Morphological differentiation of tau-green fluorescent protein embryonic stem cells into neurons after co-culture with auditory brain stem slices

Neuroscience

Volumn 162, Issue 2, 2009, Pages 472-481

  Glavaski Joksimovic, A ^a   Thonabulsombat, C ^a,b   Wendt, M ^a,c   Eriksson, M ^a   Ma, H ^a   Olivius, P ^a,c  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b MAHIDOL UNIVERSITY   (Thailand)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

cochlear implant; cochlear nucleus; embryonic stem cells; neuronal differentiation; organotypic culture; vestibulocochlear nerve

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEIN ANTIBODY; TAU PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN SLICE; BRAIN STEM; CELL DIFFERENTIATION; CELL LABELING; CELL MIGRATION; CELL STRUCTURE; CELL SURVIVAL; CELL SUSPENSION; COCHLEAR NUCLEUS; COCULTURE; CONGENITAL DEAFNESS; CONTROLLED STUDY; EMBRYONIC STEM CELL; GRAFT SURVIVAL; HAIR CELL; HEARING LOSS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INNER EAR; MONOCULTURE; NERVE CELL; NERVE TRANSPLANTATION; NONHUMAN; PERCEPTION DEAFNESS; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPIRAL GANGLION; SPRAGUE DAWLEY RAT; STEM CELL TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; COCHLEAR NUCLEUS; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; GREEN FLUORESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SYNAPSES; TAU PROTEINS; TISSUE CULTURE TECHNIQUES;

EID: 67649494322     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.04.070     Document Type: Article

References (71)

