Cellular delivery of CNTF but not NT-4/5 prevents degeneration of striatal neurons in a rodent model of Huntington's disease

Cell Transplantation

Volumn 7, Issue 2, 1998, Pages 213-225

  Emerich, Dwaine F ^a,c   Bruhn, Susan ^a   Chu, Yaping ^b   Kordower, Jeffrey H ^b  

^a CytoTherapeutics Inc   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c ALKERMES INC   (United States)

Author keywords

CNTF; Fibroblasts; Genetic modification; Huntington's disease; Neurotrophic factor; NT 4 5; Polymer encapsulation; Quinolinic acid; Transplantation

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; NEUROTROPHIN;

ANIMAL CELL; ANIMAL MODEL; CELL TRANSPLANTATION; CONFERENCE PAPER; CORPUS STRIATUM; HUNTINGTON CHOREA; MALE; NERVE DEGENERATION; NERVE TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CELL LINE; CELL TRANSPLANTATION; CILIARY NEUROTROPHIC FACTOR; CORPUS STRIATUM; CRICETINAE; DIFFUSION CHAMBERS, CULTURE; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; HUMANS; HUNTINGTON DISEASE; MALE; NERVE DEGENERATION; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; POLYMERS; QUINOLINIC ACID; RATS; RATS, SPRAGUE-DAWLEY; TRANSFECTION;

EID: 0031920726     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0963-6897(97)00163-2     Document Type: Conference Paper

References (76)

