Transplantation of rat synapsin-EGFP-labeled embryonic neurons into the intact and ischemic CA1 hippocampal region: Distribution, phenotype, and axodendritic sprouting

Cell Transplantation

Volumn 20, Issue 8, 2011, Pages 1163-1178

  Kucharova, K ^a,b   Hefferan, M P ^b   Patel, P ^b,c   Marsala, S ^b   Nejime, T ^b   Miyanohara, A ^b   Marsala, M ^b,d   Drummond, J C ^b,c  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Axonal projection; Green fluorescent protein (GFP); Hippocampus; Ischemia; Neuronal transplantation; Rat

Indexed keywords

GREEN FLUORESCENT PROTEIN; SYNAPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN ISCHEMIA; CELL MIGRATION; CONTROLLED STUDY; FOREBRAIN; HIPPOCAMPAL CA1 REGION; IMMUNOREACTIVITY; LENTIVIRINAE; MALE; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NERVE TRANSPLANTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; SEPTUM NUCLEUS; STRATUM RADIATUM; SUBICULUM; SURVIVAL;

ANIMALIA; LENTIVIRUS; RATTUS; RATTUS NORVEGICUS;

ANIMALS; AXONS; CA1 REGION, HIPPOCAMPAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DENDRITES; EMBRYO, MAMMALIAN; GREEN FLUORESCENT PROTEINS; ISCHEMIC ATTACK, TRANSIENT; LENTIVIRUS; MALE; NEURONS; NEURONS, EFFERENT; PHENOTYPE; RATS; RATS, WISTAR; STAINING AND LABELING; SYNAPSINS;

EID: 84930474902     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X564544     Document Type: Article

References (79)

