Influence of Bradykinin on Catecholamine Release from the Rat Adrenal Medulla

  • Lim, Dong-Yoon (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Kim, Il-Hwan (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Na, Gwang-Moon (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Kang, Moo-Jin (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Kim, Ok-Min (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Choi, Deok-Ho (Department of Pharmacology, College of Medicine, Chosun University) ;
  • Ki, Young-Woo (Department of Pharmacology, College of Medicine, Chosun University)
  • Published : 2003.08.21

Abstract

The present study was undertaken to investigate the effect of bradykinin on secretion of catecholamines (CA) evoked by stimulation of cholinergic receptors and membrane depolarization from the isolated perfused model of the rat adrenal glands, and to elucidate its mechanism of action. Bradykinin $(3{\times}10^{-8}M)$ alone produced a weak secretory response of the CA. however, the perfusion with bradykinin $(3{\times}10^{-8}M)$ into an adrenal vein of the rat adrenal gland for 90 min enhanced markedly the secretory responses of CA evoked by ACh $(5.32{\times}10^{-3}M)$, excess $K^+$ ($5.6{\times}10^{-2}M$, a membrane depolarizer), DMPP ($10^{-4}$ M, a selective neuronal nicotinic agonist) and McN-A-343 ($10^{-4}$ M, a selective M1-muscarinic agonist). Moreover, bradykinin ($3{\times}10^{-8}$ M) in to an adrenal vein for 90 min also augmented the CA release evoked by BAY-K-8644, an activator of the dihydropyridine L-type $Ca^{2+}$ channels. However, in the presence of $(N-Methyl-D-Phe^7)$-bradykinin trifluoroacetate salt $(3{\times}10^{-8}M)$, an antagonist of $BK_2$-bradykinin receptor, bradykinin no longer enhanced the CA secretion evoked by Ach and high potassium whereas the pretreatment with Lys-$(des-Arg^9,\;Leu^9)$-bradykinin trifluoroacetate salt $(3{\times}10^{-8}M)$, an antagonist of $BK_1$-bradykinin receptor did fail to affect them. Furthermore, the perfusion with bradykinin $(3{\times}10^{-6}M)$ into an adrenal vein of the rabbit adrenal gland for 90 min enhanced markedly the secretory responses of CA evoked by excess $K^+$ $(5.6{\times}10^{-2}M)$. Collectively, these experimental results suggest that bradykinin enhances the CA secretion from the rat adrenal medulla evoked by cholinergic stimulation (both nicotininc and muscarinic receptors) and membrane depolarization through the activation of $B_2$-bradykinin receptors, not through $B_1$-bradykinin receptors. This facilitatory effect of bradykinin seems to be associated to the increased $Ca^{2+}$ influx through the activation of the dihydropyridine L-type $Ca^{2+}$ channels.

Keywords

References

  1. Akaike A, Mine Y, Sasa M, Takaori S. Voltage and current clamp studies of muscarinic and nicotinic excitation of the rat adrenal chromaffin cells. J Pharmacol Expt Ther 255: 333-339, 1990
  2. Anton AH, Sayre DF. A study of the factors affecting the aluminum oxide trihydroxy indole procedure for the analysis of catecholamines. J Pharmacol Exp Ther 138: 360-375, 1962
  3. Appell KC, Barefoot DS. Neurotransmitter release from bradykinin- stimulated PC12 cells. Stimulation of cytosolic calcium and neurotransmitter release. Biochem J 263(1): 11-18, 1989 https://doi.org/10.1042/bj2630011
  4. Berridge MJ, Irvine RF. Inositol phosphates and cell signalling. Nature (Lond) 341: 197-205, 1989 https://doi.org/10.1038/341197a0
  5. Braas KM, Manning DC, Perry DC, Snyder SH. Bradykinin analogues: differential agonist and antagonist activities suggesting multiple receptors. Br J Pharmacol 94: 3-5, 1988 https://doi.org/10.1111/j.1476-5381.1988.tb11492.x
