Distribution of adrenomedullin-like immunoreactivity in the rat central nervous system by light and electron microscopy

Brain Research

Volumn 853, Issue 2, 2000, Pages 245-268

  Serrano, Julia ^a   Uttenthal, L Otto ^a   Martínez, Alfredo ^b   Fernández, A Patricia ^a   Martínez De Velasco, Javier ^a   Alonso, David ^a   Bentura, María Luisa ^a   Santacana, María ^a   Gallardo, José R ^a   Martínez Murillo, Ricardo ^a   Cuttitta, Frank ^b   Rodrigo, José ^a  

^a INSTITUTO CAJAL   (Spain)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Adrenomedullin like immunoreactivity; Avidin biotin peroxidase complex; Immunocytochemistry; Light and electron microscopy; Rat central nervous system

Indexed keywords

ADRENOMEDULLIN;

ADRENAL MEDULLA; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CATTLE; CENTRAL NERVOUS SYSTEM; CEREBELLUM; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FRONTAL CORTEX; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MICROSCOPY; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PURKINJE CELL; RAT; SPINAL CORD; WESTERN BLOTTING;

ADRENOMEDULLIN; ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; AXONS; BRAIN; DENDRITES; MALE; MICROCIRCULATION; MICROTUBULES; MITOCHONDRIA; NEURONS; PEPTIDE FRAGMENTS; PURKINJE CELLS; RATS; RATS, WISTAR; SPINAL CORD; SYNAPSES;

EID: 0033989163     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)02273-8     Document Type: Article

References (67)

