Implanted embryonic sensory neurons project axons toward adult auditory brainstem neurons in roller drum and Stoppini co-cultures

Brain Research

Volumn 1170, Issue SUPPL.: COMPLETE, 2007, Pages 48-58

  Thonabulsombat, Charoensri ^b,c   Johansson, Saga ^d   Spenger, Christian ^c   Ulfendahl, Mats ^c   Olivius, Petri ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MAHIDOL UNIVERSITY   (Thailand)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Axonal outgrowth; Brainstem slice; Cochlear nucleus; Embryonic sensory neuron; Implantation; Organotypic culture

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; BRAIN STEM; CELL MIGRATION; CELL SURVIVAL; CELL TRANSPLANTATION; COCHLEAR NUCLEUS; COCULTURE; CONTROLLED STUDY; EMBRYO; INNER EAR; MOUSE; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE GRAFT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION; VESTIBULOCOCHLEAR NERVE;

ANIMALS; AUDITORY PATHWAYS; BRAIN STEM; CARBOCYANINES; CELL COMMUNICATION; COCHLEAR NUCLEUS; COCULTURE TECHNIQUES; CUES; FETAL TISSUE TRANSPLANTATION; GANGLIA, SPINAL; GRAFT SURVIVAL; GROWTH CONES; MICE; NEUROGENESIS; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; RATS; SENSORY RECEPTOR CELLS; STAINING AND LABELING;

RATTUS;

EID: 34548569302     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.06.085     Document Type: Article

References (57)

