Structural insights into central hypertension regulation by human aminopeptidase A

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25638-25645

  Yang, Yang ^a   Liu, Chang ^a   Lin, Yi Lun ^a   Li, Fang ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC RESIDUES; AMINO PEPTIDASE; CALCIUM BINDING; N-TERMINALS; STRUCTURAL INSIGHTS; SUBSTRATE SPECIFICITY;

BIOCHEMISTRY; BIOLOGY;

CALCIUM;

AMASTATIN; ANGIOTENSIN II; ANGIOTENSIN III; BESTATIN; CALCIUM; GLUTAMYL AMINOPEPTIDASE;

ANIMAL CELL; ARTICLE; BINDING SITE; BLOOD PRESSURE REGULATION; CALCIUM BINDING; COMPLEX FORMATION; CRYSTAL STRUCTURE; DRUG POTENCY; ENZYME ACTIVITY; ENZYME SPECIFICITY; HYPERTENSION; NONHUMAN; PRIORITY JOURNAL;

AMINOPEPTIDASE; CALCIUM-BINDING PROTEINS; HYPERTENSION; PROTEIN STRUCTURE; X-RAY CRYSTALLOGRAPHY;

ANTIHYPERTENSIVE AGENTS; BINDING SITES; CALCIUM; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLUTAMYL AMINOPEPTIDASE; HUMANS; HYPERTENSION; PEPTIDES; PROTEASE INHIBITORS; SUBSTRATE SPECIFICITY;

EID: 84883383965     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.494955     Document Type: Article

References (42)

