Dopaminergic neuron-specific deletion of p53 gene is neuroprotective in an experimental Parkinson's disease model

Journal of Neurochemistry

Volumn , Issue , 2016, Pages 746-757

  Qi, Xin ^a   Davis, Brandon ^b   Chiang, Yung Hsiao ^c   Filichia, Emily ^b   Barnett, Austin ^b   Greig, Nigel H ^d   Hoffer, Barry ^b   Luo, Yu ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

apopotosis; cell specific knockout; MPTP; p53; parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; MESSENGER RNA; PROTEIN BAD; PROTEIN BAX; PUMA PROTEIN;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTOSIS; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; EMBRYO; GENE DELETION; MALE; MOUSE; NERVE CELL NECROSIS; NERVE ENDING; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; TUMOR SUPPRESSOR GENE; UPREGULATION;

EID: 84983670770     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13706     Document Type: Article

References (49)

1. Alves da Costa C. and Checler F. (2011) Apoptosis in Parkinson's disease: is p53 the missing link between genetic and sporadic Parkinsonism? Cell. Signal. 23, 963–968.
2. Armstrong J. F., Kaufman M. H., Harrison D. J. and Clarke A. R. (1995) High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5, 931–936.
3. Backman C. M., Malik N., Zhang Y., Shan L., Grinberg A., Hoffer B. J., Westphal H. and Tomac A. C. (2006) Characterization of a mouse strain expressing Cre recombinase from the 3′ untranslated region of the dopamine transporter locus. Genesis 44, 383–390.
4. Bernstein A. I. and O'Malley K. L. (2013) MPP+-induces PUMA- and p53-dependent, but ATF3-independent cell death. Toxicol. Lett. 219, 93–98.
5. Blesa J., Phani S., Jackson-Lewis V. and Przedborski S. (2012) Classic and new animal models of Parkinson's disease. J. Biomed. Biotechnol. 2012, 845618.
6. Cabezas R., Avila M. F., Torrente D., El-Bachá R. S., Morales L., Gonzalez J. and Barreto G. E. (2013) Astrocytes role in Parkinson: a double-edged sword, in Neurodegenerative Diseases (Kishore U. ed.), pp. 491–518, InTech, Croatia.
7. Chipuk J. E., Kuwana T., Bouchier-Hayes L., Droin N. M., Newmeyer D. D., Schuler M. and Green D. R. (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303, 1010–1014.
8. da Costa C. A., Sunyach C., Giaime E. et al. (2009) Transcriptional repression of p53 by parkin and impairment by mutations associated with autosomal recessive juvenile Parkinson's disease. Nat. Cell Biol. 11, 1370–1375.
9. Culmsee C. and Mattson M. P. (2005) p53 in neuronal apoptosis. Biochem. Biophys. Res. Commun. 331, 761–777.
10. Diaz-Ruiz O., Zapata A., Shan L., Zhang Y., Tomac A. C., Malik N., de la Cruz F. and Backman C. M. (2009) Selective deletion of PTEN in dopamine neurons leads to trophic effects and adaptation of striatal medium spiny projecting neurons. PLoS ONE 4, e7027.
11. Donehower L. A. (1996) The p53-deficient mouse: a model for basic and applied cancer studies. Semin. Cancer Biol. 7, 269–278.
12. Duplan E., Giaime E., Viotti J. et al. (2013) ER-stress-associated functional link between Parkin and DJ-1 via a transcriptional cascade involving the tumor suppressor p53 and the spliced X-box binding protein XBP-1. J. Cell Sci. 126, 2124–2133.
13. Filichia E., Shen H., Zhou X., Qi X., Jin K., Greig N., Hoffer B. and Luo Y. (2015) Forebrain neuronal specific ablation of p53 gene provides protection in a cortical ischemic stroke model. Neuroscience 295, 1–10.
14. Forno L. S., DeLanney L. E., Irwin I., Di Monte D. and Langston J. W. (1992) Astrocytes and Parkinson's disease. Prog. Brain Res. 94, 429–436.
15. Franklin K. B. J. and Paxinos P. G. (1997) The mouse brain in stereotaxic coordinates. Academic Press, USA.
16. Hartmann A., Michel P. P., Troadec J. D., Mouatt-Prigent A., Faucheux B. A., Ruberg M., Agid Y. and Hirsch E. C. (2001) Is Bax a mitochondrial mediator in apoptotic death of dopaminergic neurons in Parkinson's disease? J. Neurochem. 76, 1785–1793.
17. Hattori T. and McGeer P. L. (1973) Synaptogenesis in the corpus striatum of infant rat. Exp. Neurol. 38, 70–79.
18. Hirata H. and Cadet J. L. (1997) p53-knockout mice are protected against the long-term effects of methamphetamine on dopaminergic terminals and cell bodies. J. Neurochem. 69, 780–790.
19. Hirsch E. C., Breidert T., Rousselet E., Hunot S., Hartmann A. and Michel P. P. (2003) The role of glial reaction and inflammation in Parkinson's disease. Ann. N. Y. Acad. Sci. 991, 214–228.
20. Hutter-Saunders J. A., Gendelman H. E. and Mosley R. L. (2012) Murine motor and behavior functional evaluations for acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) intoxication. J. Neuroimmune Pharmacol. 7, 279–288.
21. Jackson-Lewis V., Vila M., Djaldetti R., Guegan C., Liberatore G., Liu J., O'Malley K. L., Burke R. E. and Przedborski S. (2000) Developmental cell death in dopaminergic neurons of the substantia nigra of mice. J. Comp. Neurol. 424, 476–488.
