Isothermal titration calorimetric studies on the interaction of the major bovine seminal plasma protein, PDC-109 with phospholipid membranes

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Anbazhagan, V ^a   Sankhala, Rajeshwer S ^a   Singh, Bhanu Pratap ^a   Swamy, Musti J ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; DIACYLPHOSPHOLIPID; DIMYRISTOYLPHOSPHATIDYLCHOLINE; LYSOPHOSPHATIDYLCHOLINE; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID; SEMINAL PLASMA PROTEIN; SEMINAL PLASMA PROTEIN PDC 109; UNCLASSIFIED DRUG; LIPOSOME; PHOSPHATIDYLGLYCEROL; SEMINAL VESICLE SECRETORY PROTEIN; SEMINAL VESICLE SECRETORY PROTEIN 109, BOS TAURUS;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENTHALPY; ENTROPY; HYDROPHOBICITY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PH; PHOSPHOLIPID MEMBRANE; PROTEIN BINDING; PROTEIN LIPID INTERACTION; TEMPERATURE; THERMODYNAMICS; WATER STRUCTURE; ANIMAL; ARTIFICIAL MEMBRANE; CALORIMETRY; CATTLE; MALE; METABOLISM; METHODOLOGY; MICELLE; SOLUBILITY; TITRIMETRY;

BOVINAE;

ANIMALS; CALORIMETRY; CATTLE; CHOLESTEROL; DIMYRISTOYLPHOSPHATIDYLCHOLINE; ENTROPY; HYDROGEN-ION CONCENTRATION; LYSOPHOSPHATIDYLCHOLINES; MALE; MEMBRANES, ARTIFICIAL; MICELLES; PHOSPHATIDYLGLYCEROLS; PHOSPHOLIPIDS; PROTEIN BINDING; SEMINAL VESICLE SECRETORY PROTEINS; SOLUBILITY; TITRIMETRY; UNILAMELLAR LIPOSOMES;

EID: 80054715587     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025993     Document Type: Article

References (58)

