Novel autocrine feedback control of catecholamine release: A discrete chromogranin A fragment is a noncompetitive nicotinic cholinergic antagonist

Journal of Clinical Investigation

Volumn 100, Issue 6, 1997, Pages 1623-1633

  Mahata, Sushil K ^a,c   O'Connor, Daniel T ^a,c   Mahata, Manjula ^a,c   Yoo, Seung Hyun ^b   Taupenot, Laurent ^a,c   Wu, Hongjiang ^a,c   Gill, Bruce M ^a,c   Parmer, Robert J ^a,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Acetylcholine; Catecholamine; Catestatin; Chromogranin A; PC12

Indexed keywords

ACETYLCHOLINE; CATECHOLAMINE; CHROMOGRANIN A; NICOTINIC RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CATECHOLAMINE RELEASE; CATTLE; CHROMAFFIN CELL; CONTROLLED STUDY; NEGATIVE FEEDBACK; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; RAT;

EID: 0030803637     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119686     Document Type: Article

References (67)

1. Blaschko, H., R.S. Comline, F.H. Schneider, M. Silver, and A.D. Smith. 1967. Secretion of a chromaffin granule protein, chromogranin, from the adrenal gland after splanchnic stimulation. Nature (Lond.). 215:58-59.
2. Schneider, F.H., A.D. Smith, and H. Winkler. 1967. Secretion from the adrenal medulla: biochemical evidence for exocytosis. Br. J. Pharmacol. Chemother. 31:94-104.
3. Winkler, H., and R. Fischer-Colbrie. 1992. The chromogranins A and B: the first 25 years and future perspectives. Neuroscience. 49:497-528.
4. Huttner, W.B., H.H. Gerdes, and P. Rosa. 1991. Chromogranins/secretogranins - widespread constituents of the secretory granule matrix in endocrine cells and neurons. In Markers for Neural and Endocrine cells. M. Gratzl and K. Langley, editors. VCH Verlagsgesellschaft mbH, Weinheim, Germany. 93-131.
5. O'Connor, D.T., and L.J. Deftos. 1986. Secretion of chromogranin A by peptide producing endocrine neoplasms. N. Engl. J. Med. 314:1145-1151.
6. Parmer, R.J., X.-P. Xi, H.J. Wu, L.J. Helman, and L.N. Petz. 1993. Secretory protein traffic: chromogranin A contains a dominant targeting signal for the regulated pathway. J. Clin. Invest. 92:1042-1054.
7. Metz-Boutigue, M.-H., P. Garcia-Sablone, R. Hogue-Angeletti, and D. Aunis. 1993. Intracellular and extracellular processing of chromogranin A: Determination of cleavage sites. Eur. J. Biochem. 217:247-257.
8. Helle, K.B., G. Serck-Hanssen, and S. Aardal. 1993. Functional aspects of the adrenal medullary chromogranins. Neurochem. Int. 22:353-360.
9. Dillen, L., B. Miserez, M. Claeys, D. Aunis, and W. DePotter. 1993. Post-translational processing of proenkephalins and chromogranins/secretogranins. Neurochem. Int. 22:315-352.
10. Parmer, R.J., L.A. Miles, X.-P. Xi, B.M. Gill, H. Wu, and D.T. O'Connor. 1993. Processing of chromaffin granule proteins: a profusion of proteases? Neurochem. Int. 22:361-367.
11. Benedum, U.M., P.A. Baeuerle, D.S. Konecki, R. Frank, J. Powell, J. Mallet, and W.B. Huttner. 1986. The primary structure of bovine chromogranin A: a representative of a class of acidic secretory proteins common to a variety of peptidergic cells. EMBO J. 5:1495-1502.
12. Iacangelo, A., H.U. Affolter, L.E. Eiden, E. Herbert, and M. Grimes. 1986. Bovine chromogranin A sequence and distribution of its messenger RNA in endocrine tissues. Nature (Lond.). 323:82-86.
13. Konecki, D.S., U.M. Benedum, H.H. Gerdes, and W.B. Huttner. 1987. The primary structure of human chromogranin A and pancreastatin. J. Biol. Chem. 262:17026-17030.
