Exploration of Potentially Bioactive Peptides Generated from the Enzymatic Hydrolysis of Hempseed Proteins

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 47, 2017, Pages 10174-10184

  Aiello, Gilda ^a   Lammi, Carmen ^a   Boschin, Giovanna ^a   Zanoni, Chiara ^a   Arnoldi, Anna ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

bioactive peptides; Cannabis sativa; hempseed hydrolysates; HMGCoAR; LC MS MS; peptidomics

Indexed keywords

ENZYMATIC HYDROLYSIS; ENZYME INHIBITION; ENZYMES; HEMP; HYDROLYSIS; PEPTIDES;

BIOACTIVE PEPTIDES; CANNABIS SATIVA; HEMPSEED HYDROLYSATES; HMGCOAR; LC-MS/MS; PEPTIDOMICS;

PROTEINS;

ANTIOXIDANT; CANNABIS; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIPEPTIDYL PEPTIDASE IV INHIBITOR; PANCREATIN; PEPSIN A; PEPTIDE; PLANT PROTEIN;

CHEMISTRY; HYDROLYSIS; PLANT SEED;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANTIOXIDANTS; CANNABIS; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; HYDROLYSIS; PANCREATIN; PEPSIN A; PEPTIDES; PLANT PROTEINS; SEEDS;

EID: 85035793166     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.7b03590     Document Type: Article

References (44)