1. Shivaji S, Scheit KH, Bhargava PM, (1990) Proteins of seminal plasma New York Wiley.
2. Yanagimachi R, (1994) Mammalian fertilization. In: Knobil E, Neill JD, editors. The Physiology of Reproduction New York Raven Press pp. 189-317.
3. Harrison RAP, (1996) Capacitation mechanisms, and the role of capacitation as seen in eutherian mammals. Reprod Fert Dev 8: 581-594.
4. Visconti PE, Calantino-Hormer H, Moore GD, Bailey JL, Ning X, et al. (1998) The molecular basis of sperm capacitation. J Androl 19: 242-248.
5. Manjunath P, Sairam MR, Uma J, (1987) Purification of four gelatin-binding proteins from bovine seminal plasma by affinity chromatography. Biosci Rep 7: 231-238.
6. Manjunath P, Sairam MR, (1987) Purification and biochemical characterization of three major acidic proteins (BSP-A1, BSP-A2 and BSP-A3) from bovine seminal plasma. Biochem J 241: 685-692.
7. Calvete JJ, Mann K, Schafer W, Sanz L, Reinert M, et al. (1995) Amino acid sequence of HSP-1, a major protein of stallion seminal plasma: effect of glycosylation on its heparin- and gelatin-binding capabilities. Biochem J 310: 615-622.
8. Calvete JJ, Raida M, Gentzel M, Urbanke C, Sanz L, et al. (1997) Isolation and characterization of heparin and phosphorylcholine binding proteins of boar and stallion seminal plasma. Primary structure of porcine pB1. FEBS Lett 407: 201-206.
9. Villemure M, Lazure C, Manjunath P, (2003) Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reprod Biol Endocrinol 1: 39-48.
10. Boisvert M, Bergeron A, Lazure C, Manjunath P, (2004) Isolation and characterization of gelatin-binding bison seminal vesicle secretory proteins. Biol Reprod 70: 656-661.
11. Bergeron A, Villemure M, Lazure C, Manjunath P, (2005) Isolation and characterization of the major proteins of ram seminal plasma. Mol Reprod Dev 71: 461-470.
12. Harper MJK, (1994) Gamete and Zygote Transport. In: Knobil E, Neill JD, editors. The Physiology of Reproduction Raven Press: New York pp. 123-187.
13. Suarez SS, (1998) The oviductal sperm reservoir in mammals. Mechanisms of formation. Biol Reprod 58: 1105-1107.
14. Scheit KH, Kemme M, Aumüller G, Seitz J, Hagendorff G, et al. (1988) The major protein of bull seminal plasma: biosynthesis and biological function. Biosci Rep 8: 589-608.
15. Baker ME, (1985) The PDC-109 protein from bovine seminal plasma is similar to the gelatin-binding domain of bovine fibronectin and a kringle domain of human tissue-type plasminogen activator. Biochem Biophys Res Commun 130: 1010-1014.
16. Esch FS, Ling NC, Bohlen P, Ying SY, Guillemin R, (1983) Primary structure of PDC-109, a major protein constituent of bovine seminal plasma. Biochem Biophys Res Commun 113: 861-867.
17. Seidah NG, Manjunath P, Rochemont J, Sairam MR, Cheretian M, (1987) Complete amino acid sequence of BSP-A3 from bovine seminal plasma, Homology to PDC-109 and to the collagen-binding domain of fibronectin. Biochem J 243: 195-203.
18. Calvete JJ, Raida M, Sanz L, Wempe F, Scheit KH, et al. (1994) Localization and structural characterization of an oligosaccharide O-linked to bovine PDC-109. Quantitation of the glycoprotein in seminal plasma and on the surface of ejaculated and capacitated spermatozoa. FEBS Lett 350: 203-206.
19. Desnoyers L, Manjunath P, (1992) Major proteins of bovine seminal plasma exhibit novel interactions with phospholipids. J Biol Chem 267: 10149-10155.
20. Thérien I, Moreau R, Manjunath P, (1998) Major proteins of bovine seminal plasma and high-density lipoprotein induce cholesterol efflux from epididymal sperm. Biol Reprod 59: 768-776.
21. Moreau R, Thérien I, Lazure C, Manjunath P, (1998) Type II domains of BSP-A1/-A2 proteins: binding properties, lipid efflux and sperm capacitation potential. Biochem Biophys Res Commun 246: 148-154.
22. Wah DA, Fernández-Tornero C, Sanz L, Romero A, Calvete JJ, (2002) Sperm coating mechanism from the 1.8 Å crystal structure of PDC-109-phosphorylcholine complex. Structure 10: 505-514.
23. Ramakrishnan M, Anbazhagan V, Pratap TV, Marsh D, Swamy MJ, (2001) Membrane insertion and lipid-protein interactions of bovine seminal plasma protein, PDC-109 investigated by spin label electron spin resonance spectroscopy. Biophys J 81: 2215-2225.
24. Swamy MJ, Marsh D, Anbazhagan V, Ramakrishnan M, (2002) Effect of cholesterol on the interaction of seminal plasma protein, PDC-109 with phosphatidylcholine membranes. FEBS Lett 528: 230-234.
25. Thomas CJ, Anbazhagan V, Ramakrishnan M, Sultan N, Surolia I, et al. (2003) Mechanism of membrane binding by the bovine seminal plasma protein, PDC-109. A surface plasmon resonance study. Biophys J 84: 3037-3044.
26. Greube A, Müller K, Töpfer-Petersen E, Herrmann A, Müller P, (2001) Influence of the bovine seminal plasma protein PDC-109 on the physical state of membrane. Biochemistry 40: 8326-8334.
27. Anbazhagan V, Damai RS, Paul A, Swamy MJ, (2008) Interaction of the major protein from bovine seminal plasma, PDC-109 with phospholipid membranes and soluble ligands investigated by fluorescence approaches. Biochim Biophys Acta 1784: 891-899.
28. Revah I, Gadella BM, Flesch FM, Colenbrander B, Suarez SS, (2000) Physiological state of bull sperm affects fucose- and mannose-binding properties. Biol Reprod 62: 1010-1015.
29. Ignotz GG, Lo MC, Perez CL, Gwathmey TM, Suarez SS, (2001) Characterization of a fucose-binding protein from bull sperm and seminal plasma that may be responsible for formation of oviductal sperm reservoir. Biol Reprod 64: 1806-1811.
