Translocation and oligomerization of Bax is regulated independently by activation of p38 MAPK and caspase-2 during MN9D dopaminergic neurodegeneration

Apoptosis

Volumn 16, Issue 11, 2011, Pages 1087-1100

  Oh, Chang Ki ^a   Han, Baek Soo ^b   Choi, Won Seok ^a   Youdim, Moussa B H ^c   Oh, Young J ^a  

^a Yonsei University   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

6 Hydroxydopamine; Bax oligomerization; Caspase 2; P38 MAPK

Indexed keywords

CASPASE 2; CYTOCHROME C; MITOGEN ACTIVATED PROTEIN KINASE P38; OXIDOPAMINE; PROTEIN BAX; SHORT HAIRPIN RNA;

ARTICLE; CONTROLLED STUDY; CYTOSOL; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NERVE DEGENERATION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 2; CELL LINE; CYTOCHROMES C; DOPAMINERGIC NEURONS; ENZYME ACTIVATION; ENZYME INHIBITORS; IMIDAZOLES; MICE; MITOCHONDRIA; OXIDOPAMINE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PARKINSON DISEASE; PHOSPHORYLATION; POLYMERIZATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 82955212814     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-011-0627-8     Document Type: Article

References (70)

1. Dawson TM, Dawson VL (2003) Molecular pathways of neuro-degeneration in Parkinson's disease. Science 302(5646):819-822 (Pubitemid 37339614)
2. Hartmann A, Hunot S, Michel PP, Muriel MP, Vyas S, Faucheux BA, Mouatt-Prigent A, Turmel H, Srinivasan A, Ruberg M, Evan GI, Agid Y, Hirsch EC (2000) Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci USA 97(6):2875-2880 (Pubitemid 30159265)
3. Anglade P, Vyas S, Javoy-Agid F, Herrero MT, Michel PP, Marquez J, Mouatt-Prigent A, Ruberg M, Hirsch EC, Agid Y (1997) Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol Histopathol 12(1):25-31 (Pubitemid 27106916)
4. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ (2007) Potential therapeutic applications of autophagy. Nat Rev Drug Discov 6(4):304-312 (Pubitemid 46505881)
5. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39(6):889-909 (Pubitemid 37130207)
6. Vila M, Przedborski S (2004) Genetic clues to the pathogenesis of Parkinson's disease. Nat Med 10(Suppl):S58-S62 (Pubitemid 38901868)
7. Javoy F, Sotelo C, Herbet A, Agid Y (1976) Specificity of dopaminergic neuronal degeneration induced by intracerebral injection of 6-hydroxydopamine in the nigrostriatal dopamine system. Brain Res 102(2):201-215
8. Irwin I, DeLanney LE, Langston JW (1993) MPTP and aging. Studies in the C57BL/6 mouse. Adv Neurol 60:197-206
9. Bove J, Prou D, Perier C, Przedborski S (2005) Toxin-induced models of Parkinson's disease. NeuroRx 2(3):484-494 (Pubitemid 41444882)
10. Han BS, Hong HS, Choi WS, Markelonis GJ, Oh TH, Oh YJ (2003) Caspase-dependent and -independent cell death pathways in primary cultures of mesencephalic dopaminergic neurons after neurotoxin treatment. J Neurosci 23(12):5069-5078 (Pubitemid 36793234)
11. Han BS, Noh JS, Gwag BJ, Oh YJ (2003) A distinct death mechanism is induced by 1-methyl-4-phenylpyridinium or by 6-hydroxydopamine in cultured rat cortical neurons: degradation and dephosphorylation of tau. Neurosci Lett 341(2):99-102 (Pubitemid 36398479)
12. Choi WS, Lee E, Lim J, Oh YJ (2008) Calbindin-D28K prevents drug-induced dopaminergic neuronal death by inhibiting caspase and calpain activity. Biochem Biophys Res Commun 371(1):127-131
13. Lim J, Kim HW, Youdim MB, Rhyu IJ, Choe KM, Oh YJ (2010) Binding preference of p62 towards LC3-ll during dopaminergic neurotoxin-induced impairment of autophagic flux. Autophagy 7(1):51-60
14. Choi WS, Eom DS, Han BS, Kim WK, Han BH, Choi EJ, Oh TH, Markelonis GJ, Cho JW, Oh YJ (2004) Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8- and -9-mediated apoptotic pathways in dopaminergic neurons. J Biol Chem 279(19):20451-20460 (Pubitemid 38623492)
15. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275(5303):1129-1132 (Pubitemid 27097312)
16. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275(5303):1132-1136 (Pubitemid 27097313)
17. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281(5381):1312-1316 (Pubitemid 28406817)
18. 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(1):147-157 (Pubitemid 26256586)
19. Chipuk JE, Green DR (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 18(4):157-164
20. Suen DF, Norris KL, Youle RJ (2008) Mitochondrial dynamics and apoptosis. Genes Dev 22(12):1577-1590 (Pubitemid 351846838)
21. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17(3):393-403 (Pubitemid 40193310)
