PINK1 overexpression protects against C2-ceramide-induced CAD cell death through the PI3K/AKT pathway

Journal of Molecular Neuroscience

Volumn 47, Issue 3, 2012, Pages 582-594

  Sánchez Mora, Ruth Mélida ^a,b   Arboleda, Humberto ^b   Arboleda, Gonzalo ^b  

^a Universidad Colegio Mayor de Cundinamarca   (Colombia)

^b UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

C2 ceramide; Mitochondria; Parkinson's disease; PI3K AKT; PINK1

Indexed keywords

CERAMIDE; PINK1 PROTEIN; PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WILD TYPE;

CELL DEATH; CELL LINE; CELL SURVIVAL; HUMANS; MITOCHONDRIAL MEMBRANES; PARKINSON DISEASE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SPHINGOSINE;

EID: 84863861489     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-011-9687-z     Document Type: Article

References (60)

1. Adams JM, Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281:1322-1326 (Pubitemid 28406819)
2. Arboleda G, Waters C, Gibson RM (2005) Metabolic activity: a novel indicator of neuronal survival in the murine dopaminergic cell line CAD. J Mol Neurosci 27:65-77
3. Arboleda G, Morales LC, Benitez B, Arboleda H (2009) Regulation of ceramide-induced neuronal death: cell metabolism meets neurodegeneration. Brain Res Rev 59:333-346
4. Beilina A, Van Der BM, Ahmad R et al (2005) Mutations in PTENinduced putative kinase 1 associated with recessive parkinsonism have differential effects on protein stability. Proc Natl Acad Sci USA 102:5703-5708 (Pubitemid 40559623)
5. bou-Sleiman PM, Muqit MM, McDonald NQ et al (2006) A heterozygous effect for PINK1 mutations in Parkinson's disease? Ann Neurol 60:414-419
6. Bras J, Singleton A, Cookson MR, Hardy J (2008) Emerging pathways in genetic Parkinson's disease: potential role of ceramide metabolism in Lewy body disease 1. FEBS J 275:5767-5773
7. Cookson MR (2010) The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson's disease. Nat Rev Neurosci 11:791-797
8. Cookson MR, Xiromerisiou G, Singleton A (2005) How genetics research in Parkinson's disease is enhancing understanding of the common idiopathic forms of the disease. Curr Opin Neurol 18:706-711 (Pubitemid 41669145)
9. Cutler RG, Kelly J, Storie K et al (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc Natl Acad Sci USA 101:2070-2075 (Pubitemid 38229016)
10. da Costa CA, Ancolio K, Checler F (2000) Wild-type but not Parkinson's disease-related ala-53 - > Thr mutant alpha-synuclein protects neuronal cells from apoptotic stimuli. J Biol Chem 275:24065-24069 (Pubitemid 30624697)
11. Dagda RK, Cherra SJ III et al (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 284:13843-13855
12. Darios F, Corti O, Lucking CB et al (2003) Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death. Hum Mol Genet 12:517-526 (Pubitemid 36305590)
13. Deng H, Jankovic J, Guo Y, Xie W, Le W (2005) Small interfering RNA targeting the PINK1 induces apoptosis in dopaminergic cells SH-SY5Y. Biochem Biophys Res Commun 337:1133-1138 (Pubitemid 41505244)
14. Dorsey ER, Constantinescu R, Thompson JP, Biglan KM, Holloway RG, Kieburtz K, Marshall FJ, Ravina BM, Schifitto G, Siderowf A, Tanner CM (2007) Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68:384-386 (Pubitemid 46184217)
15. Exner N, Treske B, Paquet D et al (2007) Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J Neurosci 27:12413-12418 (Pubitemid 350085485)
16. France-Lanord V, Brugg B, Michel PP, Agid Y, Ruberg M (1997) Mitochondrial free radical signal in ceramide-dependent apoptosis: a putative mechanism for neuronal death in Parkinson's disease. J Neurochem 69:1612-1621 (Pubitemid 27406962)
