XB-ART-50253
Cell Tissue Res
2015 Jul 01; doi: 10.1007/s00441-014-2031-5.
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Inner ear development: building a spiral ganglion and an organ of Corti out of unspecified ectoderm.
Fritzsch B
,
Pan N
,
Jahan I
,
Elliott KL
.
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The mammalian inner ear develops from a placodal thickening into a complex labyrinth of ducts with five sensory organs specialized to detect position and movement in space. The mammalian ear also develops a spiraled cochlear duct containing the auditory organ, the organ of Corti (OC), specialized to translate sound into hearing. Development of the OC from a uniform sheet of ectoderm requires unparalleled precision in the topological developmental engineering of four different general cell types, namely sensory neurons, hair cells, supporting cells, and general otic epithelium, into a mosaic of ten distinctly recognizable cell types in and around the OC, each with a unique distribution. Moreover, the OC receives unique innervation by ear-derived spiral ganglion afferents and brainstem-derived motor neurons as efferents and requires neural-crest-derived Schwann cells to form myelin and neural-crest-derived cells to induce the stria vascularis. This transformation of a sheet of cells into a complicated interdigitating set of cells necessitates the orchestrated expression of multiple transcription factors that enable the cellular transformation from ectoderm into neurosensory cells forming the spiral ganglion neurons (SGNs), while simultaneously transforming the flat epithelium into a tube, the cochlear duct, housing the OC. In addition to the cellular and conformational changes forming the cochlear duct with the OC, changes in the surrounding periotic mesenchyme form passageways for sound to stimulate the OC. We review molecular developmental data, generated predominantly in mice, in order to integrate the well-described expression changes of transcription factors and their actions, as revealed in mutants, in the formation of SGNs and OC in the correct position and orientation with suitable innervation. Understanding the molecular basis of these developmental changes leading to the formation of the mammalian OC and highlighting the gaps in our knowledge might guide in vivo attempts to regenerate this most complicated cellular mosaic of the mammalian body for the reconstitution of hearing in a rapidly growing population of aging people suffering from hearing loss.
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References [+] :
Ahmed,
EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear.
2012, Pubmed
Ahmed, EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear. 2012, Pubmed
Alam, Prosurvival and proapoptotic intracellular signaling in rat spiral ganglion neurons in vivo after the loss of hair cells. 2007, Pubmed
Appler, Gata3 is a critical regulator of cochlear wiring. 2013, Pubmed
Appler, Connecting the ear to the brain: Molecular mechanisms of auditory circuit assembly. 2011, Pubmed
Basch, Canonical Notch signaling is not necessary for prosensory induction in the mouse cochlea: insights from a conditional mutant of RBPjkappa. 2011, Pubmed
Benito-Gonzalez, Hey1 and Hey2 control the spatial and temporal pattern of mammalian auditory hair cell differentiation downstream of Hedgehog signaling. 2014, Pubmed
Bermingham, Math1: an essential gene for the generation of inner ear hair cells. 1999, Pubmed
Bok, Opposing gradients of Gli repressor and activators mediate Shh signaling along the dorsoventral axis of the inner ear. 2007, Pubmed
Bouchard, Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. 2010, Pubmed
Bruce, The development of vestibulocochlear efferents and cochlear afferents in mice. 1997, Pubmed
Bulankina, Neural circuit development in the mammalian cochlea. 2012, Pubmed
Burton, The role of Pax2 in mouse inner ear development. 2004, Pubmed , Xenbase
Cai, Conditional deletion of Atoh1 reveals distinct critical periods for survival and function of hair cells in the organ of Corti. 2013, Pubmed
Chellappa, Barhl1 regulatory sequences required for cell-specific gene expression and autoregulation in the inner ear and central nervous system. 2008, Pubmed
Chen, Induction of the inner ear: stepwise specification of otic fate from multipotent progenitors. 2013, Pubmed
