Fetal hippocampal cells grafted to kainate-lesioned CA3 region of adult hippocampus suppress aberrant supragranular sprouting of host mossy fibers

Experimental Neurology

Volumn 143, Issue 2, 1997, Pages 231-245

  Shetty, Ashok K ^a   Turner, Dennis A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; DENTATE GYRUS; EMBRYO; HIPPOCAMPUS; HISTOCHEMISTRY; MORPHOMETRICS; MOSSY FIBER; NERVE CELL; NERVE SPROUTING; NERVE TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; RAT; TEMPORAL LOBE EPILEPSY;

EID: 0031080020     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.6363     Document Type: Article

References (80)

1. Altman J., Bayer S. A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J. Comp. Neurol. 301:1990;325-342.
2. Amaral D. G. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182:1978;851-914.
3. Amaral D. G., Witter M. The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience. 31:1989;571-591.
4. Assaf S. Y., Chung S. H. Release of endogenous Zn2+ from brain tissue during activity. Nature. 308:1984;734-736.
5. Babb T. L., Kupfer W. R., Pretorius J. K., Crandall P. H., Levesque M. F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 42:1991;351-363.
6. Bayer S. A. Development of the hippocampal region in the rat. I. Neurogenesis examined with [3H]thymidine autoradiographic study. J. Comp. Neurol. 190:1980;87-114.
7. Ben-Ari Y. Limbic seizures and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 14:1985;375-403.
8. Bjorklund A. Dopaminergic transplants in experimental parkinsonism: Cellular mechanisms of graft-induced functional recovery. Curr. Opin. Neurobiol. 2:1992;683-689.
9. Bjorklund A., Dunnett S. B., Nikkhah G. Nigral transplants in the rat Parkinson model. Functional Neural Transplantation. 1994;Raven Press, New York. p. 47-69.
10. Buhl E. H., Otis T. S., Mody I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science. 271:1996;369-373.
11. Buzsaki G., Ponomareff G., Bayardo F., Shaw T., Gage F. H. Suppression and induction of epileptic activity by neuronal grafts. Proc. Natl. Acad. Sci. USA. 85:1988;9327-9330.
12. Cassel J. C., Neufang B., Kelche C., Jeltsch H., Well B. E., Herting G., Jackisch R. Effects of grafts containing cholinergic and/or serotonergic neurons on cholinergic, serotonergic and noradrenergic markers in the denervated rat hippocampus. Brain Res. 604:1993;53-63.
13. Cronin J., Obenaus A., Houser C. R., Dudek F. E. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res. 573:1992;305-310.
14. Cronin J., Dudek F. E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474:1988;181-184.
15. Danscher G. Histochemical demonstration of heavy metals: A revised version of the silver sulfide method suitable for both light and electron microscopy. Histochemistry. 71:1981;1-16.
16. Davenport C. J., Brown W. J., Babb T. L. Sprouting of GABA-ergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Expl. Neurol. 109:1990;180-190.
17. Davies S. J. A., Field P. M., Raisman G. Long fiber growth by axons of embryonic mouse hippocampal neurons microtransplanted into the adult rat fimbria. Eur. J. Neurosci. 5:1993;95-106.
18. Davies S. J. A., Field P. M., Raisman G. Long interfascicular axon growth from embryonic neurons transplanted into adult myelinated tracts. J. Neurosci. 14:1994;1596-1612.
19. Dudek F. E., Obenaus A., Schweitzer J. S., Wuarin J-P. Functional significance of hippocampal plasticity in epileptic brain: Electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus. 4:1994;259-265.
20. Dugich-Djordjevic M., Tocco G., Lapchak P., Pasinetti G., Najm I., Baudry M., Hefti F. Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in adult rat brain following seizures induced by systemic administration of kainic acid. Neuroscience. 47:1992;303-315.
21. Dunnett S. B. Functional repair of striatal systems by neural transplants: evidence of circuit reconstruction. Behav. Brain Res. 66:1995;133-142.
