Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease

Human Gene Therapy

Volumn 11, Issue 8, 2000, Pages 1177-1187

  Mittoux, Vincent ^a   Joseph, Jean Marc ^b   Conde, Françoise ^a   Palfi, Stephane ^a   Dautry, Caroline ^a   Poyot, Thomas ^a   Bloch, Jocelyne ^b   Deglon, Nicole ^b   Ouary, Stephane ^a   Nimchinsky, Esther A ^c,d   Brouillet, Emmanuel ^a   Hof, Patrick R ^d   Peschanski, Marc ^e   Aebischer, Patrick ^b   Hantraye, Philippe ^a  

^a SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIC FACTOR;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; COGNITION; CONTROLLED STUDY; DEMENTIA; FEMALE; HUNTINGTON CHOREA; MOTOR PERFORMANCE; NEOSTRIATUM; NERVE CELL DEGENERATION; NEUROPROTECTION; NONHUMAN; TREATMENT OUTCOME;

EID: 0034690615     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/10430340050015220     Document Type: Article

References (61)

1. Aebischer, P., Schluep, M., Deglon, N., Joseph, J.M., Hirt, L., Heyd, B., Goddard, M., Hammang, J.P., Zurn, A.D., Kato, A.C., Regli, F., and Baetge, E.E. (1996a). Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amyotrophic lateral sclerosis patients. Nature Med. 2, 696-699.
2. Aebischer, P., Pochon, N.A., Heyd, B., Deglon, N., Joseph, J.M., Zurn, A.D., Baetge, E.E., Hammang, J.P., Goddard, M., Lysaght, M., Kaplan, F., Kato, A.C., Schluep, M., Hirt, L., Regli, F., Porchet, F., and De Tribolet, N. (1996b). Gene therapy for amyotrophic lateral sclerosis (ALS) using a polymer encapsulated xenogenic cell line engineered to secrete hCNTF. Hum. Gene Ther. 7, 851-860.
3. Beal, M.F., Hyman, B.T., and Koroshetz, W. (1993). Do defects in mitochondrial energy metabolism underlie the pathology of neurodegenerative diseases? Trends Neurosci. 16, 125-131.
4. Bloom, F.E., Young, W.G., Nimchinsky, E.A., Hof, P.R., and Morrison, J.H. (1997). Neuronal vulnerability and informatics in human disease. In Progress in Neuroinformatics Research, Vol. 1: Neuroinformatics - An Overview of the Human Brain Project. S.H. Koslow and M.F. Huerta, eds. (Lawrence Erlbaum, Mahwah, NJ) pp. 83-123.
5. Brouillet, E., Hantraye, P., Ferrante, R.J., Dolan, R., Leory-Willig, A., Kowall, N.W., and Beal, M.F. (1995). Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc. Natl. Acad. Sci. U.S.A. 92, 7105-7109.
6. Brouillet, E., Guyot, M.C., Mittoux, V., Altairac, S., Conde, F., Palpi, S., and Hantraye, P. (1998). Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J. Neurochem. 70, 794-805.
7. Brouillet, E., Conde, F., Beal, M.F., and Hantraye, P. (1999). Replicating Huntington disease phenotype in experimental animals. Prog. Neurobiol. 59, 427-468.
8. Buzas, B., Symes, A.J., and Cox, B.M. (1999). Regulation of nociceptin/orphanin FQ gene expression by neuropoietic cytokines and neurotrophic factors in neurons and astrocytes. J. Neurochem. 72, 1882-1889.
9. Campbell, M.J., and Morrison, J.H. (1989). Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J. Comp. Neurol. 282, 191-205.
10. Cayouette, M., Behn, D., Sendtner, M., Lachapelle, P., and Gravel, C. (1998). Intraocular gene transfer of ciliary neurotrophic factor prevents death and increases responsiveness of rod photoreceptors in the retinal degeneration slow mouse. J. Neurosci. 15, 9282-9293.
11. Cedarbaum, J.M. (1995a). The pharmacokinetics of subcutaneously administered recombinant human ciliary neurotrophic factor (rHCNTF) in patients with amyotrophic lateral sclerosis: Relation to parameters of the acute-phase response. The ALS CNTF Treatment Study (ACTS) Phase I-II Study Group. Clin. Neuropharmacol. 18, 500-514.
12. Cedarbaum, J.M. (1995b). A phase I study of recombinant human ciliary neurotrophic factor (rHCNTF) in patients with amyotrophic lateral sclerosis. The ALS CNTF Treatment Study (ACTS) Phase I-II Study Group. Clin. Neuropharmacol. 18, 515-532.
13. Choi, D.W., and Viseskul, V. (1988). Opioids and non-opioid enantiomers selectively attenuate N-methyl-D-aspartate neurotoxicity on cortical neurons. Eur. J. Pharmacol. 155, 27-35.
14. Clatterbuck, R.E., Price, D.L., and Koliatsos, V.E. (1996). Ciliary neurotrophic factor stimulates the expression of glial fibrillary acidic protein by brain astrocytes in vivo. J. Comp. Neurol. 369, 543-551.
15. Coles, C.J., Edmondson, E., and Singer, T.P. (1979). Inactivation of succinate dehydrogenase by 3-nitropropionate. J. Biol. Chem. 254, 5161-5167.
