Influence of central glia on spiral ganglion neuron neurite growth

Neuroscience

Volumn 177, Issue , 2011, Pages 321-334

  Jeon, E J ^a,b   Xu, N ^a   Xu, L ^a   Hansen, M R ^a  

^a UNIVERSITY OF IOWA   (United States)

^b Bupyeong gu   (South Korea)

Author keywords

Astrocyte; Axons; Cyclic AMP; Oligodendrocytes; Protein kinase A; Schwann cell

Indexed keywords

8 (4 CHLOROPHENYLTHIO) CYCLIC AMP; FORSKOLIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COUNT; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CELL POPULATION; CONTROLLED STUDY; CULTURE MEDIUM; EXPLANT; GLIA CELL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PERIKARYON; PRIORITY JOURNAL; RAT; SCHWANN CELL; SPIRAL GANGLION;

ANIMALS; ANIMALS, NEWBORN; CELL COMMUNICATION; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; NEURITES; NEUROGLIA; NEURONS; RATS; SPIRAL GANGLION;

EID: 79952003941     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.01.014     Document Type: Article

References (77)

1. Akil O., Sun Y., Grabowski G., Lustig L.R. Cochlea spiral ganglion cells degeneration and hearing loss as a consequence of Schwann cells death in the Saposin B KO mice. Assoc Res Otolaryngol Abstract 2010, 891.
2. Alam S.A., Robinson B.K., Huang J., Green S.H. Prosurvival and proapoptotic intracellular signaling in rat spiral ganglion neurons in vivo after the loss of hair cells. J Comp Neurol 2007, 503:832-852.
3. Altschuler R.A., Cho Y., Ylikoski J., Pirvola U., Magal E., Miller J.M. Rescue and regrowth of sensory nerves following deafferentation by neurotrophic factors. Ann N Y Acad Sci 1999, 884:305-311.
4. Arnold W. Myelination of the human spiral ganglion. Acta Otolaryngol Suppl 1987, 436:76-84.
5. Benson M.D., Romero M.I., Lush M.E., Lu Q.R., Henkemeyer M., Parada L.F. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci U S A 2005, 102:10694-10699.
6. Boer J.C., Carney K.E., van der Zee S. Differentiation of mouse embryonic stem cells into spiral ganglion neurons: a therapeutic approach to deafness. J Neurosci 2009, 29:5711-5712.
7. Bok J., Zha X.M., Cho Y.S., Green S.H. An extranuclear locus of cAMP-dependent protein kinase action is necessary and sufficient for promotion of spiral ganglion neuronal survival by cAMP. J Neurosci 2003, 23:777-787.
8. Bomze H.M., Bulsara K.R., Iskandar B.J., Caroni P., Skene J.H. Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat Neurosci 2001, 4:38-43.
9. Bostrom M., Khalifa S., Bostrom H., Liu W., Friberg U., Rask-Andersen H. Effects of neurotrophic factors on growth and glial cell alignment of cultured adult spiral ganglion cells. Audiol Neuro Otol 2009, 15:175-186.
10. Busch S.A., Silver J. The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 2007, 17:120-127.
11. Cai D., Deng K., Mellado W., Lee J., Ratan R.R., Filbin M.T. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 2002, 35:711-719.
12. Cai D., Qiu J., Cao Z., McAtee M., Bregman B.S., Filbin M.T. Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J Neurosci 2001, 21:4731-4739.
13. Carlstedt T., Cullheim S., Risling M., Ulfhake B. Nerve fibre regeneration across the PNS-CNS interface at the root-spinal cord junction. Brain Res Bull 1989, 22:93-102.
14. Carulli D., Laabs T., Geller H.M., Fawcett J.W. Chondroitin sulfate proteoglycans in neural development and regeneration. Curr Opin Neurobiol 2005, 15:116-120.
15. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403:434-439.
16. Danneman P.J., Mandrell T.D. Evaluation of five agents/methods for anesthesia of neonatal rats. Lab Anim Sci 1997, 47:386-395.
17. Ernsberger U. The role of GDNF family ligand signalling in the differentiation of sympathetic and dorsal root ganglion neurons. Cell Tissue Res 2008, 333:353-371.
18. Filbin M.T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 2003, 4:703-713.
19. Fournier A.E., Gould G.C., Liu B.P., Strittmatter S.M. Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J Neurosci 2002, 22:8876-8883.
20. Fournier A.E., Takizawa B.T., Strittmatter S.M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 2003, 23:1416-1423.
21. Friedman B., Hockfield S., Black J.A., Woodruff K.A., Waxman S.G. In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, rip. Glia 1989, 2:380-390.
22. Gao Y., Deng K., Hou J., Bryson J.B., Barco A., Nikulina E., Spencer T., Mellado W., Kandel E.R., Filbin M.T. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 2004, 44:609-621.