22. Field P. M., Seeley P. J., Frotscher M., Raisman G. Selective innervation of embryonic hippocampal transplants by adult host dentate granule cell axons. Neuroscience. 41:1991;713-727.
23. Frank J. E. Dynamic alterations in hippocampal morphology following intra-ventricular kainic acid. Acta Neuropathol. 62:1984;242-253.
24. Gaarskjaer F. B. The organization and development of the hippocampal mossy fiber system. Brain Res. Rev. 11:1986;335-357.
25. Gage F. H., Fisher L. J. Intracerebral grafting: A tool for the neurobiologist. Neuron. 6:1991;1-12.
26. Garcia A. R., Deacon T. W., Dinsmore J., Isacson O. Extensive axonal and glial fiber growth from fetal porcine cortical xenografts in the adult rat cortex. Cell Transplant. 4:1995;515-527.
27. Granholm A.-C., Bergman H., Dudek F. E., Browning M. Synapsin I in intraocular hippocampal transplants during maturation and aging: effects of brainstem cografts. Cell Transplant. 4:1995;3-12.
28. Granholm A-C., Eriksdotter-Nilsson M., Stromberg I., Stieg P., Seiger A., Bygdeman M., Geffard M., Oertel W., Dahl D., Olson L. Morphological and electrophysiological studies of human hippocampal transplants in the anterior eye chamber of athymic nude rats. Expl. Neurol. 104:1989;162-171.
29. Green R., Blume H., Kupferschmid S., Mesulum M. Alterations of hippocampal acetylcholine esterase in human temporal lobe epilepsy. Ann. Neurol. 26:1989;347-351.
30. Han Z-S., Buhl E. H., Lorinczi Z., Somogyi P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5:1993;395-410.
31. Holmes G. L., Thompson J. L., Huh K., Holmes C., Carl G. F. Effect of neural transplants on seizure frequency and kindling in immature rats following kainic acid. Dev. Brain Res. 64:1991;47-56.
32. Holtzman D., Kilbridge J., Bredt D., Black S., Li Y., Clary D., Reichardt L., Mobley W. NOS induction by NGF in basal forebrain cholinergic neurons: evidence for regulation of brain NOS by a neurotrophin. Neurobiol. Dis. 1:1994;51-60.
33. Holtzman D., Kilbridge J., Li Y., Cunningham E., Lenn N., Clary D., Reichardt L., Mobley W. Trk A expression in the CNS: evidence for the existence of several novel NGF-responsive CNS neurons. J. Neurosci. 15:1995;1567-1576.
34. Holtzman D. M., Lowenstein D. H. Selective inhibition of axon outgrowth by antibodies to NGF in a model of temporal lobe epilepsy. J. Neurosci. 15:1995;7062-7070.
35. Houser C. R., Miyashiro J. E., Swartz B. E., Walsh G. O., Rich J. R., Daelgado-Escuet A. V. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10:1990;267-282.
36. Isacson O., Peschanski M. Is there capacity for anatomical and functional repair in the adult somatosensory thalamus? Expl. Neurol. 115:1992;173-176.
37. Kesslak J. P., Walencewicz A., Calin L., Nieto-Sampedro M., Cotman C. Hippocampal but not astrocyte transplants enhance recovery on a forced choice alteration task after kainate lesions. Brain Res. 454:1988;347-354.
38. Klein R., Conway D., Parada L., Barbacid M. The Trk B tyrosine kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell. 61:1990;647-656.
39. Kordower J. H., Freeman T. B., Snow B. J., Vingerhoets F. J. G., Mufson E. J., Sanberg P. R., Hauser R. A., Smith D. A., Nauert G. M., Perl D. P., Olanow C. W. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. New Engl. J. Med. 332:1995;1118-1124.
