Parvalbumin deficiency and GABAergic dysfunction in mice lacking PGC-1α

Journal of Neuroscience

Volumn 30, Issue 21, 2010, Pages 7227-7235

  Lucas, Elizabeth K ^a   Markwardt, Sean J ^b   Gupta, Swati ^b   Meador Woodruff, James H ^c   Lin, Jiandie D ^d   Overstreet Wadiche, Linda ^b   Cowell, Rita M ^c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN; PARVALBUMIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; GABAERGIC TRANSMISSION; GENE EXPRESSION; GENE FUNCTION; HEART; INTERNEURON; MALE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN TARGETING; RETINA; STIMULATION; SYNAPTIC INHIBITION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CELLS, CULTURED; DNA-BINDING PROTEINS; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; GTP PHOSPHOHYDROLASES; HEART; HIGH MOBILITY GROUP PROTEINS; HIPPOCAMPUS; HUMANS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RNA, MESSENGER; SHAW POTASSIUM CHANNELS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 77953074436     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0698-10.2010     Document Type: Article

References (49)

1. Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45-56. (Pubitemid 46011998)
2. Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci U S A 97:13372-13377.
3. Celio MR, Heizmann CW (1982) Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres. Nature 297:504-506.
4. Chard PS, Bleakman D, Christakos S, Fullmer CS, Miller RJ (1993) Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol 472:341-357. (Pubitemid 24015009)
5. Chaturvedi RK, Adhihetty P, Shukla S, Hennessy T, Calingasan N, Yang L, Starkov A, Kiaei M, Cannella M, Sassone J, Ciammola A, Squitieri F, Beal MF (2009) Impaired PGC-1alpha function in muscle in Huntington's disease. Hum Mol Genet 18:3048-3065.
6. Chen G, Racay P, Bichet S, Celio MR, Eggli P, Schwaller B (2006) Deficiency in parvalbumin, but not in calbindin D-28k upregulates mitochondrial volume and decreases smooth endoplasmic reticulum surface selectively in a peripheral, subplasmalemmal region in the soma of Purkinje cells. Neuroscience 142:97-105. (Pubitemid 44354986)
7. Chow A, Erisir A, Farb C, Nadal MS, Ozaita A, Lau D, Welker E, Rudy B (1999) K+ channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J Neurosci 19:9332-9345. (Pubitemid 30228087)
8. 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.
9. 2+ signaling. J Neurosci 25:96-107.
10. 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.
11. Cowell RM, Talati P, Blake KR, Meador-Woodruff JH, Russell JW (2009) Identification of novel targets for PGC-1alpha and histone deacetylase inhibitors in neuroblastoma cells. Biochem Biophys Res Commun 379:578-582.
12. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, Krainc D (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127:59-69. (Pubitemid 44466642)
13. Danglot L, Triller A, Marty S (2006) The development of hippocampal interneurons in rodents. Hippocampus 16:1032-1060.
14. Di Cristo G (2007) Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders. Clin Genet 72:1-8.
15. Giampà C, Middei S, Patassini S, Borreca A, Marullo F, Laurenti D, Bernardi G, Ammassari-Teule M, Fusco FR (2009) Phosphodiesterase type IV inhibition prevents sequestration of CREB binding protein, protects striatal parvalbumin interneurons and rescues motor deficits in the R6/2 mouse model of Huntington's disease. Eur J Neurosci 29:902-910.
16. Gu X, Li C, Wei W, Lo V, Gong S, Li SH, Iwasato T, Itohara S, Li XJ, Mody I, Heintz N, Yang XW (2005) Pathological cell-cell interactions elicited by a neuropathogenic form of mutant Huntingtin contribute to cortical pathogenesis in HD mice. Neuron 46:433-444.
17. Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD (2004) Calcium and mitochondria. FEBS Lett 567:96-102.
18. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319-1328. (Pubitemid 41630419)
19. Heizmann CW, Berchtold MW, Rowlerson AM (1982) Correlation of parvalbumin concentration with relaxation speed in mammalian muscles. Proc Natl Acad Sci U S A 79:7243-7247.
20. Kosinski CM, Cha JH, Young AB, Mangiarini L, Bates G, Schiefer J, Schwarz M (1999) Intranuclear inclusions in subtypes of striatal neurons in Huntington's disease transgenic mice. Neuroreport 10:3891-3896. (Pubitemid 30004852)
21. Lee SH, Schwaller B, Neher E (2000) Kinetics of Ca2+ binding to parvalbumin in bovine chromaffin cells: implications for [Ca2+] transients of neuronal dendrites. J Physiol 525:419-432.