Chen, The role of Math1 in inner ear development: Uncoupling the establishment of the sensory primordium from hair cell fate determination. 2002, Pubmed
Chonko, Atoh1 directs hair cell differentiation and survival in the late embryonic mouse inner ear. 2013, Pubmed
Coate, Making connections in the inner ear: recent insights into the development of spiral ganglion neurons and their connectivity with sensory hair cells. 2013, Pubmed
Cross, The Opdc missense mutation of Pax2 has a milder than loss-of-function phenotype. 2011, Pubmed
Dabdoub, Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. 2008, Pubmed
Defourny, Ephrin-A5/EphA4 signalling controls specific afferent targeting to cochlear hair cells. 2013, Pubmed
Delaune, Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. 2005, Pubmed , Xenbase
Doetzlhofer, Hey2 regulation by FGF provides a Notch-independent mechanism for maintaining pillar cell fate in the organ of Corti. 2009, Pubmed
Driver, The Atoh1-lineage gives rise to hair cells and supporting cells within the mammalian cochlea. 2013, Pubmed
Duncan, Continued expression of GATA3 is necessary for cochlear neurosensory development. 2013, Pubmed
Durruthy-Durruthy, Reconstruction of the mouse otocyst and early neuroblast lineage at single-cell resolution. 2014, Pubmed
Echteler, Spatiotemporal patterns of neuronal programmed cell death during postnatal development of the gerbil cochlea. 2005, Pubmed
Edlund, Foxi transcription factors promote pharyngeal arch development by regulating formation of FGF signaling centers. 2014, Pubmed
Ernfors, Complementary roles of BDNF and NT-3 in vestibular and auditory development. 1995, Pubmed
Fariñas, Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. 2001, Pubmed
Forni, High levels of Cre expression in neuronal progenitors cause defects in brain development leading to microencephaly and hydrocephaly. 2006, Pubmed
Freyer, Dual embryonic origin of the mammalian otic vesicle forming the inner ear. 2011, Pubmed
Fritzsch, Evolution of vertebrate mechanosensory hair cells and inner ears: toward identifying stimuli that select mutation driven altered morphologies. 2014, Pubmed
Fritzsch, Mice with a targeted disruption of the neurotrophin receptor trkB lose their gustatory ganglion cells early but do develop taste buds. 1997, Pubmed
Fritzsch, Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. 2005, Pubmed
Fritzsch, Dissecting the molecular basis of organ of Corti development: Where are we now? 2011, Pubmed
Fritzsch, Canal cristae growth and fiber extension to the outer hair cells of the mouse ear require Prox1 activity. 2010, Pubmed
Fritzsch, The development of the hindbrain afferent projections in the axolotl: evidence for timing as a specific mechanism of afferent fiber sorting. 2005, Pubmed
Fritzsch, Development and evolution of inner ear sensory epithelia and their innervation. 2002, Pubmed
Fritzsch, Ancestry of Photic and Mechanic Sensation? 2005, Pubmed
Fritzsch, Cells, molecules and morphogenesis: the making of the vertebrate ear. 2006, Pubmed
Fritzsch, Lack of neurotrophin 3 causes losses of both classes of spiral ganglion neurons in the cochlea in a region-specific fashion. 1997, Pubmed
Fritzsch, Development of inner ear afferent connections: forming primary neurons and connecting them to the developing sensory epithelia. 2003, Pubmed
Fritzsch, Evolution and development of the tetrapod auditory system: an organ of Corti-centric perspective. 2013, Pubmed
Fritzsch, Neurotrophins in the ear: their roles in sensory neuron survival and fiber guidance. 2004, Pubmed
Fritzsch, The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration? 2006, Pubmed
Fritzsch, The role of bHLH genes in ear development and evolution: revisiting a 10-year-old hypothesis. 2010, Pubmed
Gehring, Chance and necessity in eye evolution. 2011, Pubmed
Gokoffski, Activin and GDF11 collaborate in feedback control of neuroepithelial stem cell proliferation and fate. 2011, Pubmed
Golub, Hair cell replacement in adult mouse utricles after targeted ablation of hair cells with diphtheria toxin. 2012, Pubmed
Groves, Shaping sound in space: the regulation of inner ear patterning. 2012, Pubmed
Groves, The genetics of hair cell development and regeneration. 2013, Pubmed
Hertzano, Transcription profiling of inner ears from Pou4f3(ddl/ddl) identifies Gfi1 as a target of the Pou4f3 deafness gene. 2004, Pubmed
