Reactive astrocytosis and glial glutamate transporter clustering are early changes in a spinocerebellar ataxia type 1 transgenic mouse model

Neuron Glia Biology

Volumn 3, Issue 4, 2007, Pages 335-351

  Giovannoni, Roberto ^a   Maggio, Nicola ^b   Rosaria Bianco, Maria ^b   Cavaliere, Carlo ^b   Cirillo, Giovanni ^b   Lavitrano, Marialuisa ^a   Papa, Michele ^b  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

EAAT1; Neurodegeneration; SCA1; Synaptic plasticity

Indexed keywords

ATAXIN 1; EXCITATORY AMINO ACID TRANSPORTER 1; GLUTAMATE TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BEHAVIOR; CELL STRUCTURE; CEREBELLUM CORTEX; CONTROLLED STUDY; CORRELATION ANALYSIS; GAIT; GLIA CELL; MACROGLIA; MORPHOLOGY; MOUSE; NERVE CELL NETWORK; NEUROLOGIC DISEASE; NEUROTRANSMISSION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; ROTAROD TEST; SPINOCEREBELLAR DEGENERATION; SYNAPSE; TRANSGENIC MOUSE;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 46749137502     PISSN: 1740925X     EISSN: 17410533     Source Type: Journal    
DOI: 10.1017/S1740925X08000185     Document Type: Article

References (71)

