Long-term lentiviral-mediated expression of ciliary neurotrophic factor in the striatum of Huntington's disease transgenic mice

Experimental Neurology

Volumn 185, Issue 1, 2004, Pages 26-35

  Zala, Diana ^a   Bensadoun, Jean Charles ^a   De Almeida, Luis Pereira ^b   Leavitt, Blair R ^c   Gutekunst, Claire Anne ^d   Aebischer, Patrick ^a   Hayden, Michael R ^c   Déglon, Nicole ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c Centre for Molecular Medicine and Therapeutics   (Canada)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ciliary neurotrophic factor; CNTF; Gene therapy; HD transgenic mice; Huntington's disease; Lentiviral vector

Indexed keywords

BETA GALACTOSIDASE; BIOLOGICAL MARKER; CILIARY NEUROTROPHIC FACTOR; DOPAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUNTINGTIN; LENTIVIRUS VECTOR; PHOSPHOPROTEIN DARPP 32; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL COUNT; CELL NUCLEUS; CONTROLLED STUDY; CORPUS STRIATUM; DOWN REGULATION; GLIA CELL; HUNTINGTON CHOREA; LOCOMOTION; LONG TERM EXPOSURE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REPORTER GENE; SIGNAL TRANSDUCTION; STEREOMETRY; TRANSGENIC MOUSE; TRINUCLEOTIDE REPEAT; VIRAL GENE THERAPY; WILD TYPE;

EID: 0346993604     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2003.09.002     Document Type: Article

References (56)

