Structure and ACE-Inhibitory Activity of Peptides Derived from Hen Egg White Lysozyme

  • Mina Memarpoor-Yazdi
  • Ahmad Asoodeh
  • JamshidKhan Chamani
Article

Abstract

Angiotensin I-converting enzyme plays an important role in hypertension and therefore its inhibition is considered to be a useful procedure in the prevention of hypertension. Two novel ACE inhibitory peptides were purified and identified from the papain-trypsin hydrolysate of hen egg white lysozyme using reverse phase-high performance liquid chromatography. The sequences of identified peptides were NTDGSTDYGILQINSR (MW: 1,753.98 ± 0.5 Da) and VFGR (MW: 459.26 ± 0.5 Da), which were named F2 and F9 peptide, respectively. Analyses of the far-UV CD spectra of ACE in the absence and presence of the F2 peptide revealed ACE secondary structural changes. In the presence of the F2 peptide, a loss of helical content of ACE was observed, which can lead to decrease of the enzymatic activity. Lineweaver–Burk plots show that the identified peptides both act as non-competitive ACE inhibitors. These findings would be helpful on the understanding of interaction between ACE and its inhibitory peptides.

Keywords

RP-HPLC ACE inhibitory activity Inhibition pattern Circular dichroism spectroscopy 

Abbreviations

ACE

Angiotensin I-converting enzyme

FAPGG

N-[3-(2-furylacryloyl-Phe-Gly–Gly)]

