Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Thiols of flagellar proteins are essential for progressive motility in human spermatozoa

María Eugenia Cabrillana A B , María de los Ángeles Monclus A B , Tania Estefania Sáez Lancellotti A B , Paola Vanina Boarelli A B , Amanda Edith Vincenti A , Miguel Matias Fornés C , Eduardo Alfredo Sanabria D and Miguel Walter Fornés A B E
+ Author Affiliations
- Author Affiliations

A Andrologic Research Laboratory of Mendoza (LIAM), Histology and Embryology Institute of Mendoza (IHEM), Histology and Embryology Area, Department of Morphology and Physiology, School of Medicine, National University of Cuyo and CCT-Mendoza, CONICET, Mendoza, Argentina.

B Research Institute, School of Medicine, University of Aconcagua, Mendoza, Argentina.

C Engineering School, University of Cuyo, Mendoza, Argentina.

D Basic Science Institute, Facultad de Ciencias Exactas, Físicas y Naturales, Av. Ignacio de la Roza 590 (O), Complejo Universitario “Islas Malvinas”, Rivadavia, National University of San Juan and CCT-CONICET, San Juan, Argentina.

E Corresponding author. Email: mfornes@fcm.uncu.edu.ar

Reproduction, Fertility and Development 29(7) 1435-1446 https://doi.org/10.1071/RD16225
Submitted: 27 November 2015  Accepted: 4 June 2016   Published: 1 July 2016

Abstract

Male infertility is a disorder of the reproductive system defined by the failure to achieve a clinical pregnancy after 12 months or more of regular unprotected sexual intercourse. The presence of low-motile or immotile spermatozoa is one of many causes of infertility; however, this observation provides little or no information regarding the pathogenesis of the malfunction. Good sperm motility depends on correct assembly of the sperm tail in the testis and efficient maturation during epididymal transit. Thiols of flagellar proteins, such as outer dense fibre protein 1 (ODF1), are oxidised to form disulfides during epididymal transit and the spermatozoa become motile. This study was designed to determine how oxidative changes in protein thiol status affect progressive motility in human spermatozoa. Monobromobimane (mBBr) was used as a specific thiol marker and disruptor of sperm progressive motility. When mBBr was blocked by dithiothreitol it did not promote motility changes. The analysis of mBBr-treated spermatozoa revealed a reduction of progressive motility and an increased number of spermatozoa with non-progressive motility without affecting ATP production. Laser confocal microscopy and western blot analysis showed that one of the mBBr-positive proteins reacted with an antibody to ODF1. Monobromobimane fluorescence intensity of the sperm tail was lower in normozoospermic than asthenozoospermic men, suggesting that thiol oxidation in spermatozoa of asthenozoospermic men is incomplete. Our findings indicate that mBBr affects the thiol status of ODF1 in human spermatozoa and interferes with progressive motility.

Additional keywords: cytoskeleton, epididymus, fertility.


References

Aleem, M., Padwal, V., Choudhari, J., Balasinor, N., and Gill-Sharma, M. K. (2008). Sperm protamine levels as indicators of fertilising potential in sexually mature male rats. Andrologia 40, 29–37.
Sperm protamine levels as indicators of fertilising potential in sexually mature male rats.CrossRef | 1:CAS:528:DC%2BD1cXivVOlu7o%3D&md5=93c6d120e2e2d00f35731d806321a8caCAS | 18211299PubMed | open url image1

Baltz, J. M., Williams, P. O., and Cone, R. A. (1990). Dense fibers protect mammalian sperm against damage. Biol. Reprod. 43, 485–491.
Dense fibers protect mammalian sperm against damage.CrossRef | 1:STN:280:DyaK3M7gsFagsw%3D%3D&md5=8bf5658ee36e00e7bf301a5ba48e59eeCAS | 2271730PubMed | open url image1

Bedford, J. M., Calvin, H., and Cooper, G. W. (1973). The maturation of spermatozoa in the human epididymis. J. Reprod. Fertil. Suppl. 18, 199–213.
| 1:STN:280:DyaE3s3ktlCntQ%3D%3D&md5=c0a70bb87a8fb9909259775c30f96e16CAS | 4516681PubMed | open url image1

