Parthanatos mediates AIMP2-activated age-dependent dopaminergic neuronal loss

Nature Neuroscience

Volumn 16, Issue 10, 2013, Pages 1392-1400

  Lee, Yunjong ^a,b   Karuppagounder, Senthilkumar S ^a,b   Shin, Joo Ho ^a,b,c   Lee, Yun Il ^a,h   Ko, Han Seok ^a,d   Swing, Debbie ^e   Jiang, Haisong ^a,b   Kang, Sung Ung ^a,b   Lee, Byoung Dae ^a,f   Kang, Ho Chul ^a,g   Kim, Donghoon ^a,d   Tessarollo, Lino ^e   Dawson, Valina L ^a,b   Dawson, Ted M ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ADRIENNE HELIS MALVIN MEDICAL RESEARCH FOUNDATION   (United States)

^c Samsung Medical Center   (South Korea)

^d Diana Helis Henry Medical Research Foundation   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f Kyung Hee University   (South Korea)

^g Ajou University School of Medicine   (South Korea)

^h Samsung Advanced Institute of Technology (SAIT)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRNA SYNTHETASE COMPLEX INTERACTING MULTIFUNCTIONAL PROTEIN 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARKIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DOPAMINERGIC NERVE CELL; DRUG INHIBITION; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL;

AGE FACTORS; ANIMALS; CARRIER PROTEINS; CELL AGING; CELL DEATH; DOPAMINERGIC NEURONS; FEMALE; GENE DELETION; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PC12 CELLS; POLY(ADP-RIBOSE) POLYMERASES; PREGNANCY; RATS;

EID: 84884902975     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3500     Document Type: Article

References (52)

