Advertisement

Factors Influencing the Chaperone-Like Activity of Major Proteins of Mammalian Seminal Plasma, Equine HSP-1/2 and Bovine PDC-109: Effect of Membrane Binding, pH and Ionic Strength

  • Cheppali Sudheer Kumar
  • Bhanu Pratap Singh
  • Sk. Alim
  • Musti J. SwamyEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1112)

Abstract

HSP-1/2 and PDC-109 belong to a family of fibronectin type II proteins, present in high concentrations in bovine and equine seminal plasma, respectively. These proteins act as extracellular small heat shock proteins and protect target/client proteins against various kinds of stress. They also exhibit characteristic binding to choline phospholipids present on the sperm plasma membrane and cause efflux of choline phospholipids and cholesterol, resulting in sperm capacitation. The current study demonstrates that hypersaline conditions decrease the chaperone-like activity (CLA) of HSP-1/2. On the other hand, lipoprotein aggregates formed by the binding of choline phospholipids to this protein exhibit higher CLA than HSP-1/2 alone in vitro; the increased CLA can be correlated to the increased surface hydrophobicity of the lipoprotein aggregates. Presence of cholesterol in the membrane was found to decrease such enhancement in the CLA. We have also observed that salinity of the medium affects the chaperone activity by altering the polydisperse nature of the HSP-1/2. Together these results indicate that hydrophobicity and polydispersity are important for the chaperone-like activity of HSP-1/2 and factors that can alter these properties of HSP-1/2 can modulate its CLA. Further, studies on PDC-109 show that the chaperone-like and membrane-destabilizing activities of this protein are differentially affected by change in pH.

Keywords

Seminal plasma protein Molecular chaperone Fluorescence spectroscopy Circular dichroism Aggregation assay pH switch Capacitation Membrane destabilization Hydrophobicity 

Notes

Acknowledgements

This work was supported by a research grant from the Department of Science and Technology to MJS. CSK and BPS were supported by Senior Research Fellowships from the CSIR (India) and UGC (India), respectively. We thank Dr. G. Vinu (Lam Farm, Guntur, Andhra Pradesh) for providing samples of bovine semen and Dr. Sanjay K. Ravi (ICAR-National Research Centre on Equines, Bikaner, India) for providing samples of horse semen. Financial and infrastructural support from the University Grants Commission, New Delhi (through the UPE-II and CAS programmes), and the Department of Science and Technology, New Delhi (through the PURSE and FIST programmes), are gratefully acknowledged.

