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      The amniote paratympanic organ develops from a previously undiscovered sensory placode

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          Abstract

          The paratympanic organ (PTO), a mechanosensory hair cell-containing pouch in the amniote middle ear, was first described 100 years ago yet its origins remain unresolved. Homology with the anamniote spiracular organ is supported by association with homologous skeletal elements and similar central targets of afferent neurons, suggesting it might be a remnant of the water-dependent lateral line system, otherwise lost during the amniote transition to terrestrial life. However, this is incompatible with studies suggesting it arises from the first epibranchial (geniculate) placode. Here we show that a previously undiscovered Sox2-positive placode, immediately dorsal to the geniculate placode, forms the PTO and its afferent neurons, which are molecularly and morphologically distinct from geniculate neurons. These data remove the only obstacle to accepting the homology of the PTO and spiracular organ. We hypothesise that the PTO/spiracular organ represents an ancient head ectoderm module, developmentally and evolutionarily independent of both lateral line and epibranchial placodes.

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          A series of normal stages in the development of the chick embryo

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            Math1: an essential gene for the generation of inner ear hair cells.

            The mammalian inner ear contains the cochlea and vestibular organs, which are responsible for hearing and balance, respectively. The epithelia of these sensory organs contain hair cells that function as mechanoreceptors to transduce sound and head motion. The molecular mechanisms underlying hair cell development and differentiation are poorly understood. Math1, a mouse homolog of the Drosophila proneural gene atonal, is expressed in inner ear sensory epithelia. Embryonic Math1-null mice failed to generate cochlear and vestibular hair cells. This gene is thus required for the genesis of hair cells.
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              Sox2 is required for sensory organ development in the mammalian inner ear.

              Sensory hair cells and their associated non-sensory supporting cells in the inner ear are fundamental for hearing and balance. They arise from a common progenitor, but little is known about the molecular events specifying this cell lineage. We recently identified two allelic mouse mutants, light coat and circling (Lcc) and yellow submarine (Ysb), that show hearing and balance impairment. Lcc/Lcc mice are completely deaf, whereas Ysb/Ysb mice are severely hearing impaired. We report here that inner ears of Lcc/Lcc mice fail to establish a prosensory domain and neither hair cells nor supporting cells differentiate, resulting in a severe inner ear malformation, whereas the sensory epithelium of Ysb/Ysb mice shows abnormal development with disorganized and fewer hair cells. These phenotypes are due to the absence (in Lcc mutants) or reduced expression (in Ysb mutants) of the transcription factor SOX2, specifically within the developing inner ear. SOX2 continues to be expressed in the inner ears of mice lacking Math1 (also known as Atoh1 and HATH1), a gene essential for hair cell differentiation, whereas Math1 expression is absent in Lcc mutants, suggesting that Sox2 acts upstream of Math1.
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                Author and article information

                Journal
                101528555
                37539
                Nat Commun
                Nat Commun
                Nature communications
                2041-1723
                30 November 2012
                2012
                10 December 2012
                : 3
                : 1041
                Affiliations
                [1 ]Laboratory for Sensory Development, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-Minamimachi, Chuo-ku, Kobe 650-0047, Japan
                [2 ]Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3DY, UK
                [3 ]Department of Biology, College of Liberal Arts and Sciences, University of Iowa, 143 Biology Building, Iowa City IA 52242-1324, US
                Author notes
                [* ]Joint corresponding authors, to whom correspondence should be addressed. cvhb1@ 123456cam.ac.uk , raj-ladher@ 123456cdb.riken.jp

                Author contributions

                C.V.H.B. and P.O. conceived the project; C.V.H.B., P.O., R.K.L. and B.F. designed the experiments; P.O. performed all experiments except nerve-tracing and generated all related figures; B.F. performed all nerve-tracing experiments and generated all related figures; S.M. contributed to the histological analysis. P.O. wrote the manuscript with significant contributions from C.V.H.B., R.K.L. and B.F.

                Article
                EMS50740
                10.1038/ncomms2036
                3518548
                22948823
                2689d89d-8566-4c9f-8bfc-7d1fe54a7d01

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