Neuroectodermal grafting: A new tool for the study of neurodegenerative disease

Histology and Histopathology

Volumn 11, Issue 4, 1996, Pages 1063-1073

  Isenmann, S ^a,b   Brandner, S ^a   Aguzzi, A ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

adhesion molecule on glia (AMOG 2); Alzheimer's disease; blood brain barrier; CNS development; degeneration; differentiation; gene knockouts; immuncytochemistry; Neu differentiation factor (NDF); neural transplantation (mice); prion protein (PrP); proliferation; scrapie; transgenic mice

Indexed keywords

CELL ADHESION MOLECULE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; EMBRYO DEVELOPMENT; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PARKINSON DISEASE; PRION DISEASE; REVIEW; SHEEP DISEASE; TRANSGENIC MOUSE; TRANSPLANTATION;

ADENOSINE TRIPHOSPHATASES; ALZHEIMER DISEASE; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN DISEASES; CATION TRANSPORT PROTEINS; CELL ADHESION MOLECULES, NEURONAL; CELL DIVISION; ECTODERM; FETAL TISSUE TRANSPLANTATION; HUMANS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVOUS SYSTEM; PARKINSON DISEASE; PRION DISEASES;

ANIMALIA; MUS MUSCULUS; OVIS ARIES;

EID: 0029955041     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (92)

