High-Throughput and Rapid Screening of Novel ACE Inhibitory Peptides from Sericin Source and Inhibition Mechanism by Using in Silico and in Vitro Prescriptions

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 46, 2017, Pages 10020-10028

  Sun, Huaju ^a   Chang, Qing ^a   Liu, Long ^a   Chai, Kungang ^a   Lin, Guangyan ^a   Huo, Qingling ^a   Zhao, Zhenxia ^a   Zhao, Zhongxing ^a  

^a GUANGXI UNIVERSITY   (China)

Author keywords

ACE I inhibitory peptides; in silico prediction; inhibitory mechanism; LC MS; molecular docking; sericin hydrolysis

Indexed keywords

COMPUTATIONAL CHEMISTRY; HYDROGEN BONDS; MOLECULAR GRAPHICS; PEPTIDES; THROUGHPUT;

IN-SILICO; INHIBITORY MECHANISM; INHIBITORY PEPTIDES; LC-MS; MOLECULAR DOCKING;

BIOINFORMATICS;

DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; PEPTIDE; SERICIN;

ANIMAL; BOMBYX; CHEMISTRY; COMPUTER SIMULATION; HIGH THROUGHPUT SCREENING; ISOLATION AND PURIFICATION; KINETICS; MOLECULAR DOCKING;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; BOMBYX; COMPUTER SIMULATION; HIGH-THROUGHPUT SCREENING ASSAYS; KINETICS; MOLECULAR DOCKING SIMULATION; PEPTIDES; PEPTIDYL-DIPEPTIDASE A; SERICINS;

EID: 85035075316     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.7b04043     Document Type: Article

References (57)

