Long-Term Regulation of the Local Renin-Angiotensin System in the Myocardium of Spontaneously Hypertensive Rats by Feeding Bioactive Peptides Derived from Spirulina platensis

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 35, 2015, Pages 7765-7774

  Pan, Huanglei ^a,b   She, Xingxing ^a   Wu, Hongli ^a   Ma, Jun ^a   Ren, Difeng ^a   Lu, Jun ^b  

^a BEIJING FORESTRY UNIVERSITY   (China)

^b NATIONAL RESEARCH INSTITUTE FOR FAMILY PLANNING   (China)

Author keywords

hypertension; Ile Gln Pro; myocardium; renin angiotensin system; Spirulina platensis hydrolysates; Val Glu Pro

Indexed keywords

ENZYMES; POLYMERASE CHAIN REACTION; PROTEINS; RATS; WATER TREATMENT;

HYPERTENSION; ILE-GLN-PRO; MYOCARDIUM; RENIN-ANGIOTENSIN SYSTEM; SPIRULINA PLATENSIS; VAL-GLU-PRO;

BLOOD PRESSURE;

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ANGIOTENSIN II; ANTIHYPERTENSIVE AGENT; DIPEPTIDYL CARBOXYPEPTIDASE; PEPTIDE; PEPTIDE FRAGMENT;

ANIMAL; BLOOD PRESSURE; CHEMISTRY; DRUG EFFECTS; GENETICS; HEART MUSCLE; HUMAN; HYPERTENSION; MALE; METABOLISM; PATHOPHYSIOLOGY; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SPIRULINA; SPONTANEOUSLY HYPERTENSIVE RAT;

ANGIOTENSIN I; ANGIOTENSIN II; ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; HUMANS; HYPERTENSION; MALE; MYOCARDIUM; PEPTIDE FRAGMENTS; PEPTIDES; PEPTIDYL-DIPEPTIDASE A; RATS; RATS, INBRED SHR; RECEPTOR, ANGIOTENSIN, TYPE 1; RENIN-ANGIOTENSIN SYSTEM; SPIRULINA;

EID: 84941073656     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b02801     Document Type: Article

References (43)

