Pituitary adenylyl cyclase-activating polypeptide (PACAP) and its receptor (PAC1-R) are positioned to modulate afferent signaling in the cochlea

Neuroscience

Volumn 142, Issue 1, 2006, Pages 139-164

  Drescher, M J ^a   Drescher, D G ^a   Khan, K M ^b   Hatfield, J S ^c   Ramakrishnan, N A ^a   Abu Hamdan, M D ^a   Lemonnier, L A ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AGA KHAN UNIVERSITY   (Pakistan)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

adrenergic innervation; afferent innervation; cochlea; efferent innervation; immunolocalization; organ of Corti

Indexed keywords

BIOCHEMICAL MARKER; CATECHOLAMINE; CHOLINE ACETYLTRANSFERASE; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR; SYNAPTOPHYSIN;

ADRENERGIC NERVE; ADRENERGIC TRANSMISSION; AFFERENT NERVE GROUP 1; ANIMAL TISSUE; ARTICLE; BRIGHT FIELD MICROSCOPY; CATECHOLAMINE RELEASE; CATECHOLAMINERGIC SYSTEM; CELL SECRETION; CELL TYPE; CELLULAR DISTRIBUTION; COCHLEA; COCHLEAR NERVE; CONTROLLED STUDY; CORTI ORGAN; DENDRITE; EFFERENT NERVE; EXCITOTOXICITY; EXTERNAL AUDITORY CANAL; HAIR CELL; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; INNER EAR; MORPHOLOGY; NERVE ENDING; NERVE FIBER; NEUROFILAMENT; NEUROMODULATION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SENSORY NERVE; SIGNAL TRANSDUCTION; SPIRAL GANGLION;

AFFERENT PATHWAYS; ANIMALS; COCHLEA; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; NERVE TISSUE PROTEINS; NEURONS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I;

EID: 33748477252     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.05.065     Document Type: Article

References (73)