1. Mittal, B. V.; Singh, A. K. Hypertension in the developing world: challenges and opportunities Am. J. Kidney Dis. 2010, 55, 590-598 10.1053/j.ajkd.2009.06.044
2. Tao, M.; Wang, C.; Liao, D.; Liu, H.; Zhao, Z.; Zhao, Z. Purification, modification and inhibition mechanism of angiotensin I-converting enzyme inhibitory peptide from silkworm pupa (Bombyx mori) protein hydrolysate Process Biochem. 2017, 54, 172-179 10.1016/j.procbio.2016.12.022
3. Kim, S.; Wijesekara, I. Development and biological activities of marine-derived bioactive perptides: A review J. Funct. Foods 2010, 2, 1-9 10.1016/j.jff.2010.01.003
4. Miguel, M.; Manso, M. A.; Lopez-Fandino, R.; Alonso, M. J.; Salaices, M. Vascular effects and antihypertensive properties of kappa-casein macropeptide Int. Dairy J. 2007, 17, 1473-1477 10.1016/j.idairyj.2007.04.009
5. Vermeirssen, V.; Van Camp, J.; Verstraete, W. Fractionation of angiotensin I converting enzyme inhibitory activity from pea and whey protein in vitro gastrointestinal digests J. Sci. Food Agric. 2005, 85, 399-405 10.1002/jsfa.1926
6. Hwang, J. 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 10.1016/j.foodres.2009.12.012
7. Je, J.; Lee, K.; Lee, M. H.; Ahn, C. Antioxidant and antihypertensive protein hydrolysates produced from tuna liver by enzymatic hydrolysis Food Res. Int. 2009, 42, 1266-1272 10.1016/j.foodres.2009.06.013
8. Qian, Z.; Je, J.; Kim, S. Anti hypertensive effect of anglotensin I converting enzyme-inhibitory peptide from hydrolysates of bigeye tuna dark muscle, Thunnus obesus J. Agric. Food Chem. 2007, 55, 8398-8403 10.1021/jf0710635
9. Byun, H. G.; Kim, S. K. Purification and characterization of angiotensin I converting enzyme (ACE) inhibitory peptides from Alaska pollack (Theragra chalcogramma) skin Process Biochem. 2001, 36, 1155-1162 10.1016/S0032-9592(00)00297-1
10. Je, J. Y.; Park, P. J.; Byun, H. G.; Jung, W. K.; Kim, S. K. Angiotensin I converting enzyme (ACE) inhibitory peptide derived from the sauce of fermented blue mussel, Mytilus edulis Bioresour. Technol. 2005, 96, 1624-1629 10.1016/j.biortech.2005.01.001
11. Zhao, Y.; Li, B.; Liu, Z.; Dong, S.; Zhao, X.; Zeng, M. Antihypertensive effect and purification of an ACE inhibitory peptide from sea cucumber gelatin hydrolysate Process Biochem. 2007, 42, 1586-1591 10.1016/j.procbio.2007.08.011
12. Jang, A.; Lee, M. Purification and identification of angiotensin converting enzyme inhibitory peptides from beef hydrolysates Meat Sci. 2005, 69, 653-661 10.1016/j.meatsci.2004.10.014
13. Katayama, K.; Mori, T.; Kawahara, S.; Miake, K.; Kodama, Y.; Sugiyama, M.; Kawamura, Y.; Nakayama, T.; Maruyama, M.; Muguruma, M. Angiotensin-I converting enzyme inhibitory peptide derived from porcine skeletal muscle myosin and its antihypertensive activity in spontaneously hypertensive rats J. Food Sci. 2007, 72, S702-S706 10.1111/j.1750-3841.2007.00571.x
14. Dziuba, J.; Minkiewicz, P.; Nalecz, D.; Iwaniak, A. Database of biologically active peptide sequences Nahrung 1999, 43, 190-195 10.1002/(SICI)1521-3803(19990601)43:3<190::AID-FOOD190>3.0.CO;2-A
15. Wu, J. P.; Ding, X. L. Characterization of inhibition and stability of soy-protein-derived angiotensin I-converting enzyme inhibitory peptides Food Res. Int. 2002, 35, 367-375 10.1016/S0963-9969(01)00131-4
16. Majumder, K.; Wu, J. A new approach for identification of novel antihypertensive peptides from egg proteins by QSAR and bioinformatics Food Res. Int. 2010, 43, 1371-1378 10.1016/j.foodres.2010.04.027
17. Lafarga, T.; O'Connor, P.; Hayes, M. In silico methods to identify meat-derived prolyl endopeptidase inhibitors Food Chem. 2015, 175, 337-343 10.1016/j.foodchem.2014.11.150
18. Lafarga, T.; O'Connor, P.; Hayes, M. Identification of novel dipeptidyl peptidase-IV and angiotensin-I-converting enzyme inhibitory peptides from meat proteins using in silico analysis Peptides 2014, 59, 53-62 10.1016/j.peptides.2014.07.005
19. Nongonierma, A. B.; Mooney, C.; Shields, D. C.; FitzGerald, R. J. In silico approaches to predict the potential of milk protein-derived peptides as dipeptidyl peptidase IV (DPP-IV) inhibitors Peptides 2014, 57, 43-51 10.1016/j.peptides.2014.04.018
