ATF4 protects against neuronal death in cellular Parkinson's disease models by maintaining levels of parkin

Journal of Neuroscience

Volumn 33, Issue 6, 2013, Pages 2398-2407

  Sun, Xiaotian ^a   Liu, Jin ^a   Crary, John F ^a   Malagelada, Cristina ^b   Sulzer, David ^a   Greene, Lloyd A ^a   Levy, Oren A ^a  

^a NewYork Presbyterian Hospital   (United States)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; ACTIVATING TRANSCRIPTION FACTOR 4; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MITOGEN ACTIVATED PROTEIN KINASE; NEUROMELANIN; OXIDOPAMINE; PARKIN; SHORT HAIRPIN RNA; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; CELL DEATH; CELLS, CULTURED; HEK293 CELLS; HUMANS; MICE; NEURONS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; PC12 CELLS; RATS; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION;

EID: 84873287971     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2292-12.2013     Document Type: Article

References (53)

1. Ameri K, Harris AL (2008) Activating transcription factor 4. Int J Biochem Cell Biol 40:14-21. CrossRef Medline
2. Amino T, Orimo S, Itoh Y, Takahashi A, Uchihara T, Mizusawa H (2005) Profound cardiac sympathetic denervation occurs in Parkinson disease. Brain Pathol 15:29-34. Medline
3. Averous J, Bruhat A, Jousse C, Carraro V, Thiel G, Fafournoux P (2004) Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J Biol Chem 279:5288-5297. CrossRef Medline
4. Biswas SC, Zhang Y, Iyirhiaro G, Willett RT, Rodriguez Gonzalez Y, Cregan SP, Slack RS, Park DS, Greene LA (2010) Sertad1 plays an essential role in developmental and pathological neuron death. J Neurosci 30:3973-3982. CrossRef Medline
5. Bouman L, Schlierf A, Lutz AK, Shan J, Deinlein A, Kast J, Galehdar Z, Palmisano V, Patenge N, Berg D, Gasser T, Augustin R, Trümbach D, Irrcher I, Park DS, Wurst W, Kilberg MS, Tatzelt J, Winklhofer KF (2011) Parkin is transcriptionally regulated by ATF4: evidence for an interconnection between mitochondrial stress and ER stress. Cell Death Differ 18:769-782. CrossRef Medline
6. Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24:197-211. CrossRef Medline
7. Bromati CR, Lellis-Santos C, Yamanaka TS, Nogueira TC, Leonelli M, Caperuto LC, Gorjão R, Leite AR, Anhe GF, Bordin S (2011) UPR induces transient burst of apoptosis in islets of early lactating rats through reduced AKT phosphorylation via ATF4/CHOP stimulation of TRB3 expression. Am J Physiol Regul Integr Comp Physiol 300:R92-R100. CrossRef Medline
8. Cha GH, Kim S, Park J, Lee E, Kim M, Lee SB, Kim JM, Chung J, Cho KS (2005) Parkin negatively regulates JNK pathway in the dopaminergic neurons of Drosophila. Proc Natl Acad Sci U S A 102:10345-10350. CrossRef Medline
9. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304:1328-1331. CrossRef Medline
10. Colla E, Coune P, Liu Y, Pletnikova O, Troncoso JC, Iwatsubo T, Schneider BL, Lee MK (2012) Endoplasmic reticulum stress is important for the manifestations of synucleinopathy in vivo. J Neurosci 32:3306-3320. CrossRef Medline
11. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909. CrossRef Medline
12. Dawson TM, Dawson VL (2010) The role of parkin in familial and sporadic Parkinson's disease. Mov Disord 25 [Suppl 1]:S32-S39. CrossRef
13. De Vos KJ, Grierson AJ, Ackerley S, Miller CC (2008) Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci 31:151-173. CrossRef Medline
14. Fels DR, Koumenis C (2006) The PERK/elF2 alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biol Ther 5:723-728. CrossRef Medline
15. Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, Cregan SP (2010) Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 30:16938-16948. CrossRef Medline
16. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73:2424-2428. CrossRef Medline
17. Hai T, Curran T (1991) Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci U S A 88:3720-3724. CrossRef Medline
18. Halterman MW, Gill M, DeJesus C, Ogihara M, Schor NF, Federoff HJ (2010) The endoplasmic reticulum stress response factor CHOP-10 protects against hypoxia-induced neuronal death. J Biol Chem 285:21329-21340. CrossRef Medline
19. Hara H, Kamiya T, Adachi T (2011) Endoplasmic reticulum stress inducers provide protection against 6-hydroxydopamine-induced cytotoxicity. Neurochem Int 58:35-43. CrossRef Medline
20. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108. CrossRef Medline
21. Henn IH, Gostner JM, Lackner P, Tatzelt J, Winklhofer KF (2005) Patho-genic mutations inactivate parkin by distinct mechanisms. J Neurochem 92:114-122. CrossRef Medline
22. Holtz WA, O'Malley KL (2003) Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J Biol Chem 278:19367-19377. CrossRef Medline
23. Hoozemans JJ, van Haastert ES, Eikelenboom P, de Vos RA, Rozemuller JM, Scheper W (2007) Activation of the unfolded protein response in Parkinson's disease. Biochem Biophys Res Commun 354:707-711. CrossRef Medline
24. Imam SZ, Zhou Q, Yamamoto A, Valente AJ, Ali SF, Bains M, Roberts JL, Kahle PJ, Clark RA, Li S (2011) Novel regulation of parkin function through c-Abl-mediated tyrosine phosphorylation: implications for Parkinson's disease. J Neurosci 31:157-163. CrossRef Medline
25. Jensen LD, Vinther-Jensen T, Kahns S, Sundbye S, Jensen PH (2006) Cellular parkin mutants are soluble under non-stress conditions. Neuroreport 17:1205-1208. CrossRef Medline
26. Jiang H, Ren Y, Zhao J, Feng J (2004) Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum Mol Genet 13:1745-1754. CrossRef Medline
27. Kahns S, Lykkebo S, Jakobsen LD, Nielsen MS, Jensen PH (2002) Caspase-mediated parkin cleavage in apoptotic cell death. J Biol Chem 277:15303-15308. CrossRef Medline
28. Kahns S, Kalai M, Jakobsen LD, Clark BF, Vandenabeele P, Jensen PH (2003) Caspase-1 and caspase-8 cleave and inactivate cellular parkin. J Biol Chem 278:23376-23380. CrossRef Medline
29. Ko HS, Lee Y, Shin JH, Karuppagounder SS, Gadad BS, Koleske AJ, Pletnikova O, Troncoso JC, Dawson VL, Dawson TM (2010) Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function. Proc Natl Acad Sci U S A 107:16691-16696. CrossRef Medline
30. Lai KO, Zhao Y, Ch'ng TH, Martin KC (2008) Importin-mediated retrograde transport of CREB2 from distal processes to the nucleus in neurons. Proc Natl Acad Sci U S A 105:17175-17180. CrossRef Medline
31. Lange PS, Chavez JC, Pinto JT, Coppola G, Sun CW, Townes TM, Geschwind DH, Ratan RR (2008) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J Exp Med 205:1227-1242. CrossRef Medline
32. Lesuisse C, Martin LJ (2002) Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death. J Neurobiol 51:9-23. CrossRef Medline
33. Lewerenz J, Sato H, Albrecht P, Henke N, Noack R, Methner A, Maher P (2012) Mutation of ATF4 mediates resistance of neuronal cell lines against oxidative stress by inducing xCT expression. Cell Death Differ 19:847-858. CrossRef Medline
34. Malagelada C, Jin ZH, Greene LA (2008) RTP801 is induced in Parkinson's disease and mediates neuron death by inhibiting Akt phosphorylation/ activation. J Neurosci 28:14363-14371. CrossRef Medline
35. Martínez-Reyes I, Sánchez-Aragó M, Cuezva JM (2012) AMPKand GCN2- ATF4 signal the repression of mitochondria in colon cancer cells. Biochem J 444:249-259. CrossRef Medline
36. Meng F, Yao D, Shi Y, Kabakoff J, Wu W, Reicher J, Ma Y, Moosmann B, Masliah E, Lipton SA, Gu Z (2011) Oxidation of the cysteine-rich regions of parkin perturbs its E3 ligase activity and contributes to protein aggregation. Mol Neurodegener 6:34. CrossRef Medline
