Neuronal survival, morphology and outgrowth of spiral ganglion neurons using a defined growth factor combination

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Schwieger, Jana ^a,b   Warnecke, Athanasia ^a,c   Lenarz, Thomas ^a,c   Esser, Karl Heinz ^b   Scheper, Verena ^a   Forsythe, John ^d  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^c GERMAN RESEARCH FOUNDATION   (Germany)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIPOLAR NEURON; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PROTEIN EXPRESSION; RAT; SPIRAL GANGLION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; METABOLISM; NEURITE;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; FEMALE; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NEURITES; NEURONS; RATS; SPIRAL GANGLION;

EID: 84942868291     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133680     Document Type: Article

References (60)

1. Battmer RD, Zilberman Y, Haake P, Lenarz T. Simultaneous Analog Stimulation (SAS) - Continuous Interleaved Sampler (CIS) pilot comparison study in Europe. Ann Otol Rhinol Laryngol Suppl 1999 Apr; 177: 69-73. PMID: 10214805
2. Lousteau RJ Increased spiral ganglion cell survival in electrically stimulated, deafened guinea pig cochleae. Laryngoscope 1987 Jul; 97(7 Pt 1): 836-842. PMID: 3600136
3. Hartshorn DO, Miller JM, Altschuler RA. Protective effect of electrical stimulation in the deafened guinea pig cochlea. Otolaryngol Head Neck Surg 1991 Mar; 104(3): 311-319. PMID: 1902931
4. Leake PA, Hradek GT, Rebscher SJ, Snyder RL. Chronic intracochlear electrical stimulation induces selective survival of spiral ganglion neurons in neonatally deafened cats. Hear Res 1991 Aug; 54 (2): 251-271. PMID: 1938628
5. Leake PA, Hradek GT, Snyder RL. Chronic electrical stimulation by a cochlear implant promotes survival of spiral ganglion neurons after neonatal deafness. J Comp Neurol 1999 Oct 4; 412(4): 543-562. PMID: 10464355
6. Mitchell A, Miller JM, Finger PA, Heller JW, Raphael Y, Altschuler RA. Effects of chronic high-rate electrical stimulation on the cochlea and eighth nerve in the deafened guinea pig. Hear Res 1997 Mar; 105 (1-2): 30-43. PMID: 9083802
7. Scheper V, Paasche G, Miller JM, Warnecke A, Berkingali N, Lenarz T, et al. Effects of delayed treatment with combined GDNF and continuous electrical stimulation on spiral ganglion cell survival in deafened guinea pigs. J Neurosci Res 2009 May 1; 87(6): 1389-1399. doi: 10.1002/jnr.21964 PMID: 19084902
8. Kranz K, Warnecke A, Lenarz T, Durisin M, Scheper V. Phosphodiesterase type 4 inhibitor rolipram improves survival of spiral ganglion neurons in vitro. PLoS One 2014 Mar 18; 9(3): e92157. doi: 10.1371/journal.pone.0092157 PMID: 24642701
9. Green SH, Bailey E, Wang Q, Davis RL. The Trk A, B, C's of neurotrophins in the cochlea. Anat Rec (Hoboken) 2012 Nov; 295(11): 1877-1895.
