Human ACE and bradykinin B2 receptors form a complex at the plasma membrane

FASEB Journal

Volumn 20, Issue 13, 2006, Pages 2261-2270

  Chen, Zhenlong ^a   Deddish, Peter A ^a   Minshall, Richard D ^a   Becker, Robert P ^a   Erdös, Ervin G ^a,b   Tan, Fulong ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b Department of Pharmacology ^*  (United States)

Author keywords

Converting enzyme; FRET; Kinins; Oligomer; Peptide receptors

Indexed keywords

BRADYKININ; BRADYKININ B2 RECEPTOR; BRADYKININ RECEPTOR AGONIST; CYAN FLUORESCENT PROTEIN; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GREEN FLUORESCENT PROTEIN; HETERODIMER; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; BLEACHING; CELL MEMBRANE; CHO CELL; DRUG ACTIVITY; DRUG MECHANISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE; CHO CELLS; CRICETINAE; DIMERIZATION; DNA PRIMERS; DNA, COMPLEMENTARY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; PEPTIDYL-DIPEPTIDASE A; RECEPTOR, BRADYKININ B2; RECOMBINANT FUSION PROTEINS;

EID: 33845601598     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-6113com     Document Type: Article

References (51)

1. Webster, M. E. (1970) Kallikreins in glandular tissues. In Bradykinin, Kallidin and Kallikrein. Handbook of Experimental Pharmacology (Erdös, E. G., ed) Vol. XXV, pp. 131-155, Springer Verlag, Heidelberg
2. Werle, E. (1970) Discovery of the most important kallikreins and kallikrein inhibitors. In Handbook of Experimental Pharmacology (Erdös, E. G., ed) Vol. XXV, pp. 1-6, Springer-Verlag, Heidelberg
3. Beraldo, W. T., and Andrade, S. P. (1997) Discovery of bradykinin and the kallikrein-kinin system. In The Kinin System (Farmer, S. G., ed) pp. 1-8, Academic Press Ltd., San Diego, CA, USA
4. Page, I. H. (1988) Hypertension Research. A Memoir 1920-1960, pp. 1-167, Pergamon Press, New York
5. Yang, H. Y. T., and Erdös, E. G. (1967) Second kininase in human blood plasma. Nature 215, 1402-1403
6. Yang, H. Y. T., Erdös, E. G., and Levin, Y. (1970) A dipeptidyl carboxypeptidase that converts angiotensin I and inactivates bradykinin. Biochim. Biophys. Acta 214, 374-376
7. Gavras, H. P., Faxon, D. P., Berkoben, J., Brunner, H. R., and Ryan, T. J. (1978) Angiotensin converting enzyme inhibition in patients with congestive heart failure. Circulation 58, 770-776
8. Couture, R., and Girolami, J.-P. (2004) Putative roles of kinin receptors in the therapeutic effects of angiotensin 1-converting enzyme inhibitors in diabetes mellitus. Eur. J. Pharmacol. 500, 467-485
9. Yusuf, S., Sleight, P., Pogue, J., Bosch, J., Davies, R., and Dagenais, G. (2000) Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 342, 145-153
10. Pfeffer, M. (2001) Angiotensin-converting enzyme (ACE) inhibitors in the prevention of cardiovascular disease: clinical evidence. In Angiotensin- Converting Enzyme (ACE): Clinical and Experimental Insights (Giles, T. D., ed) pp. 219-225, Health Care Communications, Inc., Fort Lee, NJ, USA
11. Solomon, S. D., Skali, H., Bourgoun, M., Fang, J., Ghali, J. K., Martelet, M., Wojciechowski, D., Ansmite, B., Skards, J., Laks, T., et al. (2005) Effect of angiotensin-converting enzyme or vasopeptidase inhibition on ventricular size and function in patients with heart failure: the omapatrilat versus enalapril randomized trial of utility in reducing events (overture) echocardiographic study. Am. Heart J. 150, 257-262
12. Bosch, J., Lonn, E., Pogue, J., Arnold, J. M., Dagenais, G. R., and Yusuf, S. (2005) Long-term effects of ramipril on cardiovascular events and on diabetes: results of the HOPE study extension. Circulation 112, 1339-1346
13. Barbe, F., Su, J. B., Guyene, T. T., Crozatier, B., Menard, J., and Hittinger, L. (1996) Bradykinin pathway is involved in acute hemodynamic effects of enalaprilat in dogs with heart failure. Am. J. Physiol. 270, H1985-H1992
14. Hornig, B., Kohler, C., and Drexler, H. (1997) Role of bradykinin in mediating vascular effects of angiotensin-converting enzyme inhibitors in humans. Circulation 95, 1115-1118
