Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2010

Open Access 01-12-2010 | Research

Identification of calcium-binding proteins associated with the human sperm plasma membrane

Authors: Soren Naaby-Hansen, Alan Diekman, Jagathpala Shetty, Charles J Flickinger, Anne Westbrook, John C Herr

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

Login to get access

Abstract

Background

The precise composition of the human sperm plasma membrane, the molecular interactions that define domain specific functions, and the regulation of membrane associated proteins during the capacitation process, still remain to be fully understood. Here, we investigated the repertoire of calcium-regulated proteins associated with the human sperm plasma membrane.

Methods

Surface specific radioiodination was combined with two-dimensional gel electrophoresis, a 45Ca-overlay assay, computer assisted image analysis and mass spectrometry to identify calcium-binding proteins exposed on the human sperm surface.

Results

Nine acidic 45Ca-binding sperm proteins were excised from stained preparative 2D gels and identified by mass spectrometry. Five of the calcium binding proteins; HSPA2 (HSP70-1), HSPA5 (Bip), HYOU1 (ORP150), serum amyloid P-component (SAP) and protein kinase C substrate 80K-H (80K-H) were found to be accessible to Iodo-Bead catalyzed 125I-labelling on the surface of intact human sperm. Agglutination and immunofluorescence analysis confirmed that SAP is situated on the plasma membrane of intact, motile sperm as well as permeabilized cells. Western blot analysis showed increased phosphorylation of human sperm 80K-H protein following in vitro capacitation. This is the first demonstration of the 80K-H protein in a mammalian sperm.

