Expression of nerve growth factor (NGF) receptors in the developing inner ear of chick and rat

Development (Cambridge) - Tập 113 Số 2 - Trang 455-470 - 1991
Christopher S. von Bartheld1,2, Susan L. Patterson2, Josef G. Heuer2, Esther F. Wheeler2, Mark Bothwell2, Edwin W. Rubel1,2
1University of Washington School of Medicine 1 Hearing Development Laboratories RL-30 , , Seattle, WA 98195, USA
2University of Washington School of Medicine 2 Department of Physiology and Biophysics SJ-40 , , Seattle, WA 98195, USA

Tóm tắt

ABSTRACT The expression of nerve growth factor receptors (NGFRs) was studied in the developing inner ear with in situ hybridization in chick embryos and with immunocytochemistry in rat embryos to determine sites of possible functions of NGF or NGF-like molecules in inner ear development. NGFR expression in the chick otocyst and acoustic ganglion is compared with epithelial differentiation and the onset of afferent innervation as determined with fluorescent carbocyanine tracers. In the inner ear of the chick embryo, NGFR mRNA expression shows an alternating pattern in mesenchymal and epithelial tissues. NGFR mRNA is heavily expressed in the mesenchyme surrounding the otocyst (E2 –3), ceases at E3 –5, and reappears in a thin layer of mesenchymal cells surrounding the membraneous epithelia (E5 –13). In the otocyst epithelium, NGFR mRNA expression develops in one anterior and one posterior focus at E3 –4.5. NGFR mRNA is expressed in the primordia of the ampullary cristae (E5 –7) and possibly the anlage of the utricle; label transiently concentrates in the planum semilunatum of the cristae ampullares and in superior portions of the semicircular canals at E9, but is not seen in differentiating hair cells. In the acoustic ganglion, NGFR mRNA expression begins at E4; at the same time, the first peripheral acoustic nerve processes penetrate the otic epithelium (E4 –4.5). The acoustic ganglia remain weakly NGFR mRNA-labeled in the posthatch animal. In the rat embryo, NGFR immunoreactivity is present in the auditory placode at E9, in the periotic mesenchyme at E9 –10, and in the medial half of the otocyst at E10 –11. At E12, epithelial NGFR expression becomes restricted anteriorly and posteriorly in a pattern similar to that of the chick otocyst and ceases at E13. NGFR immunoreactivity appears transiently in pillar cells of the cochlea in the third week of gestation. NGFR and NGFR mRNA is expressed after Ell in the acoustic ganglia. While NGFR transcripts are expressed in the cochlear ganglion cell bodies, NGFR protein becomes restricted to neuronal processes by the third week of gestation. The vestibular, but not the cochlear (spiral) ganglia remain NGFR-labeled in the adult rat. Onset of NGFR mRNA expression in the acoustic ganglion during the period of afferent fiber ingrowth into the otocyst epithelium is consistent with the hypothesis that NGF-like molecules may have a neurotrophic function for acoustic ganglion cells. Transient expression of NGFRs in secretory cells of the vestibular endorgan and pillar cells in the organ of Corti implicate a role for neurotrophins in the differentiation of these epithelial cell types.

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Alvarez, 1989, Cell proliferation during early development of the chick embryo otic anlage: quantitative comparison of migratory and nonmigratory regions of the otic epithelium, J. comp. Neurol, 290, 278, 10.1002/cne.902900208

Alvarez, 1990, Shaping, invagination, and closure of the chick embryo otic vesicle: scanning electron microscopic and quantitative study, Anat. Rec, 228, 315, 10.1002/ar.1092280311

Amerlinck, 1930, Nouvelles recherches sur l’histogenese et la struture du labyrinthe membraneux de l’oreille des oiseaux, Arch. Biol. (Liege), 40, 19

Angelborg, 1972, Supporting elements in the organ of Corti, Acta Otolaryngol. Suppl, 301, 49, 10.3109/00016487209122689

Angerer, 1981, Detection of poly A+RNA in sea urchin eggs and embryos by quantitative tn situ hybridization, Nucl. Acids Res, 9, 2819, 10.1093/nar/9.12.2819

Ard, 1982, Trophic interactions between the stato-acoustic ganglion of the chick embryo and its synaptic targets

