Isolation and characterization of a novel angiotensin-converting enzyme-inhibitory tripeptide from enzymatic hydrolysis of soft-shelled turtle (Pelodiscus sinensis) egg white: In vitro, in vivo, and in silico study

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 50, 2014, Pages 12178-12185

  Rawendra, Reynetha D S ^a   Aisha, ^a,b   Chen, Sin Hong ^a   Chang, Chi I ^a   Shih, Wen Ling ^a   Huang, Tzou Chi ^a   Liao, Ming Huei ^a   Hsu, Jue Liang ^a  

^a NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^b BRAWIJAYA UNIVERSITY   (Indonesia)

Author keywords

ACE inhibitor; LC MS MS; Lysozyme C; Soft shelled turtle egg; Tripeptide

Indexed keywords

BLOOD PRESSURE; PEPTIDES;

ACE INHIBITORS; ANGIOTENSIN-CONVERTING ENZYME; ANTI-HYPERTENSIVE ACTIVITIES; ISOLATION AND CHARACTERIZATION; LC-MS/MS; SOFT-SHELLED TURTLE EGG; SPONTANEOUSLY HYPERTENSIVE RATS; TRIPEPTIDE;

ENZYMATIC HYDROLYSIS;

PELODISCUS SINENSIS; RATTUS; TRIONYCHIDAE;

ANTIHYPERTENSIVE AGENT; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; EGG WHITE; PEPTIDE; TRYPSIN;

ANIMAL; BIOCATALYSIS; BLOOD PRESSURE; CHEMISTRY; HUMAN; HYPERTENSION; ISOLATION AND PURIFICATION; KINETICS; MALE; METABOLISM; MOLECULAR DOCKING; PATHOPHYSIOLOGY; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; TURTLE;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; ANTIHYPERTENSIVE AGENTS; BIOCATALYSIS; BLOOD PRESSURE; EGG WHITE; HUMANS; HYPERTENSION; KINETICS; MALE; MOLECULAR DOCKING SIMULATION; PEPTIDES; PEPTIDYL-DIPEPTIDASE A; RATS; RATS, INBRED SHR; TRYPSIN; TURTLES;

EID: 84918522393     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf504734g     Document Type: Article

References (31)