1. Amantea, D.; Nappi, G.; Bernardi, G.; Bagetta, G.; Cora- saniti, M. T. Post-ischemic brain damage: Pathophysiology and role of inflammatory mediators. FEBS J. 276: 13-26; 2009.
2. Arvidsson, A.; Collin, T.; Kirik, D.; Kokaia, Z.; Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8:963-970; 2002.
3. Bacigaluppi, M.; Pluchino, S.; Martino, G.; Kilic, E.; Hermann, D. M. Neural stem/precursor cells for the treatment of ischemic stroke. J. Neurol. Sci. 265:73-77; 2008.
4. Behrstock, S.; Ebert, A. D.; Klein, S.; Schmitt, M.; Moore, J. M.; Svendsen, C. N. Lesion-induced increase in survival and migration of human neural progenitor cells releasing GDNF. Cell Transplant. 17:753-762; 2008.
5. Benavides, J.; Capdeville, C.; Dauphin, F.; Dubois, A.; Duverger, D.; Fage, D.; Gotti, B.; MacKenzie, E. T.; Scat- ton, B. The quantification of brain lesions with an omega 3 site ligand: A critical analysis of animal models of cerebral ischaemia and neurodegeneration. Brain Res. 522: 275-289; 1990.
6. Bendel, O.; Bueters, T.; von Euler, M.; Ove Ogren, S.; Sandin, J.; von Euler, G. Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. J. Cereb. Blood Flow. Metab. 25: 1586-1595; 2005.
7. Bliss, T.; Guzman, R.; Daadi, M.; Steinberg, G. K. Cell transplantation therapy for stroke. Stroke 38:817-826; 2007.
8. Buhnemann, C.; Scholz, A.; Bernreuther, C.; Malik, C. Y.; Braun, H.; Schachner, M.; Reymann, K. G.; Dihne, M. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain 129:3238-3248; 2006.
9. Chu, K.; Jung, K. H.; Kim, S. J.; Lee, S. T.; Kim, J.; Park, H. K.; Song, E. C.; Kim, S. U.; Kim, M.; Lee, S. K.; Roh, J. K. Transplantation of human neural stem cells protect against ischemia in a preventive mode via hypoxia-induc- ible factor-1alpha stabilization in the host brain. Brain Res. 1207:182-192; 2008.
10. Cizkova, D.; Kakinohana, O.; Kucharova, K.; Marsala, S.; Johe, K.; Hazel, T.; Hefferan, M. P.; Marsala, M. Functional recovery in rats with ischemic paraplegia after spinal grafting of human spinal stem cells. Neuroscience 147: 546-560; 2007.
11. Colom, L. V.; Castaneda, M. T.; Reyna, T.; Hernandez, S.; Garrido-Sanabria, E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 58:151-164; 2005.
12. Daadi, M. M.; Davis, A. S.; Arac, A.; Li, Z.; Maag, A.; Bhatnagar, R.; Jiang, K.; Sun, G.; Wu, J. C.; Steinberg, G. K. Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic-ischemic brain injury. Stroke 41:516-523; 2010.
13. Daadi, M. M.; Lee, S. H.; Arac, A.; Grueter, B. A.; Bhatnagar, R.; Maag, A.; Schaar, B.; Malenka, R. C.; Palmer, T. D.; Steinberg, G. K. Functional engraftment of the medial ganglionic eminence cells in experimental stroke model. Cell Transplant. 18:815-826; 2009.
14. Dempsey, R. J.; Kalluri, H. S. Ischemia-induced neurogenesis: Role of growth factors. Neurosurg. Clin. North Am. 18:183-190; 2007.
15. Fournier, A. E.; GrandPre, T.; Strittmatter, S. M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409:341-346; 2001.
16. Frahm, C.; Haupt, C.; Witte, O. W. GABA neurons survive focal ischemic injury. Neuroscience 127:341-346; 2004.
17. Freund, T. F.; Antal, M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173; 1988
18. Gascon, S.; Paez-Gomez, J. A.; Diaz-Guerra, M.; Scheif- fele, P.; Scholl, F. G. Dual-promoter lentiviral vectors for constitutive and regulated gene expression in neurons. J. Neurosci. Methods 168:104-112; 2008.
19. Glover, C. P.; Bienemann, A. S.; Heywood, D. J.; Cosgrave, A. S.; Uney, J. B. Adenoviral-mediated, high-level, cell- specific transgene expression: A SYN1-WPRE cassette mediates increased transgene expression with no loss of neuron specificity. Mol. Ther. 5:509-516; 2002.
20. Goutagny, R.; Manseau, F.; Jackson, J.; Danik, M.; Williams, S. In vitro activation of the medial septum-diagonal band complex generates atropine-sensitive and atropine-resistant hippocampal theta rhythm: An investigation using a complete septohippocampal preparation. Hippocampus 18:531-535; 2008.
