DOI QR코드

DOI QR Code

FGF signaling: diverse roles during cochlear development

  • Ebeid, Michael (Department of Developmental Neuroscience, Munroe Meyer Institute for Genetics and Rehabilitation, University of Nebraska Medical Center) ;
  • Huh, Sung-Ho (Mary & Dick Holland Regenerative Medicine Program, Munroe Meyer Institute for Genetics and Rehabilitation, University of Nebraska Medical Center)
  • Received : 2017.08.21
  • Published : 2017.10.31

Abstract

Mammalian inner ear comprises of six sensory organs; cochlea, utricle, saccule, and three semicircular canals. The cochlea contains sensory epithelium known as the organ of Corti which senses sound through mechanosensory hair cells. Mammalian inner ear undergoes series of morphogenesis during development beginning thickening of ectoderm nearby hindbrain. These events require tight regulation of multiple signaling cascades including FGF, Wnt, Notch and Bmp signaling. In this review, we will discuss the role of newly emerging signaling, FGF signaling, for its roles required for cochlear development.

Keywords

References

  1. Lopez-Poveda EAPARMR (2010) The neurophysiological bases of auditory perception, Springer, New York
  2. Driver EC and Kelley MW (2009) Specification of cell fate in the mammalian cochlea. Birth Defects Res C Embryo Today 87, 212-221 https://doi.org/10.1002/bdrc.20154
  3. Schimmang T (2007) Expression and functions of FGF ligands during early otic development. Int J Dev Biol 51, 473-481 https://doi.org/10.1387/ijdb.072334ts
  4. Huh SH, Jones J, Warchol ME and Ornitz DM (2012) Differentiation of the lateral compartment of the cochlea requires a temporally restricted FGF20 signal. PLoS Biol 10, e1001231 https://doi.org/10.1371/journal.pbio.1001231
  5. Huh SH, Warchol ME and Ornitz DM (2015) Cochlear progenitor number is controlled through mesenchymal FGF receptor signaling. eLife 4, e05921
  6. Ono K, Kita T, Sato S et al (2014) FGFR1-Frs2/3 signalling maintains sensory progenitors during inner ear hair cell formation. PLoS Genet 10, e1004118 https://doi.org/10.1371/journal.pgen.1004118
  7. Mansour SL, Li C and Urness LD (2013) Genetic rescue of Muenke syndrome model hearing loss reveals prolonged FGF-dependent plasticity in cochlear supporting cell fates. Genes Dev 27, 2320-2331 https://doi.org/10.1101/gad.228957.113
  8. Ornitz DM (2000) FGFs, heparan sulfate and FGFRs: complex interactions essential for development. Bioessays 22, 108-112 https://doi.org/10.1002/(SICI)1521-1878(200002)22:2<108::AID-BIES2>3.0.CO;2-M
  9. Ornitz DM and Itoh N (2001) Fibroblast growth factors. Genome Biol 2, reviews3005.3001-reviews3005.3012
  10. Rapraeger AC, Krufka A and Olwin BB (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science (New York, N.Y.) 252, 1705-1708 https://doi.org/10.1126/science.1646484
  11. Ornitz DM and Itoh N (2015) The Fibroblast Growth Factor signaling pathway. Wiley Interdiscip Rev Dev Biol 4, 215-266 https://doi.org/10.1002/wdev.176
  12. Potthoff MJ, Kliewer SA and Mangelsdorf DJ (2012) Endocrine fibroblast growth factors 15/19 and 21: from feast to famine. Genes Dev 26, 312-324 https://doi.org/10.1101/gad.184788.111
  13. Smith ER, McMahon LP and Holt SG (2014) Fibroblast growth factor 23. Ann Clin Biochem 51, 203-227 https://doi.org/10.1177/0004563213510708
  14. Goldfarb M (2005) Fibroblast growth factor homologous factors: evolution, structure, and function. Cytokine Growth Factor Rev 16, 215-220 https://doi.org/10.1016/j.cytogfr.2005.02.002
  15. Schoorlemmer J and Goldfarb M (2002) Fibroblast growth factor homologous factors and the islet brain-2 scaffold protein regulate activation of a stress-activated protein kinase. J Biol Chem 277, 49111-49119 https://doi.org/10.1074/jbc.M205520200
  16. Herr AB, Ornitz DM, Sasisekharan R, Venkataraman G and Waksman G (1997) Heparin-induced self-association of fibroblast growth factor-2. Evidence for two oligomerization processes. J Biol Chem 272, 16382-16389 https://doi.org/10.1074/jbc.272.26.16382