  6. Burgoyne RD. Mechanism of secretion from adrenal chromaffin cells. Biochem Biophys Acta 779: 201-216, 1984 https://doi.org/10.1016/0304-4157(84)90009-1
  7. Challis RAJ, Jones JA, Owen PJ, Boarder MR. Changes in inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate mass accumulations in cultured adrenal chromaffin cells in response to bradykinin and histamine. J Neurochem 56: 1083-1086, 1991 https://doi.org/10.1111/j.1471-4159.1991.tb02033.x
  8. Chulak C, Couture R, Foucart S. Modulatory effect of bradykinin on the release of noradrenaline from rat isolated atria. Br J Pharmacol 115: 330-334, 1995 https://doi.org/10.1111/j.1476-5381.1995.tb15881.x
  9. Clementi E, Scheer H, Zacchetti D, Fasolato C, Pozzan T, Meldolesi J. Receptor-activated Ca2$^+$ influx. J Biol Chem 4: 2164-2172, 1992
  10. Dendorfer A, Dominiak P. Characterisation of bradykinin receptors mediating catecholamine release in PC12 cells. Naunyn- Schmiedeberg's Arch Pharmacol 351: 274-281, 1995
  11. Dendorfer A, Fitschen M, Raasch W, Tempel K, Dominiak P. Mechanisms of bradykinin-induced catecholamine release in pithed spontaneously hypertensive rats. Immunopharmacology 44(1-2): 99-104, 1999 https://doi.org/10.1016/S0162-3109(99)00114-9
  12. Di Virgilio F, Milani D, Leon A, Meldolesi J, Pozzan T. Voltagedependent activation and inactivation of calcium channels in PC12 cells. Correlation with neurotransmitter release. J Biol Chem 262(19): 9189-9195, 1987
  13. Dray A, Bettaney J, Forster P, Perkins MN. Activation of a bradykinin receptor in peripheral nerve and spinal cord in the neonatal rat in vitro. Br J Pharmacol 95: 1008-1010, 1988 https://doi.org/10.1111/j.1476-5381.1988.tb11732.x
  14. Fasolato C, Pandiella A, MeMolesi J, Pozzan T. Generation of inositol phosphates, cytosolic Ca2$^+$, and ionic fluxes in PC12 cells treated with bradykinin. J Biol Chem 263(33): 17350-17359, 1988
  15. Gandia L, Borges R, Albillos A, Garcia AG. Multiple calcium channel subtypes in isolated rat chromaffin cells. Pflgers Arch 430: 55-63, 1995. https://doi.org/10.1007/BF00373839
  16. Garcia AG, Sala F, Reig JA, Viniegra S, Frias J, Fonteriz R, Gandia L. Dihydropyridine Bay-K-8644 activates chromaffin cell calcium channels. Nature 309: 69-71, 1984. https://doi.org/10.1038/309069a0
  17. Greene LA, Rein G. Release of (3H)norepinephrine from a clonal line of pheochromocytoma cells (PC12) by nicotinic cholinergic stimulation. Brain Res 138(3): 521-528, 1977 https://doi.org/10.1016/0006-8993(77)90687-4
  18. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73: 2424-2428, 1976 https://doi.org/10.1073/pnas.73.7.2424
  19. Grohovaz F, Zacchetti D, Clementi E, Lorenzon P, Meldolesi J, Fumagalli G. $[Ca^{2+}]_i$ imaging in PC12 cells: Multiple response patterns to receptor activation reveal new aspects of transmembrane signaling. J Cell Biol 113: 1341-1350, 1991 https://doi.org/10.1083/jcb.113.6.1341
  20. Hammer R, Giachetti A. Muscarinic receptor subtypes: M1 and M2 biochemical and functional characterization. Life Sci 31: 2992-2998, 1982
  21. Hatta E, Maruyama R, Marshall SJ, Imamura M, Levi R. Bradykinin promotes ischemic norepinephrine release in guinea pig and human hearts. J Pharmacol Exp Ther 288(3): 919-927, 1999
  22. Ilno M. Calcium-induced calcium release mechanism in guinea pig taenia caeci. J Gen Physiol 94: 363-383, 1989 https://doi.org/10.1085/jgp.94.2.363
  23. Inoue M, Kuriyama H. Muscarinic receptor is coupled with a cation channel through a GTP-binding protein in guinea-pig chromaffin cells. J Physiol (Lond) 436: 511-529, 1991 https://doi.org/10.1113/jphysiol.1991.sp018564