RP-HPLC

Reverse phase high-performance liquid chromatography

HEWL

Hen egg white lysozyme

CD

Circular dichroism

MALDI-TOF

Matrix-assisted laser desorption/ionization time of flight

References

  1. Abubakar A, Saito T, Kitazawa H, Kawai Y, Itoh T (1998) Structural analysis of new antihypertensive peptides derived from cheese whey protein by proteinase k digestion. J Dairy Res 81:3131–3138CrossRefGoogle Scholar
  2. Aleman A, Giménez B, Pérez-Santin E, Gómez-Guillén MC, Montero P (2011) Contribution of Leu and Hyp residues to antioxidant and ACE-inhibitory activities of peptide sequences isolated from squid gelatin hydrolysate. Food Chem 125:334–341CrossRefGoogle Scholar
  3. Asoodeh A, Memarpoor-Yazdi M, Chamani J (2012) Purification and characterisation of angiotensin I converting enzyme inhibitory peptides from lysozyme hydrolysates. Food Chem 131:291–295CrossRefGoogle Scholar
  4. Ferreira SH, Bartelt DC, Greene LJ (1970) Isolation of bradykinin-potentiating peptides from Bothropsjararaca venom. Biochemistry 9:2583–2593PubMedCrossRefGoogle Scholar
  5. FitzGerald RJ, Murray BA, Walsh DJ (2004) Hypotensive peptides from milk proteins. J Nutr 134:980S–988SPubMedGoogle Scholar
  6. Fujita H, Yokoyama K, Yoshikawa M (2000) Classification and antihypertensive activity of angiotensin I-converting enzyme inhibitory peptides derived from food proteins. J Food Sci 65:564–569CrossRefGoogle Scholar
  7. Greenfield NJ (1996) Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal Biochem 235:1–10PubMedCrossRefGoogle Scholar
  8. Hassan F, Kitagawa M, Kumada Y, Hashimoto N, Shiiba M, Katoh S, Terashima M (2006) Production kinetics of angiotensin-I converting enzyme inhibitory peptides from bonito meat in artificial gastric juice. Proc Biochem 41:505–511CrossRefGoogle Scholar
  9. Hernandez-Ledesma B, Davalos A, Bartolome B, Amigo L (2005) Preparation of antioxidant enzymatic hydrolysates from alpha-lactalbumin and beta-lactoglobulin, Identification of active peptides by HPLC-MS/MS. J Agric Food Chem 53:588–593PubMedCrossRefGoogle Scholar
  10. Hyun CK, Shin HK (2000) Utilization of bovine blood plasma proteins for the production of angiotensin I converting enzyme inhibitory peptide. Proc Biochem 36:65–71CrossRefGoogle Scholar
  11. Jang JH, Jeong SC, Kim JH, Lee YH, Ju YC, Lee JS (2011) Characterisation of a new antihypertensive angiotensin I-converting enzyme inhibitory peptide from Pleurotus cornucopiae. Food Chem 127:412–418CrossRefGoogle Scholar
  12. Li GH, Le GW, Shi YH, Shrestha S (2004) Angiotensin I-converting enzyme inhibitory peptides from food proteins and their physiological and pharmacological effects. J Nut Res 24:469–486Google Scholar
  13. Liu J, Yu Z, Zhao W, Lin S, Wang E, Zhang Y et al (2010) Isolation and identification of angiotensin-converting enzyme inhibitory peptides from egg white protein hydrolysates. Food Chem 122:1159–1163CrossRefGoogle Scholar
  14. Matsui T, Matsufuji H, Seki E, Osajima K, Nakashima M, Osajima Y (1994) Angiotensin I-converting enzyme inhibitory peptides in an alkaline protease hydrolysate derived from sardine muscle. Biosci Biotechnol Biochem 58:2244–2245PubMedCrossRefGoogle Scholar
  15. Matsui T, Li CH, Osajima Y (1999) Preparation and characterization of novel bioactive peptides responsible for angiotensin I-converting enzyme inhibition from wheat germ. J Pept Sci 5:289–297PubMedCrossRefGoogle Scholar
  16. Matsuo K, Sakurada Y, Tate SI, Namatame H, Taniguchi M, Gekko K (2012) Secondary-structure of alcohol-denatured proteins by vacuum-ultraviolet circular dichroism spectroscopy. Proteins: structure. Funct Bioinform 80:281–293CrossRefGoogle Scholar
  17. Memarpoor-Yazdi M, Asoodeh A, Chamani J (2012) A novel antioxidant and antimicrobial peptide from hen egg white lysozyme hydrolysates. J Funct Foods 4:278–286CrossRefGoogle Scholar
  18. Miguel M, Aleixandre A (2006) Antihypertensive peptides derived from egg proteins. J Nutr 136:1457–1460PubMedGoogle Scholar
  19. Miguel M, Recio I, Gómez-Ruiz JA, Ramos M, López-Fandiño R (2004) Angiotensin I-converting enzyme inhibitory activity of peptides derived from egg white proteins by enzymatic hydrolysis. J Food Prot 67:1914–1920PubMedGoogle Scholar
  20. Miguel M, Manso M, Aleixandre A, Alonso MJ, Salaices M, López-Fandio R (2007) Vascular effects, angiotensin I-converting enzyme (ACE)-inhibitory activity, and antihypertensive properties of peptides derived from egg white. J Agric Food Chem 55:10615–10621PubMedCrossRefGoogle Scholar
  21. Mine Y, Kovacs-Nolan J (2006) New insights in biologically active proteins and peptides derived from hen egg. Worlds Poul Sci J 62:87–95CrossRefGoogle Scholar