22. Chipuk JE, Fisher JC, Dillon CP, Kriwacki RW, Kuwana T, Green DR (2008) Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad Sci USA 105(51):20327-20332
23. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR, Newmeyer DD (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17(4):525-535 (Pubitemid 40269117)
24. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2(3):183-192 (Pubitemid 41043974)
25. Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodi-merizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74(4):609-619 (Pubitemid 23259742)
26. 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(15): 11615-11623
27. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14(16):2060-2071 (Pubitemid 30637355)
28. Suzuki M, Youle RJ, Tjandra N (2000) Structure of Bax: core-gulation of dimer formation and intracellular localization. Cell 103(4):645-654
29. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139(5):1281-1292 (Pubitemid 27523214)
30. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111(3):331-342 (Pubitemid 35341388)
31. Kim H, Tu HC, Ren D, Takeuchi O, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH (2009) Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 36(3):487-499
32. Choi HK, Won LA, Kontur PJ, Hammond DN, Fox AP, Wainer BH, Hoffmann PC, Heller A (1991) Immortalization of embryonic mesencephalic dopaminergic neurons by somatic cell fusion. Brain Res 552(1):67-76
33. Oh YJ, Wong SC, Moffat M, O'Malley KL (1995) Overexpres-sion of Bcl-2 attenuates MPP+, but not 6-ODHA, induced cell death in a dopaminergic neuronal cell line. Neurobiol Dis 2(3):157-167
34. Choi WS, Lee EH, Chung CW, Jung YK, Jin BK, Kim SU, Oh TH, Saido TC, Oh YJ (2001) Cleavage of Bax is mediated by caspase-dependent or -independent calpain activation in dopa-minergic neuronal cells: protective role of Bcl-2. J Neurochem 77(6):1531-1541 (Pubitemid 32574488)
35. Canet-Aviles RM, Wilson MA, Miller DW, Ahmad R, McLendon C, Bandyopadhyay S, Baptista MJ, Ringe D, Petsko GA, Cookson MR (2004) The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci USA 101(24):9103-9108 (Pubitemid 38781618)
36. Linseman DA, Butts BD, Precht TA, Phelps RA, Le SS, Laessig TA, Bouchard RJ, Florez-McClure ML, Heidenreich KA (2004) Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci 24(44):9993-10002 (Pubitemid 39463581)
37. Sundararajan R, Cuconati A, Nelson D, White E (2001) Tumor necrosis factor-alpha induces Bax-Bak interaction and apoptosis, which is inhibited by adenovirus E1B 19K. J Biol Chem 276(48):45120-45127
38. Makin GW, Corfe BM, Griffiths GJ, Thistlethwaite A, Hickman JA, Dive C (2001) Damage-induced Bax N-terminal change, translocation to mitochondria and formation of Bax dimers/com-plexes occur regardless of cell fate. EMBO J 20(22):6306-6315 (Pubitemid 33078704)
39. George NM, Evans JJ, Luo X (2007) A three-helix homo-oligo-merization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax. Genes Dev 21(15):1937-1948 (Pubitemid 47204932)
40. Van Laethem A, Van Kelst S, Lippens S, Declercq W, Vandenabeele P, Janssens S, Vandenheede JR, Garmyn M, Agostinis P (2004) Activation of p38 MAPK is required for Bax translocation to mitochondria, cytochrome c release and apop-tosis induced by UVB irradiation in human keratinocytes. FASEB J 18(15):1946-1948 (Pubitemid 39602293)
41. Yuan ZQ, Feldman RI, Sussman GE, Coppola D, Nicosia SV, Cheng JQ (2003) AKT2 inhibition of cisplatin-induced JNK/p38 and Bax activation by phosphorylation of ASK1: implication of AKT2 in chemoresistance. J Biol Chem 278(26):23432-23440 (Pubitemid 36830160)
42. Deacon K, Mistry P, Chernoff J, Blank JL, Patel R (2003) p38 Mitogen-activated protein kinase mediates cell death and p21-activated kinase mediates cell survival during chemotherapeutic drug-induced mitotic arrest. Mol Biol Cell 14(5):2071-2087 (Pubitemid 36583554)
43. Kim BJ, Ryu SW, Song BJ (2006) JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 281(30):21256-21265
44. Owens TW, Valentijn AJ, Upton JP, Keeble J, Zhang L, Lindsay J, Zouq NK, Gilmore AP (2009) Apoptosis commitment and activation of mitochondrial Bax during anoikis is regulated by p38 MAPK. Cell Death Differ 16(11):1551-1562
45. Bonzon C, Bouchier-Hayes L, Pagliari LJ, Green DR, Newmeyer DD (2006) Caspase-2-induced apoptosis requires bid cleavage: a physiological role for bid in heat shock-induced death. Mol Biol Cell 17(5):2150-2157 (Pubitemid 44011731)
46. Wagner KW, Engels IH, Deveraux QL (2004) Caspase-2 can function upstream of bid cleavage in the TRAIL apoptosis pathway. J Biol Chem 279(33):35047-35052 (Pubitemid 39318141)