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.; Baetge, E.E. Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amytrophic lateral sclerosis patients. Nat. Med. 2:696-699; 1996.
2. Albin, R.L.; Greenamyre, J.T. Alternative excitotoxic hypothesis. Neurology 42:733-738; 1992.
3. Alexi, T.; Venero, J.L.; Hefti, F. Protective effects of neurotrophin-4/5 and transforming growth factor-alpha on striatal neuronal phenotypic degeneration after excitotoxic lesioning with quinolinic acid. Neuroscience 78:73-86; 1997.
4. Anderson, K.D.; Panayotatos, N.; Cordoran, T.L.; Lindsay, R.M.; Wiegand, S.J. Ciliary neurotrophic factor protects striatal output neurons in an animal model of Huntington's disease. Proc. Natl. Acad. Sci. USA 93:7346-7351; 1996.
5. Apfel, S.C.; Arezzo, J.C.; Moran, M.; Kessler, J.A. Effects of administration of ciliary neurotrophic factor on normal motor and sensory peripheral nerves in vivo. Brain Res. 604:1-6; 1993.
6. Arakawa, Y.; Sendtner, M.; Thoenen, H. Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: Comparison with other neurotrophic factors and cytokines. J. Neurosci. 10:3507-3515; 1990.
7. Ardelt, A.A.; Flaris, N.A.; Roth, K.A. Neurotrophin-4 selectively promotes survival of striatal neurons in organotypic slice culture. Brain Res. 647:340-344; 1994.
8. Baetge, E.E.; Suh, Y.H.; Joh, T.H. Complete nucleotide and deduced amino acid sequence of bovine phenylethanolamine N-methyltransferase: Partial homology with rat tyrosine hydroxylase. Proc. Natl. Acad. Sci. USA 83: 5454-5458; 1986.
9. Beal, M.F.; Kowall, N.W.; Ellison, D.W.; Mazurek, M.F.; Swartz, K.J.; Martin, J.B. Replication of the neurochemical characteristics Huntington's disease by quinolinic acid. Nature 321:168-171; 1986.
10. 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. 23:562-569; 1988.
11. Beal, M.F.; Kowall, N.W.; Swartz, K.J.; Ferranti, R.J.; Martin, J.B. Differential sparing of somatostatin-neuropeptide Y and cholinergic neurons following striatal excitotoxin lesions. Synapse 3:38-47; 1989.
12. Beal, M.F. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neurol. 31:119-130; 1992.
13. Bird, E.D. Chemical pathology of Huntington's disease. Annu. Rev. Pharmacol. Toxicol. 20:533-551; 1980.
14. Buck, S.H.; Burks, T.F.; Brown, M.R.; Yamamura, H.I. Reduction in basal ganglia and substantia nigra substance P levels in Huntington's disease. Brain Res. 209:464-469; 1981.
15. Buisson, A.; Pateau, V.; Plotkine, M.; Boulu, R.G. Nigrostriatal pathway modulates striatum vulnerability to quinolinic acid. Neurosci. Lett. 131:257-259; 1991.
16. Cabasso, I. Hollow fiber membranes. In: Kirk Othmer (ed). Encyclopedia of chemical technology, vol. 12. New York: John Wiley; 1980:492-517.
17. Choi, D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634; 1988.
18. 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 90:2222-2226; 1993.
19. DiFiglia, M. Excitotoxic injury of the neostriaum: A model for Huntington's disease. Trends Neurosci. 13:286-289; 1990.
20. Emerich, D.F.; Sanberg, P.R. Animal models in Huntington's disease. In: Boulton, A.A.; Baker, G.B.; Butterworth, R.F., eds. Neuromethods, vol. 17, Animal models of neurological disease. Clifton, NJ: Humana Press; 1992:65-134.
21. Emerich, D.F.; Frydel, B.; McDermott, P.; Krueger, P.; Lavoie, M.; Sanberg, P.R.; Winn, S.R. Polymer-encapsulated PC 12 cells promote recovery of motor function in aged rats. Exp. Neurol. 122:37-47; 1993.
22. Emerich, D.F.; Winn, S.R.; Harper, J.; Hammang, J.P.; Baetge, E.E.; Kordower, J.H. Transplantation of polymer-encapsulated cells genetically modified to secrete human nerve growth factor prevents the loss of degenerating cholinergic neurons in nonhuman primates. J. Comp. Neurol. 349:148-164; 1994.
23. 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. 130:141-150; 1994.
24. Emerich, D.F.; Lindner, M.D.; Winn, S.R.; Chen, E.-Y.; Frydel, B.R.; Kordower, J.H. Implants of encapsulated CNTF-producing fibroblasts prevent behavioral deficits and striatal degeneration in a rodent model of Huntington's disease. J. Neurosci. 16:5168-5181; 1996.
25. 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. 6:249-266; 1997.
26. Emerich, D.F.; Winn, S.R.; Chen, E.-Y.; Chu, Y.; McDermott, P.; Baetge, E.; Kordower, J.H. Protection of basal ganglia circuitry by encapsulated CNTF-producing cells in a primate model of Huntington's disease. Nature 386:395-399; 1997.
27. Ferrante, R.J.; Beal, M.F.; Kowall, N.W.; Richardson, E.P.; Martin, J.B. Sparing of acetylcholinesterase-containing striatal neurons in Huntington's disease. Brain Res. 415:178-182; 1987.
28. Forger, N.G.; Roberts, S.L.; Wong, V.; Breedlove, S.M. Ciliary neurotrophic factor maintains motoneurons and their target miscles in developing rats. J. Neurosci. 13: 4720-4726; 1993.