1. Aguzzi A., Kleihues P., Heckl K. and Wiestier O.D. (1991). Cell type-specific tumor induction in neural transplants by retrovirus-mediated oncogene transfer. Oncogene 6, 113-118.
2. Aguzzi A., Brandner S., Sure U., Ruedi D. and Isenmann S. (1994). Transgenic and knock-out mice: models of neurological disease. Brain. Pathol. 4, 3-20.
3. Aguzzi A., Brandner S., Isenmann S., Steinbach J.P. and Sure U. (1995). Transgenic and gene disruption techniques in the study of neurocarcinogenesis. Glia 15, 348-364.
4. Akli S., Caillaud C., Vigne E., Stratford Perricaudet L.D. Poenaru L., Perricaudet M., Kahn A. and Peschanski M.R. (1993). Transfer of a foreign gene into the brain using adenovirus vectors. Nat. Genet. 3, 224-228.
5. Antonicek H. Persohn E. and Schachner M. (1987). Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J. Cell Biol. 104, 1587-1195.
6. Bajocchi G., Feldman S.H., Crystal R.G. and Mastrangeli A. (1993). Direct in vivo gene transfer to ependymal cells in the central nervous system using recombinant adenovirus vectors. Nat. Genet. 3, 229-34.
7. Bayer T.A., Foflgreen A., Czech C., Beyreuther K. and Wiestier O. D. (1995). Extracellular APP deposits in neural transplants harboring a mutant APP. Soc. Neurosci. Abs. 21, 979.
8. Becker C.M. Betz H. and Schröder H. (1993). Expression of inhibitory glycine receptors in postnatal rat cerebral cortex. Brain Res. 606, 220-226.
9. Bertram K.J., Shipley M.T., Ennis M., Sanberg P.R. and Norman A.B. (1994). Permeability of the blood-brain barrier within rat intrastriatal transplants assessed by simultaneous systemic injection of horse radish peroxidase and Evans blue dye. Exp. Neurol. 127, 245-252.
10. Bladt F., Riethmacher D., Isenmann S., Aguzzi A. and Birchmeier C. (1995). The c-met receptor is essential for migration of myogenic precursor cells into the anlage of the limb. Nature 376, 768-771.
11. Brandner S., Isenmann S., Raeber A., Fischer M., Sailer A., Kobayashi Y., Marino S., Weissmann C. and Aguzzi A. (1996). Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379, 339-343.
12. Broadwell R.D., Charlton H.M., Ganong W.F., Salcman M. and Sofroniew M. (1989). Allografts of CNS tissue possess a blood-brain barrier. I. Grafts of medial preoptic area in hypogonadal mice. Exp. Neurol. 105, 135-151.
13. Broadwell R.D., Charlton H.M., Ebert P., Mickey W.F., Villegas J.C. and Wolf A.L. (1990). Angiogenesis and the blood-brain barrier in solid and dissociated cell grafts within the CNS. Prog. Brain Res. 82, 95-101.
14. Brüstle O., Aguzzi A., Talarico D., Basilico C., Kleihues P. and Wiestler O.D. (1992). Angiogenic activity of the K-fgf/hst oncogene in neural transplants. Oncogene 7, 1177-1183.
15. Brüstle O., Maskos U., and McKay R.D.G. (1995). Host-guided migration allows targeted introduction of neurons into the embryonic brain. Neuron 15, 1275-1285.
16. Büeler H., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M. and Weissmann C. (1993). Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347.
17. Campbell C., Olsson M. and Björklund A. (1995). Regional incorporation and site-specific differentiation of striatal precursors transplanted to the embryonic forebrain ventricle. Neuron 15, 1259-1273.
18. Carraway K.L.R. and Cantley L.C. (1994). A neu acquaintance for erbB3 and erbB4: a role for receptor heterodimerization in growth signaling. Cell 78, 5-8.
19. Das G.D. (1990). Neural transplantation: an historical perspective. Neurosci. Biobehav. R. 14, 389-401.
20. Davidson B.L., Allen E.D., Kozarsky K.F., Wilson J.M. and Roessler B.J. (1993). A model system for in vivo gene transfer into the central nervous system using an adenoviral vector. Nat. Genet. 3, 219-223.
21. DeArmond S.J. and Prusiner S.B. (1995). Etiology and pathogenesis of prion diseases. Am. J. Pathol. 146, 785-811.
22. Dong Z., Brennan A., Liu N., Yarden Y., Lefkowitz G., Mirsky R., and Jessen K.R. (1995). Neu differentiation factor Is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15, 585-596.
23. Dunnett S.B. (1990). Neural transplantation in animal models of dementia. Eur. J. Neurosci. 2, 567-587.
24. Dunnett S.B., Bjorklund A., Stenevi U. and Iversen S. D. (1981). Grafts of embryonic substantia nigra reinnervating the ventrolateral striatum ameliorate sensorimotor impairments and akinesia in rats with 6-OHDA lesion of the nigrostriatal pathway. Brain Res. 229, 209-217.