17. Sambrook J, Fritsch EF, Maniatis T (2003) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, NY, Vol. 1, 2, 3. Protocol 6, 1.51.Ref Type: Book Chapter
18. Funayama M, Hattori N (2007) [Molecular genetics of PINK1]1107. Brain Nerve 59:831-838
19. Gandhi S, Wood-Kaczmar A, Yao Z et al (2009) PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell 33:627-638
20. Ganesan V, Perera MN, Colombini D, Datskovskiy D, Chadha K, ColombiniM(2010) Ceramide and activated Bax act synergistically to permeabilize the mitochondrial outer membrane. Apoptosis 15:553-562
21. Gautier CA, Kitada T, Shen J (2008) Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci USA 105:11364-11369
22. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33-39 (Pubitemid 29046907)
23. Ha KS, Kim KM, Kwon YG et al (2003) Nitric oxide prevents 6- hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/AKT activation. FASEB J 17:1036-1047
24. Haque ME, Thomas KJ, D'Souza C et al (2008) Cytoplasmic PINK1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc Natl Acad Sci USA 105:1716-1721 (Pubitemid 351346580)
25. Hashimoto M, Bar-On P, Ho G (2004) Beta-synuclein regulates AKT activity in neuronal cells. A possible mechanism for neuroprotection in Parkinson's disease. J Biol Chem 279:23622-23629 (Pubitemid 38685677)
26. Hay N (2005) The AKT-mTOR tango and its relevance to cancer. Cancer Cell 8:179-183
27. Healy DG, bou-Sleiman PM, Casas JP et al (2006) UCHL-1 is not a Parkinson's disease susceptibility gene. Ann Neurol 59:627-633
28. Hirsch E, Costa C, Ciraolo E (2007) Phosphoinositide 3-kinases as a common platform for multi-hormone signaling. J Endocrinol 194:243-256 (Pubitemid 47249663)
29. Jana A, Hogan EL, Pahan K (2009) Ceramide and neurodegeneration: susceptibility of neurons and oligodendrocytes to cell damage and death. J Neurol Sci 278:5-15
30. Kihara T, Shimohama S, Sawada H et al (2002) Protective effect of dopamine D2 agonists in cortical neurons via the phosphatidylinositol 3 kinase cascade. J Neurosci Res 70:274-282 (Pubitemid 35222362)
31. Kim SJ, Winter K, Nian C, Tsuneoka M, Koda Y, McIntosh CH (2005) Glucose-dependent insulinotropic polypeptide (GIP) stimulation of pancreatic beta-cell survival is dependent upon phosphatidylinositol 3-kinase (PI3K)/protein kinase B (PKB) signaling, inactivation of the forkhead transcription factor Foxo1, and down-regulation of Bax expression. J Biol Chem 280:22297-22307 (Pubitemid 40827886)
32. Kitada T, Asakawa S, Hattori N et al (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392:605-608 (Pubitemid 28207717)
33. Maj MC, Tkachyova I, Patel P et al (2010) Oxidative stress alters the regulatory control of p66Shc and AKT in PINK1 deficient cells. Biochem Biophys Res Commun 399:331-335
34. Mills RD, Sim CH, Mok SS, Mulhern TD, Culvenor JG, Cheng HC (2008) Biochemical aspects of the neuroprotective mechanism of PTEN-induced kinase-1 (PINK1). J Neurochem 105:18-33 (Pubitemid 351441646)
35. Moriwaki Y, Kim YJ, Ido Y et al (2008) L347P PINK1 mutant that fails to bind to Hsp90/Cdc37 chaperones is rapidly degraded in a proteasome-dependent manner. Neurosci Res 61:43-48
36. Murata H, Sakaguchi M, Jin Y et al (2010) A new cytosolic pathway from a Parkinson's disease-associated kinase, BRPK/ PINK1: activation of AKT via MTORC2. J. Biol, Chem
37. Nakagomi S, Suzuki Y, Namikawa K, Kiryu-Seo S, Kiyama H (2003) Expression of the activating transcription factor 3 prevents c-Jun N-terminal kinase-induced neuronal death by promoting heat shock protein 27 expression and AKT activation. J Neurosci 23:5187-5196 (Pubitemid 36793247)