14. Helman, L.J., T.G. Ahn, M.A. Levine, A. Allison, P.S. Cohen, M.J. Cooper, D.V. Cohn, and M.A. Israel. 1988. Molecular cloning and primary structure of human chromogranin A (secretory protein I) cDNA. J. Biol. Chem. 263:11559-11563.
15. Iacangelo, A., H. Okayama, and L.E. Eiden. 1988. Primary structure of rat chromogranin A and distribution of its mRNA. FEBS Lett. 227:115-121.
16. Iacangelo, A.L., R. Fischer-Colbrie, K.J. Koller, M.J. Brownstein, and L.E. Eiden. 1988. The sequence of porcine chromogranin A messenger RNA demonstrates chromogranin A can serve as the precursor for the biologically active hormone, pancreastatin. Endocrinology. 122:2339-2341.
17. Wu, H.J., D.J. Rozansky, R.J. Parmer, B.M. Gill, and D.T. O'Connor. 1991. Structure and function of the chromogranin A gene. Clues to evolution and tissue-specific expression. J. Biol. Chem. 266:13130-13134.
18. Eskeland, N.L., A. Zhou, T.Q. Dinh, H. Wu, R.J. Parmer, R.E. Mains, and D.T. O'Connor. 1996. Chromogranin A processing and secretion. Specific role of endogenous and exogenous prohormone convertases in the regulated secretory pathway. J. Clin. Invest. 98:148-156.
19. Arden, S.D., N.G. Rutherford, P.C. Guest, W.J. Curry, E.M. Bailyes, C.F. Johnston, and J.C. Hutton. 1994. The post-translational processing of chromogranin A in the pancreatic islet: involvement of the eukaryote subtilisin PC2. Biochem. J. 298:521-528.
20. Hoflehner, J., U. Eder, A. Laslop, N.G. Seidah, R. Fischer-Colbrie, and H. Winkler. 1995. Processing of secretogranin II by prohormone convertases: importance of PC1 in generation of secretoneurin. FEBS Lett. 360:294-298.
21. Tatemoto, K., S. Efendic, V. Mutt, G. Makk, G.J. Feistner, and J.D. Barchas. 1986. Pancreastatin, a novel pancreatic peptide that inhibits insulin secretion. Nature (Lond.). 324:476-478.
22. Hutton, J.C., H.W. Davidson, K.A. Grimaldi, and M. Peshavaria. 1987. Biosynthesis of beta-granin in pancreatic (beta)-cells. Biochem. J. 244: 449-456.
23. Drees, B.M., J. Rouse, J. Johnson, and J.W. Hamilton. 1991. Bovine parathyroid glands secrete a 26-kDa N-terminal fragment of chromogranin A which inhibits parathyroid cell secretion. Endocrinology. 129:3381-3387.
24. Drees, B.M., and J.W. Hamilton. 1994. Processing of chromogranin A by bovine parathyroid secretory granules: production and secretion of N-terminal fragments. Endocrinology. 134:2057-2063.
25. Aardal, S., and K.B. Helle. 1992. The vasoinhibitory activity of bovine chromogranin A fragment (vasostatin) and its independence of extracellular calcium in isolated segments of human blood vessels. Regul. Pept. 41:9-18.
26. Helle, K.B., P.D. Marley, R. Hogue-Angeletti, D. Aunis, E. Galindo, D.H. Small, and B.G. Livett. 1993. Chromogranin A: secretion of processed products from the stimulated retrogradely perfused bovine adrenal gland. J. Neuroendocrinol. 5:413-420.
27. 347-419), a novel chromogranin A-derived peptide, inhibits parathyroid cell secretion. Endocrinology. 133:461-466.
28. Simon, J.-P., M.-F. Bader, and D. Aunis. 1988. Secretion from chromaffin cells is controlled by chromogranin A-derived peptides. Proc. Natl. Acad. Sci. USA. 85:1712-1716.
29. Galindo, E., A. Rill, M.-F. Bader, and D. Aunis. 1991. Chromostatin, a 20-amino acid peptide derived from chromogranin A, inhibits chromaffin cell secretion. Proc. Natl. Acad. Sci. USA. 88:1426-1430.
30. Galindo, E., M. Mendez, S. Calvo, C. Gonzalez-Garcia, V. Cena, P. Hubert, M.-F. Bader, and D. Aunis. 1992. Chromostatin receptors control calcium channel activity in adrenal chromaffin cells. J. Biol. Chem. 267:407-412.