1. Abicht A., Lochmuller H. Technology evaluation: CRIB (CNTF delivery) CytoTherapeutics Inc. Curr. Opin. Mol. Ther. 1:1999;645-650.
2. Aebischer P., Schluep M., Déglon N., Joseph J.M., Hirt L., Heyd B., Goddard M., Hammang J.P., Zurn A.D., Kato A.C., Regli F., Baetge E.E. Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amyotrophic lateral sclerosis patients. Nat. Med. 2:1996;696-699.
3. Albrecht P.J., Dahl J.P., Stoltzfus O.K., Levenson R., Levison S.W. Ciliary neurotrophic factor activates spinal cord astrocytes, stimulating their production and release of fibroblast growth factor-2, to increase motor neuron survival. Exp. Neurol. 173:2002;46-62.
4. Alonzi T., Middleton G., Wyatt S., Buchman V., Betz U.A., Muller W., Musiani P., Poli V., Davies A.M. Role of STAT3 and PI 3-kinase/Akt in mediating the survival actions of cytokines on sensory neurons. Mol. Cell. Neurosci. 18:2001;270-282.
5. Anderson K.D., Panayotatos N., Corcoran T.L., Lindsay R.M., Wiegand S.J. Ciliary neurotrophic factor protects striatal output neurons in an animal model of Huntington disease. Proc. Natl. Acad. Sci. U. S. A. 93:1996;7346-7351.
6. Andrew S.E., Goldberg Y.P., Kremer B., Telenius H., Theilmann J., Adam S., Starr E., Squitieri F., Lin B., Kalchman M.A.et al. The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat. Genet. 4:1993;329-330.
7. Araujo D.M., Hilt D.C. Glial cell line-derived neurotrophic factor attenuates the locomotor hypofunction and striatonigral neurochemical deficits induced by chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid. Neuroscience. 82:1998;117-127.
8. Bemelmans A.P., Horellou P., Pradier L., Brunet I., Colin P., Mallet J. Brain-derived neurotrophic factor-mediated protection of striatal neurons in an excitotoxic rat model of Huntington's disease, as demonstrated by adenoviral gene transfer. Hum. Gene Ther. 10:1999;2987-2997.
9. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin proteasome system by protein aggregation. Science. 292:2001;1552-1555.
10. Bibb J.A., Yan Z., Svenningsson P., Snyder G.L., Pieribone V.A., Horiuchi A., Nairn A.C., Messer A., Greengard P. Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice. Proc. Natl. Acad. Sci. U. S. A. 97:2000;6809-6814.
11. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 96:1999;857-868.
12. Catlett-Falcone R., Landowski T.H., Oshiro M.M., Turkson J., Levitzki A., Savino R., Ciliberto G., Moscinski L., Fernandez-Luna J.L., Nunez G., Dalton W.S., Jove R. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity. 10:1999;105-115.
13. de Almeida L.P., Zala D., Aebischer P., Déglon N. Neuroprotective effect of a CNTF-expressing lentiviral vector in the quinolinic acid rat model of Huntington's disease. Neurobiol. Dis. 8:2001;433-446.
14. Déglon N., Aebischer P. Lentiviruses as vectors for CNS diseases. Curr. Top. Microbiol. Immunol. 2002;191-209.
15. Déglon N., Tseng J.L., Bensadoun J.C., Zurn A.D., Arsenijevic Y., De Almeida L.P., Zufferey R., Trono D., Aebischer P. Self-inactivating lentiviral vectors with enhanced transgene expression as potential gene transfer system in Parkinson's disease. Hum. Gene Ther. 11:2000;179-190.
16. Du K., Montminy M. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273:1998;32377-32379.
17. Dull T., Zufferey R., Kelly M., Mandel R.J., Nguyen M., Trono D., Naldini L. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:1998;8463-8471.
18. Ellison D.W., Kowall N.W., Martin J.B. Subset of neurons characterized by the presence of NADPH-diaphorase in human substantia innominata. J. Comp. Neurol. 260:1987;233-245.
19. Emerich D.F., Lindner M.D., Winn S.R., Chen E.Y., Frydel B.R., Kordower J.H. Implants of encapsulated human CNTF-producing fibroblasts prevent behavioral deficits and striatal degeneration in a rodent model of Huntington's disease. J. Neurosci. 16:1996;5168-5181.
20. Emerich D.F., Cain C.K., Greco C., Saydoff J.A., Hu Z.Y., Liu H., Lindner M.D. Cellular delivery of human CNTF prevents motor and cognitive dysfunction in a rodent model of Huntington's disease. Cell Transplant. 6:1997;249-266.
21. Emerich D.F., Winn S.R., Hantraye P.M., Peschanski M., Chen E.Y., Chu Y., McDermott P., Baetge E.E., Kordower J.H. Protective effect of encapsulated cells producing neurotrophic factor cntf in a monkey model of Huntington's disease. Nature. 386:1997;395-399.
22. Frim D.M., Short M.P., Rosenberg W.S., Simpson J., Breakefield X.O., Isacson O. Local protective effects of nerve growth factor-secreting fibroblasts against excitotoxic lesions in the rat striatum. J. Neurosurg. 78:1993;267-273.
23. Fukuda A., Deshpande S.B., Shimano Y., Nishino H. Astrocytes are more vulnerable than neurons to cellular Ca2+ overload induced by a mitochondrial toxin, 3-nitropropionic acid. Neuroscience. 87:1998;497-507.
24. Gomes F.C., Paulin D., Moura Neto V. Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz. J. Med. Biol. Res. 32:1999;619-631.
25. Hodgson J.G., Agopyan N., Gutekunst C.A., Leavitt B.R., LePiane F., Singaraja R., Smith D.J., Bissada N., McCutcheon K., Nasir J., Jamot L., Li X.J., Stevens M.E., Rosemond E., Roder J.C., Phillips A.G., Rubin E.M., Hersch S.M., Hayden M.R. A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron. 23:1999;181-192.
26. Hottinger A.F., Azzouz M., Déglon N., Aebischer P., Zurn A.D. Complete and long-term rescue of lesioned adult motoneurons by lentiviral-mediated expression of glial cell line-derived neurotrophic factor in the facial nucleus. J. Neurosci. 20:2000;5587-5593.
27. Iannicola C., Moreno S., Oliverio S., Nardacci R., Ciofi-Luzzatto A., Piacentini M. Early alterations in gene expression and cell morphology in a mouse model of Huntington's disease. J. Neurochem. 75:2000;830-839.
