Rescuing the corticostriatal synaptic disconnection in the R6/2 mouse model of Huntington's Disease: Exercise, adenosine receptors and ampakines

PLoS Currents

Volumn , Issue SEP, 2010, Pages

  Cepeda, Carlos ^a   Cummings, Damian M ^a   Hickey, Miriam A ^a   Kleiman Weiner, Max ^b   Chen, Jane ^b   Watson, Joseph B ^b   Levine, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79958024146     PISSN: None     EISSN: 21573999     Source Type: Journal    
DOI: 10.1371/currents.RRN1182     Document Type: Article

References (46)

1. The Huntington's 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. Vonsattel JP, DiFiglia M (1998) Huntington disease. J Neuropathol Exp Neurol 57:369-384.
3. Bates G, Harper PS, Jones L (2002) Huntington's disease, 3rd Edition. Oxford; New York: Oxford University Press.
4. Levine MS, Cepeda C, Hickey MA, Fleming SM, Chesselet MF (2004) Genetic mouse models of Huntington's and Parkinson's diseases: illuminating but imperfect. Trends Neurosci 27:691-697.
5. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP (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.
6. Cepeda C, Wu N, André VM, Cummings DM, Levine MS (2007) The corticostriatal pathway in Huntington's disease. Prog Neuorbiol 81:253-271.
7. Cepeda C, Cummings DM, Andre VM, Holley SM, Levine MS (2010) Genetic mouse models of Huntington's disease: focus on electrophysiological mechanisms. ASN Neuro 2:e00033.
8. Klapstein GJ, Fisher RS, Zanjani H, Cepeda C, Jokel ES, Chesselet MF, Levine MS (2001) Electrophysiological and Morphological Changes in Striatal Spiny Neurons in R6/2 Huntington's Disease Transgenic Mice. J Neurophysiol 86:2667-2677.
9. Cepeda C, Hurst RS, Calvert CR, Hernandez-Echeagaray E, Nguyen OK, Jocoy E, Christian LJ, Ariano MA, Levine MS (2003) Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease. J Neurosci 23:961-969.
10. Joshi PR, Wu NP, Andre VM, Cummings DM, Cepeda C, Joyce JA, Carroll JB, Leavitt BR, Hayden MR, Levine MS, Bamford NS (2009) Age-dependent alterations of corticostriatal activity in the YAC128 mouse model of Huntington disease. J Neurosci 29:2414-2427.
11. Cummings DM, Andre VM, Uzgil BO, Gee SM, Fisher YE, Cepeda C, Levine MS (2009) Alterations in cortical excitation and inhibition in genetic mouse models of Huntington's disease. J Neurosci 29:10371-10386.
12. Pallier PN, Maywood ES, Zheng Z, Chesham JE, Inyushkin AN, Dyball R, Hastings MH, Morton AJ (2007) Pharmacological imposition of sleep slows cognitive decline and reverses dysregulation of circadian gene expression in a transgenic mouse model of Huntington's disease. J Neurosci 27:7869-7878.
13. Masuda N, Peng Q, Li Q, Jiang M, Liang Y, Wang X, Zhao M, Wang W, Ross CA, Duan W (2008) Tiagabine is neuroprotective in the N171-82Q and R6/2 mouse models of Huntington's disease. Neurobiol Dis 30:293-302.
14. Stack EC, Dedeoglu A, Smith KM, Cormier K, Kubilus JK, Bogdanov M, Matson WR, Yang L, Jenkins BG, Luthi-Carter R, Kowall NW, Hersch SM, Beal MF, Ferrante RJ (2007) Neuroprotective effects of synaptic modulation in Huntington's disease R6/2 mice. J Neurosci 27:12908-12915.
