Perturbation of transcription factor Nur77 expression mediated by Myocyte Enhancer Factor 2D (MEF2D) regulates dopaminergic neuron loss in response to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 14362-14371

  Mount, Matthew P ^a   Zhang, Yi ^a   Amini, Mandana ^a   Callaghan, Steve ^a   Kulczycki, Jerzy ^b   Mao, Zixu ^c   Slack, Ruth S ^a   Anisman, Hymie ^b   Park, David S ^a,d  

^a UNIVERSITY OF OTTAWA   (Canada)

^b CARLETON UNIVERSITY   (Canada)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

1-METHYL-4-PHENYLPYRIDINIUM; 3 ,4-DIHYDROXYPHENYLACETIC ACIDS; BASAL CONDITIONS; DOPAMINERGIC NEURONS; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTORS; NEURONAL SURVIVAL; TETRAHYDROPYRIDINE;

MAMMALS; TRANSCRIPTION FACTORS;

NEURONS;

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CALPAIN; CYCLIN DEPENDENT KINASE 5; DOPAMINE; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2D; NUCLEAR RECEPTOR NUR77; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; HYPERSENSITIVITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL DEGENERATION; NERVE CELL LESION; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SENSITIZATION; SIGNAL TRANSDUCTION;

CDK5; CELL DEATH; DOPAMINE; MEF2; MPTP; NEURODEGENERATION; NEUROTOXIN; NUR77; PARKINSON DISEASE;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; 3,4-DIHYDROXYPHENYLACETIC ACID; ANIMALS; BRAIN; CALPAIN; CELL DEATH; CYCLIN-DEPENDENT KINASE 5; DOPAMINERGIC NEURONS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; MYOGENIC REGULATORY FACTORS; NEUROTOXINS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; RNA, SMALL INTERFERING; SUBSTANTIA NIGRA;

EID: 84877887974     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.439216     Document Type: Article

References (65)