28. Ip N.Y., Yancopoulos G.D. The neurotrophins and CNTF: two families of collaborative neurotrophic factors. Annu. Rev. Neurosci. 19:1996;491-515.
29. Kahn M.A., Ellison J.A., Speight G.J., de Vellis J. CNTF regulation of astrogliosis and the activation of microglia in the developing rat central nervous system. Brain Res. 685:1995;55-67.
30. Kahn M.A., Ellison J.A., Chang R.P., Speight G.J., de Vellis J. CNTF induces GFAP in a S-100 alpha brain cell population: the pattern of CNTF-alpha R suggests an indirect mode of action. Brain Res. Dev. Brain Res. 98:1997;221-233.
31. Kahn M.A., Huang C.J., Caruso A., Barresi V., Nazarian R., Condorelli D.F., deVellis J. Ciliary neurotrophic factor activates JAK/Stat signal transduction cascade and induces transcriptional expression of glial fibrillary acidic protein in glial cells. J. Neurochem. 68:1997;1413-1423.
32. Kane L.P., Shapiro V.S., Stokoe D., Weiss A. Induction of NF-kappaB by the Akt/PKB kinase. Curr. Biol. 9:1999;601-604.
33. Karni R., Jove R., Levitzki A. Inhibition of pp60 c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors. Oncogene. 18:1999;4654-4662.
34. Levison S.W., Hudgins S.N., Crawford J.L. Ciliary neurotrophic factor stimulates nuclear hypertrophy and increases the GFAP content of cultured astrocytes. Brain Res. 803:1998;189-193.
35. Lisovoski F., Akli S., Peltekian E., Vigne E., Haase G., Perricaudet M., Dreyfus P.A., Kahn A., Peschanski M. Phenotypic alteration of astrocytes induced by ciliary neurotrophic factor in the intact adult brain, as revealed by adenovirus-mediated gene transfer. J. Neurosci. 17:1997;7228-7236.
36. Luthi-Carter R., Strand A., Peters N.L., Solano S.M., Hollingsworth Z.R., Menon A.S., Frey A.S., Spektor B.S., Penney E.B., Schilling G., Ross C.A., Borchelt D.R., Tapscott S.J., Young A.B., Cha J.H., Olson J.M. Decreased expression of striatal signaling genes in a mouse model of Huntington's disease. Hum. Mol. Genet. 9:2000;1259-1271.
37. Mayer M., Bhakoo K., Noble M. Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Development. 120:1994;143-153.
38. Mittoux V., Joseph J.M., Conde F., Palfi S., Dautry C., Poyot T., Bloch J., Déglon N., Ouary S., Nimchinsky E.A., Brouillet E., Hof P.R., Peschanski M., Aebischer P., Hantraye P. Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Hum. Gene Ther. 11:2000;1177-1187.
39. Naldini L., Blomer U., Gallay P., Ory D., Mulligan R., Gage F.H., Verma I.M., Trono D. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 272:1996;263-267.
40. Neri C. New light on polyglutamine neurodegenerative disorders: interference with transcription. Trends Mol. Med. 7:2001;283-284.
41. Nucifora F.C. Jr., Sasaki M., Peters M.F., Huang H., Cooper J.K., Yamada M., Takahashi H., Tsuji S., Troncoso J., Dawson V.L., Dawson T.M., Ross C.A. Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science. 291:2001;2423-2428.
42. Ouimet C.C., Langley-Gullion K.C., Greengard P. Quantitative immunocytochemistry of DARPP-32-expressing neurons in the rat caudatoputamen. Brain Res. 808:1998;8-12.
43. Ozes O.N., Mayo L.D., Gustin J.A., Pfeffer S.R., Pfeffer L.M., Donner D.B. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature. 401:1999;82-85.
44. Penn R.D., Kroin J.S., York M.M., Cedarbaum J.M. Intrathecal ciliary neurotrophic factor delivery for treatment of amyotrophic lateral sclerosis (phase I trial). Neurosurgery. 40:1997.
45. Perez-Navarro E., Alberch J., Neveu I., Arenas E. Brain-derived neurotrophic factor, neurotrophin-3 and neurotrophin-4/5 differentially regulate the phenotype and prevent degenerative changes in striatal projection neurons after excitotoxicity in vivo. Neuroscience. 91:1999;1257-1264.
46. Perez-Navarro E., Akerud P., Marco S., Canals J.M., Tolosa E., Arenas E., Alberch J. Neurturin protects striatal projection neurons but not interneurons in a rat model of Huntington's disease. Neuroscience. 98:2000;89-96.
47. Saudou F., Finkbeiner S., Devys D., Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:1998;55-66.
48. Shimohata T., Nakajima T., Yamada M., Uchida C., Onodera O., Naruse S., Kimura T., Koide R., Nozaki K., Sano Y., Ishiguro H., Sakoe K., Ooshima T., Sato A., Ikeuchi T., Oyake M., Sato T., Aoyagi Y., Hozumi I., Nagatsu T., Takiyama Y., Nishizawa M., Goto J., Kanazawa I., Davidson I., Tanese N. Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nat. Genet. 26:2000;29-36.
49. Slow E.J., van Raamsdonk J., Rogers D., Coleman S.H., Graham R.K., Dheng Y., Oh R., Bissada N., Hossain S.M., Yang Y.-Z., Li X.-J., Simpson E.M., Gutekunst C.-A., Leavitt B.R., Hayden M.R. Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 12:2003;1555-1567.
50. Sugars K.L., Rubinsztein D.C. Transcriptional abnormalities in Huntington disease. Trends Genet. 19:2003;233-238.
51. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell. 72:1993;971-983.
52. Turmaine M., Raza A., Mahal A., Mangiarini L., Bates G.P., Davies S.W. Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc. Natl. Acad. Sci. U. S. A. 97:2000;8093-8097.
53. van Dellen A., Welch J., Dixon R.M., Cordery P., York D., Styles P., Blakemore C., Hannan A.J. N-acetylaspartate and DARPP-32 levels decrease in the corpus striatum of Huntington's disease mice. NeuroReport. 11:2000;3751-3757.
54. Volpe B.T., Wildmann J., Altar C.A. Brain-derived neurotrophic factor prevents the loss of nigral neurons induced by excitotoxic striatal-pallidal lesions. Neuroscience. 83:1998;741-748.
55. Vonsattel J.P., Difiglia M. Huntington disease. J. Neuropathol. Exp. Neurol. 57:1998;369-384.
56. Winter C.G., Saotome Y., Levison S.W., Hirsh D. A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc. Natl. Acad. Sci. U. S. A. 92:1995;5865-5869.