47. Yi X, Yin XM, Dong Z (2003) Inhibition of Bid-induced apop-tosis by Bcl-2. tBid insertion, Bax translocation, and Bax/Bak oligomerization suppressed. J Biol Chem 278(19):16992-16999 (Pubitemid 36799574)
48. Eskes R, Desagher S, Antonsson B, Martinou JC (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20(3):929-935 (Pubitemid 30044230)
49. Roucou X, Montessuit S, Antonsson B, Martinou JC (2002) Bax oligomerization in mitochondrial membranes requires tBid (cas-pase-8-cleaved Bid) and a mitochondrial protein. Biochem J 368(Pt 3):915-921 (Pubitemid 36042694)
50. Grinberg M, Sarig R, Zaltsman Y, Frumkin D, Grammatikakis N, Reuveny E, Gross A (2002) tBID Homooligomerizes in the mitochondrial membrane to induce apoptosis. J Biol Chem 277(14):12237-12245 (Pubitemid 34952791)
51. Kim EK, Choi EJ (2010) Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 1802(4): 396-405
52. Cookson MR, van der Brug M (2008) Cell systems and the toxic mechanism(s) of alpha-synuclein. Exp Neurol 209(1):5-11
53. Levy OA, Malagelada C, Greene LA (2009) Cell death pathways in Parkinson's disease: proximal triggers, distal effectors, and final steps. Apoptosis 14(4):478-500
54. Klegeris A, Pelech S, Giasson BI, Maguire J, Zhang H, McGeer EG, McGeer PL (2008) Alpha-synuclein activates stress signaling protein kinases in THP-1 cells and microglia. Neurobiol Aging 29(5):739-752 (Pubitemid 351400820)
55. Karunakaran S, Saeed U, Mishra M, Valli RK, Joshi SD, Meka DP, Seth P, Ravindranath V (2008) Selective activation of p38 mitogen-activated protein kinase in dopaminergic neurons of substantia nigra leads to nuclear translocation of p53 in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated mice. J Neurosci 28(47):12500-12509
56. Karunakaran S, Ravindranath V (2009) Activation of p38 MAPK in the substantia nigra leads to nuclear translocation of NF-kappaB in MPTP-treated mice: implication in Parkinson's disease. J Neurochem 109(6):1791-1799
57. Choi WS, Yoon SY, Oh TH, Choi EJ, O'Malley KL, Oh YJ (1999) Two distinct mechanisms are involved in 6-hydroxydop-amine- and MPP+-induced dopaminergic neuronal cell death: role of caspases, ROS, and JNK. J Neurosci Res 57(1):86-94 (Pubitemid 29293582)
58. Bode AM, Dong Z (2007) The functional contrariety of JNK. Mol Carcinog 46(8):591-598 (Pubitemid 47255173)
59. Kumar S, Kinoshita M, Noda M, Copeland NG, Jenkins NA (1994) Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1 beta-converting enzyme. Genes Dev 8(14):1613-1626 (Pubitemid 24236241)
60. Wang L, Miura M, Bergeron L, Zhu H, Yuan J (1994) Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78(5):739-750
61. Harvey NL, Butt AJ, Kumar S (1997) Functional activation of Nedd2/ICH-1 (caspase-2) is an early process in apoptosis. J Biol Chem 272(20):13134-13139 (Pubitemid 27216737)
62. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144(2):281-292 (Pubitemid 29066031)
63. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES (2002) Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 277(16): 13430-13437 (Pubitemid 34967937)
64. Robertson JD, Enoksson M, Suomela M, Zhivotovsky B, Orrenius S (2002) Caspase-2 acts upstream of mitochondria to promote cytochrome c release during etoposide-induced apopto-sis. J Biol Chem 277(33):29803-29809
65. Lassus P, Opitz-Araya X, Lazebnik Y (2002) Requirement for caspase-2 in stress-induced apoptosis before mitochondrial per-meabilization. Science 297(5585):1352-1354 (Pubitemid 34913174)
66. He Q, Huang Y, Sheikh MS (2004) Bax deficiency affects cas-pase-2 activation during ultraviolet radiation-induced apoptosis. Oncogene 23(6):1321-1325 (Pubitemid 38297188)
67. Lin CF, Chen CL, Chang WT, Jan MS, Hsu LJ, Wu RH, Tang MJ, Chang WC, Lin YS (2004) Sequential caspase-2 and cas-pase-8 activation upstream of mitochondria during ceramideand etoposide-induced apoptosis. J Biol Chem 279(39):40755-40761
68. Tinel A, Tschopp J (2004) The PIDDosome, a protein complex implicated in activation of caspase-2 in response to genotoxic stress. Science 304(5672):843-846 (Pubitemid 38620177)
69. Baptiste-Okoh N, Barsotti AM, Prives C (2008) A role for cas-pase 2 and PIDD in the process of p53-mediated apoptosis. Proc Natl Acad Sci USA 105(6):1937-1942 (Pubitemid 351439443)
70. Oh JH, Choi WS, Kim JE, Seo JW, O'Malley KL, Oh YJ (1998) Overexpression of HA-Bax but not Bcl-2 or Bcl-XL attenuates 6-hydroxydopamine-induced neuronal apoptosis. Exp Neurol 154(1):193-198 (Pubitemid 28553579)