Skip to main content

Advertisement

Log in

Annexin A2 and S100A10 in the mammalian oviduct

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

In many mammals, upon entry into the female reproductive tract, a subpopulation of sperm is stored in the oviduct forming a functional reservoir. In the oviducts of pig and cow, Annexin A2 (AnxA2) has been linked to the binding of sperm. This protein may exist as a monomer or bound to S100A10 and both forms are associated with different biological functions. S100A10 has not yet been reported in the oviduct. The objective of this work is to analyze for the presence of S100A10 in the oviduct and to advance the study of AnxA2 and S100A10 in this organ. This work shows the presence of both proteins, AnxA2 and S100A10, in the oviduct of human, pig, cow, cat, dog and rabbit. At least in pig, AnxA2 is found devoid of S100A10 in the outer surface of the apical plasma membrane of oviductal epithelial cells, indicating that it binds to sperm as a monomer or in association with proteins different from S100A10. In the apical cytoplasm of pig oviductal epithelial cells, AnxA2 is associated with S100A10. In primary culture of porcine oviductal cells, the expression of ANXA2 is increased by progesterone, while the expression of S100A10 is increased by progesterone and estradiol. The widespread detection of both proteins in the oviduct of mammals indicates a probable conserved function in this organ. In summary, S100A10 and AnxA2 are widespread in the mammalian oviduct but AnxA2 binds sperm in vivo devoid of S100A10 and may be related to reservoir formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen KL, Fonseca FV, Betapudi V, Willard B, Zhang J, McCrae KR (2012) A novel pathway for human endothelial cell activation by antiphospholipid/anti-β2 glycoprotein I antibodies. Blood 119(3):884–893

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ayala-Sanmartin J, Zibouche M, Illien F, Vincent M, Gallay J (2008) Insight into the location and dynamics of the annexin A2 N-terminal domain during Ca2 + −induced membrane bridging. Biochim Biophys Acta 1778:472–482

    Article  CAS  PubMed  Google Scholar 

  • Baranda-Avila N, Cardoso-Rangel ME, Cerbón M, Camacho-Arroyo I, Mendoza-Rodríguez CA, Villaseñor-Gaona H, Anzaldúa-Arce SR (2010) Differential expression of estrogen receptor alpha gene in the ampullae and isthmus regions of the rabbit oviduct during early pregnancy. Anim Reprod Sci 121(3–4):286–293

    Article  CAS  PubMed  Google Scholar 

  • Barberini F, Correr S, De Santis F, Motta PM (1991) The epithelium of the rabbit vagina: a microtopographical study by light, transmission and scanning electron microscopy. Arch Histol Cytol 54:365–378

  • Bharadwaj A, Bydoun M, Holloway R, Waisman D (2013) Annexin A2 heterotetramer: structure and function. Int J Mol Sci 14:6259–6305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Caballero J, Gervasi MG, Veiga MF, Dalvit GC, Perez-Martínez S, Cetica PD, Vazquez-Levin MH (2014) Epithelial cadherin is present in bovine oviduct epithelial cells and gametes, and is involved in fertilization-related events. Theriogenology 81:1189–1206

    Article  CAS  PubMed  Google Scholar 

  • Chatdarong K, Lohachit C, Linde-Forsberg C (2004) Distribution of spermatozoa in the female reproductive tract of the domestic cat in relation to ovulation induced by natural mating. Theriogenology 62(6):1027–1034

    Article  PubMed  Google Scholar 

  • Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450(3):191–231

    Article  CAS  PubMed  Google Scholar 

  • Drücker P, Pejic M, Galla HJ, Gerke V (2013) Lipid segregation and membrane budding induced by the peripheral membrane binding protein annexin A2. J Biol Chem 288(34):24764–24776

    Article  PubMed Central  PubMed  Google Scholar 

  • England GC, Burgess CM, Clutterbuck AL, Freeman SL (2013) Epithelial surface changes and spermatozoa storage in the reproductive tract of the bitch. Vet J 195(2):185–191

    Article  CAS  PubMed  Google Scholar 

  • Erikson E, Tomasiewicz HG, Erikson RL (1984) Biochemical characterization of a 34-kilodalton normal cellular substrate of pp60v-src and an associated 6-kilodalton protein. Mol Cell Biol 4:77–85

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371

    Article  CAS  PubMed  Google Scholar 

  • Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Nat Rev Mol Cell Biol 6:449–461

    Article  CAS  PubMed  Google Scholar 

  • Grieve AG, Moss SE, Hayes MJ (2012) Annexin A2 at the interface of actin and membrane dynamics: a focus on its roles in endocytosis and cell polarization. Int J Cell Biol 2012:852430

    Article  PubMed Central  PubMed  Google Scholar 

  • Gwathmey TM, Ignotz GG, Mueller JL, Manjunath P, Suarez SS (2006) Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct. Biol Reprod 75(4):501–507

