Pituitary adenylate cyclase-activating polypeptide receptors during development: Expression in the rat embryo at primitive streak stage

Neuroscience

Volumn 93, Issue 1, 1999, Pages 375-391

  Zhou, C J ^a,b   Shioda, S ^b,c   Shibanuma, M ^d   Nakajo, S ^d   Funahashi, H ^b   Nakai, Y ^b   Arimura, A ^c   Kikuyama, S ^a  

^a WASEDA UNIVERSITY   (Japan)

^b SHOWA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c TULANE UNIVERSITY   (United States)

^d SHOWA UNIVERSITY   (Japan)

Author keywords

Development; Immunohistochemistry; In situ hybridization histochemistry; Pituitary adenylate cyclase activating polypeptide receptor (PAC1 receptor); Rat brain; RT PCR

Indexed keywords

HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RECEPTOR AFFINITY; RECEPTOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

ANIMALS; ANTISENSE ELEMENTS (GENETICS); FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; PITUITARY GLAND; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; RECEPTORS, PITUITARY HORMONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 0033000646     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00108-6     Document Type: Article

References (101)

1. Altman J. Postnatal development of the cerebellar cortex in the rat. J. comp. Neurol. 145:1972;353-396.
2. Arimura A. Tissue distribution of PACAP as determined by RIA: highly abundant in the rat brain and testes. Endocrinology. 129:1991;2787-2789.
3. Arimura A. Pituitary adenylate cyclase-activating polypeptide (PACAP): discovery and current status of research. Regul. Pept. 37:1992;287-303.
4. Arimura A. Receptors for pituitary adenylate cyclase-activating polypeptide. Comparison with vasoactive intestinal peptide receptors. Trends Endocr. Metab. 3:1992;288-294.
5. Arimura A., Shioda S. Pituitary adenylate cyclase-activating polypeptide (PACAP) and its receptors: neuroendocrine and endocrine interaction. Front. Neuroendocr. 16:1995;53-88.
6. Arimura A., Somogyvari-Vigh A., Fiore F. C. and Will C. (1993) Prevention of natural death of motoneurons by pituitary adenylate cyclase-activating polypeptide (PACAP) in chick embryo. Endocrine Society, 75th Annual Meeting, Abstr. 897.
7. Arimura A., Somogyvari-Vigh A., Weill C., Fiore F.C., Tatsuno I., Bay V., Brenneman D.E. PACAP functions as a neurotrophic factor. Ann. N. Y. Acad. Sci. 739:1994;228-243.
8. Banks W.A., Uchida D., Arimura A., Somogyvari-Vigh A., Shioda S. Transport of pituitary adenylate cyclase-activating polypeptide across the blood-brain barrier and the prevention of ischemia-induced death of hippocampal neurons. Ann. N. Y. Acad. Sci. 805:1996;270-279.
9. Basille M., Gonzalez B.J., Desrues L., Demas M., Fournier A., Vaudry H. Pituitary adenylate cyclase-activating polypeptide (PACAP) stimulates adenylyl cyclase and phospholipase C activity in rat cerebellar neuroblasts. J. Neurochem. 65:1995;1318-1324.
10. Basille M., Gonzalez B.J., Fournier A., Vaudry H. Ontogeny of pituitary adenylate cyclase-activating polypeptide (PACAP) receptors in the rat cerebellum: a quantitative autoradiographic study. Devl Brain Res. 82:1994;81-89.
11. Basille M., Gonzalez B.J., Leroux P., Jeandel L., Fournier A., Vaudry H. Localization and characterization of PACAP receptors in the rat cerebellum during development: evidence for a stimulatory effect of PACAP on immature cerebellar granule cells. Neuroscience. 57:1993;329-338.
12. Cauvin A., Robberecht P., De Neef P., Gourlet P., Vandermeers A., Vandermeers-Piret M.C., Christophe J. Properties and distribution of receptors for pituitary adenylate cyclase-activating polypeptide (PACAP) in rat brain and spinal cord. Regul. Pept. 35:1991;161-173.
13. Cavallaro S., Copani A., D'Agata V., Musco S., Petralia S., Ventra C., Stivala F., Travali S., Canonico P.L. Pituitary adenylate cyclase-activating polypeptide prevents apoptosis in cultured cerebellar granule neurons. Molec. Pharmac. 50:1996;60-66.
