Expression Analysis of Lrrk1, Lrrk2 and Lrrk2 Splice Variants in Mice

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Giesert, Florian ^a   Hofmann, Andreas ^a   Bürger, Alexander ^a   Zerle, Julia ^a   Kloos, Karina ^a   Hafen, Ulrich ^a   Ernst, Luise ^a   Zhang, Jingzhong ^a   Vogt Weisenhorn, Daniela Maria ^a   Wurst, Wolfgang ^a,b,c,d  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; LEUCINE RICH REPEAT KINASE 2; MESSENGER RNA;

AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN REGION; CELL SPECIFICITY; CELL SUBPOPULATION; CELL TYPE; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS STRIATUM; EMBRYO; EMBRYO DEVELOPMENT; EXON; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; GENETIC VARIABILITY; IN SITU HYBRIDIZATION; LEUCINE RICH REPEAT KINASE 1 GENE; LEUCINE RICH REPEAT KINASE 2 GENE; MITRAL CELL; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; PARKINSON DISEASE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; BRAIN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ORDER; MICE; NEURONS; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER;

EID: 84877636702     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063778     Document Type: Article

References (75)

1. de Rijk MC, Breteler MM, Graveland GA, Ott A, Grobbee DE, et al. (1995) Prevalence of Parkinson's disease in the elderly: the Rotterdam Study. Neurology 45: 2143-2146.
2. Lang AE, Lozano AM, (1998) Parkinson's disease. Second of two parts. N Engl J Med 339: 1130-1143.
3. Lang AE, Lozano AM, (1998) Parkinson's disease. First of two parts. N Engl J Med 339: 1044-1053.
4. Fujioka S, Wszolek ZK, (2012) Update on genetics of parkinsonism. Neurodegener Dis 10: 257-260.
5. Houlden H, Singleton AB, (2012) The genetics and neuropathology of Parkinson's disease. Acta Neuropathol 124: 325-338.
6. Funayama M, Hasegawa K, Kowa H, Saito M, Tsuji S, et al. (2002) A new locus for Parkinson's disease (PARK8) maps to chromosome 12p11.2-q13.1. Ann Neurol 51: 296-301.
7. Paisan-Ruiz C, Jain S, Evans EW, Gilks WP, Simon J, et al. (2004) Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44: 595-600.
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. 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.
10. Kruger R, (2008) LRRK2 in Parkinson's disease- drawing the curtain of penetrance: a commentary. BMC Med 6: 33.
11. Lesage S, Ibanez P, Lohmann E, Pollak P, Tison F, et al. (2005) G2019S LRRK2 mutation in French and North African families with Parkinson's disease. Ann Neurol 58: 784-787.
12. Ozelius LJ, Senthil G, Saunders-Pullman R, Ohmann E, Deligtisch A, et al. (2006) LRRK2 G2019S as a cause of Parkinson's disease in Ashkenazi Jews. N Engl J Med 354: 424-425.
13. 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.
14. 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.
15. Funayama M, Hasegawa K, Ohta E, Kawashima N, Komiyama M, et al. (2005) An LRRK2 mutation as a cause for the parkinsonism in the original PARK8 family. Ann Neurol 57: 918-921.
16. Giasson BI, Covy JP, Bonini NM, Hurtig HI, Farrer MJ, et al. (2006) Biochemical and pathological characterization of Lrrk2. Ann Neurol 59: 315-322.
17. Rajput A, Dickson DW, Robinson CA, Ross OA, Dachsel JC, et al. (2006) Parkinsonism, Lrrk2 G2019S, and tau neuropathology. Neurology 67: 1506-1508.
18. Ross OA, Toft M, Whittle AJ, Johnson JL, Papapetropoulos S, et al. (2006) Lrrk2 and Lewy body disease. Ann Neurol 59: 388-393.
19. Bosgraaf L, Van Haastert PJ, (2003) Roc, a Ras/GTPase domain in complex proteins. Biochim Biophys Acta 1643: 5-10.
20. Marin I, (2006) The Parkinson disease gene LRRK2: evolutionary and structural insights. Mol Biol Evol 23: 2423-2433.
21. Marin I, (2008) Ancient origin of the Parkinson disease gene LRRK2. J Mol Evol 67: 41-50.
22. Gloeckner CJ, Kinkl N, Schumacher A, Braun RJ, O'Neill E, et al. (2006) The Parkinson disease causing LRRK2 mutation I2020T is associated with increased kinase activity. Hum Mol Genet 15: 223-232.
23. Greggio E, Lewis PA, van der Brug MP, Ahmad R, Kaganovich A, et al. (2007) Mutations in LRRK2/dardarin associated with Parkinson disease are more toxic than equivalent mutations in the homologous kinase LRRK1. J Neurochem 102: 93-102.
24. 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.
