Abnormalities of neurogenesis in the R6/2 mouse model of Huntington's disease are attributable to the in vivo microenvironment

Journal of Neuroscience

Volumn 25, Issue 50, 2005, Pages 11564-11576

  Phillips, Wendy ^a,b   Morton, A Jennifer ^a,c   Barker, Roger A ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Doublecortin; Huntington's disease; Neurogenesis; Quinolinic acid; R6 2; Seizures

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GENOTYPE; HUNTINGTON CHOREA; IN VIVO STUDY; MALE; MICROENVIRONMENT; MORPHOLOGY; MOUSE; MOUSE STRAIN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SEIZURE; STEM CELL; TRANSGENIC MOUSE; WILD TYPE;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FEMALE; HUNTINGTON DISEASE; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; SEIZURES; SEVERITY OF ILLNESS INDEX;

EID: 30744470119     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3796-05.2005     Document Type: Article

References (102)

1. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523-569.
2. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
3. Armstrong RJ, Barker RA (2001) Neurodegeneration: a failure of neuroregeneration? Lancet 358:1174-1176.
4. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970.
5. Bogdanov MB, Ferrante RJ, Kuemmerle S, Klivenyi P, Beal MF (1998) Increased vulnerability to 3-nitropropionic acid in an animal model of Huntington's disease. J Neurochem 71:2642-2644.
6. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG (2003a) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042-2046.
7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003b) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
8. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-209.
9. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507-518.
10. Chu-LaGraff Q, Kang X, Messer A (2001) Expression of the Huntington's disease transgene in neural stem cell cultures from R6/2 transgenic mice. Brain Res Bull 56:307-312.
11. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
12. Curtis MA, Penney EB, Pearson AG, Roon-Mom WM, Butterworth NJ, Dragunow M, Connor B, Faull RL (2003) Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci USA 100:9023-9027.
13. Curtis MA, Penney EB, Pearson J, Dragunow M, Connor B, Faull RL (2005) The distribution of progenitor cells in the subependymal layer of the lateral ventricle in the normal and Huntington's disease human brain. Neuroscience 132:777-788.
14. Duckworth EA, Butler TL, De Mesquita D, Collier SN, Collier L, Pennypacker KR (2005) Temporary focal ischemia in the mouse: technical aspects and patterns of Fluoro-Jade evident neurodegeneration. Brain Res 1042:29-36.
15. Ekdahl CT, Mohapel P, Elmer E, Lindvall O (2001) Caspase inhibitors increase short-term survival of progenitor-cell progeny in the adult rat dentate gyrus following status epilepticus. Eur J Neurosci 14:937-945.
16. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100:13632-13637.
17. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
18. Fallon J, Reid S, Kinyamu R, Opole I, Opole R, Baratta J, Korc M, Endo TL, Duong A, Nguyen G, Karkehabadhi M, Twardzik D, Patel S, Loughlin S (2000) In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 97:14686-14691.
19. Ferrante RJ, Kowall NW, Richardson EP (1991) Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: a combined study using the section-Golgi method and calbindin D28 immunocytochemistry. J Neurosci 12:3877-3887.
20. Ferrer I, Goutane E, Marin C, Rey MJ, Ribalta T (2000) Brain-derived neurotrophic factor in Huntington disease. Brain Res 866:257-261.
21. Frederiksen K, McKay RD (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144-1151.
22. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438.
23. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci USA 97:1823-1828.
24. Gibson H, Reim K, Brose N, Morton AJ, Jones S (2005) A similar impairment in CA3 mossy fibre LTP in the R6/2 mouse model of Huntington's disease and in the complexin II knockout mouse. Eur J Neurosci 22:1701-1712.
25. Gil JM, Leist M, Popovic N, Brundin P, Petersen A (2004) Asialoerythropoetin is not effective in the R6/2 line of Huntington's disease mice. BMC Neurosci 5:17-27.
26. Gil JM, Mohapel P, Araujo IM, Popovic N, Li J, Brundin P, Petersen A (2005) Reduced hippocampal neurogenesis in R6/2 transgenic Huntington's disease mice. Neurobiol Dis 20:744-751.
27. Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271.
28. Gould E (1999) Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 21:46S-51S.
29. Gundersen HJ, Jensen EB, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology - reconsidered. J Microsc 193:199-211.
30. Hansson O, Petersen A, Leist M, Nicotera P, Castilho RF, Brundin P (1999) Transgenic mice expressing a Huntington's disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity. Proc Natl Acad Sci USA 96:8727-8732.
31. Hansson O, Castilho RF, Korhonen L, Lindholm D, Bates GP, Brundin P (2001a) Partial resistance to malonate-induced striatal cell death in transgenic mouse models of Huntington's disease is dependent on age and CAG repeat length. J Neurochem 78:694-703.
