Fibronectin type II-module proteins in the bovine genital tract and their putative role in cell volume control during sperm maturation
Evrim Sahin A B , Anna M. Petrunkina C F G , Mahnaz Ekhlasi-Hundrieser B , Christiane Hettel B , Dagmar Waberski A , Robin A. P. Harrison D and Edda Töpfer-Petersen E GA Clinic for Pigs and Small Ruminants, University of Veterinary Medicine Hannover, Foundation, Unit of Reproductive Medicine of the Clinics, Bünteweg 15, Hannover 30559, Germany.
B Clinic for Cattle, University of Veterinary Medicine Hannover, Foundation, Unit of Reproductive Medicine of the Clinics, Bünteweg 15, Hannover 30559, Germany.
C Clinic for Horses, University of Veterinary Medicine Hannover, Foundation, Unit of Reproductive Medicine of the Clinics, Bünteweg 15, Hannover 30559, Germany.
D 11 London Road, Great Shelford, Cambridge CB22 5DB, UK.
E Institute for Reproductive Biology, University of Veterinary Medicine Hannover, Foundation, Unit of Reproductive Medicine of the Clinics, Bünteweg 15, Hannover 30559, Germany.
F Cambridge Institute for Medical Research, University of Cambridge, Welcome Trust/MRC Building, Hills Road, Cambridge CB2 0XY, UK.
G Corresponding authors. Email: edda.toepfer-petersen@tiho-hannover.de; anna.petrunkina@gmx.de
Reproduction, Fertility and Development 21(3) 479-488 https://doi.org/10.1071/RD08209
Submitted: 30 September 2008 Accepted: 14 November 2008 Published: 4 March 2009
Abstract
The male reproductive tract of ungulates contains two protein families bearing tandemly arranged fibronectin II (Fn2) modules; one (small Fn2 proteins) bears two modules (e.g. BSP–A1/2), the other (long Fn2 proteins) bears four (e.g. epididymal sperm-binding protein 1 (ELSPBP1)). While it is well known that small Fn2 proteins are present in bull semen, nothing is known about long Fn2 proteins. In the present study, the presence of ELSPBP1 proteins in the bull epididymis and their association with maturing spermatozoa were investigated using a specific antibody against canine ELSPBP1. Analysis of western blots showed ELSPBP1 to be present in the caput, corpus and cauda regions of the epididymis. The protein, which bound phosphorylcholine (PC) strongly, appeared to associate with the spermatozoa during maturation because it was absent from caput spermatozoa but present on cauda spermatozoa. Immunocytochemistry of cauda spermatozoa showed the protein to be bound to the post-acrosomal and midpiece regions. ELSPBP1 could not be detected on freshly ejaculated spermatozoa but was revealed after a capacitating treatment. Our previous studies have shown differences between bovine caput and cauda spermatozoa in terms of their ability to control cell volume. Because of the close homology of BSP–A1/2 PC binding regions with Fn2 regions in ELSPBP1, BSP–A1/2 was used as a model to investigate the effect of a PC-binding Fn2 protein on cell volume control. While the protein had no effect on cauda spermatozoa, it caused caput spermatozoa to swell more in response to hypotonic stress, similarly to untreated cauda spermatozoa.
Acknowledgements
The funding for the present work was generously provided by the Dr H. C. Karl Eibl Foundation (Neustadt/Aisch, Germany), the Development Association for Biotechnology Research (FBF, Bonn, Germany), and the PhD Program ‘Veterinary Research and Animal Biology’ (University of Veterinary Medicine Hannover, Germany).
Barfield, J. P. , Yeung, C. H. , and Cooper, T. G. (2005). Characterization of potassium channels involved in volume regulation of human spermatozoa. Mol. Hum. Reprod. 11, 891–897.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Esch, F. S. , Ling, N. C. , Bohlen, P. , Ying, S. Y. , and Guillemin, R. (1983). Primary structure of PDC-109, a major protein constituent of bovine seminal plasma. Biochem. Biophys. Res. Commun. 113, 861–867.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Khalil, A. A. Y. , Petrunkina, A. M. , Sahin, E. , Waberski, D. , and Töpfer-Petersen, E. (2006). Enhanced binding of sperm with superior volume regulation to oviductal epithelium. J. Androl. 27, 754–765.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kulkarni, S. B. , Sauna, Z. E. , Somlata, V. , and Sitaramam, V. (1997). Volume regulation of spermatozoa by quinine-sensitive channels. Mol. Reprod. Dev. 46, 535–550.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kussmann, M. , Lassing, U. , Sturmer, C. A. , Przybylski, M. , and Roepstorff, P. (1997). Matrix-assisted laser desorption/ionization mass spectrometric peptide mapping of the neural cell adhesion protein neurolin purified by sodium dodecyl sulfate polyacrylamide gel electrophoresis or acidic precipitation. J. Mass Spectrom. 32, 483–493.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Manjunath, P. , Soubeyrand, S. , Chandonnet, L. , and Roberts, K. D. (1994). Major proteins of bovine seminal plasma inhibit phospholipase A2. Biochem. J. 303(Pt 1), 121–128.
