Fetal hippocampal CA3 cell grafts enriched with fibroblast growth factor-2 exhibit enhanced neuronal integration into the lesioned aging rat hippocampus in a kainate model of temporal lobe epilepsy

Hippocampus

Volumn 13, Issue 5, 2003, Pages 618-632

  Zaman, Vandana ^a,b   Shetty, Ashok K ^a,b  

^a DURHAM VA MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

5 bromodeoxyuridine; Fetal cells grafts; Graft cell survival; Graft integration; Neural transplantation; Neurotrophic factors; Post lesion plasticity

Indexed keywords

BROXURIDINE; FIBROBLAST GROWTH FACTOR 2; KAINIC ACID; MITOCHONDRIAL ENZYME; NEUROFILAMENT PROTEIN; NEUROTROPHIC FACTOR; NUCLEAR PROTEIN;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; BRAIN NERVE CELL; CELL COUNT; CELL FRACTIONATION; CELL LABELING; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; FETUS CELL; HIPPOCAMPUS; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REVIEW; STATISTICAL ANALYSIS; STROKE; TEMPORAL LOBE EPILEPSY;

ANIMALS; BRAIN TISSUE TRANSPLANTATION; BROMODEOXYURIDINE; CELL DIVISION; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; FETUS; FIBROBLAST GROWTH FACTOR 2; GRAFT SURVIVAL; HIPPOCAMPUS; KAINIC ACID; MALE; MEMORY DISORDERS; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY; NEURONS; PHENOTYPE; RATS; RATS, INBRED F344; STEM CELLS;

EID: 0042090573     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10091     Document Type: Review

References (85)