20. Zhaorigetu, S.; Yanaka, N.; Sasaki, M.; Watanabe, H.; Kato, N. Inhibitory effects of silk protein, sericin on UVB-induced acute damage and tumor promotion by reducing oxidative stress in the skin of hairless mouse J. Photochem. Photobiol., B 2003, 71, 11-17 10.1016/S1011-1344(03)00092-7
21. Kato, N.; Sato, S.; Yamanaka, A.; Yamada, H.; Fuwa, N.; Nomura, M. Silk protein, sericin, inhibits lipid peroxidation and tyrosinase activity Biosci., Biotechnol., Biochem. 1998, 62, 145-147 10.1271/bbb.62.145
22. Aramwit, P.; Damrongsakkul, S.; Kanokpanont, S.; Srichana, T. Properties and antityrosinase activity of sericin from various extraction methods Biotechnol. Appl. Biochem. 2010, 55, 91-98 10.1042/BA20090186
23. Zhaorigetu, S.; Sasaki, M.; Watanabe, H.; Kato, N. Supplemental silk protein, sericin, suppresses colon tumorigenesis in 1,2-dimethylhydrazine-treated mice by reducing oxidative stress and cell proliferation Biosci., Biotechnol., Biochem. 2001, 65, 2181-2186 10.1271/bbb.65.2181
24. Takasu, Y.; Yamada, H.; Tsubouchi, K. Isolation of three main sericin components from the cocoon of the silkworm Biosci., Biotechnol., Biochem. 2002, 66, 2715-2718 10.1271/bbb.66.2715
25. Takasu, Y.; Hata, T.; Uchino, K.; Zhang, Q. Identification of Ser2 proteins as major sericin components in the non-cocoon silk of Bombyx mori Insect Biochem. Mol. Biol. 2010, 40, 339-344 10.1016/j.ibmb.2010.02.010
26. Cao, T.; Zhang, Y. Processing and characterization of silk sericin from Bombyx mori and its application in biomaterials and biomedicines Mater. Sci. Eng., C 2016, 61, 940-952 10.1016/j.msec.2015.12.082
27. Cushman, D. W.; Cheung, H. S. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung Biochem. Pharmacol. 1971, 20, 1637-48 10.1016/0006-2952(71)90292-9
28. Rawendra, R. D. S.; Aisha; Chen, S.; Chang, C.; Shih, W.; Huang, T.; Liao, M.; Hsu, J. 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, 12178-12185 10.1021/jf504734g
29. Wu, S.; Qi, W.; Su, R.; Li, T.; Lu, D.; He, Z. CoMFA and CoMSIA analysis of ACE-inhibitory, antimicrobial and bitter-tasting peptides Eur. J. Med. Chem. 2014, 84, 100-106 10.1016/j.ejmech.2014.07.015
30. Wu, J. P.; 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 10.1021/jf051263l
31. Bhonsle, J. B.; Venugopal, D.; Huddler, D. P.; Magill, A. J.; Hicks, R. P. Application of 3D-QSAR for identification of descriptors defining bioactivity of antimicrobial peptides J. Med. Chem. 2007, 50, 6545-6553 10.1021/jm070884y
32. Fu, Y.; Young, J. F.; Lokke, M. M.; Lametsch, R.; Aluko, R. E.; Therkildsen, M. Revalorisation of bovine collagen as a potential precursor of angiotensin 1-converting enzyme (ACE) inhibitory peptides based on in silico and in vitro protein digestions J. Funct. Foods 2016, 24, 196-206 10.1016/j.jff.2016.03.026
33. Wu, J. P.; Aluko, R. E.; Muir, A. D. Improved method for direct high-performance liquid chromatography assay of angiotensin-converting enzyme-catalyzed reactions J. Chromatogr. A 2002, 950, 125-130 10.1016/S0021-9673(02)00052-3
34. Schuttelkopf, A. W.; van Aalten, D. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 1355-1363 10.1107/S0907444904011679
35. Eslami, H.; Mojahedi, F.; Moghadasi, J. Molecular dynamics simulation with weak coupling to heat and material baths J. Chem. Phys. 2010, 133, 084105 10.1063/1.3474951
36. Tao, M.; Sun, H.; Liu, L.; Luo, X.; Lin, G.; Li, R.; Zhao, Z.; Zhao, Z. Graphitized Porous Carbon for Rapid Screening of Angiotensin-Converting Enzyme Inhibitory Peptide GAMVVH from Silkworm Pupa Protein and Molecular Insight into Inhibition Mechanism J. Agric. Food Chem. 2017, 65, 8626-8633 10.1021/acs.jafc.7b03195
37. He, R.; Ma, H.; Zhao, W.; Qu, W.; Zhao, J.; Luo, L.; Zhu, W. Modeling the QSAR of ACE-inhibitory peptides with ANN and its applied illustration Int. J. Pept. 2012, 2012, 620609 10.1155/2012/620609
38. Udenigwe, C. C.; Aluko, R. E. Food Protein-Derived Bioactive peptides: production, processing, and potential health benefits J. Food Sci. 2012, 77, R11-R24 10.1111/j.1750-3841.2011.02455.x