10. Brunet A, Datta SR, Greenberg ME. Transcription-dependent and-independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 2001 Jun; 11(3): 297-305. PMID: 11399427
11. Reichardt LF Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006 Sep 29; 361(1473): 1545-1564. PMID: 16939974
12. Lonze BE, Ginty DD. Function and regulation of CREB family transcription factors in the nervous system. Neuron 2002 Aug 15; 35(4): 605-623. PMID: 12194863
13. Staecker H, Liu W, Hartnick C, Lefebvre P, Malgrange B, Moonen G, et al. NT-3 combined with CNTF promotes survival of neurons in modiolus-spiral ganglion explants. Neuroreport 1995 Jul 31; 6 (11): 1533-1537. PMID: 7579142
14. Hartnick CJ, Staecker H, Malgrange B, Lefebvre PP, Liu W, Moonen G, et al. Neurotrophic effects of BDNF and CNTF, alone and in combination, on postnatal day 5 rat acoustic ganglion neurons. J Neurobiol 1996 Jun; 30(2): 246-254. PMID: 8738753
15. Marzella PL, Gillespie LN, Clark GM, Bartlett PF, Kilpatrick TJ. The neurotrophins act synergistically with LIF and members of the TGF-beta superfamily to promote the survival of spiral ganglia neurons in vitro. Hear Res 1999 Dec; 138(1-2): 73-80. PMID: 10575116
16. Vieira M, Christensen BL, Wheeler BC, Feng AS, Kollmar R. Survival and stimulation of neurite outgrowth in a serum-free culture of spiral ganglion neurons from adult mice. Hear Res 2007 Aug; 230(1-2): 17-23. PMID: 17521837
17. Lie M, Grover M, Whitlon DS. Accelerated neurite growth from spiral ganglion neurons exposed to the Rho kinase inhibitor H-1152. Neuroscience 2010 Aug 25; 169(2): 855-862. doi: 10.1016/j.neuroscience.2010.05.020 PMID: 20478368
18. Jin Y, Kondo K, Ushio M, Kaga K, Ryan AF, Yamasoba T. Developmental changes in the responsiveness of rat spiral ganglion neurons to neurotrophic factors in dissociated culture: differential responses for survival, neuritogenesis and neuronal morphology. Cell Tissue Res 2013 Jan; 351(1): 15-27. doi: 10.1007/s00441-012-1526-1 PMID: 23149719
19. Segal RA, Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 1996; 19: 463-489. PMID: 8833451
20. Bailey EM, Green SH. Postnatal expression of neurotrophic factors accessible to spiral ganglion neurons in the auditory system of adult hearing and deafened rats. J Neurosci 2014 Sep 24; 34(39): 13110-13126. doi: 10.1523/JNEUROSCI.1014-14.2014 PMID: 25253857
21. Malgrange B, Rogister B, Lefebvre PP, Mazy-Servais C, Welcher AA, Bonnet C, et al. Expression of growth factors and their receptors in the postnatal rat cochlea. Neurochem Res 1998 Aug; 23(8): 1133-1138. PMID: 9704604
22. Hafidi A, Decourt B, MacLennan AJ. CNTFRalpha and CNTF expressions in the auditory brainstem: light and electron microscopy study. Hear Res 2004 Aug; 194(1-2): 14-24. PMID: 15276672
23. Davis S, Aldrich TH, Valenzuela DM, Wong VV, Furth ME, Squinto SP, et al. The receptor for ciliary neurotrophic factor. Science 1991 Jul 5; 253(5015): 59-63. PMID: 1648265
24. Ip NY, Nye SH, Boulton TG, Davis S, Taga T, Li Y, et al. CNTF and LIFacton neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130. Cell 1992 Jun 26; 69(7): 1121-1132. PMID: 1617725
25. Davis S, Aldrich TH, Stahl N, Pan L, Taga T, Kishimoto T, et al. LIFR beta and gp 130 as heterodimerizing signal transducers of the tripartite CNTF receptor. Science 1993 Jun 18; 260(5115): 1805-1808. PMID: 8390097
26. Stahl N, Yancopoulos GD. The tripartite CNTF receptor complex: activation and signaling involves components shared with other cytokines. J Neurobiol 1994 Nov; 25(11): 1454-1466. PMID: 7852997
27. Ip NY, Yancopoulos GD. The neurotrophins and CNTF: two families of collaborative neurotrophic factors. Annu Rev Neurosci 1996; 19: 491-515. PMID: 8833452
28. Ip NY, Yancopoulos GD. Ciliary neurotrophic factor and its receptor complex. Prog Growth Factor Res 1992; 4(2): 139-155. PMID: 1338574