| PubMed | CAS |
Müller, P. , Erlemann, K. R. , Müller, K. , Calvete, J. J. , Töpfer-Petersen, E. , Marienfeld, K. , and Herrmann, A. (1998). Biophysical characterization of the interaction of bovine seminal plasma protein PDC-109 with phospholipid vesicles. Eur. Biophys. J. 27, 33–41.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nauc, V. , and Manjunath, P. (2000). Radioimmunoassays for bull seminal plasma proteins (BSP–A1/–A2, BSP–A3, and BSP–30-Kilodaltons), and their quantification in seminal plasma and sperm. Biol. Reprod. 63, 1058–1066.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Nolan, J. P. , Magargee, S. F. , Posner, R. G. , and Hammerstedt, R. H. (1995). Flow cytometric analysis of transmembrane phospholipid movement in bull sperm. Biochemistry 34, 3907–3915.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Parrish, J. J. , Susko-Parrish, J. , Winer, M. A. , and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , and Töpfer-Petersen, E. (2000). Heterogeneous osmotic behaviour in boar sperm populations and its relevance for detection of changes in plasma membrane. Reprod. Fertil. Dev. 12, 297–305.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , Harrison, R. A. P. , Hebel, M. , Weitze, K. F. , and Töpfer-Petersen, E. (2001). Role of quinine-sensitive ion channels in volume regulation in boar and bull spermatozoa. Reproduction 122, 327–336.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , Harrison, R. A. P. , Ekhlasi-Hundrieser, M. , and Töpfer-Petersen, E. (2004a). Role of volume-stimulated osmolyte and anion channels in volume regulation by mammalian sperm. Mol. Hum. Reprod. 10, 815–823.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , Radcke, S. , Günzel-Apel, A. R. , Harrison, R. A. P. , and Töpfer-Petersen, E. (2004b). Role of potassium channels, the sodium-potassium pump and the cytoskeleton in the control of dog sperm volume. Theriogenology 61, 35–54.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , Gröpper, B. , Töpfer-Petersen, E. , and Günzel-Apel, A. R. (2005a). Volume regulatory function and sperm membrane dynamics as parameters for evaluating cryoprotective efficiency of a freezing extender. Theriogenology 63, 1390–1406.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , Jebe, E. , and Töpfer-Petersen, E. (2005b). Regulatory and necrotic volume increase in boar spermatozoa. J. Cell. Physiol. 204, 508–521.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petrunkina, A. M. , Harrison, R. A. P. , Tsolova, M. , Jebe, E. , and Töpfer-Petersen, E. (2007). Signalling pathways involved in the control of sperm cell volume. Reproduction 133, 61–73.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Petzoldt, R. , and Engel, S. (1994). The spermatozoal volume as indicative of the plasma membrane integrity (modification of the hypoosmotic swelling test). II. Diagnostic approach. Andrologia 26, 315–321.
| CAS | PubMed |
Ramakrishnan, M. , Anbazhagan, V. , Pratap, T. V. , Marsh, D. , and Swamy, M. J. (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.
| PubMed | CAS |
Saalmann, A. , Münz, S. , Ellerbrock, K. , Ivell, R. , and Kirchhoff, C. (2001). Novel sperm-binding proteins of epididymal origin contain four fibronectin type II-modules. Mol. Reprod. Dev. 58, 88–100.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sahin, E. , Petrunkina, A. M. , Waberski, D. , Harrison, R. A. P. , and Töpfer-Petersen, E. (2009). Control of bull sperm cell volume during epididymal maturation. Reprod. Fertil. Dev. 21, 469–478.
| Crossref | GoogleScholarGoogle Scholar |
Schäfer, B. , von Horsten, H. H. , Dacheux, J. L. , Holtz, W. , and Kirchhoff, C. (2003). Cloning and characterization of boar epididymal secretory proteins by homology to the human. Reprod. Domest. Anim. 38, 111–118.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Therien, I. , Bleau, G. , and Manjunath, P. (1995). Phosphatidylcholine-binding proteins of bovine seminal plasma modulate capacitation of spermatozoa by heparin. Biol. Reprod. 52, 1372–1379.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tillman, T. S. , and Cascio, M. (2003). Effects of membrane lipids on ion channel structure and function. Cell Biochem. Biophys. 38, 161–190.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Töpfer-Petersen, E. (1999). Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum. Reprod. Update 5, 314–329.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Töpfer-Petersen, E. , Calvete, J. J. , Sanz, L. , and Sinowatz, F. (1995). Carbohydrate- and heparin-binding proteins in mammalian fertilization. Andrologia 27, 303–324.
| PubMed |
Wah, D. A. , Fernandez-Tornero, C. , Sanz, L. , Romero, A. , and Calvete, J. J. (2002). Sperm coating mechanism from the 1.8 Å crystal structure of PDC-109-phosphorylcholine complex. Structure 10, 505–514.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Yeung, C. H. , Anapolski, M. , Sipila, P. , Wagenfeld, A. , Poutanen, M. , Huhtaniemi, I. , Nieschlag, E. , and Cooper, T. G. (2002). Sperm volume regulation: maturational changes in fertile and infertile transgenic mice and association with kinematics and tail angulation. Biol. Reprod. 67, 269–275.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Yeung, C. H. , Anapolski, M. , Depenbusch, M. , Zitzmann, M. , and Cooper, T. G. (2003). Human sperm volume regulation. Response to physiological changes in osmolality, channel blockers and potential sperm osmolytes. Hum. Reprod. 18, 1029–1036.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Yeung, C. H. , Barfield, J. P. , Anapolski, M. , and Cooper, T. G. (2004). Volume regulation of mature and immature spermatozoa in a primate model, and possible ion channels involved. Hum. Reprod. 19, 2587–2593.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Yeung, C. H. , Barfield, J. P. , and Cooper, T. G. (2005). Chloride channels in physiological volume regulation of human spermatozoa. Biol. Reprod. 73, 1057–1063.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
