C., Hengerer B., Allegrini P.R., Schellander K., Wagner E.F., Arendt T., Kamdem R.H., Obst-Pernberg K., Narz F., Wahle P., Berns H. Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J. Cell Biol. 151:2000;1537-1548.
30. Jellinger K.A. Cell death mechanisms in Parkinson's disease. J. Neural Transm. 107:2000;1-29.
31. Kaplan D.R., Miller F.D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10:2000;381-391.
32. Karin M. The beginning of the end: IKB kinase (IKK) and NF kKB activation. J. Biol. Chem. 274:(39):1999;27339-27342.
33. Keyse S.M. Protein phosphatases and the regulation of mitogen-activated protein kinase signaling. Curr. Opin. Cell Biol. 12:2000;186-192.
34. Khwaja A. Akt is more than just a BAD kinase. Nature. 401:(6748):1999;33-34.
35. King T.D., Bijur G.N., Jope R.S. Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3beta and attenuated by lithium. Brain Res. 919:2001;106-114.
36. Le-Niculescu H., Bonfoco E., Kasuya Y., Claret F.X., Green D.R., Karin M. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol. Cell. Biol. 19:1999;751-763.
37. Levkau B., Scatena M., Giachelli C.M., Ross R., Raines E.W. Apoptosis overrides survival signals through a caspase-mediated dominant-negative NF-kB loop. Nat. Cell. Biol. 1:1999;227-233.
38. Madrid L.V., Wang C.Y., Guttridge D.C., Schottelius A.J., Baldwin A.S. Jr., Mayo M.W. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol. Cell. Biol. 20:2000;1626-1638.
39. Martinou I., Desagher S., Eskes R., Antonsson B., Andre E., Fakan S., Martinou J.-C. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell Biol. 144:(5):1999;883-889.
40. Mattson M.P., Culmsee C., Yu Z., Camandola S. Roles of nuclear factor kB in neuronal survival and plasticity. J. Neurochem. 74:2000;443-456.
41. May M.J., Ghosh S. ReI/NF-KB and IKB proteins: an overview. Cancer Biol. 8:1997;63-73.
42. Mazzoni I.E., Said F.A., Aloyz R., Miller F.D., Kaplan D. Ras regulates sympathetic neuron survival by suppressing the p53-mediated cell death pathway. J. Neurosci. 19:1999;9716-9727.
43. Meier R., Alessi D.R., Cron P., Andjelkovic M., Hemmings B.A. Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bβ J. Biol. Chem. 272:1997;30491-30497.
44. Mielke K., Herdegen T. JNK and p38 stresskinases - degenerative effectors of signal-transduction cascades in the nervous system. Prog. Neurobiol. 61:2000;45-60.
45. Ottilie S., Diaz J.-L., Horne W., Chang J., Wang Y., Wilson G., Chang S., Weeks S., Fritz L.C., Oltersdorf T. Dimerization properties of human BAD. J. Biol. Chem. 272:1997;30866-30872.
46. Ozes O.N., Mayo L.D., Gustin J.A., Pfeffer S.R., Pfeffer L.M., Donner D.B. NF-kB activation by tumor necrosis factor requires the AKT serine-threonine kinase. Nature. 401:1999;82-85.
47. Panet H., Barzilai A., Daily D., Melamed E., Offen D. Activation of nuclear transcription factor kappa B (NF-kB) is essential for dopamine-induced apoptosis in PC-12 cells. J. Neurochem. 77:2001;391-398.
48. Parrizas M., Saltiel A.R., LeRoith D. Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272:1997;154-161.
49. Pastorino J.G., Tafani M., Farber J.L. Tumor necrosis factor induces phosphorylation and translocation of BAD through phosphoinositide-3-OH kinase-dependent pathway. J. Biol. Chem. 274:1999;19411-19416.
50. Przedborski S., Jackson-Lewis V., Naini A.B., Jakowec M., Petzinger G., Miller R., Akram M. The parkinsonian toxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP): a technical review of its utility and safety. J. Neurochem. 76:2001;1265-1274.
