Expression of brain-derived neurotrophic factor and its receptor mRNA in the vestibuloauditory system of the bullfrog

Brain-derived neurotrophic factor (BDNF) is a neurotrophin which has been suggested to play a crucial role in the development and maintenance of the inner ear. In the present study, we investigated the expression of mRNAs of BDNF and its high-affinity receptor trkB in the vestibuloauditory system of the adult bullfrog. In situ hybridization was performed using riboprobes transcribed from Xenopus BDNF and trkB cDNA clones. BDNF mRNA was expressed in the sensory epithelia of the ampullary cristae, utricular and saccular maculae, lagena, and amphibian and basilar papillae. Strong hybridization for BDNF mRNA was also found in neuron somata of the vestibuloauditory nuclear complex. trkB mRNA was detected in the sensory epithelia of all vestibular and auditory endorgans. High levels of both BDNF and trkB mRNAs were found in vestibuloauditory ganglion cells. These results support the hypothesis that BDNF participates in the maintenance of vestibuloauditory neurons and may be important for the trophic regulation of vestibular and auditory sensory epithelia in this animal model.

[1]  M. F. Orr,et al.  Histogenesis of sensory epithelium in reaggregates of dissociated embryonic chick otocysts. , 1968, Developmental biology.

[2]  G. Moonen,et al.  Peripheral and central target-derived trophic factor(s) effects on auditory neurons , 1992, Hearing Research.

[3]  M. Barbacid,et al.  The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain , 1990, Cell.

[4]  H. Thoenen,et al.  Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. , 1985, Developmental biology.

[5]  M. Barbacid,et al.  trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3 , 1991, Cell.

[6]  H. Silverstein,et al.  Superior vestibular and “singular nerve” section — Animal and clinical studies , 1973, The Laryngoscope.

[7]  H. Spoendlin,et al.  Retrograde degeneration of the cochlear nerve. , 1975, Acta oto-laryngologica.

[8]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[9]  M. Bothwell,et al.  Expression of BDNF and NT-3 mRNA in hair cells of the organ of Corti: Quantitative analysis in developing rats , 1994, Hearing Research.

[10]  R. Stewart,et al.  Neurotrophin-4/5, brain-derived neurotrophic factor, and neurotrophin-3 promote survival of cultured vestibular ganglion neurons and protect them against neurotoxicity of ototoxins. , 1995, Journal of neurobiology.

[11]  P. Distefano,et al.  trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor , 1991, Cell.

[12]  M. Bothwell,et al.  Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons , 1992, Neuron.

[13]  J. T. Corwin,et al.  Supporting cells in avian vestibular organs proliferate in serum-free culture , 1993, Hearing Research.

[14]  E. Rubel,et al.  Diffusible factors regulate hair cell regeneration in the avian inner ear. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[15]  L. Olson,et al.  Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family , 1990, Neuron.

[16]  H. Thoenen,et al.  The response of chick sensory neurons to brain-derived neurotrophic factor , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  R. A. Baird,et al.  Hair cell regeneration in the bullfrog vestibular otolith organs following aminoglycoside toxicity , 1993, Hearing Research.

[18]  C. Matesz Central projection of the VIIIth cranial nerve in the frog , 1979, Neuroscience.

[19]  L. Belluscio,et al.  Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. , 1990, Science.

[20]  E. Robertis Submicroscopic changes of the synapse after nerve section in the acoustic ganglion of the guinea pig; an electron microscope study. , 1956 .

[21]  R. R. Capranica,et al.  Auditory responses from the saccule: further evidence for the mechanical origin of inhibition , 1974 .

[22]  Rudolf Jaenisch,et al.  Complementary roles of BDNF and NT-3 in vestibular and auditory development , 1995, Neuron.

[23]  J. Aran,et al.  Spiral ganglion changes after massive aminoglycoside treatment in the guinea pig. Counts and ultrastructure. , 1982, Acta oto-laryngologica.

[24]  B. Vidić,et al.  Survey of the Development of Laryngeal Epithelium , 1976, The Annals of otology, rhinology, and laryngology.

[25]  Rudolf Jaenisch,et al.  Mice lacking brain-derived neurotrophic factor develop with sensory deficits , 1994, Nature.

[26]  E. Shooter,et al.  Gene transfer and molecular cloning of the rat nerve growth factor receptor , 1987, Nature.

[27]  H. Spoendlin,et al.  LI Electronmicroscopic Study of the Efferent and Afferent Innervation of the Organ of Corti in the Cat , 1963, The Annals of otology, rhinology, and laryngology.

[28]  V. Honrubia,et al.  Central projections of primary vestibular fibers in the bullfrog: I. The vestibular nuclei , 1985, The Laryngoscope.

[29]  T. Water Effects of removal of the statoacoustic ganglion complex upon the growing otocyst. , 1976 .

[30]  T. R. Van De Water,et al.  The effect of target tissues on survival and differentiation of mammalian statoacoustic ganglion neurons in organ culture. , 1987, Acta Oto-Laryngologica.