1. Altman J, Bayer SA. 1990. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325-3421.
2. Baldwin SA, Gibson T, Callihan CT, Sullivan PG., Palmer E, Scheff SW. 1997. Neuronal cell loss in the CA3 subfield of the hippocampus following cortical contusion utilizing the optical dissector method for cell counting. J Neurotrauma 14:485-398.
3. Ballarin M, Ernfors P, Lindefors N, Persson H. 1991. Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Exp Neurol 114:35-43.
4. Ben-Ari Y. 1985. Limbic seizures and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
5. Bhatnagar M, Cintra A, Chadi G, Lindberg J, Oitzl M, De Kloet ER, Moller A, Agnati LF, Fuxe K. 1997. Neurochemical changes in the hippocampus of the brown Norway rat during aging. Neurobiol Aging 18:319-327.
6. Bjorklund A, Lindvall O. 2000. Cell replacement therapies for central nervous system disorders. Nature Neurosci 3:537-544.
7. Borlongan CV, Koutouzis TK, Poulos SG, Saporta S, Sanberg PR. 1998. Bilateral fetal striatal grafts in the 3-nitropropionic acid-induced hypoactive model of Huntington's disease. Cell Transplant 7:131-135.
8. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
9. Brewer GJ. 1999. Regeneration and proliferation of embryonic and adult rat hippocampal neurons in culture. Exp Neurol 159:237-247.
10. Brundin P, Karlsson J, Emgard M, Schierle GS, Hansson O, Petersen A, Castilho RF. 2000. Improving the survival of grafted dopaminergic neurons: a review over current approaches. Cell Transplant 9:179-195.
11. Buckmaster PS, Dudek FE. 1997. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate treated rats. J Comp Neurol 385:385-404.
12. Buckmaster PS, Jongen-Relo AL. 1999. Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519-9529.
13. Bugra K, Pollard H, Charton G, Moreau J, Ben-Ari Y, Khrestchatisky M. 1994. aFGF, bFGF and flg mRNAs show distinct patterns of induction in the hippocampus following kainate-induced seizures. Eur J Neurosci 6:58-66.
14. Claffey KP, Abrams K, Shih SC, Brown LF, Mullen A, Keough M. 2001. Fibroblast growth factor 2 activation of stromal cell vascular endothelial growth factor expression and angiogenesis. Lab Invest 81:61-75.
15. Clarkson ED, Zawada WM, Bell KP, Esplen JE, Choi PK, Heidenreich KA, Freed CR. 2001. IGF-I and bFGF improve dopamine neuron survival and behavioral outcome in parkinsonian rats receiving cultured human fetal tissue strands. Exp Neurol 168:183-191.
16. Collier TJ, Sortwell CE, Daley BF. 1999. Diminished viability, growth, and behavioral efficacy of fetal dopamine neuron grafts in aging rats with long-term dopamine depletion: an argument for neurotrophic supplementation. J Neurosci 13:5563-5573.
17. Cottrell DA, Blakely EL, Johnson MA, Ince PG, Turnbull DM. 2001. Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD. Neurology 57:260-264.
18. DeToledo JC. 1999. Changing presentation of seizures with aging: clinical and etiological factors. Gerontology 45:329-335.
19. Dugich-Djordjevic VM, Tocco G, Willoughby I, Najm G, Pasinetti R, Thompson RF, Baudry M, Lapchak P, Hefti F. 1992. BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron 8:1127-1138.
20. Dunnett SB. 1995. Functional repair of striatal systems by neural transplants: evidence of circuit reconstruction. Behav Brain Res 66:133-142.
21. Eves EM, Skoczylas C, Yoshida K, Alnemri ES, Rosner MR. 2001. FGF induces a switch in death receptor pathways in neuronal cells. J Neurosci 21:4996-5006.
22. Faught E. 1999. Epidemiology and drug treatment of epilepsy in the elderly. Drugs Aging 15:255-269.
23. Ferhet L, Represa A, Zouaoui-Aggoun D, Ferhet W, Ben-Ari Y, Khrestchatisky M. 1997. FGF-2 induces nerve growth factor expression in cultured rat hippocampal neurons. Eur J Neurosci 9:1282-1289.
24. Freeman TB, Willing A, Zigova T, Sanberg PR, Hauser RA. 2001. Neural transplantation in Parkinson's disease. Adv Neurol 86:435-45.
25. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fischer LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J. 1995. Survival and differentiation of adult neural progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A 92:11879-11183.
26. Gall C, Murray K, Isackson PJ. 1991. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Mol Brain Res 9:113-123.
27. Gareri P, Gravina T, Ferreri G, DeSarro G. 1999. Treatment of epilepsy in the elderly. Prog Neurobiol 58:389-407.
28. Gerwins P, Skoldenberg E, Claesson-Welsh L. 2000. Function of fibroblast growth factors and vascular endothelial growth factors and their receptors in angiogenesis. Crit Rev Oncol Hematol 34:185-194.
29. Goutan E, Marti E, Ferrer I. 1998. BDNF, and full length and truncated trkB expression in the hippocampus of the rat following kainic acid excitotoxic damage. Evidence of complex time-dependent and cell-specific responses. Mol Brain Res 59:154-164.
30. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Schapira AH. 1996. Mitochondrial defect in Huntington's disease caudate nucleus. Ann Neurol 39:385-389.
