LRRK2 Affects Vesicle Trafficking, Neurotransmitter Extracellular Level and Membrane Receptor Localization

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Migheli, Rossana ^a   Del Giudice, Maria Grazia ^a   Spissu, Ylenia ^a   Sanna, Giovanna ^a   Xiong, Yulan ^b   Dawson, Ted M ^b   Dawson, Valina L ^b   Galioto, Manuela ^a   Rocchitta, Gaia ^a   Biosa, Alice ^a   Serra, Pier Andrea ^a   Carri, Maria Teresa ^c,d   Crosio, Claudia ^a,c   Iaccarino, Ciro ^a,c  

^a UNIVERSITY OF SASSARI   (Italy)

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

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE 1 RECEPTOR; LEUCINE RICH REPEAT KINASE 2; MEMBRANE RECEPTOR; NEUROTRANSMITTER; LRRK2 PROTEIN, HUMAN; LRRK2 PROTEIN, MOUSE; LRRK2 PROTEIN, RAT; PROTEIN SERINE THREONINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; IN VITRO STUDY; MICRODIALYSIS; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; AMINO ACID SUBSTITUTION; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; NERVE CELL; PARKINSON DISEASE; PATHOLOGY; PC12 CELL LINE; PROTEIN TRANSPORT; RAT;

AMINO ACID SUBSTITUTION; ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; HUMANS; MICE; MUTATION, MISSENSE; NEURONS; PARKINSON DISEASE; PC12 CELLS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RATS; RECEPTORS, DOPAMINE D1;

EID: 84885989906     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077198     Document Type: Article

References (55)