  24. Kim KT, Westhead EW. Cellular responses to Ca2$^+$ from extracellular and intracellular sources are different as shown by simultaneous measurements of cytosolic Ca2$^+$ and secretion from bovine chromaffin cells. Proc Natl Acad Sci USA 86: 9881-9885, 1989 https://doi.org/10.1073/pnas.86.24.9881
  25. Kimura T, Shimamura T, Satoh S. Effects of pirenzepine and hexamethonium on adrenal catecholamine release in responses to endogenous and exogenous acetylcholine in anesthetized dogs. J Cardiovasc Pharmacol 20: 870-874, 1992 https://doi.org/10.1097/00005344-199212000-00004
  26. Kuo YJJ, Keeton TK. Captopril increases norepinephrine spillover rate in conscious spontaneously hypertensive rats. J Pharmacol Exp Ther 258: 223-231, 1991
  27. Lim DY, Hwang DH. Studies on secretion of catecholamines evoked by DMPP and McN-A-343 in the rat adrenal gland. Korean J Pharmacol 27(1): 53-67, 1991
  28. Li Q, Zhang J, Loro JF, Pfaffendorf M, van Zwieten PA. Bradykinin B2-receptor-mediated positive chronotropic effect of bradykinin in isolated rat atria. J Cardiovasc Pharmacol 32(3): 452-456, 1998 https://doi.org/10.1097/00005344-199809000-00016
  29. Llona I, Vavrek R, Stewart J, Huidobro-Toro JP. Identification of pre-and postsynaptic bradykinin receptor sites in the vas deferens: evidence for different structural prerequisites. J Pharmacol Exp Ther 24l: 608-614, 1987
  30. Llona L, Gallegllinos X, Belmar J, Huidobro-Toro JP. Bradykinin modulates the release of noradrenaline from vas deferens nerve terminals. Life Sci 48: 2585-2592, 1991 https://doi.org/10.1016/0024-3205(91)90616-J
  31. MacNeil T, Feighner S, Hreniuk DL, Hess JF, Van der Ploeg LH. Partial agonists and full antagonists at the human and murine bradykinin B1 receptors. Can J Physiol Pharmacol 75(6): 735- 740, 1997 https://doi.org/10.1139/cjpp-75-6-735
  32. McDonald RL, Kaye DF, Reeve HL, Ball SG, Peers C, Vaughan PFT. Bradykinin-evoked release of $[^3H]$noradrenaline from the human neuroblastoma SH-SY5Y. Biochem Pharmacol 48: 23-30, 1994 https://doi.org/10.1016/0091-3057(94)90492-8
  33. Misbahuddin M, Oka M. Muscarinic stimulation of guinea pig adrenal chromaffin cells stimulates catecholamine secretion without significant increase in Ca2$^+$ uptake. Neurosci Lett 87: 266-270, 1988 https://doi.org/10.1016/0304-3940(88)90459-4
  34. Nakazato Y, Oleshanskly M, Tomita U, Yamada Y. Voltage-independent catecholamine release mediated by the activation of muscarinic receptors in guinea-pig adrenal glands. Br J Pharmacol 93: 101-109, 1988 https://doi.org/10.1111/j.1476-5381.1988.tb11410.x
  35. Pozzan T, Gatti G, Dozio N, Vicemini, LM, Meldolesi J. Ca2$^+$-dependent and -lndependent release of neurotransmitters from PCI2 cells: A role for protein kinase C activation. J Cell Biol 99: 628-638, 1984 https://doi.org/10.1083/jcb.99.2.628
  36. Purkiss JR, Nahorski SR, Willars GB. Mobilization of inositol 1,4,5-trisphosphate-sensitive $Ca^{2+}$ stores supports bradykininand muscarinic-evoked release of [3H] noradrenaline from SHSY5Y cells. J Neurochem 64(3): 1175-1182, 1995 https://doi.org/10.1046/j.1471-4159.1995.64031175.x
  37. Rabe CS, Delorme E, Weight FF. Muscarine-stimulated neurotransmitter release from PC12 cells. J Pharmacol Exp Ther 243(2): 534-541, 1987
  38. Ransom JT, Cherwinski HlA, Dunne JF, Sharif NA. Flow cytometric analysis of internal calcium mobilization via a B2-bradykinin receptor on a subclone of PC12 cells. J Neurochem 56: 983-989, 1991 https://doi.org/10.1111/j.1471-4159.1991.tb02018.x
  39. Regoli D, Jukic D, Gobeil F, Rhaleb NE. Receptors for bradykinin and related kinins: a critical analysis. Can J Physiol Pharmacol 71: 556-567, 1993 https://doi.org/10.1139/y93-079