32. Hansson O, Guatteo E, Mercuri NB, Bernardi G, Li XJ, Castilho RF, Brundin P (2001b) Resistance to NMDA toxicity correlates with appearance of nuclear inclusions, behavioural deficits and changes in calcium homeostasis in mice transgenic for exon 1 of the huntington gene. Eur J Neurosci 14:1492-1504.
33. Harjes P, Wanker EE (2003) The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem Sci 28:425-433.
34. Hickey MA, Morton AJ (2000) Mice transgenic for the Huntington's disease mutation are resistant to chronic 3-nitropropionic acid-induced striatal toxicity. J Neurochem 75:2163-2171.
35. Iannicola C, Moreno S, Olivero S, Nardacci R, Ciofi-Luzzatto A, Piacentini M (2000) Early alterations in gene expression and cell morphology in a mouse model of Huntington's disease. J Neurochem 75:830-839.
36. Imura T, Kornblum HI, Sofroniew MV (2003) The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 23:2824-2832.
37. Jain M, Armstrong RJ, Tyres P, Barker RA, Rosser AE (2003) GABAergic immunoreactivity is predominant in neurons derived from expanded human neural precursor cells in vitro. Exp Neurol 182:113-123.
38. Jarabek BR, Yasuda RP, Wolfe BB (2004) Regulation of proteins affecting NMDA receptor-induced excitotoxicity in a Huntington's mouse model. Brain 127:505-516.
39. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710-4715.
40. Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-1094.
41. Katoh-Semba R, Takeuchi IK, Semba R, Kato K (1997) Distribution of brain-derived neurotrophic factor in rats and its changes with development in the brain. J Neurochem 69:34-42.
42. Kempermann G (2002) Regulation of adult hippocampal neurogenesis - implications for novel theories of major depression. Bipolar Disord 4:17-33.
43. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
44. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
45. Kish SJ, Shannak K, Hornykiewicz O (1987) Elevated serotonin and reduced dopamine in subregionally divided Huntington's disease striatum. Ann Neurol 22:386-389.
46. Koelle GB (1955) The histochemical identification of cholinesterase in cholinergic, adrenergic and sensory neurons. J Pharmacol Exp Ther 114:167-184.
47. Kornack DR, Rakic P (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294: 2127-2130.
48. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
49. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neuronal progenitors in the adult rat brain. J Neurosci 17:5820-5829.
50. Lawrence AD, Hodges JR, Rosser AE, Kershaw A, ffrench-Constant C, Rubinsztein DC, Robbins TW, Sahakian BJ (1998) Evidence for specific cognitive deficits in preclinical Huntington's disease. Brain 121:1329-1341.
51. Lazic SE, Grote H, Armstrong RJ, Blakemore C, Hannan AJ, van Dellen A, Barker RA (2004) Decreased hippocampal cell proliferation in R6/1 Huntington's mice. NeuroReport 15:811-813.
52. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
53. Ma L, Morton AJ, Nicholson LF (2003) Microglia density decreases with age in a mouse model of Huntington's disease. Glia 43:274-280.
54. MacGibbon GA, Hamilton LC, Crocker SF, Costain WJ, Murphy KM, Robertson HA, Denovan-Wright EM (2002) Immediate-early gene response to methamphetamine, haloperidol, and quinolinic acid is not impaired in Huntington's disease transgenic mice. J Neurosci Res 67:372-378.
55. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951-955.
56. 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.
57. Mohapel P, Ekdahl CT, Lindvall O (2004) Status epilepticus severity influences the long-term outcome of neurogenesis in the adult dentate gyrus. Neurobiol Dis 15:196-205.
58. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8:955-962.
59. Morton AJ, Leavens W (2000) Mice transgenic for the human Huntington's disease mutation have reduced sensitivity to kainic acid toxicity. Brain Res Bull 52:51-59.
60. Morton AJ, Hunt M, Hodges AK, Lewis PD, Redfern AJ, Dunnett SB, Jones L (2005) A combination drug therapy improves cognition and reverses gene expression changes in a mouse model of Huntington's disease. Eur J Neurosci 21:855-870.
61. Murphy KP, Carter RJ, Lione LA, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton AJ (2000) Abnormal synaptic plasticity and impaired spatial cognition in mice transgenic for exon 1 of the human Huntington's disease mutation. J Neurosci 20:5115-5123.
62. Nacher J, Crespo C, McEwen BS (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14:629-644.
63. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429-441.
64. O'Rourke NA, Sullivan DP, Kaznowski CE, Jacobs AA, McConnell SK (1995) Tangential migration of neurons in the developing cerebral cortex. Development 121:2165-2176.
65. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH (1999) Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487-8497.
66. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH (2001) Cell culture. Progenitor cells from human brain after death. Nature 411:42-43.
67. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
68. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802-813.