16. Dautry, C., Conde, F., Brouillet, E., Mittoux, V., Beal, M.F., Bloch, G., and Hantraye, P. (1999). Serial 1H-NMR spectroscopy study of metabolic impairment in primates chronically treated with the succinate dehydrogenase inhibitor 3-nitropropionic acid. Neurobiol. Dis. 6, 259-268.
17. Diamond, A. (1990). Developmental time course in human infants and infant monkeys, and the neural bases of, inhibitory control in reaching. Ann. N.Y. Acad. Sci. 608, 637-669.
18. Emerich, D.F., Lindner, M.D., Winn, S.R., Chen, E.Y., Frydel, B.R., and Kordower, J.H. (1996). Implants of encapsulated human CNTF-producing fibroblasts prevent behavioral deficits and striatal degeneration in a rodent model of Huntington' s disease. J. Neurosci. 16, 5168-5181.
19. Emerich, D.F., Winn, S.R., Hantraye, P.M., Peschanski, M., Chen, E.Y., Chu, Y., Mcdermott, P., Baetge, E.E., and Kordower, J.H. (1997). Protective effect of encapsulated cells producing neurotrophic factor CNTF in a monkey model of Huntington's disease. Nature (London) 386, 395-399.
20. Ferrante, R.J., Kowall, N.W., and Richardson, E.P., JR. (1991). Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: A combined study using the section-Golgi method and calbindin D28k immunocytochemistry. J. Neurosci. 11, 3877-3887.
21. Garnett, E.S., Firnau, G., Nahmias, C., Carbotte, R., and Bartolucci, G. (1984). Reduced striatal glucose consumption and prolonged reaction time are early features in Huntington's disease. J. Neurol. Sci. 65, 231-237.
22. Harper, P.S. (1991). In Huntington's Disease. P.S. Harper, ed. (W.B. Saunders, London) chap. 2, 3, and 5.
23. Hedreen, J.C., Peyser, C.E., Folstein, S.E., and Ross, C.A. (1991). Neuronal loss in layers V and VI of cerebral cortex in Huntington's disease. Neurosci. Lett. 133, 257-261.
24. Hirano, T., Matsuda, T., and Nakajima, K. (1994). Signal transduction through gp130 that is shared among the receptors for the interleukin 6 related cytokine subfamily. Stem Cells 12, 262-277.
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., and Hayden, M.R. (1999). A YAC mouse model for Huntington' s disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron 23, 181-192.
26. Hof, P.R., and Morrison, J.H. (1995). Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. J. Comp. Neurol. 352, 161-186.
27. Hsu, S.M., Raine, L., and Fanger, H. (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29, 577-580.
28. 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.
29. IP, N.Y. (1998). The neutrophins and neuropoietic cytokines: Two families of growth factors acting on neural and hematopoietic cells. Ann. N.Y. Acad. Sci. 840, 97-106.
30. Johnson, R.M., McNeeley, P.A., Demoor, K., Stewart, G.R., Glaeser, B.S., and Pitchford, S. (1994). Recombinant human ciliary neurotrophic factor stimulates the metabolic activity of SH-SY5Y cells as measured by a cytosensor microphysiometer. Brain Res. 646, 327-331.
31. Knoflach, F., Reinscheid, R.K., Civelli, O., and Kemp, J.A. (1996). Modulation of voltage-gated calcium channels by orphanin FQ in freshly dissociated hippcampal neurons. J. Neurosci. 16, 6657-6664.
32. Kuhl, E.D., Phelps, M.E., Markham, C.H., Metter, E.J., Riege, W.H., and Winter, J. (1982). Cerebral metabolism and atrophy in Huntington's disease determined by 18FDG and computed tomographic scan. Ann. Neurol. 12, 425-434.
33. Lipton, S.A., and Rosenberg, P.A. (1994). Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330, 613-622.
34. Lisovoski, F., Akli, S., Peltekian. E., Vigne, E., Haase, G., Perricaudet, M., Dreyfus, P.A., Kahn, A., and Peschanski, M. (1997). Phenotypic alteration of astrocytes induced by ciliary neurotrophic factor in the intact adult brain, as revealed by adenovirus-mediated gene transfer. J. Neurosci. 17, 7228-7236.
35. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W., and Bates, G.P. (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.
36. Michel, R.N., Campbell, R.J., and Jasmin, B.J. (1996). Regulation of succinate dehydrogenase within muscle fiber compartments by nerve-mediated activity and CNTF. Am. J. Physiol. 270, 80-85.
37. Miller, R.G., Petajan, J.H., Bryan, W.W., Armon, C., Barohn, R.J., Goodpasture, J.C., Hoagland, R.J., Parry, G.J., Ross, M.A., and Stromatt, S.C. (1996a). A placebo-controlled trial of recombinant human ciliary neurotrophic (rhCNTF) factor in amyotrophic lateral sclerosis. rhCNTF ALS Study Group. Ann Neurol. 39, 256-260.