14. Cavallaro S., D'Agata V., Guardabasso V., Travali S., Stivala F., Canonico P.L. Differentiation induces pituitary adenylate cyclase-activating polypeptide receptor expression in PC-12 cells. Molec. Pharmac. 48:1995;56-62.
15. Chang J.Y., Korolev V.V., Wang J.-Z. Cyclic AMP and pituitary adenylate cyclase-activating polypeptide (PACAP) prevent programmed cell death of cultured rat cerebellar granule cells. Neurosci. Lett. 206:1996;181-184.
16. Chartel N., Tonon M.C., Vaudry H., Conlon J.M. Primary structure of frog pituitary adenylate cyclase activating polypeptide (PACAP) and effects of ovine PACAP on frog pituitary. Endocrinology. 129:1991;3367-3371.
17. Chatterjee T.K., Sharma R.V., Fisher R.A. Molecular cloning of a novel variant of the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor that stimulates calcium influx by activation of L-type calcium channels. J. biol. Chem. 271:1996;32,226-32,232.
18. Ciccarese S., Tommasi S., Vonghia G. Cloning and cDNA sequence of the rat X-chromosome linked phosphoglycerate kinase. Biochem. biophys. Res. Commun. 165:1989;1337-1344.
19. D'Agata V., Cavallara S., Stivala F., Travali S., Canonico P.L. Tissue-specific and developmental expression of pituitary adenylate cyclase-activating polypeptide (PACAP) receptors in rat brain. Eur. J. Neurosci. 8:1996;310-318.
20. Deutsch P.J., Schadlow V., Barzilai N. 38-Amino-acid form of pituitary adenylate cyclase-activating polypeptide induces process outgrowth in human neuroblastoma cells. J. Neurosci. Res. 35:1992;312-320.
21. Deutsch P.J., Sun Y. The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J. biol. Chem. 267:1992;5108-5113.
22. DiCicco-Bloom E., Deutsch P.J. Pituitary adenylate cyclase activating polypeptide (PACAP) potently stimulates mitosis, neuritogenesis and survival in cultured rat sympathetic neuroblasts. Regul. Pept. 37:1992;319.
23. Dow R.C., Bennie J., Fink G. Pituitary adenylate cyclase-activating peptide-38 (PACAP-38) is released into hypophysial portal blood in the normal male and female rat. J. Endocr. 142:1994;R1-R4.
24. Fridolf T., Sundler F., Ahren B. Pituitary adenylate cyclase activating polypeptide (PACAP): occurrence in rodent pancreas and effects on insulin and glucagon secretion in the mouse. Cell Tiss. Res. 269:1992;275-279.
25. Fukuhara C., Inouye S.I., Matsumoto Y., Tsujimoto G., Aoki K., Masuo Y. Pituitary adenylate cyclase-activating polypeptide rhythm in the rat pineal gland. Neurosci. Lett. 241:1998;115-118.
26. Garnica A.D., Chan W.Y. The role of the placenta in fetal nutrition and growth. J. Am. Coll. Nutr. 15:1996;206-222.
27. Gaytan F., Martinez-Fuentes A.J., Garcia-Navaro F., Vaudry H., Aguilar E. Pituitary adenylate cyclase-activating polypeptide (PACAP) immunolocalization in lymphoid tissues of the rat. Cell Tiss. Res. 276:1994;223-227.
28. Ghatei M.A., Takahashi K., Suzuki Y., Gardiner J., Jones P.M., Bloom S.R. Distribution, molecular characterization of pituitary adenylate cyclase-activating polypeptide and its precursor encoding messenger RNA in human and rat tissues. J. Endocr. 136:1993;159-166.
29. Gottschall P.E., Tatsuno I., Arimura A. Hypothalamic binding sites for pituitary adenylate cyclase-activating polypeptide: characterization and molecular identification. Fedn Proc. Fedn Am. Socs exp. Biol. 5:1991;194-199.
30. Gottschall P.E., Tatsuno I., Miyata A., Arimura A. Characterization and distribution of binding sites for the hypothalamic peptide, pituitary adenylate cyclase-activating polypeptide. Endocrinology. 127:1990;272-277.
31. Harmar A.J., Arimura A., Gozes I., Journot L., Laburthe M., Pisegna J.R., Rawlings S.R., Robberecht P., Said S.I., Sreedharan S.P., Wank S.A., Waschek J.A. International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmac. Rev. 50:1998;265-270.
