Phosphorylation of 4E-BP1 in the Mammalian Brain Is Not Altered by LRRK2 Expression or Pathogenic Mutations

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Trancikova, Alzbeta ^a   Mamais, Adamantios ^b   Webber, Philip J ^c   Stafa, Klodjan ^a   Tsika, Elpida ^a   Glauser, Liliane ^a   West, Andrew B ^c   Bandopadhyay, Rina ^b   Moore, Darren J ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; BETA TUBULIN; INITIATION FACTOR 4E BINDING PROTEIN 1; LEUCINE RICH REPEAT KINASE 2; SYNAPTOPHYSIN;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PARKINSON DISEASE; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGED; AGED, 80 AND OVER; ANIMALS; BRAIN; CARRIER PROTEINS; FEMALE; HEK293 CELLS; HUMANS; MALE; MAMMALS; MICE; MULTIPROTEIN COMPLEXES; MUTATION; PARKINSON DISEASE; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; RATS; SUBCELLULAR FRACTIONS;

EID: 84867649477     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047784     Document Type: Article

References (47)

1. Biskup S, West AB, (2009) Zeroing in on LRRK2-linked pathogenic mechanisms in Parkinson's disease. Biochim Biophys Acta 1792: 625-633.
2. Gasser T, (2009) Mendelian forms of Parkinson's disease. Biochim Biophys Acta 1792: 587-596.
3. Healy DG, Falchi M, O'Sullivan SS, Bonifati V, Durr A, et al. (2008) Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson's disease: a case-control study. Lancet Neurol 7: 583-590.
4. Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C, et al. (2009) Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 41: 1303-1307.
5. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, et al. (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 41: 1308-1312.
6. Giasson BI, Covy JP, Bonini NM, Hurtig HI, Farrer MJ, et al. (2006) Biochemical and pathological characterization of Lrrk2. Annals of Neurology 59: 315-322.
7. Ross OA, Toft M, Whittle AJ, Johnson JL, Papapetropoulos S, et al. (2006) Lrrk2 and Lewy body disease. Ann Neurol 59: 388-393.
8. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, et al. (2004) Mutations in LRRK2 Cause Autosomal-Dominant Parkinsonism with Pleomorphic Pathology. Neuron 44: 601-607.
9. Tsika E, Moore DJ, (2012) Mechanisms of LRRK2-mediated neurodegeneration. Curr Neurol Neurosci Rep 12: 251-260.
10. West AB, Moore DJ, Biskup S, Bugayenko A, Smith WW, et al. (2005) Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc Natl Acad Sci U S A 102: 16842-16847.
11. Greggio E, Cookson MR (2009) Leucine-rich repeat kinase 2 mutations and Parkinson's disease: three questions. ASN Neuro 1.
12. Aasly JO, Vilarino-Guell C, Dachsel JC, Webber PJ, West AB, et al. (2010) Novel pathogenic LRRK2 p.Asn1437His substitution in familial Parkinson's disease. Mov Disord 25: 2156-2163.
13. Ito G, Okai T, Fujino G, Takeda K, Ichijo H, et al. (2007) GTP Binding Is Essential to the Protein Kinase Activity of LRRK2, a Causative Gene Product for Familial Parkinson's Disease†. Biochemistry 46: 1380-1388.
14. Lewis PA, Greggio E, Beilina A, Jain S, Baker A, et al. (2007) The R1441C mutation of LRRK2 disrupts GTP hydrolysis. Biochem Biophys Res Commun 357: 668-671.
15. Li X, Tan YC, Poulose S, Olanow CW, Huang XY, et al. (2007) Leucine-rich repeat kinase 2 (LRRK2)/PARK8 possesses GTPase activity that is altered in familial Parkinson's disease R1441C/G mutants. J Neurochem 103: 238-247.
16. Xiong Y, Coombes CE, Kilaru A, Li X, Gitler AD, et al. (2010) GTPase Activity Plays a Key Role in the Pathobiology of LRRK2. PLoS Genet 6: e1000902.
17. West AB, Moore DJ, Choi C, Andrabi SA, Li X, et al. (2007) Parkinson's disease-associated mutations in LRRK2 link enhanced GTP-binding and kinase activities to neuronal toxicity. Hum Mol Genet 16: 223-232.
18. Greggio E, Jain S, Kingsbury A, Bandopadhyay R, Lewis P, et al. (2006) Kinase activity is required for the toxic effects of mutant LRRK2/dardarin. Neurobiol Dis 23: 329-341.
19. Smith WW, Pei Z, Jiang H, Dawson VL, Dawson TM, et al. (2006) Kinase activity of mutant LRRK2 mediates neuronal toxicity. Nat Neurosci 9: 1231-1233.
20. Smith WW, Pei Z, Jiang H, Moore DJ, Liang Y, et al. (2005) Leucine-rich repeat kinase 2 (LRRK2) interacts with parkin, and mutant LRRK2 induces neuronal degeneration. Proc Natl Acad Sci U S A 102: 18676-18681.
21. Greggio E, Taymans JM, Zhen EY, Ryder J, Vancraenenbroeck R, et al. (2009) The Parkinson's disease kinase LRRK2 autophosphorylates its GTPase domain at multiple sites. Biochem Biophys Res Commun 389: 449-454.
