Transplanted neurons alter the course of neurodegenerative disease in Lurcher mutant mice

Experimental Neurology

Volumn 154, Issue 2, 1998, Pages 336-352

  Heckroth, John A ^a   Hobart, Nancy J H ^a   Summers, Donald ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebellum; Inferior olive; Lurcher; Neural transplantation; NSE LacZ; Purkinje cell

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL TRANSPLANTATION; CEREBELLUM; CONTROLLED STUDY; DEGENERATIVE DISEASE; EMBRYO; EMBRYO CELL; INFERIOR OLIVE; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL;

EID: 0032410567     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1998.6960     Document Type: Article

References (82)

1. Alvarado-Mallart R.-M., Sotelo C. Cerebellar grafting in murine heredodegenerative ataxia: Current limitations for a therapeutic approach. Adv. Neurol. 61:1993;181-192.
2. Anton R., Kordower J. H., Maidment N. T., Manaster J. S., Kane D. J., Rabizadeh S., Schueller S. B., Yang J., Edwards R. H., Markham C. H., Bredesen D. E. Neural-targeted gene therapy for rodent and primate hemiparkinsonism. Exp. Neurol. 127:1994;207-218.
3. Arenas E., Person H. Neurotrophin-3 prevents the death of adult central noradrenergic neuronsin vivo. Nature. 367:1994;368-371.
4. Bayer S. A., Altman J. Directions in neurogenetic gradients and patterns of anatomical connections in the telencephalon. Prog. Neurobiol. 29:1987;57-106.
5. Bregman B. S., Kunkle-Bagden E. Effect of target and non-target transplants on neuronal survival and axonal elongation after injury to the developing spinal cord. Prog. Brain Res. 78:1988;205-211.
6. Bregman B. S., Reier P. J. Neural tissue transplants rescue axotomized rubrospinal cells from retrograde death. J. Comp. Neurol. 244:1986;86-95.
7. Caddy K. W. T., Biscoe T. J. Structural and quantitative studies on the normal C3H and lurcher mutant mouse. Phil. Trans. Roy. Soc. London, Series B. 287:1979;167-201.
8. Chang A. C., Triarhou L. C., Alyea C. J., Low W. C., Ghetti B. Developmental expression of polypeptide PEP-19 in cerebellar cell suspensions transplanted into the cerebellum of pcd mutant mice. Exp. Brain Res. 76:1989;639-645.
9. Chen S., Hillman D. E. Regulation of granule cell number by a predetermined number of Purkinje cells in development. Dev. Brain Res. 45:1989;137-147.
10. Cunningham T. J., Sutilla C. B., Haun F. Trophic effects of transplants following damage to the cerebral cortex. Ann. N.Y. Acad. Sci. 495:1987;153-168.
11. Das G. D., Hallas B. H. Transplantation of brain tissue in the brain of adult rats. Experientia. 34:1978;1304-1306.
12. Das G. D., Pfaffenroth M. J. Experimental studies on the postnatal development of the brain. III. Cerebellar development following localized administration of ENU. Neuropath. Appl. Neurobiol. 3:1977;191-212.
13. Dumesnil-Bousez N., Sotelo C. Early development of the Lurcher cerebellum: Purkinje cell alterations and impairment of synaptogenesis. J. Neurocytol. 21:1992;506-529.
14. Dumesnil-Bousez N., Sotelo C. Partial reconstruction of the adult Lurcher cerebellar circuitry by neural grafting. Neuroscience. 55:1993;1-21.
15. Dunnett S. B., Richards S.-J. Neural Transplantation. From Molecular Basis to Clinical Applications. Progress in Brain Research. 1990;Elsevier, Amsterdam.
16. Fire A. Histochemical techniques for locating echerichia coli beta-galactosidase activity in transgenic organisms. Genet. Anal. Tech. Appl. 9:1992;151-158.
17. Fishell G. Striatal precursors adopt cortical identities in response to local cues. Development. 121:1995;803-812.
18. Fisher M., Trimmer P., Ruthel G. Bergmann glia require continuous association with Purkinje cells for normal phenotype expression. Glia. 8:1993;172-182.
19. Forss-Petter S., Danielson P. E., Catsicas S., Battenberg E., Price J., Nerenberg M., Sutcliffe J. G. Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron. 5:1990;187-197.
