Dissociation of progressive dopaminergic neuronal death and behavioral impairments by bax deletion in a mouse model of parkinson's diseases

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Kim, Tae Woo ^a   Moon, Younghye ^a,b   Kim, Kyungjin ^b   Lee, Jeong Eun ^c   Koh, Hyun Chul ^c   Rhyu, Im Joo ^a   Kim, Hyun ^a   Sun, Woong ^a  

^a Korea University College of Medicine   (South Korea)

^b Seoul National University   (South Korea)

^c Hanyang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; CYTOCHROME C; OXIDOPAMINE; PROTEIN BAX; PROTEIN C JUN; BAX PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATROPHY; AUTOPHAGY; BEHAVIOR DISORDER; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; DENTATE GYRUS; DISEASE COURSE; DISSOCIATION; DOPAMINERGIC NERVE CELL; GENE DELETION; HISTOPATHOLOGY; IMMUNOREACTIVITY; INNERVATION; MALE; MITOCHONDRION; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PARKINSON DISEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STEREOLOGY; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM; ANIMAL; APOPTOSIS; DISEASE MODEL; GENETICS; MENTAL DISEASE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALIA; MUS;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; ATROPHY; BCL-2-ASSOCIATED X PROTEIN; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; MENTAL DISORDERS; MICE; MICE, KNOCKOUT; OXIDOPAMINE; PARKINSON DISEASE; SUBSTANTIA NIGRA;

EID: 80054733292     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025346     Document Type: Article

References (76)