1. Adachi H., Kume A., Li M., Nakagomi Y., Niwa H., Do J. et al. (2001) Transgenic mice with an expanded CAG repeat controlled by the human AR promoter show polyglutamine nuclear inclusions and neuronal dysfunction without neuronal cell death. Human Molecular Genetics 10, 1039-1048.
2. Ajtai B.M. and Kalman M. (1998) Glial fibrillary acidic protein expression but no glial demarcation follows the lesion in the molecular layer of cerebellum. Brain Research 802, 285-288.
3. Altman J. and Bayer S.A. (1997) Basic cellular organization and circuitry of the cerebellar cortex. In Altman J. and Bayer S.A. (eds) Development of the Cerebellar System in Relation to its Evolution, Structure, and Functions. CRC Press, pp. 26-43.
4. Anderson B.J., Li X., Alcantara A.A., Isaacs K.R., Black J.E. and Greenough W.T. (1994) Glial hypertrophy is associated with synaptogenesis following motor-skill learning, but not with angiogenesis following exercise. Glia 11, 73-80.
5. Bal-Price A. and Brown G.C. (2001) Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. Journal of Neuroscience 21, 6480-6491.
6. Banfi S., Servadio A., Chung M.Y., Kwiatkowski T.J. Jr, McCall A.E., Duvick L.A. et al. (1994) Identification and characterization of the gene causing type 1 spinocerebellar ataxia. Nature Genetics 7, 513-520.
7. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F. et al. (1996) Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159-171.
8. Bodner R.A., Outeiro T.F., Altmann S., Maxwell M.M., Cho S.H., Hyman B.T. et al. (2006) Pharmacological promotion of inclusion formation: a therapeutic approach for Huntington's and Parkinson's diseases. Proceedings of the National Academy of Sciences of the U.S.A. 103, 4246-4251.
9. Boy J., Leergaard T.B., Schmidt T., Odeh F., Bichelmeier U., Nuber S. et al. (2006) Expression mapping of tetracycline-responsive prion protein promoter: digital atlasing for generating cell-specific disease models. Neuroimage 33, 449-462.
10. Burright E.N., Clark H.B., Servadio A., Matilla T., Feddersen R.M., Yunis W.S. et al. (1995) SCA1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell 82, 937-948.
11. Carmignoto G. (2000) Reciprocal communication systems between astrocytes and neurones. Progress in Neurobiology 62, 561-581.
12. Carter R.J., Lione L.A., Humby T., Mangiarini L., Mahal A., Bates G.P. et al. (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. Journal of Neuroscience 19, 3248-3257.
13. Cavaliere C., Cirillo G., Bianco M.R., Rossi F., De Novellis V., Maione S. et al. (2008) Gliosis alters expression and uptake of spinal glial amino acid transporters in a mouse neuropathic pain model. Neuron Glia Biology 3, 1-14.
14. Chaudhry F.A., Lehre K.P., van Lookeren C.M., Ottersen O.P., Danbolt N.C. and Storm-Mathisen J. (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711-720.
15. Chen H.K., Fernandez-Funez P., Acevedo S.F., Lam Y.C., Kaytor M.D., Fernandez M.H. et al. (2003) Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113, 457-468.
16. Clark H.B., Burright E.N., Yunis W.S., Larson S., Wilcox C., Hartman B. et al. (1997) Purkinje cell expression of a mutant allele of SCA1 in transgenic mice leads to disparate effects on motor behaviors, followed by a progressive cerebellar dysfunction and histological alterations. Journal of Neuroscience 17, 7385-7395.
17. Colangelo A.M., Bianco M.R., Vitagliano L., Cavaliere C., Cirillo G., De Gioia L. et al. (2008) A new nerve growth factor (NGF)-mimetic peptide active on neuropathic pain in rats. Journal of Neuroscience 28, 2698-2709.
18. Cummings C.J., Orr H.T. and Zoghbi H.Y. (1999) Progress in pathogenesis studies of spinocerebellar ataxia type 1. Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 354, 1079-1081.
19. Cummings C.J., Sun Y., Opal P., Antalffy B., Mestril R., Orr H.T. et al. (2001) Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Human Molecular Genetics 10, 1511-1518.
20. Custer S.K., Garden G.A., Gill N., Rueb U., Libby R.T., Schultz C. et al. (2006) Bergmann glia expression of polyglutamine-expanded ataxin-7 produces neurodegeneration by impairing glutamate transport. Nature Neuroscience 9, 1302-1311.
21. Danbolt N.C. (2001) Glutamate uptake. Progress in Neurobiology 65, 1-105.
22. Davies S.W., Turmaine M., Cozens B.A., DiFiglia M., Sharp A.H., Ross C.A. et al. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90, 537-548.
23. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P. et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993.
24. Emamian E.S., Kaytor M.D., Duvick L.A., Zu T., Tousey S.K., Zoghbi H.Y. et al. (2003) Serine 776 of ataxin-1 is critical for polyglutamine-induced disease in SCA1 transgenic mice. Neuron 38, 375-387.
25. Fernandez-Funez P., Nino-Rosales M.L., de Gouyon B., She W.C., Luchak J.M., Martinez P. et al. (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408, 101-106.
26. French S.J. and Totterdell S. (2004) Quantification of morphological differences in boutons from different afferent populations to the nucleus accumbens. Brain Research 1007, 167-177.
27. Furth P.A., St O.L., Boger H., Gruss P., Gossen M., Kistner A. et al. (1994) Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter. Proceedings of the National Academy of Sciences of the U.S.A. 91, 9302-9306.
28. Ginsberg S.D., Martin L.J. and Rothstein J.D. (1995) Regional deafferentation down-regulates subtypes of glutamate transporter proteins. Journal of Neurochemistry 65, 2800-2803.
29. Gossen M. and Bujard H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proceedings of the National Academy of Sciences of the U.S.A. 89, 5547-5551.
30. Griffin W.S., Liu L., Li Y., Mrak R.E. and Barger S.W. (2006) Interleukin-1 mediates Alzheimer and Lewy body pathologies. Journal of Neuroinflammation 3, 5.
31. Grosche J., Matyash V., Moller T., Verkhratsky A., Reichenbach A. and Kettenmann H. (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nature Neuroscience 2, 139-143.
32. Ikegaya Y., Matsuura S., Ueno S., Baba A., Yamada M.K., Nishiyama N. et al. (2002) Beta-amyloid enhances glial glutamate uptake activity and attenuates synaptic efficacy. Journal of Biological Chemistry 277, 32180-32186.
33. Ishiguro H., Yamada K., Sawada H., Nishii K., Ichino N., Sawada M. et al. (2001) Age-dependent and tissue-specific CAG repeat instability occurs in mouse knock-in for a mutant Huntington's disease gene. Journal of Neuroscience Research 65, 289-297.