40. Lindvall O., Widner H., Rehncrona S., Brundin P., Odin P., Gustavii B., Leenders K. L., Sawle G., Rothwell J. C., Bjorklund A., Marsden C. D. Transplantation of fetal dopamine neurons in Parkinson's disease: One year clinical and neurophysiological observations in two patients with putaminal implants. Ann. Neurol. 31:1992;155-165.
41. Lowenstein D. H., Seren M. S., Longo F. M. Prolonged increases in neurotrophic activity associated with kainate-induced hippocampal synaptic reorganization. Neuroscience. 56:1993;597-604.
42. Masukawa L. M., Urono K., Sperling M., O'Connor M. J., Burdette L. J. The functional relationship between antidromically evoked field responses of the dentate gyrus and mossy fiber reorganization in temporal lobe epileptic patients. Brain Res. 579:1992;119-127.
43. Mathern G. W., Cifuentes F., Leite J. P., Pretorius J. K., Babb T. L. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr. Clin. Neurophysiol. 87:1993;326-339.
44. Mello L. E. A. M., Cavalheiro E. A., Tan A. M., Kupfer W. R., Pretorius J. K., Babb T. L., Finch D. M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia. 34:1993;985-995.
45. Mitchell J., Best N., Sundstrom L. E., Wheal H. V. The use of sodium sulfide-fixed brain tissue for immunocytochemical staining of activated microglia and reactive astrocytes. Histochemistry. 99:1993;91-94.
46. Mudrick L. A., Baimbridge K. G. Hippocampal neurons transplanted into ischemically lesioned hippocampus: Anatomical assessment of survival, maturation and integration. Exp. Brain Res. 86:1991;233-247.
47. Mudrick L. A., Baimbridge K. G., Peet M. J. Hippocampal neurons transplanted into ischemically lesioned hippocampus: Electro-responsiveness and re-establishment of circuitries. Exp. Brain Res. 76:1989;333-342.
48. Nadler J. V., Perry B. W., Cotman C. W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature. 271:1978;676-677.
49. Nadler J. V., Perry B. W., Gentry C., Cotman C. W. Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J. Comp. Neurol. 192:1980;333-359.
50. Netto C. A., Hodges H., Sinden J. D., Le Peillet E., Kershaw T., Sowinski P., Meldrum B. S., Gray J. A. Effects of fetal hippocampal field grafts on ischemic-induced deficits in spatial navigation in the water maze. Neuroscience. 54:1993;69-92.
51. Nieto-Sampedro M., Whittemore S. R., Needels D. L., Larson J., Cotman C. W. The survival of brain transplants is enhanced by extracts from injured brain. Proc. Natl. Acad. Sci. USA. 81:1984;6250-6254.
52. Nothias F., Peschanski M. Homotypic fetal transplants into an experimental model of spinal cord neurodegeneration. J. Comp. Neurol. 301:1990;520-534.
53. Okazaki M. M., Evenson D. A., Nadler J. V. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin. J. Comp. Neurol. 352:1995;515-534.
54. Raisman G., Ebner F. F. Mossy fiber projections into and out of hippocampal transplants. Neuroscience. 9:1983;783-801.
55. Ribak C. E., Seress L., Amaral D. G. The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J. Neurocytol. 14:1985;835-857.
56. Shetty A. K., Madison R. D., Bradley J., Turner D. A. Quantitative graft integration of fetal hippocampal transplants labeled with 5′ bromodeoxyuridine into normal adult hippocampus. Expl. Neurol. 126:1994;205-224.
57. Shetty A. K., Turner D. A. Enhanced cell survival in fetal hippocampal suspension transplants grafted to adult rat hippocampus following kainate lesions: A three-dimensional graft reconstruction study. Neuroscience. 67:1995a;561-582.
58. Shetty A. K., Turner D. A. Non-phosphorylated neurofilament protein immunoreactivity in adult and developing rat hippocampus: Specificity and application in grafting studies. Brain Res. 676:1995b;293-306.
59. Shetty A. K., Turner D. A. Fetal hippocampal grafts in kainate lesioned hippocampus establish specific connections and reduce aberrant mossy fiber sprouting. Soc. Neurosci. Abstr. 21:1995c;2028.