29. Frim, D.M.; Schumacher, J.M.; Short, M.P.; Breakefield, X.O.; Isacson, O. Local response to intracerebral grafts of NGF-secreting fibroblasts: Induction of a peroxidative enzyme. Soc. Neurosci. Abstr. 18:1100; 1992.
30. Frim, D.M.; Uhler, T.A.; Short, M.P.; Exxedine, Z.D.; Klagsbrun, M.; Breakefield, X.O.; Isacson, O. Effects of biologically delivered NGF, BDNF, and bFGF on striatal excitotoxic lesions. Neuroreport 4:367-370; 1993.
31. Frim, D.M.; Simpson, J.; Uhler, T.A.; Short, M.P.; Bossi, S.R.; Breakefield, X.O.; Isacson, O. Striatal degeneration induced by mitochondrial blockade is prevented by biologically delivered NGF. J. Neurosci. Res. 35:452-458; 1993.
32. 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 8:145-158; 1993.
33. Hagg, T.; Varon, S. Ciliary neurotrophic factor prevents degeneration of adult rat substantia nigra dopaminergic neurons in vivo. Proc. Natl. Acad. Sci. USA 90:6315-6319; 1993.
34. Hsu, S.M.; Raine, L.; Fanger, H. Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques. A comparison between ABC and unlabeled antibody (PAP) procedurese. J. Histochem. Cytochem. 29: 577-580; 1981.
35. Hyman, C.; Juhasz, M.; Jackson, C.; Wright, P.; Ip, N.Y.; Lindsay, R.M. Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon. J. Neurosci. 14:335-347; 1994.
36. Hynes, M.A.; Poulsen, K.; Armanini, M.; Berkmeier, L.; Phillips, H.; Rosenthal, A. Neurotrophin-4/5 is a survival factor for embryonic midbrain dopaminergic neurons in enriched cultures. J. Neurosci. Res. 37:144-154; 1994.
37. Jackson, G.; Apfe, L.; Werrbach-Perez, K.; Perez-Polo, J.R. Role of nerve growth factor in oxidant-antioxidant balance and neuronal injury. I. Stimulation of hydrogen peroxide resistancee. J. Neurosci. Res. 25:360-368; 1990.
38. Kirk, R.E. Experimental design: Procedures for the behavioral sciences. Pacific Grove, CA: Brooks/Cole Publishing Company; 1992.
39. Kordower, J.H.; Winn, S.R.; Liu, Y-T.; Mufson, E.J.; Sladek, J.R., Jr.; Baetge, E.E.; Hammang, J.P.; Emerich, D.F. The aged monkey basal forebrain: Rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc. Natl. Acad. Sci. USA 91:10898-10902; 1994.
40. 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 NGF: Trophic effects upon cholinergic and noncholinergic neurons. Neuroscience 72:63-77; 1996.
41. Kordower, J.H.; Chen, E.-Y.; Carpenter, M.; Messing, A.; Mufson, E.J.; Charles, V.; Rosenstein, J.M.; Winkler, C.; Fricker, C.; Bjorklund, A.; Emerich, D.F.; Hammang, J. Grafts of stem cells genetically modified to secrete NMGF: Neuronal rescue, neurite sprouting, and preservation of the blood-brain barrier in a rodent model of Huntington's disease. J. Comp. Neurol. 387:96-113; 1997.
42. Kumon, Y.; Sakaki, S.; Watanabe, H.; Nakano, K.; Ohta, S.; Matsuda, S.; Yoshimura, H.; Sakanaka, M. Ciliary neurotrophic factor attenuates spatial cognition impairment, cortical infarction, and thalamic degeneration in spontaneously hypertensive rats with focal ischemia. Neurosci. Lett. 206:141-144; 1996.
43. Lin, L.-F.H.; Mismer, D.; Lile, J.D.; Armes, L.G.; Butler, E.T.; Vannice, J.L.; Collins, F. Purification, cloning, and expression of ciliary neurotrophic factor (CNTF). Science 246:1023-1025; 1989.
44. Lindner, M.D.; Kearns, C.E.; Winn, S.R.; Frydel, B.R.; Emerich, D.F. Effects of intraventricular encapsulated hNGF-secreting fibroblasts in aged rats. Cell Transplant. 5:205-223; 1996.
45. Lotz, B.; Brooks, B.; Sanjak, M.; Weasler, C.; Roelke, K.; Parnell, J.; Neville, H.; Ringel, S.; Brinkman, J.; Singh, K.; Burns, D.; Pestronk, A.; Lopate, G.; Florence, J.; Blume, G.; Eliot, J.; Mitsumoto, H.; Levin, K.; Szirony, K.; Caldwell, M.; Bosch, P.; Smith, B.; Verheijde, J.; Carr, S.; Engel, W.K.; Velazquez, L.; Miller, J.; Graves, M.; Sepulveda, L.; Garcia, S.; Smith, R.; Licht, J.; Gillie, E.; Silverman, L.; Olney, R.; Yuen, E.; Melnick, M.; Mass, J.; Bradley, W.; Sharma, K.; Hurtak, L.; Mayor, L.; Olanow, C.W.; Hauser, R.; Malapira, T.; Olanow, E.; Hopkins, L.; Weissman, J.; Pianta, T. A double-blind placebo controlled clinical trials of subcutaneous recombinant human ciliary neurotrophic factor (rhCNTF) in amyotrophic lateral sclerosis. Neurology 46:1244-1249; 1996.
46. MacLennan, J.A.; Vinson, E.N.; Marks, L.; McLaurain, D.L.; Pfiefer, M.; Lee, M. Immunohistochemical localization of ciliary neurotrophic factor receptor alpha expression in the rat nervous system. J. Neurosci. 16:621-630; 1996.
47. Martin, J.B.; Gusela, J.F. Huntington's disease: Pathogenesis and management. N. Engl. J. Med. 315:1267-1276; 1986.
48. Martinez-Serrano, A.; Bjorklund, A. Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified sneural stem cells. J. Neurosci. 16:4604-4616; 1996.
49. Masu, Y.; Wolf, E.; Holtmann, B.; Sendtner, M.; Brem, G.; Thoenen, H. Disruption of the CNTF gene results in motor neuron degeneration. Nature 365:27-32; 1993.