1. Kearney, P. M., Whelton, M., Reynolds, K., Muntner, P., Whelton, P. K., and He, J. (2005) Global burden of hypertension: analysis of worldwide data. Lancet 365, 217-223
2. Calhoun, D. A., Jones, D., Textor, S., Goff, D. C., Murphy, T. P., Toto, R. D., White, A., Cushman, W. C., White, W., Sica, D., Ferdinand, K., Giles, T. D., Falkner, B., and Carey, R. M. (2008) Resistant hypertension: diagnosis, evaluation, and treatment. A scientific statement from the American Heart Association Professional Education Committee of the Council for High Blood Pressure Research. Hypertension 51, 1403-1419
3. Radevski, I., Skudicky, D., Candy, G., Sathekge, S., Strugo, V., and Sareli, P. (1999) Antihypertensive monotherapy with nisoldipine CC is superior to enalapril in black patients with severe hypertension. Am. J. Hypertens. 12, 194-203
4. Saunders, E., Weir, M. R., Kong, B. W., Hollifield, J., Gray, J., Vertes, V., Sowers, J. R., Zemel, M. B., Curry, C., Schoenberger, J., Wright, J. T., Kirkendall, W., Conradi, E. C., Jenkins, P., McLean, B., Massie, B., Berenson, G., and Flamenbaum, W. (1990) A comparison of the efficacy and safety of a β-blocker, a calcium channel blocker, and a converting enzyme inhibitor in hypertensive blacks. Arch. Intern. Med. 150, 1707-1713
5. Matchar, D. B., McCrory, D. C., Orlando, L. A., Patel, M. R., Patel, U. D., Patwardhan, M. B., Powers, B., Samsa, G. P., and Gray, R. N. (2008) Systematic review: comparative effectiveness of angiotensin-converting enzyme inhibitors and angiotensin II receptor blockers for treating essential hypertension. Ann. Intern. Med. 148, 16-29
6. Saine, D. R., and Ahrens, E. R. (1996) Renal impairment associated with losartan. Ann. Intern. Med. 124, 7755
7. Basso, N., Ruiz, P., Mangiarua, E., and Taquini, A. C. (1981) Renin-like activity in the rat brain during the development of DOC-salt hypertension. Hypertension 3, 11-14
8. Ganten, D., Hermann, K., Bayer, C., Unger, T., and Lang, R. E. (1983) Angiotensin synthesis in the brain and increased turnover in hypertensive rats. Science 221, 869-871
9. Guyenet, P. G. (2006) The sympathetic control of blood pressure. Nat. Rev. Neurosci. 7, 335-346
10. Bakris, G., Bursztyn, M., Gavras, I., Bresnahan, M., and Gavras, H. (1997) Role of vasopressin in essential hypertension: racial differences. J. Hypertens. 15, 545-550
11. Zaman, M. A., Oparil, S., and Calhoun, D. A. (2002) Drugs targeting the renin-angiotensin-aldosterone system. Nat. Rev. Drug Discov. 1, 621-636
12. Oparil, S., and Haber, E. (1974) The renin-angiotensin system (first of two parts). N. Engl. J. Med. 291, 389-401
13. Zini, S., Fournié-Zaluski, M. C., Chauvel, E., Roques, B. P., Corvol, P., and Llorens-Cortès, C. (1996) Identification of metabolic pathways of brain angiotensin II and III using specific aminopeptidase inhibitors: predominant role of angiotensin III in the control of vasopressin release. Proc. Natl. Acad. Sci. U.S.A. 93, 11968-11973
14. Réaux, A., de Mota, N., Zini, S., Cadel, S., Fournié- Zaluski, M. C., Roques, B. P., Corvol, P., and Llorens-Cortès, C. (1999) PC18, a specific aminopeptidaseNinhibitor, induces vasopressin release by increasing the half-life of brain angiotensin III. Neuroendocrinology 69, 370-376
15. Zini, S., Demassey, Y., Fournié-Zaluski, M. C., Bischoff, L., Corvol, P., Llorens-Cortès, C., and Sanderson, P. (1998) Inhibition of vasopressinergic neurons by central injection of a specific aminopeptidase A inhibitor. Neuroreport 9, 825-828
16. Bodineau, L., Frugière, A., Marc, Y., Inguimbert, N., Fassot, C., Balavoine, F., Roques, B., and Llorens-Cortès, C. (2008) Orally active aminopeptidase A inhibitors reduce blood pressure: a new strategy for treating hypertension. Hypertension 51, 1318-1325
17. Reaux, A., Fournié-Zaluski, M. C., David, C., Zini, S., Roques, B. P., Corvol, P., and Llorens-Cortès, C. (1999) Aminopeptidase A inhibitors as potential central antihypertensive agents. Proc. Natl. Acad. Sci. U.S.A. 96, 13415-13420
18. Fournié-Zaluski, M. C., Fassot, C., Valentin, B., Djordjijevic, D., Reaux-Le Goazigo, A., Corvol, P., Roques, B. P., and Llorens-Cortès, C. (2004) Brain renin-angiotensin system blockade by systemically active aminopeptidase A inhibitors: a potential treatment of salt-dependent hypertension. Proc. Natl. Acad. Sci. U.S.A. 101, 7775-7780
19. Marc, Y., Gao, J., Balavoine, F., Michaud, A., Roques, B. P., and Llorens-Cortès, C. (2012) Central antihypertensive effects of orally active aminopeptidase A inhibitors in spontaneously hypertensive rats. Hypertension 60, 411-418
20. Zini, S., Masdehors, P., Lenkei, Z., Fournié-Zaluski, M. C., Roques, B. P., Corvol, P., and Llorens-Cortès, C. (1997) Aminopeptidase A: distribution in rat brain nuclei and increased activity in spontaneously hypertensive rats. Neuroscience 78, 1187-1193
21. Mizutani, S., Ishii, M., Hattori, A., Nomura, S., Numaguchi, Y., Tsujimoto, M., Kobayshi, H., Murohara, T., and Wright, J. W. (2008) New insights into the importance of aminopeptidase A in hypertension. Heart Fail. Rev. 13, 273-284
22. Natesh, R., Schwager, S. L. U., Sturrock, E. D., and Acharya, K. R. (2003) Crystal structure of the human angiotensin-converting enzyme-lisinopril complex. Nature 421, 551-554
23. Sielecki, A. R., Hayakawa, K., Fujinaga, M., Murphy, M. E. P., Fraser, M., Muir, A. K., Carilli, C. T., Lewicki, J. A., Baxter, J. D., and James, M. N. G. (1989) Structure of recombinant human renin, a target for cardiovascularactive drugs, at 2.5 Å resolution. Science 243, 1346-1351
24. Li, L., Wu, Q., Wang, J., Bucy, R. P., and Cooper, M. D. (1993) Widespread tissue distribution of aminopeptidase A, an evolutionarily conserved ectoenzyme recognized by the BP-1 antibody. Tissue Antigens 42, 488-496
25. Benajiba, A., and Maroux, S. (1980) Purification and characterization of an aminopeptidase A from hog intestinal brush-border membrane. Eur. J. Biochem. 107, 381-388
26. Chen, L., Lin, Y.-L., Peng, G., and Li, F. (2012) Structural basis for multifunctional roles of mammalian aminopeptidase N. Proc. Natl. Acad. Sci. U.S.A. 109, 17966-17971
27. Rozenfeld, R., Iturrioz, X., Maigret, B., and Llorens-Cortès, C. (2002) Contribution of molecular modeling and site-directed mutagenesis to the identification of two structural residues, Arg-220 and Asp-227, in aminopeptidase A. J. Biol. Chem. 277, 29242-29252
28. Rozenfeld, R., Iturrioz, X., Okada, M., Maigret, B., and Llorens-Cortès, C. (2003) Contribution of molecular modeling and site-directed mutagenesis to the identification of a new residue, glutamate 215, involved in the exopeptidase specificity of aminopeptidase A. Biochemistry 42, 14785-14793
29. Claperon, C., Rozenfeld, R., Iturrioz, X., Inguimbert, N., Okada, M., Roques, B., Maigret, B., and Llorens-Cortès, C. (2008) Asp218 participates with Asp213 to bind a Ca2+ atom into the S1 subsite of aminopeptidase A: a key element for substrate specificity. Biochem. J. 416, 37-46
30. Goto, Y., Hattori, A., Mizutani, S., and Tsujimoto, M. (2007) Aspartic acid 221 is critical in the calcium-induced modulation of the enzymatic activity of human aminopeptidase A. J. Biol. Chem. 282, 37074-37081
31. Goto, Y., Hattori, A., Ishii, Y., Mizutani, S., and Tsujimoto, M. (2006) Enzymatic properties of human aminopeptidase A. Regulation of its enzymatic activity by calcium and angiotensin IV. J. Biol. Chem. 281, 23503-23513
32. Jones, H. C., and Keep, R. F. (1988) Brain fluid calcium concentration and response to acute hypercalcaemia during development in the rat. J. Physiol. 402, 579-593
33. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
34. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861
35. Terwilliger, T. C. (2000) Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972
36. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
37. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
38. Murshudov, G. N., Vagin, A. A., Lebedev, A., Wilson, K. S., and Dodson, E. J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55, 247-255
39. Toyoshima, C., Nakasako, M., Nomura, H., and Ogawa, H. (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405, 647-655
40. Findeisen, F., and Minor, D. L., Jr. (2010) Structural basis for the differential effects of CaBP1 and calmodulin on CaV1.2 calcium-dependent inactivation. Structure 18, 1617-1631
41. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
42. Weiss, M. S. (2001) Global indicators of x-ray data quality. J. Appl. Crystallogr. 34, 130-135