15. Erdös, E. G., Deddish, P. A., and Marcic, B. M. (1999) Potentiation of bradykinin actions by ACE inhibitors. Trends Endocrinol. Metab. 10, 223-229
16. Minshall, R. D., Tan, F., Nakamura, F., Rabito, S. F., Becker, R. P., Marcic, B., and Erdös, E. G. (1997) Potentiation of the actions of bradykinin by angiotensin I converting enzyme (ACE) inhibitors. The role of expressed human bradykinin B2 receptors and ACE in CHO cells. Circ. Res. 81, 848-856
17. Marcic, B., Deddish, P. A., Skidgel, R. A., Erdös, E. G., Minshall, R. D., and Tan, F. (2000) Replacement of the transmembrane anchor in angiotensin I-converting enzyme (ACE) with a glycosylphosphatidylinositol tail affects activation of the B2 bradykinin receptor by ACE inhibitors. J. Biol. Chem. 275, 16110-16118
18. 2 receptor. Hypertension 33, 835-843
19. Chen, Z., Tan, F., Erdös, E. G., and Deddish, P. A. (2005) Hydrolysis of angiotensin peptides by human angiotensin I-converting enzyme and the resensitization of B2 kinin receptors. Hypertension 46, 1368-1373
20. Changeux, J. P., and Edelstein, S. J. (2005) Allosteric mechanisms of signal transduction. Science 308, 1424-1428
21. Siegel, R. M., Chan, F. K., Zacharias, D. A., Swofford, R., Holmes, K. L., Tsien, R. Y., and Lenardo, M. J. (2000) Measurement of molecular interactions in living cells by fluorescence resonance energy transfer between variants of the green fluorescent protein. Sci. STKE 2000, PL1
22. Bastiaens, P. I., Majoul, I. V., Verveer, P. J., Soling, H. D., and Jovin, T. M. (1996) Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J. 15, 4246-4253
23. Deddish, P. A., Jackman, H. L., Skidgel, R. A., and Erdös, E. G. (1997) Differences in the hydrolysis of enkephalin congeners by the two domains of angiotensin converting enzyme. Biochem. Pharmacol. 53, 1459-1463
24. Herrick-Davis, K., Grinde, E., and Mazurkiewicz, J. E. (2004) Biochemical and biophysical characterization of serotonin 5-HT2C receptor homodimers on the plasma membrane of living cells. Biochemistry 43, 13963-13971
25. Ferreira, S. H. (1966) Bradykinin-potentiating factor. In Hypotensive Peptides. Proceedings of the International Symposium. Firenze, Italy, 1965 (Erdös, E. G., Back, N., and Sicuteri, F., eds) pp. 356-367, Springer-Verlag, New York
26. Vogel, R., Werle, E., and Zickgraf-Rüdel, G. (1970) Neure Aspekte der Kininforschung. I. Potenzierung und Blockierung der biologischen Kininwirkung. Z. klin. Chem. u. klin. Biochem. 8, 177-185
27. Mueller, S., Gothe, R., Siems, W. D., Vietinghoff, G., Paegelow, I., and Reissmann, S. (2005) Potentiation of bradykinin actions by analogues of the bradykinin potentiating nonapeptide BPP9alpha. Peptides 26, 1235-1247
28. Rubin, B., Laffan, R. J., Kotler, D. G., O'Keefe, E. H., Demaio, D. A., and Goldberg, M. E. (1978) SQ14,225 (D-3-mercapto-2-methylpropanoyl-L-proline), a novel orally active inhibitor of angiotensin I-converting enzyme. J. Pharmacol. Exp. Ther. 204, 271-280
29. Erdös, E. G., and Skidgel, R. A. (1997) Metabolism of bradykinin by peptidases in health and disease. In The Kinin System (Farmer, S. G., ed) pp. 111-141, Academic Press, San Diego, CA, USA
30. Marcic, B. M., and Erdös, E. G. (2000) Protein kinase C and phosphatase inhibitors block the ability of angiotensin I-converting enzyme inhibitors to resensitize the receptor to bradykinin without altering the primary effects of bradykinin. J. Pharmacol. Exp. Ther. 294, 605-612
31. Ignjatovic, T., Stanisavljevic, S., Brovkovych, V., Skidgel, R. A., and Erdös, E. G. (2004) Kinin B1 receptors stimulate nitric oxide production in endothelial cells: signaling pathways activated by angiotensin I-converting enzyme inhibitors and peptide ligands. Mol. Pharmacol. 66, 1310-1316
32. Ignjatovic, T., Tan, F., Brovkovych, V., Skidgel, R. A., and Erdös, E. G. (2002) Novel mode of action of angiotensin I converting enzyme inhibitors. Direct activation of bradykinin B1 receptor. J. Biol. Chem. 277, 16847-16852