1. Abouelfetouh A., Kondoh T., Ehara K., and Kohmura E. Morphological differentiation of bone marrow stromal cells into neuron-like cells after co-culture with hippocampal slice. Brain Res 1029 (2004) 114-119
2. Altschuler R.A., O'Shea K.S., and Miller J.M. Stem cell transplantation for auditory nerve replacement. Hear Res 242 (2008) 110-116
3. Arima K. Ultrastructural characteristics of tau filaments in tauopathies: immuno-electron microscopic demonstration of tau filaments in tauopathies. Neuropathology 26 (2006) 475-483
4. Bajjalieh S.M., Frantz G.D., Weimann J.M., McConnell S.K., and Scheller R.H. Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J Neurosci 14 (1994) 5223-5235
5. Bajjalieh S.M., Peterson K., Shinghal R., and Scheller R.H. SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257 (1992) 1271-1273
6. Barraud P., Thompson L., Kirik D., Bjorklund A., and Parmar M. Isolation and characterization of neural precursor cells from the Sox1-GFP reporter mouse. Eur J Neurosci 22 (2005) 1555-1569
7. Benninger F., Beck H., Wernig M., Tucker K.L., Brustle O., and Scheffler B. Functional integration of embryonic stem cell-derived neurons in hippocampal slice cultures. J Neurosci 23 (2003) 7075-7083
8. Binder L.I., Frankfurter A., and Rebhun L.I. The distribution of tau in the mammalian central nervous system. J Cell Biol 101 (1985) 1371-1378
9. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., and McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285 (1999) 754-756
10. Brustle O., Spiro A.C., Karram K., Choudhary K., Okabe S., and McKay R.D. In vitro-generated neural precursors participate in mammalian brain development. Proc Natl Acad Sci U S A 94 (1997) 14809-14814
11. Coleman B., De Silva M.G., and Shepherd R.K. Concise review: the potential of stem cells for auditory neuron generation and replacement. Stem Cells 25 (2007) 2685-2694
12. Coleman B., Fallon J.B., Pettingill L.N., de Silva M.G., and Shepherd R.K. Auditory hair cell explant co-cultures promote the differentiation of stem cells into bipolar neurons. Exp Cell Res 313 (2007) 232-243
13. Connelly C.A., Chen L.C., and Colquhoun S.D. Metabolic activity of cultured rat brainstem, hippocampal and spinal cord slices. J Neurosci Methods 99 (2000) 1-7
14. Corrales C.E., Pan L., Li H., Liberman M.C., Heller S., and Edge A.S. Engraftment and differentiation of embryonic stem cell-derived neural progenitor cells in the cochlear nerve trunk: growth of processes into the organ of Corti. J Neurobiol 66 (2006) 1489-1500
15. Dodson H.C., and Mohuiddin A. Response of spiral ganglion neurones to cochlear hair cell destruction in the guinea pig. J Neurocytol 29 (2000) 525-537
16. Doetschman T.C., Eistetter H., Katz M., Schmidt W., and Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87 (1985) 27-45
17. Evans M.J., and Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 292 (1981) 154-156
18. Fonnum F. Glutamate: a neurotransmitter in mammalian brain. J Neurochem 42 (1984) 1-11
19. Friauf E. Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur J Neurosci 4 (1992) 798-812
20. Gahwiler B.H., Capogna M., Debanne D., McKinney R.A., and Thompson S.M. Organotypic slice cultures: a technique has come of age. Trends Neurosci 20 (1997) 471-477
21. Gerrard L., Rodgers L., and Cui W. Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 23 (2005) 1234-1241
22. Glavaski-Joksimovic A., Thonabulsombat C., Wendt M., Eriksson M., Palmgren B., Jonsson A., and Olivius P. Survival, migration, and differentiation of Sox1-GFP embryonic stem cells in coculture with an auditory brainstem slice preparation. Cloning Stem Cells 10 (2008) 75-88
23. Goedert M., Spillantini M.G., Crowther R.A., Chen S.G., Parchi P., Tabaton M., Lanska D.J., Markesbery W.R., Wilhelmsen K.C., Dickson D.W., Petersen R.B., and Gambetti P. Tau gene mutation in familial progressive subcortical gliosis. Nat Med 5 (1999) 454-457
24. Gorath M., Stahnke T., Mronga T., Goldbaum O., and Richter-Landsberg C. Developmental changes of tau protein and mRNA in cultured rat brain oligodendrocytes. Glia 36 (2001) 89-101
25. Hackney C.M., Osen K.K., Ottersen O.P., Storm-Mathisen J., and Manjaly G. Immunocytochemical evidence that glutamate is a neurotransmitter in the cochlear nerve: a quantitative study in the guinea-pig anteroventral cochlear nucleus. Eur J Neurosci 8 (1996) 79-91