21. Gulyas, A. I.; Freund, T. F. Pyramidal cell dendrites are the primary targets of calbindin D28k-immunoreactive interneurons in the hippocampus. Hippocampus 6:525-534; 1996.
22. Gulyas, A. I.; Hajos, N.; Freund, T. F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 16:3397-3411; 1996.
23. Hayashi, J.; Takagi, Y.; Fukuda, H.; Imazato, T.; Nishi- mura, M.; Fujimoto, M.; Takahashi, J.; Hashimoto, N.; Nozaki, K. Primate embryonic stem cell-derived neuronal progenitors transplanted into ischemic brain. J. Cereb. Blood Flow Metab. 26:906-914; 2006.
24. Hirrlinger, P. G.; Scheller, A.; Braun, C.; Quintela- Schneider, M.; Fuss, B.; Hirrlinger, J.; Kirchhoff, F. Expression of reef coral fluorescent proteins in the central nervous system of transgenic mice. Mol. Cell. Neurosci. 30:291-303; 2005.
25. Hughes, D. I.; Mackie, M.; Nagy, G. G.; Riddell, J. S.; Maxwell, D. J.; Szabó, G.; Erdélyi, F.; Veress, G.; Szücs, P.; Antal, M.; Todd, A. J. P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase-65 and originate from cells in deep medial dorsal horn. Proc. Nat. Acad. Sci. USA 102:9038-9043; 2005.
26. Hunt, D.; Coffin, R. S.; Anderson, P. N. The Nogo receptor, its ligands and axonal regeneration in the spinal cord; a review. J. Neurocytol. 31:93-120; 2002.
27. Ishibashi, S.; Sakaguchi, M.; Kuroiwa, T.; Yamasaki, M.; Kanemura, Y.; Shizuko, I.; Shimazaki, T.; Onodera, M.; Okano, H.; Mizusawa, H. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian ger- bils. J. Neurosci. Res. 78:215-223; 2004.
28. Jacobs, E. C.; Campagnoni, C.; Kampf, K.; Reyes, S. D.; Kalra, V.; Handley, V.; Xie, Y. Y.; Hong-Hu, Y.; Spreur, V.; Fisher, R. S.; Campagnoni, A. T. Visualization of cor- ticofugal projections during early cortical development in a tau-GFP-transgenic mouse. Eur. J. Neurosci. 25:17-30; 2007.
29. Jang, I. S.; Ito, Y.; Akaike, N. Feed-forward facilitation of glutamate release by presynaptic GABA(A) receptors. Neuroscience 135:737-748; 2005.
30. Jay, T. M.; Witter, M. P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 313:574-586; 1991.
31. Jessell, T. M.; Sanes, J. R. The development of the nervous system. In: Kandel, E. R.; Schwartz, J. H.; Jessell, T. M., eds. Principles of neural science. New York: McGraw-Hill, Health Profession Division; 2000:1019-1113.
32. Jiang, Q.; Zhang, Z. G.; Ding, G. L.; Zhang, L.; Ewing, J. R.; Wang, L.; Zhang, R.; Li, L.; Lu, M.; Meng, H.; Arbab, A. S.; Hu, J.; Li, Q. J.; Pourabdollah Nejad, D. S.; Athiraman, H.; Chopp, M. Investigation of neural progenitor cell induced angiogenesis after embolic stroke in rat using MRI. Neuroimage 28:698-707; 2005.
33. Johnston, R. E.; Dillon-Carter, O.; Freed, W. J.; Borlon- gan, C. V. Trophic factor secreting kidney cell lines: In vitro characterization and functional effects following transplantation in ischemic rats. Brain Res. 900:268-276; 2001.
34. Kakinohana, O.; Cizkova, D.; Tomori, Z.; Hedlund, E.; Marsala, S.; Isacson, O.; Marsala, M. Region-specific cell grafting into cervical and lumbar spinal cord in rat: A qualitative and quantitative stereological study. Exp. Neurol. 190:122-132; 2004.
35. Kamiguchi, H. The role of cell adhesion molecules in axon growth and guidance. Adv. Exp. Med. Biol. 621:95103; 2007.
36. Kim, D. S.; Kwak, S. E.; Kim, J. E.; Jung, J. Y.; Won, M. H.; Choi, S. Y.; Kwon, O. S.; Kang, T. C. Transient ischaemia affects plasma membrane glutamate transporter, not vesicular glutamate transporter, expressions in the ger- bil hippocampus. Anat. Histol. Embryol. 35:265-270; 2006.
37. Kirino, T. Delayed neuronal death. Neuropathology 20(Suppl.):S95-97; 2000.
38. Kurozumi, K.; Nakamura, K.; Tamiya, T.; Kawano, Y.; Ishii, K.; Kobune, M.; Hirai, S.; Uchida, H.; Sasaki, K.; Ito, Y.; Kato, K.; Honmou, O.; Houkin, K.; Date, I.; Hamada, H. Mesenchymal stem cells that produce neuro- trophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. Mol. Ther. 11:96-104; 2005.
