Cellular delivery of trophic factors for the treatment of Huntington's disease: Is neuroprotection possible?

Experimental Neurology

Volumn 159, Issue 1, 1999, Pages 4-20

  Kordower, Jeffrey H ^a   Isacson, Ole ^b   Emerich, Dwaine F ^c  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b MCLEAN HOSPITAL   (United States)

^c ALKERMES INC   (United States)

Author keywords

CNTF; Dementia; GABA; NGF; Striatum; Transplantation

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR;

CORPUS STRIATUM; GENE TARGETING; GENE THERAPY; HUMAN; HUNTINGTON CHOREA; NERVE DEGENERATION; NERVE GRAFT; NERVE TRANSPLANTATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0032826920     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7156     Document Type: Article

References (73)

1. Albin R. L., Young A. B., Penney J. B., Handelin B., Balfour R., Anderson K. D., Markel D. S., Tourtellotte W. W., Reiner A. Abnormalities of striatal projection neurons and N-methyl-d-aspartate receptors in presymptomatic Huntington's disease [see comments]. N. Engl. J. Med. 322:1990;1293-1298.
2. Albin R. L., Reiner A., Anderson K. D., Dure L. S., Handelin B., Balfour R., Whetsell W. O. J., Penney J. B., Young A. B. Preferential loss of striato-external pallidal projection neurons in presymptomatic Huntington's disease. Ann. Neurol. 31:1992;425-430.
3. Albin R. L., Greenamyre J. T. Alternative excitotoxic hypotheses. Neurology. 42:1992;733-738.
4. 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. USA. 93:1996;7346-7351.
5. Ashizawa T., Wong L. J., Richards C. S., Caskey C. T., Jankovic J. CAG repeat size and clinical presentation in Huntington's disease. Neurology. 44:1994;1137-1143.
6. Bamford K. A., Caine E. D., Kido D. K., Plassche W. M., Shoulson I. Clinical-pathologic correlation in Huntington's disease: A neuropsychological and computed tomography study. Neurology. 39:1989;796-801.
7. Beal M. F., Kowall N. W., Ellison D. W., Mazurek M. F., Swartz K. J., Martin J. B. Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature. 321:1986;168-171.
8. Beal M. F., Mazurek M. F., Ellison D. W., Swartz K. J., Mcgarvey U., Bird E. D., Martin J. B. Somatostatin and neuropeptide Y concentrations in pathologically graded cases of Huntington's disease. Ann. Neurol. 23:1988;562-569.
9. Beal M. F., Brouillet E., Jenkins B. G., Ferrante R. J., Kowall N. W., Miller J. M., Storey E., Srivastava R., Rosen B. R., Hyman B. T. Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurosci. 13:1993;4181-4192.
10. Bjorklund A., Campbell K., Sirinathsinghji D. J., Fricker R. A., Dunnett S. B. Functional capacity of striatal transplants in the rat Huntington model. Dunnett S. B., Bjorklund A. Functional Neural Transplantation. 1994;157-195 Raven Press, New York.
11. Block F., Kunkel M., Schwarz M. Quinolinic acid lesion of the striatum induces impairment in spatial learning and motor performance in rats. Neurosci. Lett. 149:1993;126-128.
12. Calne D. B., Langston J. W. Aetiology of Parkinson's disease. Lancet. 2:1983;1457-1459.
13. Clatterbuck R. E., Price D. L., Koliatsos V. E. Ciliary neurotrophic factor prevents retrograde neuronal death in the adult central nervous system. Proc. Natl. Acad. Sci. USA. 90:1993;2222-2226.
14. Conneally P. M. Huntington disease: Genetics and epidemiology. Am. J. Hum. Genet. 36:1984;506-526.
15. Coyle J. T., Schwarcz R. Lesion of striatal neurones with kainic acid provides a model for Huntington's chorea. Nature. 263:1976;244-246.