1. Acheson A., Conover J.C., Fandl J.P., DeChiara T.M., Russell M., Thadani A., Squinto S.P., Yancopoulos G.D., and Lindsay R.M. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374 6521 (1995) 450-453
2. Acosta C.G., Fabrega A.R., Masco D.H., and Lopez H.S. A sensory neuron subpopulation with unique sequential survival dependence on nerve growth factor and basic fibroblast growth factor during development. J. Neurosci. 21 (2001) 8873-8885
3. Altschuler R.A., Cho Y., Ylikoski J., Pirvola U., Magal E., and Miller J.M. Rescue and regrowth of sensory nerves following deafferentation by neurotrophic factors. Ann. N. Y. Acad. Sci. 884 (1999) 305-311
4. Bennett D.L., Michael G.J., Ramachandran N., Munson J.B., Averill S., Yan Q., McMahon S.B., and Priestley J.V. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci. 199 18 (1998) 3059-3072
5. Bergold P.J., and Casaccia-Bonnefil P. Preparation of organotypic hippocampal slice cultures using the membrane filter method. Methods Mol. Biol. 72 (1997) 15-22
6. Chen K., and Godfrey D.A. Sodium pentobarbital abolishes bursting spontaneous activity of dorsal cochlear nucleus in rat brain slices. Hear Res. 149 (2000) 216-222
7. Chen K., Waller H.J., and Godfrey D.A. Effects of endogenous acetylcholine on spontaneous activity in rat dorsal cochlear nucleus slices. Brain Res. 783 (1998) 219-226
8. Chen K., Waller H.J., Godfrey T.G., and Godfrey D.A. Glutamatergic transmission of neuronal responses to carbachol in rat dorsal cochlear nucleus slices. Neuroscience 90 (1999) 1043-1049
9. Eriksson N.P., Lindsay R.M., and Aldskogius H. BDNF and NT-3 rescue sensory but not motoneurones following axotomy in the neonate. NeuroReport 5 (1994) 1445-1448
10. Ernfors P. Local and target-derived actions of neurotrophins during peripheral nervous system development. Cell. Mol. Life Sci. 58 (2001) 1036-1044
11. Ernfors P., Van De Water T., Loring J., and Jaenisch R. Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14 (1995) 1153-1164
12. Freeman S., Khvoles R., Cherny L., and Sohmer H. Effect of long-term noise exposure on the developing and developed ear in the Rat. Audiol. Neuro-otol. 4 5 (1999) 207-218
13. Geal-Dor M., Freeman S., G.L., and Sohmer H. Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res. 69 1-2 (1993) 236-242
14. Gähwiler B.H. Development of the hippocampus in vitro: cell types, synapses and receptors. Neuroscience 11 (1984) 751-760
15. Gähwiler 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
16. Hafidi A. Distribution of BDNF, NT-3 and NT-4 in the developing auditory brainstem. Int. J. Dev. Neurosci. 17 (1999) 285-294
17. Hafidi A., Sanes D.H., and Hillman D.E. Regeneration of the auditory midbrain intercommissural projection in organotypic culture. J. Neurosci. 15 (1995) 1298-1307
18. 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
19. 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
20. Hu Z., Ulfendahl M., and Petri Olivius N. 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
21. Jahnsen H., Kristensen B.W., Thiebaud P., Noraberg J., Jakobsen B., Bove M., Martinoia S., Koudelka-Hep M., Grattarola M., and Zimmer J. Coupling of organotypic brain slice cultures to silicon-based arrays of electrodes. Methods 18 (1999) 160-172
22. 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
23. Kaltenbach J.A., Godfrey D.A., Neumann J.B., McCaslin D.L., Afman C.E., and Zhang J. Changes in spontaneous neural activity in the dorsal cochlear nucleus following exposure to intense sound: relation to threshold shift. Hear Res. 124 (1998) 78-84
24. Kozlova E.N., Rosario C.M., Stromberg I., Bygdeman M., and Aldskogius H. Peripherally grafted human foetal dorsal root ganglion cells extend axons into the spinal cord of adult host rats by circumventing dorsal root entry zone astrocytes. NeuroReport 6 2 (1995) 269-272
25. Kozlova E.N., Seiger A., and Aldskogius H. Human dorsal root ganglion neurons from embryonic donors extend axons into the host rat spinal cord along laminin-rich peripheral surroundings of the dorsal root transitional zone. J. Neurocytol. 26 (1997) 811-822
26. Levinsson A., Holmberg H., Schouenborg J., Seiger A., Aldskogius H., and Kozlova E.N. Functional connections are established in the deafferented rat spinal cord by peripherally transplanted human embryonic sensory neurons. Eur. J. Neurosci. 12 (2000) 3589-3595
27. Manis P.B., Spirou G.A., Wright D.D., Paydar S., and Ryugo D.K. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J. Comp. Neurol. 348 2 (1994) 261-276
28. Maruyama A., and Ohmori H. Fluorescent labeling of rat auditory brainstem circuits for synaptic and electrophysiological studies. J. Neurosci. Methods 152 (2006) 163-172
29. 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 4-5 (1997) 631-643
