EphA7 regulates spiral ganglion innervation of cochlear hair cells

Developmental Neurobiology

Volumn 76, Issue 4, 2016, Pages 452-469

  Kim, Young J ^a,b   Ibrahim, Leena A ^a,b   Wang, Sheng Zhi ^a   Yuan, Wei ^c   Evgrafov, Oleg V ^a   Knowles, James A ^a   Wang, Kai ^a   Tao, Huizhong W ^a   Zhang, Li I ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Axon guidance molecule; Cochlear development; Hair cell; Peripheral auditory system; Spiral ganglion

Indexed keywords

EPHRIN RECEPTOR A7; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; EPHA7 RECEPTOR, MOUSE; PRKG1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN STEM RESPONSE; COCHLEA; COCHLEAR NERVE; COMPARATIVE STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HAIR CELL; HEARING; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; INNER HAIR CELL; INNERVATION; MOUSE; NEURITE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA SEQUENCE; SIGNAL TRANSDUCTION; SPIRAL GANGLION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; CYTOLOGY; EVOKED BRAIN STEM AUDITORY RESPONSE; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; NEWBORN; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION; TISSUE CULTURE TECHNIQUE;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; COCHLEA; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE I; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MAP KINASE SIGNALING SYSTEM; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; NEURITES; NEURONS; RECEPTOR, EPHA7; SPIRAL GANGLION; SYNAPSES; SYNAPTIC TRANSMISSION; TISSUE CULTURE TECHNIQUES;

EID: 84959462895     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22326     Document Type: Article

References (67)

