Transplantation of embryonic neuroectodermal progenitor cells into the site of a photochemical lesion: Immunohistochemical and electrophysiological analysis

Journal of Neurobiology

Volumn 66, Issue 10, 2006, Pages 1084-1100

  Anděrová, Miroslava ^a,b   Kubinová, Šárka ^a,b   Jelitai, Marti ^c   Neprašová, Helena ^a,b   Glogarová, Kateřina ^a,b   Prajerová, Iva ^a,b   Urdzíková, Lucie ^a,b   Chvátal, Alexandr ^a,b   Syková, Eva ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Astrocytes; Ischemia; Membrane properties; Neurons; Oligodendrocytes; Patch clamp; Potassium and sodium currents

Indexed keywords

BETA 3 TUBULIN; BETA TUBULIN; CELL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; NUCLEAR PROTEIN; POTASSIUM ION; PROTEIN NEUN; PROTEIN P53; RETINOIC ACID; SODIUM ION; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN CORTEX LESION; BRAIN ISCHEMIA; CELL MEMBRANE; CELL STRAIN; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEURAL STEM CELL; NEUROECTODERM; NEUROFILAMENT; NONHUMAN; OLIGODENDROGLIA; PATCH CLAMP; PHOTOCHEMICAL QUENCHING; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SODIUM CURRENT; STEM CELL TRANSPLANTATION;

ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; BRAIN ISCHEMIA; CELL DIFFERENTIATION; CELL LINE; CEREBRAL CORTEX; DENERVATION; DISEASE MODELS, ANIMAL; ECTODERM; GRAFT SURVIVAL; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MICE; NEURONS; OLIGODENDROGLIA; PATCH-CLAMP TECHNIQUES; PHOTOSENSITIZING AGENTS; STEM CELL TRANSPLANTATION; STEM CELLS; TRETINOIN;

EID: 33747609382     PISSN: 00223034     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/neu.20278     Document Type: Article

References (63)