32. Hashimoto H., Ishihara T., Shigemoto R., Mori K., Nagata S. Molecular cloning and tissue distribution of a receptor for pituitary adenylate cyclase-activating polypeptide. Neuron. 11:1993;333-342.
33. Hashimoto H., Nogi H., Mori K., Ohishi H., Shigemoto R., Yamamoto K., Matsuda T., Mizuno N., Nagata S., Baba A. Distribution of the mRNA for a pituitary adenylate cyclase-activating polypeptide receptor in the rat brain: an in situ hybridization study. J. comp. Neurol. 371:1996;567-577.
34. Hashimoto H., Yamamoto K., Hagigara N., Ogawa N., Nishino A., Aino H., Nogi H., Imanishi K., Matsuda T., Baba A. cDNA cloning of a mouse pituitary adenylate cyclase-activating polypeptide receptor. Biochim. biophys. Acta. 1281:1996;129-133.
35. Hill J.M., Agoston D.V., Gressens P., McCune S.K. Distribution of VIP mRNA and two distinct VIP binding sites in the developing rat brain: relation to ontogenic events. J. comp. Neurol. 342:1994;186-205.
36. Hosoya M., Onda H., Ogi K., Masuda Y., Miyamoto Y., Ohtaki T., Okazaki H., Arimura A., Fujino M. Molecular cloning and functional expression of rat cDNAs encoding the receptor for pituitary adenylate cyclase activating polypeptide (PACAP). Biochem. biophys. Res. Commun. 194:1993;133-143.
37. Jacobson M. (1991) Developmental Neurobiology, pp. 401-452. Plenum, New York.
38. Katsuura G., Dahl R.R., Miyata A., Arimura A. A novel hypothalamic neuropeptide with 38 residues (PACAP38) stimulates adenylate cyclase activity in pituitary cells, neurons and astrocytes. Soc. Neurosci. Abstr. 15:1989;1277.
39. Kaufman M. H. (1992) The Atlas of Mouse Development. Academic, London.
40. Kimura C., Ohkubo S., Ogi K., Hosoya M., Itoh Y., Onda H., Miyata A., Jiang L., Dahl R.R., Stibbs H.H., Arimura A., Fujino M. A novel peptide which stimulates adenylate cyclase: molecular cloning and characterization of the bovine and human cDNAs. Biochem. biophys. Res. Commun. 166:1990;81-89.
41. Kivipelto L., Absood A., Arimura A., Sundler F., Hakanson R., Panula P. The distribution of pituitary adenylate cyclase-activating polypeptide-like immunoreactivity is distinct from helodermin- and helospectin-like immunoreactivities in the rat brain. J. chem. Neuroanat. 5:1992;85-94.
42. Köves K., Arimura A., Gorcs T.G., Somogyvari-Vigh A. Comparative distribution of immunoreactive pituitary adenylate cyclase activating polypeptide (PACAP) and vasoactive intestinal polypeptide (VIP) in rat forebrain. Neuroendocrinology. 54:1991;159-169.
43. Köves K., Arimura A., Somogyvari-Vigh A., Miller J. Immunohistochemical demonstration of a novel hypothalamic peptide, pituitary adenylate cyclase activating polypeptide, in the ovine hypothalamus. Endocrinology. 127:1990;264-271.
44. Köves K., Lakatos A., Somogyvari-Vigh A., Fogel K., Kantor O., Gooz P., Jamali U.K., Grandier-Vazeille X., Arimura A. Effect of the lack of light impulses on the hypothalamic PACAP and C-fos immunoreactivities in rats. Neurobiology (Bp). 5:1997;389-402.
45. Lam H.C., Takahashi K., Ghatei M.A., Kanse S.M., Polak J.M., Bloom S.R. Binding sites of a novel neuropeptide pituitary adenylate cyclase activating polypeptide in the rat brain and lung. Eur. J. Biochem. 193:1990;725-729.
46. Li M., Shioda S., Somogyvari-Vigh A., Onda H., Arimura A. Specific antibody recognition of rat pituitary adenylate cyclase activating polypeptide receptors. Endocrine. 7:1997;183-190.
47. Lu N., DiCicco-Bloom E. Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc. natn. Acad. Sci. U.S.A. 94:1997;3357-3362.
48. Masuo Y., Ohtaki T., Masuda Y., Tsuda M., Fujino M. Binding sites for pituitary adenylate cyclase-activating polypeptide (PACAP): comparison with vasoactive intestinal polypeptide (VIP) binding site localization in rat brain sections. Brain Res. 575:1992;113-123.
49. Masuo Y., Ohtaki T., Matsuda Y., Nagai Y., Suno M., Tsuda M., Fujino M. Autoradiographic distribution of pituitary adenylate cyclase activating polypeptide (PACAP) binding sites in the rat brain. Neurosci. Lett. 126:1991;103-106.