23. Gillespie L.N., Shepherd R.K. Clinical application of neurotrophic factors: the potential for primary auditory neuron protection. Eur J Neurosci 2005, 22:2123-2133.
24. Gomaa N.A., Rubinstein J.T., Lowder M.W., Tyler R.S., Gantz B.J. Residual speech perception and cochlear implant performance in postlingually deafened adults. Ear Hear 2003, 24:539-544.
25. GrandPre T., Li S., Strittmatter S.M. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 2002, 417:547-551.
26. Grimpe B., Pressman Y., Lupa M.D., Horn K.P., Bunge M.B., Silver J. The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Mol Cell Neurosci 2005, 28:18-29.
27. Hannila S.S., Filbin M.T. The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 2008, 209:321-332.
28. Hansen M.R., Vijapurkar U., Koland J.G., Green S.H. Reciprocal signaling between spiral ganglion neurons and Schwann cells involves neuregulin and neurotrophins. Hear Res 2001, 161:87-98.
29. Hansen M.R., Zha X.M., Bok J., 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 2001, 21:2256-2267.
30. Hegarty J.L., Kay A.R., Green S.H. Trophic support of cultured spiral ganglion neurons by depolarization exceeds and is additive with that by neurotrophins or cyclic AMP, and requires elevation of [Ca2+]i within a set range. J Neurosci 1997, 17:1959-1970.
31. Henley J.R., Huang K.H., Wang D., Poo M.M. Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron 2004, 44:909-916.
32. Hurley P.A., Clarke M., Crook J.M., Wise A.K., Shepherd R.K. Cochlear immunochemistry-a new technique based on gelatin embedding. J Neurosci Methods 2003, 129:81-86.
33. Hurley P.A., Crook J.M., Shepherd R.K. Schwann cells revert to non-myelinating phenotypes in the deafened rat cochlea. Eur J Neurosci 2007, 26:1813-1821.
34. Jalenques I., Albuisson E., Despres G., Romand R. Distribution of glial fibrillary acidic protein (GFAP) in the cochlear nucleus of adult and aged rats. Brain Res 1995, 686:223-232.
35. Jiao J., Huang X., Feit-Leithman R.A., Neve R.L., Snider W., Dartt D.A., Chen D.F. Bcl-2 enhances Ca(2+) signaling to support the intrinsic regenerative capacity of CNS axons. EMBO J 2005, 24:1068-1078.
36. Khan A.M., Handzel O., Burgess B.J., Damian D., Eddington D.K., Nadol J.B. Is word recognition correlated with the number of surviving spiral ganglion cells and electrode insertion depth in human subjects with cochlear implants?. Laryngoscope 2005, 115:672-677.
37. Kretz A., Kugler S., Happold C., Bahr M., Isenmann S. Excess Bcl-XL increases the intrinsic growth potential of adult CNS neurons in vitro. Mol Cell Neurosci 2004, 26:63-74.
38. Lehmann M., Fournier A., Selles-Navarro I., Dergham P., Sebok A., Leclerc N., Tigyi G., McKerracher L. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J Neurosci 1999, 19:7537-7547.
39. Lie M., Grover M., Whitlon D.S. Accelerated neurite growth from spiral ganglion neurons exposed to the Rho kinase inhibitor H-1152. Neuroscience 2010, 169:855-862.
40. Linthicum F.H., Fayad J.N. Spiral ganglion cell loss is unrelated to segmental cochlear sensory system degeneration in humans. Otol Neurotol 2009, 30:418-422.
41. Liu B.P., Cafferty W.B., Budel S.O., Strittmatter S.M. Extracellular regulators of axonal growth in the adult central nervous system. Philos Trans R Soc Lond B Biol Sci 2006, 361:1593-1610.
42. Liu B.P., Fournier A., Grandpre T., Strittmatter S.M. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002, 297:1190-1193.
43. Low K., Culbertson M., Bradke F., Tessier-Lavigne M., Tuszynski M.H. Netrin-1 is a novel myelin-associated inhibitor to axon growth. J Neurosci 2008, 28:1099-1108.
44. McCarthy K.D., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980, 85:890-902.
45. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 1994, 13:805-811.
46. Moore J.K., Linthicum F.H. Myelination of the human auditory nerve: different time courses for Schwann cell and glial myelin. Ann Otol Rhinol Laryngol 2001, 110:655-661.
47. Moreau-Fauvarque C., Kumanogoh A., Camand E., Jaillard C., Barbin G., Boquet I., Love C., Jones E.Y., Kikutani H., Lubetzki C., Dusart I., Chedotal A. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J Neurosci 2003, 23:9229-9239.
48. Morris J.K., Maklad A., Hansen L.A., Feng F., Sorensen C., Lee K.F., Macklin W.B., Fritzsch B. A disorganized innervation of the inner ear persists in the absence of ErbB2. Brain Res 2006, 1091:186-199.
49. Nadol J.B., Burgess B.J., Reisser C. Morphometric analysis of normal human spiral ganglion cells. Ann Otol Rhinol Laryngol 1990, 99:340-348.