1. Przedborski, S., and Vila, M. (2001) The last decade in Parkinson's disease research. Basic sciences. Adv. Neurol. 86, 177-186
2. Kostic, V., Przedborski, S., Flaster, E., and Sternic, N. (1991) Early development of levodopa-induced dyskinesias and response fluctuations in young-onset Parkinson's disease. Neurology 41, 202-205
3. Pines, J. (1993) Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem. Sci. 18, 195-197
4. Tsai, L. H., Takahashi, T., Caviness, V. S., Jr., and Harlow, E. (1993) Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119, 1029-1040 (Pubitemid 23358574)
5. Tsai, L. H., Delalle, I., Caviness, V. S., Jr., Chae, T., and Harlow, E. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371, 419-423 (Pubitemid 24302556)
6. Smith, P. D., Crocker, S. J., Jackson-Lewis, V., Jordan-Sciutto, K. L., Hayley, S., Mount, M. P., O'Hare, M. J., Callaghan, S., Slack, R. S., Przedborski, S., Anisman, H., and Park, D. S. (2003) Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 100, 13650-13655 (Pubitemid 37444794)
7. Smith, P. D., Mount, M. P., Shree, R., Callaghan, S., Slack, R. S., Anisman, H., Vincent, I., Wang, X., Mao, Z., and Park, D. S. (2006) Calpain-regulated p35/cdk5 plays a central role in dopaminergic neuron death through modulation of the transcription factor myocyte enhancer factor 2. J. Neurosci. 26, 440-447 (Pubitemid 43237108)
8. Qu, D., Rashidian, J., Mount, M. P., Aleyasin, H., Parsanejad, M., Lira, A., Haque, E., Zhang, Y., Callaghan, S., Daigle, M., Rousseaux, M. W., Slack, R. S., Albert, P. R., Vincent, I., Woulfe, J. M., and Park, D. S. (2007) Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron 55, 37-52 (Pubitemid 46990825)
9. Huang, E., Qu, D., Zhang, Y., Venderova, K., Haque, M. E., Rousseaux, M. W., Slack, R. S., Woulfe, J. M., and Park, D. S. (2010) The role of Cdk5-mediated apurinic/apyrimidinic endonuclease 1 phosphorylation in neuronal death. Nat. Cell Biol. 12, 563-571
10. Ko, J., Humbert, S., Bronson, R. T., Takahashi, S., Kulkarni, A. B., Li, E., and Tsai, L. H. (2001) p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 21, 6758-6771 (Pubitemid 32781119)
11. McKinsey, T. A., Zhang, C. L., and Olson, E. N. (2001) Control of muscle development by dueling HATs and HDACs. Curr. Opin. Genet. Dev. 11, 497-504 (Pubitemid 32800722)
12. Heidenreich, K. A., and Linseman, D. A. (2004) Myocyte enhancer factor-2 transcription factors in neuronal differentiation and survival. Mol. Neurobiol. 29, 155-166
13. Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M., and Greenberg, M. E. (1999) Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286, 785-790
14. Wang, X., Tang, X., Li, M., Marshall, J., and Mao, Z. (2005) Regulation of neuroprotective activity of myocyte-enhancer factor 2 by cAMP-protein kinase A signaling pathway in neuronal survival. J. Biol. Chem. 280, 16705-16713 (Pubitemid 41389128)
15. She, H., Yang, Q., Shepherd, K., Smith, Y., Miller, G., Testa, C., and Mao, Z. (2011) Direct regulation of complex I by mitochondrial MEF2D is disrupted in a mouse model of Parkinson disease and in human patients. J. Clin. Invest. 121, 930-940
16. 2+-induced release of the transcription factor MEF2. Science 286, 790-793
17. Liu, W., Youn, H. D., and Liu, J. O. (2001) Thapsigargin-induced apoptosis involves Cabin1-MEF2-mediated induction of Nur77. Eur. J. Immunol. 31, 1757-1764 (Pubitemid 32547338)
18. Ananieva, O., Macdonald, A., Wang, X., McCoy, C. E., McIlrath, J., Tournier, C., and Arthur, J. S. (2008) ERK5 regulation in naïve T-cell activation and survival. Eur. J. Immunol. 38, 2534-2547
19. Woronicz, J. D., Lina, A., Calnan, B. J., Szychowski, S., Cheng, L., and Winoto, A. (1995) Regulation of the Nur77 orphan steroid receptor in activation-induced apoptosis. Mol. Cell. Biol. 15, 6364-6376
20. Fujii, Y., Matsuda, S., Takayama, G., and Koyasu, S. (2008) ERK5 is involved in TCR-induced apoptosis through the modification of Nur77. Genes Cells 13, 411-419 (Pubitemid 351567043)
21. Lee, S. L., Wesselschmidt, R. L., Linette, G. P., Kanagawa, O., Russell, J. H., and Milbrandt, J. (1995) Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nur77). Science 269, 532-535
22. Brás, A., Albar, J. P., Leonardo, E., de Buitrago, G. G., and Martínez-A, C. (2000) Ceramide-induced cell death is independent of the Fas/Fas ligand pathway and is prevented by Nur77 overexpression in A20 B cells. Cell Death Differ. 7, 262-271
23. Suzuki, S., Suzuki, N., Mirtsos, C., Horacek, T., Lye, E., Noh, S. K., Ho, A., Bouchard, D., Mak, T. W., and Yeh, W. C. (2003) Nur77 as a survival factor in tumor necrosis factor signaling. Proc. Natl. Acad. Sci. U.S.A. 100, 8276-8280 (Pubitemid 36842535)