39. Lai, A. Y.; Todd, K. G. Microglia in cerebral ischemia: Molecular actions and interactions. Can. J. Physiol. Pharmacol. 84:49-59; 2006.
40. Lalancette-Hebert, M.; Gowing, G.; Simard, A.; Weng, Y. C.; Kriz, J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neu-rosci. 27:2596-2605; 2007.
41. Leker, R. R.; McKay, R. D. Using endogenous neural stem cells to enhance recovery from ischemic brain injury. Curr. Neurovasc. Res. 1:421-427; 2004.
42. Lin, C. H.; Cheng, F. C.; Lu, Y. Z.; Chu, L. F.; Wang, C. H.; Hsueh, C. M. Protection of ischemic brain cells is dependent on astrocyte-derived growth factors and their receptors. Exp. Neurol. 201:225-233; 2006.
43. Lin, W.; McKinney, K.; Liu, L.; Lakhlani, S.; Jennes, L. Distribution of vesicular glutamate transporter-2 messenger ribonucleic Acid and protein in the septum-hypothala- mus of the rat. Endocrinology 144:662-670; 2003.
44. Llado, J.; Haenggeli, C.; Maragakis, N. J.; Snyder, E. Y.; Rothstein, J. D. Neural stem cells protect against glutamate-induced excitotoxicity and promote survival of injured motor neurons through the secretion of neurotrophic factors. Mol. Cell. Neurosci. 27:322-331; 2004.
45. Loscher, W.; Schirmer, M.; Freichel, C.; Gernert, M. Distribution of GABAergic neurons in the striatum of amygdala-kindled rats: An immunohistochemical and in situ hybridization study. Brain Res. 1083:50-60; 2006.
46. Magavi, S. S.; Lois, C. Transplanted neurons form both normal and ectopic projections in the adult brain. Dev. Neurobiol. 68:1527-1537; 2008.
47. Marsala, M.; Kakinohana, O.; Yaksh, T. L.; Tomori, Z.; Marsala, S.; Cizkova, D. Spinal implantation of hNT neurons and neuronal precursors: Graft survival and functional effects in rats with ischemic spastic paraplegia. Eur. J. Neurosci. 20:2401-2414; 2004.
48. Mendez, I.; Hong, M. Reconstruction of the striato-nigro- striatal circuitry by simultaneous double dopaminergic grafts: A tracer study using fluorogold and horseradish peroxidase. Brain Res. 778:194-205; 1997.
49. Mochizuki, N.; Takagi, N.; Kurokawa, K.; Onozato, C.; Moriyama, Y.; Tanonaka, K.; Takeo, S. Injection of neural progenitor cells improved learning and memory dysfunction after cerebral ischemia. Exp. Neurol. 211:194-202; 2008.
50. Mukerji, S. S.; Katsman, E. A.; Wilber, C.; Haner, N. A.; Selman, W. R.; Hall, A. K. Activin is a neuronal survival factor that is rapidly increased after transient cerebral ischemia and hypoxia in mice. J. Cereb. Blood Flow Metab. 27:1161-1172; 2007.
51. Nejime, T.; Miyanohara, A.; Kakinohana, O.; Marsala, M. Efficient transduction of rat spinal cord cells in vitro and in vivo using neuron-specific and non-specific lentiviral vectors. Mol. Ther. 9:S202; 2004.
52. Oertel, W. H.; Mugnaini, E. Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci. Lett. 47(3): 233-238; 1984.
53. Onifer, S. M.; Cannon, A. B.; Whittemore, S. R. Altered differentiation of CNS neural progenitor cells after transplantation into the injured adult rat spinal cord. Cell Transplant. 6:327-338; 1997.
54. Ourednik, V.; Ourednik, J. Graft/host relationships in the developing and regenerating CNS of mammals. Ann. NY Acad. Sci. 1049:172-184; 2005.
55. Pignataro, G.; Studer, F. E.; Wilz, A.; Simon, R. P.; Boison, D. Neuroprotection in ischemic mouse brain induced by stem cell-derived brain implants. J. Cereb. Blood Flow Metab. 27:919-927; 2007.
56. Ribak, C. E.; Seress, L.; Peterson, G. M.; Seroogy, K. B.; Fallon, J. H.; Schmued, L. C. A GABAergic inhibitory component within the hippocampal commissural pathway. J. Neurosci. 6:3492-3498; 1986.
57. Sandvig, A.; Berry, M.; Barrett, L. B.; Butt, A.; Logan, A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: Expression, receptor signaling, and correlation with axon regeneration. Glia 46:225-251; 2004.