16. Davies S. W., Beardsall K. Nerve growth factor selectively prevents excitotoxin induced degeneration of striatal cholinergic neurones. Neurosci. Lett. 140:1992;161-164.
17. Emerich D. F., Hammang J. P., Baetge E. E., Winn S. R. Implantation of polymer-encapsulated human nerve growth factor-secreting fibroblasts attenuates the behavioral and neuropathological consequences of quinolinic acid injections into rodent striatum. Exp. Neurol. 130:1994;141-150.
18. Emerich D. F., Bruhn S., Chu Y., Kordower J. H. Cellular delivery of CNTF, but not NT-4/5 prevents degeneration of striatal neurons in a rodent model of Huntington's disease. Cell Transplant. 1999.
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., and P. R. Sanberg. 1992. Animal models in Huntington's disease. Pages 65-134 in A. A. Boulton, G. B. Baker, and R. F. Butterworth, Eds., Neuromethods, Vol. 17. Humana Press, Clifton, NJ.
22. 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.
23. Farrer L. A., Conneally P. M. A genetic model for age at onset in Huntington disease. Am. J. Hum. Genet. 37:1985;350-357.
24. Ferrante R. J., Kowall N. W., Beal M. F., Richardson E. P. J., Bird E. D., Martin J. B. Selective sparing of a class of striatal neurons in Huntington's disease. Science. 230:1985;561-563.
25. Ferrante R. J., Beal M. F., Kowall N. W., Richardson E. P. J., Martin J. B. Sparing of acetylcholinesterase-containing striatal neurons in Huntington's disease. Brain Res. 411:1987;162-166.
26. Freese A., Finklestein S. P., Difiglia M. Basic fibroblast growth factor protects striatal neurons in vitro from NMDA-receptor mediated excitotoxicity. Brain Res. 575:1992;351-355.
27. Frim D. M., Simpson J., Uhler T. A., Short M. P., Bossi S. R., Breakfield X. O., Isacson O. Striatal degeneration induced by mitochondrial blockade is prevented by biologically delivered NGF. J. Neurosci. Res. 35:1993;452-458.
28. Frim D. M., Uhler T. A., Short M. P., Ezzedine Z. D., Klagsbrun M., Breakefield X. O., Isacson O. Effects of biologically delivered NGF, BDNF and bFGF on striatal excitotoxic lesions. NeuroReport. 4:1993;367-370.
29. Frim D. M., Yee W. M., Isacson O. NGF reduces striatal excitotoxic neuronal loss without affecting concurrent neuronal stress. NeuroReport. 4:1993;655-658.
30. Frim D. M., Short M. P., Rosenberg W. S., Simpson J., Breakfield X. O., Isacson O. Local protective effects of nerve growth factor-secreting fibroblasts against excitotoxic lesions in the rat striatum [see comments]. J. Neurosurg. 78:1993;267-273.
31. Frim D. M., Wullner U., Beal M. F., Isacson O. Implanted NGF-producing fibroblasts induce catalase and modify ATP levels but do not affect glutamate receptor binding or NMDA receptor expression in the rat striatum. Exp. Neurol. 128:1994;172-180.
32. Gage F. H., Batchelor P., Chen K. S., Chin D., Higgins G. A., Koh S., Deputy S., Rosenberg M. B., Fischer W., Bjorklund A. NGF receptor reexpression and NGF-mediated cholinergic neuronal hypertrophy in the damaged adult neostriatum. Neuron. 2:1989;1177-1184.
33. Galpern W. R., Matthews R. T., Beal M. F., Isacson O. NGF attenuates 3-nitrotyrosine formation in a 3-NP model of Huntington's disease. NeuroReport. 7:1996;2639-2642.
34. Graveland G. A., Williams R. S., Difiglia M. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science. 227:1985;770-773.
35. Greenamyre J. T., Shoulson I. Huntington's disease. Calne D. Neurodegenerative Diseases. 1994;685-704 Saunders, Philadelphia.
36. Hagg T., Quon D., Higaki J., Varon S. Ciliary neurotrophic factor prevents neuronal degeneration and promotes low affinity NGF receptor expression in the adult rat CNS. Neuron. 8:1992;145-158.