1. Abu-Hamdan M.D., Drescher M.J., Ramakrishnan N.A., Khan K.M., Toma V.S., Hatfield J.S., and Drescher D.G. Pituitary adenylyl cyclase-activating polypeptide (PACAP) and its receptor (PAC1-R) in the cochlea: evidence for specific transcript expression of PAC1-R splice variants in microdissected cochlear subfractions. Neuroscience 140 (2006) 147-161
2. Aguila-Mansilla N., Kedzierski W., and Porter J.C. Localization of a defect in hypothalamic dopaminergic neurons of the aged brain that results in impaired PKA-dependent activation of tyrosine hydroxylase. J Pharmacol Exp Ther 267 (1993) 171-175
3. Anderson S.T., Kusters D.H.L., Clarke I.J., Pow D.V., and Curlewis J.D. Expression of pituitary adenylate cyclase activating polypeptide type 1 receptor (PAC1R) in the ewe hypothalamus: distribution and colocalization with tyrosine hydroxylase-immunoreactive neurones. J Neuroendocrinol 17 (2005) 298-305
4. Arimura A. Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems. Jpn J Physiol 48 (1998) 301-331
5. Berglund A.M., and Ryugo D.K. A monoclonal antibody labels type II neurons of the spiral ganglion. Brain Res 383 (1986) 327-332
6. Corbitt J., Hagerty T., Fernandez E., Morgan W.W., and Strong R. Transcriptional and post-transcriptional regulation of tyrosine hydroxylase messenger RNA in PC12 cells during persistent stimulation by VIP and PACAP38: differential regulation by protein kinase A and protein kinase C-dependent pathways. Neuropeptides 36 (2002) 34-45
7. D'Aldin C., Puel J.L., Leducq R., Crambes O., Eybalin M., and Pujol R. Effects of a dopaminergic agonist in the guinea pig cochlea. Hear Res 90 (1995) 202-211
8. Daniel P.B., Kieffer T.J., Leech C.A., and Habener J.F. Novel alternatively spliced exon in the extracellular ligand-binding domain of the pituitary adenylate cyclase-activating polypeptide (PACAP) type 1 receptor (PAC1R) selectively increases ligand affinity and alters signal transduction coupling during spermatogenesis. J Biol Chem 276 (2001) 12938-12944
9. Dau J., and Wenthold R.J. Immunocytochemical localization of neurofilament subunits in the spiral ganglion of normal and neomycin-treated guinea pigs. Hear Res 42 (1989) 253-263
10. Dautzenberg F.M., Mevenkamp G., Wille S., and Hauger R.L. N-terminal splice variants of the type I PACAP receptor: isolation, characterization and ligand binding/selectivity determinants. J Neuroendocrinol 11 (1999) 941-949
11. Dejda A., Sokolowska P., and Nowak J.Z. Neuroprotective potential of three neuropeptides PACAP, VIP, and PHI. Pharmacol Rep 57 (2005) 307-320
12. Drescher D.G., Drescher M.J., Khan K.M., and Hatfield J.S. Serotonin (5-HT) and norepinephrine (NE) in rat organ of Corti analyzed by HPLC and immunohistochemistry: Co-localization with synaptophysin in association with outer hair cells of the apical turn. Assoc Res Otolaryngol Abstr 26 (2003) 12
13. Drescher M.J., Kim S.Y., Hatfield J.S., and Drescher D.G. Expression of adenylyl cyclase isoforms in the mouse cochlea. Mol Biol Hear Deaf Abstr 2 (1995) 115
14. Elgoyhen A.B., Vetter D.E., Katz E., Rothlin C.V., Heinemann S.F., and Boulter J. α10: A determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory cells. Proc Natl Acad Sci U S A 98 (2001) 3501-3506
15. Eybalin M., Charachon G., and Renard N. Dopaminergic lateral efferent innervation of the guinea-pig cochlea: immunoelectron microscopy of catecholamine-synthesizing enzymes and effect of 6-hydroxydopamine. Neuroscience 54 (1993) 133-142
16. Fahrenkrug J., and Hannibal J. Neurotransmitters co-existing with VIP or PACAP. Peptides 25 (2004) 393-401
17. Falck B., Hillarp N.A., Thieme G., and Torp A. Fluorescence of catecholamines and related compounds condensed with formaldehyde. J Histochem Cytochem 10 (1962) 348
18. Fechner F.P., Nadol Jr. J.B., Burgess B.J., and Brown M.C. Innervation of supporting cells in the apical turns of the guinea pig cochlea is from type II afferent fibers. J Comp Neurol 429 (2001) 289-298
19. Felix D., and Ehrenberger K. The efferent modulation of mammalian inner hair cell afferents. Hear Res 64 (1992) 1-5
20. Figiel M., and Engele J. Pituitary adenylate cyclase-activating polypeptide (PACAP), a neuron-derived peptide regulating glial glutamate transport and metabolism. J Neurosci 20 (2000) 3596-3605
21. Groff J.A., and Liberman M.C. Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J Neurophysiol 90 (2003) 3178-3200
22. Hamelink C., Tjurmina O., Damadzic R., Young W.S., Weihe E., Lee H.W., and Eiden L.E. Pituitary adenylate cyclase-activating polypeptide is a sympathoadrenal neurotransmitter involved in catecholamine regulation and glucohomeostasis. Proc Natl Acad Sci U S A 99 (2002) 461-466
