Screening, discovery, and characterization of angiotensin-I converting enzyme inhibitory peptides derived from proteolytic hydrolysate of bitter melon seed proteins

Journal of Proteomics

Volumn 128, Issue , 2015, Pages 424-435

  Priyanto, Anugerah Dany ^a,b   Doerksen, Robert J ^c   Chang, Chi I ^a   Sung, Wang Chou ^d   Widjanarko, Simon Bambang ^b   Kusnadi, Joni ^b   Lin, Ya Chi ^a   Wang, Ting Chin ^a   Hsu, Jue Liang ^a  

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

^b BRAWIJAYA UNIVERSITY   (Indonesia)

^c UNIVERSITY OF MISSISSIPPI   (United States)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

ACE inhibitory peptide; Bitter melon seed protein; LC MS MS; Molecular docking; Momordica charantia; Momordin a

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; MOMORDICA ANTI HIV PROTEIN 30; MOMORDIN; MOMORDIN A; PROTEIN HYDROLYSATE; THERMOLYSIN; UNCLASSIFIED DRUG; VG 8; VY 7; PEPTIDE; PLANT EXTRACT; PLANT PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG SCREENING; HYPERTENSION; IC50; IN VITRO STUDY; INFANT; MALE; MOLECULAR DOCKING; MOMORDICA CHARANTIA; NONHUMAN; PLANT SEED; PRIORITY JOURNAL; RAT; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CHEMISTRY; DRUG DEVELOPMENT; MOLECULAR GENETICS; PRECLINICAL STUDY; PROCEDURES; SEQUENCE ANALYSIS; SYNTHESIS;

AMINO ACID SEQUENCE; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; MOLECULAR SEQUENCE DATA; MOMORDICA CHARANTIA; PEPTIDES; PLANT EXTRACTS; PLANT PROTEINS; PROTEIN HYDROLYSATES; SEEDS; SEQUENCE ANALYSIS, PROTEIN;

EID: 84944767837     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.08.018     Document Type: Article

References (65)