  40. Reissmann S, Schwuchow C, Seyfarth L, De Castro LFP, Liebmann C, Paegelow I, Werner H, Stewart JM. Highly selective bradykinin agonists and antagonists with replacement of proline residues by N-methyl-D- and L-phenylalanine. J Med Chem 39(4): 929-936, 1996 https://doi.org/10.1021/jm9301954
  41. Ritchi AK. Catecholamine secretion in a rat pheochromocytoma cell line: Two pathways for calcium entry. J Physiol 286: 541-561, 1979 https://doi.org/10.1113/jphysiol.1979.sp012636
  42. Schramm M, Thomas G, Towart R, Franckowiak G. Novel dihydropyridines with positive inotropic action through activation of Ca2$^+$ channels. Nature 303: 535-537, 1982 https://doi.org/10.1038/303535a0
  43. Schwieler JH, Kahan T, Nussberger J, Hjemdahl P. Converting enzyme inhibition modulates sympathetic neurotransmission in vivo via multiple mechanisms. Am J Physiol 264(4 Pt 1): E631- 637, 1993
  44. Starke K, Peskar BA, Schumacher KA, Taube JD. Bradykinin and postganglionic sympathetic transmission. Naunyn-Schmiedeberg's Arch Pharmacol 299: 23-32, 1977 https://doi.org/10.1007/BF00508633
  45. Suzuki M, Muraki K, Imaizumi Y, Watanabe M. Cyclopiazonic acid, an inhibitor of the sarcoplasmic reticulum Ca2$^+$-pump, reduces Ca2$^+$-dependent K$^+$ currents in guinea-pig smooth muscle cells. Br J Pharmacol 107: 134-140, 1992 https://doi.org/10.1111/j.1476-5381.1992.tb14475.x
  46. Tallarida RJ, Murray RB. Manual of pharmacologic calculation with computer programs. 2nd Ed. New York, Speringer-Verlag, p 132, 1987
  47. Uceda G, Artalejo AR, de la Fuente MT, Lopez MG, Albillos A, Michelena P, Garcia AG, Montiel C. Modulation by L-type Ca2$^+$ channels and apamin-sensitive K$^+$ channels of muscarinic responses in cat chromaffin cells. Am J Physiol 266(5 Pt 1): C1432 -1439, 1994 https://doi.org/10.1152/ajpcell.1994.266.5.C1432
  48. Uyama Y, Imaizumi Y, Watanabe M. Effects of cyclopiazonic acid, a novel Ca2+-ATPase inhibitor on contractile responses in skinned ileal smooth muscle. Br J Pharmacol 106: 208-214, 1992 https://doi.org/10.1111/j.1476-5381.1992.tb14316.x
  49. van Calker D, Assmann K, Greil W. Stimulation by bradykinin, angiotensin II, and carbachol of the accumulation of inositol phosphates in PC-12 pheochromocytoma cells: differential effects of lithium ions on inositol mono- and polyphosphates. J Neurochem 49(5): 1379-1385, 1987 https://doi.org/10.1111/j.1471-4159.1987.tb01003.x
  50. Vicentini LM, Ambrosini A, Di Virgilio F, Pozzan T, Meldolesi J. Muscarinic receptor-induced phosphoinositide hydrolysis at resting cytosolic Ca2$^+$ concentration in PC12 cells. J Cell Biol 100(4): 1330-1333, 1985 https://doi.org/10.1083/jcb.100.4.1330
  51. Wada Y, Satoh K, Taira N. Cardiovascular profile of Bay-K-8644, a presumed calcium channel activator in the dog. Naunyn- Schmiedebergs Arch Pharmacol 328: 382-387, 1985 https://doi.org/10.1007/BF00692905
  52. Wakade AR. Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol 313: 463-480, 1981 https://doi.org/10.1113/jphysiol.1981.sp013676
  53. Warashina A. Potentiation by indomethacin of receptor-mediated catecholamine secretion in rat adrenal medulla. Jpn J Pharmacol 73: 197-205, 1997 https://doi.org/10.1254/jjp.73.197
  54. Weiss C, Atlas D. The bradykinin receptor-a putative receptoroperated channel in PCl 2 cells: studies of neurotransmitter release and inositol phosphate accumulation. Brain Res 543(1): 102-110, 1991 https://doi.org/10.1016/0006-8993(91)91053-4
  55. Yamada Y, Teraoka H, Nakazato Y, Ohga A. Intracellular Ca2$^+$ antagonist TMB-8 blocks catecholamine secretion evoked by caffeine and acetylcholine from perfused cat adrenal glands in the absence of extracellular ca2$^+$. Neurosci Lett 90: 338-342, 1988 https://doi.org/10.1016/0304-3940(88)90212-1