  17. Mach H, Volkin DB, Burke CJ et al (1993) Nature of the interaction of heparin with acidic fibroblast growth factor. Biochemistry 32, 5480-5489 https://doi.org/10.1021/bi00071a026
  18. McKeehan WL, Wang F and Kan M (1998) The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog Nucleic Acid Res Mol Biol 59, 135-176
  19. Bottcher RT and Niehrs C (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26, 63-77 https://doi.org/10.1210/er.2003-0040
  20. Wang JK, Xu H, Li HC and Goldfarb M (1996) Broadly Expressed Snt-Like Proteins Link Fgf Receptor Stimulation to Activators Of Ras. Oncogene 13, 721-729
  21. Ong SH, Guy GR, Hadari YR et al (2000) FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol Cell Biol 20, 979-989 https://doi.org/10.1128/MCB.20.3.979-989.2000
  22. Kouhara H, Hadari YR, Spivakkroizman T et al (1997) A Lipid-Anchored Grb2-Binding Protein That Links Fgf- Receptor Activation to the Ras/Mapk Signaling Pathway. Cell 89, 693-702 https://doi.org/10.1016/S0092-8674(00)80252-4
  23. Hadari YR, Gotoh N, Kouhara H, Lax I and Schlessinger J (2001) Critical role for the docking-protein FRS2 alpha in FGF receptor-mediated signal transduction pathways. Proc Natl Acad Sci U S A 98, 8578-8583 https://doi.org/10.1073/pnas.161259898
  24. Kouhara H, Kasayama S, Saito H, Matsumoto K and Sato B (1991) Expression cDNA cloning of fibroblast growth factor (FGF) receptor in mouse breast cancer cells: A variant form in FGF-responsive transformed cells. Biochem Biophys Res Comm 176, 31-37 https://doi.org/10.1016/0006-291X(91)90885-B
  25. Janknecht R, Monte D, Baert JL and de Launoit Y (1996) The ETS-related transcription factor ERM is a nuclear target of signaling cascades involving MAPK and PKA. Oncogene 13, 1745-1754
  26. Johnson DE and Williams LT (1993) Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60, 1-41
  27. Groth C and Lardelli M (2002) The structure and function of vertebrate fibroblast growth factor receptor 1. Int J Dev Biol 46, 393-400
  28. Ornitz DM, Xu J, Colvin JS et al (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271, 15292-15297 https://doi.org/10.1074/jbc.271.25.15292
  29. Xu J, Liu Z and Ornitz DM (2000) Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 127, 1833-1843
  30. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M and Ornitz DM (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281, 15694-15700 https://doi.org/10.1074/jbc.M601252200
  31. Avivi A, Yayon A and Givol D (1993) A novel form of FGF receptor-3 using an alternative exon in the immunoglobulin domain III. FEBS Lett 330, 249-252 https://doi.org/10.1016/0014-5793(93)80882-U
  32. Gilbert E, Del Gatto F, Champion-Arnaud P, Gesnel MC and Breathnach R (1993) Control of BEK and K-SAM splice sites in alternative splicing of the fibroblast growth factor receptor 2 pre-mRNA. Mol Cell Biol 13, 5461-5468 https://doi.org/10.1128/MCB.13.9.5461
  33. Hacohen N, Kramer S, Sutherland D, Hiromi Y and Krasnow MA (1998) sprouty Encodes a Novel Antagonist of FGF Signaling that Patterns Apical Branching of the Drosophila Airways. Cell 92, 253-263 https://doi.org/10.1016/S0092-8674(00)80919-8
  34. Colvin JS, Feldman B, Nadeau JH, Goldfarb M and Ornitz DM (1999) Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev Dyn 216, 72-88 https://doi.org/10.1002/(SICI)1097-0177(199909)216:1<72::AID-DVDY9>3.0.CO;2-9
  35. Colvin JS, White A, Pratt SJ and Ornitz DM (2001) Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128, 2095-2106
  36. White AC, Xu J, Yin Y, Smith C, Schmid G and Ornitz DM (2006) FGF9 and SHH signaling coordinate lung growth and development through regulation of distinct mesenchymal domains. Development 133, 1507-1517 https://doi.org/10.1242/dev.02313
  37. Bellusci S, Grindley J, Emoto H, Itoh N and Hogan BL (1997) Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124, 4867-4878