50. Masuo Y., Suzuki N., Matsumoto H., Tokito F., Matsumoto Y., Tsuda M., Fujino M. Regional distribution of pituitary adenylate cyclase activating polypeptide (PACAP) in the rat central nervous system as determined by sandwich-enzyme immunoassay. Brain Res. 602:1993;57-63.
51. Masuo Y., Tokito F., Matsumoto Y., Shimamoto N., Fujino M. Ontogeny of pituitary adenylate cyclase-activating polypeptide (PACAP) and its binding sites in the rat brain. Neurosci. Lett. 170:1994;43-46.
52. Matsuda K., Arimura A., Shioda S., Takei Y., Shimomura H. and Uchiyama M. (1997) Pituitary adenylate cyclase-activating polypeptide (PACAP) in fishes: purification, distribution and physiological function. In Advances in Comparative Endocrinology (eds Kawashima S. and Kikuyama S.), Vol. 1, pp. 687-691. Monduzzi Editore, Bologna, Italy.
53. Matsuda K., Yoshida T., Nagano Y., Kashimoto K., Yatohgo T., Shimomura H., Shioda S., Arimura A., Uchiyama M. Purification and primary structure of pituitary adenylate cyclase activating polypeptide (PACAP) from the brain of an elasmobranch, stingray, Dasyatis akajei. Peptides. 19:1998;1489-1495.
54. Matsuda K., Takei Y., Katoh J., Shioda S., Arimura A., Uchiyama M. Isolation and structural characterization of pituitary adenylate cyclase-activating polypeptide (PACAP)-like peptide from the brain of a teleost, stargazer, Uranoscopus japonicus. Peptides. 18:1997;723-727.
55. Miyamoto Y., Habata Y., Ohtaki T., Masuda Y., Ogi K., Onda H., Fujino M. Cloning and expression of a complementary DNA encoding the bovine receptor for pituitary adenylate cyclase activating polypeptide (PACAP). Biochim. biophys. Acta. 1218:1994;297-307.
56. Miyata A., Arimura A., Dahl R.D., Minamino N., Uehara A., Jiang L., Culler M.D., 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.
57. Miyata A., Jiang L., Dahl R.D., Kitada C., Kubo K., Fujino M., Minamino N., 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.
58. Morrow J.A., Lutz E.M., West K.M., Fink G., Hamar A.J. Molecular cloning and expression of a cDNA encoding a receptor for pituitary adenylate cyclase activating polypeptide (PACAP). Fedn Eur. biochem. Socs Lett. 329:1993;99-105.
59. Muroi M., Shioda S., Yada T., Zhou C.J., Nakai Y., Nakajo S., Arimura A. Distribution and ultrastructural localization of PACAP receptors in the rat pancreatic islets. Ann. N. Y. Acad. Sci. 865:1998;438-440.
60. Ogi K., Kimura C., Onda H., Arimura A., Fujino M. Molecular cloning and characterization of cDNA for the precursor of rat pituitary adenylate cyclase activating polypeptide (PACAP). Biochem. biophys. Res. Commun. 173:1990;1271-1279.
61. O'Rahilly R. and Muller F. (1987) Development Stages in Human Embryos, Publication No. 637. Carnegie Institute, Washington, DC.
62. Pantaloni C., Brabet P., Bilanges B., Dumuis A., Houssami S., Spengler D., Bockaert J. 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;22,146-22,151.
63. Paxinos G., Ashwell K. W. S. and Törk I. (1994) Atlas of the Developing Rat Nervous System, 2nd edn. Academic, San Diego.
64. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic, San Diego.
65. Pei L. Genomic structure and embryonic expression of the rat type 1 vasoactive intestinal polypeptide receptor gene. Regul. Pept. 71:1997;153-161.
66. Pisegna J.R., Moody T.W., Wank S.A. Differential signaling and immediate-early gene activation by four splice variants of the human pituitary adenylate cyclase-activating polypeptide receptor (hPACAP-R). Ann. N. Y. Acad. Sci. 805:1996;54-64.
67. Pisegna J.R., Wank S.A. Cloning and characterization of the signal transduction of four splice variants of the human pituitary adenylate cyclase-activating polypeptide receptor. Evidence for dual coupling to adenylate cyclase and phospholipase C. J. biol. Chem. 271:1996;17,267-17,274.