34. Karl T., Pabst R. and von Horsten S. (2003) Behavioral phenotyping of mice in pharmacological and toxicological research. Experimental Toxicology and Pathology 55, 69-83.
35. Klement I.A., Skinner P.J., Kaytor M.D., Yi H., Hersch S.M., Clark H.B. et al. (1998) Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95, 41-53.
36. Lehre K.P. and Danbolt N.C. (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. Journal of Neuroscience 18, 8751-8757.
37. Lorenzetti D., Watase K., Xu B., Matzuk M.M., Orr H.T. and Zoghbi H.Y. (2000) Repeat instability and motor incoordination in mice with a targeted expanded CAG repeat in the Sca1 locus. Human Molecular Genetics 9, 779-785.
38. Mrak R.E. and Griffin W.S. (2005) Glia and their cytokines in progression of neurodegeneration. Neurobiology of Aging 26, 349-354.
39. Okuda T., Hattori H., Takeuchi S., Shimizu J., Ueda H., Palvimo J.J. et al. (2003) PQBP-1 transgenic mice show a late-onset motor neuron disease-like phenotype. Human Molecular Genetics 12, 711-725.
40. Orr H.T. and Zoghbi H.Y. (2007) Trinucleotide repeat disorders. Annual Reveiw of Neuroscience 30, 575-621.
41. Papa M., Boscia F., Canitano A., Castaldo P., Sellitti S., Annunziato L. et al. (2003) Expression pattern of the ether-a-gogo-related (ERG) K+ channel-encoding genes ERG1, ERG2, and ERG3 in the adult rat central nervous system. Journal of Comparative Neurology 466, 119-135.
42. Papa M., Bundman M.C., Greenberger V. and Segal M. (1995) Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. Journal of Neuroscience 15, 1-11.
43. Paulson H.L. (1999) Protein fate in neurodegenerative proteinopathies: polyglutamine diseases join the (mis)fold. American Journal of Human Genetics 64, 339-345.
44. Peters A., Palay S.L. and Webster H.deF. (1991). The Fine Structure of the Nervous System. Oxford University Press.
45. Rimoldi M., Servadio A. and Zimarino V. (2001) Analysis of heat shock transcription factor for suppression of polyglutamine toxicity. Brain Research Bulletin 56, 353-362.
46. Robitaille Y., Schut L. and Kish S.J. (1995) Structural and immunocytochemical features of olivopontocerebellar atrophy caused by the spinocerebellar ataxia type 1 (SCA-1) mutation define a unique phenotype. Acta Neuropathologica 90, 572-581.
47. Rothstein J.D. (1996) Excitotoxicity hypothesis. Neurology 47, S19-S25.
48. Rozen S. and Skaletsky H. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132, 365-386.
49. Saulle E., Gubellini P., Picconi B., Centonze D., Tropepi D., Pisani A. et al. (2004) Neuronal vulnerability following inhibition of mitochondrial complex II: a possible ionic mechanism for Huntington's disease. Molecular and Cellular Neuroscience 25, 9-20.
50. Sausbier M., Hu H., Arntz C., Feil S., Kamm S., Adelsberger H. et al. (2004) Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated K+ channel deficiency. Proceedings of the National Academy of Sciences of the U.S.A. 101, 9474-9478.
51. Schikorski T. and Stevens C.F. (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. Journal of Neuroscience 17, 5858-5867.
52. Schols L., Bauer P., Schmidt T., Schulte T. and Riess O. (2004) Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis. Lancet Neurology 3, 291-304.
53. Serra H.G., Byam C.E., Lande J.D., Tousey S.K., Zoghbi H.Y. and Orr H.T. (2004) Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Human Molecular Genetics 13, 2535-2543.
54. Serra H.G., Duvick L., Zu T., Carlson K., Stevens S., Jorgensen N. et al. (2006) RORalpha-mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell 127, 697-708.
55. Servadio A., Koshy B., Armstrong D., Antalffy B., Orr H.T. and Zoghbi H.Y. (1995) Expression analysis of the ataxin-1 protein in tissues from normal and spinocerebellar ataxia type 1 individuals. Nature Genetics 10, 94-98.
56. Shahbazian M.D., Orr H.T. and Zoghbi H.Y. (2001) Reduction of Purkinje cell pathology in SCA1 transgenic mice by p53 deletion. Neurobiology of Disease 8, 974-981.
57. Shakkottai V.G., Chou C.H., Oddo S., Sailer C.A., Knaus H.G., Gutman G.A. et al. (2004) Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. Journal of Clinical Investigation 113, 582-590.
58. Sheldon A.L. and Robinson M.B. (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochemistry International 51, 333-355.
59. Skinner P.J., Koshy B.T., Cummings C.J., Klement I.A., Helin K., Servadio A. et al. (1997) Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures. Nature 389, 971-974.
60. Smith S.J. (1998) Glia help synapses form and function. Current Biology 8, R158-R160.
61. Spacek J. (1985) Relationships between synaptic junctions, puncta adhaerentia and the spine apparatus at neocortical axospinous synapses. A serial section study. Anatomy and Embryology 173, 129-135.
62. Tremblay P., Meiner Z., Galou M., Heinrich C., Petromilli C., Lisse T. et al. (1998) Doxycycline control of prion protein transgene expression modulates prion disease in mice. Proceedings of the National Academy of Sciences of the U.S.A. 95, 12580-12585.
63. Tyler W.J., Zhang X.L., Hartman K., Winterer J., Muller W., Stanton P.K. et al. (2006) BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. Journal of Physiology 574, 787-803.
64. Unger J.W. (1998) Glial reaction in aging and Alzheimer's disease. Microscopy Research and Technique 43, 24-28.
65. Vandaele S., Nordquist D.T., Feddersen R.M., Tretjakoff I., Peterson A.C. and Orr H.T. (1991) Purkinje cell protein-2 regulatory regions and transgene expression in cerebellar compartments. Genes and Development 5, 1136-1148.
66. Ventura R. and Harris K.M. (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. Journal of Neuroscience 19, 6897-6906.
67. Watanabe M. (2002) Glial processes are glued to synapses via Ca(2+)-permeable glutamate receptors. Trends in Neurosciences 25, 5-6.
68. Watase K., Hashimoto K., Kano M., Yamada K., Watanabe M., Inoue Y. et al. (1998) Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. European Journal of Neuroscience 10, 976-988.
69. Watase K., Weeber E.J., Xu B., Antalffy B., Yuva-Paylor L., Hashimoto K. et al. (2002) A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 34, 905-919.
70. Watkins L.R. and Maier S.F. (2003) Glia: a novel drug discovery target for clinical pain. Nature Reviews Drug Discovery 2, 973-985.
71. Zu T., Duvick L.A., Kaytor M.D., Berlinger M.S., Zoghbi H.Y., Clark H.B. et al. (2004) Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. Journal of Neuroscience 24, 8853-8861.