  38. Park WY, Miranda B, Lebeche D, Hashimoto G and Cardoso WV (1998) FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol 201, 125-134 https://doi.org/10.1006/dbio.1998.8994
  39. Min H, Danilenko DM, Scully SA et al (1998) Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 12, 3156-3161 https://doi.org/10.1101/gad.12.20.3156
  40. Sekine K, Ohuchi H, Fujiwara M et al (1999) Fgf10 is essential for limb and lung formation. Nat Genet 21, 138-141 https://doi.org/10.1038/5096
  41. Ohuchi H, Hori Y, Yamasaki M et al (2000) FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multiorgan development. Biochem Biophys Res Commun 277, 643-649 https://doi.org/10.1006/bbrc.2000.3721
  42. Arman E, Haffner-Krausz R, Gorivodsky M and Lonai P (1999) Fgfr2 is required for limb outgrowth and lungbranching morphogenesis. Proc Natl Acad Sci U S A 96, 11895-11899 https://doi.org/10.1073/pnas.96.21.11895
  43. Morsli H, Choo D, Ryan A, Johnson R and Wu DK (1998) Development of the mouse inner ear and origin of its sensory organs. J Neurosci 18, 3327-3335 https://doi.org/10.1523/JNEUROSCI.18-09-03327.1998
  44. Ohyama T, Basch ML, Mishina Y, Lyons KM, Segil N and Groves AK (2010) BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. J Neurosci 30, 15044-15051 https://doi.org/10.1523/JNEUROSCI.3547-10.2010
  45. Riccomagno MM, Martinu L, Mulheisen M, Wu DK and Epstein DJ (2002) Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16, 2365-2378 https://doi.org/10.1101/gad.1013302
  46. Riccomagno MM, Takada S and Epstein DJ (2005) Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev 19, 1612-1623 https://doi.org/10.1101/gad.1303905
  47. Kiernan AE, Xu J and Gridley T (2006) The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet 2, e4 https://doi.org/10.1371/journal.pgen.0020004
  48. Kiernan AE, Pelling AL, Leung KK et al (2005) Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434, 1031-1035 https://doi.org/10.1038/nature03487
  49. Lee YS, Liu F and Segil N (2006) A morphogenetic wave of p27Kip1 transcription directs cell cycle exit during organ of Corti development. Development 133, 2817-2826 https://doi.org/10.1242/dev.02453
  50. Chen P, Johnson JE, Zoghbi HY and Segil N (2002) The role of Math1 in inner ear development: Uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129, 2495-2505
  51. Kelley MW (2006) Regulation of cell fate in the sensory epithelia of the inner ear. Nat Rev Neurosci 7, 837-849 https://doi.org/10.1038/nrn1987
  52. Zhai S, Shi L, Wang BE et al (2005) Isolation and culture of hair cell progenitors from postnatal rat cochleae. J Neurobiol 65, 282-293 https://doi.org/10.1002/neu.20190
  53. Montcouquiol M and Kelley MW (2003) Planar and vertical signals control cellular differentiation and patterning in the mammalian cochlea. J Neurobiol 23, 9469-9478
  54. Swanson GJ, Howard M and Lewis J (1990) Epithelial autonomy in the development of the inner ear of a bird embryo. Dev Biol 137, 243-257 https://doi.org/10.1016/0012-1606(90)90251-D
  55. Pirvola U, Zhang X, Mantela J, Ornitz DM and Ylikoski J (2004) Fgf9 signaling regulates inner ear morphogenesis through epithelial-mesenchymal interactions. Dev Biol 273, 350-360 https://doi.org/10.1016/j.ydbio.2004.06.010
  56. Hayashi T, Ray CA and Bermingham-McDonogh O (2008) Fgf20 is required for sensory epithelial specification in the developing cochlea. J Neurosci 28, 5991-5999 https://doi.org/10.1523/JNEUROSCI.1690-08.2008
  57. Pirvola U, Ylikoski J, Trokovic R, Hebert JM, McConnell SK and Partanen J (2002) FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35, 671-680 https://doi.org/10.1016/S0896-6273(02)00824-3
  58. Ono K, Kita T, Sato S et al (2014) FGFR1-Frs2/3 Signalling Maintains Sensory Progenitors during Inner Ear Hair Cell Formation. PLoS Genet 10, e1004118 https://doi.org/10.1371/journal.pgen.1004118