1. Abbas, N. et al. A wide variety of mutations in the parkin gene are responsible for autosomal recessive parkinsonism in Europe. French Parkinson's Disease Genetics Study Group and the European Consortium on Genetic Susceptibility in Parkinson's Disease. Hum. Mol. Genet. 8, 567-574 (1999).
2. Kitada, T. et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608 (1998). (Pubitemid 28207717)
3. Corti, O., Lesage, S. & Brice, A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev. 91, 1161-1218 (2011).
4. Dawson, T.M. Parkin and defective ubiquitination in Parkinson's disease. J. Neural Transm. Suppl. 70, 209-213 (2006). (Pubitemid 44622201)
5. Moore, D.J. Parkin: a multifaceted ubiquitin ligase. Biochem. Soc. Trans. 34, 749-753 (2006).
6. Chung, K.K. et al. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304, 1328-1331 (2004). (Pubitemid 38697430)
7. Imam, S.Z. et al. Novel regulation of parkin function through c-Abl-mediated tyrosine phosphorylation: implications for Parkinson's disease. J. Neurosci. 31, 157-163 (2011).
8. Kim, M.Y., Mauro, S., Gevry, N., Lis, J.T. & Kraus, W.L. NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119, 803-814 (2004). (Pubitemid 40017687)
9. Ko, H.S. et al. Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function. Proc. Natl. Acad. Sci. USA 107, 16691-16696 (2010).
10. LaVoie, M.J., Ostaszewski, B.L., Weihofen, A., Schlossmacher, M.G. & Selkoe, D.J. Dopamine covalently modifies and functionally inactivates parkin. Nat. Med. 11, 1214-1221 (2005). (Pubitemid 43093669)
11. Meng, F. et al. Oxidation of the cysteine-rich regions of parkin perturbs its E3 ligase activity and contributes to protein aggregation. Mol. Neurodegener. 6, 34 (2011).
12. Wang, C. et al. Stress-induced alterations in parkin solubility promote parkin aggregation and compromise parkin's protective function. Hum. Mol. Genet. 14, 3885-3897 (2005). (Pubitemid 43020090)
13. Yao, D. et al. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc. Natl. Acad. Sci. USA 101, 10810-10814 (2004). (Pubitemid 38955824)
14. Geisler, S. et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131 (2010).
15. Olzmann, J.A. & Chin, L.S. Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 4, 85-87 (2008).
16. Cookson, M.R. Parkin's substrates and the pathways leading to neuronal damage. Neuromolecular Med. 3, 1-13 (2003). (Pubitemid 37070578)
17. Corti, O. et al. The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration. Hum. Mol. Genet. 12, 1427-1437 (2003). (Pubitemid 36758455)
18. Ko, H.S. et al. Accumulation of the authentic parkin substrate aminoacyl-tRNA synthetase cofactor, p38/JTV-1, leads to catecholaminergic cell death. J. Neurosci. 25, 7968-7978 (2005). (Pubitemid 41254399)
19. Kistner, A. et al. Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice. Proc. Natl. Acad. Sci. USA 93, 10933-10938 (1996). (Pubitemid 26333095)
20. Sprengel, R. & Hasan, M.T. Tetracycline-controlled genetic switches. Handb. Exp. Pharmacol. 178, 49-72 (2007).
21. de Murcia, G. et al. Structure and function of poly(ADP-ribose) polymerase. Mol. Cell Biochem. 138, 15-24 (1994). (Pubitemid 24365390)
22. Wang, Y., Dawson, V.L. & Dawson, T.M. Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp. Neurol. 218, 193-202 (2009).
23. Andrabi, S.A. et al. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc. Natl. Acad. Sci. USA 103, 18308-18313 (2006). (Pubitemid 44871654)
24. Wang, Y. et al. Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci. Signal. 4, ra20 (2011).
25. Mayford, M. et al. Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683 (1996). (Pubitemid 26414891)
26. German, D.C., Manaye, K., Smith, W.K., Woodward, D.J. & Saper, C.B. Midbrain dopaminergic cell loss in Parkinson's disease: computer visualization. Ann. Neurol. 26, 507-514 (1989). (Pubitemid 19247226)
27. Park, S.G., Choi, E.C. & Kim, S. Aminoacyl-tRNA synthetase- interacting multifunctional proteins (AIMPs): a triad for cellular homeostasis. IUBMB Life 62, 296-302 (2010).
28. MacCallum, P.R. et al. Cap-dependent and hepatitis C virus internal ribosome entry site-mediated translation are modulated by phosphorylation of eIF2alpha under oxidative stress. J. Gen. Virol. 87, 3251-3262 (2006). (Pubitemid 44608360)
29. Plummer, R. et al. Phase I study of the poly(ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin. Cancer Res. 14, 7917-7923 (2008).
30. Rudow, G. et al. Morphometry of the human substantia nigra in ageing and Parkinson's disease. Acta Neuropathol. 115, 461-470 (2008).
31. Ko, H.S., Kim, S.W., Sriram, S.R., Dawson, V.L. & Dawson, T.M. Identification of far upstream element-binding protein-1 as an authentic Parkin substrate. J. Biol. Chem. 281, 16193-16196 (2006).
32. Shin, J.H. et al. PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 144, 689-702 (2011).
33. Obeso, J.A. et al. Missing pieces in the Parkinson's disease puzzle. Nat. Med. 16, 653-661 (2010).
34. Dawson, T.M., Ko, H.S. & Dawson, V.L. Genetic animal models of Parkinson's disease. Neuron 66, 646-661 (2010).
35. Rouleau, M., Patel, A., Hendzel, M.J., Kaufmann, S.H. & Poirier, G.G. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer 10, 293-301 (2010).
36. Von Coelln, R. et al. Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proc. Natl. Acad. Sci. USA 101, 10744-10749 (2004). (Pubitemid 38955813)
37. Lee, B.D. et al. Inhibitors of leucine-rich repeat kinase-2 protect against models of Parkinson's disease. Nat. Med. 16, 998-1000 (2010).
38. Kirik, D. et al. Nigrostriatal alpha-synucleinopathy induced by viral vector-mediated overexpression of human alpha-synuclein: a new primate model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 100, 2884-2889 (2003). (Pubitemid 36297593)
39. Chesselet, M.F. & Richter, F. Modeling of Parkinson's disease in mice. Lancet Neurol. 10, 1108-1118 (2011).
40. Lee, Y., Dawson, V.L. & Dawson, T.M. Animal models of Parkinson's disease: vertebrate genetics. Cold Spring Harb. Perspect. Med. 2, a009324 (2012).
41. Lin, X. et al. Conditional expression of Parkinson's disease-related mutant alpha-synuclein in the midbrain dopaminergic neurons causes progressive neurodegeneration and degradation of transcription factor nuclear receptor related 1. J. Neurosci. 32, 9248-9264 (2012).
42. Royo, N.C. et al. Specific AAV serotypes stably transduce primary hippocampal and cortical cultures with high efficiency and low toxicity. Brain Res. 1190, 15-22 (2008).
43. Corti, O. & Brice, A. Mitochondrial quality control turns out to be the principal suspect in parkin and PINK1-related autosomal recessive Parkinson's disease. Curr. Opin. Neurobiol. 23, 100-108 (2013).
44. Han, J.M. et al. AIMP2/p38, the scaffold for the multi-tRNA synthetase complex, responds to genotoxic stresses via p53. Proc. Natl. Acad. Sci. USA 105, 11206-11211 (2008).
45. Kim, J.Y. et al. p38 is essential for the assembly and stability of macromolecular tRNA synthetase complex: implications for its physiological significance. Proc. Natl. Acad. Sci. USA 99, 7912-7916 (2002). (Pubitemid 34650979)
46. Chan, C.S. et al. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447, 1081-1086 (2007). (Pubitemid 47014425)
47. Guzman, J.N. et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468, 696-700 (2010).
48. Mandir, A.S. et al. Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc. Natl. Acad. Sci. USA 96, 5774-5779 (1999). (Pubitemid 29234694)
49. Wang, H., Shimoji, M., Yu, S.W., Dawson, T.M. & Dawson, V.L. Apoptosis inducing factor and PARP-mediated injury in the MPTP mouse model of Parkinson's disease. Ann. NY Acad. Sci. 991, 132-139 (2003). (Pubitemid 36793809)
50. Lin, X. et al. Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's disease-related mutant alpha-synuclein. Neuron 64, 807-827 (2009).
51. Yu, S.W. et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297, 259-263 (2002).
52. West, M.J. New stereological methods for counting neurons. Neurobiol. Aging 14, 275-285 (1993). (Pubitemid 23214693)