20. Garcia-Segura L. M., Baetens D., Roth J., Norman A. W., Orci L. Immunohistochemical mapping of calcium-binding protein immunoreactivity in the rat central nervous system. Brain Res. 296:1984;75-86.
21. Gardette R., Alvarado-Mallart R. M., Crepel F., Sotelo C. Electrophysiological demonstration of a synaptic integration of transplanted Purkinje cells into the cerebellum of the adult Purkinje cell degeneration mutant mouse. Neuroscience. 24:1988;777-789.
22. Gardette R., Crepel F., Alvarado-Mallart R. M., Sotelo C. Fate of grafted embryonic Purkinje cells in the cerebellum of the adult "Purkinje cell degeneration" mutant mouse. II. Development of synaptic responses: Anin vitro. J. Comp. Neurol. 295:1990;188-196.
23. Gash D., Sladek J. R. Transplantation into the Mammalian CNS. Progress in Brain Research. 1988;Elsevier, Amsterdam.
24. Gash D. M. Neural transplants in mammals: A historical overview. Neural Transplants: Development and Function. 1984;Plenum Press, New York. p. 1-12.
25. Ghetti B., Triarhou L. C., Alyea C. J., Low W. C., Chang A. C. Timing of neuronal replacement in cerebellar degenerative ataxia of Purkinje cell type. Prog. Brain Res. 82:1990;197-202.
26. Heckroth J. A. Development of glutamic acid decarboxylase-immunoreactive elements in the cerebellar cortex of normal and lurcher mutant mice. J. Comp. Neurol. 315:1992;85-97.
27. Heckroth J. A., Eisenman L. M. Olivary morphology and olivocerebellar topography in adult lurcher mutant mice. J. Comp. Neurol. 312:1991;641-651.
28. Heckroth J. A., Goldowitz D., Eisenman L. M. Olivocerebellar fiber maturation in normal and lurcher mutant mice: Defective development in lurcher. J. Comp. Neurol. 291:1990;415-430.
29. Herrup K., Mullen R. J. Staggerer chimeras: Intrinsic nature of Purkinje cell defects and implications for normal cerebellar development. Brain Res. 178:1979;443-457.
30. Herrup K., Sunter K. Numerical matching during cerebellar development: Quantitative analysis of granule cell death in staggerer mouse chimeras. J. Neurosci. 7:1987;829-836.
31. Hofer M., Pagliusi S., Hohn A., Leibrock J., Barde Y. A. Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 9:1990;2459-2464.
32. Kawamura K., Nanami T., Kikuchi Y., Kitakami A. Grafted granule and Purkinje cells can migrate into the mature cerebellum of normal adult rats. Exp. Brain Res. 70:1988;477-484.
33. Kromer L. E., Bjorklund A., Stenevi U. Intracephalic implants: A technique for studying neuronal interactions. Science. 204:1979;1117-1119.
34. Landis D. M. D., Sidman R. L. Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J. Comp. Neurol. 179:1978;831-864.
35. Lindvall O., Odin P. Clinical application of cell transplantation and neurotrophic factors in CNS disorders. Curr. Opin. Neurobiol. 4:1994;752-757.
36. Lindvall O., Rehncrona S., Brundin P. Human fetal dopamine neurons grafted into the striatum in two patients with severe Parkinson's disease: A detailed account of methodology and a 6-month follow-up. Arch. Neurol. 46:1989;615-631.
37. Mallet J., Huchet M., Pougeois R., Changeux J.-P. Anatomical, physiological and biochemical studies on the cerebellum from mutant mice. III. Protein differences associated with the weaver, staggerer, and nervous mutations. Brain Res. 103:1976;291-312.
38. Maness L. M., Kastin A. J., Weber J. T., Banks W. A., Beckman B. S., Zadina J. E. The neurotrophins and their receptors: Structure, function, and neuropathology. Neurosci. Biobehav. Rev. 18:1994;143-159.
39. Mariani J., Crepel F., Mikoshiba K., Changeux J. P., Sotelo C. Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mouse. Phil. Trans. Roy. Soc. London, Series B. 281:1977;1-28.
40. McKay R. Stem cells in the central nervous system. Science. 276:1997;66-71.
41. Merlio J.-P., Ernfors P., Jaber M., Persson H. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience. 51:1992;513-532.
