Study on the role of calmodulin in sperm function through the enrichment and identification of calmodulin-binding proteins in bovine ejaculated spermatozoa.
biological process
calmodulin pull-down
gene ontology
mammalian spermatozoa
proteomics
sperm head proteins
Journal
Journal of cellular physiology
ISSN: 1097-4652
Titre abrégé: J Cell Physiol
Pays: United States
ID NLM: 0050222
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
20
06
2019
accepted:
19
12
2019
pubmed:
7
1
2020
medline:
10
3
2021
entrez:
7
1
2020
Statut:
ppublish
Résumé
Calmodulin is a small, highly conserved acidic protein present at high levels in spermatozoa that mediates numerous intracellular Ca
Substances chimiques
Calmodulin
0
Calmodulin-Binding Proteins
0
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5340-5352Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Adeoya-Osiguwa, S. A., & Fraser, L. R. (1996). Evidence for Ca2+-dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm. Molecular Reproduction and Development, 44(1), 111-120.
Aitken, R. J., Clarkson, J. S., Hulme, M. J., & Henderson, C. J. (1988). Analysis of calmodulin acceptor proteins and the influence of calmodulin antagonists on human spermatozoa. Gamete Research, 21, 93-111.
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., … Sherlock, G. (2000). Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics, 25(1), 25-29. https://doi.org/10.1038/75556
Baba, T., Niida, Y., Michikawa, Y., Kashiwabara, S., Kodaira, K., Takenaka, M., … Arai, Y. (1994). An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. Journal of Biological Chemistry, 269(13), 10133-10140.
Bailey, J. L., Bilodeau, J. F., & Cormier, N. (2000). Semen cryopreservation in domestic animals: A damaging and capacitating phenomenon. Journal of Andrology, 21(1), 1-7.
Bendahmane, M., Lynch, C., 2nd, & Tulsiani, D. R. (2001). Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Archives of Biochemistry and Biophysics, 390(1), 1-8.
Brokaw, C. J., & Nagayama, S. M. (1985). Modulation of the asymmetry of sea urchin sperm flagellar bending by calmodulin. Journal of Cell Biology, 100, 1875-1883.
Carafoli, E., & Krebs, J. (2016). Why calcium? How calcium became the best communicator. Journal of Biological Chemistry, 291, 20849-20857. https://doi.org/10.1074/jbc.R116.735894
Carrera, A., Moos, J., Ning, X. P., Gerton, G. L., Tesarik, J., Kopf, G. S., & Moss, S. B. (1996). Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: Identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Developmental Biology, 180, 284-296.
Chan, P. J., & Dukelow, W. R. (1985). Calmodulin level changes associated with cyclic AMP treatment in cultured squirrel monkey oocytes and sperm. Zoological Science, 2, 219-223.
Chin, D., & Means, A. R. (2000). Calmodulin: A prototypical calcium sensor. Trends in Cell Biology, 10, 322-328.
D'Amours, O., Frenette, G., Bourassa, S., Calvo, E., Blondin, P., & Sullivan, R. (2018). Proteomic markers of functional sperm population in bovines: Comparison of low- and high-density spermatozoa following cryopreservation. Journal of Proteome Research, 17, 177-188. https://doi.org/10.1021/acs.jproteome.7b00493
D'Amours, O., Frenette, G., Caron, P., Belleannee, C., Guillemette, C., & Sullivan, R. (2016). Evidences of biological functions of biliverdin reductase A in the bovine epididymis. Journal of Cellular Physiology, 231(5), 1077-1089. https://doi.org/10.1002/jcp.25200
D'Amours, O., Frenette, G., Fortier, M., Leclerc, P., & Sullivan, R. (2010). Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction, 139(3), 545-556.
Dun, M. D., Smith, N. D., Baker, M. A., Lin, M., Aitken, R. J., & Nixon, B. (2011). The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm-oocyte interaction. Journal of Biological Chemistry, 286(42), 36875-36887. https://doi.org/10.1074/jbc.M110.188888
Ellerman, D. A., Pei, J., Gupta, S., Snell, W. J., Myles, D., & Primakoff, P. (2009). Izumo is part of a multiprotein family whose members form large complexes on mammalian sperm. Molecular Reproduction and Development, 76(12), 1188-1199.