Conclusion

The presence of SAP on the surface of mature sperm implies that SAP has a physiological role in reproduction, which is thought to be in the removal of spermatozoa from the female genital tract via phagocytosis. Since 80K-H is a Ca2+-sensor recently implicated in the regulation of both inositol 1,4,5-trisphosphate receptor and transient receptor potential (TRP) cation channel activities, its detection in sperm represents the first direct signaling link between PKC and store-operated calcium channels identified in human sperm.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jovine L, Darie CC, Litscher ES, Wassarman PM: Zona Pellucida Domain Proteins. Annu Rev Biochem. 2005, 74: 83-114. 10.1146/annurev.biochem.74.082803.133039.CrossRefPubMed Jovine L, Darie CC, Litscher ES, Wassarman PM: Zona Pellucida Domain Proteins. Annu Rev Biochem. 2005, 74: 83-114. 10.1146/annurev.biochem.74.082803.133039.CrossRefPubMed
2.
go back to reference Florman HM, Jungnickel MK, Sutton KA: Regulating the acrosome reaction. Int J Dev Biol. 2008, 52 (5-6): 503-510. 10.1387/ijdb.082696hf.CrossRefPubMed Florman HM, Jungnickel MK, Sutton KA: Regulating the acrosome reaction. Int J Dev Biol. 2008, 52 (5-6): 503-510. 10.1387/ijdb.082696hf.CrossRefPubMed
3.
go back to reference Darszon A, Beltrán C, Felix R, Nishigaki T, Treviño CL: Ion transport in sperm signaling. Dev Biol. 2001, 240 (1): 1-14. 10.1006/dbio.2001.0387.CrossRefPubMed Darszon A, Beltrán C, Felix R, Nishigaki T, Treviño CL: Ion transport in sperm signaling. Dev Biol. 2001, 240 (1): 1-14. 10.1006/dbio.2001.0387.CrossRefPubMed
4.
go back to reference Darszon A, López-Martínez P, Acevedo JJ, Hernández-Cruz A, Treviño CL: T-type Ca2+ channels in sperm function. Cell Calcium. 2006, 40 (2): 241-252. 10.1016/j.ceca.2006.04.028.CrossRefPubMed Darszon A, López-Martínez P, Acevedo JJ, Hernández-Cruz A, Treviño CL: T-type Ca2+ channels in sperm function. Cell Calcium. 2006, 40 (2): 241-252. 10.1016/j.ceca.2006.04.028.CrossRefPubMed
5.
go back to reference Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M, Florman HM: Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. PNAS. 1999, 96: 6757-6762. 10.1073/pnas.96.12.6757.PubMedCentralCrossRefPubMed Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M, Florman HM: Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. PNAS. 1999, 96: 6757-6762. 10.1073/pnas.96.12.6757.PubMedCentralCrossRefPubMed
6.
go back to reference Felix R: Molecular physiology and pathology of Ca2+-conducting channels in the plasma membrane of mammalian sperm. Reproduction. 2005, 129 (3): 251-262. 10.1530/rep.1.00478.CrossRefPubMed Felix R: Molecular physiology and pathology of Ca2+-conducting channels in the plasma membrane of mammalian sperm. Reproduction. 2005, 129 (3): 251-262. 10.1530/rep.1.00478.CrossRefPubMed
7.
go back to reference O'Toole CM, Arnoult C, Darszon A, Steinhardt RA, Florman HM: Ca(2+) entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Mol Biol Cell. 2000, 11 (5): 1571-1584.PubMedCentralCrossRefPubMed O'Toole CM, Arnoult C, Darszon A, Steinhardt RA, Florman HM: Ca(2+) entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Mol Biol Cell. 2000, 11 (5): 1571-1584.PubMedCentralCrossRefPubMed
8.
go back to reference De Blas G, Michaut M, Treviño CL, Tomes CN, Yunes R, Darszon A, Mayorga LS: The intraacrosomal calcium pool plays a direct role in acrosomal exocytosis. J Biol Chem. 2002, 277 (51): 49326-49331. 10.1074/jbc.M208587200.CrossRefPubMed De Blas G, Michaut M, Treviño CL, Tomes CN, Yunes R, Darszon A, Mayorga LS: The intraacrosomal calcium pool plays a direct role in acrosomal exocytosis. J Biol Chem. 2002, 277 (51): 49326-49331. 10.1074/jbc.M208587200.CrossRefPubMed
9.
go back to reference Naaby-Hansen S, Wolkowicz M, Klotz K, Bush LA, Westbrook VA, Shibahara H, Shetty J, Coonrod SA, Reddi PP, Shannon J, Kinter M, Sherman NE, Fox J, Flickinger CJ, Herr JC: Co-localization of the inositol 1,4,5-triphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa. Mol Hum Reprod. 2001, 7 (10): 923-933. 10.1093/molehr/7.10.923.CrossRefPubMed Naaby-Hansen S, Wolkowicz M, Klotz K, Bush LA, Westbrook VA, Shibahara H, Shetty J, Coonrod SA, Reddi PP, Shannon J, Kinter M, Sherman NE, Fox J, Flickinger CJ, Herr JC: Co-localization of the inositol 1,4,5-triphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa. Mol Hum Reprod. 2001, 7 (10): 923-933. 10.1093/molehr/7.10.923.CrossRefPubMed
10.
go back to reference Jungnickel MK, Marrero H, Birnbaumer L, Lémos JR, Florman HM: Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol. 2001, 3 (5): 499-502. 10.1038/35074570.CrossRefPubMed Jungnickel MK, Marrero H, Birnbaumer L, Lémos JR, Florman HM: Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol. 2001, 3 (5): 499-502. 10.1038/35074570.CrossRefPubMed
11.
go back to reference Naaby-Hansen S, Herr JC: Heat shock proteins on the human sperm surface. J Reprod Immunol. Naaby-Hansen S, Herr JC: Heat shock proteins on the human sperm surface. J Reprod Immunol.
12.
go back to reference Malm J, Sonesson A, Hellman J, Bjartell A, Frohm B, Hillarp A: The pentraxin serum amyloid P component is found in the male genital tract and attached to spermatozoa. Int J Androl. 2007, 31: 508-517. 10.1111/j.1365-2605.2007.00800.x.CrossRefPubMed Malm J, Sonesson A, Hellman J, Bjartell A, Frohm B, Hillarp A: The pentraxin serum amyloid P component is found in the male genital tract and attached to spermatozoa. Int J Androl. 2007, 31: 508-517. 10.1111/j.1365-2605.2007.00800.x.CrossRefPubMed