26. Hansen M.R., Zha X.M., Bok J., and Green S.H. Multiple distinct signal pathways, including an autocrine neurotrophic mechanism, contribute to the survival-promoting effect of depolarization on spiral ganglion neurons in vitro. J Neurosci 21 (2001) 2256-2267
27. Holley M.C. Application of new biological approaches to stimulate sensory repair and protection. Br Med Bull 63 (2002) 157-169
28. Hossain W.A., D'Sa C., and Morest D.K. Interactive roles of fibroblast growth factor 2 and neurotrophin 3 in the sequence of migration, process outgrowth, and axonal differentiation of mouse cochlear ganglion cells. J Neurosci Res 86 (2008) 2376-2391
29. Hu Z., Ulfendahl M., and Olivius N.P. Central migration of neuronal tissue and embryonic stem cells following transplantation along the adult auditory nerve. Brain Res 1026 (2004) 68-73
30. Hu Z., Ulfendahl M., and Olivius N.P. Survival of neuronal tissue following xenograft implantation into the adult rat inner ear. Exp Neurol 185 (2004) 7-14
31. Hu Z., Ulfendahl M., and Olivius P. NGF stimulates extensive neurite outgrowth from implanted dorsal root ganglion neurons following transplantation into the adult rat inner ear. Neurobiol Dis 18 (2005) 184-192
32. Hunter C., Petralia R.S., Vu T., and Wenthold R.J. Expression of AMPA-selective glutamate receptor subunits in morphologically defined neurons of the mammalian cochlear nucleus. J Neurosci 13 (1993) 1932-1946
33. Imitola J., Raddassi K., Park K.I., Mueller F.J., Nieto M., Teng Y.D., Frenkel D., Li J., Sidman R.L., Walsh C.A., Snyder E.Y., and Khoury S.J. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 101 (2004) 18117-18122
34. Johansson S., and Stromberg I. Guidance of dopaminergic neuritic growth by immature astrocytes in organotypic cultures of rat fetal ventral mesencephalon. J Comp Neurol 443 (2002) 237-249
35. Kamei N., Oishi Y., Tanaka N., Ishida O., Fujiwara Y., and Ochi M. Neural progenitor cells promote corticospinal axon growth in organotypic co-cultures. Neuroreport 15 (2004) 2579-2583
36. Kawata M., Sekiya S., Kera K., Kimura H., and Takamizawa H. Neural rosette formation within in vitro spheroids of a clonal human teratocarcinoma cell line, PA-1/NR: role of extracellular matrix components in the morphogenesis. Cancer Res 51 (1991) 2655-2669
37. Koch P., Opitz T., Steinbeck J.A., Ladewig J., and Brustle O. A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration. Proc Natl Acad Sci U S A 106 (2009) 3225-3230
38. Layton M.G., Robertson D., Everett A.W., Mulders W.H., and Yates G.K. Cellular localization of voltage-gated calcium channels and synaptic vesicle-associated proteins in the guinea pig cochlea. J Mol Neurosci 27 (2005) 225-244
39. Lee C.S., Tee L.Y., Dusenbery S., Takata T., Golden J.P., Pierchala B.A., Gottlieb D.I., Johnson Jr. E.M., Choi D.W., and Snider B.J. Neurotrophin and GDNF family ligands promote survival and alter excitotoxic vulnerability of neurons derived from murine embryonic stem cells. Exp Neurol 191 (2005) 65-76
40. Lendahl U., Zimmerman L.B., and McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 60 (1990) 585-595
41. Li H., Roblin G., Liu H., and Heller S. Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc Natl Acad Sci U S A 100 (2003) 13495-13500
42. Martinez-Monedero R., and Edge A.S. Stem cells for the replacement of inner ear neurons and hair cells. Int J Dev Biol 51 (2007) 655-661
43. Martinez-Monedero R., Yi E., Oshima K., Glowatzki E., and Edge A.S. Differentiation of inner ear stem cells to functional sensory neurons. Dev Neurobiol 68 (2008) 669-684
44. Matsumoto M., Nakagawa T., Kojima K., Sakamoto T., Fujiyama F., and Ito J. Potential of embryonic stem cell-derived neurons for synapse formation with auditory hair cells. J Neurosci Res 86 (2008) 3075-3085
45. McFadden S.L., Ding D., Jiang H., and Salvi R.J. Time course of efferent fiber and spiral ganglion cell degeneration following complete hair cell loss in the chinchilla. Brain Res 997 (2004) 40-51
46. Miller J.M., Chi D.H., O'Keeffe L.J., Kruszka P., Raphael Y., and Altschuler R.A. Neurotrophins can enhance spiral ganglion cell survival after inner hair cell loss. Int J Dev Neurosci 15 (1997) 631-643
47. Ogata Y., Slepecky N.B., and Takahashi M. Study of the gerbil utricular macula following treatment with gentamicin, by use of bromodeoxyuridine and calmodulin immunohistochemical labelling. Hear Res 133 (1999) 53-60
48. Ohira A., Yamamoto M., Honda O., Ohnishi Y., Inomata H., and Honda Y. Glial-, neuronal- and photoreceptor-specific cell markers in rosettes of retinoblastoma and retinal dysplasia. Curr Eye Res 13 (1994) 799-804
