Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: Association with oviductal exosomes and uptake in sperm

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Al Dossary, Amal A ^a   Strehler, Emanuel E ^b   Martin DeLeon, Patricia A ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTIGENS, CD9; BIOLOGICAL MARKERS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CYTOPLASMIC VESICLES; ESTRUS; EXOSOMES; FEMALE; FERTILITY; GENE EXPRESSION; ISOENZYMES; MALE; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; OVIDUCTS; PROTEIN TRANSPORT; REPRODUCTION; SPERMATOZOA; UTERUS; VAGINA;

EID: 84893581157     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080181     Document Type: Article

References (40)

1. Rodriguez-Martinez H (2007) Role of the oviduct in sperm capacitation. Theriogenology 68 Suppl 1: S138-S146. doi:10.1016/j.theriogenology.2007.03.018. PubMed: 17452049.
2. de Lamirande E, Leclerc P, Gagnon C (1997) Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 3: 175-194. doi:10.1093/molehr/3.3.175. PubMed: 9237244. (Pubitemid 127509475)
3. Wennemuth G, Babcock DF, Hille B (2003) Calcium clearance mechanisms of mouse sperm. J Gen Physiol 122: 115-128. doi:10.1085/jgp.200308839. PubMed: 12835474. (Pubitemid 36859135)
4. Okunade GW, Miller ML, Pyne GJ, Sutliff RL, O'Connor KT et al. (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. J Biol Chem 279: 33742-33750. doi:10.1074/jbc.M404628200. PubMed: 15178683. (Pubitemid 39063023)
5. Schuh K, Cartwright EJ, Jankevics E, Bundschu K, Liebermann J et al. (2004) Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility. J Biol Chem 279: 28220-28226. doi:10.1074/jbc.M312599200. PubMed: 15078889. (Pubitemid 38900098)
6. Aravindan RG, Fomin VP, Naik UP, Modelski MJ, Naik MU et al. (2012) CASK interacts with PMCA4b and JAM-A on the mouse sperm flagellum to regulate Ca2+ homeostasis and motility. J Cell Physiol 227: 3138-3150. doi:10.1002/jcp.24000. PubMed: 22020416.
7. Patel R, Al-Dossary AA, Stabley DL, Barone C, Galileo DS et al. (2013) Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation. Biol Reprod 89: 6. doi:10.1095/biolreprod.113.108712. PubMed: 23699388.
8. Yeung CH, Cooper TG (2002) Acquisition and development of sperm motility upon maturation in the epididymis.; B RobaireB.T. Hinton. New Kluwer: York Academic/Plenum Publishers.
9. Coy P, García-Vázquez FA, Visconti PE, Avilés M (2012) Roles of the oviduct in mammalian fertilization. Reproduction 144: 649-660. doi:10.1530/REP-12-0279. PubMed: 23028122.
10. Kirchhoff C, Pera I, Derr P, Yeung CH, Cooper T (1997) The molecular biology of the sperm surface. Post-testicular membrane remodelling. Adv Exp Med Biol 424: 221-232. doi:10.1007/978-1-4615-5913-9-40. PubMed: 9361796. (Pubitemid 27479694)
11. Zhang H, Martin-DeLeon PA (2003) Mouse Spam1 (PH-20) is a multifunctional protein: evidence for its expression in the female reproductive tract. Biol Reprod 69: 446-454. doi:10.1095/biolreprod.102.013854. PubMed: 12672666. (Pubitemid 36885947)
12. Griffiths GS, Galileo DS, Reese K, Martin-Deleon PA (2008) Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Mol Reprod Dev 75: 1627-1636. doi:10.1002/mrd.20907. PubMed: 18384048.
13. Caride AJ, Filoteo AG, Penniston JT, Strehler EE (2007) The plasma membrane Ca2+ pump isoform 4a differs from isoform 4b in the mechanism of calmodulin binding and activation kinetics: implications for Ca2+ signaling. J Biol Chem 282: 25640-25648. doi:10.1074/jbc.M701129200. PubMed: 17595168. (Pubitemid 47372818)
14. Brandenburger T, Strehler EE, Filoteo AG, Caride AJ, Aumüller G et al. (2011) Switch of PMCA4 splice variants in bovine epididymis results in altered isoform expression during functional sperm maturation. J Biol Chem 286: 7938-7946. doi:10.1074/jbc.M110.142836. PubMed: 21187283.
15. Filoteo AG, Elwess NL, Enyedi A, Caride A, Aung HH et al. (1997) Plasma membrane Ca2+ pump in rat brain. Patterns of alternative splices seen by isoform-specific antibodies. J Biol Chem 272: 23741-23747. doi:10.1074/jbc.272. 38.23741. PubMed: 9295318. (Pubitemid 27410950)
16. Chen H, Griffiths G, Galileo DS, Martin-DeLeon PA (2006) Epididymal SPAM1 is a marker for sperm maturation in the mouse. Biol Reprod 74: 923-930. doi:10.1095/biolreprod.105.048587. PubMed: 16436526.
17. Goldman JM, Murr AS, Cooper RL (2007) The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol 80: 84-97. doi:10.1002/bdrb.20106. PubMed: 17342777. (Pubitemid 46762318)
18. Griffiths GS, Galileo DS, Aravindan RG, Martin-DeLeon PA (2009) Clusterin facilitates exchange of glycosyl phosphatidylinositol-linked SPAM1 between reproductive luminal fluids and mouse and human sperm membranes. Biol Reprod 81: 562-570. doi:10.1095/biolreprod.108.075739. PubMed: 19357365.