13.
go back to reference Bronson RA, Fusi F: Sperm-oolemmal interaction: role of the Arg-Gly-Asp (RGD) adhesion peptide. Fertil Steril. 1990, 54 (3): 527-529.PubMed Bronson RA, Fusi F: Sperm-oolemmal interaction: role of the Arg-Gly-Asp (RGD) adhesion peptide. Fertil Steril. 1990, 54 (3): 527-529.PubMed
14.
go back to reference Naaby-Hansen S, Flickinger CJ, Herr JC: Two-dimensional gel electrophoretic analysis of vectorially labeled surface proteins of human sperm. Biol Reprod. 1997, 56: 771-787. 10.1095/biolreprod56.3.771.CrossRefPubMed Naaby-Hansen S, Flickinger CJ, Herr JC: Two-dimensional gel electrophoretic analysis of vectorially labeled surface proteins of human sperm. Biol Reprod. 1997, 56: 771-787. 10.1095/biolreprod56.3.771.CrossRefPubMed
15.
go back to reference Naaby-Hansen S, Mandal A, Wolkowicz MJ, Buer S, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Bush LA, Flickinger CF, Herr JC: CABYR, A Novel Calcium Binding Tyrosine-Phosphorylation Regulated Fibrous Sheath Protein Involved in Capacitation. Develop Biol. 2002, 242: 236-254. 10.1006/dbio.2001.0527.CrossRefPubMed Naaby-Hansen S, Mandal A, Wolkowicz MJ, Buer S, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Bush LA, Flickinger CF, Herr JC: CABYR, A Novel Calcium Binding Tyrosine-Phosphorylation Regulated Fibrous Sheath Protein Involved in Capacitation. Develop Biol. 2002, 242: 236-254. 10.1006/dbio.2001.0527.CrossRefPubMed
16.
go back to reference Henzel WJ, Billeci TM, Stults JT, Wong SC, Grimley C, Watanabe C: Identifying proteins from two-dimensional gels by molecular mass searching of peptide fragments in protein sequence databases. PNAS. 1993, 90 (11): 5011-5015. 10.1073/pnas.90.11.5011.PubMedCentralCrossRefPubMed Henzel WJ, Billeci TM, Stults JT, Wong SC, Grimley C, Watanabe C: Identifying proteins from two-dimensional gels by molecular mass searching of peptide fragments in protein sequence databases. PNAS. 1993, 90 (11): 5011-5015. 10.1073/pnas.90.11.5011.PubMedCentralCrossRefPubMed
17.
go back to reference Matsudaira P: Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987, 262 (21): 10035-10038.PubMed Matsudaira P: Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987, 262 (21): 10035-10038.PubMed
18.
go back to reference Maruyama K, Mikawa T, Ebashi S: Detection of Calcium Binding Proteins by a 45 Ca Autoradiography on Nitrocellulose Membrane after Sodium Dodecyl Sulfate Gel Electrophoresis. J Biochem. 1984, 95: 511-519.PubMed Maruyama K, Mikawa T, Ebashi S: Detection of Calcium Binding Proteins by a 45 Ca Autoradiography on Nitrocellulose Membrane after Sodium Dodecyl Sulfate Gel Electrophoresis. J Biochem. 1984, 95: 511-519.PubMed
19.
go back to reference Diekman AB, Westbrook-Case VA, Naaby-Hansen S, Klotz KL, Flickinger CJ, Herr JC: Biochemical characterization of Spermatozoa Agglutination Antigen-1, a human spermatozoa antigen implicated in gamete interactions. Biol Reprod. 1997, 56: 771-787. 10.1095/biolreprod56.3.771.CrossRef Diekman AB, Westbrook-Case VA, Naaby-Hansen S, Klotz KL, Flickinger CJ, Herr JC: Biochemical characterization of Spermatozoa Agglutination Antigen-1, a human spermatozoa antigen implicated in gamete interactions. Biol Reprod. 1997, 56: 771-787. 10.1095/biolreprod56.3.771.CrossRef
20.
go back to reference Shetty J, Diekman AB, Jayes FCL, Sherman N, Naaby-Hansen S, Flickinger CJ, Herr JC: Differential Extraction and Enrichment of Human Spermatozoa Surface Proteins in a Proteome: Identification of Immunocontraceptive Candidates. Electrophoresis. 2001, 22: 3053-3066. 10.1002/1522-2683(200108)22:14<3053::AID-ELPS3053>3.0.CO;2-K.CrossRefPubMed Shetty J, Diekman AB, Jayes FCL, Sherman N, Naaby-Hansen S, Flickinger CJ, Herr JC: Differential Extraction and Enrichment of Human Spermatozoa Surface Proteins in a Proteome: Identification of Immunocontraceptive Candidates. Electrophoresis. 2001, 22: 3053-3066. 10.1002/1522-2683(200108)22:14<3053::AID-ELPS3053>3.0.CO;2-K.CrossRefPubMed
21.
go back to reference Primakoff P, Myles DG: Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science. 2002, 296: 2183-2185. 10.1126/science.1072029.CrossRefPubMed Primakoff P, Myles DG: Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science. 2002, 296: 2183-2185. 10.1126/science.1072029.CrossRefPubMed
22.
go back to reference Shin BK, Wang H, Yim AM, Naour FL, Brichory F, Jang JH, Zhao R, Puravs E, Tra J, Michael CW, Misek DE, Hanash SM: Global Profiling of the Cell Surface Proteome of Cancer Cells Uncovers an Abundance of Proteins with Chaperone Function. J Biol Chem. 2003, 278: 7607-7616. 10.1074/jbc.M210455200.CrossRefPubMed Shin BK, Wang H, Yim AM, Naour FL, Brichory F, Jang JH, Zhao R, Puravs E, Tra J, Michael CW, Misek DE, Hanash SM: Global Profiling of the Cell Surface Proteome of Cancer Cells Uncovers an Abundance of Proteins with Chaperone Function. J Biol Chem. 2003, 278: 7607-7616. 10.1074/jbc.M210455200.CrossRefPubMed
23.
go back to reference Calvert ME, Digilio LC, Herr JC, Coonrod SA: Oolemmal proteomics--identification of highly abundant heat shock proteins and molecular chaperones in the mature mouse egg and their localization on the plasma membrane. Reprod Biol Endocrinol. 2003, 1: 27-36. 10.1186/1477-7827-1-27.PubMedCentralCrossRefPubMed Calvert ME, Digilio LC, Herr JC, Coonrod SA: Oolemmal proteomics--identification of highly abundant heat shock proteins and molecular chaperones in the mature mouse egg and their localization on the plasma membrane. Reprod Biol Endocrinol. 2003, 1: 27-36. 10.1186/1477-7827-1-27.PubMedCentralCrossRefPubMed