    Article  CAS  PubMed  Google Scholar 

  • He KL, Deora AB, Xiong H, Ling Q, Weksler BB, Niesvizky R, Hajjar KA (2008) Endothelial cell annexin A2 regulates polyubiquitination and degradation of its binding partner S100A10/p11. J Biol Chem 283:19192–19200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hess AP, Nayak NR, Giudice LC (1994) Chapter 9. In: Knobil and Neill (ed) Physiology of Reproduction. Raven Press, New York, USA, pp 341–345 and pp 337–381

  • Holt W, Elliott RM, Fazeli A, Satake N, Watson PF (2005) Validation of a strategy for studying surface-exposed proteins involved in porcine sperm-oviduct contact interaction. Reprod Fert Dev 17:683–692

    Article  CAS  Google Scholar 

  • Hunter RH (1984) Pre-ovulatory arrest and peri-ovulatory redistribution of competent spermatozoa in the isthmus of the pig oviduct. J Reprod Fertil 72:203–211

    Article  CAS  PubMed  Google Scholar 

  • Hunter RH, Wilmut I (1984) Sperm transport in the cow: peri-ovulatory redistribution of viable cells within the oviduct. Reprod Nutr Dev 24:597–608

    Article  CAS  PubMed  Google Scholar 

  • Hunter RH, Barwise L, King R (1982) Sperm transport, storage and release in the sheep oviduct in relation to the time of ovulation. Br Vet J 138:225–232

    CAS  PubMed  Google Scholar 

  • Ignotz GG, Cho MY, Suarez SS (2007) Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol Reprod 77(6):906–913

    Article  CAS  PubMed  Google Scholar 

  • Illien F, Finet S, Lambert O, Ayala-Sanmartin J (2010) Different molecular arrangements of the tetrameric annexin 2 modulate the size and dynamics of membrane aggregation. Biochim Biophys Acta 1798:1790–1796

    Article  CAS  PubMed  Google Scholar 

  • Jung Y, Wang J, Song J, Shiozawa Y, Wang J, Havens A, Wang Z, Sun YX, Emerson SG, Krebsbach PH, Taichman RS (2007) Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation. Blood 110(1):82–90

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Liberda J, Manásková P, Prelovská L, Tichá M, Jonáková V (2006) Saccharide-mediated interactions of boar sperm surface proteins with components of the porcine oviduct. J Reprod Immunol 71(2):112–125

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Myrvang HK, Dekker LV (2015) Annexin A2 complexes with S100 proteins: structure, function and pharmacological manipulation. Br J Pharmacol 172:1664–1676

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Luo M, Hajjar KA (2013) Annexin A2 system in human biology: cell surface and beyond. Semin Thromb Hemost 39(4):338–346

    Article  CAS  PubMed  Google Scholar 

  • Madureira PA, O'Connell PA, Surette AP, Miller VA, Waisman DM (2012) The biochemistry and regulation of S100A10: a multifunctional plasminogen receptor involved in oncogenesis. J Biomed Biotech. doi:10.1155/2012/353687

    Google Scholar 

  • Marini PE, Cabada MO (2003) One step purification and biochemical characterization of a spermatozoa-binding protein from porcine oviductal epithelial cells. Mol Reprod Dev 66:383–390

    Article  CAS  PubMed  Google Scholar 

  • Mariscal DV, Bergfeld EGM, Cupp AS, Kojima FN, Fike KE, Sánchez T, Wehrman ME, Johnson RK, Kittok RJ, Ford JJ, Kinder JE (1998) Concentrations of gonadotropins, estradiol and progesterone in sows selected on an index of ovulation rate and embryo survival. Anim Reprod Sci 54:31–43

    Article  CAS  PubMed  Google Scholar 

  • Mburu JN, Rodriguez-Martinez H, Einarsson S (1997) Changes in sperm ultrastructure and localisation in the porcine oviduct around ovulation. Anim Reprod Sci 47:137–148

    Article  CAS  PubMed  Google Scholar 

  • Motulsky H (1995) Intuitive biostatistics. Oxford University Press, New York

    Google Scholar 

  • Myrvang HK, Guo LC, Dekker LV (2013) Protein interactions between surface annexin A2 and S100A10 mediate adhesion of breast cancer cells to microvascular endothelial cells. FEBS Lett 587(19):3210–3215

    Article  CAS  PubMed  Google Scholar 

  • Pacey AA, Hill CJ, Scudamore IW, Warren MA, Barratt CL, Cooke ID (1995) The interaction in vitro of human spermatozoa with epithelial cells from the human uterine (fallopian) tube. Hum Reprod 10:360–366

    CAS  PubMed  Google Scholar 

  • Pacey AA, Freeman SL, England GC (2000) Contact of dog spermatozoa with homologous uterine tube epithelium prolongs flagellar activity in relation to the stage of the estrous cycle. Theriogenology 54(1):109–118