23. Hannibal J., Mikkelsen J.D., Clausen H., Holst J.J., Wulff B.S., and Fahrenkrug J. Gene expression of pituitary adenylate cyclase activating polypeptide (PACAP) in the rat hypothalamus. Regul Pept 55 (1995) 133-148
24. Hannibal J., Moller M., Ottersen O.P., and Fahrenkrug J. PACAP and glutamate are co-stored in the retinohypothalamic tract. J Comp Neurol 418 (2000) 147-155
25. Hannibal J. Pituitary adenylate cyclase-activating peptide in the rat central nervous system: an immunohistochemical and in situ hybridization study. J Comp Neurol 453 (2002) 389-417
26. Haycock J.W. Phosphorylation of tyrosine hydroxylase in situ at serine 8, 19, 31, and 40. J Biol Chem 265 (1990) 11682-11691
27. Haycock J.W. Short- and long-term regulation of tyrosine hydroxylase in chromaffin cells by VIP and PACAP. Ann N Y Acad Sci 805 (1996) 219-230
28. Hou X.-E., and Dahlström A. Synaptic vesicle proteins and neuronal plasticity in adrenergic neurons. Neurochem Res 25 (2000) 1275-1300
29. Housley G.D., and Ashmore J.F. Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc R Soc Lond B Biol Sci 244 (1991) 161-167
30. Jones N., Fex J., and Altschuler R.A. Tyrosine hydroxylase immunoreactivity identifies possible catecholaminergic fibers in the organ of Corti. Hear Res 30 (1987) 33-38
31. Kawano H., Shimozono M., Tono T., Miyata A., and Komune S. Expression of pituitary adenylate cyclase-activating polypeptide mRNA in the cochlea of rats. Mol Brain Res 94 (2001) 200-203
32. Khan K.M., Drescher M.J., Hatfield J.S., Khan A.M., and Drescher D.G. Muscarinic receptor subtypes are differentially distributed in the rat cochlea. Neuroscience 111 (2002) 291-302
33. Kimura R.S. Sensory and accessory epithelia of the cochlea. In: Friedmann I., and Ballantyne J. (Eds). Ultrastructural atlas of the inner ear (1984), Butterworths, London 101-132
34. Knipper M., Zimmermann U., Rohbock K., Köpschall I., and Zenner H.-P. Synaptophysin and GAP-43 proteins in efferent fibers of the inner ear during postnatal development. Dev Brain Res 89 (1995) 73-86
35. Liberman M.C., Dodds L.W., and Pierce S. Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol 301 (1990) 443-460
36. Liu D.-M., Cuevas J., and Adams D.J. VIP and PACAP potentiation of nicotinic ACh-evoked currents in rat parasympathetic neurons is mediated by G-protein activation. Eur J Neurosci 12 (2000) 2243-2251
37. Margiotta J.F., and Pardi D. Pituitary adenylate cyclase-activating polypeptide type 1 receptors mediate cyclic AMP-dependent enhancement of neuronal acetylcholine sensitivity. Mol Pharmacol 48 (1995) 63-71
38. Matsubara A., Laake J.H., Davanger S., Usami S., and Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci 16 (1996) 4457-4467
39. May V., Beaudet M.M., Parsons R.L., Hardwick J.C., Gauthier E.A., Durda J.P., and Braas K.M. Mechanisms of pituitary adenylate cyclase activating polypeptide (PACAP)-induced depolarization of sympathetic superior cervical ganglion (SCG) neurons. Ann N Y Acad Sci 865 (1998) 164-175
40. Miyata A., Arimura A., Dahl R.R., Minamino N., Uehara A., Jiang L., Culler M.D., and Coy D.H. Isolation of a novel 38 residue hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 164 (1989) 567-574
41. Miyata A., Jiang L., Dahl R.D., Kitada C., Kubo K., Fujino M., Minamino N., and Arimura A. Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP38). Biochem Biophys Res Commun 170 (1990) 643-648
42. Morio H., Tatsuno I., Hirai A., Tamura Y., and Saito Y. Pituitary adenylate cyclase-activating polypeptide protects rat-cultured cortical neurons from glutamate-induced cytotoxicity. Brain Res 741 (1996) 82-88
43. Morley B.J., Li H.-S., Hiel H., Drescher D.G., and Elgoyhen A.B. Identification of the subunits of the nicotinic cholinergic receptors in the rat cochlea using RT-PCR and in situ hybridization. Mol Brain Res 53 (1998) 78-87
44. Nadol Jr. J.B., and Burgess B.J. Supranuclear efferent synapses on outer hair cells and Deiters' cells in the human organ of Corti. Hear Res 81 (1994) 49-56
45. Nielsen H.S., Hannibal J., and Fahrenkrug J. Expression of pituitary adenylate cyclase activating polypeptide (PACAP) in the postnatal and adult rat cerebellar cortex. Neuroreport 9 (1998) 2639-2642
46. Onoue S., Endo K., Yajima T., and Kashimoto K. Pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal peptide attenuate glutamate-induced nNOS activation and cytotoxicity. Regul Pept 107 (2002) 43-47
47. Pantaloni C., Brabet P., Bilanges B., Dumuis A., Houssami S., Spengler D., Bockaert J., and Journot L. Alternative splicing in the N-terminal extracellular domain of the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor modulates receptor selectivity and relative potencies of PACAP-27 and PACAP-38 in phospholipase C activation. J Biol Chem 271 (1996) 22146-22151