49. Olivius P., Alexandrov L., Miller J., Ulfendahl M., Bagger-Sjoback D., and Kozlova E.N. Allografted fetal dorsal root ganglion neuronal survival in the guinea pig cochlea. Brain Res 979 (2003) 1-6
50. Park K.I., Hack M.A., Ourednik J., Yandava B., Flax J.D., Stieg P.E., Gullans S., Jensen F.E., Sidman R.L., Ourednik V., and Snyder E.Y. Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp Neurol 199 (2006) 156-178
51. Park K.I., Himes B.T., Stieg P.E., Tessler A., Fischer I., and Snyder E.Y. Neural stem cells may be uniquely suited for combined gene therapy and cell replacement: evidence from engraftment of neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp Neurol 199 (2006) 179-190
52. Pratt T., Sharp L., Nichols J., Price D.J., and Mason J.O. Embryonic stem cells and transgenic mice ubiquitously expressing a tau-tagged green fluorescent protein. Dev Biol 228 (2000) 19-28
53. Radojevic V., and Kapfhammer J.P. Repair of the entorhino-hippocampal projection in vitro. Exp Neurol 188 (2004) 11-19
54. Rask-Andersen H., Bostrom M., Gerdin B., Kinnefors A., Nyberg G., Engstrand T., Miller J.M., and Lindholm D. Regeneration of human auditory nerve. In vitro/in video demonstration of neural progenitor cells in adult human and guinea pig spiral ganglion. Hear Res 203 (2005) 180-191
55. Regala C., Duan M., Zou J., Salminen M., and Olivius P. Xenografted fetal dorsal root ganglion, embryonic stem cell and adult neural stem cell survival following implantation into the adult vestibulocochlear nerve. Exp Neurol 193 (2005) 326-333
56. Rivolta M.N., Li H., and Heller S. Generation of inner ear cell types from embryonic stem cells. Methods Mol Biol 330 (2006) 71-92
57. Sanchez-Calderon H., Milo M., Leon Y., and Varela-Nieto I. A network of growth and transcription factors controls neuronal differentiation and survival in the developing ear. Int J Dev Biol 51 (2007) 557-570
58. Scheffler B., Schmandt T., Schroder W., Steinfarz B., Husseini L., Wellmer J., Seifert G., Karram K., Beck H., Blumcke I., Wiestler O.D., Steinhauser C., and Brustle O. Functional network integration of embryonic stem cell-derived astrocytes in hippocampal slice cultures. Development 130 (2003) 5533-5541
59. Steward O. The process of reinnervation in the dentate gyrus of adult rats: gene expression by neurons during the period of lesion-induced growth. J Comp Neurol 359 (1995) 391-411
60. Stoppini L., Buchs P.A., and Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37 (1991) 173-182
61. Takuma H., Sakurai M., and Kanazawa I. In vitro formation of corticospinal synapses in an organotypic slice co-culture. Neuroscience 109 (2002) 359-370
62. Thanos S., and Bonhoeffer F. Axonal arborization in the developing chick retinotectal system. J Comp Neurol 261 (1987) 155-164
63. Thonabulsombat C., Johansson S., Spenger C., Ulfendahl M., and Olivius P. Implanted embryonic sensory neurons project axons toward adult auditory brainstem neurons in roller drum and Stoppini co-cultures. Brain Res 1170C (2007) 48-58
64. Uchida K., Okano H., Hayashi T., Mine Y., Tanioka Y., Nomura T., and Kawase T. Grafted swine neuroepithelial stem cells can form myelinated axons and both efferent and afferent synapses with xenogeneic rat neurons. J Neurosci Res 72 (2003) 661-669
65. Uziel A., Romand R., and Marot M. Development of cochlear potentials in rats. Audiology 20 (1981) 89-100
66. Webster M., and Webster D.B. Spiral ganglion neuron loss following organ of Corti loss: a quantitative study. Brain Res 212 (1981) 17-30
67. Wernig M., Tucker K.L., Gornik V., Schneiders A., Buschwald R., Wiestler O.D., Barde Y.A., and Brustle O. Tau EGFP embryonic stem cells: an efficient tool for neuronal lineage selection and transplantation. J Neurosci Res 69 (2002) 918-924
68. Wobus A.M., Holzhausen H., Jakel P., and Schoneich J. Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp Cell Res 152 (1984) 212-219
69. Woodhams P.L., and Atkinson D.J. Regeneration of entorhino-dentate projections in organotypic slice cultures: mode of axonal regrowth and effects of growth factors. Exp Neurol 140 (1996) 68-78
70. Zappia J.J., and Altschuler R.A. Evaluation of the effect of ototopical neomycin on spiral ganglion cell density in the guinea pig. Hear Res 40 (1989) 29-37
71. Zheng J.L., Keller G., and Gao W.Q. Immunocytochemical and morphological evidence for intracellular self-repair as an important contributor to mammalian hair cell recovery. J Neurosci 19 (1999) 2161-2170