Proteolytic activation of proteose peptone component 3 by release of a C-terminal peptide with antibacterial properties

Journal of Dairy Science

Volumn 95, Issue 6, 2012, Pages 2819-2829

  Pedersen, L R L ^a   Hansted, J G ^a,b   Nielsen, S B ^a,b   Petersen, T E ^a   Sorensen U S ^a   Otzen, D ^a,b   Sorensen E S ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Antibacterial peptide; Antimicrobial activity; Lactophoricin; Proteose peptone component 3

Indexed keywords

ANTIINFECTIVE AGENT; CASEIN; GLYCOPROTEIN; LACTOPHORIN PROTEIN, BOS TAURUS; MILK PROTEIN; PEPTIDE FRAGMENT; PP3 PROTEIN, BOS TAURUS; PROTEOSE PEPTONE COMPONENT 3 (110 135); PROTEOSE PEPTONE COMPONENT 3 (110-135);

ANIMAL; ARTICLE; CATTLE; CIRCULAR DICHROISM; DRUG EFFECT; ESCHERICHIA COLI; FEMALE; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN DEGRADATION; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS THERMOPHILUS;

ANIMALS; ANTI-BACTERIAL AGENTS; CASEINS; CATTLE; CIRCULAR DICHROISM; ESCHERICHIA COLI; FEMALE; GLYCOPROTEINS; MILK PROTEINS; PEPTIDE FRAGMENTS; PROTEOLYSIS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS THERMOPHILUS;

ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS THERMOPHILUS;

EID: 84862072352     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2011-4837     Document Type: Article

References (46)