30. Chandonnet L, Roberts KD, Chapdelaine A, Manjunath P, (1990) Identification of heparin-binding proteins in bovine seminal plasma. Mol Reprod Dev 26: 313-318.
31. Liberda J, Kraus M, Ryslava H, Vlaskova M, Jonakova V, et al. (2001) D-Fructose-binding proteins in bull seminal plasma. Isolation and characterization. Folia Biol (Praha) 47: 113-119.
32. Manjunath P, Marcel YL, Uma J, Seidah NG, Cheretian M, et al. (1989) Apolipoprotein A-1 binds to a family of bovine seminal plasma proteins. J Biol Chem 264: 16853-16857.
33. Manjunath P, Nauc V, Bergeron A, Menard M, (2002) Major proteins of bovine seminal plasma bind to the low density lipoprotein fraction of hen's egg yolk. Biol Reprod 67: 1250-1258.
34. Sankhala RS, Swamy MJ, (2010) The major protein of bovine seminal plasma, PDC-109, is a molecular chaperone. Biochemistry 49: 3908-3918.
35. Sankhala RS, Damai RS, Swamy MJ, (2011) Correlation of membrane binding and hydrophobicity to the chaperone-like activity of PDC-109, the major protein of bovine seminal plasma. PLoS ONE 6: e17330.
36. Anbazhagan V, Swamy MJ, (2005) Thermodynamics of phosphorylcholine and lysophosphatidylcholine binding to the major protein of bovine seminal plasma, PDC-109. FEBS Lett 579: 2933-2938.
37. Swamy MJ, (2004) Interaction of bovine seminal plasma proteins with model membranes and sperm plasma membranes. Curr Sci 87: 203-211.
38. Lassiseraye D, Courtemanche L, Bergeron A, Manjunath P, Lafleur M, (2008) Binding of bovine seminal plasma protein BSP-A1/A2 to model membranes: Lipid specificity and effect of the temperature. Biochim Biophys Acta 1778: 502-513.
39. Calvete JJ, Paloma FV, Sanz L, Romero A, (1996) A procedure for the large-scale isolation of major bovine seminal plasma proteins. Protein Expr Purif 8: 48-56.
40. Laemmli UK, (1970) Cleavage of structural proteins during assembly of bacteriophage T4. Nature 227: 680-685.
41. Wiseman T, Williston S, Brandts JF, Lin L-N, (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179: 131-137.
42. ITC Data Analysis in Origin® (1998) Tutorial Guide Version 5.0.
43. Wieprecht T, Beyermann M, Seelig J, (1999) Binding of antibacterial magainin peptides to electrically neutral membranes: Thermodynamics and structure. Biochemistry 38: 10377-10387.
44. Arnulphi C, Jin L, Tricerri MA, Jonas A, (2004) Enthalpy-driven apolipoprotein A-I and lipid bilayer interaction indicating protein penetration upon binding. Biochemisry 43: 12258-12264.
45. Torrecillas A, Laynez J, Menéndez M, Corbálan-García S, Gomez-Fernández JC, (2004) Calorimetric study of the interaction of the C2 domains of classical protein kinase C isoenzymes with Ca2+ and phospholipids. Biochemistry 43: 11727-11739.
46. Abraham T, Lewis RNAH, Hodges RS, McElhaney RN, (2005) Isothermal titration calorimetry studies of the binding of a rationally designed analogue of the antimicrobial peptide gramicidin S to phospholipids bilayer membranes. Biochemistry 44: 2103-2112.
47. Gasset M, Magdaleno L, Calvete JJ, (2000) Biophysical study of the perturbation of model membrane structure caused by seminal plasma protein PDC-109. Arch Biochem Biophys 374: 241-247.
48. Zhang W, Krishnan N, Becker DF, (2006) Kinetic and thermodynamic analysis of Bradyrhizobium japonicum PutA-membrane associations. Arch Biochem Biophys 445: 174-183.
49. Lin M-S, Chiu H-M, Fan F-J, Tsai H-T, Wang SS-S, et al. (2007) Kinetics and enthalpy measurements of interaction between β-amyloid and liposomes by surface plasmon resonance and isothermal titration calorimetry. Colloids Surf B 58: 231-236.
50. Scolari S, Müller K, Bittman R, Herrmann A, Müller P, (2010) Interaction of mammalian seminal plasma protein PDC-109 with cholesterol: implications for a putative CRAC domain. Biochemistry 49: 9027-9031.
51. Epand RM, (2006) Cholesterol and the interaction of proteins with membrane domains. Prog Lipid Res 45: 279-294.
52. Sigurskjold BW, Bundle DR, (1992) Thermodynamics of oligosaccharide binding to a monoclonal antibody specific for a Salmonella O-antigen point to hydrophobic interactions in the binding site. J Biol Chem 267: 8371-8376.
53. Sultan NAM, Swamy MJ, (2005) Energetics of carbohydrate binding to Momordica charantia (bitter gourd) lectin: An isothermal titration calorimetric study. Arch Biochem Biophys 437: 115-125.
54. Brummell DA, Sharma VP, Anand NN, Bilous D, Dubuc G, et al. (1993) Probing the combining site of an anti-carbohydrate antibody by saturation-mutagenesis: Role of the heavy-chain CDR3 residues. Biochemistry 32: 1180-1187.
55. Swamy MJ, Ramakrishnan M, Angerstein B, Marsh D, (2000) Spin-label electron spin resonance studies on the mode of anchoring and vertical location of the N-acyl chain in N-acylphosphatidylethanolamines. Biochemistry 39: 12476-12484.
56. Marsh D, (1990) CRC handbook of Lipid Bilayers: CRC press: Boca Raton, FL.
57. Gasset M, Saiz JL, Sanz L, Gentzel M, Töpfer-Petersen E, et al. (1997) Conformational features and thermal stability of bovine seminal plasma protein PDC-109 oligomers and phosphorylcholine-bound complexes. Eur J Biochem 250: 735-744.
58. Cabra V, Arreguin R, Vazquez-Duhalt R, Farres A, (2006) Effect of temperature and pH on the secondary structure and processes of oligomerization of 19 kDa alpha-zein. Biochim Biophy Acta 1764: 1110-1118.