1. Martínez-Maqueda, D.; Miralles, B.; Recio, I.; Hernández-Ledesma, B. Antihypertensive peptides from food proteins: A review Food Funct. 2012, 3 (4) 350-361 10.1039/c2fo10192k
2. Foltz, M.; Meynen, E. E.; Bianco, V.; van Platerink, C.; Koning, T. M.; Kloek, J. Angiotensin converting enzyme inhibitory peptides from a lactotripeptide-enriched milk beverage are absorbed intact into the circulation J. Nutr. 2007, 137 (4) 953-958
3. Pripp, A. H.; Isaksson, T.; Stepaniak, L.; Sorhaug, T.; Ardo, Y. Quantitative structure activity relationship modelling of peptides and proteins as a tool in food science Trends Food Sci. Technol. 2005, 16 (11) 484-494 10.1016/j.tifs.2005.07.003
4. Holton, T. A.; Dillon, E. T.; Robinson, A.; Wynne, K.; Cagney, G.; Shields, D. C. Optimal computational comparison of mass spectrometric peptide profiles of alternative hydrolysates from the same starting material Lwt-Food Sci. Technol. 2016, 73, 296-302 10.1016/j.lwt.2016.06.025
5. Michalski, A.; Damoc, E.; Hauschild, J. P.; Lange, O.; Wieghaus, A.; Makarov, A.; Nagaraj, N.; Cox, J.; Mann, M.; Horning, S. Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer Mol. Cell. Proteomics 2011, 10 (9) M111.011015 10.1074/mcp.M111.011015
6. Ibáñez, C.; Simó, C.; García-Cañas, V.; Cifuentes, A.; Castro-Puyana, M. Metabolomics, peptidomics and proteomics applications of capillary electrophoresis-mass spectrometry in Foodomics: A review Anal. Chim. Acta 2013, 802, 1-13 10.1016/j.aca.2013.07.042
7. Lahrichi, S. L.; Affolter, M.; Zolezzi, I. S.; Panchaud, A. Food peptidomics: Large scale analysis of small bioactive peptides - a pilot study J. Proteomics 2013, 88, 83-91 10.1016/j.jprot.2013.02.018
8. Panchaud, A.; Affolter, M.; Kussmann, M. Mass spectrometry for nutritional peptidomics: How to analyze food bioactives and their health effects J. Proteomics 2012, 75 (12) 3546-3559 10.1016/j.jprot.2011.12.022
9. Aiello, G.; Fasoli, E.; Boschin, G.; Lammi, C.; Zanoni, C.; Citterio, A.; Arnoldi, A. Proteomic characterization of hempseed (Cannabis sativa L.) J. Proteomics 2016, 147, 187-196 10.1016/j.jprot.2016.05.033
10. Malomo, S. A.; He, R.; Aluko, R. E. Structural and functional properties of hemp seed protein products J. Food Sci. 2014, 79 (8) C1512-C1521 10.1111/1750-3841.12537
11. Wang, X.-S.; Tang, C.-H.; Yang, X.-Q.; Gao, W.-R. Characterization, amino acid composition and in vitro digestibility of hemp (Cannabis sativa L.) proteins Food Chem. 2008, 107 (1) 11-18 10.1016/j.foodchem.2007.06.064
12. Girgih, A. T.; Alashi, A. M.; He, R.; Malomo, S. A.; Raj, P.; Netticadan, T.; Aluko, R. E. A novel hemp seed meal protein hydrolysate reduces oxidative stress factors in spontaneously hypertensive rats Nutrients 2014, 6 (12) 5652-5666 10.3390/nu6125652
13. Girgih, A. T.; He, R.; Aluko, R. E. Kinetics and molecular docking studies of the inhibitions of angiotensin converting enzyme and renin activities by hemp seed (Cannabis sativa L.) peptides J. Agric. Food Chem. 2014, 62 (18) 4135-4144 10.1021/jf5002606
14. Girgih, A. T.; Udenigwe, C. C.; Aluko, R. E. In vitro antioxidant properties of hemp seed (Cannabis sativa L.) protein hydrolysate fractions J. Am. Oil Chem. Soc. 2011, 88 (3) 381-389 10.1007/s11746-010-1686-7
15. Girgih, A. T.; Udenigwe, C. C.; Aluko, R. E. Reverse-phase HPLC separation of hemp seed (Cannabis sativa L.) protein hydrolysate produced peptide fractions with enhanced antioxidant capacity Plant Foods Hum. Nutr. 2013, 68 (1) 39-46 10.1007/s11130-013-0340-6
16. Gavel, N. T.; Edel, A. L.; Bassett, C. M. C.; Weber, A. M.; Merchant, M.; Rodriguez-Leyva, D.; Pierce, G. N. The effect of dietary hempseed on atherogenesis and contractile function in aortae from hypercholesterolemic rabbits Acta Physiol. Hung. 2011, 98 (3) 273-283 10.1556/APhysiol.98.2011.3.4
17. Prociuk, M. A.; Edel, A. L.; Gavel, N. T.; Lukas, A.; Pierce, G. N. Influence of dietary hempseed on arrhythmia generation by ischemia/reperfusion J. Mol. Cell Cardiol. 2004, 37 (1) 275
18. Prociuk, M. A.; Edel, A. L.; Richard, M. N.; Gavel, N. T.; Ander, B. P.; Dupasquier, C. M. C.; Pierce, G. N. Cholesterol-induced stimulation of platelet aggregation is prevented by a hempseed-enriched diet Can. J. Physiol. Pharmacol. 2008, 86 (4) 153-159 10.1139/Y08-011
19. Zanoni, C.; Aiello, G.; Arnoldi, A.; Lammi, C. Hempseed Peptides Exert Hypocholesterolemic Effects with a Statin-Like Mechanism J. Agric. Food Chem. 2017, 65, 8829 10.1021/acs.jafc.7b02742
20. Ambigaipalan, P.; Al-Khalifa, A. S.; Shahidi, F. Antioxidant and angiotensin I converting enzyme (ACE) inhibitory activities of date seed protein hydrolysates prepared using Alcalase, Flavourzyme and Thermolysin J. Funct. Foods 2015, 18, 1125-1137 10.1016/j.jff.2015.01.021
21. Boschin, G.; Scigliuolo, G. M.; Resta, D.; Arnoldi, A. ACE-inhibitory activity of enzymatic protein hydrolysates from lupin and other legumes Food Chem. 2014, 145, 34-40 10.1016/j.foodchem.2013.07.076
22. Levashov, P. A.; Sutherland, D. S.; Besenbacher, F.; Shipovskov, S. A robust method of determination of high concentrations of peptides and proteins Anal. Biochem. 2009, 395 (1) 111-112 10.1016/j.ab.2009.08.017
