Developmental alterations in motor coordination and medium spiny neuron markers in mice lacking PGC-1α

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Lucas, Elizabeth K ^a,b   Dougherty, Sarah E ^b   McMeekin, Laura J ^b   Trinh, Alisa T ^b   Reid, Courtney S ^b   Cowell, Rita M ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; DOPAMINE; MU OPIATE RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL VACUOLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DISEASE ASSOCIATION; HINDLIMB; HUNTINGTON CHOREA; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOUSE; NERVE CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REARING; ROTAROD TEST; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL MARKERS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DOPAMINE; GENE EXPRESSION PROFILING; HUNTINGTON DISEASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PSYCHOMOTOR PERFORMANCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; ROTAROD PERFORMANCE TEST; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84865054287     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042878     Document Type: Article

References (61)

1. The Huntington Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
2. Cicchetti F, Prensa L, Wu Y, Parent A, (2000) Chemical anatomy of striatal interneurons in normal individuals and in patients with Huntington's disease. Brain Res Brain Res Rev 34: 80-101.
3. Walker FO, (2007) Huntington's Disease. Semin Neurol 27: 143-150.
4. Heng MY, Detloff PJ, Albin RL, (2008) Rodent genetic models of Huntington disease. Neurobiol Dis 32: 1-9.
5. Lin MT, Beal MF, (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795.
6. Bossy-Wetzel E, Petrilli A, Knott AB, (2008) Mutant huntingtin and mitochondrial dysfunction. Trends Neurosci 31: 609-616.
7. Cha JH, (2007) Transcriptional signatures in Huntington's disease. Prog Neurobiol 83: 228-248.
8. McGill JK, Beal MF, (2006) PGC-1alpha, a new therapeutic target in Huntington's disease? Cell 127: 465-468.
9. Tsunemi T, La Spada AR, (2011) PGC-1alpha at the intersection of bioenergetics regulation and neuron function: From Huntington's disease to Parkinson's disease and beyond. Prog Neurobiol.
10. Puigserver P, Wu Z, Park CW, Graves R, Wright M, et al. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839.
11. Lin J, Handschin C, Spiegelman BM, (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1: 361-370.
12. Wareski P, Vaarmann A, Choubey V, Safiulina D, Liiv J, et al. (2009) PGC-1{alpha} and PGC-1{beta} regulate mitochondrial density in neurons. J Biol Chem 284: 21379-21385.
13. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, et al. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119: 121-135.
14. Cowell RM, Blake KR, Russell JW, (2007) Localization of the transcriptional coactivator PGC-1alpha to GABAergic neurons during maturation of the rat brain. J Comp Neurol 502: 1-18.
15. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, et al. (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127: 59-69.
16. Weydt P, Pineda VV, Torrence AE, Libby RT, Satterfield TF, et al. (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab 4: 349-362.
17. Chaturvedi RK, Adhihetty P, Shukla S, Hennessy T, Calingasan N, et al. (2009) Impaired PGC-1alpha function in muscle in Huntington's disease. Hum Mol Genet 18: 3048-3065.
18. Kim J, Moody JP, Edgerly CK, Bordiuk OL, Cormier K, et al. (2010) Mitochondrial loss, dysfunction and altered dynamics in Huntington's disease. Hum Mol Genet 19: 3919-3935.
19. Taherzadeh-Fard E, Saft C, Andrich J, Wieczorek S, Arning L, (2009) PGC-1alpha as modifier of onset age in Huntington disease. Mol Neurodegener 4: 10.
20. Weydt P, Soyal SM, Gellera C, Didonato S, Weidinger C, et al. (2009) The gene coding for PGC-1alpha modifies age at onset in Huntington's Disease. Mol Neurodegener 4: 3.
21. Che HV, Metzger S, Portal E, Deyle C, Riess O, et al. (2011) Localization of sequence variations in PGC-1alpha influence their modifying effect in Huntington disease. Mol Neurodegener 6: 1.
22. Chaturvedi RK, Calingasan NY, Yang L, Hennessey T, Johri A, et al. (2010) Impairment of PGC-1alpha expression, neuropathology and hepatic steatosis in a transgenic mouse model of Huntington's disease following chronic energy deprivation. Hum Mol Genet 19: 3190-3205.
23. Lee ST, Chu K, Jung KH, Im WS, Park JE, et al. (2009) Slowed progression in models of Huntington disease by adipose stem cell transplantation. Ann Neurol 66: 671-681.
24. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, et al. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87: 493-506.
25. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, et al. (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19: 3248-3257.
26. Ma D, Li S, Lucas EK, Cowell RM, Lin JD, (2010) Neuronal inactivation of peroxisome proliferator-activated receptor gamma coactivator 1alpha (PGC-1alpha) protects mice from diet-induced obesity and leads to degenerative lesions. J Biol Chem 285: 39087-39095.
27. Gerfen CR, (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15: 285-320.
28. Bolam JP, Hanley JJ, Booth PA, Bevan MD, (2000) Synaptic organisation of the basal ganglia. J Anat 196 (Pt 4): 527-542.
29. Gerfen CR, Baimbridge KG, Miller JJ, (1985) The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci U S A 82: 8780-8784.
30. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, et al. (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250: 1429-1432.
31. Surmeier DJ, Song WJ, Yan Z, (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 16: 6579-6591.
32. Le Moine C, Normand E, Guitteny AF, Fouque B, Teoule R, et al. (1990) Dopamine receptor gene expression by enkephalin neurons in rat forebrain. Proc Natl Acad Sci U S A 87: 230-234.
33. Le Moine C, Normand E, Bloch B, (1991) Phenotypical characterization of the rat striatal neurons expressing the D1 dopamine receptor gene. Proc Natl Acad Sci U S A 88: 4205-4209.
34. Kita H, Kitai ST, (1988) Glutamate decarboxylase immunoreactive neurons in rat neostriatum: their morphological types and populations. Brain Res 447: 346-352.
35. Tepper JM, Tecuapetla F, Koos T, Ibanez-Sandoval O, (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4: 150.
36. Kubota Y, Mikawa S, Kawaguchi Y, (1993) Neostriatal GABAergic interneurones contain NOS, calretinin or parvalbumin. Neuroreport 5: 205-208.
37. Lucas EK, Markwardt SJ, Gupta S, Meador-Woodruff JH, Lin JD, et al. (2010) Parvalbumin deficiency and GABAergic dysfunction in mice lacking PGC-1alpha. J Neurosci 30: 7227-7235.
38. Zheng B, Liao Z, Locascio JJ, Lesniak KA, Roderick SS, et al. (2010) PGC-1alpha, a potential therapeutic target for early intervention in Parkinson's disease. Sci Transl Med 2: 52ra73.
39. Shin JH, Ko HS, Kang H, Lee Y, Lee YI, et al. (2011) PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 144: 689-702.
40. Stoof JC, Kebabian JW, (1981) Opposing roles for D-1 and D-2 dopamine receptors in efflux of cyclic AMP from rat neostriatum. Nature 294: 366-368.
41. Gerfen CR, McGinty JF, Young WS 3rd, (1991) Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. J Neurosci 11: 1016-1031.
42. Albin RL, Young AB, Penney JB, (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375.
43. Berardelli A, Noth J, Thompson PD, Bollen EL, Curra A, et al. (1999) Pathophysiology of chorea and bradykinesia in Huntington's disease. Mov Disord 14: 398-403.
44. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, et al. (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466: 622-626.
45. Guttenberg ND, Klop H, Minami M, Satoh M, Voorn P, (1996) Co-localization of mu opioid receptor is greater with dynorphin than enkephalin in rat striatum. Neuroreport 7: 2119-2124.
46. Bibb JA, Yan Z, Svenningsson P, Snyder GL, Pieribone VA, et al. (2000) Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice. Proc Natl Acad Sci U S A 97: 6809-6814.
47. Luthi-Carter R, Strand A, Peters NL, Solano SM, Hollingsworth ZR, et al. (2000) Decreased expression of striatal signaling genes in a mouse model of Huntington's disease. Hum Mol Genet 9: 1259-1271.
48. Menalled L, Zanjani H, MacKenzie L, Koppel A, Carpenter E, et al. (2000) Decrease in striatal enkephalin mRNA in mouse models of Huntington's disease. Exp Neurol 162: 328-342.
49. Sun Z, Del Mar N, Meade C, Goldowitz D, Reiner A, (2002) Differential changes in striatal projection neurons in R6/2 transgenic mice for Huntington's disease. Neurobiol Dis 11: 369-385.
50. Ariano MA, Aronin N, Difiglia M, Tagle DA, Sibley DR, et al. (2002) Striatal neurochemical changes in transgenic models of Huntington's disease. J Neurosci Res 68: 716-729.
51. Cipriani S, Bizzoco E, Gianfriddo M, Melani A, Vannucchi MG, et al. (2008) Adenosine A2A receptor antagonism increases nNOS-immunoreactive neurons in the striatum of Huntington transgenic mice. Exp Neurol 213: 163-170.
52. Luthi-Carter R, Hanson SA, Strand AD, Bergstrom DA, Chun W, et al. (2002) Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain. Hum Mol Genet 11: 1911-1926.
53. Smith R, Chung H, Rundquist S, Maat-Schieman ML, Colgan L, et al. (2006) Cholinergic neuronal defect without cell loss in Huntington's disease. Hum Mol Genet 15: 3119-3131.
54. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, et al. (2006) Regional and cellular gene expression changes in human Huntington's disease brain. Hum Mol Genet 15: 965-977.
55. Kuhn A, Goldstein DR, Hodges A, Strand AD, Sengstag T, et al. (2007) Mutant huntingtin's effects on striatal gene expression in mice recapitulate changes observed in human Huntington's disease brain and do not differ with mutant huntingtin length or wild-type huntingtin dosage. Hum Mol Genet 16: 1845-1861.
56. Turmaine M, Raza A, Mahal A, Mangiarini L, Bates GP, et al. (2000) Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc Natl Acad Sci U S A 97: 8093-8097.
57. Stack EC, Kubilus JK, Smith K, Cormier K, Del Signore SJ, et al. (2005) Chronology of behavioral symptoms and neuropathological sequela in R6/2 Huntington's disease transgenic mice. J Comp Neurol 490: 354-370.
58. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, et al. (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127: 397-408.
59. Taylor TN, Greene JG, Miller GW, (2010) Behavioral phenotyping of mouse models of Parkinson's disease. Behav Brain Res 211: 1-10.
60. Mudo G, Makela J, Liberto VD, Tselykh TV, Olivieri M, et al. (2012) Transgenic expression and activation of PGC-1alpha protect dopaminergic neurons in the MPTP mouse model of Parkinson's disease. Cell Mol Life Sci 69: 1153-1165.
61. Xiang Z, Valenza M, Cui L, Leoni V, Jeong HK, et al. (2011) Peroxisome-proliferator-activated receptor gamma coactivator 1 alpha contributes to dysmyelination in experimental models of Huntington's disease. J Neurosci 31: 9544-9553.