37. Hagg T., Varon S. Ciliary neurotrophic factor prevents degeneration of adult rat substantia nigra dopaminergic neurons in vivo. Proc. Natl. Acad. Sci. USA. 90:1993;6315-6319.
38. Higgins G. A., Koh S., Chen K. S., Gage F. H. NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat. Neuron. 3:1989;247-256.
39. Huntington's Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell72: 971-978.
40. Isacson O. On neuronal health. Trends Neurosci. 16:1993;306-308.
41. Isacson O., Brundin P., Kelly P. A., Gage F. H., Bjorklund A. Functional neuronal replacement by grafted striatal neurones in the ibotenic acid-lesioned rat striatum. Nature. 311:1984;458-460.
42. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J. C., Smith C. D., Beckman J. S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298:1992;431-437.
43. Kordower J. H., Mufson E. J. NGF receptor (p75)-immunoreactivity in the developing primate basal ganglia. J. Comp. Neurol. 327:1993;359-375.
44. Kordower J. H., Chen E. Y., Sladek J. R. J., Mufson E. J. Trk-immunoreactivity in the monkey central nervous system: Forebrain. J. Comp. Neurol. 349:1994;20-35.
45. Kordower J. H., Charles V., Bayer R., Bartus R. T., Putney S., Walus L. R., Friden P. M. Intravenous administration of a transferrin receptor antibody-nerve growth factor conjugate prevents the degeneration of cholinergic striatal neurons in a model of Huntington disease. Proc. Natl. Acad. Sci. USA. 91:1994;9077-9080.
46. Kordower J. H., Chen E. Y., Mufson E. J., Winn S. R., Emerich D. F. Intrastriatal implants of polymer encapsulated cells genetically modified to secrete human nerve growth factor: Trophic effects upon cholinergic and noncholinergic striatal neurons. Neuroscience. 72:1996;63-77.
47. Kordower J. H., Chen E. Y., Winkler C., Fricker R., Charles V., Messing A., Mufson E. J., Wong S. C., Rosenstein J. M., Bjorklund A., Emerich D. F., Hammang J., Carpenter M. K. Grafts of EGF-responsive neural stem cells derived from GFAP-hNGF transgenic mice: Trophic and tropic effects in a rodent model of Huntington's disease. J. Comp. Neurol. 387:1997;96-113.
48. Kowall N. W., Ferrante R. J., Martin J. B. Pattern of cell loss in Huntington's disease. Trends Neurosci. 10:1987;24-29.
49. Levi-Montalcini R., Aangeletti P. U. Nerve growth factor. Physiol. Rev. 48:1968;534-569.
50. Lindsay R. M., Wiegand S. J., Altar C. A., Distephano P. S. Neurotrophic factors, from molecules to man. Trends Neurosci. 17:1994;182-190.
51. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S. W., Bates G. P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 87:1996;493-506.
52. Martin J. B., Gusella J. F. Huntington's disease. Pathogenesis and management. N. Engl. J. Med. 315:1986;1267-1276.
53. Martinez-Serrano A., Bjorklund A. Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified neural stem cells. J. Neurosci. 16:1996;4604-4616.
54. Martinez H. J., Dreyfus C. F., Jonakait G. M., Black I. B. Nerve growth factor promotes cholinergic development in brain striatal cultures. Proc. Natl. Acad. Sci. USA. 82:1985;7777-7781.
55. Mizuno K., Carnahan J., Nawa H. Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev. Biol. 165:1994;243-256.
56. Mobley W. C., Rutkowski J. L., Tennekoon G. I., Buchanan K., Johnston M. V. Choline acetyltransferase activity in striatum of neonatal rats increased by nerve growth factor. Science. 229:1985;284-287.
57. Mufson E. J., Kordower J. H. Nerve growth factor and its receptors in the primate forebrain: Alterations in Alzheimer's disease and potential use in experimental therapeutics. Mattson M. Neuroprotective Signal Transduction. 1999;Humana Press, Clifton.