Ard, 1985, Trophic interactions between the cochleovestibular ganglion of the chick embryo and its synaptic targets in culture, Neuroscience, 16, 151, 10.1016/0306-4522(85)90053-3

Baumann, 1947, 1. Développement et structure histologique du noyau tangentiel du nerf vestibulaire, compares a ceux du ganglion acoustique, chez un oiseau, Schweiz. Arch. Neurol. Psychiat, 59, 1

Bernd, 1989, Characterization and localization of nerve growth factor receptors in the embryonic otic vesicle and cochleovestibular ganglion, Devl Biol, 134, 11, 10.1016/0012-1606(89)90073-0

Bothwell, 1991, Keeping track of neurotrophin receptors, Cell, 65, 915, 10.1016/0092-8674(91)90540-F

Chandler, 1984, A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells, J. biol. Chem, 259, 6882, 10.1016/S0021-9258(17)39810-1

Cohen, 1978, The development of hair cells in the embryonic chick’s basilar papilla, Acta Otolaryngol, 86, 342, 10.3109/00016487809124756

Corwin, 1988, Regeneration of hair cells after acoustic trauma, Science, 240, 1772, 10.1126/science.3381100

Cox, 1984, Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes, Devl Biol, 101, 485, 10.1016/0012-1606(84)90162-3

D’Amico-martel, 1982, Temporal patterns of neurogenesis in avian cranial sensory and autonomic ganglia, Am. J. Anat, 163, 351, 10.1002/aja.1001630407

D’Amico-martel, 1983, Contributions of placodal and neural crest cells to avian cranial peripheral ganglia, Am. J. Anat, 166, 445, 10.1002/aja.1001660406

Davies, 1985, The cranial sensory ganglia in culture: differences in the response of placode-denved and neural crest-derived neurons to nerve growth factor, Devl Biol, 111, 62, 10.1016/0012-1606(85)90435-X

Després, 1988, Immunohistochemical localisation of nerve growth factor-like protein in the organ of Corti of the developing rat, Neurosci Lett, 85, 5, 10.1016/0304-3940(88)90418-1

Després, 1991, Immunohistochemical localization of nerve growth factor receptor in the cochlea and in the brainstem of the perinatal rat, Hearing Res, 52, 157, 10.1016/0378-5955(91)90195-F

Detwiler, 1950, The role of the medulla in the differentiation of the otic vesicle, J. exp. Zool, 113, 179, 10.1002/jez.1401130108

Dohlman, 1964, Secretion and absorption of endolymph, Ann Otol. Rhinol. Lar, 73, 708, 10.1177/000348946407300311

Finn, 1987, Immunohistochemical evidence for the distribution of nerve growth factor in the embryonic mouse, J. Neurocytol, 16, 639, 10.1007/BF01637656

Frenkel, 1990, Nerve growth factor in skeletal tissues of the embryonic chick, Cell Tissue Res, 260, 507, 10.1007/BF00297230

Friedmann, 1969, The innervation of the developing fowl embryo otocyst m vivo and in vitro, Acta Otolaryngol, 67, 224, 10.3109/00016486909125447

Fuchs, 1923, Die Entwicklung des hâutigen Labyrinths beirn Kiebitz (Vanellus cristatus). Ein Beitrag zur Entwicklungsgeschichte des Gehôrorgans der VOgel, Z. Anat. Entwicklungsgesch, 69, 205, 10.1007/BF02593696

Ginzberg, 1979, Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium, Devl Biol, 68, 110, 10.1016/0012-1606(79)90247-1

Ginzberg, 1980, Synaptogenesis in the vestibular sensory epithelium of the chick embryo, J.Neurocytol, 9, 405, 10.1007/BF01181545

Guareschi, 1930, Studi sullo sviluppo dell’otocisti degli anfibi anuri, Wihelm Roux Arch. EntwMech. Org, 122, 179, 10.1007/BF00576972

Hall, 1939, On the duration of the polarization process in the ear primordium of embryos of Amblystoma punctatum (Linn, J. exp. Zool, 82, 173, 10.1002/jez.1400820202

Hall, 1941, Reversal of the polarization in the ear primordium of Amblystoma punctatum (Linn, J. exp. Zool, 86, 141, 10.1002/jez.1400860109