15. Levine MS, Klapstein GJ, Koppel A, Gruen E, Cepeda C, Vargas ME, Jokel ES, Carpenter EM, Zanjani H, Hurst RS, Efstratiadis A, Zeitlin S, Chesselet MF (1999) Enhanced sensitivity to N-methyl-D-aspartate receptor activation in transgenic and knockin mouse models of Huntington's disease. J Neurosci Res 58:515-532.
16. Cepeda C, Ariano MA, Calvert CR, Flores-Hernandez J, Chandler SH, Leavitt BR, Hayden MR, Levine MS (2001) NMDA receptor function in mouse models of Huntington disease. J Neurosci Res 66:525-539.
17. Okamoto S, Pouladi MA, Talantova M, Yao D, Xia P, Ehrnhoefer DE, Zaidi R, Clemente A, Kaul M, Graham RK, Zhang D, Vincent Chen HS, Tong G, Hayden MR, Lipton SA (2009) Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med 15:1407-1413.
18. Milnerwood AJ, Gladding CM, Pouladi MA, Kaufman AM, Hines RM, Boyd JD, Ko RW, Vasuta OC, Graham RK, Hayden MR, Murphy TH, Raymond LA (2010) Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 65:178-190.
19. Smith AD, Zigmond MJ (2003) Can the brain be protected through exercise? Lessons from an animal model of parkinsonism. Exp Neurol 184:31-39.
20. Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295-301.
21. Siegenthaler MM, Berchtold NC, Cotman CW, Keirstead HS (2008) Voluntary running attenuates age-related deficits following SCI. Exp Neurol 210:207-216.
22. van Praag H (2008) Neurogenesis and exercise: past and future directions. Neuromolecular Med 10:128-140.
23. van Dellen A, Blakemore C, Deacon R, York D, Hannan AJ (2000) Delaying the onset of Huntington's in mice. Nature 404:721-722.
24. Kase H, Aoyama S, Ichimura M, Ikeda K, Ishii A, Kanda T, Koga K, Koike N, Kurokawa M, Kuwana Y, Mori A, Nakamura J, Nonaka H, Ochi M, Saki M, Shimada J, Shindou T, Shiozaki S, Suzuki F, Takeda M, Yanagawa K, Richardson PJ, Jenner P, Bedard P, Borrelli E, Hauser RA, Chase TN (2003) Progress in pursuit of therapeutic A2A antagonists: the adenosine A2A receptor selective antagonist KW6002: research and development toward a novel nondopaminergic therapy for Parkinson's disease. Neurology 61:S97-100.
25. Pinna A (2009) Novel investigational adenosine A2A receptor antagonists for Parkinson's disease. Expert Opin Investig Drugs 18:1619-1631.
26. Tarditi A, Camurri A, Varani K, Borea PA, Woodman B, Bates G, Cattaneo E, Abbracchio MP (2006) Early and transient alteration of adenosine A2A receptor signaling in a mouse model of Huntington disease. Neurobiol Dis 23:44-53.
27. Martire A, Calamandrei G, Felici F, Scattoni ML, Lastoria G, Domenici MR, Tebano MT, Popoli P (2007) Opposite effects of the A2A receptor agonist CGS21680 in the striatum of Huntington's disease versus wild-type mice. Neurosci Lett 417:78-83.
28. Chou SY, Lee YC, Chen HM, Chiang MC, Lai HL, Chang HH, Wu YC, Sun CN, Chien CL, Lin YS, Wang SC, Tung YY, Chang C, Chern Y (2005) CGS21680 attenuates symptoms of Huntington's disease in a transgenic mouse model. J Neurochem 93:310-320.
29. Domenici MR, Scattoni ML, Martire A, Lastoria G, Potenza RL, Borioni A, Venerosi A, Calamandrei G, Popoli P (2007) Behavioral and electrophysiological effects of the adenosine A2A receptor antagonist SCH 58261 in R6/2 Huntington's disease mice. Neurobiol Dis 28:197-205.