1. World Health Organization (WHO). World Health Statistics, 2012; http://www.who.int/gho/publications/world-health-statistics/2012/en/ (accessed June 13, 2012).
2. Udenigwe, C. C.; Mohan, A. Mechanisms of food protein-derived antihypertensive peptides other than ACE inhibition J. Funct. Foods 2014, 8, 45-52 10.1016/j.jff.2014.03.002
3. World Health Organizaion (WHO). Controlling High Blood Pressure; http://www.who.int/cardiovascular-diseases/en/
4. Patel, S. K.; Velkoska, E.; Freeman, M.; Wai, B.; Lancefield, T. F.; Burrell, L. M. From gene to protein-experimental and clinical studies of ACE2 in blood pressure control and arterial hypertension Front. Physiol. 2014, 5, 227 10.3389/fphys.2014.00227
5. Martínez-maqueda, D.; Beatriz, M.; Recio, I.; Hernández-ledesma, B. Antihypertensive peptides from food proteins: a review Food Funct. 2012, 4, 350-361 10.1039/c2fo10192k
6. Lu, J.; Ren, D. F.; Xue, Y. L.; Sawano, Y.; Miyakawa, T.; Tanokura, M. Isolation of an antihypertensive peptide from alcalase digest of spirulina platensis J. Agric. Food Chem. 2010, 58, 7166-7171 10.1021/jf100193f
7. Lu, J.; Ren, D. F.; Wang, J. Z.; Tanokura, M. Purification and characterization of an angiotensin I-converting enzyme inhibitory peptide derived from Spirulina platensis Shengwu Huaxue Yu Shengwu Wuli Jinzhan 2010, 37, 568-574 10.3724/SP.J.1206.2009.00647
8. Lu, J.; Sawano, Y.; Miyakawa, T.; Xue, Y. L.; Cai, M. Y.; Egashira, Y.; Ren, D. F.; Tanokura, M. One-week antihypertensive effect of Ile-Gln-Pro in spontaneously hypertensive rats J. Agric. Food Chem. 2011, 59, 559-563 10.1021/jf104126a
9. Lu, J.; Yang, Y.; Chen, L.; Ren, D. F.; Cai, M. Y.; Wang, J. Z.; Egashira, Y.; Tanokura, M. In vivo antihypertensive effect of Val-Glu-Pro in spontaneously hypertensive rats Shengwu Huaxue Yu Shengwu Wuli Jinzhan 2011, 38, 353-360 10.3724/SP.J.1206.2010.00533
10. Iwai, M.; Horiuchi, M. Devil and angel in the renin-angiotensin system: ACE-angiotensin II-AT1 receptor axis vs. ACE2-angiotensin-(1-7)-Mas receptor axis Hypertens. Res. 2009, 32, 533-536 10.1038/hr.2009.74
11. Geng, J.; Zhao, Z.; Kang, W.; Wang, W.; Zhang, Y.; Zhiming, G. Atorvastatin reverses cardiac remodeling possibly through regulation of protein kinase D/myocyte enhancer factor 2D activation in spontaneously hypertensive rats Pharmacol. Res. 2010, 61, 40-47 10.1016/j.phrs.2009.08.004
12. Miguel, M.; López-Fandiño, R.; Ramos, M.; Aleixandre, A. Short-term effect of egg-white hydrolysate products on the arterial blood pressure of hypertensive rats Br. J. Nutr. 2005, 94, 731-737 10.1079/BJN20051570
13. Sipola, M.; Finckenberg, P.; Korpela, R.; Vapaatalo, H.; Nurminen, M. L. Effect of long-term intake of milk products on blood pressure in hypertensive rats J. Dairy Res. 2002, 69, 103-111 10.1017/S002202990100526X
14. Silva-Antonialli, M. M.; Tostes, R. C. A.; Fernandes, L.; Fior-Chadi, D. R.; Akamine, E. H.; Carvalho, M. H. C.; Fortes, Z. B.; Nigro, D. A lower ratio of AT1/AT2 receptors of angiotensin II is found in female than in male spontaneously hypertensive rats Cardiovasc. Res. 2004, 62, 587-593 10.1016/S0008-6363(04)00045-8
15. Miguel, M.; López-Fandiño, R.; Ramos, M.; Aleixandre, A. Long-term intake of egg white hydrolysate attenuates the development of hypertension in spontaneously hypertensive rats Life Sci. 2006, 78, 2960-2966 10.1016/j.lfs.2005.11.025
16. Cabassi, A.; Vinci, S.; Calzolari, M.; Bruschi, G.; Cavatorta, A.; Borghetti, A. The relationship between regional sympathetic activity and the onset of arterial hypertension in spontaneously hypertensive rats Cardiologia 1997, 42, 393-396
17. Saito, Y.; Wanezaki, K.; Kawato, A.; Imayasu, S. Structure and activity of angiotensin I converting enzyme inhibitory peptides from sake and sake lees Biosci., Biotechnol., Biochem. 1994, 58, 1767-1771 10.1271/bbb.58.1767
18. Marczak, E. D.; Usui, H.; Fujita, H.; Yang, Y.; Yokoo, M.; Lipkowski, A. W.; Yoshikawa, M. New antihypertensive peptides isolated from rapeseed Peptides 2003, 24, 791-798 10.1016/S0196-9781(03)00174-8
19. Sipola, M.; Finckenberg, P.; Santisteban, J.; Korpela, R.; Vapaatalo, H.; Nurminen, M.-L. Long-term intake of milk peptides attenuates development of hypertension in spontaneously hypertensive rats J. Physiol. Pharmacol. 2001, 52, 745-754
20. Ben Henda, Y.; Labidi, A.; Arnaudin, I.; Bridiau, N.; Delatouche, R.; Maugard, T.; Piot, J. M.; Sannier, F.; Thiéry, V.; Bordenave-Juchereau, S. Measuring angiotensin-I converting enzyme inhibitory activity by micro plate assays: comparison using marine cryptides and tentative threshold determinations with captopril and losartan J. Agric. Food Chem. 2013, 61, 10685-10690 10.1021/jf403004e