58. Nakao N., Brundin P., Funa K., Lindvall O., Odin P. Trophic and protective actions of brain-derived neurotrophic factor on striatal DARPP-32-containing neurons in vitro. Brain Res. Dev. Brain Res. 90:1995;92-101.
59. Nistico G., Ciriolo M. R., Fiskin K., Iannone M., Martino A. De, Rotilio G. NGF restores decrease in catalase activity and increases superoxide dismutase and glutathione peroxidase activity in the brain of aged rats. Free Radical Biol. Med. 12:1992;177-181.
60. Pelleymounter M. A., Cullen M. J., Baker M. B., Gollub M., Wellman C. The effects of intrahippocampal BDNF and NGF on spatial learning in aged Long Evans rats. Mol. Chem. Neuropathol. 29:1996;211-226.
61. Schulz J. B., Matthews R. T., Jenkins B. G., Ferrante R. J., Siwek D., Henshaw D. R., Cipolloni P. B., Mecocci P., Kowall N. W., Rosen B. R. Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J. Neurosci. 15:1995;8419-8429.
62. Schumacher J. M., Short M. P., Hyman B. T., Breakefield X. O., Isacson O. Intracerebral implantation of nerve growth factor-producing fibroblasts protects striatum against neurotoxic levels of excitatory amino acids. Neuroscience. 45:1991;561-570.
63. Shannon K. M., Kordower J. H. Neural transplantation for Huntington's disease: Experimental rationale and recommendations for clinical trials. Cell Transplant. 5:1996;339-352.
64. Simpson J. R., Isacson O. Mitochondrial impairment reduces the threshold for in vivo NMDA-mediated neuronal death in the striatum. Exp. Neurol. 121:1993;57-64.
65. Sims N. R., Bowen D. M., Allen S. J., Smith C. C., Neary D., Thomas D. J., Davison A. N. Presynaptic cholinergic dysfunction in patients with dementia. J. Neurochem. 40:1983;503-509.
66. Sobreviela T., Clary D. O., Reichardt L. F., Brandabur M. M., Kordower J. H., Mufson E. J. TrkA-immunoreactive profiles in the central nervous system: Colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J. Comp. Neurol. 350:1994;587-611.
67. Steininger T. L., Wainer B. H., Klein R., Barbacid M., Palfrey H. C. High-affinity nerve growth factor receptor (Trk) immunoreactivity is localized in cholinergic neurons of the basal forebrain and striatum in the adult rat brain. Brain Res. 612:1993;330-335.
68. + pump may mediate the control of nerve cells by nerve growth factor. Trends Biol. Sci.22-25.
69. Venero J. L., Beck K. D., Hefti F. Intrastriatal infusion of nerve growth factor after quinolinic acid prevents reduction of cellular expression of choline acetyltransferase messenger RNA and trkA messenger RNA, but not glutamate decarboxylase messenger RNA. Neuroscience. 61:1994;257-268.
70. Ventimiglia R., Mather P. E., Jones B. E., Lindsay R. M. The neurotrophins BDNF, NT-3 and NT-4/5 promote survival and morphological and biochemical differentiation of striatal neurons in vitro. Eur. J. Neurosci. 7:1995;213-222.
71. Vonsattel J. P., Myers R. H., Stevens T. J., Ferrante R. J., Bird E. D., Richardson E. P. J. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44:1985;559-577.
72. Widmer H. R., Hefti F. Neurotrophin-4/5 promotes survival and differentiation of rat striatal neurons developing in culture. Eur. J. Neurosci. 6:1994;1669-1679.
73. Winn S. R., Lindner M. D., Lee A., Haggett G., Francis J. M., Emerich D. F. Polymer-encapsulated genetically modified cells continue to secrete human nerve growth factor for over one year in rat ventricles: Behavioral and anatomical consequences. Exp. Neurol. 140:1996;126-138.