25. Falls D.L., Rosen K.M., Corfas G., Lane W.S. and Fischbach G.D. (1993). ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72, 801-815.
26. Fischer M., Rülicke T., Räber A., Sailer A., Oesch B., Brandner S., Aguzzi A. and Weissmann C. (1996). Prion protein (PrP) with amino terminal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15, 1255-1264.
27. Fisher L.J. and Gage F.H. (1993). Grafting in the mammalian central nervous system. Physiol. Rev. 73, 583-616.
28. Fisher L.J. and Ray J. (1994). In vivo and ex vivo gene transfer to the brain. Curr. Opin. Neurobiol. 4, 735-741.
29. Fisher L.J., Jinnah H.A., Kale L.C., Higgins G.A. and Gage F.H. (1991). Survival and function of intrastriatally grafted primary fibroblasts genetically modified to produce L-dopa. Neuron 6, 371-380.
30. Freed C.R., Breeze R.E., Rosenberg N.L., Schneck S.A., Kriek E., Qi J.X., Lone T., Zhang Y.B., Snyder JA, Wells T.H., Olson Ramig L., Thompson L., Mazziotta J.C., Huang S.C., Grafton S.C., Brooks D., Sawle G., Schroter G., and Ansari A.A. (1992). Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson's disease. New Engl. J. Med. 327, 1549-1555.
31. Frim D.M., Uhler T.A., Galpern W.R., Beal M.F., Breakefield X.O. and Isacson O. (1994). Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in the rat. Proc. Natl. Acad. Sci. USA 91, 5104-5108.
32. Gage F.H., Coates P.W., Palmer T.D., Kuhn H.G., Fisher L.J., Suhonen J.O., Petersen D.A., Suhr ST. and Ray J. (1995). Survival and differentiation of adult neural progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. USA 92, 11879-11883.
33. Games D., Adams D., Allessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagoplan S., Johnson-Wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Mesliah E., McConlogue L., Montoya-Zavala M., Mucke L., Paganini L., Pennyman E., Power M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale J., Wadsworth S., Wolozin B. and Zhao J. (1995). Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373, 523-527.
34. Garry D.J., Caplan A.L. Vawter D.E. and Kearney W. (1992). Are there really alternatives to the use of fetal tissue from elective abortions in transplantation research? New Engl. J. Med. 327, 1592159-5.
35. Gassmann M., Casagranda F., Orioli D., Simon H., Lai C., Klein R. and Lemke G. (1995). Aberrant neural and cardiac development in mice lacking the Erbb4 neuregulin receptor. Nature 378, 390-394.
36. Geering K. (1991). The functional role of the beta-subunit in the maturation and intracellular transport of Na,K-ATPase. FEBS Lett. 285, 189-193.
37. Gloor S., Antonicek H., Sweadner K.J., Pagliusi S., Frank R., Moos M. and Schachner M. (1990). The adhesion molecule on glia (AMOG) is a homologue of the beta subunit of the Na,K-ATPase. J. Cell Biol. 110, 165-174.
38. Goate A., Chartier-Harlin M.C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., Mant R., Newton P., Rooke K., Roques P., Talbot C., Pericak-Vance M., Roses A., Williamson R., Rossor M., Owen M. and Hardy J. (1991). Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706.
39. Gratzner H. G. (1982). Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218, 474-5.
40. Huffman D., Breakefield X.O., Short M.P. and Aebischer P. (1993). Transplantation of a polymer-encapsulated cell line genetically engineered to release NGF. Exp. Neurol. 122, 100-106.
41. Isenmann S., Molthagen M., Brandner S., Bartsch U., Kühne G., Magyar J., Sure U., Schachner M., and Aguzzi A. (1995). The AMOG/β2 Subunit of the Na,K-ATPase is not necessary for long-term survival of telencephalic grafts. Glia 15, 377-388.
42. Isenmann S., Brandner S., Sure U. and Aguzzi, A. (1996a). Telencephalic transplants in mice: characterization of growth and differentiation patterns. Neuropathol. Appl. Neurobiol. 21, 108-117.
43. Isenmann S., Brandner S., Kühne G., Boner J. and Aguzzi A. (1996b). Comparative in vivo and pathological analysis of the Blood-Brain Barrier in mouse telencephalic transplants. Neuropathol. Appl. Neurobiol. 21, 118-128.
44. Isenmann S., Bähr M. and Dichgans J. (1996c). Gentherapie Neurologischer Erkrankungen - Experimentelle Ansätze und Klinische Perspektiven [Gene therapy of neurological disorders experimental paradigms and clinical perspectives]. Nervenarzt 67, 91-108.
45. Jaeger C.B. and Lund R.D. (1980). Transplantation of embryonic occipital cortex to the brain of newborn rats. An autoradiographic study of transplant histogenesis. Exp. Brain Res. 40, 265-272.