1. Hirsch E, Graybiel AM, Agid YA, (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334: 345-348.
2. Sauer H, Oertel WH, (1994) Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 59: 401-415.
3. Blum D, Torch S, Lambeng N, Nissou M, Benabid AL, et al. (2001) Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog Neurobiol 65: 135-172.
4. Przedborski S, (2005) Pathogenesis of nigral cell death in Parkinson's disease. Parkinsonism Relat Disord 11 (Suppl 1): S3-7.
5. Putcha GV, Deshmukh M, Johnson EM Jr, (1999) BAX translocation is a critical event in neuronal apoptosis: regulation by neuroprotectants, BCL-2, and caspases. J Neurosci 19: 7476-7485.
6. Roucou X, Martinou JC, (2001) Conformational change of Bax: a question of life or death. Cell Death Differ 8: 875-877.
7. Spooren WP, Gentsch C, Wiessner C, (1998) TUNEL-positive cells in the substantia nigra of C57BL/6 mice after a single bolus of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 85: 649-651; discussion 653.
8. Yang L, Matthews RT, Schulz JB, Klockgether T, Liao AW, et al. (1998) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyride neurotoxicity is attenuated in mice overexpressing Bcl-2. J Neurosci 18: 8145-8152.
9. Turmel H, Hartmann A, Parain K, Douhou A, Srinivasan A, et al. (2001) Caspase-3 activation in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. Mov Disord 16: 185-189.
10. Novikova L, Garris BL, Garris DR, Lau YS, (2006) Early signs of neuronal apoptosis in the substantia nigra pars compacta of the progressive neurodegenerative mouse 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine/probenecid model of Parkinson's disease. Neuroscience 140: 67-76.
11. Offen D, Beart PM, Cheung NS, Pascoe CJ, Hochman A, et al. (1998) Transgenic mice expressing human Bcl-2 in their neurons are resistant to 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine neurotoxicity. Proc Natl Acad Sci U S A 95: 5789-5794.
12. Vila M, Jackson-Lewis V, Vukosavic S, Djaldetti R, Liberatore G, et al. (2001) Bax ablation prevents dopaminergic neurodegeneration in the 1-methyl- 4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease. Proc Natl Acad Sci U S A 98: 2837-2842.
13. Wang H, Shimoji M, Yu SW, Dawson TM, Dawson VL, (2003) Apoptosis inducing factor and PARP-mediated injury in the MPTP mouse model of Parkinson's disease. Ann N Y Acad Sci 991: 132-139.
14. Chu CT, Zhu JH, Cao G, Signore A, Wang S, et al. (2005) Apoptosis inducing factor mediates caspase-independent 1-methyl-4-phenylpyridinium toxicity in dopaminergic cells. J Neurochem 94: 1685-1695.
15. Chu CT, Zhu J, Dagda R, (2007) Beclin 1-independent pathway of damage-induced mitophagy and autophagic stress: implications for neurodegeneration and cell death. Autophagy 3: 663-666.
16. Han BS, Hong HS, Choi WS, Markelonis GJ, Oh TH, et al. (2003) Caspase-dependent and-independent cell death pathways in primary cultures of mesencephalic dopaminergic neurons after neurotoxin treatment. J Neurosci 23: 5069-5078.
17. Shimohama S, Sawada H, Kitamura Y, Taniguchi T, (2003) Disease model: Parkinson's disease. Trends Mol Med 9: 360-365.
18. Ichitani Y, Okamura H, Nakahara D, Nagatsu I, Ibata Y, (1994) Biochemical and immunocytochemical changes induced by intrastriatal 6-hydroxydopamine injection in the rat nigrostriatal dopamine neuron system: evidence for cell death in the substantia nigra. Exp Neurol 130: 269-278.
19. Kramer BC, Mytilineou C, (2004) Alterations in the cellular distribution of bcl-2, bcl-x and bax in the adult rat substantia nigra following striatal 6-hydroxydopamine lesions. J Neurocytol 33: 213-223.
20. Cutillas B, Espejo M, Gil J, Ferrer I, Ambrosio S, (1999) Caspase inhibition protects nigral neurons against 6-OHDA-induced retrograde degeneration. Neuroreport 10: 2605-2608.
21. Marti MJ, Saura J, Burke RE, Jackson-Lewis V, Jimenez A, et al. (2002) Striatal 6-hydroxydopamine induces apoptosis of nigral neurons in the adult rat. Brain Res 958: 185-191.
22. Oiwa Y, Sanchez-Pernaute R, Harvey-White J, Bankiewicz KS, (2003) Progressive and extensive dopaminergic degeneration induced by convection-enhanced delivery of 6-hydroxydopamine into the rat striatum: a novel rodent model of Parkinson disease. J Neurosurg 98: 136-144.
23. Mladenovic A, Perovic M, Raicevic N, Kanazir S, Rakic L, et al. (2004) 6-Hydroxydopamine increases the level of TNFalpha and bax mRNA in the striatum and induces apoptosis of dopaminergic neurons in hemiparkinsonian rats. Brain Res 996: 237-245.
24. Crocker SJ, Wigle N, Liston P, Thompson CS, Lee CJ, et al. (2001) NAIP protects the nigrostriatal dopamine pathway in an intrastriatal 6-OHDA rat model of Parkinson's disease. Eur J Neurosci 14: 391-400.