1. Alonso G. 2005. NG2 proteoglycan-expressing cells of the adult rat brain: possible involvement in the formation of glial scar astrocytes following stab wound. Glia 49:318-338.
2. Anderova M, Antonova T, Petrik D, Neprasova H, Chvatal A, Sykova E. 2004. Voltage-dependent potassium currents in hypertrophied rat astrocytes after a cortical stab wound. Glia 48:311-326.
3. Balasubramaniyan V, de Haas AH, Bakels R, Koper A, Boddeke HW, Copray JC. 2004. Functionally deficient neuronal differentiation of mouse embryonic neural stem cells in vitro. Neurosci Res 49:261-265.
4. Benninger F, Beck H, Wernig M, Tucker KL, Brustle O, Scheffler B. 2003. Functional integration of embryonic stem cell-derived neurons in hippocampal slice cultures. J Neurosci 23:7075-7083.
5. Bergles DE, Jahr CE. 1997. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19:1297-1308.
6. Bergles DE, Jahr CE. 1998. Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 18:7709-7716.
7. Berry M, Hubbard P, Butt AM. 2002. Cytology and lineage of NG2-positive glia. J Neurocytol 31:457-467.
8. Bjorklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O. 2002. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A 99:2344-2349.
9. Bordey A, Lyons SA, Hablitz JJ, Sontheimer H. 2001. Electrophysiological characteristics of reactive astrocytes in experimental cortical dysplasia. J Neurophysiol 85:1719-1731.
10. Calhoun JD, Lambert NA. Mitalipova MM, Noggle SA, Lyons I, Condie BG, Stice SL. 2003. Differentiation of rhesus embryonic stem cells to neural progenitors and neurons. Biochem Biophys Res Commun 306:191-197.
11. Calza L, Giuliani A, Fernandez M, Pirondi S, D'Intino G, Aloe L. Giardino L. 2003. Neural stem cells and cholinergic neurons: regulation by immunolesion and treatment with mitogens, retinoic acid, and nerve growth factor. Proc Natl Acad Sci U S A 100:7325-7330.
12. Clark RA, Gurd JW, Bissoon N, Tricaud N, Molnar E, Zamze SE, Dwek RA, McIlhinney RA, and Wing DR. 1998. Identification of lectin-purified neural glyco-proteins, GPs 180, 116, and 110, with NMDA and AMPA receptor subunits: conservation of glycosylation at the synapse. J Neurochem 70:2594-2605.
13. Chu K, Kim M, Jeong SW, Kim SU, Yoon BW. 2003. Human neural stem cells can migrate, differentiate, and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci Lett 343: 129-133.
14. Demeter K, Herberth B, Duda E, Domonkos A, Jaffredo T, Herman JP, Madarasz E. 2004. Fate of cloned embryonic neuroectodermal cells implanted into the adult, newborn and embryonic forebrain. Exp Neurol 188:254-267.
15. Englund U, Bjorklund A, Wictorin K, Lindvall O, Kokaia M. 2002. Grafted neural stem cells develop into functional pyramidal neurons and integrate into host cortical circuitry. Proc Natl Acad Sci U S A 99:17089-17094.
16. Frisen J, Johansson CB, Torok C, Risling M, Lendahl U. 1995. Rapid, widespread, and long lasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453-464.
17. Fujiwara Y, Tanaka N, Ishida O, Fujimoto Y, Murakami T, Kajihara H, Yasunaga Y, Ochi M. 2004. Intravenously injected neural progenitor cells of transgenic rats can migrate to the injured spinal cord and differentiate into neurons, astrocytes and oligodendrocytes. Neurosci Lett 366:287-291.
18. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL. 1996. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16: 1091-1100.
19. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100.
20. Hayashi J, Takagi Y, Fukuda H, Imazato T, Nishimura M, Fujimoto M, Takahashi J, Hashimoto N, Nozaki K. 2006. Primate embryonic stem cell-derived neuronal progenitors transplanted into ischemic brain. J Cereb Blood Flow Metab. In press.
21. Herberth B, Pataki A, Jelitai M, Schlett, Deak, Spat A, Madarasz E. 2002. Changes of KCl sensitivity of proliferating neural progenitors during in vitro neurogenesis. J Neurosci Res, 67:574-582.
22. Jelitai M, Anderova M, Marko K, Kekesi K, Koncz P, Sykova E, Madarasz E. 2004. Role of gamma-aminobutyric acid in early neuronal development: studies with an embryonic neuroectodermal stem cell clone. J Neurosci Res 76:801-811.
23. Jelitai M, Schlett K, Varju P, Eisel U, Madarasz E. 2002. Regulated appearance of NMDA receptor subunits and channel functions during in vitro neuronal differentiation. J Neurobiol 51:54-65.
24. Jendelova P, Herynek V, Urdzikova L, Glogarova K, Kroupova J, Andersson B, Bryja V, Burian M, Hajek M, Sykova E. 2004. Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J Neurosci Res 76:232-243.
25. Johe KK, Hazal TG, Muller T, Dugich-Djordjevic MM, McKay RDG. 1996. Single factors direct the differentiation of stem cells from fetal and adult nervous system. Genes Dev 10:3129-3140.
26. Kamei N, Oishi Y, Tanaka N, Ishida O, Fujiwara Y, Ochi M. 2004. Neural progenitor cells promote corticospinal axon growth in organotypic co-cultures. Neuroreport 15:2579-2583.
27. Kim JH, Auerbach JM, Rodriguez-Gomez JA, Velasco I, Gavin D, Lumelsky N, Lee SH, Nguyen J, Sanchez-Pernaute R, Bankiewicz K, McKay R. 2002. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418:50-56.
28. Kornyei Z, Szlavik V, Szabo B, Gocza E, Czirok A, Madarasz E. 2005. Humoral and contact interactions in astroglia/stem cell co-cultures in the course of glia-induced neurogenesis. Glia 49:430-444.
29. + conductances in glial cells of mouse hippocampal brain slices. Glia 15:173-187.
30. Lendahl U, Zimmerman LB, McKay RD. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
31. Lin SC, Bergles DE. 2002. Physiological characteristics of NG2-expressing glial cells. J Neurocytol 31:537-549.
32. Liu S, Qu Y, Stewart TJ, Howard MJ, Chakrabortty S, Holekamp TF, McDonald JW. 2000. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci US A97:6126-6131.