46. Janzer R.C. and Raff M.C. (1987). Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325, 253-257.
47. Jiao S., Gurevich V. and Wolff J.A. (1993). Long-term correction of rat model of Parkinson's disease by gene therapy. Nature 362, 450-453.
48. Kaplitt M.G. Leone P., Samulsky R.J., Xiao X., Pfaff D.W., OMalley K.L. and During M.J. (1994). Long-term gene expression and phenotypic correction using adeno-associated virus-vectors in the mammalian brain. Nat. Genet. 8, 148-154.
49. Kassirer J.P. and Angell M. (1992). The use of fetal tissue in research on Parkinson's disease. New Engl. J. Med. 327, 1591-1592.
50. Klein R., Smeyne R.J., Wurst W., Long L.K., Auerbach B.A., Joyner A L. and Barbacid M. (1993). Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75, 113-122.
51. Kromer L.F., Björklund A. and Stenevi U. (1979). Intracephalic Implants: a technique for studying neuronal interactions. Science 204, 1117-1119.
52. LaFerla F.M., Tinkle B.T., Bieberich C.J., Haudenschild C.C. and Jay G. (1995). The Alzheimer's A beta peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat. Genet. 9, 21-30.
53. Le Gal La Salle G., Robert J.J., Berrard S., Ridoux V., Stratford Perricaudet L.D., Perricaudet M. and Mallet J. (1993). An adenovirus vector for gene transfer into neurons and glia in the brain. Science 259, 988-990.
54. Lee K.F., Simon H., Chen H., Bates B., Hung M.C. and Hauser C. (1995). Requirement for neuregulin receptor Erbb2 in neural and cardiac development. Nature 378, 394-398.
55. Lindvall O. (1991). Prospects of transplantation in human neurodegenerative diseases. Trends. Neurosci. 14, 376-384.
56. Lund R.D. and Hauschka S.D. (1976). Transplanted neural tissue develops connections with host rat brain. Science 193, 582-584.
57. Magyar J.P., Bartsch U., Wang Z.-Q., Howells N., Aguzzi A., Wagner E. F. and Schachner M. (1994). Degeneration of neural cells in the central nervous system of mice deficient in the gene for the adhesion molecule on glia, the β2 subunit of murine Na,K-ATPase. J. Cell Biol. 127, 135-146.
58. Marchionni M.A., Goodearl A.D., Chen M.S., Bermingham-McDonogh O., Kirk C., Hendricks M., Danehy F., Misumi D., Sudhalter J., Kobayashi K., Wroblewski D., Lynch C., Baldassare M., Hues I., Davis J.B., Hsuan J.J., Totty N.F. Otsu M., McBurney R.N., Waterfield M.D., Stroobant P. and Gwynne D. (1993). Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362, 312-318.
59. Meyer D. and Birchmeier C. (1995). Multiple essential functions of neuregulin In development. Nature 378, 386-390.
60. Mullan M., Crawford F., Axelman K., Houlden H., Lilius L., Winblad B. and Lannfelt L. (1992). A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of beta-amyloid. Nat. Genet. 1, 345-347.
61. Murrell J., Farlow M., Ghetti B. and Benson M. D. (1991). A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 254, 97-99.
62. O'Leary D.D.M. and Stanfield B.B. (1989). Selective elimination of axons extended by developing cortical neurons is dependent on regional locale: experiments utilizing fetal cortical transplants. J. Neurosci. 9, 2230-2246.
63. Peles E., Bacus S.S., Koski R.A., Lu H.S., Wen D., Ogden S.G., Levy R.B. and Yarden Y. (1992). Isolation of the neu/HER-2 stimulatory ligand: a 44 kd glycoprotein that induces differentiation of mammary tumor cells. Cell 69, 205-216.
64. Perlow M.J., Freed W.J., Hoffer B.J., Seiger A., Olson L. and Wyatt R.J. (1979). Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system. Science 204, 643-647.
65. Pinkas-Kramarski R., Eilam R., Spiegier O., Lavi S., Liu N., Chang D., Wen D., Schwartz M. and Yarden Y. (1994). Brain neurons and glial cells express Neu differentiation factor/heregulin: a survival factor for astrocytes. Proc. Natl. Acad. Sci. USA 91, 9387-9391.
66. Prusiner S.B. (1991). Molecular biology of prion diseases. Science 252, 1515-1522.
67. Renfranz P.J., Cunningham M.G. and McKay R.D.G. (1991). Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell 68, 713-729.
68. Richards S.J., Waters J.J., Beyreuther K., Masters C.L., Wischik C.M., Sparkman D.R., White C.L., III, Abraham C.R. and Dunnett S.B. (1991). Transplants of mouse trisomy 16 hippocampus provide a model of Alzheimer's disease neuropathology. EMBO J. 10, 297-303.
69. Risau W. and Wolburg H. (1990). Development of the blood-brain barrier. Trends. Neurosci. 13, 174-178.