Hallbook, 1990, Expression of nerve growth factor receptor mRNA during early development of the chicken embryo: emphasis on cranial ganglia, Development, 108, 693, 10.1242/dev.108.4.693

Hamburger, 1951, A series of normal stages in the development of the chick embryo, J. Morph, 88, 49, 10.1002/jmor.1050880104

Harrison, 1936, Relations of symmetry in the developing ear of Amblystoma punctatum, Proc. natn. Acad. Sci. U.S.A, 22, 238, 10.1073/pnas.22.4.238

Hauger, 1989, Trophic support of the developing cochleovestibular ganglion by its peripheral target in vitro does not depend on neural cell division, Neuroscience, 33, 241, 10.1016/0306-4522(89)90203-0

Hemond, 1986, A study of the temporal and spatial sequence of the sensory innervation of the chick auditory receptor, Soc. Neurosci. Abstr, 12, 1209

Hempstead, 1991, High affinity NGF binding requires co-expression of the trk proto-oncogene and the low-affinity NGF receptor, Nature

Heuer, 1990, Structure and developmental expression of the chicken NGF receptor, Devl Biol, 137, 283, 10.1016/0012-1606(90)90255-H

Hohn, 1990, Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family, Nature, 344, 339, 10.1038/344339a0

Johnson, 1988, Expression and possible functions of nerve growth factor receptors on Schwann cells, Trends Neurosci, 7, 299, 10.1016/0166-2236(88)90090-2

Kaan, 1926, Experiments on the development of the ear of Amblystoma punctatum, J. exp. Zool, 46, 13, 10.1002/jez.1400460103

Katayama, 1989, Cell production in the chicken cochlea, J. comp. Neurol, 281, 129, 10.1002/cne.902810110

Kikuchi, 1965, The development of the organ of Corti in the mouse, Acta Otolaryngol, 60, 207, 10.3109/00016486509127003

Kimura, 1964, Secretory epithelial linings in the ampullae of the guinea pig labyrinth, Acta Otolaryngol. (Stockh.), 57, 517, 10.3109/00016486409137114

Knowlton, 1967, Correlation of the development of membranous and bony labyrinths, acoustic ganglion, nerves and brain centers of the chick embryo, J. Morph, 121, 179, 10.1002/jmor.1051210302

Koh, 1989, Localization of nerve growth factor receptor messenger RNA and protein in the adult rat brain, Expl Neurol, 106, 209, 10.1016/0014-4886(89)90154-4

Kuratani, 1988, Early development of the facial nerve in the chick embryo with special reference to the development of the chorda tympani, Am. J. Anat, 182, 169, 10.1002/aja.1001820207

Lefebvre, 1990, Neuronotrophic effect of developing otic vesicle on cochleo-vestibular neurons: evidence for nerve growth factor involvement, Brain Res, 507, 254, 10.1016/0006-8993(90)90279-K

Lehnert, 1988, Embryonic expression of TGF beta type-1 RNA suggests both parakrine and autocrine mechanisms of action, Development, 104, 263, 10.1242/dev.104.2.263

Lenoir, 1980, Cochlear receptor development in the rat with emphasis on synaptogenesis, Anat. Embryol, 160, 253, 10.1007/BF00305106

Li, 1978, The fate mapping of the the eleventh and twelfth day mouse otocyst: an in vitro study of the sites of origin of the embryonic inner ear sensory structures, J. Morph, 157, 249, 10.1002/jmor.1051570302

Lindsay, 1985, Differences and similarities in the neurotrophic growth factor requirements of sensory neurons derived from neural crest and neural placode, J. Cell Set. Suppl, 3, 115, 10.1242/jcs.1985.Supplement_3.12

Maisonpierre, 1990, Neurotrophin-3: a neurotrophic factor related to NGF and BDNF, Science, 247, 1446, 10.1126/science.2321006

Mayer, 1990, The role of nerve growth factor in the development of the inner ear: preliminary studies, Assoc. Res. Otolaryngol. Abstr, 13, 66

Mbœne, 1988, Early innervation and differentiation of hair cells in the vestibular epithelia of mouse embryos: SEM and TEM study, Anat. Embryol, 177, 331, 10.1007/BF00315841

McPhee, 1986, Epithelial-mesenchymal tissue interactions guiding otic capsule formation: the role of the otocyst, J. Embryol. exp. Morph, 97, 1