21. Fujita, H.; Yoshikawa, M. LKPNM: a prodrug-type ACE-inhibitory peptide derived from fish protein Immunopharmacology 1999, 44, 123-127 10.1016/S0162-3109(99)00118-6
22. Hernández-Ledesma, B.; Del, M. C. M.; Recio, I. Antihypertensive peptides: production, bioavailability and incorporation into foods Adv. Colloid Interface Sci. 2011, 165, 23-35 10.1016/j.cis.2010.11.001
23. Cohn, J. N.; Ferrari, R.; Sharpe, N. Cardiac remodeling-concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling J. Am. Coll. Cardiol. 2000, 35, 569-582 10.1016/S0735-1097(99)00630-0
24. Thakur, V. M.; Richards, R. M.; Reisin, E. M. Obesity, hypertension, and the heart Am. J. Med. Sci. 2001, 321, 242-248 10.1097/00000441-200104000-00005
25. Messerli, F. H.; Sundgaard-Riise, K.; Reisin, E. D.; Dreslinski, G. R.; Ventura, H. O.; Oigman, W.; Frohlich, E. D.; Dunn, F. G. Dimorphic cardiac adaptation to obesity and arterial hypertension Ann. Intern. Med. 1983, 99, 757-761
26. Chakko, S.; Mayor, M.; Allison, M. D.; Kessler, K. M.; Materson, B. J.; Myerburg, R. J. Abnormal left ventricular diastolic filling in eccentric left ventricular hypertrophy of obesity Am. J. Cardiol. 1991, 68, 95-98 10.1016/0002-9149(91)90718-Z
27. Arata, Y.; Geshi, E.; Nomizo, A.; Aoki, S.; Katagiri, T. Alterations in sarcoplasmic reticulum and angiotensin II receptor type 1 gene expression in spontaneously hypertensive rat hearts Jpn. Circ. J. 1999, 63, 367-372 10.1253/jcj.63.367
28. Natsume, T.; Kardon, M. B.; Pegram, B. L.; Frohlich, E. D. Ventricular performance in spontaneously hypertensive rats (SHR) with reduced cardiac mass Cardiovasc. Drugs Ther. 1989, 3, 433-439 10.1007/BF01858115
29. Horinaka, S.; Frohlich, E. D. Cardiovascular mass and ventricular function after celiprolol in Wistar-Kyoto and spontaneously hypertensive rats Cardiovasc. Res. 1992, 26, 396-400 10.1093/cvr/26.4.396
30. Zong, W. N.; Yang, X. H.; Chen, X. M.; Huang, H. J.; Zheng, H. J.; Qin, X. Y.; Yong, Y. H.; Cao, K.; Huang, J.; Lu, X. Z. Regulation of angiotensin-(1-7) and angiotensin II type 1 receptor by telmisartan and losartan in adriamycin-induced rat heart failure Acta Pharmacol. Sin. 2011, 32, 1345-1350 10.1038/aps.2011.96
31. Unger, T. The role of the renin-angiotensin system in the development of cardiovascular disease Am. J. Cardiol. 2002, 89, 3-9 10.1016/S0002-9149(01)02321-9
32. Murray, B.; Fitzgerald, R. Angiotensin converting enzyme inhibitory peptides derived from food proteins: biochemistry, bioactivity and production Curr. Pharm. Des. 2007, 13, 773-791 10.2174/138161207780363068
33. Saleh, A. S.; Zhang, Q.; Shen, Q. Recent research in antihypertensive activity of food protein-derived hydrolyzates and peptides Crit. Rev. Food. Sci. Nutr. 2014, 10.1080/10408398.2012.724478
34. Bader, M.; Ganten, D. Update on tissue renin-angiotensin systems J. Mol. Med. 2008, 86, 615-621 10.1007/s00109-008-0336-0
35. Ferreira, A. J.; Santos, R. A.; Bradford, C. N.; Mecca, A. P.; Sumners, C.; Katovich, M. J.; Raizada, M. K. Therapeutic implications of the vasoprotective axis of the renin-angiotensin system in cardiovascular diseases Hypertension 2010, 55, 207-213 10.1161/HYPERTENSIONAHA.109.140145
36. Ferreira, A.; Santos, R. Cardiovascular actions of angiotensin-(1-7) Braz. J. Med. Biol. Res. 2005, 38, 499-507 10.1590/S0100-879X2005000400003
37. Bader, M. Tissue renin-angiotensin-aldosterone systems: targets for pharmacological therapy Annu. Rev. Pharmacol. Toxicol. 2010, 50, 439-465 10.1146/annurev.pharmtox.010909.105610
38. Santos, R. A. S; Ferreira, A. J.; Simões e Silva, A. C. Recent advances in the angiotensin-converting enzyme 2-angiotensin (1-7)-Mas axis Exp. Physiol. 2008, 93, 519-527 10.1113/expphysiol.2008.042002
39. Savoia, C.; D'Agostino, M.; Lauri, F.; Volpe, M. Angiotensin type 2 receptor in hypertensive cardiovascular disease Curr. Opin. Nephrol. Hypertens. 2011, 20, 125-132 10.1097/MNH.0b013e3283437fcd
40. Huentelman, M. J.; Grobe, J. L.; Vazquez, J.; Stewart, J. M.; Mecca, A. P.; Katovich, M. J.; Ferrario, C. M.; Raizada, M. K. Protection from angiotensin II-induced cardiac hypertrophy and fibrosis by systemic lentiviral delivery of ACE2 in rats Exp. Physiol. 2005, 90, 783-790 10.1113/expphysiol.2005.031096
41. Diez-Freire, C.; Vázquez, J.; de Adjounian, M. F. C.; Ferrari, M. F.; Yuan, L.; Silver, X.; Torres, R.; Raizada, M. K. ACE2 gene transfer attenuates hypertension-linked pathophysiological changes in the SHR Physiol. Genomics 2006, 27, 12-19 10.1152/physiolgenomics.00312.2005
42. Johnston, C. I. Tissue angiotensin converting enzyme in cardiac and vascular hypertrophy, repair, and remodeling Hypertension 1994, 23, 258-268 10.1161/01.HYP.23.2.258
43. Danilczyk, U.; Penninger, J. M. Angiotensin-converting enzyme II in the heart and the kidney Circ. Res. 2007, 98, 463-471 10.1161/01.RES.0000205761.22353.5f