Esposito, G., Jaiswal, B. S., Xie, F., Krajnc-Franken, M. A., Robben, T. J., Strik, A. M., … Gossen, J. A. (2004). Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proceedings of the National Academy of Sciences of the United States of America, 101(9), 2993-2998.
Fang, P., Xu, W., Li, D., Zhao, X., Dai, J., Wang, Z., … Qiao, Z. (2015). A novel acrosomal protein, IQCF1, involved in sperm capacitation and the acrosome reaction. Andrology, 3(2), 332-344. https://doi.org/10.1111/andr.296
Frenette, G., Chafouleas, J. G., Tremblay, R. R., & Dubé, J. Y. (1990). In vitro interactions of calmodulin with the ovine proacrosin-acrosin system. Journal of Andrology, 11(1), 25-31.
Goupil, S., Marechal, L., El Hajj, H., Tremblay, M. E., Richard, F. J., & Leclerc, P. (2016). Identification and localization of the cyclic nucleotide phosphodiesterase 10A in bovine testis and mature spermatozoa. PLoS One, 11(8), e0161035. https://doi.org/10.1371/journal.pone.0161035
Hess, K. C., Jones, B. H., Marquez, B., Chen, Y., Ord, T. S., Kamenetsky, M., … Moss, S. B. (2005). The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Developmental Cell, 9(2), 249-259.
Ignotz, G. G., & Suarez, S. S. (2005). Calcium/calmodulin and calmodulin kinase II stimulate hyperactivation in demembranated bovine sperm. Biology of Reproduction, 73, 519-526.
Jaiswal, B. S., & Conti, M. (2003). Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proceedings of the National Academy of Sciences of the United States of America, 100(19), 10676-10681.
Jones, H. P., Lenz, R. W., Palevitz, B. A., & Cormier, M. J. (1980). Calmodulin localization in mammalian spermatozoa. Proceedings of the National Academy of Sciences of the United States of America, 77(5), 2772-2776.
Kaleka, K. S., Petersen, A. N., Florence, M. A., & Gerges, N. Z. (2012). Pull-down of calmodulin-binding proteins. Journal of Visualized Experiments, 23(59), e3502. https://doi.org/10.3791/3502
Keller, A., Nesvizhskii, A. I., Kolker, E., & Aebersold, R. (2002). Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical Chemistry, 74(20), 5383-5392.
Kwon, W. S., Rahman, M. S., Lee, J. S., Yoon, S. J., Park, Y. J., & Pang, M. G. (2015). Discovery of predictive biomarkers for litter size in boar spermatozoa. Molecular & Cellular Proteomics, 14(5), 1230-1240. https://doi.org/10.1074/mcp.M114.045369
Leclerc, P., & Goupil, S. (2000). Distribution and localization of calmodulin-binding proteins in bull spermatozoa. Biology of Reproduction, 62(6), 1875-1881.
Leclerc, P., de Lamirande, E., & Gagnon, C. (1998). Interactions between Ca2+, cyclic 3′,5′-adenosine monophosphate, the superoxide anion, and tyrosine phosphorylation pathways in the regulation of human sperm capacitation. Journal of Andrology, 19(4), 434-443.
Leclerc, P., Langlais, J., Lambert, R. D., Sirard, M. A., & Chafouleas, J. G. (1989). Effect of heparin on the expression of calmodulin-binding proteins in bull spermatozoa. Journal of Reproduction and Fertility, 85, 615-622.
Leclerc, P., Sirard, M. -A., Chafouleas, J. G., & Lambert, R. D. (1990). Decreased binding of calmodulin to bull sperm proteins during heparin-induced capacitation. Biology of Reproduction, 42, 483-489.
Leclerc, P., Sirard, M. A., Chafouleas, J. G., & Lambert, R. D. (1992). Decrease in calmodulin concentrations during heparin-induced capacitation in bovine spermatozoa. Journal of Reproduction and Fertility, 94, 23-32.