33. Martinez-Serrano A, Bjorklund A. 1997. Immortalized neural progenitor cells for CNS gene transfer and repair. Trends Neurosci 20:530-538.
34. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C. 2003. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750-1758.
35. McIlhinney RA, Le Bourdelles B, Molnar E, Tricaud N, Streit P, Whiting PJ. 1998. Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NR1a and NR2A in transfected cells. Neuropharmacology 37: 1355-1367.
36. McIlhinney RA, Molnar E, Atack JR, and Whiting PJ. 1996. Cell surface expression of the human N-methyl-D-aspartate receptor subunit 1a requires the co-expression of the NR2A subunit in transfected cells. Neuroscience 70:989-997.
37. Miles GB, Yohn DC, Wichterle H, Jessell TM, Rafuse VF, Brownstone RM. 2004. Functional properties of motoneurons derived from mouse embryonic stem cells. J Neurosci 24:7848-7858.
38. Mistry SK, Keefer EW, Cunningham BA, Edelman GM, Crossin KL. 2002. Cultured rat hippocampal neural progenitors generate spontaneously active neural networks. Proc Natl Acad Sci U S A 99:1621-1626.
39. Mizoguchi A, Nakanishi H, Kimura K, Matsubara K, Ozaki-Kuroda K, Katata T, Honda T, Kiyohara Y, Heo K, Higashi M, Tsutsumi T, Sonoda S, Ide C, Takai Y. 2002. Nectin: an adhesion molecule involved in formation of synapses. J Cell Biol 156: 555-565.
40. Mori H, and Mishina M. 1995. Structure and function of the NMDA receptor channel. Neuropharmacology 34: 1219-1237.
41. Nakayama T, Momoki-Soga T, Inoue N. 2003. Astrocyte-derived factors instruct differentiation of embryonic stem cells into neurons. Neurosci Res 46:241-249.
42. Park S, Lee KS, Lee YJ, Shin HA, Cho HY, Wang KC, Kim YS, Lee HT, Chung KS, Kim EY, Lim J. 2004. Generation of dopaminergic neurons in vitro from human embryonic stem cells treated with neurotrophic factors. Neurosci Lett 359:99-103.
43. Pastor A, Chvatal A, Sykova E, Kettenmann H. 1995. Glycine- and GABA-activated currents in identified glial cells of the developing rat spinal cord slice. Eur J Neurosci 7:1188-1198.
44. Piper DR, Mujtaba T, Rao MS, Lucero MT. 2000. Immunocytochemical and physiological characterization of a population of cultured human neural precursors. J Neurophysiol 84:534-548.
45. Plachta N, Bibel M, Tucker KL, Barde YA. 2004. Developmental potential of defined neural progenitors derived from mouse embryonic stem cells. Development 131: 5449-5456.
46. Ruschenschmidt C, Koch PG, Brustle O, Beck, H. 2005. Functional properties of ES cell-derived neurons engrafted into the hippocampus of adult normal and chronically epileptic rats. Epilepsia 46:174-183.
47. Satoh M, Sugino H, Yoshida T. 2000. Activin promotes astrocytic differentiation of a multipotent neural stem cell line and an astrocyte progenitor cell line from murine central nervous system. Neurosci Lett 284:143-146.
48. Schlett K, Herberth B, Madarasz E. 1997. In vitro pattern formation during neurogenesis in neuroectodermal progenitor cells immortalized by p53-deficiency. Int J Dev Neurosci 15:795-804.
49. Schlett K, Czirok A, Tarnok K, Vicsek T, Madarasz E. 2000. Dynamics of cell aggregation during in vitro neurogenesis by immortalized neuroectodermal progenitors. J Neurosci Res 60:184-194.
50. Schlett K, Madarasz E. 1997. Retinoic acid induced neural differentiation in a neuroectodermal cell line immortalized by p53 deficiency. J Neurosci Res 47: 405-415.
51. Seifert G, Rehn L, Weber M, Steinhauser C. 1997. AMPA receptor subunits expressed by single astrocytes in the juvenile mouse hippocampus. Brain Res Mol Brain Res 47:286-294.
52. Song HJ, Stevens CF, Gage FH. 2002. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5:438-445.
53. Stewart RR, Zigova T, Luskin MB. 1999. Potassium currents in precursor cells isolated from the anterior subventricular zone of the neonatal rat forebrain. J Neurophysiol 81:95-102.
54. Takagi Y, Takahashi J, Saiki H, Morizane A, Hayashi T, Kishi Y, Fukuda H, Okamoto Y, Koyanagi M, Ideguchi M, Hayashi H, Imazato T, Kawasaki H, Suemori H, Omachi S, Iida H, Itoh N, Nakatsuji N, Sasai Y, Hashimoto N. 2005. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 115:102-109.
55. Tamura Y, Kataoka Y, Cui Y, Yamada H. 2004. Cellular proliferation in the cerebral cortex following neural excitation in rats. Neurosci Res 50:129-133.
56. Uchida K, Momiyama T, Okano H, Yuzaki M, Koizumi A, Mine Y, Kawase T. 2005. Potential functional neural repair with grafted neural stem cells of early embryonic neuroepithelial origin. Neurosci Res 52:276-286.
57. Wang DD, Krueger DD, Bordey A. 2003. Biophysical properties and ionic signature of neuronal progenitors of the postnatal subventricular zone in situ. J Neurophysiol 90:2291-2302.
58. Wang LP, Kempermann G, Kettenmann H. 2005. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29:181-189.
59. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD. 1985. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17: 497-504.
60. Wernig M, Benninger F, Schmandt T, Rade M, Tucker KL, Bussow H, Beck H, Brustle O. 2004. Functional integration of embryonic stem cell-derived neurons in vivo. J Neurosci 24:5258-5268.
61. Westerlund U, Moe MC, Varghese M, Berg-Johnsen J, Ohlsson M, Langmoen IA, Svensson M. 2003. Stem cells from the adult human brain develop into functional neurons in culture. Exp Cell Res 289:378-383.
62. Yoshizaki T, Inaji M, Kouike H, Shimazaki T, Sawa-moto K, Ando K, Date I, Kobayashi K, Suhara T, Uchiyama Y, Okano H. 2004. Isolation and transplantation of dopaminergic neurons generated from mouse embryonic stem cells. Neurosci Lett 363:33-37.
63. Zhou M, Kimelberg HK. 2001. Freshly isolated hippocampal CA1 astrocytes comprise two populations differing in glutamate transporter and AMPA receptor expression. J Neurosci 21:7901-7908.