Cabrillana, M. E., Monclus, M. A., Saez Lanzelotti, T. E., Boarelli, P. V., Clementi, M. A., Vincenti, A. E., Yunes, R. M. F., and Fornés, M. W. (2011). Characterization of flagellar cysteine-rich sperm proteins, involved in motility, by the combination of cellular fractionation, fluorescence detection and mass spectrometry analysis. Cytoskeleton 68, 491–500.
Characterization of flagellar cysteine-rich sperm proteins, involved in motility, by the combination of cellular fractionation, fluorescence detection and mass spectrometry analysis.CrossRef | 1:CAS:528:DC%2BC3MXhtFyjs73O&md5=51be2591e81c793d3979122eba91c666CAS | 21780308PubMed | open url image1

Cleland, W. W. (1964). Dithiothreitol, a new protective reagent for SH groups. Biochemistry 3, 480–482.
Dithiothreitol, a new protective reagent for SH groups.CrossRef | 1:CAS:528:DyaF2cXmvFCqsw%3D%3D&md5=12293786a8c957f98ca35cd760183a05CAS | 14192894PubMed | open url image1

Cooper, T. G. (2011). The epididymis, cytoplasmic droplets and male fertility. Asian J. Androl. 13, 130–138.
The epididymis, cytoplasmic droplets and male fertility.CrossRef | 21076437PubMed | open url image1

Cornwall, G. A., and Chang, T. S. K. (1990). Characterization of sulphydryl proteins involved in the maintenance of flagellar straightness in hamster spermatozoa. J. Androl. 11, 168–181.
Characterization of sulphydryl proteins involved in the maintenance of flagellar straightness in hamster spermatozoa.CrossRef | 1:CAS:528:DyaK3cXktVektb4%3D&md5=184e0246419b5595a2e4d1799149f33aCAS | 2324004PubMed | open url image1

Cornwall, G. A., Vindivich, D., Tillman, S., and Chang, T. S. (1988). The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro. Biol. Reprod. 39, 141–155.
The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro.CrossRef | 1:CAS:528:DyaL1cXkvFSntr4%3D&md5=4c1df1845a7a765d40140e3e2a0ca0efCAS | 3207793PubMed | open url image1

de Mateo, S., Ramos, L., van der Vlag, J., de Boer, P., and Oliva, R. (2011). Improvement in chromatin maturity of human spermatozoa selected through density gradient centrifugation. Int. J. Androl. 34, 256–267.
Improvement in chromatin maturity of human spermatozoa selected through density gradient centrifugation.CrossRef | 1:STN:280:DC%2BC3Mvos1Cjtw%3D%3D&md5=b8e0ccc69f013880d595b50c35645a31CAS | 20569271PubMed | open url image1

Dias, G. M., López, M. L., Ferreira, A. T. S., Chapeaurouge, D. A., Rodrigues, A., Perales, J., and Retamal, C. A. (2014). Thiol-disulfide proteins of stallion epididymal spermatozoa. Anim. Reprod. Sci. 145, 29–39.
Thiol-disulfide proteins of stallion epididymal spermatozoa.CrossRef | 1:CAS:528:DC%2BC2cXhtlGks7o%3D&md5=721fd4c61e5cc005d6157ed2436a9614CAS | 24418125PubMed | open url image1

Ferguson, K. A. (1964). Starch-gel electrophoresis – application to the classification of pituitary proteins and polypeptides. Metabolism 13, 985–1002.
Starch-gel electrophoresis – application to the classification of pituitary proteins and polypeptides.CrossRef | 1:CAS:528:DyaF2MXjvVegsA%3D%3D&md5=f264572e9d1beb4acf19c9a1eeb63d74CAS | 14228777PubMed | open url image1

Gastmann, O., Burfeind, P., Günther, E., Hameister, H., Szpirer, C., and Hoyer-Fender, S. (1993). Sequence, expression and chromosomal assignment of a human sperm outer dense fiber gene. Mol. Reprod. Dev. 36, 407–418.
Sequence, expression and chromosomal assignment of a human sperm outer dense fiber gene.CrossRef | 1:CAS:528:DyaK2cXlvFOisrc%3D&md5=760cbd8a81377c6bc7039fb0b72f0113CAS | 8305202PubMed | open url image1