42. Mullen R. J., Eicher E. M., Sidman R. L. Purkinje cell degeneration, a new neurological mutation in the mouse. Proc. Nat. Acad. Sci. USA. 73:1976;208-212.
43. Oblinger M., Hallas B. H., Das G. D. Neocortical transplants in the cerebellum of the rat: Their afferents and efferents. Brain Res. 189:1980;228-232.
44. Oertel W. H., Mugnaini E., Schmechel D. E., Tappaz M. L., Kopin I. J. The immunocytochemical demonstration of gamma-aminobutyric acid- ergic neurons-Methods and application. Chan-Palay V., Palay S. L. Cytochemical Methods in Neuroanatomy. 1982;297-329 A. R. Liss, New York.
45. Papaioannou V. E., Fox J. G. Efficacy of tribromoethanol anesthesia in mice. Lab. Animal. Sci. 43:1993;189-192.
46. Peschanski M., Cesaro P., Hantray P. Rationale for intrastriatal grafting of striatal neuroblasts in patients with Huntington's disease. Neuroscience. 68:1995;273-285.
47. Phillips R. J. S. J. Genet. 57:1960;35-42.
48. Redmond D. E. J., Roth R. H., Spencer D. D., Naftolin F., Leranth C., Robbins R. J., Marek K. L., Elsworth J. D., Taylor J. R., Sas K. J., Sladek J. R. Jr. Neural transplantation for neurodegenerative diseases: Past, present, and future. Ann. N.Y. Acad. Sci. 695:1993;258-266.
49. Renfranz P. J., Cunningham M. G., McKay R. D. G. Region specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell. 66:1991;713-729.
50. Riddle D. R., Lo D. C., Katz L. C. NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature. 378:1995;189-191.
51. Rocamora N., García-Ladona F. J., Palacios J. M., Mengod G. Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and low-affinity nerve growth factor receptor during the postnatal development of the rat cerebellar system. Mol. Brain Res. 17:1993;1-8.
52. Rossi F., Wiklund L., Van Der Want J. J. L., Strata P. Reinnervation of cerebellar Purkinje cells by climbing fibres surviving a subtotal lesion of the inferior olive in the adult rat. I. Development of new collateral branches and terminal plexuses. J. Comp. Neurol. 308:1991;513-535.
53. Roth J., Baetens D., Norman A. W., Garcia-Segura L. M. Specific neurons in chick central nervous system stain with an antibody against chick intestinal vitaminD. Brain Res. 222:1981;452-457.
54. Senut M.-C., Tuszynski M. H., Raymon H. K., Suhr S. T., Liou N. H., Jones K. R., Reichardt L. F., Gage F. H. Regional differences in responsiveness of adult CNS axons to grafts of cells expressing human neurotrophin 3. Exp. Neurol. 135:1995;36-55.
55. Smeyne R. J., Chu T., Lewin A., Bian F., -Crisman S. S., Kunsch C., Lira S. A., Oberdick J. Local control of granule cell generation by cerebellar Purkinje cells. Mol. Cell. Neurosci. 6:1995;230-251.
56. Snyder E. Y., Park K. I., Flax J. D., Liu S., Rosario C. M., Yandava B. D., Aurora S. Potential of neural "stem-like" cells for gene therapy and repair of the degenerating central nervous system. Acta Neuropathol. 72:1997;121-132.
57. Sotelo C. Neuronal transplantation: Purkinje cell replacement and reconstruction of a defective cerebellar circuitry in mice with heredo-degenerative ataxia. Boll. Soc. Ital. Biol. Sper. 62:1986;1479-1485.
58. Sotelo C., Alvarado-Mallart R.-M. Cerebellar grafting as a tool to analyze new aspects of cerebellar development and plasticity. Llinas R., Sotelo C. The Cerebellum Revisited. 1992;84-115 Springer-Verlag, New York.
59. Sotelo C., Alvarado-Mallart R. M. Growth and differentiation of cerebellar suspensions transplanted into the adult cerebellum of mice with heredodegenerative ataxia. Proc. Natl. Acad. Sci. USA. 83:1986;1135-1139.
60. Sotelo C., Alvarado-Mallart R. M. Embryonic and adult neurons interact to allow Purkinje cell replacement in mutant cerebellum. Nature. 327:1987;421-423.
61. Sotelo C., Alvarado-Mallart R. M. Cerebellar transplantations in adult mice with heredo-degenerative ataxia. Ann. N.Y. Acad. Sci. 495:1987;242-267.