1. Mason K., Chockalingam A., Prudhomme S., Stachenko S., Pearson T. Policy depot: a tool to build global capacity in cardiovascular health policy. Glob. Health 2012, 7(1):47-51.
2. Perk J., De Backer G., Gohlke H., Graham I., Reiner Z., Verschuren W.M.M., Albus C., Benlian P., Boysen G., Cifkova R., Deaton C., Ebrahim S., Fisher M., Germano G., Hobbs R., Hoes A., Karadeniz S., Mezzani A., Prescott E., Ryden L., Scherer M., Syvänne M., Op Reimer W.J.M.S., Vrints C., Wood D., Zamorano J.L., Zannad F. The fifth joint task force of the European society of cardiology and other societies on cardiovascular disease prevention in clinical practice (constituted by representatives of nine societies and by invited experts). Eur. Heart J. 2012, 33(13):1635-1701.
3. Lawes C.M., Vander Hoorn S., Rodgers A. International society of hypertension. Global burden of blood-pressure-related disease, 2001. Lancet 2008, 371(9623):1513-1518.
4. Law M.R., Morris J.K., Wald N.J. Use of blood pressure lowering drugs in the prevention of cardiovascular disease: meta-analysis of 147 randomised trials in the content of expectations from prospective epidemiological studies. Br. Med. J. 2009, 338:1245-1261.
5. De Dios A.M. Angiotensin-converting enzyme inhibitors in the treatment of hypertension. Rev. Argent. Cardiol. 2011, 79(2):103-105.
6. Martin J. Hypertension guidelines: revisiting the JNC 7 recommendations. J. Lancaster Gen. Hosp. 2008, 3(3):91-97.
7. Turnbull F. Blood pressure lowering treatment trialists' collaboration. Effects of different blood-pressure-lowering regimens on major cardiovascular events: results of prospectively-designed overviews of randomised trials. Lancet 2003, 362:1527-1535.
8. Liu J., Yu Z., Zhao W., Lin S., Wang E., Zhang Y., Hao H., Wang Z., Chen F. Isolation and identification of angiotensin-converting enzyme inhibitory peptides from egg white protein hydrolysates. Food Chem. 2010, 122:1159-1163.
9. Katzung B.G., Masters S.B., Trevor A.J. Basic and Clinical Pharmacology 2012, McGraw-Hill, New York.
10. Ogihara T., Mikami H., Katahira K., Otsuka A. Comparative study of the effects of three angiotensin converting enzyme inhibitors on the cough reflex. Am. J. Hypertens. 1991, 4(2):46S-51S.
11. Boelsma E., Kloek J. Lactotripeptides and antihypertensive effects: a critical review. Br. J. Nutr. 2009, 101:776-786.
12. Ong L., Shah N.P. Release and identification of angiotensin-converting enzyme-inhibitory peptides as influenced by ripening temperatures and probiotic adjuncts in cheddar cheeses. LWT Food Sci. Technol. 2008, 41:1555-1566.
13. Rao S., Sun J., Liu Y., Zeng H., Su Y., Yang Y. ACE inhibitory peptides and antioxidant peptides derived from in vitro digestion hydrolysate of hen egg white lysozyme. Food Chem. 2012, 135:1245-1252.
14. Hwang J.S. Impact of processing on stability of angiotensin I-converting enzyme (ACE) inhibitory peptides obtained from tuna cooking juice. Food Res. Int. 2010, 43:902-906.
15. Chen J., Liu S., Ye R., Cai G., Ji B., Wu Y. Angiotensin-I converting enzyme (ACE) inhibitory tripeptides from rice protein hydrolysate: purification and characterization. J. Funct. Foods 2013, 5:1684-1692.
16. Gu Y., Wu J. LC-MS/MS coupled with QSAR modeling in characterising of angiotensin I-converting enzyme inhibitory peptides from soybean proteins. Food Chem. 2013, 141:2682-2690.
17. White B.L., Sanders T.H., Davis J.P. Potential ACE-inhibitory activity and nanoLC-MS/MS sequencing of peptides derived from aflatoxin contaminated peanut meal. LWT Food Sci. Technol. 2014, 56:537-542.
18. Ngo D.H., Ryu B.M., Kim S.K. Active peptides from skate (Okamejei kenojei) skin gelatin diminish angiotensin-I converting enzyme activity and intracellular free radical-mediated oxidation. Food Chem. 2014, 143:246-255.
19. Udenigwe C.C., Lin Y.S., Hou W.C., Aluko R.E. Kinetics of the inhibition of renin and angiotensin I-converting enzyme by flaxseed protein hydrolysate fractions. J. Funct. Foods 2009, 1:199-207.
20. Vaštag Z., Popović L., Popović S., Krimer V., Peričin D. Production of enzymatic hydrolysates with antioxidant and angiotensin-I converting enzyme inhibitory activity from pumpkin oil cake protein isolate. Food Chem. 2011, 124:1316-1321.