  22. Mine Y, Ma FP, Lauriau S (2004) Antimicrobial peptides released by enzymatic hydrolysis of hen egg white lysozyme. J Agric Food Chem 52:1088–1094PubMedCrossRefGoogle Scholar
  23. Murakami M, Tonouchi H, Takahashi R, Kitazawa H, Kawai Y, Negishi H et al (2004) Structural analysis of a new anti-hypertensive peptide (b-lactosin B) isolated from a commercial whey product. J Dairy Res 87:1967–1974CrossRefGoogle Scholar
  24. Muruyama S, Suzuki H (1982) A peptide inhibitor of angiotensin I converting enzyme in the tryptic hydrolysate of casein. Agric Biol Chem 46:1393–1394CrossRefGoogle Scholar
  25. Nakagomi K, Fujimura A, Ebisu H, Sakai T, Sadkane Y, Fuji N, Tanimura T (1998) Acein-1, a novel angiotensin-I-converting enzyme inhibitory peptide isolated from tryptic hydrolysate of human plasma. FEBS Lett 438:225–257CrossRefGoogle Scholar
  26. Nakagomi K, Ebisu H, Sadakane Y, Fujii N, Akizawa T, Tnimura T (2000) Properties and human origine of two angiotensin I-converting enzyme inhibitory peptides isolated from a tryptic hydrolysate of human serum albumin. Biol Pharm Bull 23:879–883PubMedCrossRefGoogle Scholar
  27. Natesh R, Schwager SL, Sturrock ED, Acharya KR (2003) Crystal structure of the human angiotensin-converting enzyme-lisinopril complex. Nature 421:551–554PubMedCrossRefGoogle Scholar
  28. Palmer T (2001) Enzymes, biochemistry, biotechnology and clinical chemistry (1st), Chap. 8. Harwood Publishing, ChichesterGoogle Scholar
  29. Phelan M, Aherne A, FitzGerald RJ, O’Brien NM (2009) Casein-derived bioactive peptides: biological effects, industrial uses, safety aspects and regulatory status. Int Dairy J 19:643–654CrossRefGoogle Scholar
  30. Pihlanto-Leppala A (2000) Bioactive peptides derived from bovine whey proteins: opioid and ace-inhibitory peptides. Trends Food Sci Tech 11:347–356CrossRefGoogle Scholar
  31. Pihlanto-Leppala A, Rokka T, Korhonen H (1998) Angiotensin I converting enzyme inhibitory properties peptides derived from bovine milk proteins. Int Dairy J 8:325–331CrossRefGoogle Scholar
  32. Pihlanto-Leppälä A, Koskinen P, Phlola K, Tupasela T, Korhonen H (2000) Angiotensin I-converting enzyme inhibitory properties of whey protein digests: concentration and characterization of active peptides. J Dairy Res 67:53–64PubMedCrossRefGoogle Scholar
  33. Rao SQ, Ju T, Sun J, Su YJ, Xu RR, Yang YJ (2012) Purification and characterization of angiotensin I-converting enzyme inhibitory peptides from enzymatic hydrolysate of hen egg white lysozyme. Food Res Int 46:127–134CrossRefGoogle Scholar
  34. Shin ZI, Ahn CW, Nam HS, Lee HJ, Moon TH (1995) Fractionation of angiotensin converting enzyme inhibitory peptide from soybean paste. Korean J Food Sci Technol 27:30–234Google Scholar
  35. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded set. Anal Biochem 287:252–260PubMedCrossRefGoogle Scholar
  36. Suersuna K (1998) Isolation and characterization of angiotensin I-converting enzyme inhibitor dipeptide derived from Allium sativum L. (garlic). J Nutr Biochem 9:415–419CrossRefGoogle Scholar
  37. Takakuwa T, Konno T, Meguro H (1985) A new standard substance for calibration of circular dichroism: ammonium d-10-camphorsulfonate. Anal Sci 1:215–218CrossRefGoogle Scholar
  38. Tsuruki T, Kishi K, Takahashi M, Tanaka M, Matsukawa T, Yoshikawa M (2003) Soymetide an immunostimulating peptide derived from soybean β-conglycinin, is an fMLP agonist. FEBS Lett 540:206–210PubMedCrossRefGoogle Scholar
  39. Vahedian-Movahed H, Saberi MR, Chamani J (2011) Comparison of binding interactions of lomefloxacin to serum albumin and serum transferrin by resonance light scattering and fluorescence quenching methods. J Biomol Struct Dyn 28:483–502PubMedCrossRefGoogle Scholar
  40. Yamamoto N, Akino A, Takano T (1994) Antihypertensive effect of the peptides derived from casein by an extracellular propeinase from Lactobacillus heveticus CP790. J Dairy Res 77:917–922CrossRefGoogle Scholar
  41. Yoshii H, Tachi N, Ohba R, Sakamura O, Takeyama H, Itani T (2001) Antihypertensive effect of ACE inhibitory oligopeptides from chicken egg yolks. Comp Biochem Physiol 128C:27–33Google Scholar
  42. You SJ, Udenigwe CC, Aluko RE, Wu JP (2010) Multifunctional peptides from egg white lysozyme. Food Res Int 43:848–855CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Mina Memarpoor-Yazdi
    • 1
  • Ahmad Asoodeh
    • 2
    • 3
  • JamshidKhan Chamani
    • 1
  1. 1.Department of Biology, Faculty of Sciences, Mashhad BranchIslamic Azad UniversityMashhadIran
  2. 2.Department of Chemistry, Faculty of SciencesFerdowsi University of MashhadMashhadIran
  3. 3.Cellular and Molecular Research Group, Institute of BiotechnologyFerdowsi University of MashhadMashhadIran

Personalised recommendations