58. Sanes, D. H.; Reh, T. A.; Harris, W. A. Axon growth and guidance. In: Sanes, D. H.; Reh, T. A.; Harris, W. A., eds. Development of the nervous system, 3rd ed. New York: Academic Press; 2000:145-202.
59. Shen, L. H.; Li, Y.; Chen, J.; Zhang, J.; Vanguri, P.; Borneman, J.; Chopp, M. Intracarotid transplantation of bone marrow stromal cells increases axon-myelin remodeling after stroke. Neuroscience 137:393-399; 2006.
60. 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. Exp. Neurol. 126:205-224; 1994.
61. Shetty, A. K.; Turner, D. A. Development of fetal hippocampal grafts in intact and lesioned hippocampus. Prog. Neurobiol. 50:597-653; 1996.
62. 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: 561-582; 1995.
63. Shetty, A. K.; Zaman, V.; Hattiangady, B. Repair of the injured adult hippocampus through graft-mediated modulation of the plasticity of the dentate gyrus in a rat model of temporal lobe epilepsy. J. Neurosci. 25:8391-8401; 2005.
64. Speed, H. E.; Dobrunz, L. E. Developmental changes in short-term facilitation are opposite at temporoammonic synapses compared to Schaffer collateral synapses onto CA1 pyramidal cells. Hippocampus 19:187-204; 2009.
65. Stoppinni, L.; Helm, G. A.; Stringer, J. L.; Lothman, W.; Bennett, Jr., J. P. In vitro and in vivo transplantation of fetal rat brain cells following incubation with various anatomic tracing substances. J. Neurosci. Methods 27: 121-132; 1989.
66. Thierry, A. M.; Gioanni, Y.; Degenetais, E.; Glowinski, J. Hippocampo-prefrontal cortex pathway: Anatomical and electrophysiological characteristics. Hippocampus 10: 411-419; 2000.
67. Tierney, P. L.; Degenetais, E.; Thierry, A. M.; Glowinski, J.; Gioanni, Y. Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur. J. Neurosci. 20:514524; 2004.
68. Toda, H.; Takahashi, J.; Iwakami, N.; Kimura, T.; Hoki, S.; Mozumi-Kitamura, K.; Ono, S.; Hashimoto, N. Grafting neural stem cells improved the impaired spatial recognition in ischemic rats. Neurosci. Lett. 316:9-12; 2001.
69. Toth, K.; Borhegyi, Z.; Freund, T. F. Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex. J. Neurosci. 13: 3712-3724; 1993.
70. Trendelenburg, G.; Dirnagl, U. Neuroprotective role of astrocytes in cerebral ischemia: Focus on ischemic preconditioning. Glia 50:307-320; 2005.
71. Vizi, E. S.; Kiss, J. P. Neurochemistry and pharmacology of the major hippocampal transmitter systems: Synaptic and nonsynaptic interactions. Hippocampus 8:566-607; 1998.
72. Wang, Y. Q.; Guo, X.; Qiu, M. H.; Feng, X. Y.; Sun, Y. VEGF overexpression enhances striatal neurogenesis in brain of adult rat after a transient middle cerebral artery occlusion. J. Neurosci. Res. 85:73-82; 2007.
73. Wictorin, K.; Bjorklund, A. Axon outgrowth from grafts of human embryonic spinal cord in the lesioned adult rat spinal cord. Neuroreport 3:1045-1048; 1992.
74. Wictorin, K.; Brundin, P.; Gustavii, B.; Lindvall, O.; Bjor- klund, A. Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 347:556-558; 1990.
75. Wiedenmann, B.; Franke, W. W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41:1017-1028; 1985.
76. Wong, A. M.; Hodges, H.; Horsburgh, K. Neural stem cell grafts reduce the extent of neuronal damage in a mouse model of global ischaemia. Brain Res. 1063:140-150; 2005.
77. Xiong, Y.; Mahmood, A.; Chopp, M. Angiogenesis, neurogenesis and brain recovery of function following injury. Curr. Opin. Investig. Drugs 11:298-308; 2010.
78. Yamashita, T.; Deguchi, K.; Nagotani, S.; Kamiya, T.; Abe, K. Gene and stem cell therapy in ischemic stroke. Cell Transplant. 18:999-1002; 2009.
79. Zhang, Z. H.; Wang, R. Z.; Li, G. L.; Wei, J. J.; Li, Z. J.; Feng, M.; Kang, J.; Du, W. C.; Ma, W. B.; Li, Y. N.; Yang, Y.; Kong, Y. G. Transplantation of neural stem cells modified by human neurotrophin-3 promotes functional recovery after transient focal cerebral ischemia in rats. Neurosci. Lett. 444:227-230; 2008.