21. Horax R., Hettiarachchy N., Kannan A., Chen P. Protein extraction optimisation, characterisation, and functionalities of protein isolate from bitter melon (Momordica charantia) seed. Food Chem. 2011, 124:545-550.
22. Lee-Huang S., Huang P.L., Nara P.L., Chen H.C., Kung H.F., Huang P., Huang H.I. MAP 30: a new inhibitor of HIV-1 infection and replication. Fed. Eur. Biochem. Soc. Lett. 1990, 272:12-18.
23. Fang E.F., Zhang C.F., Wong J.H., Shen J.Y., Li C.H., Ng T.B. The MAP30 protein from bitter gourd (Momordica charantia) seeds promotes apoptosis in liver cancer cells in vitro and in vivo. Cancer Lett. 2012, 324(1):66-74.
24. Li M., Chen Y., Liu Z., Shen F., Bian X., Meng Y. Anti-tumor activity and immunological modification of ribosome-inactivating protein (RIP) from momordica charantia by covalent attachment of polyethylene glycol. Acta Biochim. Biophys. Sin. 2009, 41(9):792-799.
25. Turk B. Targeting proteases: successes, failures and future prospects. Nat. Rev. Drug Discov. 2006, 5(9):785-799.
26. Rawendra R.D., 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.
27. Duan X., Wu F., Li M., Yang N., Wu C., Jin Y., Yang J., Jin Z., Xu X. Naturally occurring angiotensin I-converting enzyme inhibitory peptide from a fertilized egg and its inhibitory mechanism. J. Agric. Food Chem. 2014, 62(24):5500-5506.
28. 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 1997, 16(25):5484-5491.
29. Rawendra R.D., Aisha, Chen S.H., Chang C.I., Shih W.L., Huang T.C., Liao M.H., Hsu J.L. 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. J. Agric. Food Chem. 2014, 62(50):12178-12185.
30. Gómez-Ruiz J.A., Ramos M., Recio L. Angiotensin-converting enzyme-inhibory activity of peptides isolated from Manchego cheese. Stability under simulated gastrointestinal digestion. Int. Dairy J. 2004, 14:1075-1080.
31. Quiróz A., Contreras M.M., Ramos M., Amigo L., Recio I. Stability to gastrointestinal enzymes and structure-activity relationship of beta-casein-peptides with antihypertensive properties. Peptides 2009, 30:1848-1853.
32. Basha S.H., Prasad R.N. In-silico screening of pleconaril and its novel substituted derivatives with neuraminidase of H1N1 influenza strain. BMC Res. Notes 2012, 5:105.
33. Brooks B.R., Brooks C.L., MacKerell A.D., Nilsson L., Petrella R.J., Roux B., Won Y., et al. CHARMM: the biomolecular simulation program. J. Comput. Chem. 2009, 30:1545-1614.
34. Natesh R., Schwanger S.L.U., Sturrock E.D., Acharya K.R. Crystal structure of the human angiotensin-converting enzyme-Lisinopril complex. Nature 2003, 421(6922):551-554.
35. Sivaprakasam P., Tosso P.N., Doerksen R.J. Structure-activity relationship and comparative docking studies for cycloguanil analogs as PfDHFR-TS inhibitors. J. Chem. Inf. Model. 2009, 49(7):1787-1796.
36. Thomsen R., Christensen M.H. MolDock: a new technique for high-accuracy molecular docking. J. Med. Chem. 2006, 49(11):3315-3321.
37. Wu X., Xiong E., Wang W., Scali M., Cresti M. Universal sample preparation method integrating trichloroacetic acid/acetone precipitation with phenol extraction for crop proteomic analysis. Nat. Protoc. 2014, 9:362-374.
38. Priyanto A.D., Doerksen R.J., Chang C.I., Sung W.C., Widjanarko S.B., Kusnadi J., Lin Y.C., Wang T.C., Hsu J.L. Data in support of optimized production of angiotensin-I converting enzyme inhibitory peptides derived from proteolytic hydrolysate of bitter melon seed proteins 2015, (Data in Brief submitted for publication).
39. Matsubara H. Observations on the specificity of thermolysin with synthetic peptides. Biochem. Biophys. Res. Commun. 1966, 24(3):427-430.
40. Arnold U., Rücknagel K.P., Schierhorn A., Ulbrich-Hofmann R. Thermal unfolding and proteolytic susceptibility of ribonuclease a. Eur. J. Biochem. 1996, 237(3):862-869.
41. Wu J.P., Aluko R.E., Nakai S. Structural requirements of angiotensin I-converting enzyme inhibitory peptides: quantitative structure-activity relationship modeling of peptides containing 4-10 amino acid residues. QSAR Comb. Sci. 2006, 25:873-880.
42. Jimsheena V.K., Gowda L.R. Angiotensin I-converting enzyme (ACE) inhibitory peptides derived from arachin by simulated gastric digestion. Food Chem. 2011, 125:561-569.