Meier, 1978, Development of the embryonic chick otic placode, Anat. Rec, 191, 447, 10.1002/ar.1091910405

Melton, 1984, Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promotor, Nucl. Acids Res, 12, 7035, 10.1093/nar/12.18.7035

Noden, 1984, The use of chimeras in analyses of craniofacial development, In Chimeras in Developmental Biology, 241

Norris, 1892, Studies on the development of the ear of Amblystoma, J. Morph, 7, 23, 10.1002/jmor.1050070103

Obata, 1988, Molecular differentiation of the otic vesicle and neural tube in the chick embryo demonstrated by monoclonal antibodies, Neurosci. Res, 6, 131, 10.1016/0168-0102(88)90015-6

Orr, 1975, A light and electron microscopic study of the embryonic chick otocyst. The effects of trypsin and Ca- and Mg-free salt solution, Devl Biol, 47, 325, 10.1016/0012-1606(75)90287-0

Pearson, 1983, Effects of antibodies to nerve growth factor on intrauterine development of derivatives of cranial neural crest and placode in the guinea pig, Devl Biol, 96, 32, 10.1016/0012-1606(83)90308-1

Perkins, 1975, A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarski optics, J. comp. Neurol, 163, 129, 10.1002/cne.901630202

Pioro, 1990, Distribution of nerve growth factor receptor-like immunoreactivity in the adult rat central nervous system. Effect of colchicine and correlation with the cholinergic system, n. Brainstem, cerebellum and spinal cord, Neuroscience, 34, 89, 10.1016/0306-4522(90)90305-N

Proctor, 1967, Understanding hereditary nerve deafness, Arch. Otolaryngol, 85, 23, 10.1001/archotol.1967.00760040025007

Radeke, 1987, Gene transfer and molecular cloning of the rat nerve growth factor receptor, Nature, 325, 593, 10.1038/325593a0

Ratvich, 1987, Nerve growth factor (NGF) receptor expression in chicken cranial development, J. comp. Neurol, 256, 229, 10.1002/cne.902560204

Ramon Y Cajal, 1929, Studies on Vertebrate Neurogenesis

Raphael, 1987, Modulation of intermediate-filament expression in developing cochlear epithelium, Differentiation, 35, 151, 10.1111/j.1432-0436.1987.tb00163.x

Raphael, 1988, The modulation of cell adhesion molecule expression and intercellular junction formation in the developing avian inner ear, Devl Biol, 128, 222, 10.1016/0012-1606(88)90284-9

Represa, 1989, Nerve growth factor and serum differentially regulate development of the embryonic otic vesicle and cochleovestibular ganglion in vitro, Devl Biol, 134, 21, 10.1016/0012-1606(89)90074-2

Represa, 1988, Bombesin and other growth factors activate cell profiferation on chick otic vesicles in culture, Development, 103, 87, 10.1242/dev.103.1.87

Represa, 1991, Temporal pattern of nerve growth factor receptor expression in the sensory epithelium of the developing quail inner ear, Assoc. Res. Otolaryngol. Abstr, 14, 136

Richardson, 1987, Expression of cell adhesion molecules during embryonic induction. III. Development of the otic placode, Devl Biol, 119, 217, 10.1016/0012-1606(87)90223-5

Rodriguez-Tebar, 1990, Binding of brain-derived neurotrophic factor to the nerve growth factor receptor, Neuron, 4, 487, 10.1016/0896-6273(90)90107-Q

Romanoff, 1960, The Avian Embryo

Rubel, 1978, Ontogeny of structure and function in the vertebrate auditory system, In Handbook of Sensory Physiology, 135

Ryals, 1988, Hair cell regeneration after acoustic trauma in adult Cotumix quail, Science, 240, 1774, 10.1126/science.3381101

Seilheimer, 1987, Regulation of neural cell adhesion molecule expression on cultured Schwann cells by nerve growth factor, EMBO J, 6, 1611, 10.1002/j.1460-2075.1987.tb02408.x

Swanson, 1990, Epithelial autonomy in the development of the inner ear of a bird embryo, Devl Biol, 137, 243, 10.1016/0012-1606(90)90251-D

Taniuchi, 1986, Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties, J. Neurosci, 8, 664, 10.1523/JNEUROSCI.08-02-00664.1988