24.
go back to reference Bohring C, Krause W: Characterization of spermatozoa surface antigens by antisperm antibodies and its influence on acrosomal exocytosis. Am J Reprod Immunol. 2003, 50: 411-419. 10.1034/j.1600-0897.2003.00103.x.CrossRefPubMed Bohring C, Krause W: Characterization of spermatozoa surface antigens by antisperm antibodies and its influence on acrosomal exocytosis. Am J Reprod Immunol. 2003, 50: 411-419. 10.1034/j.1600-0897.2003.00103.x.CrossRefPubMed
25.
go back to reference Hastie C, Saxton M, Akpan A, Cramer R, Masters JR, Naaby-Hansen S: Combined affinity labelling and mass spectrometry analysis of differential cell surface protein expression in normal and prostate cancer cells. Oncogene. 2005, 24 (38): 5905-5913. 10.1038/sj.onc.1208747.CrossRefPubMed Hastie C, Saxton M, Akpan A, Cramer R, Masters JR, Naaby-Hansen S: Combined affinity labelling and mass spectrometry analysis of differential cell surface protein expression in normal and prostate cancer cells. Oncogene. 2005, 24 (38): 5905-5913. 10.1038/sj.onc.1208747.CrossRefPubMed
26.
go back to reference Mandal A, Naaby-Hansen S, Wolkowicz MJ, Klotz K, Shetty J, Retief JD, Coonrod SA, Kinter M, Sherman N, Cesar F, Flickinger CF, Herr JC: FSP95, a testis specific 95 kDa fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol Reprod. 1999, 61: 1184-1197. 10.1095/biolreprod61.5.1184.CrossRefPubMed Mandal A, Naaby-Hansen S, Wolkowicz MJ, Klotz K, Shetty J, Retief JD, Coonrod SA, Kinter M, Sherman N, Cesar F, Flickinger CF, Herr JC: FSP95, a testis specific 95 kDa fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol Reprod. 1999, 61: 1184-1197. 10.1095/biolreprod61.5.1184.CrossRefPubMed
27.
28.
go back to reference Kiernan UA, Nedelkov D, Tubbs KA, Niederkofler EE, Nelson RW: Proteomic characterization of novel serum amyloid P component variants from human plasma and urine. Proteomics. 2004, 4: 1825-1829. 10.1002/pmic.200300690.CrossRefPubMed Kiernan UA, Nedelkov D, Tubbs KA, Niederkofler EE, Nelson RW: Proteomic characterization of novel serum amyloid P component variants from human plasma and urine. Proteomics. 2004, 4: 1825-1829. 10.1002/pmic.200300690.CrossRefPubMed
29.
go back to reference Sriram M, Osipiuk J, Freeman B, Morimoto R, Joachimiak A: Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure. 1997, 5: 403-414. 10.1016/S0969-2126(97)00197-4.CrossRefPubMed Sriram M, Osipiuk J, Freeman B, Morimoto R, Joachimiak A: Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure. 1997, 5: 403-414. 10.1016/S0969-2126(97)00197-4.CrossRefPubMed
30.
go back to reference Serrano L, Valencia A, Caballero R, Avila J: Localization of the high affinity calcium-binding site on tubulin molecule. J Biol Chem. 1986, 261: 7076-7081.PubMed Serrano L, Valencia A, Caballero R, Avila J: Localization of the high affinity calcium-binding site on tubulin molecule. J Biol Chem. 1986, 261: 7076-7081.PubMed
31.
go back to reference Fong KC, Babitch JA, Anthony FA: Calcium binding to tubulin. Biochim Biophys Acta. 1988, 952: 13-19.CrossRefPubMed Fong KC, Babitch JA, Anthony FA: Calcium binding to tubulin. Biochim Biophys Acta. 1988, 952: 13-19.CrossRefPubMed
32.
go back to reference Kitao Y, Ozawa K, Miyazaki M, Tamatani M, Kobayashi T, Yanagi H, Okabe M, Ikawa M, Yamashima T, Stern DM, Hori O, Ogawa S: Expression of the endoplasmic reticulum molecular chaperone (ORP150) rescues hippocampal neurons from glutamate toxicity. J Clin Invest. 2001, 108: 1439-1450.PubMedCentralCrossRefPubMed Kitao Y, Ozawa K, Miyazaki M, Tamatani M, Kobayashi T, Yanagi H, Okabe M, Ikawa M, Yamashima T, Stern DM, Hori O, Ogawa S: Expression of the endoplasmic reticulum molecular chaperone (ORP150) rescues hippocampal neurons from glutamate toxicity. J Clin Invest. 2001, 108: 1439-1450.PubMedCentralCrossRefPubMed
33.
go back to reference Miller D, Brough S, al-Harbi O: Characterization and cellular distribution of human spermatozoal heat shock proteins. Hum Reprod. 1992, 7: 637-645.PubMed Miller D, Brough S, al-Harbi O: Characterization and cellular distribution of human spermatozoal heat shock proteins. Hum Reprod. 1992, 7: 637-645.PubMed
34.
go back to reference Danielsen B, Sørensen IJ, Nybo M, Nielsen EH, Kaplan B, Svehag SE: Calcium-dependent and -independent binding of the pentraxin serum amyloid P component to glycosaminoglycans and amyloid proteins: enhanced binding at slightly acid pH. Biochim Biophys Acta. 1997, 1339: 73-78.CrossRefPubMed Danielsen B, Sørensen IJ, Nybo M, Nielsen EH, Kaplan B, Svehag SE: Calcium-dependent and -independent binding of the pentraxin serum amyloid P component to glycosaminoglycans and amyloid proteins: enhanced binding at slightly acid pH. Biochim Biophys Acta. 1997, 1339: 73-78.CrossRefPubMed
35.
go back to reference Heegaard NH, He X, Blomberg LG: Binding of Ca2+, Mg2+, and heparin by human serum amyloid P component in affinity capillary electrophoresis. Electrophoresis. 2006, 27: 2609-2615. 10.1002/elps.200600005.CrossRefPubMed Heegaard NH, He X, Blomberg LG: Binding of Ca2+, Mg2+, and heparin by human serum amyloid P component in affinity capillary electrophoresis. Electrophoresis. 2006, 27: 2609-2615. 10.1002/elps.200600005.CrossRefPubMed
36.
go back to reference Hicks PS, Saunero-Nava L, Du Clos TW, Mold C: Serum amyloid P component binds to histones and activates the classical complement pathway. J Immunol. 1992, 149: 3689-3694.PubMed Hicks PS, Saunero-Nava L, Du Clos TW, Mold C: Serum amyloid P component binds to histones and activates the classical complement pathway. J Immunol. 1992, 149: 3689-3694.PubMed