  59. Hayashi T, Ray CA, Younkins C and Bermingham-McDonogh O (2010) Expression patterns of FGF receptors in the developing mammalian cochlea. Dev Dyn 239, 1019-1026 https://doi.org/10.1002/dvdy.22236
  60. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM and Leder P (1994) Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev 8, 3045-3057 https://doi.org/10.1101/gad.8.24.3045
  61. Yamaguchi TP, Harpal K, Henkemeyer M and Rossant J (1994) Fgfr-1 is Required for Embryonic Growth and Mesodermal Patterning during Mouse Gastrulation. Genes Dev 8, 3032-3044 https://doi.org/10.1101/gad.8.24.3032
  62. Colvin JS, Bohne BA, Harding GW, McEwen DG and Ornitz DM (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat Genet 12, 390-397 https://doi.org/10.1038/ng0496-390
  63. Mueller KL, Jacques BE and Kelley MW (2002) Fibroblast growth factor signaling regulates pillar cell development in the organ of corti. J Neurosci 22, 9368-9377 https://doi.org/10.1523/JNEUROSCI.22-21-09368.2002
  64. Jacques BE, Montcouquiol ME, Layman EM, Lewandoski M and Kelley MW (2007) Fgf8 induces pillar cell fate and regulates cellular patterning in the mammalian cochlea. Development 134, 3021-3029 https://doi.org/10.1242/dev.02874
  65. Peters K, Ornitz D, Werner S and Williams L (1993) Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev Biol 155, 423-430 https://doi.org/10.1006/dbio.1993.1040
  66. Mansour SL, Twigg SR, Freeland RM, Wall SA, Li C and Wilkie AO (2009) Hearing loss in a mouse model of Muenke syndrome. Hum Mol Genet 18, 43-50 https://doi.org/10.1093/hmg/ddn311
  67. Urness LD, Wang X, Shibata S, Ohyama T and Mansour SL (2015) Fgf10 is required for specification of non-sensory regions of the cochlear epithelium. Dev Biol 400, 59-71 https://doi.org/10.1016/j.ydbio.2015.01.015
  68. Shams I, Rohmann E, Eswarakumar VP et al (2007) Lacrimo-auriculo-dento-digital syndrome is caused by reduced activity of the fibroblast growth factor 10 (FGF10)-FGF receptor 2 signaling pathway. Mol Cell Biol 27, 6903-6912 https://doi.org/10.1128/MCB.00544-07
  69. Zhang H, Dessimoz J, Beyer TA et al (2004) Fibroblast growth factor receptor 1-IIIb is dispensable for skin morphogenesis and wound healing. Eur J Cell Biol 83, 3-11 https://doi.org/10.1078/0171-9335-00355
  70. del Moral PM, De Langhe SP, Sala FG et al (2006) Differential role of FGF9 on epithelium and mesenchyme in mouse embryonic lung. Dev Biol 293, 77-89 https://doi.org/10.1016/j.ydbio.2006.01.020
  71. Ku YC, Renaud NA, Veile RA et al (2014) The transcriptome of utricle hair cell regeneration in the avian inner ear. J Neurosci 34, 3523-3535 https://doi.org/10.1523/JNEUROSCI.2606-13.2014
  72. Alvarez Y, Alonso MT, Vendrell V et al (2003) Requirements for FGF3 and FGF10 during inner ear formation. Development 130, 6329-6338 https://doi.org/10.1242/dev.00881
  73. Wright TJ and Mansour SL (2003) Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130, 3379-3390 https://doi.org/10.1242/dev.00555
  74. Urness LD, Paxton CN, Wang X, Schoenwolf GC and Mansour SL (2010) FGF signaling regulates otic placode induction and refinement by controlling both ectodermal target genes and hindbrain Wnt8a. Dev Biol 340, 595-604 https://doi.org/10.1016/j.ydbio.2010.02.016
  75. Ohuchi H, Yasue A, Ono K et al (2005) Identification of cis-element regulating expression of the mouse Fgf10 gene during inner ear development. Dev Dyn 233, 177-187 https://doi.org/10.1002/dvdy.20319
  76. Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K and Fritzsch B (2003) Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 227, 203-215 https://doi.org/10.1002/dvdy.10297
  77. Pirvola U, Spencer-Dene B, Xing-Qun L et al (2000) FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. J Neurosci 20, 6125-6134 https://doi.org/10.1523/JNEUROSCI.20-16-06125.2000
  78. Hayashi T, Cunningham D and Bermingham-McDonogh O (2007) Loss of Fgfr3 leads to excess hair cell development in the mouse organ of Corti. Dev Dyn 236, 525-533 https://doi.org/10.1002/dvdy.21026