    Article  CAS  PubMed  Google Scholar 

  • Rescher U, Gerke V (2004) Annexins—unique membrane binding proteins with diverse functions. J Cell Sci 117:2631–2639

    Article  CAS  PubMed  Google Scholar 

  • Singh P, Wu H, Clark C, Owlia A (2007) Annexin II binds progastrin and gastrin-like peptides, and mediates growth factor effects of autocrine and exogenous gastrins on colon cancer and intestinal epithelial cells. Oncogene 26(3):425–440

    Article  CAS  PubMed  Google Scholar 

  • Smith TT, Yanagimachi R (1991) Attachment and release of spermatozoa from the caudal isthmus of the hamster oviduct. J Reprod Fertil 91:567–573

    Article  CAS  PubMed  Google Scholar 

  • Su SC, Maxwell SA, Bayless KJ (2010) Annexin 2 regulates endothelial morphogenesis by controlling AKT activation and junctional integrity. J Biol Chem 285:40624–40634

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suarez SS (1987) Sperm transport and motility in the mouse oviduct: observations in situ. Biol Reprod 36:203–210

    Article  CAS  PubMed  Google Scholar 

  • Suarez S, Redfern K, Raynor P, Martin F, Phillips DM (1991) Attachment of boar sperm to mucosal explants of oviduct in vitro: possible role in formation of a sperm reservoir. Biol Reprod 44(6):998–1004

    Article  CAS  PubMed  Google Scholar 

  • Swisher JF, Burton N, Bacot SM, Vogel SN, Feldman GM (2010) Annexin A2 tetramer activates human and murine macrophages through TLR4. Blood 115(3):549–558

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Talevi R, Gualtieri R (2010) Molecules involved in sperm-oviduct adhesion and release. Theriogenology 73(6):796–801

    Article  CAS  PubMed  Google Scholar 

  • Teijeiro JM, Marini PE (2012) Apical membranes prepared by peeling from whole porcine oviducts interact with homologous sperm. Cell Tissue Res 348(1):213–223

    Article  CAS  PubMed  Google Scholar 

  • Teijeiro JM, Ignotz GG, Marini PE (2009) Annexin A2 is involved in pig (Sus scrofa) sperm–oviduct interaction. Mol Reprod Develop 76:334–341

    Article  CAS  Google Scholar 

  • Thomas PG, Ball BA, Brinsko SP (1994) Interaction of equine spermatozoa with oviduct epithelial cell explants is affected by estrous cycle and anatomic origin of explant. Biol Reprod 51(2):222–228

    Article  CAS  PubMed  Google Scholar 

  • Töpfer-Petersen E, Wagner A, Friedrich J, Petrunkina A, Ekhlasi-Hundrieser M, Waberski D, Drommer W (2002) J Exp Zool 292(2):210–215

    Article  PubMed  Google Scholar 

  • Tummaruk P, Tienthai P (2010) Number of spermatozoa in the crypts of the sperm reservoir at about 24 h after a low-dose intrauterine and deep intrauterine insemination in sows. Reprod Domest Anim 45(2):208–213

    Article  CAS  PubMed  Google Scholar 

  • Valapala M, Maji S, Borejdo J, Vishwanatha JK (2014) Cell surface translocation of annexin A2 facilitates glutamate-induced extracellular proteolysis. J Biol Chem 289(23):15915–15926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vedeler A, Hollås H, Grindheim AK, Raddum AM (2012) Multiple roles of annexin A2 in post-transcriptional regulation of gene expression. Curr Protein Pept Sci 13(4):401–412

    Article  CAS  PubMed  Google Scholar 

  • Waisman DM (1995) Annexin II tetramer: structure and function. Mol Cell Biochem 149–150:301–322

    Article  PubMed  Google Scholar 

  • Yamada A, Irie K, Hirota T, Ooshio T, Fukuhara A, Takai Y (2005) Involvement of the annexin II-S100A10 complex in the formation of E-cadherin-based adherens junctions in Madin-Darby canine kidney cells. J Biol Chem 280:6016–6027

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Wu WX (2007) Separate and synergistic effect of progesterone and estradiol on induction of annexin 2 and its interaction protein p11 in pregnant sheep myometrium. J Mol Endocrinol 38(4):441–454

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Gerke for HH7 anti-AnxA2 antibodies and Dr. Melle for anti-S100A10 antibodies. We also thank Frigorífico Paladini SA for providing gilt oviducts and IMUSA, Rosario for pet oviducts.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia Estela Marini.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Teijeiro, J.M., Roldán, M.L. & Marini, P.E. Annexin A2 and S100A10 in the mammalian oviduct. Cell Tissue Res 363, 567–577 (2016). https://doi.org/10.1007/s00441-015-2266-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-015-2266-9

Keywords

Navigation