50. Mattson, M.P.; Murrain, M.; Guthrie, P.B.; Kater, S.B. Fibroblast growth factor and glutamate: Opposing roles ion the generation and degeneration of hippocampal neuroarchitecture. J. Neurosci. 9:3728-3743; 1989.
51. Mattson, M.P.; Cheng, B.; Smith-Swintosky, V.L. Mechanisms of neurotrophic factor protection against calcium-and free radical-mediated excitotoxic injury: Implications for treating neurodegenerative disorders. Exp. Neurol. 124:89-95; 1993.
52. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem. 65:1740-1751; 1995.
53. Olney, J.W. Excitatory amino acids and neuropsychiatric disorders. Biol. Psychiatry 26:505-525; 1989.
54. Oppenheim, R.W.; Prevette, D.; Qin-Wei, Y.; Collins, F.; MacDonald, J. Control of embryonic motoneuron survival in vivo by ciliary neuortrophic factor. Science 251:1616-1618; 1991.
55. Parker, W.D.; Boyson, S.J.; Luder, A.S.; Parks, J.K. Evidence for a defect on NADH: Ubiquinone oxidoreductase (complex I) in Huntington's disease. Neurology 40: 1231-1234; 1990.
56. Paxinos, G.; Watson, C. The rat brain in stereotaxic coordinates. Sydney: Academic Press; 1984.
57. Reiner, A.; Albin, D.L.; Anderson, K.D.; D'Amato, C.J.; Penny, J.B.; Young, A.B. Differential loss of striatal projection neurons in Huntington's disease. Proc. Natl. Acad. Sci. USA 85:5733-5737; 1988.
58. Roberts, R.C.; DiFiglia, M. Short- and long-term survival of large neurons in the excitotoxic lesioned rat caudate nucleus: A light and electron microscopic study. Synapse 3:363-371; 1989.
59. Rothman, S.M. The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J. Neurosci. 5:1483-1490; 1985.
60. Rudge, J.S.; Li, Y.; Pasnikowski, E.M.; Mattson, K.; Pan, L.; Yancopoulos, G.D.; Wiegand, S.J.; Lindsay, R.M.; Ip, N.Y. Neurotrophic factor receptors and their signal transduction capabilities in rat astrocytes. Eur. J. Neurosci. 6:693-705; 1994.
61. SAS Institute Inc.e SAS/STAT user's guide, version 6, 4th ed., vol. 1. Cary, NC: SAS Institute Inc; 1989.
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 45:561-70; 1991.
63. + pump necessary for NGF mediated neuronal survival? J. Neurosci. 8:458-462; 1988.
64. Sendtner, M.; Kreutzberg, G.W.; Thoenen, H. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345:440-341; 1990.
65. Sendtner, M.; Schmalbruch, H.; Stockli, K.A.; Carroll, P.; Kreutzberg, G.W.; Thoenen, H. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronpathy. Nature 358:502-504; 1992.
66. Stockli, K.A.; Lottspeich, F.; Sendtner, M.; Masiakowski, P.; Carrol, P.; Gotz, R.; Lindholm, D.; Thoenen, H. Molecular cloning, expression, and regional distribution of rat ciliary neurotrophic factor. Nature 342:920-923; 1989.
67. Stockli, K.A.; Lillien, L.E.; Naher-Noe, M.; Breitfeld, G.; Hughes, R.A.; Raff, M.C.; Thoenen, H.; Sendtner, M. Regional distribution, developmental changes and cellular localization of CNTF-mRNA and protein in the rat brain. J. Cell Biol. 115:447-459; 1991.
68. Tatter, S.B.; Gelpern, W.R.; Isacson, O. Neurotrophic factor protection against excitotoxic neuronal death. Neuroscientist 1:286-297; 1995.
69. Timmusk, T.; Belluardo, N.; Metsis, M.; Persson, H. Widespread and developmentally regulated expression of neurotrophin-4 mRNA in rat brain and peripheral tissues. Eur. J. Neurosci. 5:605-613; 1993.
70. Ulenkate, H.J.L.M.; Kaal, E.C.A.; Jennekens, F.G.I. Ciliary neurotrophic factor induces hypophagia, hypodipsia, and diminished weight gain in young adult rats. Neurosci. Res. Commun. 16:67-74; 1995.
71. Wallace, D.C. Mitochondrial genetics: A paradigm for aging and degenerative diseases? Science 256:628-632; 1992.
72. Wen, T.C.; Matsuda, S.; Yoshimura, H.; Kawabe, T.; Sakanaka, M. Ciliary neurotrophic factor prevents isch-emia-induced learning disability and neuronal loss in gerbils. Neurosci. Lett. 191:55-58; 1995.
73. Widmer, H.R.; Hefti, F. Neurotrophin-4/5 promotes survival and differentiation of rat striatal neurons developing in culture. Eur. J. Neurosci. 6:1669-1679; 1994.
74. Winn, S.R.; Hammang, J.P.; Emerich, D.F.; Lee, A.; Palmiter, R.D.; Baetge, E.E. Polymer-encapsulated cells genetically modified to secrete human nerve growth factor promote the survival of axotomized septal cholinergic neurons. Proc. Natl. Acad. Sci. USA 91:23-28; 1994.
75. Winn, S.R.; Lindner, M.D.; Francis, J.M.; Haggett, G.; Greco, C.; Frydel, B.; Emerich, D.F. Encapsulated engineered cells continue to secrete human nerve growth factor for over one year in rat ventricles: A behavioral and anatomical analysis. Exp. Neurol. 140:126-138; 1996.
76. Young, W.G.; Morrison, J.H.; Hof, P.Q.; Nimchinski, E.A.; Bloom, F.E. NeuroZoom - Topographical mapping and stereological counting, distribution of data and collaboraive computing. Soc. Neurosci. Abstr. 22:1238; 1996.