22. Leone TC, Lehman JJ, Finck BN, Schaeffer PJ, Wende AR, Boudina S, Courtois M, Wozniak DF, Sambandam N, Bernal-Mizrachi C, Chen Z, Holloszy JO, Medeiros DM, Schmidt RE, Saffitz JE, Abel ED, Semenkovich CF, Kelly DP (2005) PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 3:e101.
23. Lewis DA, González-Burgos G (2008) Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology 33:141-165.
24. Liang HL, Wong-Riley MT (2006) Activity-dependent regulation of nuclear respiratory factor-1, nuclear respiratory factor-2, and peroxisome proliferator-activated receptor gamma coactivator-1 in neurons. Neuroreport 17: 401-405.
25. Liang HL, Dhar SS, Wong-Riley MT (2010) p38 mitogen-activated protein kinase and calcium channels mediate signaling in depolarization-induced activation of peroxisome proliferator-activated receptor gamma coactivator-1alpha in neurons. J Neurosci Res 88:640-649.
26. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slowtwitch muscle fibres. Nature 418:797-801.
27. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jäger S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, et al. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119:121-135.
28. Lin J, Handschin C, Spiegelman BM (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1:361-370. (Pubitemid 43960626)
29. Luo Y, Zhu W, Jia J, Zhang C, Xu Y (2009) NMDA receptor dependent PGC-1alpha up-regulation protects the cortical neuron against oxygen-glucose deprivation/reperfusion injury. J Mol Neurosci 39:262-268.
30. Luthi-Carter R, Hanson SA, Strand AD, Bergstrom DA, Chun W, Peters NL, Woods AM, Chan EY, Kooperberg C, Krainc D, Young AB, Tapscott SJ, Olson JM (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.
31. Maetzler W, Nitsch C, Bendfeldt K, Racay P, Vollenweider F, Schwaller B (2004) Ectopic parvalbumin expression in mouse forebrain neurons increases excitotoxic injury provoked by ibotenic acid injection into the striatum. Exp Neurol 186:78-88. (Pubitemid 38229907)
32. Marin O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076. (Pubitemid 30658400)
33. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
34. Marmolino D, Acquaviva F (2009) Friedreich's ataxia: from the (GAA)n repeat mediated silencing to new promising molecules for therapy. Cerebellum 8:245-259.
35. Meade CA, Deng YP, Fusco FR, Del Mar N, Hersch S, Goldowitz D, Reiner A (2002) Cellular localization and development of neuronal intranuclear inclusions in striatal and cortical neurons in R6/2 transgenic mice. J Comp Neurol 449:241-269. (Pubitemid 34734283)
36. Meng H, Liang HL, Wong-Riley M (2007) Quantitative immuno-electron microscopic analysis of depolarization-induced expression of PGC-1alpha in cultured rat visual cortical neurons. Brain Res 1175:10-16. (Pubitemid 47513012)
37. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839. (Pubitemid 28155321)
38. Qin W, Haroutunian V, Katsel P, Cardozo CP, Ho L, Buxbaum JD, Pasinetti GM (2009) PGC-1alpha expression decreases in the Alzheimer disease brain as a function of dementia. Arch Neurol 66:352-361.
39. Rudy B, McBain CJ (2001) Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci 24:517-526. (Pubitemid 32744706)
40. Spampanato J, Gu X, Yang XW, Mody I (2008) Progressive synaptic pathology of motor cortical neurons in a BAC transgenic mouse model of Huntington's disease. Neuroscience 157:606-620.
41. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jäger S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408.
42. Vongvatcharanon S, Vongvatcharanon U, Boonyoung P (2008) Immuno-histochemical localization of parvalbumin calcium-binding protein in the heart tissues of various species. Acta Histochem 110:26-33.
43. Vreugdenhil M, Jefferys JG, Celio MR, Schwaller B (2003) Parvalbumindeficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J Neurophysiol 89:1414-1422.
44. Wareski P, Vaarmann A, Choubey V, Safiulina D, Liiv J, Kuum M, Kaasik A (2009) PGC-1{alpha} and PGC-1{beta} regulate mitochondrial density in neurons. J Biol Chem 284:21379-21385.
45. Wässle H, Grünert U, Röhrenbeck J (1993) Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin. J Comp Neurol 332:407-420.
46. Weydt P, Pineda VV, Torrence AE, Libby RT, Satterfield TF, Lazarowski ER, Gilbert ML, Morton GJ, Bammler TK, Strand AD, Cui L, Beyer RP, Easley CN, Smith AC, Krainc D, Luquet S, Sweet IR, Schwartz MW, La Spada AR (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab 4:349-362.
47. Wonders CP, Anderson SA (2006) The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687-696.
48. Wright DC, Geiger PC, Han DH, Jones TE, Holloszy JO (2007) Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 282:18793-18799.
49. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296:349-352.