Haidl, G., Becker, A., and Henkel, R. (1991). Poor development of outer dense fibers as a major cause of tail abnormalities in the spermatozoa of asthenoteratozoospermic men. Hum. Reprod. 6, 1431–1438.
| 1:STN:280:DyaK387itFeqtw%3D%3D&md5=6d92fc531904a9f2ab036dcc98f4ad9dCAS | 1770140PubMed | open url image1

Harper, S., and Speicher, D. W. (2001). Detection of proteins on blot membranes. In ‘Current Protocols in Protein Science’. pp. 10.8.1–10.8.7. (John Wiley & Sons, Inc.)

Hofferbert, S., Burfeind, P., Hoyer-Fender, S., Lange, R., Haidl, G., and Engel, W. (1993). A homozygous deletion of 27 base pairs in the coding region of the human outer dense fiber protein gene does not result in a pathologic phenotype. Hum. Mol. Genet. 2, 2167–2170.
A homozygous deletion of 27 base pairs in the coding region of the human outer dense fiber protein gene does not result in a pathologic phenotype.CrossRef | 1:CAS:528:DyaK2cXktVKmt78%3D&md5=0b045903a80f70f8fa42fdac6fd369ffCAS | 8111388PubMed | open url image1

Ijiri, T. W., Vadnais, M. L., Huang, A. P., Lin, A. M., Levin, L. R., Buck, J., and Gerton, G. L. (2014). Thiol changes during epididymal maturation: a link to flagellar angulation in mouse spermatozoa? Andrology 2, 65–75.
Thiol changes during epididymal maturation: a link to flagellar angulation in mouse spermatozoa?CrossRef | 1:CAS:528:DC%2BC3sXitVSqtL7N&md5=4f7e926a661cca1383f07f2f0af55844CAS | 24254994PubMed | open url image1

Jeyendran, R. S., Van der Ven, H. H., Perez-Pelaez, M., Crabo, B. G., and Zaneveld, L. J. (1984). Development of an essay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. J. Reprod. Fertil. 70, 219–228.
Development of an essay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics.CrossRef | 1:STN:280:DyaL2c7hsVKntA%3D%3D&md5=b69a64c95a94f522ce31b1dd60a28836CAS | 6694140PubMed | open url image1

Kierszenbaum, A. L. (2002). Keratins: unraveling the coordinated construction of scaffolds in spermatogenic cells. Mol. Reprod. Dev. 61, 1–2.
Keratins: unraveling the coordinated construction of scaffolds in spermatogenic cells.CrossRef | 1:CAS:528:DC%2BD3MXptVejtb0%3D&md5=63cd7cbdb18faacfdc844859b43f6a73CAS | 11774369PubMed | open url image1

Kierszenbaum, A. L., and Tres, L. L. (2004). The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch. Histol. Cytol. 67, 271–284.
The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head.CrossRef | 1:CAS:528:DC%2BD2MXhslKrs7k%3D&md5=e0f3d41e3c2e2e914ed0f527315bdc40CAS | 15700535PubMed | open url image1

Kosower, N. S., and Kosower, E. M. (1987). Thiol labeling with bromobimanes. Methods Enzymol. 143, 76–84.
Thiol labeling with bromobimanes.CrossRef | 1:CAS:528:DyaL1cXjsVemtg%3D%3D&md5=11eb24a01440332f1191b5114c1af5aeCAS | 3657564PubMed | open url image1

Kosower, N. S., Kosower, E. M., Newton, G. L., and Ranney, H. M. (1979). Bimane fluorescent labels: labeling of normal human red cells under physiological conditions. Proc. Natl. Acad. Sci. USA 76, 3382–3386.
Bimane fluorescent labels: labeling of normal human red cells under physiological conditions.CrossRef | 1:CAS:528:DyaE1MXltlKnurg%3D&md5=10959687b2e8514f1b186552da9c1551CAS | 291011PubMed | open url image1

Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of the bacteriophage T4.CrossRef | 1:CAS:528:DC%2BD3MXlsFags7s%3D&md5=eaef889ef44ef5add96fde2f9929889fCAS | 5432063PubMed | open url image1

Lindemann, C. B. (1996). Functional significance of the outer dense fibers of mammalian sperm examined by computer simulation with the geometric clutch model. Cell Motil. Cytoskeleton 34, 258–270.
Functional significance of the outer dense fibers of mammalian sperm examined by computer simulation with the geometric clutch model.CrossRef | 1:STN:280:DyaK2s%2FisFKgtg%3D%3D&md5=0f3339a0a8f11330a0d2af7d4c7f34ffCAS | 8871813PubMed | open url image1

Lishko, P. V., Botchkina, I. L., Fedorenko, A., and Kirichok, Y. (2010). Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell 140, 327–337.
Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel.CrossRef | 1:CAS:528:DC%2BC3cXlt1Klsb4%3D&md5=4188965aad50d29aaabee31a29b3a937CAS | 20144758PubMed | open url image1

Meijering, E., Dzyubachyk, O., and Smal, I. (2012). Methods for cell and particle tracking in imaging and spectroscopic analysis of living cells. Methods Enzymol. 504, 183–200.
Methods for cell and particle tracking in imaging and spectroscopic analysis of living cells.CrossRef | 22264535PubMed | open url image1

Menkveld, R., Stander, F. S. H., Kotze, T., Jv, W., Kruger, T. F., and van Zyl, J. A. (1990). The evaluation of morphological characteristics of human spermatozoa according to stricter criteria. Hum. Reprod. 5, 586–592.
| 1:STN:280:DyaK3czmvV2jug%3D%3D&md5=22e433038eecf21803962a07f637c8c0CAS | 2394790PubMed | open url image1

Mortimer, D. (1994). Sperm recovery techniques to maximize fertilizing capacity. Reprod. Fertil. Dev. 6, 25–31.
Sperm recovery techniques to maximize fertilizing capacity.CrossRef | 1:STN:280:DyaK2czksFWgsw%3D%3D&md5=3545529adaebd8d6b972fa6222c86304CAS | 8066218PubMed | open url image1

Mukai, C., and Okuno, M. (2004). Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol. Reprod. 71, 540–547.
Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement.CrossRef | 1:CAS:528:DC%2BD2cXmtFWgur4%3D&md5=4f557c41f0f5d02a67d9bb84f9b8dcfaCAS | 15084484PubMed | open url image1

Nascimento, J. M., Shi, L. Z., Tam, J., Chandsawangbhuwana, C., Durrant, B., Botvinick, E. L., and Berns, M. W. (2008). Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J. Cell. Physiol. 217, 745–751.
Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping.CrossRef | 1:CAS:528:DC%2BD1cXhtlOqt7rJ&md5=e35111644ec98bdc6382305333bb0949CAS | 18683212PubMed | open url image1

Oko, R. (1988). Comparative analysis of proteins from the fibrous sheath and outer dense fibers of rat spermatozoa. Biol. Reprod. 39, 169–182.
Comparative analysis of proteins from the fibrous sheath and outer dense fibers of rat spermatozoa.CrossRef | 1:CAS:528:DyaL1cXkvFSitb4%3D&md5=4d0e534aed570e32ff292bf7e6713e57CAS | 3207795PubMed | open url image1

Oko, R., and Clermont, Y. (1989). Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat. Rec. 225, 46–55.
| 1:STN:280:DyaL1Mznt1ahsQ%3D%3D&md5=df15101b77e44bf81c33033b3ad774eeCAS | 2476045PubMed | open url image1

Olson, G. E., and Sammons, D. W. (1980). Structural chemistry of outer dense fibers of rat sperm. Biol. Reprod. 22, 319–332.
Structural chemistry of outer dense fibers of rat sperm.CrossRef | 1:CAS:528:DyaL3cXhslOqs7g%3D&md5=bad8fa49b853bda8579631b713e72995CAS | 7378538PubMed | open url image1