38. Petit A, Kawarai T, Paitel E et al (2005) Wild-type PINK1 prevents basal and induced neuronal apoptosis, a protective effect abrogated by Parkinson disease-related mutations. J Biol Chem 280:34025-34032
39. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
40. Plun-Favreau H, Klupsch K, Moisoi N et al (2007) The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat Cell Biol 9:1243-1252 (Pubitemid 350042356)
41. Pridgeon JW, Olzmann JA, Chin LS, Li L (2007) PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol 5:e172
42. Qi Y, Wang JK, McMillian M, Chikaraishi DM (1997) Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation 1106. J Neurosci 17:1217-1225 (Pubitemid 27073725)
43. Rogaeva E, Johnson J, Lang AE et al (2004) Analysis of the PINK1 gene in a large cohort of cases with Parkinson disease. Arch Neurol 61:1898-1904
44. Rolland SG, Conradt B (2010) New role of the BCL2 family of proteins in the regulation of mitochondrial dynamics. Curr Opin Cell Biol 22:852-858
45. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM (2005) Phosphorylation and regulation of AKT/PKB by the rictor-mTOR complex 3. Science 307:1098-1101 (Pubitemid 40262113)
46. Sato S, Fujita N, Tsuruo T (2000) Modulation of AKT kinase activity by binding to Hsp90. Proc Natl Acad Sci USA 97:10832-10837
47. Shan Y, Liu B, Li L et al (2009) Regulation of PINK1 by NR2Bcontaining NMDA receptors in ischemic neuronal injury. J Neurochem 111:1149-1160
48. Shimoke K, Chiba H (2001) 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 therapeutical application for Parkinson's disease. J Neurosci Res 63:402-409 (Pubitemid 32183789)
49. Silvestri L, Caputo V, Bellacchio E et al (2005) Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet 14:3477-3492 (Pubitemid 41672130)
50. Sim CH, Lio DS, Mok SS et al (2006) C-terminal truncation and Parkinson's disease-associated mutations down-regulate the protein serine/threonine kinase activity of PTEN-induced kinase-1. Hum Mol Genet 15:3251-3262 (Pubitemid 44605504)
51. Singleton AB, Farrer M, Johnson J et al (2003) Alpha-synuclein locus triplication causes Parkinson's disease. Science 302:841 (Pubitemid 37339619)
52. Siskind LJ, Mullen TD, Romero RKet al (2010) The BCL-2 protein BAK is required for long-chain ceramide generation during apoptosis. J Biol Chem 285:11818-11826
53. Valente EM, bou-Sleiman PM, Caputo Vet al (2004) Hereditary earlyonset Parkinson's disease caused by mutations in PINK1. Science 304:1158-1160
54. Vives-Bauza C, de Vries RL, TocilescuM, Przedborski S (2010) PINK1/ parkin direct mitochondria to autophagy. Autophagy 6:315-316
55. Wang HL, ChouAH, Yeh TH et al (2007) PINK1mutants associated with recessive Parkinson's disease are defective in inhibiting mitochondrial release of cytochrome c. Neurobiol Dis 28:216-226
56. Weihofen A, Ostaszewski B, Minami Y, Selkoe DJ (2008) PINK1 Parkinson mutations, the Cdc37/Hsp90 chaperones and Parkin all influence the maturation or subcellular distribution of PINK1. Hum Mol Genet 17:602-616 (Pubitemid 351201772)
57. Wirdefeldt K, Adami HO, Cole P, Trichopoulos D, Mandel J (2011) Epidemiology and etiology of Parkinson's disease: a review of the evidence. Eur J Epidemiol 26(Suppl 1):S1-58
58. Wood-Kaczmar A, Gandhi S, Yao Z, Abramov AYet al (2008) PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS One 3:e2455
59. Yamaguchi H, Wang HG (2001) The protein kinase PKB/AKT regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 20:7779-7786 (Pubitemid 33121951)
60. Zhou L, Chang DC (2008) Dynamics and structure of the Bax-Bak complex responsible for releasing mitochondrial proteins during apoptosis. J Cell Sci 121:2186-2196