29. Sleeman MW, Anderson KD, Lambert PD, Yancopoulos GD, Wiegand SJ. The ciliary neurotrophic factor and its receptor, CNTFR alpha. Pharm Acta Helv 2000 Mar; 74(2-3): 265-272. PMID: 10812968
30. Turnley AM, Bartlett PF. Cytokines that signal through the leukemia inhibitory factor receptor-beta complex in the nervous system. J Neurochem 2000 Mar; 74(3): 889-899. PMID: 10693919
31. Stahl N, Boulton TG, Farruggella T, Ip NY, Davis S, Witthuhn BA, et al. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components. Science 1994 Jan 7; 263 (5143): 92-95. PMID: 8272873
32. Stahl N, Farruggella TJ, Boulton TG, Zhong Z, Darnell JE Jr, Yancopoulos GD. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 1995 Mar 3; 267(5202): 1349-1353. PMID: 7871433
33. Boulton TG, Stahl N, Yancopoulos GD. Ciliary neurotrophic factor/leukemia inhibitory factor/interleukin 6/oncostatin M family of cytokines induces tyrosine phosphorylation of a common set of proteins overlapping those induced by other cytokines and growth factors. J Biol Chem 1994 Apr 15; 269 (15): 11648-11655. PMID: 7512571
34. Hirano T, Nakajima K, Hibi M. Signaling mechanisms through gp130: a model of the cytokine system. Cytokine Growth Factor Rev 1997 Dec; 8(4): 241-252. PMID: 9620640
35. Dolcet X, Soler RM, Gould TW, Egea J, Oppenheim RW, Comella JX. Cytokines promote motoneuron survival through the Janus kinase-dependent activation of the phosphatidylinositol 3-kinase pathway. Mol Cell Neurosci 2001 Dec; 18(6): 619-631. PMID: 11749038
36. Nakaizumi T, Kawamoto K, Minoda R, Raphael Y. Adenovirus-mediated expression of brain-derived neurotrophic factor protects spiral ganglion neurons from ototoxic damage. Audiol Neurootol 2004 May-Jun; 9(3): 135-143. PMID: 15084818
37. Alonzi T, Middleton G, Wyatt S, Buchman V, Betz UA, Muller W, et al. Role of STAT3 and PI 3-kinase/Akt in mediating the survival actions of cytokines on sensory neurons. Mol Cell Neurosci 2001 Sep; 18 (3): 270-282. PMID: 11591128
38. Schweizer U, Gunnersen J, Karch C, Wiese S, Holtmann B, Takeda K, et al. Conditional gene ablation of Stat3 reveals differential signaling requirements for survival of motoneurons during development and after nerve injury in the adult. J Cell Biol 2002 Jan 21; 156(2): 287-297. PMID: 11807093
39. Ip NY, Yancopoulos GD. Neurotrophic factor receptors: just like other growth factor and cytokine receptors? Curr Opin Neurobiol 1994 Jun; 4(3): 400-405. PMID: 7919935
40. Leake PA, Hradek GT, Hetherington AM, Stakhovskaya O. Brain-derived neurotrophic factor promotes cochlear spiral ganglion cell survival and function in deafened, developing cats. J Comp Neurol 2011 Jun 1; 519(8): 1526-1545. doi: 10.1002/cne.22582 PMID: 21452221
41. Shibata SB, Cortez SR, Beyer LA, Wiler JA, Di Polo A, Pfingst BE, et al. Transgenic BDNF induces nerve fiber regrowth into the auditory epithelium in deaf cochleae. Exp Neurol 2010 Jun; 223(2): 464-472. doi: 10.1016/j.expneurol.2010.01.011 PMID: 20109446
42. Landry TG, Fallon JB, Wise AK, Shepherd RK. Chronic neurotrophin delivery promotes ectopic neurite growth from the spiral ganglion of deafened cochleae without compromising the spatial selectivity of cochlear implants. J Comp Neurol 2013 Aug 15; 521(12): 2818-2832. doi: 10.1002/cne.23318 PMID: 23436344
43. Staecker H, Van De Water TR, Lefebvre PP, Liu W, Moghadassi M, Galinovic-Schwartz V, et al. NGF, BDNF and NT-3 play unique roles in the in vitro development and patterning of innervation of the mammalian inner ear. Brain Res Dev Brain Res 1996 Mar 29; 92(1): 49-60. PMID: 8861722
44. Wise AK, Richardson R, Hardman J, Clark G, O'leary S. Resprouting and survival of guinea pig cochlear neurons in response to the administration of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3. J Comp Neurol 2005 Jun 27; 487(2): 147-165. PMID: 15880560
45. Wise AK, Hume CR, Flynn BO, Jeelall YS, Suhr CL, Sgro BE, et al. Effects of localized neurotrophin gene expression on spiral ganglion neuron resprouting in the deafened cochlea. Mol Ther 2010 Jun; 18 (6): 1111-1122. doi: 10.1038/mt.2010.28 PMID: 20216530
46. Glueckert R, Bitsche M, Miller JM, Zhu Y, Prieskorn DM, Altschuler RA, et al. Deafferentation-associated changes in afferent and efferent processes in the guinea pig cochlea and afferent regeneration with chronic intrascalar brain-derived neurotrophic factor and acidic fibroblast growth factor. J Comp Neurol 2008 Apr 1; 507(4): 1602-1621. doi: 10.1002/cne.21619 PMID: 18220258
47. Gillespie LN, Clark GM, Bartlett PF, Marzella PL. LIF is more potent than BDNFin promoting neurite outgrowth of mammalian auditory neurons in vitro. Neuroreport 2001 Feb 12; 12(2): 275-279. PMID: 11209934
48. Wefstaedt P, Scheper V, Lenarz T, Stover T. Brain-derived neurotrophicfactor/glial cell line-derived neurotrophic factor survival effects on auditory neurons are not limited by dexamethasone. Neuroreport 2005 Dec 19; 16(18): 2011-2014. PMID: 16317344
49. Ogilvie JM, Speck JD, Lett JM. Growth factors in combination, but not individually, rescue rd mouse photoreceptors in organ culture. Exp Neurol 2000 Feb; 161(2): 676-685. PMID: 10686086
50. Whitlon DS, Grover M, Tristano J, Williams T, Coulson MT. Culture conditions determine the prevalence of bipolar and monopolar neurons in cultures of dissociated spiral ganglion. Neuroscience 2007 May 11; 146(2): 833-840. PMID: 17331652
51. Whitlon DS, Ketels KV, Coulson MT, Williams T, Grover M, Edpao W, et al. Survival and morphology of auditory neurons in dissociated cultures of newborn mouse spiral ganglion. Neuroscience 2006; 138 (2): 653-662. PMID: 16413120
52. Berkingali N, Warnecke A, Gomes P, Paasche G, Tack J, Lenarz T, et al. Neurite outgrowth on cultured spiral ganglion neurons induced by erythropoietin. Hear Res 2008 Sep; 243(1-2): 121-126. doi: 10.1016/j.heares.2008.07.003 PMID: 18672044
53. Kaiser O, Paasche G, Stover T, Ernst S, Lenarz T, Kral A, et al. TGF-betasuperfamily member activin A acts with BDNF and erythropoietin to improve survival of spiral ganglion neurons in vitro. Neuropharmacology 2013 Dec; 75: 416-425. doi: 10.1016/j.neuropharm.2013.08.008 PMID: 23973291
54. Warnecke A, Wissel K, Hoffmann A, Hofmann N, Berkingali N, Gro G, et al. The biological effects of cell-delivered brain-derived neurotrophic factor on cultured spiral ganglion cells. Neuroreport 2007 Oct 29; 18(16): 1683-1686. PMID: 17921868
55. Nayagam BA, Muniak MA, Ryugo DK. The spiral ganglion: connecting the peripheral and central auditory systems. Hear Res 2011 Aug; 278(1-2): 2-20. doi: 10.1016/j.heares.2011.04.003 PMID: 21530629
56. Brand Y, Sung M, Chavez E, Wei E, Pak KK, Housley GD, et al. Neural cell adhesion molecule L1 modulates type I but not type II inner ear spiral ganglion neurite outgrowth in an in vitro alternate choice assay. J Mol Neurosci 2013 Nov; 51(3): 663-670. doi: 10.1007/s12031-013-0040-6 PMID: 23760987
57. Liu W, Edin F, Atturo F, Rieger G, Lowenheim H, Senn P, et al. The pre-and post-somatic segments of the human type I spiral ganglion neurons - structural and functional considerations related to cochlear implantation. Neuroscience 2015 Jan 22; 284: 470-482. doi: 10.1016/j.neuroscience.2014.09.059 PMID: 25316409
58. Shinohara T, Bredberg G, Ulfendahl M, Pyykko I, Olivius NP, Kaksonen R, et al. Neurotrophic factor intervention restores auditory function in deafened animals. Proc Natl Acad Sci U S A 2002 Feb 5; 99 (3): 1657-1660. PMID: 11818566
59. Yamagata T, Miller JM, Ulfendahl M, Olivius NP, Altschuler RA, Pyykko I, et al. Delayed neurotrophic treatment preserves nerve survival and electrophysiological responsiveness in neomycin-deafened guinea pigs. J Neurosci Res 2004 Oct 1; 78(1): 75-86. PMID: 15372491
60. Shepherd RK, Hatsushika S, Clark GM. Electrical stimulation of the auditory nerve: the effect of electrode position on neural excitation. Hear Res 1993 Mar; 66(1): 108-120. PMID: 8473242