1. Allen M.A., Ferguson A.V. In vitro recordings from area postrema neurons demonstrate responsiveness to adrenomedullin. Am. J. Physiol. 270:1996;R920-R925.
2. Aoki C., Pickel V.M. Neuropeptide Y in cortex and striatum. Ultrastructural distribution and coexistence with classical neurotransmitters and neuropeptides. Ann. N. Y. Acad. Sci. 611:1990;186-205.
3. Baskaya M.K., Suzuki Y., Anzai M., Seki Y., Saito K., Takayasu M., Shibuya M., Sugita K. Effects of adrenomedullin, calcitonin gene-related peptide, and amylin on cerebral circulation in dogs. J. Cereb. Blood Flow Metab. 15:1995;827-834.
4. Charles C.J., Rademaker M.T., Richards A.M., Cooper G.J.S., Coy D.H., Nichols M.G. Hemodynamic, hormonal and renal effects of intracerebroventricular adrenomedullin in conscious sheep. Endocrinology. 139:1998;1746-1751.
5. Chronwall B.M., DiMaggio D.A., Massari V.J., Pickel V.M., Ruggiero D.A., O'Donohue T.L. The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience. 15:1985;1159-1181.
6. Cooper G.J.S., Willis A.C., Clark A., Turner R.C., Sim R.B., Reid K.B.M. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. U. S. A. 84:1987;8628-8632.
7. Cormier-Regard S., Nguyen S.V., Claycomb W.C. Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem. 273:1998;17787-17792.
8. Cuttitta F., Fedorko J., Gu J., Lebacq-Verheyden A.M., Linnoila R.I., Battey J.F. Gastrin-releasing peptide gene-associated peptides are expressed in normal human fetal lung and small cell lung cancer: a novel peptide family found in man. J. Clin. Endocrinol. Metab. 67:1988;576-583.
9. De Quidt M.E., Emson P.C. Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system: II. Immunohistochemical analysis. Neuroscience. 18:1986;545-618.
10. Eguchi S., Hirata Y., Iwasaki H., Sato K., Watanabe T.X., Inui T., Nakajima K., Sakakibara S., Marumo F. Structure-activity relationship of adrenomedullin, a novel vasodilatory peptide, in cultured rat vascular smooth muscle cells. Endocrinology. 135:1994;2454-2458.
11. González A., Marín O., Sánchez-Camacho C., Peña J.J., Zudaire E., Martínez A., Cuttitta F., Muñoz M. Localization of adrenomedullin-like immunoreactivity in the hypothalamo-hypophysial system of amphibians. Neurosci. Lett. 242:1998;13-16.
12. Guesdon J.L., Ternynck T., Avrameas S. The use of avidin-biotin interaction in immunoenzymatic techniques. J. Histochem. Cytochem. 27:1979;1131-1139.
13. Hao Q., Chang J.-K., Gharavi H., Fortenberry Y., Hyman A., Lippton H. An adrenomedullin (ADM) fragment retains the systemic vasodilator activity of human ADM. Life Sci. 54:1994;PL265-PL270.
14. Hirata Y., Hayakawa H., Suzuki Y., Suzuki E., Ikenouchi H., Kohmoto O., Kimura K., Kitamura K., Eto T., Kangawa K. Mechanisms of adrenomedullin-induced vasodilation in the rat kidney. Hypertension. 25:1995;790-795.
15. Hsu S.M., Raine L. Protein A, avidin and biotin in immunocytochemistry. J. Histochem. Cytochem. 29:1981;1349-1353.
16. Hsu S.M., Raine L., Fanfer H. Use of avidin-biotin complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:1981;577-580.
17. Hwang I.S.S., Tang F. The distribution and gene expression of adrenomedullin in the rat brain: peptide/mRNA and precursor/active peptide relationships. Neurosci. Lett. 267:1999;85-88.
18. Ichiki Y., Kitamura K., Kangawa K., Kawamoto M., Matsuo H., Eto T. Distribution and characterization of immunoreactive adrenomedullin in human tissue and plasma. FEBS Lett. 338:1994;6-10.
19. Ichiki Y., Kitamura K., Kangawa K., Kawamoto M., Matsuo H., Eto T. Distribution and characterization of immunoreactive adrenomedullin in porcine tissue, and isolation of adrenomedullin [26-52] and adrenomedullin [34-52] from porcine duodenum. J. Biochem. 118:1995;765-770.
20. Imai T., Hirata Y., Iwashima M., Marumo F. Hormonal regulation of rat adrenomedullin gene in vasculature. Endocrinology. 136:1995;1544-1547.
21. Ishimitsu T., Kojima M., Kangawa K., Hino J., Matsuoka H., Kitamura K., Eto T., Matsuo H. Genomic structure of human adrenomedullin gene. Biochem. Biophys. Res. Commun. 203:1994;631-639.
22. Jougasaki M., Wei C.M., Aarhus L.L., Heublen D.M., Sandberg S.M., Burnett J.C. Renal localization and actions of adrenomedullin: a natriuretic peptide. Am. J. Physiol. 268:1995;F657-F663.
23. Kapas S., Catt K.J., Clark A.J.L. Cloning and expression of cDNA encoding a rat adrenomedullin receptor. J. Biol. Chem. 270:1995;25344-25347.
24. Kitamura K., Ichiki Y., Tanaka M., Kawamoto M., Emura J., Sakakibara S., Kangawa K., Matsuo H., Eto T. Immunoreactive adrenomedullin in human plasma. FEBS Lett. 341:1994;288-290.