68. Pisegna J.R., Wank S.A. Molecular cloning and functional expression of the pituitary adenylate cyclase-activating polypeptide type 1 receptor. Proc. natn. Acad. Sci. U.S.A. 90:1993;6345-6349.
69. Seki T., Shioda S., Ogino D., Nakai Y., Arimura A., Koide R. Distribution and ultrastructural localization of a receptor for pituitary adenylate cyclase-activating polypeptide and its mRNA in the rat retina. Neurosci. Lett. 238:1997;127-130.
70. Sheward W.J., Lutz E.M., Harmar A.J. Expression of pituitary adenylate cyclase activating polypeptide receptors in the early mouse embryo as assessed by reverse transcription-polymerase chain reaction and in situ hybridization. Neurosci. Lett. 216:1996;45-48.
71. Shioda S., Legradi G., Leung W.C., Nakajo S., Nakaya K., Arimura A. Localization of pituitary adenylate cyclase-activating polypeptide and its messenger ribonucleic acid in the rat testis by light and electron microscopic immunocytochemistry and in situ hybridization. Endocrinology. 135:1994;818-825.
72. Shioda S., Muroi M., Nakai Y. and Arimura A. (1997) Expression of the receptor for PACAP in the rat adrenal medulla by immunocytochemistry and in situ hybridization. In Advances in Comparative Endocrinology (eds Kawashima S. and Kikuyama S.), Vol. 1, pp. 651-654. Monduzzi Editore, Bologna, Italy.
73. Shioda S., Nakai Y., Nakajo S., Nakaya K., Arimura A. Localization of pituitary adenylate cyclase-activating polypeptide and its type 1 receptors in the rat ovary: immunohistochemistry and in situ hybridization. Ann. N. Y. Acad. Sci. 805:1996;677-683.
74. Shioda S., Nakai Y., Nakajo S., Nakaya K., Arimura A. Pituitary adenylate cyclase-activating polypeptide and its type 1 receptors in the rat hypothalamus: neuroendocrine interactions. Ann. N. Y. Acad. Sci. 805:1996;670-676.
75. Shioda S., Ozawa H., Dohi K., Mizushima H., Matsumoto K., Nakajo S., Takaki A., Zhou C.J., Nakai Y., Arimura A. PACAP protects hippocampal neurons against apoptosis. Involvement of JNK/SAPK signaling pathway. Ann. N. Y. Acad. Sci. 865:1998;111-117.
76. Shioda S., Shuto Y., Somogyvari-Vigh A., Legradi G., Onda H., Coy D.H., Nakajo S., 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.
77. Shioda S., Yada T., Nakajo S., Nakaya K., Nakai Y., Arimura A. Pituitary adenylate cyclase-activating polypeptide (PACAP): a novel regulator of vasopressin-containing neurons. Brain Res. 765:1997;81-90.
78. Shivers B.D., Gores T.J., Gottschall P.E., Arimura A. Two high affinity binding sites for pituitary adenylate cyclase-activating polypeptide have different tissue distributions. Endocrinology. 128:1991;3055-3065.
79. Shuto Y., Uchida D., Onda H., Arimura A. Ontogeny of pituitary adenylate cyclase activating polypeptide and its receptor mRNA in the mouse brain. Regul. Pept. 67:1996;79-83.
80. Spengler D., Waeber C., Pantaloni C., Holsboer F., Bockaert J., Seeburg P.H., Journot L. Differential signal transduction by five splice variants of the PACAP receptor. Nature. 365:1993;170-175.
81. Sreedharan S.P., Patel D.R., Huang J.X., Goetzl E.J. Cloning and functional expression of a human neuroendocrine vasoactive intestinal peptide receptor. Biochem. biophys. Res. Commun. 193:1993;546-553.
82. 1 receptors expressed by stable transfectants couple to two distinct signaling pathways. Biochem. biophys. Res. Commun. 203:1993;141-148.
83. Sundler F., Ekblad E., Absood A., Hakanson R., Koves K., Arimura A. Pituitary adenylate cyclase activating polypeptide: a novel vasoactive intestinal peptide-like neuropeptide in the gut. Neuroscience. 46:1992;439-454.
84. Svoboda M., Tastenoy M., Ciccaralli E., Stievenart M., Christophe J. Cloning of a splice variant of the pituitary adenylate cyclase-activating polypeptide (PACAP) type 1 receptor. Biochem. biophys. Res. Commun. 195:1993;881-888.
85. Svoboda M., Tastenoy M., Van Rampelbergh J., Grossens J.F., DeNeef P., Waelbroeck M., Robberecht P. Molecular cloning and functional characterization of a human VIP receptor from SUP-T1 lymphoblasts. Biochem. biophys. Res. Commun. 205:1994;1617-1624.