22. Jaleel M, Nichols RJ, Deak M, Campbell DG, Gillardon F, et al. (2007) LRRK2 phosphorylates moesin at threonine-558: characterization of how Parkinson's disease mutants affect kinase activity. Biochem J 405: 307-317.
23. Kamikawaji S, Ito G, Iwatsubo T, (2009) Identification of the autophosphorylation sites of LRRK2. Biochemistry 48: 10963-10975.
24. Webber PJ, Smith AD, Sen S, Renfrow MB, Mobley JA, et al. (2011) Autophosphorylation in the leucine-rich repeat kinase 2 (LRRK2) GTPase domain modifies kinase and GTP-binding activities. J Mol Biol 412: 94-110.
25. Imai Y, Gehrke S, Wang HQ, Takahashi R, Hasegawa K, et al. (2008) Phosphorylation of 4E-BP by LRRK2 affects the maintenance of dopaminergic neurons in Drosophila. EMBO J 27: 2432-2443.
26. Gillardon F, (2009) Leucine-rich repeat kinase 2 phosphorylates brain tubulin-beta isoforms and modulates microtubule stability - a point of convergence in Parkinsonian neurodegeneration? J Neurochem 110: 1514-1522.
27. Kanao T, Venderova K, Park DS, Unterman T, Lu B, et al. (2010) Activation of FoxO by LRRK2 induces expression of proapoptotic proteins and alters survival of postmitotic dopaminergic neuron in Drosophila. Hum Mol Genet 19: 3747-3758.
28. Gloeckner CJ, Schumacher A, Boldt K, Ueffing M, (2009) The Parkinson disease-associated protein kinase LRRK2 exhibits MAPKKK activity and phosphorylates MKK3/6 and MKK4/7, in vitro. J Neurochem 109: 959-968.
29. Hsu CH, Chan D, Greggio E, Saha S, Guillily MD, et al. (2010) MKK6 binds and regulates expression of Parkinson's disease-related protein LRRK2. J Neurochem 112: 1593-1604.
30. Stafa K, Trancikova A, Webber PJ, Glauser L, West AB, et al. (2012) GTPase activity and neuronal toxicity of Parkinson's disease-associated LRRK2 is regulated by ArfGAP1. PLoS Genet 8: e1002526.
31. Xiong Y, Yuan C, Chen R, Dawson TM, Dawson VL, (2012) ArfGAP1 is a GTPase activating protein for LRRK2: reciprocal regulation of ArfGAP1 by LRRK2. J Neurosci 32: 3877-3886.
32. Lin TA, Kong X, Haystead TA, Pause A, Belsham G, et al. (1994) PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266: 653-656.
33. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, et al. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371: 762-767.
34. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, et al. (1999) Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13: 1422-1437.
35. Tain LS, Mortiboys H, Tao RN, Ziviani E, Bandmann O, et al. (2009) Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat Neurosci 12: 1129-1135.
36. Kumar A, Greggio E, Beilina A, Kaganovich A, Chan D, et al. (2010) The Parkinson's disease associated LRRK2 exhibits weaker in vitro phosphorylation of 4E-BP compared to autophosphorylation. PLoS One 5: e8730.
37. Herzig MC, Kolly C, Persohn E, Theil D, Schweizer T, et al. (2011) LRRK2 protein levels are determined by kinase function and are crucial for kidney and lung homeostasis in mice. Hum Mol Genet 20: 4209-4223.
38. Ramonet D, Daher JP, Lin BM, Stafa K, Kim J, et al. (2011) Dopaminergic neuronal loss, reduced neurite complexity and autophagic abnormalities in transgenic mice expressing G2019S mutant LRRK2. PLoS One 6: e18568.
39. Glauser L, Sonnay S, Stafa K, Moore DJ, (2011) Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J Neurochem 118: 636-645.
40. Zhou H, Beaudet AL, (2000) A new vector system with inducible E2a cell line for production of higher titer and safer adenoviral vectors. Virology 275: 348-357.
41. Young SM Jr, Neher E, (2009) Synaptotagmin has an essential function in synaptic vesicle positioning for synchronous release in addition to its role as a calcium sensor. Neuron 63: 482-496.
42. Dusonchet J, Kochubey O, Stafa K, Young SM Jr, Zufferey R, et al. (2011) A Rat Model of Progressive Nigral Neurodegeneration Induced by the Parkinson's Disease-Associated G2019S Mutation in LRRK2. J Neurosci 31: 907-912.
43. Ng P, Graham FL, (2002) Construction of first-generation adenoviral vectors. Methods Mol Med 69: 389-414.
44. Biskup S, Moore DJ, Celsi F, Higashi S, West AB, et al. (2006) Localization of LRRK2 to membranous and vesicular structures in mammalian brain. Ann Neurol 60: 557-569.
45. Hallett PJ, Collins TL, Standaert DG, Dunah AW (2008) Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr Protoc Neurosci Chapter 1: Unit 1 16.
46. Stafa K, Trancikova A, Webber PJ, Glauser L, West A, et al. (2012) GTPase Activity and Neuronal Toxicity of Parkinson's Disease-Associated LRRK2 is Regulated by ArfGAP1. PLoS Genet 8: e1002527.
47. McKeith IG, Dickson DW, Lowe J, Emre M, O'Brien JT, et al. (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65: 1863-1872.