37.
go back to reference Riley-Vargas RC, Lanzendorf S, Atkinson JP: Targeted and restricted complement activation on acrosome-reacted spermatozoa. J Clin Invest. 2005, 115: 1241-1249.PubMedCentralCrossRefPubMed Riley-Vargas RC, Lanzendorf S, Atkinson JP: Targeted and restricted complement activation on acrosome-reacted spermatozoa. J Clin Invest. 2005, 115: 1241-1249.PubMedCentralCrossRefPubMed
38.
go back to reference Familian A, Zwart B, Huisman HG, Rensink I, Roem D, Hordijk PL, Aarden LA, Hack CE: Chromatin-Independent Binding of Serum Amyloid P Component to Apoptotic Cells. J Immunol. 2001, 167: 647-654.CrossRefPubMed Familian A, Zwart B, Huisman HG, Rensink I, Roem D, Hordijk PL, Aarden LA, Hack CE: Chromatin-Independent Binding of Serum Amyloid P Component to Apoptotic Cells. J Immunol. 2001, 167: 647-654.CrossRefPubMed
39.
go back to reference Ciurana CLF, Hack CE: Competitive binding of pentraxins and IgM to newly exposed epitopes on late apoptotic cells. Cell Immunol. 2006, 239: 14-21. 10.1016/j.cellimm.2006.02.006.CrossRefPubMed Ciurana CLF, Hack CE: Competitive binding of pentraxins and IgM to newly exposed epitopes on late apoptotic cells. Cell Immunol. 2006, 239: 14-21. 10.1016/j.cellimm.2006.02.006.CrossRefPubMed
40.
go back to reference Bijl M, Horst G, Bijzet J, Bootsma H, Limburg PC, Kallenberg CGM: Serum amyloid P component binds to late apoptotic cells and mediates their uptake by monocyte-derived macrophages. Arthritis & Rheumatism. 2003, 48 (1): 248-254. 10.1002/art.10737.CrossRef Bijl M, Horst G, Bijzet J, Bootsma H, Limburg PC, Kallenberg CGM: Serum amyloid P component binds to late apoptotic cells and mediates their uptake by monocyte-derived macrophages. Arthritis & Rheumatism. 2003, 48 (1): 248-254. 10.1002/art.10737.CrossRef
41.
go back to reference van Rossum AP, Fazzini F, Limburg PC, Manfredi AA, Rovere-Querini P, Mantovani A, Kallenberg CG: The prototypic tissue pentraxin PTX3, in contrast to the short pentraxin serum amyloid P, inhibits phagocytosis of late apoptotic neutrophils by macrophages. Arthritis Rheum. 2004, 50 (8): 2667-2674. 10.1002/art.20370.CrossRefPubMed van Rossum AP, Fazzini F, Limburg PC, Manfredi AA, Rovere-Querini P, Mantovani A, Kallenberg CG: The prototypic tissue pentraxin PTX3, in contrast to the short pentraxin serum amyloid P, inhibits phagocytosis of late apoptotic neutrophils by macrophages. Arthritis Rheum. 2004, 50 (8): 2667-2674. 10.1002/art.20370.CrossRefPubMed
42.
go back to reference Bharadwaj D, Mold C, Markham E, Du Clos TW: Serum Amyloid P Component Binds to Fc gamma Receptors and Opsonizes Particles for Phagocytosis. J Immunol. 2001, 166: 6735-6741.CrossRefPubMed Bharadwaj D, Mold C, Markham E, Du Clos TW: Serum Amyloid P Component Binds to Fc gamma Receptors and Opsonizes Particles for Phagocytosis. J Immunol. 2001, 166: 6735-6741.CrossRefPubMed
43.
go back to reference Mold C, Baca R, Du Clos TW: Serum Amyloid P Component and C-Reactive Protein Opsonize Apoptotic Cells for Phagocytosis through Fcγ Receptors. J Autoimmunity. 2002, 19 (3): 147-154. 10.1006/jaut.2002.0615.CrossRef Mold C, Baca R, Du Clos TW: Serum Amyloid P Component and C-Reactive Protein Opsonize Apoptotic Cells for Phagocytosis through Fcγ Receptors. J Autoimmunity. 2002, 19 (3): 147-154. 10.1006/jaut.2002.0615.CrossRef
44.
go back to reference Kim SJ, Gershov D, Ma X, Brot N, Elkon KB: Opsonization of Apoptotic Cells and Its Effect on Macrophage and T Cell Immune Responses. Ann N Y Acad Sci. 2003, 987: 68-78. 10.1111/j.1749-6632.2003.tb06034.x.CrossRefPubMed Kim SJ, Gershov D, Ma X, Brot N, Elkon KB: Opsonization of Apoptotic Cells and Its Effect on Macrophage and T Cell Immune Responses. Ann N Y Acad Sci. 2003, 987: 68-78. 10.1111/j.1749-6632.2003.tb06034.x.CrossRefPubMed
45.
go back to reference Pittoni V, Valesini G: The clearance of apoptotic cells: implications for autoimmunity. Autoimmun Rev. 2002, 1 (3): 154-161. 10.1016/S1568-9972(02)00032-0.CrossRefPubMed Pittoni V, Valesini G: The clearance of apoptotic cells: implications for autoimmunity. Autoimmun Rev. 2002, 1 (3): 154-161. 10.1016/S1568-9972(02)00032-0.CrossRefPubMed
46.
go back to reference Roos A, Xu W, Castellano G, Nauta AJ, Garred P, Daha MR, van Kooten C: A pivotal role for innate immunity in the clearance of apoptotic cells. Eur J Immunol. 2004, 34 (4): 921-929. 10.1002/eji.200424904.CrossRefPubMed Roos A, Xu W, Castellano G, Nauta AJ, Garred P, Daha MR, van Kooten C: A pivotal role for innate immunity in the clearance of apoptotic cells. Eur J Immunol. 2004, 34 (4): 921-929. 10.1002/eji.200424904.CrossRefPubMed
47.
go back to reference Gewurz H, Zhang X-H, Lint TF: Structure and function of the pentraxins. Curr Opin Immunol. 1995, 7 (1): 54-64. 10.1016/0952-7915(95)80029-8.CrossRefPubMed Gewurz H, Zhang X-H, Lint TF: Structure and function of the pentraxins. Curr Opin Immunol. 1995, 7 (1): 54-64. 10.1016/0952-7915(95)80029-8.CrossRefPubMed
48.
go back to reference Brown MR, Anderson BE: Receptor-ligand interactions between serum amyloid P component and model soluble immune complexes. J Immunol. 1993, 151: 2087-2095.PubMed Brown MR, Anderson BE: Receptor-ligand interactions between serum amyloid P component and model soluble immune complexes. J Immunol. 1993, 151: 2087-2095.PubMed
49.