31. Galindo, E., A. Rill, M.-F. Bader, and D. Aunis. 1994. Chromostatin, a 20-amino acid peptide derived from chromogranin A, inhibits chromaffin cell secretion. Proc. Natl. Acad. Sci. USA. 91:832 (correction to Proc. Natl. Acad. Sci. USA. 1991. 88:1426-1430).
32. Greene, L.A., and A.S. Tischler. 1976. Establishment of a noradrenergic clonal cell line of rat adrenal pheochromocytoma cells which respond to a nerve growth factor. Proc. Natl. Acad. Sci. USA. 73:2424-2428.
33. Milligan, G. 1988. Techniques used in the identification and analysis of function of pertussis toxin-sensitive guanine nucleotide binding proteins. Biochem. J. 255:1-13.
34. Bader, M.-F., D. Thierse, D. Aunis, G. Ahnert-Hilger, and M. Gratzl. 1986. Characterization of hormone and protein release from alpha-toxin-permeabilized chromaffin cells in primary culture. J. Biol. Chem. 261:5777-5783.
35. Mahata, M., S.K. Mahata, R.J. Parmer, and D.T. O'Connor. 1996. Vesicular monoamine transport inhibitors. Novel action at calcium channels to prevent catecholamine secretion. Hypertension (Dallas). 28:414-420.
36. Smith, A.D., and H. Winkler. 1967. Purification and properties of an acidic protein from chromaffin granules of bovine adrenal medulla. Biochem. J. 103:483-492.
37. Syversen, U., H.L. Waldum, and D.T. O'Connor. 1992. Rapid, high-yield isolation of human chromogranin A from chromaffin granules of pheochromocytomas. Neuropeptides. 22:235-240.
38. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 7:248-254.
39. Merrifield, R.B. 1963. Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J. Am. Chem. Soc. 85:2149-2154.
40. Hagiwara, D., H. Miyake, H. Morimoto, M. Masako, T. Fujii, and M. Matsuo. 1992. Studies on neurokinin antagonists. 1. The design of novel tripeptides possessing the glutaminyl-D-tryptophylphenylalanine sequence as substance P antagonists. J. Med. Chem. 35:2015-2025.
41. Barbosa, J.A., B.M. Gill, M.A. Takiyyuddin, and D.T. O'Connor. 1991. Chromogranin A: posttranslational modifications in secretory granules. Endocrinology. 128:174-190.
42. Gill, B.M., J.A. Barbosa, R. Hogue-Angeletti, N. Varki, and D.T. O'Connor. 1992. Chromogranin A epitopes: clues from synthetic peptides and peptide mapping. Neuropeptides. 21:105-108.
43. O'Connor, D.T., R.P. Frigon, and R.L. Sokoloff. 1984. Human chromogranin A. Purification and characterization from catecholamine storage vesides of human pheochromocytoma. Hypertension (Dallas). 6:2-12.
44. + uptake and catecholamine secretion by primary cultures of adrenal medulla cells. J. Neurochem. 39:132-142.
45. 2+ influx mechanism. J. Biol. Chem. 262:16963-16968.
46. Taupenot, L., J. Ciesielski-Treska, G. Ulrich, S. Chasserot-Golaz, D. Aunis, and M.-F. Bader. 1996. Chromogranin A triggers a phenotypic transformation and the generation of nitric oxide in brain microglial cells. Neuroscience. 72:377-389.
47. O'Connor, D.T., and R.P. Frigon. 1984. Chromogranin A, the major catecholamine storage vesicle soluble protein: multiple size forms, subcellular storage and regional distribution in chromaffin and nervous tissue elucidated by radioimmunoassay. J. Biol. Chem. 259:3237-3247.
48. Molloy, S.S., P.A. Bresnahan, K. Klimpel, L. Leppla, and G. Thomas. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267:16396-16402.
49. Curry, W.J., C. Shaw, C.F. Johnston, L. Thim, and K.D. Buchanan. 1992. Isolation and primary structure of a novel chromogranin A-derived peptide. WE14, from a human midgut carcinoid tumour. FEBS Lett. 30:319-321.