Petersen, C., Füzesi, L., and Hoyer-Fender, S. (1999). Outer dense fiber proteins from human sperm tail: molecular cloning and expression analyses of two cDNA transcripts encoding proteins of approximately 70 kDa. Mol. Hum. Reprod. 5, 627–635.
Outer dense fiber proteins from human sperm tail: molecular cloning and expression analyses of two cDNA transcripts encoding proteins of approximately 70 kDa.CrossRef | 1:CAS:528:DyaK1MXltVOit78%3D&md5=6a82ea262a37ea7d3cf28e412c4bcfc5CAS | 10381817PubMed | open url image1

Petrotchenko, E. V., Pasek, D., Elms, P., Dokholyan, M. V., Maissner, G., and Borchers, C. H. (2006). Combining fluorescence detection and mass spectrometric analysis for comprehensive and quantitative analysis of redox-sensitive cysteine in native membrane proteins. Anal. Chem. 78, 7959–7966.
Combining fluorescence detection and mass spectrometric analysis for comprehensive and quantitative analysis of redox-sensitive cysteine in native membrane proteins.CrossRef | 1:CAS:528:DC%2BD28XhtVGmsbzN&md5=dbe4e2bbffe5c56599e4b47737b0831bCAS | 17134128PubMed | open url image1

Ramos, L., van der Heijden, G. W., Derijck, A., Berden, J. H., Kremer, J. A., van der Vlag, J., and de Boer, P. (2008). Incomplete nuclear transformation of human spermatozoa in oligo-astheno-teratospermia: characterization by indirect immunofluorescence of chromatin and thiol status. Hum. Reprod. 23, 259–270.
Incomplete nuclear transformation of human spermatozoa in oligo-astheno-teratospermia: characterization by indirect immunofluorescence of chromatin and thiol status.CrossRef | 1:CAS:528:DC%2BD1cXptlCkug%3D%3D&md5=bb4a5a1bcc02e2d29998be2e1f43375dCAS | 18056059PubMed | open url image1

Schalles, U., Shao, X., van der Hoorn, F. A., Oko, R., Petersen, C., Füzesi, L., and Hoyer-Fender, S. (1998). Developmental expression of the 84-kDa ODF sperm protein: localization to both the cortex and medulla of outer dense fibers and to the connecting piece. Dev. Biol. 199, 250–260.
Developmental expression of the 84-kDa ODF sperm protein: localization to both the cortex and medulla of outer dense fibers and to the connecting piece.CrossRef | 1:CAS:528:DyaK1cXltFyntbg%3D&md5=c32c9972de2a6bbed1faaec2687aa5ffCAS | 9698445PubMed | open url image1

Seligman, J., Shalgi, R., Oschry, Y., and Kosower, N. S. (1991). Sperm analysis by flow cytometry using the fluorescent thiol labeling agent monobromobimane. Mol. Reprod. Dev. 29, 276–281.
Sperm analysis by flow cytometry using the fluorescent thiol labeling agent monobromobimane.CrossRef | 1:CAS:528:DyaK3MXmsFWgt7k%3D&md5=310c29685d12c3fdbccfd0c25ae31b20CAS | 1931044PubMed | open url image1

Seligman, J., Kosower, N. S., Weissenberg, R., and Shalgi, R. (1994). Thiol disulfide status of human sperm proteins. J. Reprod. Fertil. 101, 435–443.
Thiol disulfide status of human sperm proteins.CrossRef | 1:CAS:528:DyaK2cXmslOnsrg%3D&md5=667bf552f23cb89fc48dafae6d684c2cCAS | 7932379PubMed | open url image1

Shalgi, R., Seligman, J., and Kosower, N. S. (1989). Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol. Reprod. 40, 1037–1045.
Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane.CrossRef | 1:CAS:528:DyaL1MXltFakurY%3D&md5=daabb25687d0844a819adb77118262ccCAS | 2765609PubMed | open url image1