1. Biskup S, Gerlach M, Kupsch A, Reichmann H, Riederer P, et al. (2008) Genes associated with Parkinson syndrome. J Neurol 255Suppl 5: 8-17.
2. 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.
3. 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.
4. Marin I, van Egmond WN, van Haastert PJ, (2008) The Roco protein family: a functional perspective. Faseb J 22: 3103-3110.
5. 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.
6. 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.
7. 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.
8. Greggio E, Cookson MR (2009) Leucine-rich repeat kinase 2 mutations and Parkinson's disease: three questions. ASN Neuro 1.
9. Bonifati V, (2006) The pleomorphic pathology of inherited Parkinson's disease: lessons from LRRK2. Curr Neurol Neurosci Rep 6: 355-357.
10. Gehrke S, Imai Y, Sokol N, Lu B, (2010) Pathogenic LRRK2 negatively regulates microRNA-mediated translational repression. Nature 466: 637-641.
11. 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.
12. Parisiadou L, Xie C, Cho HJ, Lin X, Gu XL, et al. (2009) Phosphorylation of ezrin/radixin/moesin proteins by LRRK2 promotes the rearrangement of actin cytoskeleton in neuronal morphogenesis. J Neurosci 29: 13971-13980.
13. 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.
14. 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.
15. Tong Y, Giaime E, Yamaguchi H, Ichimura T, Liu Y, et al. (2012) Loss of leucine-rich repeat kinase 2 causes age-dependent bi-phasic alterations of the autophagy pathway. Mol Neurodegener 7: 2.
16. 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.
17. Liu Z, Lee J, Krummey S, Lu W, Cai H, et al. (2011) The kinase LRRK2 is a regulator of the transcription factor NFAT that modulates the severity of inflammatory bowel disease. Nat Immunol 12: 1063-1070.
18. Sanna G, Del Giudice MG, Crosio C, Iaccarino C, (2012) LRRK2 and vesicle trafficking. Biochem Soc Trans 40: 1117-1122.
19. 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.
20. 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.
21. Li Y, Liu W, Oo TF, Wang L, Tang Y, et al. (2009) Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson's disease. Nat Neurosci 12: 826-828.
22. 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.
23. Zhou H, Huang C, Tong J, Hong WC, Liu YJ, et al. (2011) Temporal expression of mutant LRRK2 in adult rats impairs dopamine reuptake. Int J Biol Sci 7: 753-761.
24. 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.
25. Shin N, Jeong H, Kwon J, Heo HY, Kwon JJ, et al. (2008) LRRK2 regulates synaptic vesicle endocytosis. Exp Cell Res 314: 2055-2065.
26. Iaccarino C, Crosio C, Vitale C, Sanna G, Carri MT, et al. (2007) Apoptotic mechanisms in mutant LRRK2-mediated cell death. Hum Mol Genet 16: 1319-1326.
27. Migheli R, Godani C, Sciola L, Delogu MR, Serra PA, et al. (1999) Enhancing effect of manganese on L-DOPA-induced apoptosis in PC12 cells: role of oxidative stress. J Neurochem 73: 1155-1163.
28. Serra PA, Migheli R, Rocchitta G, Taras MG, Mura MP, et al. (2003) Role of the nitric oxide/cyclic GMP pathway and ascorbic acid in 3-morpholinosydnonimine (SIN-1)-induced increases in dopamine secretion from PC12 cells. A microdialysis in vitro study. Neurosci Lett 353: 5-8.
29. Migheli R, Puggioni G, Dedola S, Rocchitta G, Calia G, et al. (2008) Novel integrated microdialysis-amperometric system for in vitro detection of dopamine secreted from PC12 cells: design, construction, and validation. Anal Biochem 380: 323-330.
30. Serra PA, Rocchitta G, Delogu MR, Migheli R, Taras MG, et al. (2003) Role of the nitric oxide/cyclic GMP pathway and extracellular environment in the nitric oxide donor-induced increase in dopamine secretion from PC12 cells: a microdialysis in vitro study. J Neurochem 86: 1403-1413.
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. Iaccarino C, Mura ME, Esposito S, Carta F, Sanna G, et al. (2011) Bcl2-A1 interacts with pro-caspase-3: implications for amyotrophic lateral sclerosis. Neurobiol Dis 43: 642-650.
33. Bradberry CW, Sprouse JS, Sheldon PW, Aghajanian GK, Roth RH, (1991) In vitro microdialysis: a novel technique for stimulated neurotransmitter release measurements. J Neurosci Methods 36: 85-90.
34. Wick PF, Senter RA, Parsels LA, Uhler MD, Holz RW, (1993) Transient transfection studies of secretion in bovine chromaffin cells and PC12 cells. Generation of kainate-sensitive chromaffin cells. J Biol Chem 268: 10983-10989.
35. Lee HW, Park JW, Sandagsuren EU, Kim KB, Yoo JJ, et al. (2008) Overexpression of APP stimulates basal and constitutive exocytosis in PC12 cells. Neurosci Lett 436: 245-249.
36. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG, (1998) Dopamine receptors: from structure to function. Physiol Rev 78: 189-225.
37. Esposito G, Ana Clara F, Verstreken P, (2012) Synaptic vesicle trafficking and Parkinson's disease. Dev Neurobiol 72: 134-144.
38. Ghijsen WE, Leenders AG, (2005) Differential signaling in presynaptic neurotransmitter release. Cell Mol Life Sci 62: 937-954.
39. Buckley KM, Melikian HE, Provoda CJ, Waring MT, (2000) Regulation of neuronal function by protein trafficking: a role for the endosomal pathway. J Physiol 525 Pt 1: 11-19.
40. Martin TF, Grishanin RN, (2003) PC12 cells as a model for studies of regulated secretion in neuronal and endocrine cells. Methods Cell Biol 71: 267-286.
41. Markey KA, Kondo H, Shenkman L, Goldstein M, (1980) Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol Pharmacol 17: 79-85.
42. Roda LG, Nolan JA, Kim SU, Hogue-Angeletti RA, (1980) Isolation and characterization of chromaffin granules from a pheochromocytoma (PC 12) cell line. Exp Cell Res 128: 103-109.
43. Finberg JP, Youdim MB, (1983) Selective MAO A and B inhibitors: their mechanism of action and pharmacology. Neuropharmacology 22: 441-446.
44. Fujita K, Lazarovici P, Guroff G, (1989) Regulation of the differentiation of PC12 pheochromocytoma cells. Environ Health Perspect 80: 127-142.
45. 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.
46. Heo HY, Kim KS, Seol W, (2010) Coordinate Regulation of Neurite Outgrowth by LRRK2 and Its Interactor, Rab5. Exp Neurobiol 19: 97-105.
47. Rizzoli SO, Betz WJ, (2005) Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
48. Rizzoli SO, Betz WJ, (2004) The structural organization of the readily releasable pool of synaptic vesicles. Science 303: 2037-2039.
49. Matta S, Van Kolen K, da Cunha R, van den Bogaart G, Mandemakers W, et al. (2012) LRRK2 Controls an EndoA Phosphorylation Cycle in Synaptic Endocytosis. Neuron 75: 1008-1021.
50. Groc L, Choquet D, (2006) AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res 326: 423-438.
51. Kotowski SJ, Hopf FW, Seif T, Bonci A, von Zastrow M, (2011) Endocytosis promotes rapid dopaminergic signaling. Neuron 71: 278-290.
52. Kawakami F, Yabata T, Ohta E, Maekawa T, Shimada N, et al. (2012) LRRK2 phosphorylates tubulin-associated tau but not the free molecule: LRRK2-mediated regulation of the tau-tubulin association and neurite outgrowth. PLoS One 7: e30834.
53. Schapira AH, Jenner P, (2011) Etiology and pathogenesis of Parkinson's disease. Mov Disord 26: 1049-1055.
54. Jiang Y, Pei L, Li S, Wang M, Liu F, (2008) Extracellular dopamine induces the oxidative toxicity of SH-SY5Y cells. Synapse 62: 797-803.
55. Stokes AH, Lewis DY, Lash LH, Jerome WG 3rd, Grant KW, et al. (2000) Dopamine toxicity in neuroblastoma cells: role of glutathione depletion by L-BSO and apoptosis. Brain Res 858: 1-8.