Trampusch, 1941, On ear-induction, Acta Need. Morphol, 4, 195

Van Campenhout, 1937, Le développement du système nerveux crânien chez le poulet, Arch. biol. (Liege), 48, 611

Van De Water, 1976, Effects of removal of the statoacoustic ganglion complex upon the growing otocyst, Ann. Otol. Rhinol. Laryngol, 85, 1

Van De Water, 1988, Tissue interactions and cell differentiation: neurone-sensory cell interaction during otic development, Development, 103, 185, 10.1242/dev.103.Supplement.185

Van De Water, 1991, Nerve growth factor in the developing auditory system of the mouse: immunolocalization, binding and biological effects, Assoc. Res. Otolaryngol. Abstr, 14, 125

Van De Water, 1984, Neurotrophic interactions during in vitro development of the inner ear, Ann. Otol. Rhinol. Laryngol, 93, 558, 10.1177/000348948409300606

Vazquez-Nin, 1968, Electron microscope study of the developing nerve terminals in the acoustic organs of the chick embryo. Z, Zellforsch, 92, 325, 10.1007/BF00455590

Visintini, 1939, 7. Relazione tra differenziazione strutturale e funzionale dei centri e delle vie nervose nell’embrione di polio, Schweiz. Arch. Neurol. Psychiatr, 44, 119

Von Bartheld, 1990, Development and innervation of the paratympanic organ (Vitali organ) in chick embryos, Brain Behav. Evol, 35, 1, 10.1159/000115851

Von Bartheld, 1990, Neuronal tracing with Dil: decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis, J. Histochem. Cytochem, 38, 725, 10.1177/38.5.2185313

Von Bartheld, 1990, Expression of nerve growth factor (NGF) receptor mRNA in the otocyst of chicken embryos, Assoc. Res. Otolaryngol. Abstr, 13, 3

Warr, 1986, Organization of efferent fibers: the lateral and medial olivocochlear systems, In Neurobiology of Hearing, 333

Wheeler, 1990, Sites of NGF and NGFR mRNA synthesis in the developing rat embryo, Soc. Neurosci. Abstr, 16, 988

White, 1983, The dual origin of the olivocochlear bundle in the albino rat, J. comp. Neurol, 219, 203, 10.1002/cne.902190206

Whitehead, 1985, The development of innervation patterns in the avian cochlea, Neuroscience, 14, 255, 10.1016/0306-4522(85)90177-0

Whitehead, 1985, The growth of cochlear fibers and the formation of synaptic endings in the avian inner ear: a study with the electron microscope, Neuroscience, 14, 277, 10.1016/0306-4522(85)90178-2

Wilkinson, 1989, Expression pattern of the FGF-related proto-oncogene int-2 suggests multiple roles in fetal development, Development, 105, 131, 10.1242/dev.105.1.131

Wilkinson, 1988, Expression of the FGF-related proto-oncogene int-2 during gastrulation and neurulation in the mouse, EMBO J, 7, 691, 10.1002/j.1460-2075.1988.tb02864.x

Windle, 1939, Neurofibrillar development in the central nervous system of chick embryos up to 5 days’ incubation, J. comp. Neurol, 63, 431, 10.1002/cne.900630304

Wyatt, 1990, Expression of the NGF receptor gene in sensory neurons and their cutaneous targets prior to and during innervation, Neuron, 4, 421, 10.1016/0896-6273(90)90054-J

Yan, 1988, An immunohistochemical study of the nerve growth factor receptor in developing rats, J. Neurosci, 8, 3481, 10.1523/JNEUROSCI.08-09-03481.1988

Yntema, 1950, An analysis of induction of the ear from foreign ectoderm in the salamander embryo, J. exp. Zool, 113, 211, 10.1002/jez.1401130110

Yntema, 1955, Ear and nose, In Analysis of Development, 415

Zhou, 1987, The effect of target tissues on survival and differentiation of mammalian statoacoustic ganglion neurons in organ culture, Acta Otolaryngol. (Stockh.), 104, 90, 10.3109/00016488709109052

Zimmermann, 1983, Nerve growth factor (NGF) receptors on glial cells. Cell-cell interaction between neurons and Schwann cells in cultures of chick sensory ganglia, EMBO J, 2, 879, 10.1002/j.1460-2075.1983.tb01517.x