References

  1. Anbazhagan V, Swamy MJ (2005) Thermodynamics of phosphorylcholine and lysophosphatidylcholine binding to the major protein of bovine seminal plasma, PDC-109. FEBS Lett 579:2933–2938CrossRefGoogle Scholar
  2. 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 1784:891–899CrossRefGoogle Scholar
  3. Anbazhagan V, Sankhala RS, Singh BP, Swamy MJ (2011) Isothermal titration calorimetric studies on the interaction of the major bovine seminal plasma protein, PDC-109 with phospholipid membranes. PLoS One 6:e25993CrossRefGoogle Scholar
  4. Bakthisaran R, Tangirala R, Rao Ch M (2015) Small heat shock proteins: role in cellular functions and physiology. Biochim Biophys Acta 1854:291–319CrossRefGoogle Scholar
  5. Bhattacharyya M, Ray S, Bhattacharya S, Chakrabarthi A (2004) Chaperone activity and prodan binding at the self-association domain of erythroid spectrin. J Biol Chem 53:55080–55088CrossRefGoogle Scholar
  6. Calvete JJ, Mann KH, Schafer W, Sanz L, Reinert M, Nessau S, Töpfer-Petersen E (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 310:615–622CrossRefGoogle Scholar
  7. 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 8:48–56CrossRefGoogle Scholar
  8. Calvete JJ, Raida M, Gentzel M, Urbanke C, Sanz L, Töpfer-Petersen E (1997) Isolation and characterization of heparin- and phosphorylcholine-binding proteins of boar and stallion seminal plasma. Primary structure of porcine pB1. FEBS Lett 407:201–206CrossRefGoogle Scholar
  9. Damai RS, Sankhala RS, Anbazhagan V, Swamy MJ (2010) 31P-NMR and AFM studies on the cell and model membranes by the major bovine seminal plasma protein, PDC-109. IUBMB Life 62:841–851CrossRefGoogle Scholar
  10. Damai RS, Tarafdar PK, Singh BP, Reddy ST, Swamy MJ (2015) Biophysical characterization of the interaction of O-acylcholines with the major bovine seminal plasma protein, PDC-109. Adv Exp Med Biol 842:279–292CrossRefGoogle Scholar
  11. Desnoyers L, Manjunath P (1992) Major proteins of bovine seminal plasma exhibit novel interaction with phospholipids. J Biol Chem 267:10149–10155PubMedGoogle Scholar
  12. Gasset M, Saiz JL, Sanz L, Gentzel M, Töpfer-Petersen E, Calvete JJ (1997) Conformational features and thermal stability of bovine seminal plasma protein PDC-109 oligomers and phosphoryl choline bound complexes. Eur J Biochem 250:735–744CrossRefGoogle Scholar
  13. 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 374:241–247CrossRefGoogle Scholar
  14. 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 40:8326–8334CrossRefGoogle Scholar
  15. Greube A, Müller K, Töpfer-Petersen E, Herrmann A, Müller P (2004) Interaction of Fn type II proteins with membranes: the stallion seminal plasma protein SP-1/2. Biochemistry 43:464–472CrossRefGoogle Scholar
  16. Kirichok Y, Lishko PV (2011) Rediscovering sperm ion channels with patch-clamp technique. Mol Hum Reprod 17:478–499CrossRefGoogle Scholar
  17. Kumar CS, Swamy MJ (2016a) A pH switch regulates the inverse relationship between membranolytic and chaperone-like activities of HSP-1/2, a major protein of horse seminal plasma. Biochemistry 55:3650–3657CrossRefGoogle Scholar
  18. Kumar CS, Swamy MJ (2016b) HSP-1/2 a major horse seminal plasma protein, acts as a chaperone against oxidative stress. Biochem Biophys Res Commun 473:1058–1063CrossRefGoogle Scholar
  19. Kumar CS, Swamy MJ (2017a) Differential modulation of chaperone-like activity of HSP-1/2, a major protein of horse seminal plasma by anionic and cationic surfactants. Int J Biol Macromol 96:524–531CrossRefGoogle Scholar
  20. Kumar CS, Swamy MJ (2017b) Modulation of chaperone-like and membranolytic activities of major horse seminal plasma protein, HSP-1/2 by L-carnitine. J Biosci 42:469–479CrossRefGoogle Scholar
  21. Kumar CS, Sivaramakrishna D, Ravi SK, Swamy MJ (2016) Fluorescence investigations on choline phospholipid binding and chemical unfolding of HSP-1/2, a major protein of horse seminal plasma. J Photochem Photobiol B Biol 158:89–98CrossRefGoogle Scholar