38. Miller, R.G., Bryan, W.W., Dietz, M.A., Munsat, T.L., Petajan, J.H., Smith, S.A., and Goodpasture, J.C. (1996b). Toxicity and tolerability of recombinant human ciliary neurotrophic factor in patients with amyotrophic lateral sclerosis. Neurology 5, 1329-1331.
39. Mullen, R.J., Buck, C.R., and Smith, A.M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211.
40. Nimchinsky, E.A., Young, W.G., Yeung, G., Shah, R.A., Gordon, J.W., Bloom, P.E., Morrison, J.H., and Hof, P.R. (2000). Differential vulnerability of occulomotor, facial, and hypoglossal nuclei in G86R superoxide dismutase transgenic mice. J. Comp. Neurol. 416, 112-125.
41. Palfi, S., Ferrante, R.J., Brouillet, E., Beal, M.F., Dolan, R. Guyot, M.C., Peschanski, M., and Hantraye, P. (1996). Chronic 3-nitropropionic acid treatment in baboons replicates the cognitive and motor deficits of Huntington's disease. J. Neurosci. 16, 3019-3025.
42. Palfi, S., Conde, F., Riche, D., Brouillet, E., Dautry, C., Mittoux, V., Chibois, A., Peschanski, M., and Hantraye, P. (1998). Fetal striatal allografts reverse cognitive deficits in a primate model of Huntington disease. Nature Med. 4, 963-966.
43. Parent, A., Cote, P.Y., and Lavoie, B. (1995). Chemical anatomy of primate basal ganglia. Prog. Neurobiol. 46, 131-197.
44. Reiner, A., Albin, R.L., Anderson, K.D., D'Amato, C.J., Penney, J.B., and Young, A.B. (1988). Differential loss of striatal projection neurons in Huntington disease. Proc. Natl. Acad. Sci. U.S.A. 85, 5733-5737.
45. Reinscheid, R.K., Nothacker, H.P., Bourson, A., Ardati, A., Henningsen, R.A., Bunzow, J.R., Grandy, D.K., Langen, H., Monsma, F.J., JR., and Civelli, O. (1995). Orphanin FQ: A neuropeptide that activates an opioid-like G protein-coupled receptor. Science 270, 792-794.
46. Saudou, P., Finkbeiner, S., Devys, D., and Greenberg, M.E. (1998). Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95, 55-66.
47. Schulz, J.B., Matthews, R.T., Klockgether, T., Dichgans, J., and Beal, M.F. (1997). The role of mitochondrial dysfunction and neuronal nitric oxide in animal models of neurodegenerative diseases. Mol. Cell. Biochem. 174, 193-197.
48. Segal, R.A., and Greenberg, M.E. (1996). Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 463-489.
49. Selemon, L.D., and Goldman-Rakic, P.S. (1985). Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 5, 776-794.
50. Selemon, L.D., Rajkowska, G., and Goldman-Rakic, P.S. (1998). Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: Application of a three-dimensional, stereologic counting method. J. Comp. Neurol. 392, 402-412.
51. Seto-Ohshima, A., Emson, P.C., Lawson, E., Mountjoy, C.Q., and Carrasco, L.H. (1988). Loss of matrix calcium-binding protein-containing neurons in Huntington's disease. Lancet 1, 1252-1255.
52. Shu, Y.S., Zhao, Z.Q., Li, M.Y., and Zhou, G.M. (1998). Orphanin FQ/nociceptin modulates glutamate-and kainic acid-induced currents in acutely isolated rat spinal dorsal horm neurons. Neuropeptides 32, 567-571.
53. Stoop, R., and Poo, M.M. (1995). Potentiation of transmitter release by ciliary neurotrophic factor requires somatic signaling. Science 267, 695-699.
54. Stoop, R., and Poo, M.M. (1996). Synaptic modulation by neurotrophic factors: Differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J. Neurosci. 16, 3256-3264.
55. Szabo, J., and Cowan, W.M. (1984). A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J. Comp. Neurol. 222, 265-300.
56. Vedel Jensen, E.B., and Gundersen, H.J.G. (1993). The rotator. J. Microsc. 171, 35-44.
57. Vonsattel, J.P., and Difiglia, M. (1998). Huntington disease. J. Neuropathol. Exp. Neurol. 57, 369-384.
58. Vonsattel, J.P., Myers, R.H., Stevens, T.J., Ferrante, R.J., Bird, E.D., and Richardson, E.P., JR. (1985). Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44, 559-577.
59. Wellington, C.L., Brinkman, R.R., O'Kusky, J.R., and Hayden, M.R. (1997). Toward understanding the molecular pathology of Huntington's disese. Brain Pathol. 7, 979-1002.
60. West, M.J., Slomianka, L., and Gundersen, H.J.G. (1991). Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anal Rec. 231, 482-497.
61. Young, W.G., Nimchinsky, E.A., Hof, P.R., Morrison, J.H., and Bloom, F.E. (1997). In NeuroZoom Software User Guide and Reference Books. (YBM Software Associates, San Diego, CA; http://neurozoom-scripps.edu) [On CD-ROM]