Shao, X., and van der Hoorn, F. A. (1996). Self-interaction of the major 27-kilodalton outer dense fiber protein is in part mediated by a leucine zipper domain in the rat. Biol. Reprod. 55, 1343–1350.
Self-interaction of the major 27-kilodalton outer dense fiber protein is in part mediated by a leucine zipper domain in the rat.CrossRef | 1:CAS:528:DyaK2sXkvFSltQ%3D%3D&md5=055a672bb72b34a0fa0fcdfd13202b89CAS | 8949892PubMed | open url image1

Shao, X., Xue, J., and van der Hoorn, F. A. (2001). Testicular protein Spag5 has similarity to mitotic spindle protein Deepest and binds outer dense fiber protein Odf1. Mol. Reprod. Dev. 59, 410–416.
Testicular protein Spag5 has similarity to mitotic spindle protein Deepest and binds outer dense fiber protein Odf1.CrossRef | 1:CAS:528:DC%2BD3MXltVWmsLs%3D&md5=ade93c5ac396fb340ab8d1514d5a4cd1CAS | 11468777PubMed | open url image1

Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4354.
Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.CrossRef | 1:CAS:528:DyaE1MXmtVKltLw%3D&md5=9a63ae993f243c65565e8d75c50c8b1aCAS | 388439PubMed | open url image1

Turner, R. M. (2006). Moving to the beat: a review of mammalian sperm motility regulation. Reprod. Fertil. Dev. 18, 25–38.
Moving to the beat: a review of mammalian sperm motility regulation.CrossRef | 16478600PubMed | open url image1

Vera, J. C., Brito, M., Zuvic, T., and Burziog, L. O. (1984). Polypeptide composition of rat sperm outer dense fibers. A simple procedure to isolate the fibrillar complex. J. Biol. Chem. 259, 5970–5977.
| 1:CAS:528:DyaL2cXitVKit78%3D&md5=bfc659d66f84d5217519ba5eb9e5b283CAS | 6715381PubMed | open url image1

World Health Organization (2010). ‘Laboratory Manual for the Examination of Human Semen and Sperm–Cervical Mucus Interaction’. pp. 7–107. (Cambridge University Press: New York.)

Xiao, X., and Yang, W. X. (2007). Actin-based dynamics during spermatogenesis and its significance. J. Zhejiang Univ. Sci. B 8, 498–506.
Actin-based dynamics during spermatogenesis and its significance.CrossRef | 1:CAS:528:DC%2BD2sXptFGmsrw%3D&md5=4e5e82c2d04a4060622b620eb4304b92CAS | 17610330PubMed | open url image1

Yang, K., Meinhardt, A., Zhang, B., Grzmil, P., Adham, I. M., and Hoyer-Fender, S. (2012). The small heat shock protein ODF1/HSPB10 is essential for tight linkage of sperm head to tail and male fertility in mice. Mol. Cell. Biol. 32, 216–225.
The small heat shock protein ODF1/HSPB10 is essential for tight linkage of sperm head to tail and male fertility in mice.CrossRef | 22037768PubMed | open url image1

Yeung, C. H., Sonnenberg-Riethmacher, E., and Cooper, T. G. (1999). Infertile spermatozoa of c-ros tyrosine kinase receptor knockout mice show flagellar angulation and maturational defects in cell volume regulatory mechanisms. Biol. Reprod. 61, 1062–1069.
Infertile spermatozoa of c-ros tyrosine kinase receptor knockout mice show flagellar angulation and maturational defects in cell volume regulatory mechanisms.CrossRef | 1:CAS:528:DyaK1MXmtlajt7s%3D&md5=ce54c53305c9d7ab41ab8afbe0ddd0b7CAS | 10491645PubMed | open url image1

Zarelli, V. E., Ruete, M. C., Roggero, C. M., Mayorga, L. S., and Tomes, C. N. (2009). PTP1B dephosphorylates N-ethylmaleimide-sensitive factor and elicits SNARE complex disassembly during human sperm exocytosis. J. Biol. Chem. 284, 10491–10503.
PTP1B dephosphorylates N-ethylmaleimide-sensitive factor and elicits SNARE complex disassembly during human sperm exocytosis.CrossRef | 1:CAS:528:DC%2BD1MXktlGkt7c%3D&md5=c7b951563ed768f62e514c7fa0add339CAS | 19208619PubMed | open url image1



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