50. Kirchmair, R., B. Leitner, R. Fischer-Colbrie, J. Marksteiner, R. Hogue-Angeletti, and H. Winkler. 1995. Large variations in the proteolytic formation of a chromogranin A-derived peptide (GE-25) in neuroendocrine tissues. Biochem. J. 310:331-336.
51. Sigafoos, J., W.G. Chestnut, B.M. Merrill, L.C. Taylor, E.J. Diliberto, Jr., and O.H. Viveros. 1993. Novel peptides from adrenomedullary chromaffin vesicles. J. Anal. 183:253-264.
52. Parmer, R.J., A.H. Koop, M.T. Handa, and D.T. O'Connor. 1989. Molecular cloning of chromogranin A from rat pheochromocytoma cells. Hypertension (Dallas.). 14:435-444.
53. Inoue, K., K. Nakazawa, M. Ohara-Imaizumi, T. Obama, K. Fujimori, and A. Takanaka. 1991. Antagonism by reactive blue 2 but not by brilliant blue G of extracellular ATP-evoked responses in PC12 phaeochromocytoma cells. Br. J. Pharmacol. 102:851-854.
54. Lin, L.F., M.C. Bott, L.-S. Kao, and E.W. Westhead. 1995. ATP stimulated catecholamine secretion: response in perfused adrenal glands and a subpopulation of cultured chromaffin cells. Neurosci. Lett. 183:147-150.
55. Conley, E.C. 1996. The Ion Channel FactsBook. I. Extracellular Ligand-Gated Channels. Academic Press, Inc., San Diego. 426 pg.
56. Cheung, N.S., P. Karlsson, J.X. Wang, M. Bienert, P. Oehme, and B.G. Livett. 1994. Functional studies with substance P analogues: effects of N-terminal, C-Terminal, and C-terminus-extended analogues of substance P on nicotine-induced secretion and desensitization in cultured bovine adrenal chromaffin cells. J. Neurochem. 62(6):2246-2253.
57. Livett, B.G., and P.D. Marley. 1993. Noncholinergic control of adrenal catecholamine secretion. J. Anal. 183(pt. 2):277-289.
58. Kirshner, N. 1987. Sodium and calcium channels in cultured bovine adrenal medulla cells. In Stimulus-Secretion Coupling in Chromaffin Cells. Volume II. K. Rosenheck and P.I. Lelkes, editors. CRC Press, Boca Raton, FL. 71-86.
59. McLane, K.E., X.D. Wu, and B.M. Conti-Tronconi. 1990. Identification of a brain acetylcholine receptor alpha subunit able to bind alpha-bungarotoxin. J. Biol. Chem. 265:9816-9824.
60. 3H]nicotine binding to a nicotinic cholinergic receptor on PC12 cells. Endocrinology. 130:825-830.
61. Rogers, S.W., A. Mandelzys, E.S. Deneris, C. Cooper, and S. Heinemann. 1992. The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J. Neurosci. 12:4611-4623.
62. Holst, J.J., C.G. Ostenson, H. Harling, and T. Messell. 1990. Porcine pancreastatin has no effect on endocrine secretion from the pig pancreas. Diabetologia 33(7):403-406.
63. Khalil, Z., P.D. Marley, and B.C. Livett. 1988. Effect of substance P on nicotine-induced desensitization of cultured bovine adrenal chromaffin cells: possible receptor subtypes. Brain Res. 459(2):282-288.
64. Blanton, M.P., Y.M. Li, E.R. Stimson, J.E. Maggio, and J.B. Cohen. 1994. Agonist-induced photoincorporation of a p-benzoylphenylalanine derivative of substance P into membrane-spanning region 2 of the Torpedo nicotinic acetylcholine receptor delta subunit. Mol. Pharmacol. 46(6):1048-1055.
65. Chattopadhyay, N., A. Mithal, and E.M. Brown. 1996. The calcium-sensing receptor: a window into the physiology and pathophysiology of mineral ion metabolism. Endocr. Rev. 17(4):289-307.
66. Winkler, H., D.K. Apps, and R. Fischer-Colbrie. 1986. The molecular function of adrenal chromaffin granules: established facts and unresolved topics. Neuroscience. 18:261-290.
67. Wightman, R.M. 1995. Kinetics of catecholamine release during exocytosis. International Symposium on Chromaffin Cell Biology, 8th, Edinburgh. S-25:66.