25. 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.
26. 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.
27. Korr D, Toschi L, Donner P, Pohlenz HD, Kreft B, et al. (2006) LRRK1 protein kinase activity is stimulated upon binding of GTP to its Roc domain. Cell Signal 18: 910-920.
28. Haugarvoll K, Toft M, Ross OA, White LR, Aasly JO, et al. (2007) Variants in the LRRK1 gene and susceptibility to Parkinson's disease in Norway. Neurosci Lett 416: 299-301.
29. Taylor JP, Hulihan MM, Kachergus JM, Melrose HL, Lincoln SJ, et al. (2007) Leucine-rich repeat kinase 1: a paralog of LRRK2 and a candidate gene for Parkinson's disease. Neurogenetics 8: 95-102.
30. Biskup S, Moore DJ, Rea A, Lorenz-Deperieux B, Coombes CE, et al. (2007) Dynamic and redundant regulation of LRRK2 and LRRK1 expression. BMC Neurosci 8: 102.
31. Westerlund M, Belin AC, Anvret A, Bickford P, Olson L, et al. (2008) Developmental regulation of leucine-rich repeat kinase 1 and 2 expression in the brain and other rodent and human organs: Implications for Parkinson's disease. Neuroscience 152: 429-436.
32. 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.
33. Delic S, Streif S, Deussing JM, Weber P, Ueffing M, et al. (2008) Genetic mouse models for behavioral analysis through transgenic RNAi technology. Genes Brain Behav 7: 821-830.
34. Bauer M, Kinkl N, Meixner A, Kremmer E, Riemenschneider M, et al. (2009) Prevention of interferon-stimulated gene expression using microRNA-designed hairpins. Gene Ther 16: 142-147.
35. Meixner A, Boldt K, Van Troys M, Askenazi M, Gloeckner CJ, et al. (2011) A QUICK screen for Lrrk2 interaction partners-leucine-rich repeat kinase 2 is involved in actin cytoskeleton dynamics. Mol Cell Proteomics 10: M110 001172.
36. Piccoli G, Condliffe SB, Bauer M, Giesert F, Boldt K, et al. (2011) LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. J Neurosci 31: 2225-2237.
37. Dagerlind A, Friberg K, Bean AJ, Hokfelt T, (1992) Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98: 39-49.
38. Lutz AK, Exner N, Fett ME, Schlehe JS, Kloos K, et al. (2009) Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J Biol Chem 284: 22938-22951.
39. Saura J, Tusell JM, Serratosa J, (2003) High-yield isolation of murine microglia by mild trypsinization. Glia 44: 183-189.
40. 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.
41. Galter D, Westerlund M, Carmine A, Lindqvist E, Sydow O, et al. (2006) LRRK2 expression linked to dopamine-innervated areas. Ann Neurol 59: 714-719.
42. Han BS, Iacovitti L, Katano T, Hattori N, Seol W, et al. (2008) Expression of the LRRK2 gene in the midbrain dopaminergic neurons of the substantia nigra. Neurosci Lett 442: 190-194.
43. Higashi S, Biskup S, West AB, Trinkaus D, Dawson VL, et al. (2007a) Localization of Parkinson's disease-associated LRRK2 in normal and pathological human brain. Brain Res 1155: 208-219.
44. Higashi S, Moore DJ, Colebrooke RE, Biskup S, Dawson VL, et al. (2007b) Expression and localization of Parkinson's disease-associated leucine-rich repeat kinase 2 in the mouse brain. J Neurochem 100: 368-381.
45. Larsen K, Madsen LB, (2009) Sequence conservation between porcine and human LRRK2. Mol Biol Rep 36: 237-243.
46. Maekawa T, Kubo M, Yokoyama I, Ohta E, Obata F, (2010) Age-dependent and cell-population-restricted LRRK2 expression in normal mouse spleen. Biochem Biophys Res Commun 392: 431-435.
47. Mandemakers W, Snellinx A, O'Neill MJ, de Strooper B (2012) LRRK2 expression is enriched in the striosomal compartment of mouse striatum. Neurobiol Dis.
48. Melrose H, Lincoln S, Tyndall G, Dickson D, Farrer M, (2006) Anatomical localization of leucine-rich repeat kinase 2 in mouse brain. Neuroscience 139: 791-794.
49. Melrose HL, Kent CB, Taylor JP, Dachsel JC, Hinkle KM, et al. (2007) A comparative analysis of leucine-rich repeat kinase 2 (Lrrk2) expression in mouse brain and Lewy body disease. Neuroscience 147: 1047-1058.
50. Miklossy J, Arai T, Guo JP, Klegeris A, Yu S, et al. (2006) LRRK2 expression in normal and pathologic human brain and in human cell lines. J Neuropathol Exp Neurol 65: 953-963.