25. Ebert AD, Hann HJ, Bohn MC, (2008) Progressive degeneration of dopamine neurons in 6-hydroxydopamine rat model of Parkinson's disease does not involve activation of caspase-9 and caspase-3. J Neurosci Res 86: 317-325.
26. de Torres C, Munell F, Ferrer I, Reventos J, Macaya A, (1997) Identification of necrotic cell death by the TUNEL assay in the hypoxic-ischemic neonatal rat brain. Neurosci Lett 230: 1-4.
27. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, et al. (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-1228.
28. Moubarak RS, Yuste VJ, Artus C, Bouharrour A, Greer PA, et al. (2007) Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cell Biol 27: 4844-4862.
29. Sun W, Gould TW, Newbern J, Milligan C, Choi SY, et al. (2005) Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J Neurosci 25: 5595-5603.
30. Park OH, Lee KJ, Rhyu IJ, Geum D, Kim H, et al. (2007) Bax-dependent and-independent death of motoneurons after facial nerve injury in adult mice. Eur J Neurosci 26: 1421-1432.
31. Lim J, Kim HW, Youdim MB, Rhyu IJ, Choe KM, et al. (2011) Binding preference of p62 towards LC3-ll during dopaminergic neurotoxin-induced impairment of autophagic flux. Autophagy 7: 51-60.
32. Iancu R, Mohapel P, Brundin P, Paul G, (2005) Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson's disease in mice. Behav Brain Res 162: 1-10.
33. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST, (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39: 777-787.
34. Vaudano E, Rosenblad C, Bjorklund A, (2001) Injury induced c-Jun expression and phosphorylation in the dopaminergic nigral neurons of the rat: correlation with neuronal death and modulation by glial-cell-line-derived neurotrophic factor. Eur J Neurosci 13: 1-14.
35. Jung AR, Kim TW, Rhyu IJ, Kim H, Lee YD, et al. (2008) Misplacement of Purkinje cells during postnatal development in Bax knock-out mice: a novel role for programmed cell death in the nervous system? J Neurosci 28: 2941-2948.
36. Sun W, Gould TW, Vinsant S, Prevette D, Oppenheim RW, (2003) Neuromuscular development after the prevention of naturally occurring neuronal death by Bax deletion. J Neurosci 23: 7298-7310.
37. Sun W, Oppenheim RW, (2003) Response of motoneurons to neonatal sciatic nerve axotomy in Bax-knockout mice. Mol Cell Neurosci 24: 875-886.
38. Gould TW, Buss RR, Vinsant S, Prevette D, Sun W, et al. (2006) Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J Neurosci 26: 8774-8786.
39. Buss RR, Gould TW, Ma J, Vinsant S, Prevette D, et al. (2006) Neuromuscular development in the absence of programmed cell death: phenotypic alteration of motoneurons and muscle. J Neurosci 26: 13413-13427.
40. Hartmann A, Hunot S, Michel PP, Muriel MP, Vyas S, et al. (2000) Caspase-3: A vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci U S A 97: 2875-2880.
41. Xia XG, Harding T, Weller M, Bieneman A, Uney JB, et al. (2001) Gene transfer of the JNK interacting protein-1 protects dopaminergic neurons in the MPTP model of Parkinson's disease. Proc Natl Acad Sci U S A 98: 10433-10438.
42. Eberhardt O, Coelln RV, Kugler S, Lindenau J, Rathke-Hartlieb S, et al. (2000) Protection by synergistic effects of adenovirus-mediated X-chromosome-linked inhibitor of apoptosis and glial cell line-derived neurotrophic factor gene transfer in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J Neurosci 20: 9126-9134.
43. Mogi M, Togari A, Kondo T, Mizuno Y, Komure O, et al. (2000) Caspase activities and tumor necrosis factor receptor R1 (p55) level are elevated in the substantia nigra from parkinsonian brain. J Neural Transm 107: 335-341.
44. Tatton NA, (2000) Increased caspase 3 and Bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp Neurol 166: 29-43.
45. Chen G, Bower KA, Ma C, Fang S, Thiele CJ, et al. (2004) Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J 18: 1162-1164.
46. Ding YM, Jaumotte JD, Signore AP, Zigmond MJ, (2004) Effects of 6-hydroxydopamine on primary cultures of substantia nigra: specific damage to dopamine neurons and the impact of glial cell line-derived neurotrophic factor. J Neurochem 89: 776-787.
47. Hanrott K, Gudmunsen L, O'Neill MJ, Wonnacott S, (2006) 6-hydroxydopamine-induced apoptosis is mediated via extracellular auto-oxidation and caspase 3-dependent activation of protein kinase Cdelta. J Biol Chem 281: 5373-5382.
48. Boujrad H, Gubkina O, Robert N, Krantic S, Susin SA, (2007) AIF-mediated programmed necrosis: a highly regulated way to die. Cell Cycle 6: 2612-2619.