37. Milani M, Rzymski T, Mellor HR, Pike L, Bottini A, Generali D, Harris AL (2009) The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Cancer Res 69:4415-4423. CrossRef Medline
38. Poole AC, Thomas RE, Andrews LA, McBride HM, Whitworth AJ, Pallanck LJ (2008) The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci U S A 105:1638-1643. CrossRef Medline
39. Ritter B, Zschuntzsch J, Kvachnina E, Zhang WQ, Ponimaskin EG (2004) The GABA(B) receptor subunits R1 and R2 interact differentially with the activation transcription factor ATF4 in mouse brain during the postnatal development. Dev Brain Res 149:73-77. CrossRef
40. Ryu EJ, Harding HP, Angelastro JM, Vitolo OV, Ron D, Greene LA (2002) Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J Neurosci 22:10690-10698. Medline
41. Rzymski T, Milani M, Pike L, Buffa F, Mellor HR, Winchester L, Pires I, Hammond E, Ragoussis I, Harris AL (2010) Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 29:4424-4435. CrossRef Medline
42. Shin JH, Ko HS, Kang H, Lee Y, Lee YI, Pletinkova O, Troconso JC, Dawson VL, Dawson TM (2011) PARIS (ZNF746) repression of PGC-1+ contributes to neurodegeneration in Parkinson's disease. Cell 144:689-702. CrossRef Medline
43. Smith WW, Jiang H, Pei Z, Tanaka Y, Morita H, Sawa A, Dawson VL, Dawson TM, Ross CA (2005) Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Hum Mol Genet 14:3801-3811. CrossRef Medline
44. Staal RG, Rayport S, Sulzer D (2007) Amperometric detection of dopamine exocytosis from synaptic terminals. In: Electrochemical methods for neuroscience, Ed January 2011 (Michael AC, Borland LM, eds). Boca Raton, FL: CRC.
45. Um JW, Park HJ, Song J, Jeon I, Lee G, Lee PH, Chung KC (2010) Formation of parkin aggregates and enhanced PINK1 accumulation during the pathogenesis of Parkinson's disease. Biochem Biophys Res Commun 393: 824-828. CrossRef Medline
46. Vallejo M, Ron D, Miller CP, Habener JF (1993) C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc Natl Acad Sci U S A 90:4679-4683. CrossRef Medline
47. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS, Magrané J, Moore DJ, Dawson VL, Grailhe R, Dawson TM, Li C, Tieu K, Przedborski S (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 107:378-383. CrossRef Medline
48. Wang C, Tan JM, Ho MW, Zaiden N, Wong SH, Chew CL, Eng PW, Lim TM, Dawson TM, Lim KL (2005a) Alterations in the solubility and intracellular localization of parkin by several familial Parkinson's disease-linked point mutations. J Neurochem 93:422-431. CrossRef Medline
49. Wang C, Ko HS, Thomas B, Tsang F, Chew KC, Tay SP, Ho MW, Lim TM, Soong TW, Pletnikova O, Troncoso J, Dawson VL, Dawson TM, Lim KL (2005b) Stress-induced alterations in parkin solubility promote parkin aggregation and compromise parkin's protective function. Hum Mol Genet 14:3885-3897. CrossRef Medline
50. Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, Palmer LA, Rockenstein EM, Zhang Z, Masliah E, Uehara T, Lipton SA (2004) Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci U S A 101:10810-10814. CrossRef Medline
51. Ye J, Koumenis C (2009) ATF4, an ER stress and hypoxia-inducible transcription factor and its potential role in hypoxia tolerance and tumorigenesis. Curr Mol Med 9:411-416. CrossRef Medline
52. Yu F, Zhou J (2008) Parkin is ubiquitinated by Nrdp1 and abrogates Nrdp1-induced oxidative stress. Neurosci Lett 440:4-8. CrossRef Medline
53. Zou W, Yue P, Khuri FR, Sun SY (2008) Coupling of endoplasmic reticulum stress to CDDO-Me-induced up-regulation of death receptor 5 via a CHOP-dependent mechanism involving JNK activation. Cancer Res 68: 7484-7492. CrossRef Medline