51. Sharma S, Bandopadhyay R, Lashley T, Renton AE, Kingsbury AE, et al. (2011) LRRK2 expression in idiopathic and G2019S positive Parkinson's disease subjects: a morphological and quantitative study. Neuropathol Appl Neurobiol 37: 777-790.
52. Simon-Sanchez J, Herranz-Perez V, Olucha-Bordonau F, Perez-Tur J, (2006) LRRK2 is expressed in areas affected by Parkinson's disease in the adult mouse brain. Eur J Neurosci 23: 659-666.
53. Taymans JM, Van den Haute C, Baekelandt V, (2006) Distribution of PINK1 and LRRK2 in rat and mouse brain. J Neurochem 98: 951-961.
54. Zechel S, Meinhardt A, Unsicker K, von Bohlen Und Halbach O, (2010) Expression of leucine-rich-repeat-kinase 2 (LRRK2) during embryonic development. Int J Dev Neurosci 28: 391-399.
55. Kawamura K, Kouki T, Kawahara G, Kikuyama S, (2002) Hypophyseal development in vertebrates from amphibians to mammals. Gen Comp Endocrinol 126: 130-135.
56. Hinkle KM, Yue M, Behrouz B, Dachsel JC, Lincoln SJ, et al. (2012) LRRK2 knockout mice have an intact dopaminergic system but display alterations in exploratory and motor co-ordination behaviors. Mol Neurodegener 7: 25.
57. Li X, Patel JC, Wang J, Avshalumov MV, Nicholson C, et al. (2010) Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson's disease mutation G2019S. J Neurosci 30: 1788-1797.
58. Maekawa T, Mori S, Sasaki Y, Miyajima T, Azuma S, et al. (2012) The I2020T Leucine-rich repeat kinase 2 transgenic mouse exhibits impaired locomotive ability accompanied by dopaminergic neuron abnormalities. Mol Neurodegener 7: 15.
59. Tong Y, Yamaguchi H, Giaime E, Boyle S, Kopan R, et al. (2010) Loss of leucine-rich repeat kinase 2 causes impairment of protein degradation pathways, accumulation of alpha-synuclein, and apoptotic cell death in aged mice. Proc Natl Acad Sci U S A 107: 9879-9884.
60. Mensah PL, (1982) An electron microscopical study of neuronal cell clustering in postnatal mouse striatum, with special emphasis on neuronal cell death. Anat Embryol (Berl) 164: 387-401.
61. Ishikawa Y, Katoh H, Negishi M, (2003) A role of Rnd1 GTPase in dendritic spine formation in hippocampal neurons. J Neurosci 23: 11065-11072.
62. Tong Y, Pisani A, Martella G, Karouani M, Yamaguchi H, et al. (2009) R1441C mutation in LRRK2 impairs dopaminergic neurotransmission in mice. Proc Natl Acad Sci U S A 106: 14622-14627.
63. Melrose HL, Dachsel JC, Behrouz B, Lincoln SJ, Yue M, et al. (2010) Impaired dopaminergic neurotransmission and microtubule-associated protein tau alterations in human LRRK2 transgenic mice. Neurobiol Dis 40: 503-517.
64. Cho HJ, Liu G, Jin SM, Parisiadou L, Xie C, et al. (2012) MicroRNA-205 regulates the expression of Parkinson's disease-related leucine-rich repeat kinase 2 protein. Hum Mol Genet.
65. Moehle MS, Webber PJ, Tse T, Sukar N, Standaert DG, et al. (2012) LRRK2 inhibition attenuates microglial inflammatory responses. J Neurosci 32: 1602-1611.
66. Gillardon F, Schmid R, Draheim H, (2012) Parkinson's disease-linked leucine-rich repeat kinase 2(R1441G) mutation increases proinflammatory cytokine release from activated primary microglial cells and resultant neurotoxicity. Neuroscience 208: 41-48.
67. Kim B, Yang MS, Choi D, Kim JH, Kim HS, et al. (2012) Impaired inflammatory responses in murine Lrrk2-knockdown brain microglia. PLoS One 7: e34693.
68. Gerfen CR, Surmeier DJ, (2011) Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34: 441-466.
69. 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.
70. Hatano T, Kubo S, Imai S, Maeda M, Ishikawa K, et al. (2007) Leucine-rich repeat kinase 2 associates with lipid rafts. Hum Mol Genet 16: 678-690.
71. 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.
72. Lewis PA, Manzoni C, (2012) LRRK2 and human disease: a complicated question or a question of complexes? Sci Signal 5: pe2.
73. Lesage S, Condroyer C, Lannuzel A, Lohmann E, Troiano A, et al. (2009) Molecular analyses of the LRRK2 gene in European and North African autosomal dominant Parkinson's disease. J Med Genet 46: 458-464.
74. Jorgensen ND, Peng Y, Ho CC, Rideout HJ, Petrey D, et al. (2009) The WD40 domain is required for LRRK2 neurotoxicity. PLoS One 4: e8463.
75. Klein CL, Rovelli G, Springer W, Schall C, Gasser T, et al. (2009) Homo- and heterodimerization of ROCO kinases: LRRK2 kinase inhibition by the LRRK2 ROCO fragment. J Neurochem 111: 703-715.