PP3 forms stable tetrameric structures through hydrophobic interactions via the C-terminal amphipathic helix and undergoes reversible thermal dissociation and denaturation

FEBS Journal

Volumn 279, Issue 2, 2012, Pages 336-347

  Pedersen, Lise R L ^a   Nielsen, Søren B ^a,b   Hansted, Jon G ^a,b   Petersen, Torben E ^a   Otzen, Daniel E ^a,b   Sørensen, Esben S ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

asymmetric flow field flow fractionation; bovine milk; lactophorin; multimerization; proteose peptone component 3

Indexed keywords

GLYCOPROTEIN; OLEIC ACID; PROTEOSE PEPTONE COMPONENT 3; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; DISSOCIATION; FIELD FLOW FRACTIONATION; FOOD PROCESSING; HYDROPHOBICITY; LIGHT SCATTERING; MILK; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING; STOMACH PH; THERMAL DISSOCIATION;

BOVINAE;

EID: 84855457924     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08428.x     Document Type: Article

References (58)

1. Rowland SJ, (1937) The soluble fraction of milk. J Dairy Res 8, 6-14.
2. Rowland SJ, (1938) The precipitation of the proteins in milk. J Dairy Res 9, 30-41.
3. Paquet D, Nejjar Y, &, Linden G, (1988) Study of a hydrophobic protein fraction isolated from milk proteose-peptone. J Dairy Sci 71, 1464-1471.
4. Andrews AT, &, Alichanidis E, (1983) Proteolysis of caseins and the proteose-peptone fraction of bovine milk. J Dairy Res 50, 275-290.
5. Paquet D, (1989) Review: the proteose peptone fraction of milk. Lait 69, 1-21.
6. Kanno C, (1989) Purification and separation of multiple forms of lactophorin from bovine milk whey and their immunological and electrophoretical properties. J Dairy Sci 72, 883-891.
7. Kanno C, (1989) Characterization of multiple forms of lactophorin isolated from bovine milk whey. J Dairy Sci 72, 1732-1739.
8. Paquet D, Nejjar Y, &, Alais C, (1985) Electrophoretic and chromatographic behavior of the proteose-peptone fraction of cows milk. Milchwissenschaft 40, 200-203.
9. Beg OU, von Bahr-Lindstrom H, Zaidi ZH, &, Jornvall H, (1987) Characterization of a heterogeneous camel milk whey non-casein protein. FEBS Lett 216, 270-274.
10. Cantisani A, Napolitano L, Giuffrida MG, &, Conti A, (1990) Direct identification and characterization of llama (Lama glama L.) whey proteins by microsequencing after western blotting. J Biochem Biophys Methods 21, 227-236. (Pubitemid 20299070)
11. Sørensen ES, Rasmussen LK, Moller L, &, Petersen TE, (1997) The localization and multimeric nature of component PP3 in bovine milk: purification and characterization of PP3 from caprine and ovine milks. J Dairy Sci 80, 3176-3181. (Pubitemid 127447049)
12. Lister IM, Rasmussen LK, Johnsen LB, Moller L, Petersen TE, &, Sørensen ES, (1998) 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 81, 2111-2115. (Pubitemid 128445909)
13. Rasmussen LK, Johnsen LB, Petersen TE, &, Sørensen ES, (2002) Human GlyCAM-1 mRNA is expressed in the mammary gland as splicing variants and encodes various aberrant truncated proteins. Immunol Lett 83, 73-75. (Pubitemid 34607542)
14. Sørensen ES, &, Petersen TE, (1993) Phosphorylation, glycosylation and amino acid sequence of component PP3 from the proteose peptone fraction of bovine milk. J Dairy Res 60, 535-542. (Pubitemid 2003311)
15. Sørensen ES, &, Petersen TE, (1993) Purification and characterization of three proteins isolated from the proteose peptone fraction of bovine milk. J Dairy Res 60, 189-197.
16. Johnsen LB, Sørensen ES, Petersen TE, &, Berglund L, (1995) Characterization of a bovine mammary gland PP3 cDNA reveals homology with mouse and rat adhesion molecule GlyCAM-1. Biochim Biophys Acta 1260, 116-118.
17. Groenen MA, Dijkhof RJ, &, van der Poel JJ, (1995) 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 158, 189-195.
18. Lasky LA, Singer MS, Dowbenko D, Imai Y, Henzel WJ, Grimley C, Fennie C, Gillett N, Watson SR, &, Rosen SD, (1992) An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell 69, 927-938.
