Rgs6 is Required for Adult Maintenance of Dopaminergic Neurons in the Ventral Substantia Nigra

PLoS Genetics

Volumn 10, Issue 12, 2014, Pages

  Bifsha, Panojot ^a,b   Yang, Jianqi ^c   Fisher, Rory A ^c   Drouin, Jacques ^a,b  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE TRANSPORTER; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; REGULATOR OF G PROTEIN SIGNALING 6; RGS PROTEIN; TRANSCRIPTION FACTOR PITX3; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; RGS6 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

AGED; ALDH1A1 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BDNF GENE; CELL LOSS; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; DOPAMINERGIC NERVE CELL; FGF10 GENE; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENE PRODUCT; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; VENTRAL SUBSTANTIA NIGRA COMPACTA; VMAT2 GENE; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PARKINSON DISEASE; PATHOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; DOPAMINERGIC NEURONS; HOMEODOMAIN PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SPECIFICITY; PARKINSON DISEASE; RGS PROTEINS; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; TRANSCRIPTION FACTORS;

EID: 84919682713     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004863     Document Type: Article

References (52)

1. Jellinger KA, (2012) Neuropathology of sporadic Parkinson's disease: evaluation and changes of concepts. Mov Disord 27: 8–30.
2. Gonzalez-Hernandez T, Cruz-Muros I, Afonso-Oramas D, Salas-Hernandez J, Castro-Hernandez J, (2010) Vulnerability of mesostriatal dopaminergic neurons in Parkinson's disease. Front Neuroanat 4: 140.
3. Obeso JA, Rodriguez-Oroz MC, Goetz CG, Marin C, Kordower JH, et al. (2010) Missing pieces in the Parkinson's disease puzzle. Nat Med 16: 653–661.
4. Dawson TM, Ko HS, Dawson VL, (2010) Genetic animal models of Parkinson's disease. Neuron 66: 646–661.
5. Westerlund M, Hoffer B, Olson L, (2010) Parkinson's disease: Exit toxins, enter genetics. Prog Neurobiol 90: 146–156.
6. 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.
7. Rousseaux MW, Marcogliese PC, Qu D, Hewitt SJ, Seang S, et al. (2012) Progressive dopaminergic cell loss with unilateral-to-bilateral progression in a genetic model of Parkinson disease. Proc Natl Acad Sci U S A 109: 15918–15923.
8. Dave KD, De Silva S, Sheth NP, Ramboz S, Beck MJ, et al. (2014) Phenotypic characterization of recessive gene knockout rat models of Parkinson's disease. Neurobiol Dis 70: 190–203.
9. Liss B, Neu A, Roeper J, (1999) The weaver mouse gain-of-function phenotype of dopaminergic midbrain neurons is determined by coactivation of wvGirk2 and K-ATP channels. J Neurosci 19: 8839–8848.
10. Smits SM, Burbach JP, Smidt MP, (2006) Developmental origin and fate of meso-diencephalic dopamine neurons. Prog Neurobiol 78: 1–16.
11. Simeone A, Di Salvio M, Di Giovannantonio LG, Acampora D, Omodei D, Tomasetti C, (2011) The role of otx2 in adult mesencephalic-diencephalic dopaminergic neurons. Mol Neurobiol 43: 107–113.
12. van den Munckhof P, Luk KC, Sainte-Marie L, Montgomery J, Blanchet PJ, et al. (2003) Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development 130: 2535–2542.
13. Hwang DY, Ardayfio P, Kang UJ, Semina EV, Kim KS, (2003) Selective loss of dopaminergic neurons in the substantia nigra of Pitx3-deficient aphakia mice. Brain Res Mol Brain Res 114: 123–131.
14. Nunes I, Tovmasian LT, Silva RM, Burke RE, Goff SP, (2003) Pitx3 is required for development of substantia nigra dopaminergic neurons. Proc Natl Acad Sci USA 100: 4245–4250.