1. Andrade M.A., Chacón P., Merelo J.J., Morán F. Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 1993, 6:383-390.
2. Bak M., Sørensen M.D., Sørensen E.S., Rasmussen L.K., Sørensen O.W., Petersen T.E., Nielsen N.C. The structure of the membrane-binding 38 C-terminal residues from bovine PP3 determined by liquid- and solid-state NMR spectroscopy. Eur. J. Biochem. 2000, 267:188-199.
3. Barzyk W., Campagna S., Wie{ogonek}cław K., Korchowiec B., Rogalska E. The affinity of two antimicrobial peptides derived from bovine milk proteins for model lipid membranes. Colloids Surf. A 2009, 343:104-110.
4. Beg O.U., von Bahr-Lindström H., Zaidi Z.H., Jörnvall H. Characterization of a heterogeneous camel milk whey non-casein protein. FEBS Lett. 1987, 216:270-274.
5. Campagna S., Cosette P., Molle G., Gaillard J.-L. Evidence for membrane affinity of the C-terminal domain of bovine milk PP3 component. Biochim. Biophys. Acta 2001, 1513:217-222.
6. Campagna S., Mathot A.G., Fleury Y., Girardet J.-M., Gaillard J.-L. Antibacterial activity of lactophoricin, a synthetic 23-residues peptide derived from the sequence of bovine milk component-3 of proteose peptone. J. Dairy Sci. 2004, 87:1621-1626.
7. Campagna S., Van Mau N., Heitz F., Humbert G., Gaillard J.-L. Specific interaction between anionic phospholipids and milk bovine component PP3 and its 119-135 C-terminal fragment. Colloids Surf. B 1999, 13:299-309.
8. Campagna S., Vitoux B., Humbert G., Girardet J.M., Linden G., Haertle T., Gaillard J.L. Conformational studies of a synthetic peptide from the putative lipid-binding domain of bovine milk component PP3. J. Dairy Sci. 1998, 81:3139-3148.
9. Cantisani A., Napolitano L., Giuffrida M.G., Conti A. Direct identification and characterization of llama (Lama glama L.) whey proteins by microsequencing after Western blotting. J. Biochem. Biophys. Methods 1990, 21:227-236.
10. Chen F.-Y., Lee M.-T., Huang H.W. Sigmoidal concentration dependence of antimicrobial peptide activities: A case study on alamethicin. Biophys. J. 2002, 82:908-914.
11. Christensen B., Petersen T.E., Sørensen E.S. Post-translational modification and proteolytic processing of urinary osteopontin. Biochem. J. 2008, 411:53-61.
12. De Feijter J.A., Benjamins J., Veer F.A. Ellipsometry as a tool to study the adsorption behavior of synthetic and biopolymers at the air-water interface. Biopolymers 1978, 17:1759-1772.
13. Dowbenko D., Kikuta A., Fennie C., Gillett N., Lasky L.A. Glycosylation-dependent cell adhesion molecule 1 (GlyCAM 1) mucin is expressed by lactating mammary gland epithelial cells and is present in milk. J. Clin. Invest. 1993, 92:952-960.
14. Dowbenko D., Watson S.R., Lasky L.A. Cloning of a rat homologue of mouse GlyCAM 1 reveals conservation of structural domains. J. Biol. Chem. 1993, 268:14399-14403.
15. Expósito I.L., Recio I. Antibacterial activity of peptides and folding variants from milk proteins. Int. Dairy J. 2006, 16:1294-1305.
16. Graham J.M., Higgins J.A. Membrane Analysis 1997, Taylor & Francis Inc, New York, NY.
17. Groenen M.A.M., Dijkhof R.J.M., van der Poel J.J. Characterization of a GlyCAM1-like gene (glycosylation-dependent cell adhesion molecule 1) which is highly and specifically expressed in the lactating bovine mammary gland. Gene 1995, 158:189-195.
18. Hunt J.F., Rath P., Rothschild K.J., Engelman D.M. Spontaneous, pH-dependent membrane insertion of a transbilayer alpha-helix. Biochemistry 1997, 36:15177-15192.
19. Jirgensons B. Effects of n-propyl alcohol and detergents on the optical rotatory dispersion of alpha-chymotrypsinogen, beta-casein, histone fraction F1, and soybean trypsin inhibitor. J. Biol. Chem. 1967, 242:912-918.
20. Johnsen L.B., Sørensen E.S., Petersen T.E., Berglund L. Characterization of a bovine mammary gland PP3 cDNA reveals homology with mouse and rat adhesion molecule GlyCAM-1. Biochim. Biophys. Acta 1995, 1260:116-118.
21. Kanoh N., Dai C.F., Tanaka T., Izawa D., Li Y.F., Kawashima H., Miyasaka M. Constitutive expression of GlyCAM-1 core protein in the rat cochlea. Cell Adhes. Commun. 1999, 7:259-266.
22. Lasky L.A., Singer M.S., Dowbenko D., Imai Y., Henzel W.J., Grimley C., Fennie C., Gillett N., Watson S.R., Rosen S.D. An endothelial ligand for l-selectin is a novel mucin-like molecule. Cell 1992, 69:927-938.