go back to reference Pepys MB, Booth SE, Tennent GA, Butler PJG, Williams DG: Binding of pentraxins to different nuclear structures: C--reactive protein binds to small nuclear ribonucleoprotein particles, serum amyloid P component binds to chromatin and nucleoli. Clin Exp Immunol. 1994, 97 (1): 152-157.PubMedCentralCrossRefPubMed Pepys MB, Booth SE, Tennent GA, Butler PJG, Williams DG: Binding of pentraxins to different nuclear structures: C--reactive protein binds to small nuclear ribonucleoprotein particles, serum amyloid P component binds to chromatin and nucleoli. Clin Exp Immunol. 1994, 97 (1): 152-157.PubMedCentralCrossRefPubMed
50.
go back to reference Bickerstaff MCM, Botto M, Hutchinson WL, Herbert J, Tennent GA, Bybee A, Mitchell DA, Cook HT, Butler PJG, Walport MJ, Pepys MB: Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat Med. 1999, 5: 694-697. 10.1038/9544.CrossRefPubMed Bickerstaff MCM, Botto M, Hutchinson WL, Herbert J, Tennent GA, Bybee A, Mitchell DA, Cook HT, Butler PJG, Walport MJ, Pepys MB: Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat Med. 1999, 5: 694-697. 10.1038/9544.CrossRefPubMed
51.
go back to reference Pandya IJ, Cohen J: The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril. 1985, 43 (3): 417-421.PubMed Pandya IJ, Cohen J: The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril. 1985, 43 (3): 417-421.PubMed
52.
go back to reference Phillips DM, Mahler S: Leukocyte emigration and migration in the vagina following mating in the rabbit. Anat Rec. 1977, 189: 45-56. 10.1002/ar.1091890104.CrossRefPubMed Phillips DM, Mahler S: Leukocyte emigration and migration in the vagina following mating in the rabbit. Anat Rec. 1977, 189: 45-56. 10.1002/ar.1091890104.CrossRefPubMed
53.
go back to reference Bedford JM: Effect of environment on phagocytosis of rabbit spermatozoa. J Reprod Fertil. 1965, 9: 249-256.CrossRefPubMed Bedford JM: Effect of environment on phagocytosis of rabbit spermatozoa. J Reprod Fertil. 1965, 9: 249-256.CrossRefPubMed
54.
go back to reference Venkatachalam K, van Rossum DB, Patterson RL, Ma HT, Gill DL: The cellular and molecular basis of store-operated calcium entry. Nat Cell Biol. 2002, 4 (11): E263-272. 10.1038/ncb1102-e263.CrossRefPubMed Venkatachalam K, van Rossum DB, Patterson RL, Ma HT, Gill DL: The cellular and molecular basis of store-operated calcium entry. Nat Cell Biol. 2002, 4 (11): E263-272. 10.1038/ncb1102-e263.CrossRefPubMed
55.
go back to reference Treviño CL, Serrano CJ, Beltrán C, Felix R, Darszon A: Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett. 2001, 509 (1): 119-125. 10.1016/S0014-5793(01)03134-9.CrossRefPubMed Treviño CL, Serrano CJ, Beltrán C, Felix R, Darszon A: Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett. 2001, 509 (1): 119-125. 10.1016/S0014-5793(01)03134-9.CrossRefPubMed
56.
go back to reference Treviño CL, De la Vega-Beltrán JL, Nishigaki T, Felix R, Darszon A: Maitotoxin potently promotes Ca2+ influx in mouse spermatogenic cells and sperm, and induces the acrosome reaction. J Cell Physiol. 2006, 206 (2): 449-456. 10.1002/jcp.20487.CrossRefPubMed Treviño CL, De la Vega-Beltrán JL, Nishigaki T, Felix R, Darszon A: Maitotoxin potently promotes Ca2+ influx in mouse spermatogenic cells and sperm, and induces the acrosome reaction. J Cell Physiol. 2006, 206 (2): 449-456. 10.1002/jcp.20487.CrossRefPubMed
57.
go back to reference Zhu X, Jiang M, Peyton M, Boulay G, Hurst R, Stefani E, Birnbaumer L: trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell. 1996, 85 (5): 661-671. 10.1016/S0092-8674(00)81233-7.CrossRefPubMed Zhu X, Jiang M, Peyton M, Boulay G, Hurst R, Stefani E, Birnbaumer L: trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell. 1996, 85 (5): 661-671. 10.1016/S0092-8674(00)81233-7.CrossRefPubMed
58.
go back to reference Vannier B, Peyton M, Boulay G, Brown D, Qin N, Jiang M, Zhu X, Birnbaumer L: Mouse trp2, the homologue of the human trpc2 pseudogene, encodes mTrp2, a store depletion-activated capacitative Ca2+ entry channel. PNAS. 1999, 96 (5): 2060-2064. 10.1073/pnas.96.5.2060.PubMedCentralCrossRefPubMed Vannier B, Peyton M, Boulay G, Brown D, Qin N, Jiang M, Zhu X, Birnbaumer L: Mouse trp2, the homologue of the human trpc2 pseudogene, encodes mTrp2, a store depletion-activated capacitative Ca2+ entry channel. PNAS. 1999, 96 (5): 2060-2064. 10.1073/pnas.96.5.2060.PubMedCentralCrossRefPubMed
59.
go back to reference Nilius B, Voets T: TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch. 2005, 451 (1): 1-10. 10.1007/s00424-005-1462-y.CrossRefPubMed Nilius B, Voets T: TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch. 2005, 451 (1): 1-10. 10.1007/s00424-005-1462-y.CrossRefPubMed
60.
go back to reference Stowers L, Holy TE, Meister M, Dulac C, Koentges G: Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science. 2002, 295 (5559): 1493-1500. 10.1126/science.1069259.CrossRefPubMed Stowers L, Holy TE, Meister M, Dulac C, Koentges G: Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science. 2002, 295 (5559): 1493-1500. 10.1126/science.1069259.CrossRefPubMed
61.
go back to reference Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R: Altered sexual and social behaviors in trp2 mutant mice. PNAS. 2002, 99 (9): 6376-6381. 10.1073/pnas.082127599.PubMedCentralCrossRefPubMed Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R: Altered sexual and social behaviors in trp2 mutant mice. PNAS. 2002, 99 (9): 6376-6381. 10.1073/pnas.082127599.PubMedCentralCrossRefPubMed
62.
go back to reference Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD: STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature. 2005, 437 (7060): 902-9055. 10.1038/nature04147.PubMedCentralCrossRefPubMed Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD: STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature. 2005, 437 (7060): 902-9055. 10.1038/nature04147.PubMedCentralCrossRefPubMed