Huang, Brn3a is a transcriptional regulator of soma size, target field innervation and axon pathfinding of inner ear sensory neurons. 2001, Pubmed
Hudspeth, Integrating the active process of hair cells with cochlear function. 2014, Pubmed
Huh, Differentiation of the lateral compartment of the cochlea requires a temporally restricted FGF20 signal. 2012, Pubmed
Ikeda, Transcription factors with conserved binding sites near ATOH1 on the POU4F3 gene enhance the induction of cochlear hair cells. 2015, Pubmed
Imayoshi, bHLH factors in self-renewal, multipotency, and fate choice of neural progenitor cells. 2014, Pubmed
Ishimura, RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. 2014, Pubmed
Jahan, Beyond generalized hair cells: molecular cues for hair cell types. 2013, Pubmed
Jahan, Neurod1 regulates survival and formation of connections in mouse ear and brain. 2010, Pubmed
Jahan, Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. 2010, Pubmed
Jahan, Expression of Neurog1 instead of Atoh1 can partially rescue organ of Corti cell survival. 2012, Pubmed
Karis, Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. 2001, Pubmed
Kelly, Atoh1 directs the formation of sensory mosaics and induces cell proliferation in the postnatal mammalian cochlea in vivo. 2012, Pubmed
Kelly, Development of form and function in the mammalian cochlea. 2009, Pubmed
Kersigo, The role of sensory organs and the forebrain for the development of the craniofacial shape as revealed by Foxg1-cre-mediated microRNA loss. 2011, Pubmed
Kiernan, Sox2 is required for sensory organ development in the mammalian inner ear. 2005, Pubmed
Kiernan, The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. 2006, Pubmed
Kim, NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. 2001, Pubmed
Kopecky, Scanning thin-sheet laser imaging microscopy elucidates details on mouse ear development. 2012, Pubmed
Kopecky, Correct timing of proliferation and differentiation is necessary for normal inner ear development and auditory hair cell viability. 2013, Pubmed
Koundakjian, Auditory neurons make stereotyped wiring decisions before maturation of their targets. 2007, Pubmed
Krüger, Functional redundancy of NSCL-1 and NeuroD during development of the petrosal and vestibulocochlear ganglia. 2006, Pubmed
Ladhams, Morphology of the monotreme organ of Corti and macula lagena. 1996, Pubmed
Lamb, Evolution of phototransduction, vertebrate photoreceptors and retina. 2013, Pubmed
Leake, Postnatal refinement of auditory nerve projections to the cochlear nucleus in cats. 2002, Pubmed
Li, Hearing loss caused by progressive degeneration of cochlear hair cells in mice deficient for the Barhl1 homeobox gene. 2002, Pubmed
Liu, Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. 2000, Pubmed
Liu, Characterization of transcriptomes of cochlear inner and outer hair cells. 2014, Pubmed
Luo, Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. 2011, Pubmed
Ma, Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. 2000, Pubmed
Ma, neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. 1998, Pubmed , Xenbase
Maklad, Development of vestibular afferent projections into the hindbrain and their central targets. 2003, Pubmed
Mao, Reprogramming amacrine and photoreceptor progenitors into retinal ganglion cells by replacing Neurod1 with Atoh7. 2013, Pubmed
Mao, Targeted deletion of Sox10 by Wnt1-cre defects neuronal migration and projection in the mouse inner ear. 2014, Pubmed
Matei, Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. 2005, Pubmed
Nakano, A mutation in the Srrm4 gene causes alternative splicing defects and deafness in the Bronx waltzer mouse. 2012, Pubmed
Nayagam, The spiral ganglion: connecting the peripheral and central auditory systems. 2011, Pubmed
Nichols, Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. 2008, Pubmed
Northcutt, The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. 1983, Pubmed
O'Neill, The amniote paratympanic organ develops from a previously undiscovered sensory placode. 2012, Pubmed
Ohyama, BMP signaling is necessary for patterning the sensory and nonsensory regions of the developing mammalian cochlea. 2010, Pubmed
Ohyama, The first steps towards hearing: mechanisms of otic placode induction. 2007, Pubmed
Pan, Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti. 2011, Pubmed