15. Luk KC, Rymar VV, van den Munckhof P, Nicolau S, Steriade C, et al. (2013) The transcription factor Pitx3 is expressed selectively in midbrain dopaminergic neurons susceptible to neurodegenerative stress. J Neurochem 125: 932–943.
16. van den Munckhof P, Gilbert F, Chamberland M, Lévesque D, Drouin J, (2006) Striatal neuroadaptation and rescue of locomotor deficit by L-dopa in aphakia mice, a model of Parkinson's disease. J Neurochem 96: 160–170.
17. Hwang DY, Fleming SM, Ardayfio P, Moran-Gates T, Kim H, et al. (2005) 3,4-dihydroxyphenylalanine reverses the motor deficits in Pitx3-deficient aphakia mice: behavioral characterization of a novel genetic model of Parkinson's disease. J Neurosci 25: 2132–2137.
18. Fuchs J, Mueller JC, Lichtner P, Schulte C, Munz M, et al. (2007) The transcription factor PITX3 is associated with sporadic Parkinson's disease. Neurobiol Aging 30: 731–8.
19. Jacobs FM, Veenvliet JV, Almirza WH, Hoekstra EJ, von Oerthel L, et al. (2011) Retinoic acid-dependent and -independent gene-regulatory pathways of Pitx3 in meso-diencephalic dopaminergic neurons. Development 138: 5213–5222.
20. Jacobs FM, Smits SM, Noorlander CW, von Oerthel L, van der Linden AJ, et al. (2007) Retinoic acid counteracts developmental defects in the substantia nigra caused by Pitx3 deficiency. Development 134: 2673–2684.
21. Liu G, Yu J, Ding J, Xie C, Sun L, et al. (2014) Aldehyde dehydrogenase 1 defines and protects a nigrostriatal dopaminergic neuron subpopulation. J Clin Invest 124: 3032–3046.
22. Jacobs FM, van Erp S, van der Linden AJ, von Oerthel L, Burbach JP, et al. (2009) Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 136: 531–540.
23. Peng C, Aron L, Klein R, Li M, Wurst W, et al. (2011) Pitx3 is a critical mediator of GDNF-induced BDNF expression in nigrostriatal dopaminergic neurons. J Neurosci 31: 12802–12815.
24. Pascual A, Hidalgo-Figueroa M, Piruat JI, Pintado CO, Gomez-Diaz R, et al. (2008) Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat Neurosci 11: 755–761.
25. Anderson GR, Posokhova E, Martemyanov KA, (2009) The R7 RGS protein family: multi-subunit regulators of neuronal G protein signaling. Cell Biochem Biophys 54: 33–46.
26. Yang J, Huang J, Maity B, Gao Z, Lorca RA, et al. (2010) RGS6, a modulator of parasympathetic activation in heart. Circ Res 107: 1345–1349.
27. Posokhova E, Wydeven N, Allen KL, Wickman K, Martemyanov KA, (2010) RGS6/Gbeta5 complex accelerates IKACh gating kinetics in atrial myocytes and modulates parasympathetic regulation of heart rate. Circ Res 107: 1350–1354.
28. Maity B, Stewart A, Yang J, Loo L, Sheff D, et al. (2012) Regulator of G protein signaling 6 (RGS6) protein ensures coordination of motor movement by modulating GABAB receptor signaling. J Biol Chem 287: 4972–4981.
29. Stewart A, Maity B, Wunsch AM, Meng F, Wu Q, et al. (2014) Regulator of G-protein signaling 6 (RGS6) promotes anxiety and depression by attenuating serotonin-mediated activation of the 5-HT1A receptor-adenylyl cyclase axis. FASEB J 28: 1735–1744.
30. Fu Y, Yuan Y, Halliday G, Rusznak Z, Watson C, et al. (2012) A cytoarchitectonic and chemoarchitectonic analysis of the dopamine cell groups in the substantia nigra, ventral tegmental area, and retrorubral field in the mouse. Brain Struct Funct 217: 591–612.
31. Di Salvio M, Di Giovannantonio LG, Acampora D, Prosperi R, Omodei D, et al. (2010) Otx2 controls neuron subtype identity in ventral tegmental area and antagonizes vulnerability to MPTP. Nat Neurosci 13: 1481–1488.
32. Moeller C, Yaylaoglu MB, Alvarez-Bolado G, Thaller C, Eichele G, (2002) Murine Lix1, a novel marker for substantia nigra, cortical layer 5, and hindbrain structures. Brain Res Gene Expr Patterns 1: 199–203.