86. Tabarin A., Chen D., Hakanson R., Sundler F. Pituitary adenylate cyclase-activating polypeptide in the adrenal gland of mammals: distribution, characterization and responses to drugs. Neuroendocrinology. 59:1994;113-119.
87. Tatsuno I., Gottschall P.E., Arimura A. Specific binding sites for pituitary adenylate cyclase activating polypeptide (PACAP) in rat cultured astrocytes: molecular identification and interaction with vasoactive intestinal peptide (VIP). Peptides. 12:1991;617-621.
88. Tatsuno I., Gottschall P.E., Koves K., Arimura A. Demonstration of specific binding sites for pituitary adenylate cyclase activating polypeptide (PACAP) in rat astrocytes. Biochem. biophys. Res. Commun. 168:1990;1027-1033.
89. Tatsuno I., Somogyvari-Vigh A., Arimura A. Developmental changes of pituitary adenylate cyclase activating polypeptide (PACAP) and its receptor in the rat brain. Peptides. 15:1994;55-60.
90. Theiler K. (1989) The House Mouse: Atlas of Embryonic Development. Springer, New York.
91. Uchida D., Arimura A., Somogyvari-Vigh A., Shioda S., Banks W.A. Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase-activating polypeptide. Brain Res. 736:1996;280-286.
92. Uddman R., Luts A., Arimura A., Sundler F. Pituitary adenylate cyclase activating polypeptide (PACAP), a new vasoactive intestinal peptide (VIP)-like peptide in the respiratory tract. Cell Tiss. Res. 265:1991;197-201.
93. Usdin T.B., Bonner T.I., Mezey E. Two receptors for vasoactive intestinal polypeptide with similar specificity and complementary distributions. Endocrinology. 135:1994;2662-2680.
94. Vigh S., Arimura A., Koves K., Somogyvari-Vigh A., Sitton J., Fermin C.D. Immunohistochemical localization of the neuropeptide, pituitary adenylate cyclase activating polypeptide (PACAP), in the human and primate hypothalamus. Peptides. 12:1991;313-318.
95. Waschek J.A., Casillas R.A., Nguyen T.B., DiCicco-Bloom E.M., Carpenter E.M., Rodriguez W.I. Neural tube expression of pituitary adenylate cyclase-activating peptide (PACAP) and receptor: potential role in patterning and neurogenesis. Proc. natn. Acad. Sci. U.S.A. 95:1998;9602-9607.
96. Waschek J.A., Ellison J., Bravo D.T., Handley V. Embryonic expression of vasoactive intestinal peptide (VIP) and VIP receptor genes. J. Neurochem. 66:1996;1762-1765.
97. Witschi E. (1962) Development: rat. In Growth Including Reproduction and Morphological Development (eds Altman P. L. and Dittmer D. S.), pp. 304-314. Biological Handbooks of the Federation of American Societies for Experimental Biology, Washington, DC.
98. Yada T., Sakurada M., Ihida K., Nakata M., Murata F., Arimura A., Kikuchi M. Pituitary adenylate cyclase activating polypeptide is an extraordinarily potent intra-pancreatic regulator of insulin secretion from islet B-cells. J. biol. Chem. 269:1994;1290-1293.
99. Yada T., Sakurada M., Ishihara H., Nakata M., Shioda S., Yaekura K., Hamakawa N., Yanagita K., Kikuchi M., Oka Y. Pituitary adenylate cyclase-activating polypeptide (PACAP) is an islet substance serving as an intra-islet amplifier of glucose-induced insulin secretion in rats. J. Physiol., Lond. 505:1997;319-328.
100. Yon L., Freuilloley M., Chartrel N., Arimura A., Conlon J.M., Fournier A., Vaudry H. Immunohistochemical distribution and biological activity of pituitary adenylate cyclase activating polypeptide (PACAP) in the central nervous system of the frog Rana ridibunda. J. comp. Neurol. 324:1992;485-499.
101. Zhou C. J., Kikuyama S., Shioda S., Nakai Y., Nakajo S. and Arimura A. (1997) Expression of pituitary adenylate cyclase-activating polypeptide (PACAP) receptor messenger RNA in the development rat brain by in situ hybridization. In Advances in Comparative Endocrinology (eds Kawashima S. and Kikuyama S.), Vol. 1, pp. 671-675. Monduzzi Editore, Bologna, Italy.