49. Wang Y, Kim NS, Li X, Greer PA, Koehler RC, et al. (2009) Calpain activation is not required for AIF translocation in PARP-1-dependent cell death (parthanatos). J Neurochem 110: 687-696.
50. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441-446.
51. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, et al. (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 14: 729-739.
52. Chipuk JE, Green DR, (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 18: 157-164.
53. Bidere N, Lorenzo HK, Carmona S, Laforge M, Harper F, et al. (2003) Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem 278: 31401-31411.
54. Cregan SP, Fortin A, MacLaurin JG, Callaghan SM, Cecconi F, et al. (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 158: 507-517.
55. Cheung EC, Melanson-Drapeau L, Cregan SP, Vanderluit JL, Ferguson KL, et al. (2005) Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. J Neurosci 25: 1324-1334.
56. Burguillos MA, Hajji N, Englund E, Persson A, Cenci AM, et al. (2011) Apoptosis-inducing factor mediates dopaminergic cell death in response to LPS-induced inflammatory stimulus: evidence in Parkinson's disease patients. Neurobiol Dis 41: 177-188.
57. Zhang X, Chen J, Graham SH, Du L, Kochanek PM, et al. (2002) Intranuclear localization of apoptosis-inducing factor (AIF) and large scale DNA fragmentation after traumatic brain injury in rats and in neuronal cultures exposed to peroxynitrite. J Neurochem 82: 181-191.
58. Fonfria E, Dare E, Benelli M, Sunol C, Ceccatelli S, (2002) Translocation of apoptosis-inducing factor in cerebellar granule cells exposed to neurotoxic agents inducing oxidative stress. Eur J Neurosci 16: 2013-2016.
59. Zhu C, Qiu L, Wang X, Hallin U, Cande C, et al. (2003) Involvement of apoptosis-inducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain. J Neurochem 86: 306-317.
60. Reix S, Mechawar N, Susin SA, Quirion R, Krantic S, (2007) Expression of cortical and hippocampal apoptosis-inducing factor (AIF) in aging and Alzheimer's disease. Neurobiol Aging 28: 351-356.
61. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, et al. (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263.
62. Yu SW, Wang H, Dawson TM, Dawson VL, (2003) Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol Dis 14: 303-317.
63. Wang H, Yu SW, Koh DW, Lew J, Coombs C, et al. (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 24: 10963-10973.
64. Polster BM, Basanez G, Etxebarria A, Hardwick JM, Nicholls DG, (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280: 6447-6454.
65. Cao G, Xing J, Xiao X, Liou AK, Gao Y, et al. (2007) Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J Neurosci 27: 9278-9293.
66. Yu SW, Wang Y, Frydenlund DS, Ottersen OP, Dawson VL, et al. (2009) Outer mitochondrial membrane localization of apoptosis-inducing factor: mechanistic implications for release. ASN Neuro 1.
67. Joshi A, Bondada V, Geddes JW, (2009) Mitochondrial micro-calpain is not involved in the processing of apoptosis-inducing factor. Exp Neurol 218: 221-227.
68. Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, et al. (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1: 223-232.
69. Pope S, Land JM, Heales SJ, (2008) Oxidative stress and mitochondrial dysfunction in neurodegeneration; cardiolipin a critical target? Biochim Biophys Acta 1777: 794-799.
70. Gonzalvez F, Gottlieb E, (2007) Cardiolipin: setting the beat of apoptosis. Apoptosis 12: 877-885.
71. Wright KM, Linhoff MW, Potts PR, Deshmukh M, (2004) Decreased apoptosome activity with neuronal differentiation sets the threshold for strict IAP regulation of apoptosis. J Cell Biol 167: 303-313.
72. Kirik D, Rosenblad C, Bjorklund A, Mandel RJ, (2000) Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson's model: intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system. J Neurosci 20: 4686-4700.
73. Zheng JS, Tang LL, Zheng SS, Zhan RY, Zhou YQ, et al. (2005) Delayed gene therapy of glial cell line-derived neurotrophic factor is efficacious in a rat model of Parkinson's disease. Brain Res Mol Brain Res 134: 155-161.
74. Kim WR, Kim Y, Eun B, Park OH, Kim H, et al. (2007) Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J Neurosci 27: 14392-14403.
75. Mori A, Ohashi S, Nakai M, Moriizumi T, Mitsumoto Y, (2005) Neural mechanisms underlying motor dysfunction as detected by the tail suspension test in MPTP-treated C57BL/6 mice. Neurosci Res 51: 265-274.
76. Gage FH, Batchelor P, Chen KS, Chin D, Higgins GA, et al. (1989) NGF receptor reexpression and NGF-mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron 2: 1177-1184.