62. Sotelo C., Alvarado-Mallart R. M. Reconstruction of the defective cerebellar circuitry in adult Purkinje cell degeneration mutant mice by Purkinje cell replacement through transplantation of solid embryonic implants. Neuroscience. 20:1987;1-22.
63. Sotelo C., Alvarado-Mallart R. M. Integration of grafted Purkinje cell into the host cerebellar circuitry in Purkinje cell degeneration mutant mouse. Prog. Brain Res. 78:1988;141-154.
64. Sotelo C., Alvarado-Mallart R. M., Gardette R., Crepel F. Fate of grafted embryonic Purkinje cells in the cerebellum of the adult "Purkinje cell degeneration" mutant mouse. I. Development of reciprocal graft-host interactions. J. Comp. Neurol. 295:1990;165-187.
65. Stein D. G., Glasier M. M. Some practical and theoretical issues concerning fetal brain tissue grafts as therapy for brain dysfunctions. Behav. Brain Sci. 18:1995;36-45.
66. Sterio D. C. The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134:1984;127.
67. Tomac A., Lindqvist E., Lin L.-F. H., Ogren S. O., Young D., Hoffer B. J., Olson L. Protection and repair of the nigrostriatal dopaminergic system by GDNFin vivo. Nature. 373:1995;335-339.
68. Tomey D. A., Heckroth J. A. Transplantation of normal embryonic cerebellar cell suspensions into the cerebellum of lurcher mutant mice. Exp. Neurol. 122:1993;165-170.
69. Triarhou L. C. The cerebellar model of neuronal grafting: Structural integration and functional recovery. Brain Res. Bull. 39:1996;127-138.
70. Triarhou L. C., Ghetti B. Stabilisation of neurone number in the inferior olivary complex of aged "Purkinje cell degeneration" mutant mice. Acta Neuropathol. 81:1991;597-602.
71. Triarhou L. C., Low W. C., Ghetti B. Intraparenchymal grafting of cerebellar cell suspensions to the deep cerebellar nuclei of pcd mutant mice, with particular emphasis on re-establishment of a Purkinje cell cortico-nuclear projection. Anat. Embryol. (Berl). 185:1992;409-420.
72. Turner D. A., Kearney W. Scientific and ethical concerns in neural fetal tissue transplantation. Neurosurgery. 33:1993;1031-1037.
73. Vicario-Abejon C., Cunningham M. G., McKay R. D. G. Cerebellar precursors transplanted to the neonatal dentate gyrus express features characteristic of hippocampal neurons. J. Neurosci. 15:1995;6351-6363.
74. Vogel M. W., McInnes M., Zanjani H. S., Herrup K. Cerebellar Purkinje cells provide target support over a limited spatial range: Evidence from lurcher chimeric mice. Dev. Brain Res. 64:1991;87-94.
75. Wetmore C., Ernfors P., Persson H., Olson L. Localization of brain derived neurotrophic factor mRNA to neurons in the brain by in situ hybridization. Exp. Neurol. 109:1990;141-152.
76. Wetts R., Herrup K. Interaction of granule, Purkinje and inferior olivary neurons in lurcher chimeric mice. II. Granule cell death. Brain Res. 250:1982;358-362.
77. Wetts R., Herrup K. Interaction of granule, Purkinje and inferior olivary neurons in Lurcher chimaeric mice. I. Qualitative studies. J. Embryol. Exp. Morphol. 68:1982;87-98.
78. Wetts R., Herrup K. Direct correlation between Purkinje cell number in the cerebella of lurcher chimeras and wild-type mice. Dev. Brain Res. 10:1983;41-47.
79. Whittemore S. R., Eaton M. J., Onifer S. M. Gene therapy and the use of stem cells for central nervous system regeneration. Acta Neuropathol. 72:1997;113-119.
80. Wu J.-Y., Lin C. T., Brandon C., Chan T.-S., Mohler H., Richards J. G. Regulation and immunocytochemical characterization of glutamic acid decarboxylase. Chan-Palay V., Palay S. L. Cytochemical Methods In Neuroanatomy. 1982;279-296 A. R. Liss, New York.
81. Zhang W., Lee W. H., Triarhou L. C. Grafted cerebellar cells in a mouse model of hereditary ataxia express IGF-I system genes and partially restore function. Nature Med. 2:1996;65-71.
82. Zhou X.-F., Rush R. A. Localization of neurotrophin-3-like immunoreactivity in the rat central nervous system. Brain Res. 643:1994;162-172.