19. Pisitkun T, Shen RF, Knepper MA (2004) Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 101: 13368-13373. doi:10.1073/pnas.0403453101. PubMed: 15326289. (Pubitemid 39209672)
20. Caballero JN, Frenette G, Belleannée C, Sullivan R (2013) CD9-Positive Microvesicles Mediate the Transfer of Molecules to Bovine Spermatozoa during Epididymal Maturation. PLOS ONE 8: e65364. doi:10.1371/journal.pone.0065364. PubMed: 23785420.
21. Théry C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: 569-579. PubMed: 12154376. (Pubitemid 37328732)
22. Andrews JC, Nolan JP, Hammerstedt RH, Bavister BD (1994) Role of zinc during hamster sperm capacitation. Biol Reprod 51: 1238-1247. doi:10.1095/biolreprod51.6.1238. PubMed: 7888501. (Pubitemid 24354284)
23. Suarez SS, Pacey AA (2006) Sperm transport in the female reproductive tract. Hum Reprod Update 12: 23-37. PubMed: 16272225. (Pubitemid 43013744)
24. Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G et al. (2007) All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci U S A 104: 1219-1223. doi:10.1073/pnas.0610286104. PubMed: 17227845. (Pubitemid 46183985)
25. Driscoll MD, Sathya G, Muyan M, Klinge CM, Hilf R et al. (1998) Sequence requirements for estrogen receptor binding to estrogen response elements. J Biol Chem 273: 29321-29330. doi:10.1074/jbc.273.45.29321. PubMed: 9792632. (Pubitemid 28509931)
26. Belan PV, Gerasimenko OV, Tepikin AV, Petersen OH (1996) Localization of Ca2+ extrusion sites in pancreatic acinar cells. J Biol Chem 271: 7615-7619. doi:10.1074/jbc.271.13.7615. PubMed: 8631796.
27. Lee MG, Xu X, Zeng W, Diaz J, Kuo TH et al. (1997) Polarized expression of Ca2+ pumps in pancreatic and salivary gland cells. Role in initiation and propagation of [Ca2+]i waves. J Biol Chem 272: 15771-15776. doi:10.1074/jbc.272. 25.15771. PubMed: 9188473. (Pubitemid 27265553)
28. Post H, Wiche R, Sen PC, Hoffbauer G, Albrecht M et al. (2002) Identification of a plasma membrane Ca2+-ATPase in epithelial cells and aposomes of the rat coagulating gland. Prostate 52: 159-166. doi:10.1002/pros.10109. PubMed: 12111707. (Pubitemid 34663328)
29. Reinhardt TA, Filoteo AG, Penniston JT, Horst RL (2000) Ca(2+)-ATPase protein expression in mammary tissue. Am J Physiol Cell Physiol 279: C1595-C1602. PubMed: 11029307.
30. Griffiths GS, Miller KA, Galileo DS, Martin-DeLeon PA (2008) Murine SPAM1 is secreted by the estrous uterus and oviduct in a form that can bind to sperm during capacitation: acquisition enhances hyaluronic acid-binding ability and cumulus dispersal efficiency. Reproduction 135: 293-301. doi:10.1530/REP-07- 0340. PubMed: 18299422. (Pubitemid 351405036)
31. Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593. doi:10.1038/nri2567. PubMed: 19498381.
32. Hermo L, Jacks D (2002) Nature's ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev 63: 394-410. doi:10.1002/mrd.90023. PubMed: 12237956.
33. Saez F, Frenette G, Sullivan R (2003) Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J Androl 24: 149-154. PubMed: 12634297.
34. Frenette G, Sullivan R (2001) Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev 59: 115-121. doi:10.1002/mrd.1013. PubMed: 11335953.
35. Strehler EE, Filoteo AG, Penniston JT, Caride AJ (2007) Plasmamembrane Ca(2+) pumps: structural diversity as the basis for functional versatility. Biochem Soc Trans 35: 919-922. doi:10.1042/BST0350919. PubMed: 17956246. (Pubitemid 350206396)
36. Barratt CL, Cooke ID (1991) Sperm transport in the human female reproductive tract - a dynamic interaction. Int J Androl 14: 394-411. doi:10.1111/j.1365-2605.1991.tb01268.x. PubMed: 1761321.
37. Morales P, Palma V, Salgado AM, Villalon M (1996) Sperm interaction with human oviductal cells in vitro. Hum Reprod 11: 1504-1509. doi:10.1093/ oxfordjournals.humrep.a019426. PubMed: 8671493. (Pubitemid 26335102)
38. Ren D, Navarro B, Perez G, Jackson AC, Hsu S et al. (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413: 603-609. doi:10.1038/35098027. PubMed: 11595941. (Pubitemid 32964054)
39. Shao M, Ghosh A, Cooke VG, Naik UP, Martin-DeLeon PA (2008) JAM-A is present in mammalian spermatozoa where it is essential for normal motility. Dev Biol 313: 246-255 (Pubitemid 350298312)
40. Boilard M, Bailey J, Collin S, Dufour M, Sirard MA (2002) Effect of bovine oviduct epithelial cell apical plasma membranes on sperm function assessed by a novel flow cytometric approach. Biol Reprod 67: 1125-1132. doi:10.1095/biolreprod67.4.1125. PubMed: 12297527.