  22. Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16:659–671CrossRefGoogle Scholar
  23. Leemans B, Gadella BM, Sostaric E, Neils H, Stout TA, Hoogewijis M, Van Soom A (2014) Oviduct binding and elevated pH induce protein tyrosine phosphorylation in stallion spermatozoa. Biol Reprod 91(13):1–12Google Scholar
  24. Liang JN, Li XY (1991) Interaction and aggregation of lens crystallins. Exp Eye Res 53:61–66CrossRefGoogle Scholar
  25. Manjunath P, Thérein I (2002) Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 53:109–119CrossRefGoogle Scholar
  26. Marsh D, Horváth LI, Swamy MJ, Mantripragada S, Kleinschmidt JH (2002) Interaction of membrane-spanning proteins with peripheral and lipid-anchored membrane proteins: perspectives from protein-lipid interactions. Mol Membr Biol 19:247–255CrossRefGoogle Scholar
  27. McPartlin LA, Suarez SS, Czaya CA, Hinrichs K, Bedford-Guaus SJ (2009) Hyper activation of stallion sperm is required for the successful in vitro fertilization of equine oocytes. Biol Reprod 81:199–206CrossRefGoogle Scholar
  28. Moparthi SB, Fristedt R, Mishra R, Almstedt K, Karlsson M, Hammarstrom P, Carlsson U (2010) Chaperone activity of Cyp18 through hydrophobic condensation that enables rescue of transient misfolded molten globule intermediates. Biochemistry 49:1137–1145CrossRefGoogle Scholar
  29. Plante G, Prud’homme B, Fan J, Lafleur M, Manjunath P (2016) Evolution and function of mammalian binder of sperm proteins. Cell Tissue Res 363:105–127CrossRefGoogle Scholar
  30. 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 81:2215–2225CrossRefGoogle Scholar
  31. Sankhala RS, Swamy MJ (2010) The major protein of bovine seminal plasma, PDC-109 is a molecular chaperone. Biochemistry 49:3908–3918CrossRefGoogle Scholar
  32. 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:e17330CrossRefGoogle Scholar
  33. Sankhala RS, Kumar CS, Singh BP, Arangasamy A, Swamy MJ (2012) HSP-1/2, a major protein of equine seminal plasma, exhibits chaperone-like activity. Biochem Biophys Res Commun 427:18–23CrossRefGoogle Scholar
  34. Scolari S, Müller K, Bittman R, Hermann A, Müller P (2010) Interaction of mammalian seminal plasma protein, PDC-109 with cholesterol: implications for a putative CRAC domain. Biochemistry 49:9027–9031CrossRefGoogle Scholar
  35. Sheluho D, Ackerman SH (2001) An accessible hydrophobic surface is a key element of molecular chaperone action of Atp11p. J Biol Chem 276(43):39945–39949Google Scholar
  36. Swamy MJ (2004) Interaction of bovine seminal plasma proteins with model membranes and sperm plasma membranes. Curr Sci 87:203–211Google Scholar
  37. 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 528:230–234CrossRefGoogle Scholar
  38. Thomas CJ, Anbazhagan V, Ramakrishnan M, Sultan N, Surolia I, Swamy MJ (2003) Mechanism of membrane binding by the bovine seminal plasma protein, PDC-109. A surface plasmon resonance study. Biophys J 84:3037–3044CrossRefGoogle Scholar
  39. Voellmy R, Boellmann F (2007) Chaperone regulation of heat shock protein response. Adv Exp Med Biol 594:88–99Google Scholar
  40. Wah DA, Tornero CF, Sanz L, Romero A, Calvete JJ (2002) Sperm coating mechanism from the 1.8 Å crystal structure of PDC-109-phosphorylcholine complex. Structure 10:505–514CrossRefGoogle Scholar
  41. Welker S, Rudolph B, Frenzel E, Hagn F, Liebisch G, Schmitz G, Scheuring J, Kerth A, Blume A, Weinkauf S, Haslback M (2010) Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol Cell 39:507–552CrossRefGoogle Scholar
  42. Whited AM, Johs A (2015) The interactions of peripheral membrane proteins with biological membranes. Chem Phys Lipids 192:51–59CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Cheppali Sudheer Kumar
    • 1
  • Bhanu Pratap Singh
    • 2
  • Sk. Alim
    • 2
  • Musti J. Swamy
    • 2
    Email author
  1. 1.State Key Laboratory of Biomembrane and Membrane biotechnology, School of LifesciencesTsinghua UniversityBeijingChina
  2. 2.School of ChemistryUniversity of HyderabadHyderabadIndia

Personalised recommendations