48. Pardi D., and Margiotta J.F. Pituitary adenylate cyclase-activating polypeptide activates a phospholipase C-dependent signal pathway in chick ciliary ganglion neurons that selectively inhibits alpha7-containing nicotinic receptors. J Neurosci 19 (1999) 6327-6337
49. Pisegna J.R., and Wank S.A. Molecular cloning and functional expression of the pituitary adenylate cyclase-activating polypeptide type I receptor. Proc Natl Acad Sci U S A 90 (1993) 6345-6349
50. Puel J.L. Chemical synaptic transmission in the cochlea. Prog Neurobiol 47 (1995) 449-476
51. Puel J.L., Pujol R., Tribillac F., Ladrech S., and Eybalin M. Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity. J Comp Neurol 341 (1994) 241-256
52. Puel J.L., Safieddine S., Gervais D'Aldin C., Eybalin M., and Pujol R. Synaptic regeneration and functional recovery after excitotoxic injury in the guinea pig cochlea. C R Acad Sci III 318 (1995) 67-75
53. Pugh P.C., and Margiotta J.F. Nicotinic acetylcholine receptor agonists promote survival and reduce apoptosis of chick ciliary ganglion neurons. Mol Cell Neurosci 15 (2000) 113-122
54. Pujol R., Lenoir M., Robertson D., Eybalin M., and Johnstone B.M. Kainic acid selectively alters auditory dendrites connected with cochlear inner hair cells. Hear Res 18 (1985) 145-151
55. Pujol R., and Puel J.L. Excitotoxicity, synaptic repair, and functional recovery in the mammalian cochlea: a review of recent findings. Ann N Y Acad Sci 884 (1999) 249-254
56. Raphael Y., and Altschuler R.A. Structure and innervation of the cochlea. Brain Res Bull 60 (2003) 397-422
57. Safieddine S., and Eybalin M. Triple immunofluorescence evidence for the coexistence of acetylcholine, enkephalins and calcitonin gene-related peptide within efferent (olivocochlear) neurons of rats and guinea-pigs. Eur J Neurosci 4 (1992) 981-992
58. Safieddine S., Prior A.M., and Eybalin M. Choline acetyltransferase, glutamate decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig. Eur J Neurosci 9 (1997) 356-367
59. Shintani N., Suetake S., Hashimoto H., Koga K., Kasai A., Kawaguchi C., Morita Y., Hirose M., Sakai Y., Tomimoto S., Matsuda T., and Baba A. Neuroprotective action of endogenous PACAP in cultured rat cortical neurons. Regul Pept 126 (2005) 123-128
60. Shioda S., Shuto Y., Somogyvári-Vigh A., Legradi G., Onda H., Coy D.H., Nakajo S., and Arimura A. Localization and gene expression of the receptor for pituitary adenylate cyclase-activating polypeptide in the rat brain. Neurosci Res 28 (1997) 345-354
61. Shioda S., Yada T., Muroya S., Uramura S., Nakajo S., Ohtaki H., Hori T., Shimoda Y., and Funahashi H. Functional significance of co-localization of PACAP and catecholamine in nerve terminals. Ann N Y Acad Sci 921 (2000) 211-217
62. Spengler D., Waeber C., Pantaloni C., Holsboer F., Bockaert J., Seeburg P.H., and Journot L. Differential signal transduction by five splice variants of the PACAP receptor. Nature 365 (1993) 170-175
63. Spoendlin H. Primary neurons and synapses. In: Friedmann I., and Ballantyne J. (Eds). Ultrastructural atlas of the inner ear (1984), Butterworths, London 133-164
64. 1-R) in reactive astrocytes. Mol Brain Res 115 (2003) 10-20
65. Taupenot L., Mahata M., Mahata S.K., and O'Connor D.T. Time-dependent effects of the neuropeptide PACAP on catecholamine secretion: stimulation and desensitization. Hypertension 34 (1999) 1152-1162
66. Trigueiros-Cunha N., Renard N., Humbert G., Tavares M.A., and Eybalin M. Catecholamine-independent transient expression of tyrosine hydroxylase in primary auditory neurons is coincident with the onset of hearing in the rat cochlea. Eur J Neurosci 18 (2003) 2653-2662
67. Tytell M., Gulley R.L., Wenthold R.J., and Lasek R.J. Fast axonal transport in auditory neurons of the guinea pig: a rapidly turned-over glycoprotein. Proc Natl Acad Sci U S A 77 (1980) 3042-3046
68. Usami S., Hozawa J., Tazawa M., Yoshihara T., Igarashi M., and Thompson G.C. Immunocytochemical study of catecholaminergic innervation in the guinea pig cochlea. Acta Otolaryngol Suppl 447 (1988) 36-45
69. Vaudry D., Gonzalez B.J., Basille M., Yon L., Fournier A., and Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52 (2000) 269-324
70. Wenthold R.J., and McGarvey M.L. Different polypeptides are rapidly transported in auditory and optic neurons. J Neurochem 39 (1982) 27-35
71. Wenthold R.J., and McGarvey M.L. Changes in rapidly transported proteins in the auditory nerve after hair cell loss. Brain Res 253 (1982) 263-269
72. Wiechers B., Gestwa G., Mack A., Carroll P., Zenner H.-P., and Knipper M. A changing pattern of brain-derived neurotrophic factor expression correlates with the rearrangement of fibers during cochlear development of rats and mice. J Neurosci 19 (1999) 3033-3042
73. NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J Neurosci 17 (1997) 7594-7605