22. Jin Y., Raviv N., Barnett A., Bambakidis N. C., Filichia E. and Luo Y. (2015) The shh signaling pathway is upregulated in multiple cell types in cortical ischemia and influences the outcome of stroke in an animal model. PLoS ONE 10, e0124657.
23. Jonkers J., Meuwissen R., van der Gulden H., Peterse H., van der Valk M. and Berns A. (2001) Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418–425.
24. Kawamata M. and Ochiya T. (2012) Two distinct knockout approaches highlight a critical role for p53 in rat development. Sci. Rep. 2, 945.
25. Kim W. R. and Sun W. (2011) Programmed cell death during postnatal development of the rodent nervous system. Dev. Growth Differ. 53, 225–235.
26. Langston J. W., Forno L. S., Tetrud J., Reeves A. G., Kaplan J. A. and Karluk D. (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann. Neurol. 46, 598–605.
27. Lee K. S., Lee J. K., Kim H. G. and Kim H. R. (2013) Differential effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on motor behavior and dopamine levels at brain regions in three different mouse strains. Korean J. Physiol. Pharmacol. 17, 89–97.
28. Liang Y., Liu J. and Feng Z. (2013) The regulation of cellular metabolism by tumor suppressor p53. Cell Biosci. 3, 9.
29. Linden R. (1994) The survival of developing neurons: a review of afferent control. Neuroscience 58, 671–682.
30. Luft A. R. and Buitrago M. M. (2005) Stages of motor skill learning. Mol. Neurobiol. 32, 205–216.
31. Luo Y., Kuo C. C., Shen H., Chou J., Greig N. H., Hoffer B. J. and Wang Y. (2009) Delayed treatment with a p53 inhibitor enhances recovery in stroke brain. Ann. Neurol. 65, 520–530.
32. Luo Y., Wang Y., Kuang S. Y., Chiang Y. H. and Hoffer B. (2010) Decreased level of Nurr1 in heterozygous young adult mice leads to exacerbated acute and long-term toxicity after repeated methamphetamine exposure. PLoS ONE 5, e15193.
33. Miklossy J., Doudet D. D., Schwab C., Yu S., McGeer E. G. and McGeer P. L. (2006) Role of ICAM-1 in persisting inflammation in Parkinson disease and MPTP monkeys. Exp. Neurol. 197, 275–283.
34. Miller R. M., Callahan L. M., Casaceli C. et al. (2004) Dysregulation of gene expression in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse substantia nigra. J. Neurosci. 24, 7445–7454.
35. Miller R. M., Chen L. L., Kiser G. L., Giesler T. L., Kaysser-Kranich T. M., Palaniappan C. and Federoff H. J. (2005) Temporal evolution of mouse striatal gene expression following MPTP injury. Neurobiol. Aging 26, 765–775.
36. Mogi M., Kondo T., Mizuno Y. and Nagatsu T. (2007) p53 protein, interferon-gamma, and NF-kappaB levels are elevated in the parkinsonian brain. Neurosci. Lett. 414, 94–97.
37. de la Monte S. M., Sohn Y. K., Ganju N. and Wands J. R. (1998) P53- and CD95-associated apoptosis in neurodegenerative diseases. Lab. Invest. 78, 401–411.
38. O'Callaghan J. P. and Jensen K. F. (1992) Enhanced expression of glial fibrillary acidic protein and the cupric silver degeneration reaction can be used as sensitive and early indicators of neurotoxicity. Neurotoxicology 13, 113–122.
39. Perier C., Bove J., Wu D. C. et al. (2007) Two molecular pathways initiate mitochondria-dependent dopaminergic neurodegeneration in experimental Parkinson's disease. Proc. Natl Acad. Sci. USA 104, 8161–8166.
40. Schumm S., Sebban C., Cohen-Salmon C. et al. (2012) Aging of the dopaminergic system and motor behavior in mice intoxicated with the parkinsonian toxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J. Neurochem. 122, 1032–1046.
41. Tatton N. A. (2000) Increased caspase 3 and Bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp. Neurol. 166, 29–43.
42. Trimmer P. A., Smith T. S., Jung A. B. and Bennett J. P. Jr (1996) Dopamine neurons from transgenic mice with a knockout of the p53 gene resist MPTP neurotoxicity. Neurodegeneration 5, 233–239.
43. Vila M., Jackson-Lewis V., Guegan C., Wu D. C., Teismann P., Choi D. K., Tieu K. and Przedborski S. (2001a) The role of glial cells in Parkinson's disease. Curr. Opin. Neurol. 14, 483–489.
44. Vila M., Jackson-Lewis V., Vukosavic S., Djaldetti R., Liberatore G., Offen D., Korsmeyer S. J. and Przedborski S. (2001b) 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. USA 98, 2837–2842.
45. West M. J. and Gundersen H. J. (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296, 1–22.
46. Yin H. H., Mulcare S. P., Hilario M. R., Clouse E., Holloway T., Davis M. I., Hansson A. C., Lovinger D. M. and Costa R. M. (2009) Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333–341.
47. Yokoyama H., Uchida H., Kuroiwa H., Kasahara J. and Araki T. (2011) Role of glial cells in neurotoxin-induced animal models of Parkinson's disease. Neurol. Sci. 32, 1–7.
48. Yokoyama M., Okada S., Nakagomi A. et al. (2014) Inhibition of endothelial p53 improves metabolic abnormalities related to dietary obesity. Cell Rep. 7, 1691–1703.
49. Zhang Y., Granholm A. C., Huh K. et al. (2012) PTEN deletion enhances survival, neurite outgrowth and function of dopamine neuron grafts to MitoPark mice. Brain 135, 2736–2749.