33. Bian GL, Wei LC, Shi M, Wang YQ, Cao R, et al. (2007) Fluoro-Jade C can specifically stain the degenerative neurons in the substantia nigra of the 1-methyl-4-phenyl-1,2,3,6-tetrahydro pyridine-treated C57BL/6 mice. Brain Res 1150: 55–61.
34. Ehara A, Ueda S, (2009) Application of Fluoro-Jade C in acute and chronic neurodegeneration models: utilities and staining differences. Acta Histochem Cytochem 42: 171–179.
35. Oliveras-Salva M, Van Rompuy AS, Heeman B, Van den HC, Baekelandt V, (2011) Loss-of-function rodent models for parkin and PINK1. J Parkinsons Dis 1: 229–251.
36. Xie Z, Zhuang X, Chen L, (2009) DJ-1 mRNA anatomical localization and cell type identification in the mouse brain. Neurosci Lett 465: 214–219.
37. Taymans JM, Van den HC, Baekelandt V, (2006) Distribution of PINK1 and LRRK2 in rat and mouse brain. J Neurochem 98: 951–961.
38. Ogawa O, Lee HG, Zhu X, Raina A, Harris PL, et al. (2003) Increased p27, an essential component of cell cycle control, in Alzheimer's disease. Aging Cell 2: 105–110.
39. Maity B, Yang J, Huang J, Askeland RW, Bera S, et al. (2011) Regulator of G protein signaling 6 (RGS6) induces apoptosis via a mitochondrial-dependent pathway not involving its GTPase-activating protein activity. J Biol Chem 286: 1409–1419.
40. Lebel M, Gauthier Y, Moreau A, Drouin J, (2001) Pitx3 activates mouse tyrosine hydroxylase promoter via a high affinity binding site. J Neurochem 76: 1–11.
41. Bolan EA, Kivell B, Jaligam V, Oz M, Jayanthi LD, et al. (2007) D2 receptors regulate dopamine transporter function via an extracellular signal-regulated kinases 1 and 2-dependent and phosphoinositide 3 kinase-independent mechanism. Mol Pharmacol 71: 1222–1232.
42. Sonders MS, Zhu SJ, Zahniser NR, Kavanaugh MP, Amara SG, (1997) Multiple ionic conductances of the human dopamine transporter: the actions of dopamine and psychostimulants. J Neurosci 17: 960–974.
43. Vaughan RA, Foster JD, (2013) Mechanisms of dopamine transporter regulation in normal and disease states. Trends Pharmacol Sci 34: 489–496.
44. Caudle WM, Richardson JR, Wang MZ, Taylor TN, Guillot TS, et al. (2007) Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J Neurosci 27: 8138–8148.
45. Lipski J, Nistico R, Berretta N, Guatteo E, Bernardi G, et al. (2011) L-DOPA: a scapegoat for accelerated neurodegeneration in Parkinson's disease? Prog Neurobiol 94: 389–407.
46. Grimm J, Mueller A, Hefti F, Rosenthal A, (2004) Molecular basis for catecholaminergic neuron diversity. Proc Natl Acad Sci U S A 101: 13891–13896.
47. Greene JG, Dingledine R, Greenamyre JT, (2005) Gene expression profiling of rat midbrain dopamine neurons: implications for selective vulnerability in parkinsonism. Neurobiol Dis 18: 19–31.
48. Chung CY, Seo H, Sonntag KC, Brooks A, Lin L, et al. (2005) Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. Hum Mol Genet 14: 1709–1725.
49. Melamed P, Koh M, Preklathan P, Bei L, Hew C, (2002) Multiple mechanisms for Pitx-1 transactivation of a luteinizing hormone beta subunit gene. J Biol Chem 277: 26200–26207.
50. Afonso-Oramas D, Cruz-Muros I, Alvarez dlR, Abreu P, Giraldez T, et al. (2009) Dopamine transporter glycosylation correlates with the vulnerability of midbrain dopaminergic cells in Parkinson's disease. Neurobiol Dis 36: 494–508.
51. Sawamoto K, Nakao N, Kobayashi K, Matsushita N, Takahashi H, et al. (2001) Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc Natl Acad Sci USA 98: 6423–6428.
52. L'Honoré A, Coulon V, Marcil A, Lebel M, Lafrance-Vanasse J, et al. (2007) Sequential expression and redundancy of Pitx2 and Pitx3 genes during muscle development. Dev Biol 307: 421–433.