39. Nongonierma, A. B.; FitzGerald, R. J. Learnings from quantitative structure-activity relationship (QSAR) studies with respect to food protein-derived bioactive peptides: a review RSC Adv. 2016, 6, 75400-75413 10.1039/C6RA12738J
40. Aluko, R. E.; Girgih, A. T.; He, R.; Malomo, S.; Li, H.; Offengenden, M.; Wu, J. Structural and functional characterization of yellow field pea seed (Pisum sativum L.) protein-derived antihypertensive peptides Food Res. Int. 2015, 77, 10-16 10.1016/j.foodres.2015.03.029
41. Bohm, M.; Sturzebecher, J.; Klebe, G. Three-dimensional quantitative structure-activity relationship analyses using comparative molecular field analysis and comparative molecular similarity indices analysis to elucidate selectivity differences of inhibitors binding to trypsin, thrombin, and factor Xa J. Med. Chem. 1999, 42, 458-477 10.1021/jm981062r
42. Bringmann, G.; Rummey, C. 3D QSAR investigations on antimalarial naphthylisoquinoline alkaloids by comparative molecular similarity indices analysis (CoMSIA), based on different alignment approaches J. Chem. Inf. Comp. Sci. 2003, 43, 304-316 10.1021/ci025570s
43. Roy, P. P.; Leonard, J. T.; Roy, K. Exploring the impact of size of training sets for the development of predictive QSAR models Chemom. Intell. Lab. Syst. 2008, 90, 31-42 10.1016/j.chemolab.2007.07.004
44. Caballero, J.; Saavedra, M.; Fernandez, M.; Gonzalez-Nilo, F. D. Quantitative structure-activity relationship of rubiscolin analogues as delta opioid peptides using comparative molecular field analysis (CoMFA) and comparative molecular similarity indices analysis (CoMSIA) J. Agric. Food Chem. 2007, 55, 8101-8104 10.1021/jf071031h
45. Zhou, Z.; Cheng, C.; Li, Y. Structure-based design and optimization of antihypertensive peptides to obtain high inhibitory potency against both renin and angiotensin I-converting enzyme SAR QSAR Environ. Res. 2015, 26, 1001-1016 10.1080/1062936X.2015.1104725
46. 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, 401-7
47. Hellberg, S.; Eriksson, L.; Jonsson, J.; Lindgren, F.; Sjostrom, M.; Skagerberg, B.; Wold, S.; Andrews, P. Minimum analogue peptide sets (MAPS) for quantitative structure-activity relationships Int. J. Pept. Protein Res. 1991, 37, 414-24 10.1111/j.1399-3011.1991.tb00756.x
48. Ariyoshi, Y. Angiotensin-converting enzyme inhibitors derived from food proteins Trends Food Sci. Technol. 1993, 4, 139-144 10.1016/0924-2244(93)90033-7
49. C. K. Rajendran, S. R.; Mason, B.; Udenigwe, C. C. Peptidomics of peptic digest of selected potato tuber proteins: post-translational modifications and limited cleavage specificity J. Agric. Food Chem. 2016, 64, 2432-2437 10.1021/acs.jafc.6b00418
50. Fu, Y.; Wu, W.; Zhu, M.; Xiao, Z. In silico assessment of the potential of patatin as a precursor of bioactive peptides J. Food Biochem. 2016, 40, 366-370 10.1111/jfbc.12213
51. Sentandreu, M. A.; Toldra, F. Evaluation of ACE inhibitory activity of dipeptides generated by the action of porcine muscle dipeptidyl peptidases Food Chem. 2007, 102, 511-515 10.1016/j.foodchem.2006.04.018
52. 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, 1116-1124 10.1016/j.jff.2013.03.008
53. 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 (1) 52-58 10.1016/j.peptides.2011.11.006
54. Blat, Y. Non-Competitive Inhibition by Active Site Binders Chem. Biol. Drug Des. 2010, 75, 535-540 10.1111/j.1747-0285.2010.00972.x
55. Sornwatana, T.; Bangphoomi, K.; Roytrakul, S.; Wetprasit, N.; Choowongkomon, K.; Ratanapo, S. Chebulin: Terminalia chebula Retz fruit-derived peptide with angiotensin-I-converting enzyme inhibitory activity Biotechnol. Appl. Biochem. 2015, 62, 746-753 10.1002/bab.1321
56. Wu, Q.; Du, J.; Jia, J.; Kuang, C. Production of ACE inhibitory peptides from sweet sorghum grain protein using alcalase: hydrolysis kinetic, purification and molecular docking study Food Chem. 2016, 199, 140-149 10.1016/j.foodchem.2015.12.012
57. Jing, P.; Qian, B.; He, Y.; Zhao, X.; Zhang, J.; Zhao, D.; Lv, Y.; Deng, Y. Screening milk-derived antihypertensive peptides using quantitative structure activity relationship (QSAR) modelling and in vitro/in vivo studies on their bioactivity Int. Dairy J. 2014, 35, 95-101 10.1016/j.idairyj.2013.10.009