23. Lammi, C.; Aiello, G.; Vistoli, G.; Zanoni, C.; Arnoldi, A.; Sambuy, Y.; Ferruzza, S.; Ranaldi, G. A multidisciplinary investigation on the bioavailability and activity of peptides from lupin protein J. Funct. Foods 2016, 24, 297-306 10.1016/j.jff.2016.04.017
24. Nielsen, P. M.; Petersen, D.; Dambmann, C. Improved method for determining food protein degree of hydrolysis J. Food Sci. 2001, 66 (5) 642-646 10.1111/j.1365-2621.2001.tb04614.x
25. Schägger, H. Tricine-SDS-PAGE Nat. Protoc. 2006, 1 (1) 16-22 10.1038/nprot.2006.4
26. Wilkins, M. R.; Gasteiger, E.; Bairoch, A.; Sanchez, J. C.; Williams, K. L.; Appel, R. D.; Hochstrasser, D. F. Protein identification and analysis tools in the ExPASy server Methods Mol. Biol. 1999, 112, 531-552
27. Mooney, C.; Haslam, N. J.; Pollastri, G.; Shields, D. C. Towards the improved discovery and design of functional peptides: Common features of diverse classes permit generalized prediction of bioactivity PLoS One 2012, 7 (10) e45012 10.1371/journal.pone.0045012
28. Malomo, S. A.; Onuh, J. O.; Girgih, A. T.; Aluko, R. E. Structural and antihypertensive properties of enzymatic hemp seed protein hydrolysates Nutrients 2015, 7 (9) 7616-7632 10.3390/nu7095358
29. Bauchart, C.; Morzel, M.; Chambon, C.; Mirand, P. P.; Reynès, C.; Buffière, C.; Rémond, D. Peptides reproducibly released by in vivo digestion of beef meat and trout flesh in pigs Br. J. Nutr. 2007, 98 (6) 1187-1195 10.1017/S0007114507761810
30. Sarver, R. W.; Bills, E.; Bolton, G.; Bratton, L. D.; Caspers, N. L.; Dunbar, J. B.; Harris, M. S.; Hutchings, R. H.; Kennedy, R. M.; Larsen, S. D.; Pavlovsky, A.; Pfefferkorn, J. A.; Bainbridge, G. Thermodynamic and structure guided design of statin based inhibitors of 3-hydroxy-3-methylglutaryl coenzyme A reductase J. Med. Chem. 2008, 51 (13) 3804-3813 10.1021/jm7015057
31. Zhong, F.; Zhang, X. M.; Ma, J. G.; Shoemaker, C. F. Fractionation and identification of a novel hypocholesterolemic peptide derived from soy protein Alcalase hydrolysates Food Res. Int. 2007, 40 (6) 756-762 10.1016/j.foodres.2007.01.005
32. Lammi, C.; Zanoni, C.; Arnoldi, A.; Vistoli, G. Two Peptides from Soy β-Conglycinin Induce a Hypocholesterolemic Effect in HepG2 Cells by a Statin-Like Mechanism: Comparative in Vitro and in Silico Modeling Studies J. Agric. Food Chem. 2015, 63 (36) 7945-7951 10.1021/acs.jafc.5b03497
33. Sarmadi, B. H.; Ismail, A. Antioxidative peptides from food proteins: A review Peptides 2010, 31 (10) 1949-1956 10.1016/j.peptides.2010.06.020
34. Li, H.; Aluko, R. E. Identification and inhibitory properties of multifunctional peptides from pea protein hydrolysate J. Agric. Food Chem. 2010, 58 (21) 11471-11476 10.1021/jf102538g
35. Kobayashi, Y.; Yamauchi, T.; Katsuda, T.; Yamaji, H.; Katoh, S. Angiotensin-I converting enzyme (ACE) inhibitory mechanism of tripeptides containing aromatic residues J. Biosci Bioeng 2008, 106 (3) 310-312 10.1263/jbb.106.310
36. Huang, G. J.; Lu, T. L.; Chiu, C. S.; Chen, H. J.; Wu, C. H.; Lin, Y. C.; Hsieh, W. T.; Liao, J. C.; Sheu, M. J.; Lin, Y. H. Sweet potato storage root defensin and its tryptic hydrolysates exhibited angiotensin converting enzyme inhibitory activity in vitro Bot. Stud. 2011, 52 (3) 257-264
37. O'Keeffe, M. B.; Norris, R.; Alashi, M. A.; Aluko, R. E.; FitzGerald, R. J. Peptide identification in a porcine gelatin prolyl endoproteinase hydrolysate with angiotensin converting enzyme (ACE) inhibitory and hypotensive activity J. Funct. Foods 2017, 34, 77-88 10.1016/j.jff.2017.04.018
38. Bailey, C. J.; Tahrani, A. A.; Barnett, A. H. Future glucose-lowering drugs for type 2 diabetes Lancet Diabetes Endocrinol. 2016, 4 (4) 350-359 10.1016/S2213-8587(15)00462-3
39. Boots, J.-W. P. Protein hydrolysate enriched in peptides inhibiting DPP-IV and their use. WO Patent 2006068480 A2, June 29, 2006.
40. Lammi, C.; Zanoni, C.; Arnoldi, A.; Vistoli, G. Peptides derived from soy and lupin protein as Dipeptidyl-Peptidase IV inhibitors: In vitro biochemical screening and in silico molecular modeling study J. Agric. Food Chem. 2016, 64 (51) 9601-9606 10.1021/acs.jafc.6b04041
41. Nongonierma, A. B.; FitzGerald, R. J. Investigation of the Potential of Hemp, Pea, Rice and Soy Protein Hydrolysates as a Source of Dipeptidyl Peptidase IV (DPP-IV) Inhibitory Peptides Food Dig Res. Curr. Opin. 2015, 6 (1-3) 19-29
42. Amigo-Benavent, M.; Clemente, A.; Caira, S.; Stiuso, P.; Ferranti, P.; del Castillo, M. D. Use of phytochemomics to evaluate the bioavailability and bioactivity of antioxidant peptides of soybean β-conglycinin Electrophoresis 2014, 35 (11) 1582-1589 10.1002/elps.201300527
43. Regazzo, D.; Mollé, D.; Gabai, G.; Tomé, D.; Dupont, D.; Leonil, J.; Boutrou, R. The (193-209) 17-residues peptide of bovine β-casein is transported through Caco-2 monolayer Mol. Nutr. Food Res. 2010, 54 (10) 1428-1435 10.1002/mnfr.200900443
44. Miguel, M.; Dávalos, A.; Manso, M. A.; de la Peña, G.; Lasunción, M. A.; López-Fandiño, R. Transepithelial transport across Caco-2 cell monolayers of antihypertensive egg-derived peptides. PepT1-mediated flux of Tyr-Pro-Ile Mol. Nutr. Food Res. 2008, 52 (12) 1507-1513 10.1002/mnfr.200700503