63.
go back to reference Stamboulian S, Moutin MJ, Treves S, Pochon N, Grunwald D, Zorzato F, De Waard M, Ronjat M, Arnoult C: Junctate, an inositol 1,4,5-triphosphate receptor associated protein, is present in rodent sperm and binds TRPC2 and TRPC5 but not TRPC1 channels. Dev Biol. 2005, 286 (1): 326-337. 10.1016/j.ydbio.2005.08.006.CrossRefPubMed Stamboulian S, Moutin MJ, Treves S, Pochon N, Grunwald D, Zorzato F, De Waard M, Ronjat M, Arnoult C: Junctate, an inositol 1,4,5-triphosphate receptor associated protein, is present in rodent sperm and binds TRPC2 and TRPC5 but not TRPC1 channels. Dev Biol. 2005, 286 (1): 326-337. 10.1016/j.ydbio.2005.08.006.CrossRefPubMed
64.
go back to reference Suh BC, Hille B: Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol. 2005, 15 (3): 370-378. 10.1016/j.conb.2005.05.005.CrossRefPubMed Suh BC, Hille B: Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol. 2005, 15 (3): 370-378. 10.1016/j.conb.2005.05.005.CrossRefPubMed
65.
go back to reference Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM: Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol. 2004, 274 (2): 426-435. 10.1016/j.ydbio.2004.07.031.CrossRefPubMed Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM: Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol. 2004, 274 (2): 426-435. 10.1016/j.ydbio.2004.07.031.CrossRefPubMed
66.
go back to reference Gkika D, Mahieu F, Nilius B, Hoenderop JG, Bindels RJ: 80K-H as a new Ca2+ sensor regulating the activity of the epithelial Ca2+ channel transient receptor potential cation channel V5 (TRPV5). J Biol Chem. 2004, 279 (25): 26351-26357. 10.1074/jbc.M403801200.CrossRefPubMed Gkika D, Mahieu F, Nilius B, Hoenderop JG, Bindels RJ: 80K-H as a new Ca2+ sensor regulating the activity of the epithelial Ca2+ channel transient receptor potential cation channel V5 (TRPV5). J Biol Chem. 2004, 279 (25): 26351-26357. 10.1074/jbc.M403801200.CrossRefPubMed
67.
go back to reference Hirai M, Shimizu N: Purification of two distinct proteins of approximate Mr 80,000 from human epithelial cells and identification as proper substrates for protein kinase C. Biochem J. 1990, 270 (3): 583-589.PubMedCentralCrossRefPubMed Hirai M, Shimizu N: Purification of two distinct proteins of approximate Mr 80,000 from human epithelial cells and identification as proper substrates for protein kinase C. Biochem J. 1990, 270 (3): 583-589.PubMedCentralCrossRefPubMed
68.
go back to reference Goh KC, Lim YP, Ong SH, Siak CB, Cao X, Tan YH, Guy GR: Identification of p90, a Prominent Tyrosine-phosphorylated Protein in Fibroblast Growth Factor-stimulated Cells, as 80K-H. J Biol Chem. 1996, 271: 5832-5838. 10.1074/jbc.271.10.5832.CrossRefPubMed Goh KC, Lim YP, Ong SH, Siak CB, Cao X, Tan YH, Guy GR: Identification of p90, a Prominent Tyrosine-phosphorylated Protein in Fibroblast Growth Factor-stimulated Cells, as 80K-H. J Biol Chem. 1996, 271: 5832-5838. 10.1074/jbc.271.10.5832.CrossRefPubMed
69.
go back to reference Kanai M, Göke M, Tsunekawa S, Podolsky DK: Signal transduction pathway of human fibroblast growth factor receptor 3. Identification of a novel 66-kDa phosphoprotein. J Biol Chem. 1997, 272 (10): 6621-6628. 10.1074/jbc.272.10.6621.CrossRefPubMed Kanai M, Göke M, Tsunekawa S, Podolsky DK: Signal transduction pathway of human fibroblast growth factor receptor 3. Identification of a novel 66-kDa phosphoprotein. J Biol Chem. 1997, 272 (10): 6621-6628. 10.1074/jbc.272.10.6621.CrossRefPubMed
70.
go back to reference Li YM, Mitsuhashi T, Wojciechowicz D, Shimizu N, Li J, Stitt A, He C, Banerjee D, Vlassara H: Molecular identity and cellular distribution of advanced glycation endproduct receptors: relationship of p60 to OST-48 and p90 to 80K-H membrane proteins. PNAS. 1996, 93 (20): 11047-11052. 10.1073/pnas.93.20.11047.PubMedCentralCrossRefPubMed Li YM, Mitsuhashi T, Wojciechowicz D, Shimizu N, Li J, Stitt A, He C, Banerjee D, Vlassara H: Molecular identity and cellular distribution of advanced glycation endproduct receptors: relationship of p60 to OST-48 and p90 to 80K-H membrane proteins. PNAS. 1996, 93 (20): 11047-11052. 10.1073/pnas.93.20.11047.PubMedCentralCrossRefPubMed
71.
go back to reference Brûlé S, Rabahi F, Faure R, Beckers JF, Silversides DW, Lussier JG: Vacuolar system-associated protein-60: a protein characterized from bovine granulosa and luteal cells that is associated with intracellular vesicles and related to human 80K-H and murine beta-glucosidase II. Biol Reprod. 2000, 62 (3): 642-654. 10.1095/biolreprod62.3.642.CrossRefPubMed Brûlé S, Rabahi F, Faure R, Beckers JF, Silversides DW, Lussier JG: Vacuolar system-associated protein-60: a protein characterized from bovine granulosa and luteal cells that is associated with intracellular vesicles and related to human 80K-H and murine beta-glucosidase II. Biol Reprod. 2000, 62 (3): 642-654. 10.1095/biolreprod62.3.642.CrossRefPubMed
72.
go back to reference Smithers NP, Hodgkinson CP, Cuttle M, Sale GJ: 80K-H acts as a signaling bridge in intact living cells between PKCzeta and the GLUT4 translocation regulator Munc18c. J Recept Signal Transduct Res. 2008, 28 (6): 581-589. 10.1080/10799890802598571.CrossRefPubMed Smithers NP, Hodgkinson CP, Cuttle M, Sale GJ: 80K-H acts as a signaling bridge in intact living cells between PKCzeta and the GLUT4 translocation regulator Munc18c. J Recept Signal Transduct Res. 2008, 28 (6): 581-589. 10.1080/10799890802598571.CrossRefPubMed