70. Rosenberg M.B., Friedmann T., Robertson R.C., Tuszynski M., Wolff J. A., Breakefield X.O. and Gage F.H. (1988). Grafting genetically modified cells to the damaged brain: restorative effects of NGF expression. Science 242, 1575-1578.
71. Rosenstein J.M. (1987). Neocortical transplants in the mammalian brain lack a blood-brain barrier to macromolecules. Science 235, 772-774.
72. Rosenstein J.M. and Brightman M.W. (1983). Circumventing the Blood-Brain Barrier with autonomic ganglion transplants. Science 221, 879-881.
73. Rosenstein J.M. and Brightman M.W. (1986). Alterations of the blood-brain barrier after transplantation of autonomic ganglia into the mammalian central nervous system. J. Comp. Neurol. 250, 339-351.
74. Sabatè O., Horellou P., Vigne E., Colin P., Perricaudet M., Buccaron M. H. and Mallet J. (1995). Transplantation to the rat brain of human neural progenitors that were genetically modified using adenoviruses. Nat. Genet. 9, 256-260.
75. Sailer A., Büeler H., Fischer M., Aguzzi A. and Weissmann, C. (1994). No propagation of prions in mice devoid of PrP. Cell 77, 967-968.
76. Schenk D., Games K.D. and McConlogue L. (1995). The potential utility of transgenic mice harboring beta-amyloid precursor protein. Neurobiol. Aging 16, 711-713.
77. Selkoe D.J. (1994). Amyloid beta-protein precursor: new clues to the genesis of Alzheimer's disease. Curr. Opin. Neurobiol. 4, 708-716.
78. Smeyne R.J., Klein R., Schnapp A., Long L.K., Bryant S., Lewin A., Lira S.A. and Barbacid M. (1994). Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368, 246-249.
79. Spencer D.D., Robbins R.J., Naftolin F., Marek K.L., Vollmer T., Leranth C., Roth R.H., Price L.H., Gjedde A., Bunney B.S., Sass K.J., Elsworth J.D., Kier E.L., Makuch R., Hoffer P.B. and Redmond D.E. (1992). Unilateral transplantation of human fetal mesencephalic tissue into the caudate nucleus of patients with Parkinson's disease. New Engl. J. Med. 327, 1541-1548.
80. Stewart P.A. and Wiley M.J. (1981). Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev. Biol. 84, 183-192.
81. Svendgaard N.A, Björklund A., Hardebo J.E. and Stenevi U. (1975). Axonal degeneration associated with a defective blood-brain barrier in cerebral implants. Nature 255, 334-337.
82. Swenson R.S., Shaw P., Alones V., Kozlowski G., Zimmer J. and Castro A.J. (1989). Neocortical transplants grafted into the newborn rat brain demonstrate a blood-brain barrier to macromolecules. Neurosci. Lett. 100, 35-39.
83. Tam P.P.L. (1990). Studying development in embryo fragments. In: Postimplantation mammalian embryos. A practical approach. Copp A.J. and Cockroft D.L. (eds). IRL Press. Oxford.
84. Telling G.C., Scott M., Mastrianni J., Gabizon R., Torchia M., Cohen F. E., DeArmond S.J. and Prusiner S.B. (1995). Prion propagation in mice expressing human and chimeric Prp transgenes implicates the interaction of cellular Prp with another protein. Cell 83, 79-90.
85. Thomas K.R. and Capecchi M.R. (1987). Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503-512.
86. Tomac A., Lindqvist E., Un L.F.H., Ògren S.O., Young D., Hoffer B.J. and Olson L. (1995). Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373, 335-339.
87. Vartanian T., Corfas G., Li Y., Fischbach G.D. and Stefansson K. (1994). A role for the acetylcholine receptor-inducing protein ARIA in oligodendrocyte development. Proc. Natl. Acad. Sci. USA 91, 11626-11630.
88. Wen D., Peles E., Cupples R., Suggs S.V., Bacus S.S., Luo Y., Trail G., Hu S., Silbiger S.M., Levy R.B., Koski R.A., Lu H.S. and Yarden Y. (1992). Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 69, 559-572.
89. Widner H., Tetrud J., Rehncrona S., Snow B., Brundin P., Gustavii B., Bjorklund A., Lindvall O. and Langston J.W. (1992). Bilateral fetal mesencephalic grafting in two patients with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). New Engt. J. Med. 327, 1556-1563.
90. Wiestler O.D., Brüstle O., Eibl R.H., Radner H., Aguzzi A. and Kleihues P. (1992). Retrovirus-mediated oncogene transfer into neural transplants. Brain Pathol. 2, 47-59.
91. Woerly S. and Marchand R. (1990). A century of neurotransplantation in mammals. Neurochirurgie 36, 71-95.
92. Wolff JA, Fisher L.J., Xu L., Jinnah H.A., Langlais P.J., Iuvone P.M., O'Malley K.L., Rosenberg M.B., Shimohama S., Friedmann T. and Gage F.H. (1989). Grafting fibroblasts genetically modified to produce L-dopa in a rat model of Parkinson disease. Proc. Natl. Acad. Sci. USA 86, 9011-9014.