33. Stanisavljevic, S., Ignjatovic, T., Deddish, P. A., Brovkovych, V., Zhang, K., Erdös, E. G., and Skidgel, R. A. (2006) Angiotensin I-converting enzyme inhibitors block PKCε by activating bradykinin B1 receptors in human endothelial cells. J. Pharmacol. Exp. Ther. 316, 1153-1158
34. Marianayagam, N. J., Sunde, M., and Matthews, J. M. (2004) The power of two: protein dimerization in biology. Trends Biochem. Sci. 29, 618-625
35. Salahpour, A., Angers, S., Mercier, J.-F., Lagace, M., Marullo, S., and Bouvier, M. (2004) Homodimerization of the β2-adrenergic receptor as a prerequisite for cell surface targeting. J. Biol. Chem. 279, 33390-33397
36. Pfeiffer, M., Kirscht, S., Stumm, R., Koch, T., Wu, D., Laugsch, M., Schroder, H., Hollt, V., and Schulz, S. (2003) Heterodimerization of substance P and μ-opioid receptors regulates receptor trafficking and resensitization. J. Biol. Chem. 278, 51630-51637
37. Deddish, P. A., Marcic, B. M., Tan, F., Jackman, H. L., Chen, Z., and Erdös, E. G. (2002) Neprilysin inhibitors potentiate effects of bradykinin on B2 receptor. Hypertension 39, 619-623
38. Valentin, G., Verheggen, C., Piolot, T., Neel, H., Coppey-Moisan, M., and Bertrand, E. (2005) Photoconversion of YFP into a CFP-like species during acceptor photobleaching FRET experiments. Nature Methods 2, 801
39. Erdös, E. G., and Gafford, J. T. (1983) Human converting enzyme. Clin. Exp. Hypertension A5, 1251-1262
40. Corvol, P., Eyries, M., and Soubrier, F. (2004) Peptidyl-dipeptidase A/angiotensin I-converting enzyme. In Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Vol. 1, pp. 332-346, Academic Press, San Diego, CA, USA
41. Skidgel, R. A., and Erdös, E. G. (1993) Biochemistry of angiotensin converting enzyme. In The Renin-Angiotensin System (Robertson, J. I. S., and Nicholls, M. G., eds) Vol. 1, pp. 10.10-10.11, Gower Medical Publishers, London, England
42. Jaspard, E., Wei, L., and Alhenc-Gelas, F. (1993) Differences in the properties and enzymatic specificities of the two active sites of angiotensin I-converting enzyme (kininase II). Studies with bradykinin and other natural peptides. J. Biol. Chem. 268, 9496-9503
43. Soubrier, F., Alhenc-Gelas, F., Hubert, C., Allegrini, J., John, M., Tregear, G., and Corvol, P. (1988) Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc. Natl. Acad. Sci. U. S. A. 85, 9386-9390
44. Kohlstedt, K., Busse, R., and Fleming, I. (2005) Signaling via the angiotensin-converting enzyme enhances the expression of cyclooxygenase-2 in endothelial cells. Hypertension 45, 126-132
45. Frohlich, E. D., and Re, R. N., eds (2006) The Local Cardiac Renin Angiotensin-Aldosterone System, pp. 1-224, Springer Science + Business Media, Inc., New York
46. Cruden, N. L. M., Witherow, F. N., Webb, D. J., Fox, K. A. A., and Newby, D. E. (2004) Bradykinin contributes to the systemic hemodynamic effects of chronic angiotensin-converting enzyme inhibition in patients with heart failure. Arterioscler. Thromb. Vasc. Biol. 24, 1043-1048
47. Bhoola, K. D., Figueroa, C. D., and Worthy, K. (1992) Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44, 1-80
48. Witherow, F. N., Helmy, A., Webb, D. J., Fox, K. A. A., and Newby, D. E. (2001) Bradykinin contributes to the vasodilator effects of chronic angiotensin-converting enzyme inhibition in patients with heart failure. Circulation 104, 2177-2181
49. Peng, H., Carretero, O. A., Vuljaj, N., Liao, T. D., Motivala, A., Peterson, E. L., and Rhaleb, N. E. (2005) Angiotensin-converting enzyme inhibitors: a new mechanism of action. Circulation 112, 2436-2445
50. Tschöpe C., Schultheiss, H. P., and Walther, T. (2002) Multiple interactions between the renin-angiotensin and the kallikreinkinin systems: role of ACE inhibition and the AT1 receptor blockade. J. Cardiovasc. Pharmacol. 39, 478-487
51. Auch-Schwelk, W., Bossaller, C., Claus, M., Graf, K., Gräfe, M., and Fleck, E. (1993) ACE inhibitors are endothelium dependent vasodilators of coronary arteries during submaximal stimulation with bradykinin. Cardiovasc. Res. 27, 312-317