1. Basu, S.; Millett, C. Social epidemiology of hypertension in middle-income countries: Determinants of prevalence, diagnosis, treatment, and control in the WHO SAGE study. Hypertension 2013, 62, 18-26.
2. Quist, E. E.; Phillips, R. D.; Saalia, F. K. Angiotensin converting enzyme inhibitory activity of proteolytic digests of peanut (Arachis hypogaea L.) flour. LWT - Food Sci. Technol. 2009, 42, 694-699.
3. Katzung, B. G.; Masters, S. B.; Trevor, A. J. Basic and Clinical Pharmacology; McGraw-Hill: New York, 2012.
4. Aleixandre, A.; Miguel, M.; Muguerza, B. Peptides with antihypertensive activity obtained from milk and egg proteins. Nutr. Hosp. 2008, 23, 313-318.
5. Iwaniak, A.; Minkiewicz, P.; Darewicz, M. Food-originating ACE inhibitors, including antihypertensive peptides, as preventive food components in blood pressure reduction. Compr. Rev. Food Sci. Food Saf. 2014, 13, 114-134.
6. Martinez-Maqueda, D.; Miralles, B.; Recio, I.; Hernandez-Ledesma, B. Antihypertensive peptides from food proteins: A review. Food Funct. 2012, 3, 350-361.
7. Nalinanon, S.; Benjakul, S.; Kishimura, H.; Shahidi, F. Functionalities and antioxidant properties of protein hydrolysates from the muscle of ornate threadfin bream treated with pepsin from skipjack tuna. Food Chem. 2011, 124, 1354-1362.
8. Rawendra, R. D. S.; Aisha; Chang, C. I.; Aulanni'am; Chen, H. H.; Huang, T. C.; Hsu, J. L. A novel angiotensin converting enzyme inhibitory peptide derived from proteolytic digest of Chinese soft-shelled turtle egg white proteins. J. Proteomics 2013, 94, 359-369.
9. Yu, H. L.; Li, Y.; Wang, J. B.; Zheng, L. P.; Yan, W. X. Chinese soft-shelled turtle egg powder lowers serum cholesterol, increases faecal neutral steroids and bile acid excretion, and up-regulates liver cytochrome P450 mRNA level in rats. Br. J. Nutr. 2005, 94, 315-320.
10. Chiu, L. H.; Hsu, G. S. W.; Lu, Y. F. Antihypertensive capacity of defatted soft-shelled turtle powder after hydrolysis by gastrointestinal enzymes. J. Food Biochem. 2006, 30, 589-603.
11. Liu, L.; Lu, B.; Gong, L.; Liu, L.; Wu, X.; Zhang, Y. Studies on bioactive peptide from Chinese soft-shelled turtle (Pelodiscus sinensis) with functionalities of ACE inhibition and antioxidation. Afr. J. Biotechnol. 2012, 11, 6723-6729.
12. Mathews, D.; Adibi, S. Peptide absorption. Gastroenterology 1976, 71, 151-161.
13. Cushman, D. W.; Cheung, H. S.; Sabo, E. F.; Ondetti, M. A. Design of potent competitive inhibitors of angiotensin-converting enzyme. Carboxyalkanoyl and mercaptoalkanoyl amino acids. Biochemistry 1977, 16, 5484-5491.
14. Rao, S. Q.; Ju, T.; Sun, J.; Su, Y. J.; Xu, R. R.; Yang, Y. J. Purification and characterization of angiotensin I-converting enzyme inhibitory peptides from enzymatic hydrolysate of hen egg white lysozyme. Food Res. Int. 2012, 46, 127-134.
15. Natesh, R.; Schwager, S. L.U.; Sturrock, E. D.; Acharya, K. R. Crystal structure of the human angiotensinconverting enzyme-lisinopril complex. Nature 2003, 421, 551-554.
16. Jimsheena, V. K.; Gowda, L. R. Arachin derived peptides as selective angiotensin-I converting enzyme (ACE) inhibitors: Structure-activity relationship. Peptides 2010, 31, 1165-1176.
17. Masuyer, G.; Akif, M.; Czarny, B.; Beau, F.; Schwager, S. L.; Sturrock, E. D.; Isaac, R. E.; Dive, V.; Acharya, K. R. Crystal structures of highly specific phosphinic tripeptide enantiomers in complex with the angiotensin-I converting enzyme. FEBS J. 2014, 281, 943-956.
18. Thomsen, R.; Christensen, M. H. MolDock: A new technique for high-accuracy molecular docking. J. Med. Chem. 2006, 49, 3315-3321.
19. De Leo, F.; Panarese, S.; Gallerani, R.; Ceci, L. R. Angiotensin converting enzyme (ACE) inhibitory peptides: Production and implementation of functional food. Curr. Pharm. Des. 2009, 15, 3622-3643.
20. Ricci, I.; Artacho, R.; Olalla, M. Milk protein peptides with angiotensin i-converting enzyme inhibitory (ACEI) activity. Crit. Rev. Food. Sci. Nutr. 2010, 50, 390-402.
21. Miguel, M.; Recio, I.; Gómez-Ruiz, J.; Ramos, M.; López-Fandiño, R. Angiotensin I-converting enzyme inhibitory activity of peptides derived from egg white proteins by enzymatic hydrolysis. J. Food Prot. 2004, 67, 1914-1920.
22. Fujita, H.; Yoshikawa, M. LKPNM: A prodrug-type ACE-inhibitory peptide derived from fish protein. Immunopharmacology 1999, 44, 123-127.
23. Wu, J.; Aluko, R. E.; Nakai, S. Structural requirements of angiotensin I-converting enzyme inhibitory peptides: Quantitative structure-activity relationship study of di- and tripeptides. J. Agric. Food Chem. 2006, 54, 732-738.
24. Nakamura, Y.; Yamamoto, N.; Sakai, K.; Okubo, A.; Yamazaki, S.; Takano, T. Purification and characterization of angiotensin I-converting enzyme inhibitors from sour milk. J. Dairy Sci. 1995, 78, 777-783.
25. Cheung, H. S.; Wang, F. L.; Ondetti, M. A.; Sabo, E. F.; Cushman, D. W. Binding of peptide substrates and inhibitors of angiotensin-converting enzyme. Importance of the COOH-terminal dipeptide sequence. J. Biol. Chem. 1980, 255, 401-407.
26. Fujita, H.; Yokoyama, K.; Yoshikawa, M. Classification and antihypertensive activity of angiotensin I-converting enzyme inhibitory peptides derived from food proteins. J. Food Sci. 2000, 65, 564-569.
27. Murray, B. A.; FitzGerald, R. J. Angiotensin I-converting enzyme inhibitory peptides derived from food proteins and their physiological and pharmacological effects. Curr. Pharm. Des. 2007, 13, 773-791.
28. Chen, J.; Wang, Y.; Zhong, Q.; Wu, Y.; Xia, W. Purification and characterization of a novel angiotensin-I converting enzyme (ACE) inhibitory peptide derived from enzymatic hydrolysate of grass carp protein. Peptides 2012, 33, 52-58.
29. Choudhary, G.; Wu, S. L.; Shieh, P.; Hancock, W. S. Multiple enzymatic digestion for enhanced sequence coverage of proteins in complex proteomic mixtures using capillary LC with ion trap MS/MS. J. Proteome Res. 2003, 2, 59-67.
30. Saito, T.; Nakamura, T.; Kitazawa, H.; Kawai, Y.; Itoh, T. Isolation and structural analysis of antihypertensive peptides that exist naturally in gouda cheese. J. Dairy Sci. 2000, 83, 1434-1440.
31. Nakamura, Y.; Yamamoto, N.; Sakai, K.; Takano, T. Antihypertensive effect of sour milk and peptides isolated from it that are inhibitors to angiotensin I-converting enzyme. J. Dairy Sci. 1995, 78, 1253-1257.