50. Nash M., Pribiag H., Fournier A.E., Jacobson C. Central nervous system regeneration inhibitors and their intracellular substrates. Mol Neurobiol 2009, 40:224-235.
51. Niederost B., Oertle T., Fritsche J., McKinney R.A., Bandtlow C.E. Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J Neurosci 2002, 22:10368-10376.
52. Nishimura K., Nakagawa T., Ono K., Ogita H., Sakamoto T., Yamamoto N., Okita K., Yamanaka S., Ito J. Transplantation of mouse induced pluripotent stem cells into the cochlea. Neuroreport 2009, 20:1250-1254.
53. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
54. Pettingill L.N., Richardson R.T., Wise A.K., O'Leary S.J., Shepherd R.K. Neurotrophic factors and neural prostheses: potential clinical applications based upon findings in the auditory system. IEEE Trans Biomed Eng 2007, 54:1138-1148.
55. Phifer C.B., Terry L.M. Use of hypothermia for general anesthesia in preweanling rodents. Physiol Behav 1986, 38:887-890.
56. Qiu J., Cai D., Dai H., McAtee M., Hoffman P.N., Bregman B.S., Filbin M.T. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 2002, 34:895-903.
57. Reyes J.H., O'Shea K.S., Wys N.L., Velkey J.M., Prieskorn D.M., Wesolowski K., Miller J.M., Altschuler R.A. Glutamatergic neuronal differentiation of mouse embryonic stem cells after transient expression of neurogenin 1 and treatment with BDNF and GDNF: in vitro and in vivo studies. J Neurosci 2008, 28:12622-12631.
58. Rind H.B., von Bartheld C.S. Anterograde axonal transport of internalized GDNF in sensory and motor neurons. Neuroreport 2002, 13:659-664.
59. Roehm P.C., Hansen M.R. Strategies to preserve or regenerate spiral ganglion neurons. Curr Opin Otolaryngol Head Neck Surg 2005, 13:294-300.
60. Roehm P.C., Xu N., Woodson E.A., Green S.H., Hansen M.R. Membrane depolarization inhibits spiral ganglion neurite growth via activation of multiple types of voltage sensitive calcium channels and calpain. Mol Cell Neurosci 2008, 37:376-387.
61. Rubinstein J.T. How cochlear implants encode speech. Curr Opin Otolaryngol Head Neck Surg 2004, 12:444-448.
62. Schnell L., Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 1990, 343:269-272.
63. Song H., Ming G., He Z., Lehmann M., McKerracher L., Tessier-Lavigne M., Poo M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 1998, 281:1515-1518.
64. Spoendlin H. Retrograde degeneration of the cochlear nerve. Acta Otolaryngol 1975, 79:266-275.
65. Spoendlin H. Anatomy of cochlear innervation. Am J Otolaryngol 1985, 6:453-467.
66. Spoendlin H., Suter R. Regeneration in the VIII nerve. Acta Otolaryngol 1976, 81:228-236.
67. Sugawara M., Corfas G., Liberman M.C. Influence of supporting cells on neuronal degeneration after hair cell loss. J Assoc Res Otolaryngol 2005, 6:136-147.
68. Toesca A. Central and peripheral myelin in the rat cochlear and vestibular nerves. Neurosci Lett 1996, 221:21-24.
69. Valderrama-Canales F.J., Gil-Loyzaga P., Merchan-Perez A., Sanchez J.G. Astrocyte cytoarchitecture in cochlear nuclei of the rat: an immunocytochemical study. ORL J Otorhinolaryngol Relat Spec 1993, 55:313-316.
70. Wang K.C., Kim J.A., Sivasankaran R., Segal R., He Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002, 420:74-78.
71. Wang K.C., Koprivica V., Kim J.A., Sivasankaran R., Guo Y., Neve R.L., He Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417:941-944.
72. Watanabe M., Sakurai Y., Ichinose T., Aikawa Y., Kotani M., Itoh K. Monoclonal antibody Rip specifically recognizes 2',3'-cyclic nucleotide 3'-phosphodiesterase in oligodendrocytes. J Neurosci Res 2006, 84:525-533.
73. Whitlon D.S., Tieu D., Grover M., Reilly B., Coulson M.T. Spontaneous association of glial cells with regrowing neurites in mixed cultures of dissociated spiral ganglia. Neuroscience 2009, 161:227-235.
74. Xu L., Pfingst B.E. Spectral and temporal cues for speech recognition: implications for auditory prostheses. Hear Res 2008, 242:132-140.
75. Yiu G., He Z. Signaling mechanisms of the myelin inhibitors of axon regeneration. Curr Opin Neurobiol 2003, 13:545-551.
76. Yiu G., He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 2006, 7:617-627.
77. Ylikoski J., Pirvola U., Virkkala J., Suvanto P., Liang X.Q., Magal E., Altschuler R., Miller J.M., Saarma M. Guinea pig auditory neurons are protected by glial cell line-derived growth factor from degeneration after noise trauma. Hear Res 1998, 124:17-26.