24. Gilbert, F., Morissette, M., St-Hilaire, M., Paquet, B., Rouillard, C., Di Paolo, T., and Lévesque, D. (2006) Nur77 gene knockout alters dopamine neuron biochemical activity and dopamine turnover. Biol. Psychiatry 60, 538-547 (Pubitemid 44402380)
25. Lee, S. L., Tourtellotte, L. C., Wesselschmidt, R. L., and Milbrandt, J. (1995) Growth and differentiation proceeds normally in cells deficient in the immediate early gene NGFI-A. J. Biol. Chem. 270, 9971-9977
26. Mount, M. P., Lira, A., Grimes, D., Smith, P. D., Faucher, S., Slack, R., Anisman, H., Hayley, S., and Park, D. S. (2007) Involvement of interferongamma in microglial-mediated loss of dopaminergic neurons. J. Neurosci. 27, 3328-3337 (Pubitemid 46474138)
27. Crocker, S. J., Liston, P., Anisman, H., Lee, C. J., Smith, P. D., Earl, N., Thompson, C. S., Park, D. S., Korneluk, R. G., and Robertson, G. S. (2003) Attenuation of MPTP-induced neurotoxicity and behavioural impairment in NSE-XIAP transgenic mice. Neurobiol. Dis. 12, 150-161 (Pubitemid 36349406)
28. Gundersen, H. J., Bagger, P., Bendtsen, T. F., Evans, S. M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K., Nyengaard, J. R., and Pakkenberg, B. (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96, 857-881
29. Rymar, V. V., Sasseville, R., Luk, K. C., and Sadikot, A. F. (2004) Neurogenesis and stereological morphometry of calretinin-immunoreactive GABAergic interneurons of the neostriatum. J. Comp. Neurol. 469, 325-339 (Pubitemid 38140641)
30. Gong, X., Tang, X., Wiedmann, M., Wang, X., Peng, J., Zheng, D., Blair, L. A., Marshall, J., and Mao, Z. (2003) Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 38, 33-46 (Pubitemid 36423351)
31. Milbrandt, J. (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1, 183-188
32. Sedarous, M., Keramaris, E., O'Hare, M., Melloni, E., Slack, R. S., Elce, J. S., Greer, P. A., and Park, D. S. (2003) Calpains mediate p53 activation and neuronal death evoked by DNA damage. J. Biol. Chem. 278, 26031-26038 (Pubitemid 36835370)
33. O'Hare, M. J., Kushwaha, N., Zhang, Y., Aleyasin, H., Callaghan, S. M., Slack, R. S., Albert, P. R., Vincent, I., and Park, D. S. (2005) Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J. Neurosci. 25, 8954-8966 (Pubitemid 41384464)
34. Tsukahara, T., and Haniu, H. (2011) Nanoparticle-mediated intracellular lipid accumulation during C2C12 cell differentiation. Biochem. Biophys. Res. Commun. 406, 558-563
35. Cheung, N. S., Hickling, Y. M., and Beart, P. M. (1997) Development and survival of rat embryonic mesencephalic dopaminergic neurones in serum-free, antioxidant-rich primary cultures. Neurosci. Lett. 233, 13-16 (Pubitemid 27402541)
36. Zhang, Y., Qu, D., Morris, E. J., O'Hare, M. J., Callaghan, S. M., Slack, R. S., Geller, H. M., and Park, D. S. (2006) The Chk1/Cdc25A pathway as activators of the cell cycle in neuronal death induced by camptothecin. J. Neurosci. 26, 8819-8828 (Pubitemid 44319417)
37. Zhang, Y., Parsanejad, M., Huang, E., Qu, D., Aleyasin, H., Rousseaux, M. W., Gonzalez, Y. R., Cregan, S. P., Slack, R. S., and Park, D. S. (2010) Pim-1 kinase as activator of the cell cycle pathway in neuronal death induced by DNA damage. J. Neurochem. 112, 497-510
38. Hayley, S., Crocker, S. J., Smith, P. D., Shree, T., Jackson-Lewis, V., Przedborski, S., Mount, M., Slack, R., Anisman, H., and Park, D. S. (2004) Regulation of dopaminergic loss by Fas in a 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine model of Parkinson's disease. J. Neurosci. 24, 2045-2053 (Pubitemid 38292818)
39. Youn, H. D., and Liu, J. O. (2000) Cabin1 represses MEF2-dependent Nur77 expression and T cell apoptosis by controlling association of histone deacetylases and acetylases with MEF2. Immunity 13, 85-94
40. Dequiedt, F., Kasler, H., Fischle, W., Kiermer, V., Weinstein, M., Herndier, B. G., and Verdin, E. (2003) HDAC7, a thymus-specific class II histone deacetylase, regulates Nur77 transcription and TCR-mediated apoptosis. Immunity 18, 687-698 (Pubitemid 36588585)
41. Mahmoudi, S., Samadi, P., Gilbert, F., Ouattara, B., Morissette, M., Grégoire, L., Rouillard, C., Di Paolo, T., and Lévesque, D. (2009) Nur77mRNA levels and L-Dopa-induced dyskinesias in MPTP monkeys treated with docosahexaenoic acid. Neurobiol. Dis. 36, 213-222
42. Harbison, R. A., Ryan, K. R., Wilkins, H. M., Schroeder, E. K., Loucks, F. A., Bouchard, R. J., and Linseman, D. A. (2011) Calpain plays a central role in 1-methyl-4-phenylpyridinium (MPP+)-induced neurotoxicity in cerebellar granule neurons. Neurotox. Res. 19, 374-388