25. Kitamura K., Kangawa K., Kawamoto M., Ichiki Y., Nakamura S., Matsuo H., Eto T. Adrenomedullin: a novel hypotensive peptide isolated from human pheochromocytoma. Biochem. Biophys. Res. Commun. 192:1993;553-560.
26. Kitamura K., Kangawa K., Kojima M., Ichiki Y., Matsuo H., Eto T. Complete amino acid sequence of porcine adrenomedullin and cloning of cDNA encoding its precursor. FEBS Lett. 338:1994;306-310.
27. Kitamura K., Sakata J., Kangawa K., Kojima M., Matsuo H., Eto T. Cloning and characterization of cDNA encoding a precursor for human adrenomedullin. Biochem. Biophys. Res. Commun. 194:1993;720-725.
28. Majid D.S., Kadowitz P.J., Coy D.H., Navar D.J. Renal responses to intra-arterial administration of adrenomedullin in dogs. Am. J. Physiol. 270:1996;F200-F205.
29. Martínez A., Miller M.J., Unsworth E.J., Siegfried J.M., Cuttitta F. Expression of adrenomedullin in normal human lung and in pulmonary tumors. Endocrinology. 136:1995;4099-4105.
30. Martínez A., Unsworth E.J., Cuttitta F. Adrenomedullin-like immunoreactivity in the nervous system of the starfish Marthasterias glacialis. Cell Tissue Res. 283:1996;169-172.
31. Matsunaga K., Iwasaki T., Yonetani Y., Kitamura K., Eto T., Kangawa K., Matsuo H. Nitric oxide dependent hypotensive effects of adrenomedullin in rats. Drug Dev. Res. 37:1996;55-60.
32. Matsunaga K., Iwasaki T., Yonetani Y., Kitamura K., Eto T., Kangawa K., Matsuo H. Nitric oxide-associated relaxing effects of adrenomedullin in rat aorta. Drug Dev. Res. 38:1996;62-66.
33. G-nitro-L-arginine but not glibenclamide. Br. J. Pharmacol. 115:1995;917-924.
34. Montuenga L.M., Martínez A., Miller M.J., Unsworth E.J., Cuttitta F. Expression of adrenomedullin and its receptor during embryogenesis suggests autocrine or paracrine modes of action. Endocrinology. 138:1997;440-451.
35. Mori Y., Takayasu M., Suzuki Y., Shibuya M., Yoshida J., Hidaka H. Effects of adrenomedullin on rat cerebral arterioles. Eur. J. Pharmacol. 330:1997;195-198.
36. Murphy T.C., Samson W.K. The novel vasoactive hormone, adrenomedullin, inhibits water drinking in the rat. Endocrinology. 136:1995;2459-2463.
37. Nagata D., Hirata Y., Suzuki E., Kakoki M., Hayakawa H., Goto A., Ishimitsu T., Minamino N., Ono Y., Kangawa K., Matsuo H., Omata M. Hypoxia-induced adrenomedullin production in the kidney. Kidney Int. 55:1999;1259-1267.
38. Nakayama M., Takahashi K., Murakami O., Shirato K., Shibahara S. Induction of adrenomedullin by hypoxia and cobalt chloride in human colorectal carcinoma cells. Biochem. Biophys. Res. Commun. 243:1998;514-517.
39. Nossaman B.D., Feng C.J., Kaye A.D., DeWitt B., Coy D.H., Murphy W.A., Kadowitz P.J. Pulmonary vasodilator responses to adrenomedullin are reduced by NOS inhibitors in rats but not in cats. Am. J. Physiol. 14:1996;L782-L789.
40. Parkes D.G., May C.N. ACTH-suppressive and vasodilator actions of adrenomedullin in conscious sheep. J. Neuroendocrinol. 7:1995;923-929.
41. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates, 2nd edn., Academic Press, New York, 1986.
42. Perret M., Broussard H., LeGros T., Burns A., Chang J.-K., Summer W., Hyman A., Lippton H. The effect of adrenomedullin on the isolated heart. Life Sci. 53:1993;PL377-PL379.
43. Rodrigo J., Springall D.R., Uttenthal O., Bentura M.L., Abadia-Molina F., Riveros-Moreno V., Martínez-Murillo R., Polak J.M., Moncada S. Localization of nitric oxide synthase in the adult rat brain. Philos. Trans. R. Soc. London, Ser. B. 345:1994;175-221.
44. Rosenfeld M.G., Mermod J.-J., Amara S.G., Swanson L.W., Sawchenko P.E., Rivier J., Vale W.W., Evans R.M. Nature. 304:1983;129-135.
45. Sakata J., Shimokubo T., Kitamura K., Nakamura S., Kangawa K., Matsuo H., Eto T. Molecular cloning and biological activities of rat adrenomedullin, a hypotensive peptide. Biochem. Biophys. Res. Commun. 195:1993;921-927.
46. Sakata J., Shimokubo T., Kitamura K., Nishizono M., Iehiki Y., Kangawa K., Matsuo H., Eto T. Distribution and characterization of immunoreactive rat adrenomedullin in tissue and plasma. FEBS Lett. 352:1994;105-108.
47. Samson W.K., Murphy T., Shell D.A. A novel vasoactive peptide, adrenomedullin, inhibits pituitary adrenocorticotropin release. Endocrinology. 136:1995;2349-2352.
48. Santacana M., Uttenthal L.O., Bentura M.L., Fernández A.P., Serrano J., Martínez de Velasco J., Alonso D., Rodrigo J. Expression of neuronal nitric oxide synthase in the cerebral cortex during the embryonic development of the rat. Dev. Brain Res. 111:1998;205-222.