69. Petersen A, Hansson O, Puschban Z, Sapp E, Romero N, Castilho RF, Sulzer D, Rice M, DiFiglia M, Przedborski S, Brundin P (2001) Mice transgenic for exon 1 of the Huntington's disease gene display reduced striatal sensitivity to neurotoxicity induced by dopamine and 6-hydroxydopamine. Eur J Neurosci 14:1425-1435.
70. Petersen A, Chase K, Puschban Z, DiFiglia M, Brundin P, Aronin N (2002) Maintenance of susceptibility to neurodegeneration following intrastriatal injections of quinolinic acid in a new transgenic mouse model of Huntington's disease. Exp Neurol 175:297-300.
71. Prickaerts J, Koopmans G, Blokland A, Scheepens A (2004) Learning and adult neurogenesis: survival with or without proliferation? Neurobiol Learn Mem 81:1-11.
72. Racine RJ, Gartner JG, Burnham WM (1972) Epileptiform activity and neural plasticity in limbic structures. Brain Res 47:262-268.
73. Rao MS, Shetty AK (2004) Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19:234-246.
74. Reynolds GP, Pearson SJ (1987) Decreased glutamic acid and increased 5-hydroxytryptamine in Huntington's disease brain. Neurosci Lett 78:233-238.
75. Reynolds GP, Dalton CF, Tillery CL, Mangiarini L, Davies SW, Bates G (1999) Brain neurotransmitter deficits in mice transgenic for the Huntington's disease mutation. J Neurochem 72:1773-1776.
76. Ribchester RR, Thomson D, Wood NI, Hinks T, Gillingwater TH, Wishart TW, Court FA, Morton AJ (2004) Progressive abnormalities in skeletal muscle and neuromuscular junctions of transgenic mice expressing the Huntington's disease mutation. Eur J Neurosci 20:3092-3114.
77. Rosas HD, Koroshetz WJ, Chen YI, Skeuse C, Vangel M, Cudkowicz ME, Caplan K, Marek K, Seidman LJ, Makris N, Jenkins BG, Goldstein JM (2003) Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 27:1615-1620.
78. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, Fraser RA, Couldwell WT, Kawaguchi A, Okano H, Nedergaard M, Goldman SA (2000) In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 6:271-277.
79. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740-744.
80. Sapp E, Kegel KB, Aronin N, Hashikawa T, Uchiyama Y, Tohyama K, Bhide PG, Vonsattel JP, DiFiglia M (2001) Early and progressive accumulation of reactive microglia in the Huntington disease brain. J Neuropathol Exp Neurol 60:161-172.
81. Sathanoori M, Dias BG, Nair AR, Banerjee SB, Tole S, Vaidya VA (2004) Differential regulation of multiple brain-derived neurotrophic factor transcripts in the postnatal and adult rat hippocampus during development, and in response to kainate administration. Brain Res Mol Brain Res 130:170-177.
82. Schauwecker PE (2002) Modulation of cell death by mouse genotype: differential vulnerability to excitatory amino acid-induced lesions. Exp Neurol 178:219-235.
83. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
84. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
85. Scott BW, Wang S, Burnham WM, De Boni U, Wojtowicz JM (1998) Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci Lett 248:73-76.
86. Seaberg RM, van der Kooy D (2002) Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 22:1784-1793.
87. Seaberg RM, Smukler SR, van der KD (2005) Intrinsic differences distinguish transiently neurogenic progenitors from neural stem cells in the early postnatal brain. Dev Biol 278:71-85.
88. Sen A, Kallos MS, Behie LA (2004) New tissue dissociation protocol for scaled-up production of neural stem cells in suspension bioreactors. Tissue Eng 10:904-913.
89. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
90. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578-584.
91. Song HJ, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44.
92. Spires TL, Grote HE, Garry S, Cordery PM, Van Dellen A, Blakemore C, Hannan AJ (2004a) Dendritic spine pathology and deficits in experience-dependent dendritic plasticity in R6/1 Huntington's disease transgenic mice. Eur J Neurosci 10:2799-2807.
93. Spires TL, Grote HE, Varshney NK, Cordery PM, Van Dellen A, Blakemore C, Hannan AJ (2004b) Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J Neurosci 24:2270-2276.
94. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56:149-171.
95. Takahashi J, Palmer TD, Gage FH (1999) Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J Neurobiol 38:65-81.
96. Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
97. Vaidya VA, Siuciak JA, Du F, Duman RS (1999) Hippocampal mossy fiber sprouting induced by chronic electroconvulsive seizures. Neuroscience 89:157-166.
98. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
99. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP Jr (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44:559-577.
100. Wachs FP, Couillard-Despres S, Engelhardt M, Wilhelm D, Ploetz S, Vroemen M, Kaesbauer J, Uyanik G, Klucken J, Karl C, Tebbing J, Svendsen C, Weidner N, Kuhn HG, Winkler J, Aigner L (2003) High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest 83:949-962.
101. Zeron MM, Hansson O, Chen N, Wellington CL, Leavitt BR, Brundin P, Hayden MR, Raymond LA (2002) Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33:849-860.
102. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, MacDonald ME, Friedlander RM, Silani V, Hayden MR, Timmusk T, Sipione S, Cattaneo E (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293:493-498.