73.
go back to reference Kawaai K, Hisatsune C, Kuroda Y, Mizutani A, Tashiro T, Mikoshiba K: 80K-H interacts with inositol 1,4,5-trisphosphate (IP3) receptors and regulates IP3-induced calcium release activity. J Biol Chem. 2009, 284 (1): 372-380. 10.1074/jbc.M805828200.CrossRefPubMed Kawaai K, Hisatsune C, Kuroda Y, Mizutani A, Tashiro T, Mikoshiba K: 80K-H interacts with inositol 1,4,5-trisphosphate (IP3) receptors and regulates IP3-induced calcium release activity. J Biol Chem. 2009, 284 (1): 372-380. 10.1074/jbc.M805828200.CrossRefPubMed
74.
go back to reference Schoeber JP, Hoenderop JG, Bindels RJ: Concerted action of associated proteins in the regulation of TRPV5 and TRPV6. Biochem Soc Trans. 2007, 35 (1): 115-119. 10.1042/BST0350115.CrossRefPubMed Schoeber JP, Hoenderop JG, Bindels RJ: Concerted action of associated proteins in the regulation of TRPV5 and TRPV6. Biochem Soc Trans. 2007, 35 (1): 115-119. 10.1042/BST0350115.CrossRefPubMed
75.
go back to reference Chang Q, Hoefs S, Kemp van der AW, Topala CN, Bindels RJ, Hoenderop JG: The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science. 2005, 310 (5747): 490-493. 10.1126/science.1114245.CrossRefPubMed Chang Q, Hoefs S, Kemp van der AW, Topala CN, Bindels RJ, Hoenderop JG: The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science. 2005, 310 (5747): 490-493. 10.1126/science.1114245.CrossRefPubMed
76.
go back to reference Cohen DM: Regulation of TRP channels by N-linked glycosylation. Semin Cell Dev Biol. 2006, 17 (6): 630-637. 10.1016/j.semcdb.2006.11.007.CrossRefPubMed Cohen DM: Regulation of TRP channels by N-linked glycosylation. Semin Cell Dev Biol. 2006, 17 (6): 630-637. 10.1016/j.semcdb.2006.11.007.CrossRefPubMed
77.
go back to reference Trombetta ES, Simons JF, Helenius A: Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL-containing subunit. J Biol Chem. 1996, 271 (44): 27509-27516. 10.1074/jbc.271.44.27509.CrossRefPubMed Trombetta ES, Simons JF, Helenius A: Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL-containing subunit. J Biol Chem. 1996, 271 (44): 27509-27516. 10.1074/jbc.271.44.27509.CrossRefPubMed
78.
go back to reference Arendt CW, Ostergaard HL: Identification of the CD45-associated 116-kDa and 80-kDa proteins as the alpha- and beta-subunits of alpha-glucosidase II. J Biol Chem. 1997, 272 (20): 13117-13125. 10.1074/jbc.272.20.13117.CrossRefPubMed Arendt CW, Ostergaard HL: Identification of the CD45-associated 116-kDa and 80-kDa proteins as the alpha- and beta-subunits of alpha-glucosidase II. J Biol Chem. 1997, 272 (20): 13117-13125. 10.1074/jbc.272.20.13117.CrossRefPubMed
79.
80.
go back to reference O'Toole CM, Roldan ER, Fraser LR: Protein kinase C activation during progesterone-stimulated acrosomal exocytosis in human spermatozoa. Mol Hum Reprod. 1996, 2 (12): 921-927. 10.1093/molehr/2.12.921.CrossRefPubMed O'Toole CM, Roldan ER, Fraser LR: Protein kinase C activation during progesterone-stimulated acrosomal exocytosis in human spermatozoa. Mol Hum Reprod. 1996, 2 (12): 921-927. 10.1093/molehr/2.12.921.CrossRefPubMed
81.
go back to reference Sousa M, Barros A, Mendoza C, Tesarik J: Effects of protein kinase C activation and inhibition on sperm-, thimerosal-, and ryanodine-induced calcium responses of human oocytes. Mol Hum Reprod. 1996, 2 (9): 699-708. 10.1093/molehr/2.9.699.CrossRefPubMed Sousa M, Barros A, Mendoza C, Tesarik J: Effects of protein kinase C activation and inhibition on sperm-, thimerosal-, and ryanodine-induced calcium responses of human oocytes. Mol Hum Reprod. 1996, 2 (9): 699-708. 10.1093/molehr/2.9.699.CrossRefPubMed
82.
go back to reference Liu DY, Baker HW: Protein kinase C plays an important role in the human zona pellucida-induced acrosome reaction. Mol Hum Reprod. 1997, 3 (12): 1037-1043. 10.1093/molehr/3.12.1037.CrossRefPubMed Liu DY, Baker HW: Protein kinase C plays an important role in the human zona pellucida-induced acrosome reaction. Mol Hum Reprod. 1997, 3 (12): 1037-1043. 10.1093/molehr/3.12.1037.CrossRefPubMed
83.
go back to reference Breitbart H: Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol Cell Endocrinol. 2002, 187 (1-2): 139-144. 10.1016/S0303-7207(01)00704-3.CrossRefPubMed Breitbart H: Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol Cell Endocrinol. 2002, 187 (1-2): 139-144. 10.1016/S0303-7207(01)00704-3.CrossRefPubMed
84.
go back to reference Breitbart H: Signaling pathways in sperm capacitation and acrosome reaction. Cell Mol Biol (Noisy-le-grand). 2003, 49 (3): 321-327. Breitbart H: Signaling pathways in sperm capacitation and acrosome reaction. Cell Mol Biol (Noisy-le-grand). 2003, 49 (3): 321-327.
85.
go back to reference Naaby-Hansen S, Waterfield MD, Cramer R: Proteomics--Post-genomic cartography to understand cell function. Trends Pharmacol Sci. 2001, 22 (7): 376-384. 10.1016/S0165-6147(00)01663-1.CrossRefPubMed Naaby-Hansen S, Waterfield MD, Cramer R: Proteomics--Post-genomic cartography to understand cell function. Trends Pharmacol Sci. 2001, 22 (7): 376-384. 10.1016/S0165-6147(00)01663-1.CrossRefPubMed
Metadata
Title
Identification of calcium-binding proteins associated with the human sperm plasma membrane
Authors
Soren Naaby-Hansen
Alan Diekman
Jagathpala Shetty
Charles J Flickinger
Anne Westbrook
John C Herr
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-8-6

Other articles of this Issue 1/2010

Reproductive Biology and Endocrinology 1/2010 Go to the issue