31. Gundersen HJG. 1986. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones. J Microsc 143:3-45.
32. Gundersen HJG, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
33. Guthrie KM, Nguyen T, Gall CM. 1995. Insulin-like growth factor-1 mRNA is increased in deafferented hippocampus: spatio-temporal correspondence of a trophic event with axon sprouting. J Comp Neurol 352:147-160.
34. Kordower JH, Freeman TB, Snow BJ, Vingerhoets FJG, Mufson EJ, Sanberg PR, Hauser RA, Smith DA, Nauert GM, Perl DP, Olanow CW. 1995. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N Engl J Med 332:1118-1124.
35. Kordower JH, Freeman TB, Chen EY, Mufson EJ, Sanberg PR, Hauser RA, Snow B, Olanow CW. 1998. Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Movement Disord 13:383-393.
36. Lowenstein DH, Seren MS, Longo FM. 1993. Prolonged increases in neurotrophic activity associated with kainate-induced hippocampal synaptic reorganization. Neuroscience 56:597-604.
37. Mattson MP, Kumar KN, Wang H, Cheng B, Michaelis EK. 1993. Basic FGF regulates the expression of a functional 71 kDa NMDA receptor protein that mediates calcium influx and neurotoxicity in hippocampal neurons. J Neurosci 13:4575-4588.
38. Mudrick LA, Baimbridge KG. 1991. Hippocampal neurons transplanted into ischemically lesioned hippocampus: anatomical assessment of survival, maturation and integration. Exp Brain Res 86:233-247.
39. Nadler JV, Perry BW, Cotman CW. 1978. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271:676-677.
40. Nadler JV, Perry BW, Gentry C, Cotman CW. 1980a. Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J Comp Neurol 192:333-359.
41. Nadler JV, Perry BW, Cotman CW. 1980b. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res 182:1-9.
42. Okazaki MM, Evenson DA, Nadler JV. 1995. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 352: 515-534.
43. Okazaki MM, Molnar P, Nadler JV. 1999. Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth. J Neurophysiol 81:1645-1660.
44. Olanow CW, Kordower JH, Freeman TB. 1996. Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci 19:102-109.
45. Oorschot DE. 1994. Are you using neuronal densities, synaptic densities or neurochemical densities as your definitive data? There is a better way to go. Prog Neurobiol 44:233-247.
46. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. 1999. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487-8497.
47. Rudge JS, Mather PE, Pasnikowski EM, Cai N, Corcoran T, Acheson A, Anderson K, Lindsay RM, Wiegand SJ. 1998. Endogenous BDNF protein is increased in adult rat hippocampus after a kainic acid induced excitotoxic insult but exogenous BDNF is not neuroprotective. Exp Neurol 149:398-410.
48. Scallet AC, Nony PL, Rountree RL, Binienda ZK. 2001. Biomarkers of 3-nitropropionic acid (3-NPA)-induced mitochondrial dysfunction as indicators of neuroprotection. Ann NY Acad Sci 939:381-392.
49. Scott SA, Liang S, Weingartner JA, Crutcher KA. 1994. Increased NGF-like activity in young but not aged rat hippocampus after septal lesions. Neurobiol Aging 15:337-346.
50. Shetty AK. 2001. Fetal hippocampal CA3 cell grafts into the lesioned adult CA3 region restore host hippocampal calbindin expression in a rat model of temporal lobe epilepsy. Soc Neurosci Abs 27.
51. Shetty AK. 2002. Entorhinal axons exhibit sprouting in CA1 subfield of the adult hippocampus in a rat model of temporal lobe epilepsy. Hippocampus 12:534-542.
52. Shetty AK, Turner DA. 1995a. Enhanced cell survival in fetal hippocampal suspension transplants grafted to adult rat hippocampus following kainate lesions: a three-dimensional graft reconstruction study. Neuroscience 67:561-582.
53. Shetty AK, Turner DA. 1995b. Non-phosphorylated neurofilament protein immunoreactivity in adult and developing rat hippocampus: specificity and application in grafting studies. Brain Res 676:293-306.
54. Shetty AK, Turner DA. 1996. Development of fetal hippocampal grafts in intact and lesioned hippocampus. Prog Neurobiol 50:597-653.
55. Shetty AK, Turner DA. 1997a. Development of long-distance efferent projections from fetal hippocampal grafts depends upon pathway specificity and graft location in kainate-lesioned adult hippocampus. Neuroscience 76:1205-1219.
56. Shetty AK, Turner DA. 1997b. Fetal hippocampal cells grafted to kainate-lesioned CA3 region of adult hippocampus suppress aberrant supragranular sprouting of host mossy fibers. Exp Neurol 143:231-245.
57. Shetty AK, Turner DA. 1998. In vitro survival and differentiation of neurons derived from epidermal growth factor-responsive postnatal hippocampal stem cells: inducing effects of brain-derived neurotrophic factor. J Neurobiol 35:395-425.
58. Shetty AK, Turner DA. 1999a. Aging impairs axonal sprouting response of dentate granule cells following target loss and partial deafferentation. J Comp Neurol 414:238-254.
59. Shetty AK, Turner DA. 1999b. Vulnerability of the dentate gyrus to aging and intracerebroventricular administration of kainic acid. Exp Neurol 158:491-503.