1. Arvanitis D, Davy A. 2008. Eph/ephrin signaling: networks. Genes Dev 22:416-429.
2. Benson MD, Romero MI, Lush ME, Lu QR, Henkemeyer M, Parada LF. 2005. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci USA 102:10694-10699.
3. Bianchi LM, Gale NM. 1998. Distribution of Eph-related molecules in the developing and mature cochlea. Hear Res 117:161-172.
4. Bianchi LM, Gray NA. 2002. EphB receptors influence growth of ephrin-B1-positive statoacoustic nerve fibers. Eur J Neurosci 16:1499-1506.
5. Bianchi LM, Liu H. 1999. Comparison of ephrin-A ligand and EphA receptor distribution in the developing inner ear. Anat Rec 254:127-134.
6. Browning JL, Patel T, Brandt PC, Young KA, Holcomb LA, Hicks PB. 2005. Clozapine and the mitogen-activated protein kinase signal transduction pathway: implications for antipsychotic actions. Biol Psychiatry 15:617-623.
7. Brownlee H, Gao PP, Frisen J, Dreyfus C, Zhou R, Black IB. 2000. Multiple ephrins regulate hippocampal neurite outgrowth. J Comp Neurol 425:315-322.
8. Chai G, Zhou L, Manto M, Helmbacher F, Clotman F, Goffinet AM, Tissir F. 2014. Celsr3 is required in motor neurons to steer their axons in the hindlimb. Nat Neurosci 19:1171-1179.
9. Clifford MA, Athar W, Leonard CE, Russo A, Sampognaro PJ, Van der Goes MS, Burton DA, et al. 2014. EphA7 signaling guides cortical dendritic development and spine maturation. Proc Natl Acad Sci USA 111:4994-4999.
10. Coate TM, Raft S, Zhao X, Ryan AK, Crenshaw EB III, Kelley MW. 2012. Otic mesenchyme cells regulate spiral ganglion axon fasciculation through a Pou3f4/EphA4 signaling pathway. Neuron 73:49-63.
11. Colamarino SA, Tessier-Lavigne M. 1995. The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81:621-629.
12. Cowan CA, Yokoyama N, Bianchi LM, Henkemeyer M, Fritzsch B. 2000. EphB2 guides axons at the midline and is necessary for normal vestibular function. Neuron 26:417-430.
13. Cramer KS, Gabriele ML. 2014. Axon guidance in the audtiory system: Multiple functions of eph receptors. Neuroscience 26:152-162.
14. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, Goldfarb M, Yancopoulos GD. 1994. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816-819.
15. Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, Feuerstein C, Robbins SM. 1999. Compartmentalized signalling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev 13:3125-3135.
16. Defourny J, Poirrier AL, Lallemend F, Mateo Sanchez S, Neef J, Vanderhaeghen P, Soriano E, et al. 2013. Ephrin-A5/EphA4 signalling controls specific afferent targeting to cochlear hair cells. Nat Commun 4:1438.
17. Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, Ledent C, et al. 2005. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435:1244-1250.
18. Dottori M, Hartley L, Galea M, Paxinos G, Polizzotto M, Kilpatrick T, Bartlett PF, et al. 1998. EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc Natl Acad Sci USA 95:13248-13253.
19. Drescher U, Kremoser C, Handwerker C, Löschinger J, Noda M, Bonhoeffer F. 1995. In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
20. Feldheim DA, Kim YI, Bergemann AD, Frisen J, Barbacid M, Flanagan JG. 2000. Genetic analysis of ephrin-A2 and ephrin-A5 show their requirement in multiple aspects of retinocollicular mapping. Neuron 25:563-574.
21. Forcet C, Stein E, Pays L, Corset V, Llambi F, Tessier-Lavigne M, Mehlen P. 2002. Netrin-1-mediated axon outgrowth requires deleted in colorectal cancer-dependent MAPK activation. Nature 417:443-447.
22. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, et al. 1996. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19.
23. Gambelli F, Di P, Niu X, Friedman M, Hammond T, Riches DW, Ortiz LA. 2004. Phosphorylation of tumor necrosis factor receptor 1 (p55) protects macrophages from silica-induced apoptosis. J Biol Chem 279:2020-2029.
24. Gao PP, Sun CH, Zhou XF, DiCicco-Bloom E, Zhou R. 2000. Ephrins stimulate or inhibit neurite outgrowth and survival as a function of neuronal cell type. J Neurosci Res 60:427-436.
25. Hansen MJ, Dallal GE, Flanagen JG. 2004. Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 42:717-730.
26. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S. 2005. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3:e159.
27. Holmberg J, Armulik A, Senti KA, Edoff K, Spalding K, Momma S, Cassidy R, et al. 2005. Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes Dev 19:462-471.
28. Huang LC, Thorne PR, Housley GD, Montgomery JM. 2007. Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development 134:2925-2933.
29. Jaumann M, Dettling J, Gubelt M, Zimmermann U, Gerling A, Paquet-Durand F, Feil S, et al. 2012. cGMP-Prkg1 signaling and Pde5 inhibition shelter cochlear hair cells and hearing function. Nat Med 18:252-259.
30. Klein R. 2004. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr Opin Cell Biol 16:580-589.
31. Komalavilas P, Shah PK, Jo H, Lincoln TM. 1999. Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem 274:34301-34309.
32. Koundakjian EJ, Appler JL, Goodrich LV. 2007. Auditory neurons make stereotyped wiring decisions before maturation of their targets. J Neurosci 27:14078-14088.
33. Kullander K, Mather NK, Diella F, Dottori M, Boyd AW, Klein R. 2001. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 29:73-84.
34. Lee KH, Warchol ME. 2005. Ephrin A2 may play a role in axon guidance during hair cell regeneration. Laryngoscope 115:1021-1025.
35. Lewcock JW, Genoud N, Lettieri K, Pfaff SL. 2007. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56:604-620.
36. Lim BK, Matsuda N, Poo MM. 2008. Ephrin-B reverse signalling promotes structural and functional synaptic maturation in vivo. Nat Neurosci 11:160-169.
37. Lu CC, Appler JM, Houseman EA, Goodrich LV. 2011. Developmental profiling of spiral ganglion neurons reveals insights into auditory circuit assembly. J Neurosci 31:10903-10918.
38. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, et al. 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133-140.
39. Mao Y, Reiprichm S, Wegnerm M, Fritzsch B. 2014. Targeted deletion of Sox10 by Wnt1-cre defects neuronal migration and projection in the mouse inner ear. PLoS One 9:e94580.
40. Marquardt T, Shirasaki R, Ghosh S, Andrews SE, Carter N, Hunter T, Pfaff SL. 2005. Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigation from distinct membrane domains. Cell 121:127-139.
41. Meier C, Anastasiadou S, Knöll B. 2011. Ephrin-A5 suppresses neurotrophin evoked neuronal motility, ERK activation and gene expression. PLoS One 6:e26089.
42. Melcher JR, Kiang NY. 1996. Generators of the brainstem auditory evoked potential in cat. III. Identified cell populations. Hear Res 93:52-71.
43. Nakanishi H, Nakamura T, Canaani E, Croce CM. 2007. ALL1 fusion proteins induce deregulation of EphA7 and ERK phosphorylation in human acute leukemias. Proc Natl Acad Sci USA 104:14442-14447.
44. Niu H, Makmura L, Shen T, Sheth SS, Blair K, Friedman RA. 2006. Identification of two major loci that suppress hearing loss and cochlear dysmorphogenesis in Eya1bor/bor mice. Genomics 88:302-308.
45. Ohori M, Kinoshita T, Okubo M, Sato K, Yamazaki A, Arakawa H, Nishimura S, et al. 2005. Identification of a selective ERK inhibitor and structural determination of the inhibitor-ERK2 complex. Biochem Biophys Res Commun 336:357-363.
46. Oricchio E, Nanjangud G, Wolfe AL, Schatz JH, Mavrakis KJ, Jiang M, Liu X, et al. 2011. The Eph-receptor A7 is a soluble tumor suppressor for follicular lymphoma. Cell 147:554-564.
47. Orioli D, Henkemeyer M, Lemke G, Klein R, Pawson T. 1996. Sek4 and Nuk receptors cooperate in guidance of commuissural axons and in palate formation. Embo J 15:6035-6049.
48. Pasquale EB. 2005. Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6:462-475.
49. Passante L, Gaspard N, Degraeve M, Frisen J, Kullander K, De Maertelaer V, Vanderhaeghen P. 2008. Temporal regulation of ephrin/Eph signalling is required for the spatial patterning of the mammalian striatum. Development 135:3281-3290.
50. Perkins RE, Morest DK. 1975. A study of cochlear innervations patterns in cats and rats with the Golgi method and Nomarkski optics. J Comp Neurol 163:129-158.
51. Pickles JO. 2003. Expression of Ephs and ephrins in developing mouse inner ear. Hear Res 178:44-51.
52. Pickles JO, Claxton C, Van Heumen WR. 2002. Complementary and layered expression of Ephs and ephrins in developing mouse inner ear. J Comp Neurol 449:207-216.
53. Rashid T, Upton AL, Blentic A, Ciossek T, Knöll B, Thompson ID, Drescher U. 2005. Opposing gradients of ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system. Neuron 47:57-69.
54. Saeger BM, Suhm M, Neubuser A. 2011. Ephrin/ephrin receptor expression during early stages of mouse inner ear development. Dev Dyn 240:1578-1585.
55. Schaette R, McAlpine D. 2011. Tinnitus with a normal audiogram: Physiological evidence for hidden hearing loss and computational model. J Neurosci 31:13452-13457.
56. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M. 1994. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-424.
57. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. 2003. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
58. Torii M, Levitt P. 2005. Dissociation of corticothalamic and thalamocortical axon targeting by an EphA7-mediated mechanism. Neuron 48:563-575.
59. Veeranna AND, Ahn NG, Jaffe H, Winters CA, Grant P, Pant HC. 1998. Mitogen-activated protein kinases (Erk1, 2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J Neurosci 18:4008-4021.
60. Wang HU, Anderson DJ. 1997. Eph family transmembrane ligands can mediae repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18:383-396.
61. Wang SZ, Ibrahim LA, Kim YJ, Gibson DA, Leung HC, Yuan W, Zhang KK, et al. 2013. Slit/Robo signaling mediates spatial positioning of spiral ganglion neurons during development of cochlear innervations. J Neurosci 33:12242-12254.
62. Wang YF, Hatton GI. 2007. Interaction of extracellular signal-regulated protein kinase 1/2 with actin cytoskeleton in supraoptic oxytocin neurons and astrocytes: Role in burst firing. J Neurosci 27:13822-13834.
63. Wegener JW, Nawrath H, Wolfsgruber W, Kühbandner S, Werner C, Hofmann F, Feil R. 2002. cGMP-dependent protein kinase I mediates the negative inotropic effect of cGMP in the murine myocardium. Circ Res 90:18-20.
64. Weiss AC, Airik R, Bohnenpoll T, Greulich F, Foik A, Trowe MO, Rudat C, et al. 2014. Nephric duct insertion requires EphA4/EphA7 signaling from pericloacal mesenchyme. Development 141:3420-3430.
65. Young ED, Barta PE. 1986. Rate responses of auditory nerve fibers to tones in noise near masked threshold. J Acoust Soc Am 79:426-442.
66. Zhou CQ, Lee J, Henkemeyer MJ, Lee KH. 2011. Disruption of ephrin B/Eph B interaction results in abnormal cochlear innervation patterns. Laryngoscope 121:1541-1547.
67. Zhou X, Suh J, Cerretti DP, Zhou R, DiCicco-Bloom E. 2001. Ephrins stimulate neurite outgrowth during early cortical neurogenesis. J Neurosci Res 66:1054-1063.