23. Lister I.M.B., Rasmussen L.K., Johnsen L.B., Møller L., Petersen T.E., Sørensen E.S. The primary structure of caprine PP3: Amino acid sequence, phosphorylation, and glycosylation of component PP3 from the proteose-peptone fraction of caprine milk. J. Dairy Sci. 1998, 81:2111-2115.
24. Liu L.-P., Deber C.M. Anionic phospholipids modulate peptide insertion into membranes. Biochemistry 1997, 36:5476-5482.
25. Matsuzaki K., Murase O., Fujii N., Miyajima K. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 1996, 35:11361-11368.
26. Mukerjee P. The nature of the association equilibria and hydrophobic bonding in aqueous solutions of association colloids. Adv. Colloid Interface Sci. 1967, 1:241-275.
27. Nielsen S.B., Otzen D.E. Impact of the antimicrobial peptide Novicidin on membrane structure and integrity. J. Colloid Interface Sci. 2010, 345:248-256.
28. Oren Z., Shai Y. Mode of action of linear amphipathic α-helical antimicrobial peptides. Biopolymers 1998, 47:451-463.
29. Otzen D.E. Amyloid formation in surfactants and alcohols: Membrane mimetics or structural switchers?. Curr. Protein Pept. Sci. 2010, 11:355-371.
30. Paquet D., Nejjar Y., Alais C. Electrophoretic and chromatographic behavior of the proteose-peptone fraction of cows milk. Milchwissenschaft 1985, 40:200-203.
31. Pedersen L.R.L., Nielsen S.B., Hansted J.G., Petersen T.E., Otzen D.E., Sørensen E.S. PP3 forms stable tetrameric structures through hydrophobic interactions via the C-terminal amphipathic helix and undergoes reversible thermal dissociation and denaturation. FEBS J. 2012, 279:336-347.
32. Rasmussen L.K., Johnsen L.B., Petersen T.E., Sørensen E.S. Human GlyCAM-1 mRNA is expressed in the mammary gland as splicing variants and encodes various aberrant truncated proteins. Immunol. Lett. 2002, 83:73-75.
33. Rhimi M., Boisson A., Dejob M., Boudebouze S., Maguin E., Haser R., Aghajari N. Efficient bioconversion of lactose in milk and whey: Immobilization and biochemical characterization of a beta-galactosidase from the dairy Streptococcus thermophilus LMD9 strain. Res. Microbiol. 2010, 161:515-525.
34. Roccatano D., Colombo G., Fioroni M., Mark A.E. Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: A molecular dynamics study. Proc. Natl. Acad. Sci. USA 2002, 99:12179-12184.
35. Sansom M.S. The biophysics of peptide models of ion channels. Prog. Biophys. Mol. Biol. 1991, 55:139-235.
36. Sørensen E.S., Petersen T.E. Phosphorylation, glycosylation and amino acid sequence of component PP3 from the proteose peptone fraction of bovine milk. J. Dairy Res. 1993, 60:535-542.
37. Sørensen E.S., Petersen T.E. Purification and characterization of three proteins isolated from the proteose peptone fraction of bovine milk. J. Dairy Res. 1993, 60:189-197.
38. Sørensen E.S., Rasmussen L.K., Møller L., Petersen T.E. The localization and multimeric nature of component PP3 in bovine milk: Purification and characterization of PP3 from caprine and ovine milks. J. Dairy Sci. 1997, 80:3176-3181.
39. Spencer T.E., Bartol F.F., Bazer F.W., Johnson G.A., Joyce M.M. Identification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus. Biol. Reprod. 1999, 60:241-250.
40. Vad B., Thomsen L.A., Bertelsen K., Franzmann M., Pedersen J.M., Nielsen S.B., Vosegaard T., Valnickova Z., Skrydstrup T., Enghild J.J., Wimmer R., Nielsen N.C., Otzen D.E. Divorcing folding from function: How acylation affects the membrane-perturbing properties of an antimicrobial peptide. Biochim. Biophys. Acta 2010, 1804:806-820.
41. Whitmore L., Wallace B.A. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases. Biopolymers 2008, 89:392-400.
42. Wilmes M., Cammue B.P.A., Sahl H.-G., Thevissen K. Antibiotic activities of host defense peptides: More to it than lipid bilayer perturbation. Nat. Prod. Rep. 2011, 28:1350-1358.
43. Winston P.W., Bates D.H. Saturated solutions for the control of humidity in biological research. Ecology 1960, 41:232-237.
44. Wu Y., Huang H.W., Olah G.A. Method of oriented circular dichroism. Biophys. J. 1990, 57:797-806.
45. Yang L., Harroun T.A., Weiss T.M., Ding L., Huang H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 2001, 81:1475-1485.
46. Zimecki M., Kruzel M.L. Milk-derived proteins and peptides of potential therapeutic and nutritive value. J. Exp. Ther. Oncol. 2007, 6:89-106.