19. Dowbenko D, Watson SR, &, Lasky LA, (1993) Cloning of a rat homologue of mouse GlyCAM 1 reveals conservation of structural domains. J Biol Chem 268, 14399-14403. (Pubitemid 23195568)
20. Dowbenko D, Kikuta A, Fennie C, Gillett N, &, Lasky LA, (1993) 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 92, 952-960. (Pubitemid 23262419)
21. Kanoh N, Dai CF, Tanaka T, Izawa D, Li YF, Kawashima H, &, Miyasaka M, (1999) Constitutive expression of GlyCAM-1 core protein in the rat cochlea. Cell Adhes Commun 7, 259-266. (Pubitemid 129725809)
22. Spencer TE, Bartol FF, Bazer FW, Johnson GA, &, Joyce MM, (1999) Identification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus. Biol Reprod 60, 241-250. (Pubitemid 29063862)
23. Girardet JM, Coddeville B, Plancke Y, Strecker G, Campagna S, Spik G, &, Linden G, (1995) Structure of glycopeptides isolated from bovine milk component PP3. Eur J Biochem 234, 939-946. (Pubitemid 26024337)
24. Kjeldsen F, Haselmann KF, Budnik BA, Sørensen ES, &, Zubarev RA, (2003) Complete characterization of posttranslational modification sites in the bovine milk protein PP3 by tandem mass spectrometry with electron capture dissociation as the last stage. Anal Chem 75, 2355-2361. (Pubitemid 36582819)
25. Bak M, Sørensen MD, Sørensen ES, Rasmussen LK, Sørensen OW, Petersen TE, &, Nielsen NC, (2000) The structure of the membrane-binding 38 C-terminal residues from bovine PP3 determined by liquid- and solid-state NMR spectroscopy. Eur J Biochem 267, 188-199. (Pubitemid 30029753)
26. Mikkelsen TL, Bakman S, Sørensen ES, Barkholt V, &, Frokiaer H, (2005) Sialic acid-containing milk proteins show differential immunomodulatory activities independent of sialic acid. J Agric Food Chem 53, 7673-7680. (Pubitemid 41499607)
27. Sugahara T, Onda H, Shinohara Y, Horii M, Akiyama K, Nakamoto K, &, Hara K, (2005) Immunostimulation effects of proteose-peptone component 3 fragment on human hybridomas and peripheral blood lymphocytes. Biochim Biophys Acta 1725, 233-240. (Pubitemid 41253933)
28. Grenby TH, Andrews AT, Mistry M, &, Williams RJ, (2001) Dental caries-protective agents in milk and milk products: investigations in vitro. J Dent 29, 83-92. (Pubitemid 33660544)
29. Inagaki M, Nagai S, Yabe T, Nagaoka S, Minamoto N, Takahashi T, Matsuda T, Nakagomi O, Nakagomi T, Ebina T, et al. (2010) The bovine lactophorin C-terminal fragment and PAS6/7 were both potent in the inhibition of human rotavirus replication in cultured epithelial cells and the prevention of experimental gastroenteritis. Biosci Biotechnol Biochem 74, 1386-1390.
30. Campagna S, Cosette P, Molle G, &, Gaillard JL, (2001) Evidence for membrane affinity of the C-terminal domain of bovine milk PP3 component. Biochim Biophys Acta 1513, 217-222. (Pubitemid 32706419)
31. Campagna S, Mathot AG, Fleury Y, Girardet JM, &, Gaillard JL, (2004) Antibacterial activity of lactophoricin, a synthetic 23-residues peptide derived from the sequence of bovine milk component-3 of proteose peptone. J Dairy Sci 87, 1621-1626. (Pubitemid 38893292)
32. Barzyk W, Campagna S, Wieclaw K, Korchowiec B, &, Rogalska E, (2009) The affinity of two antimicrobial peptides derived from bovine milk proteins for model lipid membranes. Colloid Surface A 343, 104-110.
33. Innocente N, Corradini C, Blecker C, &, Paqout M, (1998) Emulsifying properties of the total fraction and the hydrophobic fraction of the bovine milk proteose-peptones. Int Dairy J 8, 981-985. (Pubitemid 29532190)
34. Courthaudon J-L, Girardet J-M, Chapal C, Lorient D, &, Linden G, (1995) Surface activity and competitive adsorption of milk component 3 and porcine pancretic lipase at the dodecane-water interface. In. Food Macromolecules and Colloids (, Dickinson E, &, Lorient D, eds.), pp. 58-70. The Royal Society of Chemistry, Cambridge, UK.
35. Ng WC, Brunner JR, &, Rhee KC, (1970) Proteose-peptone fraction of bovine milk: lacteum serum component 3-a whey glycoprotein. J Dairy Sci 53, 987-996.
36. Sousa A, Passarinha LA, Rodrigues LR, Teixeira JA, Mendonca A, &, Queiroz JA, (2008) Separation of different forms of proteose peptone 3 by hydrophobic interaction chromatography with a dual salt system. Biomed Chromatogr 22, 447-449. (Pubitemid 351722142)