60. Shetty AK, Turner DA. 1999c. Stem cells from fetal hippocampal field CA3 proliferate in response to FGF or EGF, and differentiate into field-specific phenotypic neurons. Soc Neurosci Abs 25.
61. Shetty AK, Turner DA. 2000. Fetal hippocampal transplants containing CA3 Cells restore host hippocampal interneuron numbers in a rat model of temporal lobe epilepsy. J Neurosci 20:8788-8801.
62. Shetty AK, Madison RD, Bradley J, Turner DA. 1994. Quantitative graft integration of fetal hippocampal transplants labeled with 5′ bromodeoxyuridine into normal adult hippocampus. Exp Neurol 126:205-224.
63. Shetty AK, Zaman V, Turner DA. 2000. Pattern of long-distance projections from fetal hippocampal field CA3 and CA1 cell grafts in lesioned CA3 of adult hippocampus follows intrinsic character of respective donor cells. Neuroscience 99:243-255.
64. Shihabuddin LS, Holets VR, Whittemore SR. 1996. Selective hippocampal lesions differentially affects the phenotypic fate of transplanted neuronal precursor cells. Exp Neurol 139:61-72.
65. Sperk G. 1994. Kainic acid seizures in the rat. Prog Neurobiol 42:1-32.
66. Sterio DC. 1984. The unbiased estimation of number and sizes of arbitrary particles using the dissector. J Microsc 134:127-136.
67. Szebenyi G, Dent EW, Callaway JL, Seys C, Lueth H, Kalil K. 2001. Fibroblast growth factor-2 promotes axon branching of cortical neurons by influencing morphology and behavior of the primary growth cone. J Neurosci 21:3932-3941
68. Takayama H, Ray J, Raymon HK, Baird A, Hogg J, Fisher LJ, Gage FH. 1995. Basic fibroblast growth factor increases dopaminergic graft survival and function in a rat model of Parkinson's disease. Nat Med 1:53-58.
69. Tamatini M, Ogawa S, Nunez G, Tohyama M. 1998. Growth factors prevent changes in Bcl-2 and Bax expression and neuronal apoptosis induced by nitric oxide. Cell Death Differ 5:911-919.
70. Tarricone BJ, Simon JR, Li YJ, Low WC. 1996. Neural grafting of cholinergic neurons in the hippocampal formation. Behav Brain Res 74: 25-44.
71. Tonder N. 1995. Neural transplantation to the normal and lesioned brain: an experimental study of the rat hippocampus. Acta Neurol Scand 91:6-30.
72. Tornqvist N, Bjorklund L, Almqvist P, Wahlberg L, Stromberg I. 2000. Implantation of bioactive growth factor-secreting rods enhances fetal dopaminergic graft survival, outgrowth density, and functional recovery in a rat model of Parkinson's disease. Exp Neurol 164:130-138.
73. Tretter YP, Hertel M, Munz B, ten Bruggencate G, Werner S, Alzheimer C. 2000. Induction of activin A is essential for the neuroprotective action of basic fibroblast growth factor in vivo. Nat Med 6:812-815.
74. Turner DA, Wheal HV. 1991. Excitatory synaptic potentials in kainic-acid denervated rat CA1 pyramidal neurons. J Neurosci 11:2786-2794.
75. Wagner JP, Black IB, DiCicco-Bloom E. 1999. Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 19:6006-6016.
76. Walicke PA. 1988. basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J Neurosci 8:2618-2627.
77. West MJ, Solmianka L, Gundersen HJG. 1991. Unbiased stereological estimation of the total number of neurons in subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
78. Woodruff ML, Baisden RH, Nonneman AJ. 1992. Effects of transplantation of fetal hippocampal or hindbrain tissue into the brains of adult rats with hippocampal lesions on water maze acquisition. Behav Neurosci 106:39-50.
79. Woods AG, Guthrie KM, Kurlawalla MA, Gall CM. 1998. Deafferentation-induced increases in hippocampal IGF-1 mRNA expression are severely attenuated in middle aged and aged rats. Neuroscience 83: 663-668.
80. Yurek DM, Fletcher-Turner A. 2001. Differential expression of GDNF, BDNF, and NT-3 in the aging nigrostriatal system following a neurotoxic lesion. Brain Res 89:228-235.
81. Zaman V, Shetty AK. 2001. Fetal hippocampal CA3 cell grafts transplanted to lesioned CA3 region of the adult hippocampus exhibit long-term survival in a rat model of temporal lobe epilepsy. Neurobiol Dis 8:942-952.
82. Zaman V, Shetty AK. 2002. Combined neurotrophic supplementation and Caspase inhibition enhances survival of fetal hippocampal CA3 cell grafts in lesioned CA3 region of the aging hippocampus. Neuroscience 109:537-553.
83. Zaman V, Turner DA, Shetty AK. 2000. Survival of grafted fetal neural cells in kainic acid lesioned CA3 region of adult hippocampus depends upon cell specificity. Exp Neurol 161:535-561.
84. Zaman V, Turner DA, Shetty AK. 2001. Prolonged post-lesion transplantation delay adversely influences survival of both homotopic and heterotopic fetal hippocampal cell grafts in kainate-lesioned CA3 region of adult hippocampus. Cell Transplant 10:41-52.
85. Zawada WM, Zastrow DJ, Clarkson ED, Adams FS, Bell KP, Freed CR. 1998. Growth factors improve immediate survival of embryonic dopamine neurons after transplantation into rats. Brain Res 786:96-103.