Litvin, T. N., Kamenetsky, M., Zarifyan, A., Buck, J., & Levin, L. R. (2003). Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. Journal of Biological Chemistry, 278(18), 15922-15926. https://doi.org/10.1074/jbc.M212475200
Manjunath, P., Chandonnet, L., Baillargeon, L., & Roberts, K. D. (1993). Calmodulin-binding proteins in bovine semen. Journal of Reproduction and Fertility, 97, 75-81.
Marin-Briggiler, C. I., Jha, K. N., Chertihin, O., Buffone, M. G., Herr, J. C., Vazquez-Levin, M. H., & Visconti, P. E. (2005). Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation. Journal of Cell Science, 118(Pt 9), 2013-2022. https://doi.org/10.1242/jcs.02326
Marshall, C. B., Nishikawa, T., Osawa, M., Stathopulos, P. B., & Ikura, M. (2015). Calmodulin and STIM proteins: Two major calcium sensors in the cytoplasm and endoplasmic reticulum. Biochemical and Biophysical Research Communications, 460(1), 5-21. https://doi.org/10.1016/j.bbrc.2015.01.106
Miyagawa, Y., Tanaka, H., Iguchi, N., Kitamura, K., Nakamura, Y., Takahashi, T., … Nishimune, Y. (2002). Molecular cloning and characterization of the human orthologue of male germ cell-specific actin capping protein alpha3 (cpalpha3). Molecular Human Reproduction, 8(6), 531-539.
Miyata, H., Satouh, Y., Mashiko, D., Muto, M., Nozawa, K., Shiba, K., … Ikawa, M. (2015). Sperm calcineurin inhibition prevents mouse fertility with implications for male contraceptive. Science, 350, 442-445. https://doi.org/10.1126/science.aad0836
Moore, P. B., & Dedman, J. R. (1984). Calmodulin, a calmodulin acceptor protein, and calcimedins: Unique antibody localizations in hamster sperm. Journal of Cellular Biochemistry, 25, 99-107.
Morin, G., Sullivan, R., Laflamme, I., Robert, C., & Leclerc, P. (2010). SPAM1 isoforms from two tissue origins are differentially localized within ejaculated bull sperm membranes and have different roles during fertilization. Biology of Reproduction, 82, 271-281. https://doi.org/10.1095/biolreprod.109.079582
Mruk, K., Farley, B. M., Ritacco, A. W., & Kobertz, W. R. (2014). Calmodulation meta-analysis: Predicting calmodulin binding via canonical motif clustering. Journal of General Physiology, 144(1), 105-114. https://doi.org/10.1085/jgp.201311140
Navarrete, F. A., Garcia-Vazquez, F. A., Alvau, A., Escoffier, J., Krapf, D., Sanchez-Cardenas, C., … Visconti, P. E. (2015). Biphasic role of calcium in mouse sperm capacitation signaling pathways. Journal of Cellular Physiology, 230, 1758-1769. https://doi.org/10.1002/jcp.24873
Nesvizhskii, A. I., Keller, A., Kolker, E., & Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Analytical Chemistry, 75(17), 4646-4658.
Noland, T. D., Van Eldik, L. J., Garbers, D. L., & Burgess, W. H. (1985). Distribution of calmodulin and calmodulin-binding proteins in membranes from bovine epididymal spermatozoa. Gamete Research, 11, 297-303.
Nomikos, M., Blayney, L. M., Larman, M. G., Campbell, K., Rossbach, A., Saunders, C. M., … Lai, F. A. (2005). Role of phospholipase C-zeta domains in Ca2+-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and cytoplasmic Ca2+ oscillations. Journal of Biological Chemistry, 280(35), 31011-31018. https://doi.org/10.1074/jbc.M500629200
Nomikos, M., Sanders, J. R., Parthimos, D., Buntwal, L., Calver, B. L., Stamatiadis, P., … Lai, F. A. (2015). Essential role of the EF-hand domain in targeting sperm phospholipase czeta to membrane phosphatidylinositol 4,5-bisphosphate (PIP2). Journal of Biological Chemistry, 290(49), 29519-29530. https://doi.org/10.1074/jbc.M115.658443
Okunade, G. W., Miller, M. L., Pyne, G. J., Sutliff, R. L., O'Connor, K. T., Neumann, J. C., … Shull, G. E. (2004). Targeted ablation of plasma membrane Ca2+-ATPase (PMCA) 1 and 4 indicates a major housekeeping function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4. Journal of Biological Chemistry, 279(32), 33742-33750.