Pan, A novel Atoh1 "self-terminating" mouse model reveals the necessity of proper Atoh1 level and duration for hair cell differentiation and viability. 2012, Pubmed
Pan, Understanding the evolution and development of neurosensory transcription factors of the ear to enhance therapeutic translation. 2012, Pubmed
Pani, Ancient deuterostome origins of vertebrate brain signalling centres. 2012, Pubmed
Patthey, The evolutionary history of vertebrate cranial placodes--I: cell type evolution. 2014, Pubmed , Xenbase
Pauley, Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. 2006, Pubmed
Pauley, Stem cells and molecular strategies to restore hearing. 2008, Pubmed
Pauley, Expression and function of FGF10 in mammalian inner ear development. 2003, Pubmed
Pirvola, FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. 2000, Pubmed
Prasov, Pushing the envelope of retinal ganglion cell genesis: context dependent function of Math5 (Atoh7). 2012, Pubmed
Puligilla, Disruption of fibroblast growth factor receptor 3 signaling results in defects in cellular differentiation, neuronal patterning, and hearing impairment. 2007, Pubmed
Puligilla, Sox2 induces neuronal formation in the developing mammalian cochlea. 2010, Pubmed
Raft, Cross-regulation of Ngn1 and Math1 coordinates the production of neurons and sensory hair cells during inner ear development. 2007, Pubmed
Raft, Segregating neural and mechanosensory fates in the developing ear: patterning, signaling, and transcriptional control. 2015, Pubmed
Raft, Suppression of neural fate and control of inner ear morphogenesis by Tbx1. 2004, Pubmed
Reiprich, From CNS stem cells to neurons and glia: Sox for everyone. 2015, Pubmed
Rubel, Auditory system development: primary auditory neurons and their targets. 2002, Pubmed
Ruben, Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. 1967, Pubmed
Sandell, Cochleovestibular nerve development is integrated with migratory neural crest cells. 2014, Pubmed
Schlosser, The evolutionary history of vertebrate cranial placodes II. Evolution of ectodermal patterning. 2014, Pubmed , Xenbase
Shubin, Deep homology and the origins of evolutionary novelty. 2009, Pubmed
Sienknecht, Evolution and development of hair cell polarity and efferent function in the inner ear. 2014, Pubmed
Simmons, Development of the inner ear efferent system across vertebrate species. 2002, Pubmed
Soukup, Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. 2009, Pubmed
Spoendlin, The spiral ganglion and the innervation of the human organ of Corti. 1988, Pubmed
Sprinzak, Mutual inactivation of Notch receptors and ligands facilitates developmental patterning. 2011, Pubmed
Srinivasan, A BMP-FGF morphogen toggle switch drives the ultrasensitive expression of multiple genes in the developing forebrain. 2014, Pubmed
Steventon, Neural crest and placode interaction during the development of the cranial sensory system. 2014, Pubmed
Streit, Initiation of neural induction by FGF signalling before gastrulation. 2000, Pubmed
Torres, Pax2 contributes to inner ear patterning and optic nerve trajectory. 1996, Pubmed
Tritsch, The origin of spontaneous activity in the developing auditory system. 2007, Pubmed
Wallis, The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. 2003, Pubmed
Woods, Math1 regulates development of the sensory epithelium in the mammalian cochlea. 2004, Pubmed
Wright, Fgf3 and Fgf10 are required for mouse otic placode induction. 2003, Pubmed
Xiang, Brn3c null mutant mice show long-term, incomplete retention of some afferent inner ear innervation. 2003, Pubmed
Yamamoto, Myosin II regulates extension, growth and patterning in the mammalian cochlear duct. 2009, Pubmed
Yang, The molecular basis of making spiral ganglion neurons and connecting them to hair cells of the organ of Corti. 2011, Pubmed
Yang, Generation and characterization of Atoh1-Cre knock-in mouse line. 2010, Pubmed
Zetes, Structure and mechanics of supporting cells in the guinea pig organ of Corti. 2012, Pubmed
Zhu, The transcription factor Pou3f1 promotes neural fate commitment via activation of neural lineage genes and inhibition of external signaling pathways. 2014, Pubmed
von Bartheld, Comparative analysis of neurotrophin receptors and ligands in vertebrate neurons: tools for evolutionary stability or changes in neural circuits? 2006, Pubmed
von Bartheld, Expression of nerve growth factor (NGF) receptors in the developing inner ear of chick and rat. 1991, Pubmed