49. Satoh F., Takahashi K., Murakami O., Totsune K., Sone M., Ohneda M., Abe K., Miura Y., Hayashi Y., Sasano H., Mouri T. Adrenomedullin in human brain, adrenal glands and tumor tissues of pheochromocytoma, ganglioneuroblastoma and neuroblastoma. J. Clin. Endocrinol. Metab. 80:1995;1750-1752.
50. Satoh F., Takahashi K., Murakami O., Totsune K., Sone M., Ohneda M., Sasano H., Mouri T. Immunocytochemical localization of adrenomedullin-like immunoreactivity in the human hypothalamus and the adrenal gland. Neurosci. Lett. 203:1996;207-210.
51. 2+ mobilization, in bovine aortic endothelial cells. J. Biol. Chem. 270:1995;4412-4417.
52. Shu S., Ju G., Fan L. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85:1988;169-171.
53. Sugo S., Minamino N., Kangawa K., Miyamoto K., Kitamura K., Sakata J., Eto T., Matsuo H. Endothelial cells actively synthesize and secrete adrenomedullin. Biochem. Biophys. Res. Commun. 201:1994;1160-1166.
54. Sugo S., Minamino N., Shoji H., Kangawa K., Kitamura K., Eto T., Matsuo H. Production and secretion of adrenomedullin from vascular smooth muscle cells: augmented production by tumor necrosis factor-α Biochem. Biophys. Res. Commun. 203:1994;710-726.
55. Takahashi H., Watanabe T.X., Nishimura M., Nakanishi T., Sakamoto M., Yoshimura M., Komiyama Y., Masuda M., Murakami T. Centrally induced vasopressor and sympathetic responses to a novel endogenous peptide, adrenomedullin, in anesthetized rats. Am. J. Hypertens. 7:1994;478-482.
56. Takahashi K., Satoh F., Hara E., Sone M., Murakami O., Kayama T., Yoshimoto T., Shibahara S. Production and secretion of adrenomedullin from glial cell tumors and its effects on cAMP production. Peptides. 18:1997;1117-1124.
57. Takahashi K., Satoh F., Sone M., Murakami O., Sasano H., Mouri T., Shibahara S. Expression of adrenomedullin mRNA in human brain and pituitary. Peptides. 18:1997;1051-1053.
58. Takahashi K., Sone M., Satoh F., Murakami O., Totsune K., Tanji H., Sato N., Ito H., Mouri T. Presence of adrenomedullin-like immunoreactivity in the human cerebrospinal fluid. Peptides. 18:1997;459-461.
59. Taylor G.M., Meeran K., O'Shea D., Smith D.M., Ghatei M.A., Bloom S.R. Adrenomedullin inhibits feeding in the rat by a mechanism involving calcitonin gene-related peptide receptors. Endocrinology. 137:1996;3260-3264.
60. Turton M.D., O'Shea D., Gunn I., Beak S.A., Edwards C.M., Meeran K., Choi S.J., Taylor G.M., Heath M.M., Lambert P.D., Wilding J.P., Smith D.M., Ghatei M.A., Herbert J., Bloom S.R. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature. 379:1996;69-72.
61. Ueta Y., Kitamura K., Isse T., Shibuya I., Kabashima N., Yamamoto S., Kangawa K., Matsuo H., Eto T., Yamashita H. Adrenomedullin-immunoreactive neurons in the paraventricular and supraoptic nuclei of the rat. Neurosci. Lett. 202:1995;37-40.
62. Uttenthal L.O., Alonso D., Fernández A.P., Campbell R.O., Moro M.A., Leza J.C., Esteban F.J., Barroso J.B., Valderrama R., Pedrosa J.A., Peinado M.A., Serrano J., Richart A., Bentura M.L., Santacana M., Martínez-Murillo R., Rodrigo J. Neuronal and inducible nitric oxide synthase and nitrotyrosine immunoreactivities in the cerebral cortex of the aging rat. Microsc. Res. Tech. 43:1998;75-88.
63. Wang X., Yue T.-L., Barone F.C., White R.F., Clark R.K., Willete R.N., Sulpizio A.C., Aiyar N.V., Ruffolo R.R. Jr., Feuerstein G.Z. Discovery of adrenomedullin in rat ischemic cortex and evidence for its role in exacerbating focal rain ischemic damage. Proc. Natl. Acad. Sci. U. S. A. 92:1995;11480-11484.
64. Washimine H., Asada Y., Kitamura K., Ichiki Y., Hara S., Yamamoto Y., Kangawa K., Sumiyoshi A., Eto T. Immunohistochemical identification of adrenomedullin in human rat and porcine tissue. Histochem. Cell Biol. 103:1995;251-254.
65. Wei Y., Cao Y., Zhu Y., Chang J., Tang J. Immunohistochemistry and reverse transcription-polymerase chain reaction for detecting adrenomedullin in the central nervous system. Chin. Med. J. 111:1998;793-796.
66. Wei Y., Li Q., Song L., Ouyang D., He R., Tang J. The central distribution of adrenomedullin and its central effects on hemodynamic parameters in rats. Circulation, Suppl. 92:1995;141-148.
67. Yang B.C., Lippton H., Gumusel B., Hyman A., Mehta J.L. Adrenomedullin dilates rat pulmonary artery rings during hypoxia: role of nitric oxide and vasodilator prostaglandins. J. Cardiovasc. Pharmacol. 28:1996;458-462.