60. Shetty A. K., Turner D. A. Development of fetal hippocampal grafts in intact and lesioned hippocampus. Prog. Neurobiol. 50:1996;597-653.
61. Shetty A. K., Turner D. A. Development of long-distance efferent projections from fetal hippocampal grafts depends upon pathway specificity and graft location in kainate-lesioned adult hippocampus. Neuroscience. 1997.
62. Shihabuddin L. S., Hertz J. A., Holets V. R., Whittemore S. R. The adult CNS retains the potential to direct region-specific differentiation of a transplanted neuronal precursor cell line. J. Neurosci. 15:1995;6666-6678.
63. Sorensen T., Zimmer J. Ultrastructural organization of normal and transplanted fascia dentata: II. A quantitative analysis of the synaptic organization of intracerebral and intraocular grafts. J. Comp. Neurol. 267:1988;43-54.
64. Sprick U. Morphology of embryonic hippocampus transplants and generation of long-distance extrinsic graft fiber connections to the lateral septum and the entorhinal cortex in the mature rat brain. Restor. Neurol. Neurosci. 3:1991;23-34.
65. Stanfield B. B. Excessive intra- and supragranular mossy fibers in the dentate gyrus of tottering (tg/tg) mice. Brain Res. 480:1989;294-299.
66. Sunde N. A., Laurberg S., Zimmer J. Brain grafts can restore irradiation damaged neuronal connections in the newborn rat. Nature. 310:1984;51-53.
67. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26:1989;321-330.
68. Sutula T., He X.-X., Cavazos J., Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science. 239:1988;1147-1150.
69. Tauck D. L., Nadler J. V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 4:1985;1016-1022.
70. Tonder N. Neural transplantation to the normal and lesioned brain: An experimental study of the rat hippocampus. Acta Neurol. Scand. 91:1995;6-30.
71. Tonder N., Sorensen T., Zimmer J. Grafting of fetal CA3 neurons to excitotoxic, axon-sparing lesions of the hippocampal CA3 area in adult rats. Prog. Brain Res. 83:1990;391-409.
72. Tsoulfas P., Soppet D., Escandon E., Tessarollo L., Mendoza-Ramirez J-L., Rosenthal A., Nikolics K., Parada L. The rat Trk C locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC 12. Neuron. 10:1993;975-990.
73. Turner D. A., Kearney W. Scientific and ethical concerns in neural fetal tissue transplantation. Neurosurgery. 33:1993;1031-1037.
74. Turner D. A., Wheal H. V. Excitatory synaptic potentials in kainic-acid denervated rat CA1 pyramidal neurons. J. Neurosci. 11:1991;2786-2794.
75. Valenzuela D., Maisonpierre P., Glass D. J., Rojas E., Nunez L., Kong Y., Gies D., Stitt T., Ip N., Yancopoulos G. Alternative forms of rat trk C with different functional capabilities. Neuron. 10:1993;963-974.
76. Wictorin K. Anatomy and connectivity of intrastriatal striatal transplants. Prog. Neurobiol. 38:1992;611-639.
77. Woodruff M. L., Baisden R. H., Nonneman A. J. Anatomical and behavioral sequelae of fetal brain transplants in rats with trimethyltin-induced neurodegeneration. Neurotoxicology. 12:1991;427-444.
78. Woodruff M. L., Baisden R. H., Nonneman A. J. Effects of transplantation of fetal hippocampal or hindbrain tissue into the brains of adult rats with hippocampal lesions on water maze acquisition. Behav. Neurosci. 106:1992;39-50.
79. Wuarin J-P., Dudek F. E. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slice from kainate treated epileptic rats. J. Neurosci. 16:1996;4438-4448.
80. Yurek D., Sladek J. R. Jr. Dopamine cell replacement: Parkinson's disease. Annu. Rev. Neurosci. 13:1990;415-440.