Olson, G. E., Winfrey, V. P., Garbers, D. L., & Noland, T. D. (1985). Isolation and characterization of a macromolecular complex associated with the outer acrosomal membrane of bovine spermatozoa. Biology of Reproduction, 33, 761-779.
Park, Y. J., Kwon, W. S., Oh, S. A., & Pang, M. G. (2012). Fertility-related proteomic profiling bull spermatozoa separated by percoll. Journal of Proteome Research, 11(8), 4162-4168. https://doi.org/10.1021/pr300248s
Peterson, R. N., Ashraf, M., & Russell, L. D. (1983). Effect of calmodulin antagonists on Ca2+ uptake by boar spermatozoa. Biochemical and Biophysical Research Communications, 114(1), 28-33.
Redgrove, K. A., Anderson, A. L., Dun, M. D., McLaughlin, E. A., O'Bryan, M. K., Aitken, R. J., & Nixon, B. (2011). Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae. Developmental Biology, 356, 460-474.
Redgrove, K. A., Nixon, B., Baker, M. A., Hetherington, L., Baker, G., Liu, D. Y., & Aitken, R. J. (2012). The molecular chaperone HSPA2 plays a key role in regulating the expression of sperm surface receptors that mediate sperm-egg recognition. PLoS One, 7(11), e50851. https://doi.org/10.1371/journal.pone.0050851
Saunders, C. M., Larman, M. G., Parrington, J., Cox, L. J., Royse, J., Blayney, L. M., … Lai, F. A. (2002). PLC zeta: A sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development, 129(15), 3533-3544.
Schlingmann, K., Michaut, M. A., McElwee, J. L., Wolff, C. A., Travis, A. J., & Turner, R. M. (2007). Calmodulin and CaMKII in the sperm principal piece: Evidence for a motility-related calcium/calmodulin pathway. Journal of Andrology, 28(5), 706-716. https://doi.org/10.2164/jandrol.106.001669
Si, Y., & Olds-Clarke, P. (2000). Evidence for the involvement of calmodulin in mouse sperm capacitaiton. Biology of Reproduction, 62, 1231-1239.
Tash, J. S., Krinks, M., Patel, J., Means, R. L., Klee, C. B., & Means, A. R. (1988). Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm. Journal of Cell Biology, 106, 1625-1633.
The Gene Ontology, C. (2019). The Gene Ontology Resource: 20 years and still GOing strong. Nucleic Acids Research, 47(D1), D330-D338. https://doi.org/10.1093/nar/gky1055
Towbin, H., Staehlin, T., & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America, 76, 4350-4354.
Trejo, R., & Mújica, A. (1990). Changes in calmodulin compartmentalization throughout capacitation and acrosome reaction in guinea pig spermatozoa. Molecular Reproduction and Development, 26, 366-376.
Weinman, S., Ores-Carton, C., Rainteau, D., & Puszkin, S. (1986). Immunoelectron microscopic localization of calmodulin and phospholipase A2 in spermatozoa. I. Journal of Histochemistry and Cytochemistry, 34(9), 1171-1179.
Yunes, R., Tomes, C., Michaut, M., De Blas, G., Rodriguez, F., Regazzi, R., & Mayorga, L. S. (2002). Rab3A and calmodulin regulate acrosomal exocytosis by mechanisms that do not require a direct interaction. FEBS Letters, 525(1-3), 126-130.
Zeng, H. T., & Tulsiani, D. R. (2003). Calmodulin antagonists differentially affect capacitation-associated protein tyrosine phosphorylation of mouse sperm components. Journal of Cell Science, 116(Pt 10), 1981-1989.
Zhang, P., Jiang, W., Luo, N., Zhu, W., & Fan, L. (2019). IQ motif containing D (IQCD), a new acrosomal protein involved in the acrosome reaction and fertilisation. Reproduction, Fertility, and Development, 31(5), 898-914. https://doi.org/10.1071/RD18416