[31]  R R Stewart,et al.  Neurotrophin-4/5 enhances survival of cultured spiral ganglion neurons and protects them from cisplatin neurotoxicity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  R. Vandlen,et al.  Neurotrophin-4/5 is a mammalian-specific survival factor for distinct populations of sensory neurons , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. Goeddel,et al.  Neurotrophin-5: A novel neurotrophic factor that activates trk and trkB , 1991, Neuron.

[34]  M. Saarma,et al.  Brain-derived neurotrophic factor and neurotrophin 3 mRNAs in the peripheral target fields of developing inner ear ganglia. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Ard,et al.  Trophic interactions between the cochleovestibular ganglion of the chick embryo and its synaptic targets in culture , 1985, Neuroscience.

[36]  H. Thoenen,et al.  Purification of a new neurotrophic factor from mammalian brain. , 1982, The EMBO journal.

[37]  E. Rubel,et al.  Expression of nerve growth factor (NGF) receptors in the developing inner ear of chick and rat. , 1991, Development.

[38]  G. Moonen,et al.  Neurotrophins affect survival and neuritogenesis by adult injured auditory neurons in vitro. , 1994, Neuroreport.

[39]  T. Hunter,et al.  trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors , 1991, Molecular and cellular biology.

[40]  C. Ibáñez,et al.  Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in xenopus ovary , 1991, Neuron.

[41]  Regeneration of the eighth cranial nerve. III. Central projections of the primary afferent fibers from individual vestibular receptors in the bullfrog , 1989, The Laryngoscope.

[42]  A. Davies,et al.  Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. , 1993, Development.

[43]  P. Ernfors,et al.  Developmentally Regulated Expression of HDNF/NT‐3 mRNA in Rat Spinal Cord Motoneurons and Expression of BDNF mRNA in Embryonic Dorsal Root Ganglion , 1991, The European journal of neuroscience.

[44]  M. Barbacid,et al.  The trk proto-oncogene encodes a receptor for nerve growth factor , 1991, Cell.

[45]  J. Wersäll,et al.  Experimental studies on the nerve--sensory cell relationship during degeneration and regeneration in ampullar nerves of the frog labyrinth. , 1975, Acta oto-laryngologica. Supplementum.

[46]  Regeneration of the eighth cranial nerve II. Physiologic verification in the bullfrog , 1987, The Laryngoscope.

[47]  M. Anniko,et al.  Embryogenesis of the inner ear , 2005, Archives of oto-rhino-laryngology.

[48]  Y. Barde,et al.  Binding of brain-derived neurotrophic factor to the nerve growth factor receptor , 1990, Neuron.

[49]  M. Huntsman,et al.  Comparison of mammalian, chicken and Xenopus brain‐derived neurotrophic factor coding sequences , 1991, FEBS letters.

[50]  J T Corwin,et al.  Regenerated hair cells can originate from supporting cell progeny: evidence from phototoxicity and laser ablation experiments in the lateral line system , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  S. Fraser,et al.  BDNF in the development of the visual system of Xenopus , 1994, Neuron.

[52]  C. Fernández,et al.  Pathological and functional changes following hemisection of the lateral ampullary nerve. , 1966, Acta oto-laryngologica.

[53]  Y. Barde,et al.  Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family , 1990, Nature.

[54]  M. Saarma,et al.  Coordinated expression and function of neurotrophins and their receptors in the rat inner ear during target innervation , 1994, Hearing Research.

[55]  M. Saarma,et al.  Expression patterns of neurotrophin and their receptor mRNAs in the rat inner ear , 1993, Hearing Research.

[56]  Y. Barde,et al.  Regional distribution of brain‐derived neurotrophic factor mRNA in the adult mouse brain. , 1990, The EMBO journal.

[57]  R. R. Capranica,et al.  An anatomical and physiological study of regeneration of the eighth nerve in the leopard frog , 1981, Brain Research.

[58]  T. Hunter,et al.  The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor , 1991, Cell.

[59]  M. Avila,et al.  Brain-derived neurotrophic factor and neurotrophin-3 support the survival and neuritogenesis response of developing cochleovestibular ganglion neurons , 1993 .

[60]  V Honrubia,et al.  Regeneration of the eighth cranial nerve. i. anatomic verification in the bullfrog , 1986, The Laryngoscope.

[61]  I. Lopez,et al.  Intraotic Administration of Gentamicin: A New Method to Study Ototoxicity in the Crista Ampullaris of the Bullfrog , 1997, The Laryngoscope.

[62]  F. Sohrabji,et al.  Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[63]  G. Yancopoulos,et al.  A BDNF autocrine loop in adult sensory neurons prevents cell death , 1995, Nature.

[64]  A. Ross,et al.  Gene transfer and molecular cloning of the human NGF receptor. , 1986, Science.

[65]  D. Kaplan,et al.  The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. , 1991, Science.

[66]  J. T. Corwin,et al.  Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[67]  I. Fariñas,et al.  Severe sensory and sympathetic deficits in mice lacking neurotrophin-3 , 1994, Nature.

[68]  M. Bothwell,et al.  Neurotrophin and neurotrophin receptor mRNA expression in developing inner ear , 1994, Hearing Research.

[69]  M. Igarashi,et al.  Dynamic equilibrium in squirrel monkeys after unilateral and bilateral labyrinthectomy. , 1970, Acta oto-laryngologica.