43. Rui X., Boye J.I., Simpson B.K., Prasher S.O. Purification and characterization of angiotensin I-converting enzyme inhibitory peptides of small red bean (Phaseolus vulgaris) hydrolysates. J. Funct. Foods 2013, 5(3):1116-1124.
44. Chen J., Wang Q., Zhong Y., Wu Y., Xia W. Purification and characterization of a novel angiotensin-I converting enzyme (ACE) inhibitory peptide derived from enzymatic hydrolysate of grass carp. Peptides 2012, 33:52-58.
45. Ahn C.B., Jeon Y.J., Kim Y.T., Je J.Y. Angiotensin I converting enzyme (ACE) inhibitory peptides from salmon byproduct protein hydrolysate by alcalase hydrolysis. Process Biochem. 2012, 47:2240-2245.
46. Miguel M., Aleixandre M.A., Ramos M., López-Fandiño R. Effect of simulated gastrointestinal digestion on the antihypertensive properties of ACE-inhibitory peptides derived from ovalbumin. J. Agric. Food Chem. 2006, 54(3):726-731.
47. Tavares T., Contreras M.M., Amorim M., Pintado M., Recio I., Malcata F.X. Novel whey-derived peptides with inhibitory effect against angiotensin-converting enzyme: in vitro effect and stability to gastrointestinal enzymes. Peptides 2011, 32:1013-1019.
48. Je J.Y., Park P.J., Kwon J.Y., Kim S.K. A novel angiotensin I converting enzyme inhibitory peptide from allaska Pollack (Theragra chalcogramma) frame protein hydrolysate. J. Agric. Food Chem. 2004, 52:7842-7845.
49. Fitzgerald R.J., Murray B.A. Bioactive peptides and lactic fermentations. Int. J. Dairy Technol. 2006, 59:118-125.
50. Vermeirssen V., Verstraete W., van Camp J. Bioavailibility of angiotensin I converting enzyme inhibitory peptides. Br. J. Nutr. 2004, 92:357-366.
51. Jao C.L., Huang S.L., Hsu K.C. Angiotensin I-converting enzyme inhibitory peptides: inhibition mode, bioavailibility, and antihypertensive effects. Biomedicine 2012, 2:130-136.
52. Meng Y., Liu B., Lei N., Zheng J., He Q., Li D., Zhao X., Shen F. Alpha-momorcharin possessing high immunogenicity, immunotoxicity and hepatotoxicity in SD rats. J. Ethnopharmacol. 2012, 39(2):590-598.
53. Rao S., 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.
54. Holland D.R., Hausrath A.C., Juers D., Matthews B.W. Structural analysis of zinc substitutions in the active site of thermolysin. Protein Sci. 1995, 4(10):1955-1965.
55. Matthews B.W., Weaver L.H., Kester W.R. The conformation of thermolysin. J. Biol. Chem. 1974, 249(24):8030-8044.
56. 50) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22:3099-3108.
57. Fujita H., Yoshikawa M. LKPNM: a prodrug-type ACE-inhibitory peptide derived from fish protein. Immunopharmacology 1999, 44:123-127.
58. Maeno M., Yamamoto N., Takano T. Identification of an antihypertensive peptide from casein hydrolysate produced by a proteinase from Lactobacillus helveticus CP790. J. Dairy Sci. 1996, 79:1316-1321.
59. Durak A., Baraniak B., Jakubczyk A., Świeca M. Biologically active peptides obtained by enzymatic hydrolysis of adzuki bean seeds. Food Chem. 2013, 141(3):2177-2183.
60. Yea C.S., Ebrahimpour A., Hamid A.A., Bakar J., Muhammad K., Saari N. Winged bean [Psophorcarpus tetragonolobus (L.) DC] seeds as an underutilised plant source of bifunctional proteolysate and biopeptides. Food Funct. 2014, 5(5):1007-1016.
61. Jakubczyk A., Baraniak B. Angiotensin I converting enzyme inhibitory peptides obtained after in vitro hydrolysis of pea (Pisum sativum var. Bajka) globulins. BioMed Res. Int. 2014, 2014:438459.
62. Pihlanto A., Mäkinen S. Antihypertensive Properties of Plant Protein Derived Peptides (Chapter 6) in Bioactive Food Peptides in Health and Disease. Edited by Hernández-Ledesma B, and Hsieh CC 2013, Publisher, InTech.
63. Ruiz-Giménez P., Marcos J.F., Torregrosa G., Lahoz A., Fernández-Musoles R., Valles S., Alborch E., Manzanares P., Salom J.B. Novel antihypertensive hexa- and heptapeptides with ACE-inhibiting properties: from the in vitro assay to the spontaneously hypertensive rat. Peptides 2011, 32:1431-1438.
64. Rajamani R., Good A.C. Ranking poses in structure-based lead discovery and optimization: current trends in scoring function development. Curr. Opin. Drug Discov. Devel. 2007, 10:308-315.
65. Natesh R., Schwanger S.L.U., Sturrock E.D., Acharya K.R. Crystal structure of the human angiotensin-converting enzyme-Lisinopril complex. Nature 2003, 421(6922):551-554.