51. Romashkova J.A., Makarov S.S. NF-kappaB is a target of AKT in anti-apoptotic PDGF signaling. Nature. 401:1999;86-90.
52. Sabbatini P., McCormick F. Phosphoinositide 3-OH kinase (PI3K) and PKB/Akt delay the onset of p53-mediated, transcriptionally dependent apoptosis. J. Biol. Chem. 274:1999;24263-24269.
53. Saporito M.S., Brown E.M., Miller M.S., Carswell S. CEP-1347/KT-7515, an inhibitor of c-jun N-terminal kinase activation, attenuates the 1-methyl-4-phenyl tetrahydropyridine-mediated loss of nigrostriatal dopaminergic neurons in vivo. J. Pharmacol. Exp. Ther. 288:1999;421-427.
54. Saporito M.S., Thomas B.A., Scott R.W. MPTP activates c-Jun NH(2)-terminal kinase (JNK) and its upstream regulatory kinase MKK4 in nigrostriatal neurons in vivo. J. Neurochem. 75:2000;1200-1208.
55. Scheid M.P., Schubert K.M., Duroni V. Regulation of BAD phosphorylation and association with Bcl-xL by the MAPK/Erk kinase. J. Biol. Chem. 274:1999;31108-31113.
56. Schouten G.J., Vertegaal A.C., Whiteside S.T., Israel A., Toebes M., Dorsman J.C., van der Eb A.J., Zantema A. IkappaB alpha is a target for the mitogen-activated 90 kDa ribosomal S6 kinase. EMBO J. 16:1997;3133-3144.
57. Shimoke K., Chiba H. Nerve growth factor prevents 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced cell death via the Akt pathway by suppressing caspase-3-like activity using PC12 cells: relevance to therapeutic application for Parkinson's disease. J. Neurosci. Res. 63:2001;402-409.
58. Swerdlow R.H., Parks J.K., Miller S.W., Tuttle J.B., Trimmer P.A., Sheehan J.P., Bennett J.P. Jr., Davis R.E., Parker W.D. Jr. Origin and functional consequences of the complex I defect in Parkinson's disease. Ann. Neurol. 40:1996;663-671.
59. Tatton N.A. Increased caspase 3 and Bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp. Neurol. 166:2000;29-43.
60. Tatton N.A., Kish S.J. In situ detection of apoptotic nuclei in the substantia nigra compacta of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mice using terminal deoxynucleotidyl transferase labelling and acridine orange staining. Neuroscience. 77:1997;1037-1048.
61. Turmel H., Hartmann A., Parain K., Douhou A., Srinivasan A., Agid Y., Hirsch E.C. Caspase-3 activation in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. Mov. Disord. 16:2001;185-189.
62. Vaillant A.R., Mazzoni I., Tudan C., Boudreau M., Kaplan D.R., Miller F.D. Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal survival. J. Cell Biol. 146:1999;955-966.
63. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. Jr. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science. 281:1998;1680-1683.
64. Wang C.Y., Guttridge D.C., Mayo M.W., Baldwin A.S. Jr. NF-kappaB induces expression of the Bcl-2 homologue A 1/BfI-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 19:1999;5923-5929.
65. Wymann M.P., Pirola L. Structure and function of phosphoinositide 3-kinases. Biochim. Biophys. Acta. 1436:1998;127-150.
66. Xia X.G., Harding T., Weller M., Bieneman A., Uney J.B., Schulz J.B. Gene transfer of the JNK interacting protein-1 protects dopaminergic neurons in the MPTP model of Parkinson's disease. Proc. Natl. Acad. Sci. USA. 98:2001;10433-10438.
67. Xue L., Murray J.H., Tolkovsky A.M. The Ras/phosphatidylinositol 3-kinase and Ras/ERK pathways function as independent survival modules each of which inhibits a distinct apoptotic signaling pathway in sympathetic neurons. J. Biol. Chem. 275:2000;8817-8824.
68. Zhuang S., Demirs J.T., Kochevar I.E. p38 Mitogen-activated protein kinase mediates bid cleavage, mitochondrial dysfunction, and caspase-3 activation during apoptosis induced by singlet oxygen but not by hydrogen peroxide. J. Biol. Chem. 275:2000;25939-25948.