30. Minichiello L., Piehl F., Vazquez E., Schimmang T., Hokfelt T., Represa J., and Klein R. Differential effects of combined trk receptor mutations on dorsal root ganglion and inner ear sensory neurons. Development 121 (1995) 4067-4075
31. Namaka M.P., Sawchuk M., MacDonald S.C., Jordan L.M., and Hochman S. Neurogenesis in postnatal mouse dorsal root ganglia. Exp. Neurol. 172 (2001) 60-69
32. Oertel D., and Wu S.H. Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J. Comp. Neurol. 283 2 (1989) 228-247 (May 8)
33. 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
34. Olivius P., Alexandrov L., Miller J.M., Ulfendahl M., Bagger-Sjoback D., and Kozlova E.N. A model for implanting neuronal tissue into the cochlea. Brain Res. Protocols 12 (2004) 152-156
35. Otto D., Unsicker K., and Grothe C. Pharmacological effects of nerve growth factor and fibroblast growth factor applied to the transectioned sciatic nerve on neuron death in adult rat dorsal root ganglia. Neurosci. Lett. 83 (1987) 156-160
36. Pujol R., Lavigne-Rebillard M., and Lenoir M. Development of sensory and neural structures in the mammalian cochlea. In: Rubel W.E., Popper N., and Fay R.R. (Eds). Development of the Auditory System (1998), Springer-Verlag, New York 146-192
37. Ramer M.S., Priestley J.V., and McMahon S.B. Functional regeneration of sensory axons into the adult spinal cord. Nature 403 (2000) 312-316
38. 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
39. Rosario C.M., Aldskogius H., Carlstedt T., and Sidman R.L. Centrifugal growth in orthotopic grafts of allogeneic dorsal root ganglia in adult rats: evidence for possible central ingrowth?. Exp. Neurol. 115 (1992) 158-162
40. Rosario C.M., Aldskogius H., Carlstedt T., and Sidman R.L. Differentiation and axonal outgrowth pattern of fetal dorsal root ganglion cells orthotopically allografted into adult rats. Exp. Neurol. 120 (1993) 16-31
41. Rosario C.M., Dubovy P., Sidman R.L., and Aldskogius H. Peripheral target reinnervation following orthotopic grafting of fetal allogeneic and xenogeneic dorsal root ganglia. Exp. Neurol. 132 (1995) 251-261
42. Sekiya T., Kojima K., Matsumota M., Holley C.M., and Ito J. Rebuilding lost hearing using cell transplantation. Neurosurgery 60 (2007) 417-433
43. Snider W.D., and McMahon S.B. Tackling pain at the source: new ideas about nociceptors. Neuron 20 (1998) 629-632
44. Stoppini L., Buchs P.A., and Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37 (1991) 173-182
45. Thanos S., and Bonhoeffer F. Axonal arborization in the developing chick retinotectal system. J. Comp. Neurol. 261 (1987) 155-164
46. Thiebaud P., de Rooij N.F., Koudelka-Hep M., and Stoppini L. Microelectrode arrays for electrophysiological monitoring of hippocampal organotypic slice cultures. IEEE Trans. Biomed. Eng. 44 11 (1997) 1159-1163
47. Tierney T.S., Doubell P.T., Xia G., and Moore D.R. Development of brain-derived neutrophic factor and neurotrophin-3 immunoreactivity in the lower auditory brainstem of the postnatal gerbil. Eur. J. Neurosci. 14 (2001) 785-793
48. Waller H.J., and Godfrey D.A. Functional characteristics of spontaneously active neurons in rat dorsal cochlear nucleus in vitro. J. Neurophysiol. 71 (1994) 467-478
49. Waller H.J., Godfrey D.A., and Chen K. Effects of parallel fiber stimulation on neurons of rat dorsal cochlear nucleus. Hear Res. 98 (1996) 169-179
50. Wetts R., and Vaughn J.E. Peripheral and central target requirements for survival of embryonic rat dorsal root ganglion neurons in slice cultures. J. Neurosci. 18 (1998) 6905-6913
51. White F.A., Silos-Santiago I., Molliver D.C., Nishimura M., Phillips H., Barbacid M., and Snider W.D. Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J. Neurosci. 16 (1996) 4662-4672
52. 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
53. Yagi M., Kanzaki S., Kawamoto K., Shin B., Shah P.P., Magal E., Sheng J., and Raphael Y. Spiral ganglion neurons are protected from degeneration by GDNF gene therapy. J. Assoc. Res. Otolaryngol. 1 (2000) 315-325
54. Ylikoski J., Pirvola U., Virkkala J., Suvanto P., Liang X.Q., Magal E., Altschuler R., Miller J.M., and Saarma M. Guinea pig auditory neurons are protected by glial cell line-derived growth factor from degeneration after noise trauma. Hear Res. 124 (1998) 17-26
55. Zhang J.S., and Kaltenbach J.A. Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound. Neurosci. Lett. 250 (1998) 197-200
56. Zimmer J., and Gahwiler B.H. Cellular and connective organization of slice cultures of the rat hippocampus and fascia dentata. J. Comp. Neurol. 228 3 (1984) 432-446
57. Zimmer J., Kristensen B.W., Jakobsen B., and Noraberg J. Excitatory amino acid neurotoxicity and modulation of glutamate receptor expression in organotypic brain slice cultures. Amino Acids 19 (2000) 7-21