37. Sørensen ES, Rasmussen LK, &, Petersen TE, (1999) Component PP3 from bovine milk is a substrate for transglutaminase. Sequence location of putative crosslinking sites. J Dairy Res 66, 145-150. (Pubitemid 29083830)
38. Ewaschuk JB, Unger S, Harvey S, O'Connor DL, &, Field CJ, (2011) Effect of pasteurization on immune components of milk: implications for feeding preterm infants. Appl Physiol Nutr Metab 36, 175-182.
39. Otzen DE, (2011) Protein-surfactant interactions: a tale of many states. Biochim Biophys Acta 1814, 562-591.
40. Otzen DE, (2010) Amyloid formation in surfactants and alcohols: membrane mimetics or structural switchers? Curr Protein Pept Sci 11, 355-371.
41. Yohannes G, Wiedmer SK, Elomaa M, Jussila M, Aseyev V, &, Riekkola ML, (2010) Thermal aggregation of bovine serum albumin studied by asymmetrical flow field-flow fractionation. Anal Chim Acta 675, 191-198.
42. Wen J, Arakawa T, &, Philo JS, (1996) Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal Biochem 240, 155-166. (Pubitemid 26304259)
43. Otzen DE, Sehgal P, &, Westh P, (2009) Alpha-Lactalbumin is unfolded by all classes of surfactants but by different mechanisms. J Colloid Interface Sci 329, 273-283.
44. Sehgal P, Bang Nielsen S, Pedersen S, Wimmer R, &, Otzen DE, (2007) Modulation of cutinase stability and structure by phospholipid detergents. Biochim Biophys Acta 1774, 1544-1554. (Pubitemid 350235347)
45. MÃ¥nsson HL, (2008) Fatty acids in bovine milk fat. Food & Nutrition Research, doi:.
46. Kappeler S, Farh Z, &, Puhan Z, (1999) Alternative splicing og lactophorin mRAN from lactating mammary gland of the camel (Camelus dromedarius). J Dairy Sci 82, 2084-2093. (Pubitemid 129552445)
47. Girardet JM, Saulnier F, Gaillard JL, Ramet JP, &, Humbert G, (2000) Camel (Camelus dromedarius) milk PP3: evidence for an insertion in the amino-terminal sequence of the camel milk whey protein. Biochem Cell Biol 78, 19-26. (Pubitemid 30158956)
48. Cartier P, (1990) Inhibiting and activating effects of skim milks and proteose-peptone fractions on spontaneous lipolysis and purified lipoprotein lipase activity in bovine milk. J Dairy Sci 73, 1173-1177.
49. De Feijter JA, Benjamins J, &, Veer FA, (1978) Ellipsometry as a tool to study the adsorption behavior of synthetic and biopolymers at the air-water interface. Biopolymers 17, 1759-1772. (Pubitemid 8367473)
50. Yadav S, &, Ahmad F, (2000) A new method for the determination of stability parameters of proteins from their heat-induced denaturation curves. Anal Biochem 283, 207-213. (Pubitemid 30626271)
51. Mogensen JE, Ipsen H, Holm J, &, Otzen DE, (2004) Elimination of a misfolded folding intermediate by a single point mutation. Biochemistry 43, 3357-3367. (Pubitemid 38391692)
52. Andrade MA, Chacon P, Merelo JJ, &, Moran F, (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng 6, 383-390. (Pubitemid 23197398)
53. Whitmore L, &, Wallace BA, (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89, 392-400.
54. Frauenhofer W, &, Winter G, (2004) The use of asymmetrical flow field-flow fractionation in pharmaceutics and biopharmaceutics. Eur J Pharm Biopharm 58, 369-383. (Pubitemid 39037242)
55. Kunitani M, Dollinger G, Johnson D, &, Kresin L, (1991) On-line characterization of polyethylene glycol-modified proteins. J Chromatogr 588, 125-137.
56. Kendrick BS, Kerwin BA, Chang BS, &, Philo JS, (2001) Online size-exclusion high-performance liquid chromatography light scattering and differential refractometry methods to determine degree of polymer conjugation to proteins and protein-protein or protein-ligand association states. Anal Biochem 299, 136-146. (Pubitemid 34053402)
57. Kunitani M, &, Kresin L, (1993) High-performance liquid chromatographic analysis of carbohydrate mass composition in glycoproteins. J Chromatogr 632, 19-28. (Pubitemid 23065990)
58. Favicchio R, Dragan AI, Kneale GG, &, Read CM, (2009) Fluorescence spectroscopy and anisotropy in the analysis of DNA-protein interactions. Methods Mol Biol 543, 589-611.