30. Jin R, Clark S, Weeks AM, Dudman JT, Gouaux E, Partin KM (2005) Mechanism of positive allosteric modulators acting on AMPA receptors. J Neurosci 25:9027-9036.
31. Lynch G (2006) Glutamate-based therapeutic approaches: ampakines. Curr Opin Pharmacol 6:82-88.
32. Lauterborn JC, Truong GS, Baudry M, Bi X, Lynch G, Gall CM (2003) Chronic elevation of brain-derived neurotrophic factor by ampakines. J Pharmacol Exp Ther 307:297-305.
33. Simmons DA, Rex CS, Palmer L, Pandyarajan V, Fedulov V, Gall CM, Lynch G (2009) Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice. Proc Natl Acad Sci U S A 106:4906-4911.
34. Hickey MA, Gallant K, Gross GG, Levine MS, Chesselet MF (2005) Early behavioral deficits in R6/2 mice suitable for use in preclinical drug testing. Neurobiol Dis 20:1-11.
35. Hickey MA, Kosmalska A, Enayati J, Cohen R, Zeitlin S, Levine MS, Chesselet MF (2008) Extensive early motor and non-motor behavioral deficits are followed by striatal neuronal loss in knock-in Huntington's disease mice. Neuroscience 157:280-295.
36. Watson JB, Hatami A, David H, Masliah E, Roberts K, Evans CE, Levine MS (2009) Alterations in corticostriatal synaptic plasticity in mice overexpressing human alpha-synuclein. Neuroscience 159:501-513.
37. Cepeda C, Colwell CS, Itri JN, Chandler SH, Levine MS (1998) Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J Neurophysiol 79:82-94.
38. Cepeda C, Andre VM, Yamazaki I, Wu N, Kleiman-Weiner M, Levine MS (2008) Differential electrophysiological properties of dopamine D1 and D2 receptor-containing striatal medium-sized spiny neurons. Eur J Neurosci 27:671-682.
39. Ariano MA, Cepeda C, Calvert CR, Flores-Hernandez J, Hernandez-Echeagaray E, Klapstein GJ, Chandler SH, Aronin N, DiFiglia M, Levine MS (2005) Striatal potassium channel dysfunction in Huntington's disease transgenic mice. J Neurophysiol 93:2565-2574.
40. Canals JM, Pineda JR, Torres-Peraza JF, Bosch M, Martin-Ibanez R, Munoz MT, Mengod G, Ernfors P, Alberch J (2004) Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J Neurosci 24:7727-7739.
41. Pang TY, Stam NC, Nithianantharajah J, Howard ML, Hannan AJ (2006) Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience 141:569-584.
42. Zuccato, C, Cattaneo E (2007) Role of brain-derived neurotrophic factor in Huntington's disease. Prog Neurobiol 81:294-330.
43. Tozzi A, Tscherter A, Belcastro V, Tantucci M, Costa C, Picconi B, Centonze D, Calabresi P, Borsini F (2007) Interaction of A2A adenosine and D2 dopamine receptors modulates corticostriatal glutamatergic transmission. Neuropharmacology 53:783-789.
44. Cummings DM, Yim MM, Alaghband Y, Malvar JS, Tsuruyama K, Joshi PR, Cepeda C, Levine MS (2008) The R6/2 phenotype is CAG repeat length-dependent. Abstract Viewer/Itinerary Planner Washington, DC: Society for Neuroscience Program No 443.11.
45. Dragatsis I, Goldowitz D, Del Mar N, Deng YP, Meade CA, Liu L, Sun Z, Dietrich P, Yue J, Reiner A (2009) CAG repeat lengths > or =335 attenuate the phenotype in the R6/2 Huntington's disease transgenic mouse. Neurobiol Dis 33:315-330.
46. Morton AJ, Glynn D, Leavens W, Zheng Z, Faull RL, Skepper JN, Wight JM (2009) Paradoxical delay in the onset of disease caused by super-long CAG repeat expansions in R6/2 mice. Neurobiol Dis 33:331-341.