43. Sheline, C. T., Zhu, J., Zhang, W., Shi, C., and Cai, A. L. (2013) Mitochondrial inhibitor models of Huntington's disease and Parkinson's disease induce zinc accumulation and are attenuated by inhibition of zinc neurotoxicity in vitro or in vivo. Neurodegener. Dis. 11, 49-58
44. Meissner, W., Prunier, C., Guilloteau, D., Chalon, S., Gross, C. E., and Bezard, E. (2003) Time-course of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. Mol. Neurobiol. 28, 209-218 (Pubitemid 38156419)
45. Jackson-Lewis, V., and Przedborski, S. (2007) Protocol for the MPTP mouse model of Parkinson's disease. Nat Protoc 2, 141-151 (Pubitemid 47044700)
46. Dragunow, M., Butterworth, N., Waldvogel, H., Faull, R. L., and Nicholson, L. F. (1995) Prolonged expression of Fos-related antigens, Jun B and TrkB in dopamine-denervated striatal neurons. Brain Res. Mol. Brain Res. 30, 393-396
47. Verdaguer, E., Alvira, D., Jiménez, A., Rimbau, V., Camins, A., and Pallàs, M. (2005) Inhibition of the cdk5/MEF2 pathway is involved in the antiapoptotic properties of calpain inhibitors in cerebellar neurons. Br. J. Pharmacol. 145, 1103-1111 (Pubitemid 43079983)
48. He, Y. W. (2002) Orphan nuclear receptors in T lymphocyte development. J. Leukoc. Biol. 72, 440-446
49. Verdin, E., Dequiedt, F., and Kasler, H. (2004) HDAC7 regulates apoptosis in developing thymocytes. Novartis Found. Symp. 259, 115-129; discussion 129-31, 163-169
50. Tian, X., Kai, L., Hockberger, P. E., Wokosin, D. L., and Surmeier, D. J. (2010) MEF-2 regulates activity-dependent spine loss in striatopallidal medium spiny neurons. Mol. Cell. Neurosci. 44, 94-108
51. Lam, B. Y., Zhang, W., Ng, D. C., Maruthappu, M., Roderick, H. L., and Chawla, S. (2010) CREB-dependent Nur77 induction following depolarization in PC12 cells and neurons is modulated by MEF2 transcription factors. J. Neurochem. 112, 1065-1073
52. Chao, L. C., Bensinger, S. J., Villanueva, C. J., Wroblewski, K., and Tontonoz, P. (2008) Inhibition of adipocyte differentiation by Nur77, Nurr1, and Nor1. Mol. Endocrinol. 22, 2596-2608
53. Zhao, Y., and Bruemmer, D. (2010) NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler. Thromb. Vasc. Biol. 30, 1535-1541
54. de Léséleuc, L., and Denis, F. (2006) Inhibition of apoptosis by Nur77 through NF-κB activity modulation. Cell Death Differ. 13, 293-300 (Pubitemid 43102212)
55. Green, D. R., Droin, N., and Pinkoski, M. (2003) Activation-induced cell death in T cells. Immunol. Rev. 193, 70-81 (Pubitemid 36688041)
56. Cheng, Z., Völkers, M., Din, S., Avitabile, D., Khan, M., Gude, N., Mohsin, S., Bo, T., Truffa, S., Alvarez, R., Mason, M., Fischer, K. M., Konstandin, M. H., Zhang, X. K., Heller Brown, J., and Sussman, M. A. (2011) Mitochondrial translocation of Nur77 mediates cardiomyocyte apoptosis. Eur. Heart J. 32, 2179-2188
57. Cho, S. D., Yoon, K., Chintharlapalli, S., Abdelrahim, M., Lei, P., Hamilton, S., Khan, S., Ramaiah, S. K., and Safe, S. (2007) Nur77 agonists induce proapoptotic genes and responses in colon cancer cells through nuclear receptor-dependent and nuclear receptor-independent pathways. Cancer Res. 67, 674-683 (Pubitemid 46192207)
58. Lin, B., Kolluri, S. K., Lin, F., Liu, W., Han, Y. H., Cao, X., Dawson, M. I., Reed, J. C., and Zhang, X. K. (2004) Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116, 527-540 (Pubitemid 38264430)
59. Thompson, J., and Winoto, A. (2008) During negative selection, Nur77 family proteins translocate to mitochondria where they associate with Bcl-2 and expose its proapoptotic BH3 domain. J. Exp. Med. 205, 1029-1036 (Pubitemid 351679679)
60. Lévesque, D., and Rouillard, C. (2007) Nur77 and retinoid X receptors: crucial factors in dopamine-related neuroadaptation. Trends Neurosci. 30, 22-30 (Pubitemid 46001681)
61. St-Hilaire, M., Bourhis, E., Lévesque, D., and Rouillard, C. (2006) Impaired behavioural and molecular adaptations to dopamine denervation and repeated L-DOPA treatment in Nur77-knockout mice. Eur. J. Neurosci. 24, 795-805
62. Chao, L. C., Zhang, Z., Pei, L., Saito, T., Tontonoz, P., and Pilch, P. F. (2007) Nur77 coordinately regulates expression of genes linked to glucose metabolism in skeletal muscle. Mol. Endocrinol. 21, 2152-2163 (Pubitemid 47347379)
63. Kim, M. K., Kim, S. C., Kang, J. I., Hyun, J. H., Boo, H. J., Eun, S. Y., Park, D. B., Yoo, E. S., Kang, H. K., and Kang, J. H. (2011) 6-Hydroxydopamine-induced PC12 cell death is mediated by MEF2D down-regulation. Neurochem. Res. 36, 223-231
64. Wang, X., She, H., and Mao, Z. (2009) Phosphorylation of neuronal survival factor MEF2D by glycogen synthase kinase 3β in neuronal apoptosis. J. Biol. Chem. 284, 32619-32626
65. Paxinos, G., and Franklin, K. B. J. (2001) The Mouse Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA