Changes in Sef levels influence auditory brainstem development and function

Journal of Neuroscience

Volumn 27, Issue 16, 2007, Pages 4273-4282

  Abraira, Victoria E ^a   Hyun, Naomi ^a   Tucker, Andrew F ^a   Coling, Donald E ^b   Brown, M Christian ^c   Lu, Cindy ^a   Hoffman, Gregory R ^a   Goodrich, Lisa V ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

Auditory brainstem response; Central auditory processing defect; Cochlear nucleus; FGF; Rhombic lip; Sef

Indexed keywords

FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR RECEPTOR 1; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDES AND PROTEINS; PROTEIN SEF; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; BRAIN DEVELOPMENT; BRAIN FUNCTION; CHICK; COCHLEAR NUCLEUS; CONTROLLED STUDY; EVOKED BRAIN STEM AUDITORY RESPONSE; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STIMULUS RESPONSE;

ANIMALS; BRAIN STEM; CHICK EMBRYO; COCHLEAR NUCLEUS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FIBROBLAST GROWTH FACTORS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICE; MICE, NEUROLOGIC MUTANTS; MORPHOGENESIS;

EID: 34247403457     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3477-06.2007     Document Type: Article

References (61)

1. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R, Gross I, Martin GR, Lufkin T, McMahon AP, Wilson PD, Costantini FD, Mason IJ, Licht JD (2005) Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev Cell 8:229-239.
2. Cramer KS, Fraser SE, Rubel EW (2000) Embryonic origins of auditory brainstem nuclei in the chick hindbrain. Dev Biol 224:138-151.
3. Cramer KS, Bermingham-McDonogh O, Krull CE, Rubel EW (2004) EphA4 signaling promotes axon segregation in the developing auditory system. Dev Biol 269:26-35.
4. Cramer KS, Cerretti DP, Siddiqui SA (2006) EphB2 regulates axonal growth at the midline in the developing auditory brainstem. Dev Biol 295:76-89.
5. Darby S, Sahadevan K, Khan MM, Robson CN, Leung HY, Gnanapragasam VJ (2006) Loss of Sef (similar expression to FGF) expression is associated with high grade and metastatic prostate cancer. Oncogene 25:4122-4127.
6. Dono R (2003) Fibroblast growth factors as regulators of central nervous system development and function. Am J Physiol Regul Integr Comp Physiol 284:R867-R881.
7. Farago AF, Awatramani RB, Dymecki SM (2006) Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50:205-218.
8. Foucher I, Mione M, Simeone A, Acampora D, Bally-Cuif L, Houart C (2006) Differentiation of cerebellar cell identities in absence of Fgf signalling in zebrafish Otx morphants. Development 133:1891-1900.
9. Furthauer M, Lin W, Ang SL, Thisse B, Thisse C (2002) Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat Cell Biol 4:170-174.
10. Gopal KV, Kowalski J (1999) Slope analysis of Auditory Brainstem Responses in children at risk of central auditory processing disorders. Scand Audiol 28:85-90.
11. Gray PA, Fu H, Luo P, Zhao Q, Yu J, Ferrari A, Tenzen T, Yuk DI, Tsung EF, Cai Z, Alberta JA, Cheng LP, Liu Y, Stenman JM, Valerius MT, Billings N, Kim HA, Greenberg ME, McMahon AP, Rowitch DH, et al. (2004) Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306:2255-2257.
12. Harduf H, Halperin E, Reshef R, Ron D (2005) Sef is synexpressed with FGFs during chick embryogenesis and its expression is differentially regulated by FGFs in the developing limb. Dev Dyn 233:301-312.
13. Harkmark W (1954) Cell migrations from the rhombic lip to the inferior olive, the nucleus raphe and the pons. A morphological and experimental investigation of chick embryos. J Comp Neurol 100:115-209.
14. Hossain WA, D'Sa C, Morest DK (2006) Site-specific interactions of neurotrophin-3 and fibroblast growth factor (FGF2) in the embryonic development of the mouse cochlear nucleus. J Neurobiol 66:897-915.
15. Kaga K, Shinoda Y, Suzuki JI (1997) Origin of auditory brainstem responses in cats: whole brainstem mapping, and a lesion and HRP study of the inferior colliculus. Acta Otolaryngol 117:197-201.
16. Kaga K, Ono M, Yakumaru K, Owada M, Mizutani T (1998) Brainstem pathology of infantile Gaucher's disease with only wave I and II of auditory brainstem response. J Laryngol Otol 112:1069-1073.
17. Kataoka K, Fujiwara KT, Noda M, Nishizawa M (1994) MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol Cell Biol 14:7581-7591.
18. Kovalenko D, Yang X, Nadeau RJ, Harkins LK, Friesel R (2003) Sef inhibits fibroblast growth factor signaling by inhibiting FGFR1 tyrosine phosphorylation and subsequent ERK activation. J Biol Chem 278:14087-14091.
19. Kovalenko D, Yang X, Chen PY, Nadeau RJ, Zubanova O, Pigeon K, Friesel R (2006) A role for extracellular and transmembrane domains of Sef in Sef-mediated inhibition of FGF signaling. Cell Signal 18:1958-1966.
20. Krull CE (2004) A primer on using in ovo electroporation to analyze gene function. Dev Dyn 229:433-439.
21. Lacey DJ, Terplan K (1984) Correlating auditory evoked and brainstem histologic abnormalities in infantile Gaucher's disease. Neurology 34:539-541.
22. Landsberg RL, Awatramani RB, Hunter NL, Farago AF, DiPietrantonio HJ, Rodriguez CI, Dymecki SM (2005) Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48:933-947.
23. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M (2001) Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410:174-179.
24. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300-304.
25. Lin W, Furthauer M, Thisse B, Thisse C, Jing N, Ang SL (2002) Cloning of the mouse Sef gene and comparative analysis of its expression with Fgf8 and Spry2 during embryogenesis. Mech Dev 113:163-168.
26. Lin W, Jing N, Basson MA, Dierich A, Licht J, Ang SL (2005) Synergistic activity of Sef and Sprouty proteins in regulating the expression of Gbx2 in the mid-hindbrain region. Genesis 41:110-115.
27. Liu M, Pereira FA, Price SD, Chu MJ, Shope C, Himes D, Eatock RA, Brownell WE, Lysakowski A, Tsai MJ (2000) Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev 14:2839-2854.
28. Luo L, Moore JK, Baird A, Ryan AF (1995) Expression of acidic FGF mRNA in rat auditory brainstem during postnatal maturation. Brain Res Dev Brain Res 86:24-34.
29. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24.
30. Martin MR (1981) Morphology of the cochlear nucleus of the normal and reeler mutant mouse. J Comp Neurol 197:141-152.
31. Melcher JR, Kiang NY (1996) Generators of the brainstem auditory evoked potential in cat. III: Identified cell populations. Hear Res 93:52-71.
32. Melcher JR, Knudson IM, Fullerton BC, Guinan Jr JJ, Norris BE, Kiang NY (1996a) Generators of the brainstem auditory evoked potential in cat. I. An experimental approach to their identification. Hear Res 93:1-27.
33. Melcher JR, Guinan Jr JJ, Knudson IM, Kiang NY (1996b) Generators of the brainstem auditory evoked potential in cat. II. Correlating lesion sites with waveform changes. Hear Res 93:28-51.
34. Mitchell KJ, Pinson KI, Kelly OG, Brennan J, Zupicich J, Scherz P, Leighton PA, Goodrich LV, Lu X, Avery BJ, Tate P, Dill K, Pangilinan E, Wakenight P, Tessier-Lavigne M, Skarnes WC (2001) Functional analysis of secreted and transmembrane proteins critical to mouse development. Nat Genet 28:241-249.
35. Newman EA (2003) New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 26:536 -542.
36. Peters K, Ornitz D, Werner S, Williams L (1993) Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev Biol 155:423-430.
37. Peters KG, Werner S, Chen G, Williams LT (1992) Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114:233-243.
38. Pierce ET (1967) Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study. J Comp Neurol 131:27-54.
39. Preger E, Ziv I, Shabtay A, Sher I, Tsang M, Dawid IB, Altuvia Y, Ron D (2004) Alternative splicing generates an isoform of the human Sef gene with altered subcellular localization and specificity. Proc Natl Acad Sci USA 101:1229-1234.
40. Pringle NP, Yu WP, Howell M, Colvin JS, Ornitz DM, Richardson WD (2003) Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130:93-102.
41. Riedel B, Friauf E, Grothe C, Unsicker K (1995) Fibroblast growth factor-2-like immunoreactivity in auditory brainstem nuclei of the developing and adult rat: correlation with onset and loss of hearing. J Comp Neurol 354:353-360.
42. Rodriguez CI, Dymecki SM (2000) Origin of the precerebellar system. Neuron 27:475-486.
43. Ryugo DK, Parks TN (2003) Primary innervation of the avian and mammalian cochlear nucleus. Brain Res Bull 60:435-456.
44. Sato T, Nakamura H (2004) The Fgf8 signal causes cerebellar differentiation by activating the Ras-ERK signaling pathway. Development 131:4275-4285.
45. Shim K, Minowada G, Coling DE, Martin GR (2005) Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev Cell 8:553-564.
46. Smith L, Gross J, Morest DK (2002) Fibroblast growth factors (FGFs) in the cochlear nucleus of the adult mouse following acoustic overstimulation. Hear Res 169:1-12.
47. Steel K, Erven A, Kiernan A (2002) Mice as models for human hereditary deafness. In: Genetics and auditory disorders (Keats BJB, Popper AN, Fay RR, eds), pp 247-296. New York: Springer.
48. Storm EE, Garel S, Borello U, Hebert JM, Martinez S, McConnell SK, Martin GR, Rubenstein JL (2006) Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133:1831-1844.
49. Taketomi T, Yoshiga D, Taniguchi K, Kobayashi T, Nonami A, Kato R, Sasaki M, Sasaki A, Ishibashi H, Moriyama M, Nakamura KI, Nishimura J, Yoshimura A (2005) Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat Neurosci 8:855-857.
50. Timmer JR, Wang C, Niswander L (2002) BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loophelix transcription factors. Development 129:2459-2472.
51. Torii S, Kusakabe M, Yamamoto T, Maekawa M, Nishida E (2004) Sef is a spatial regulator for Ras/MAP kinase signaling. Dev Cell 7:33-44.
52. Tsang M, Dawid IB (2004) Promotion and attenuation of FGF signaling through the Ras-MAPK pathway. Sci STKE 2004:pe17.
53. Tsang M, Friesel R, Kudoh T, Dawid IB (2002) Identification of Sef, a novel modulator of FGF signalling. Nat Cell Biol 4:165-169.
54. Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31-43.
55. Willard FH, Martin GF (1986) The development and migration of large multipolar neurons into the cochlear nucleus of the North American opossum. J Comp Neurol 248:119-132.
56. Wingate RJ (2001) The rhombic lip and early cerebellar development. Curr Opin Neurobiol 11:82-88.
57. Wright TJ, Ladher R, McWhirter J, Murre C, Schoenwolf GC, Mansour SL (2004) Mouse FGF15 is the ortholog of human and chick FGF19, but is not uniquely required for otic induction. Dev Biol 269:264-275.
58. Yamaguchi TP, Conlon RA, Rossant J (1992) Expression of the fibroblast growth factor receptor FGFR-1/flg during gastrulation and segmentation in the mouse embryo. Dev Biol 152:75-88.
59. Yang RB, Ng CK, Wasserman SM, Komuves LG, Gerritsen ME, Topper JN (2003) A novel interleukin-17 receptor-like protein identified in human umbilical vein endothelial cells antagonizes basic fibroblast growth factor-induced signaling. J Biol Chem 278:33232-33238.
60. Zaaroor M, Starr A (1991) Auditory brain-stem evoked potentials in cat after kainic acid induced neuronal loss. II. Cochlear nucleus. Electroencephalogr Clin Neurophysiol 80:436-445.
61. Zhou X, Hossain WA, Rutledge A, Baier C, Morest DK (1996) Basic fibroblast growth factor (FGF-2) affects development of acoustico-vestibular neurons in the chick embryo brain in vitro. Hear Res 101:187-207.