Submit
Search
Submit
Menu

  • Information

  • References

  • Contents

  • [1]Yanagimachi R. Mammalian fertilization. In: The Physiology of Reproduction, 2nd ed. Eds. E. Knobil, JD Neill New York, Raven Press; 194-317 (1994)

  • [2]Zhang H, Martin-DeLeon PA: Mouse Spam1 (PH-20) is a Multifunctional Protein: Evidence for Its Expression in the Female Tract. Biol Reprod 69:446-454 (2003)

  • [3]King RS, Anderson SH, Killian GJ: Effect of bovine oviductal estrus-associated protein on the ability of sperm to capacitate and fertilize oocytes. J Androl 15:468-478 (1994)

  • [4]Boatman DE, Magnoni GE: Identification of a sperm penetration factor in the oviduct of the golden hamster. Biol Reprod 52, 199-207 (1995)

  • [5]Kan F, Esperanza P: Surface mapping of binding of oviductin to the plasma membrane of golden hamster spermatozoa during in vitro capacitation and acrosome reaction. Mol Reprod Dev 73:756-766 (2006)

  • [6]Deng X, He Y, Martin-DeLeon PA: Mouse Spam1 (PH-20): Evidence for Its Expression in the Epididymis and for a New Category of Spermatogenic Expressed Genes. J Androl 21:822-832 (2000)

  • [7]Zhang H, Martin-DeLeon PA: Mouse Epididymal Spam1 (Ph-20) is released in vivo and in vitro, and Spam1 is differentially regulated in testis and epididymis. Biol Reprod 65:1586-1593 (2001)

  • [8]Zhang H, Martin-DeLeon PA: Mouse Epididymal Spam1 (PH-20) is Released in the Luminal Fluid With its Lipid Anchor. J Androl 1:51-58 (2003)

  • [9]Chen H, Griffiths GS, Galileo DS, Martin-DeLeon PA: Epididymal SPAM1 is a marker for Sperm Maturation in the Mouse. Biol Reprod 74:923-930 (2006)

  • [10]Zhang H, Morales CR, Badran H, El-Alfy M, Martin-DeLeon, PA: Expression of Spam1 (PH-20) in the extratesticular duct and accessory organs of the mouse: A possible role in sperm fluid reabsorption. Biol Reprod 71:1101-1107 (2004)

  • [11]Griffiths GS, Reese KL, Galileo DS, Martin-DeLeon PA: 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 (2008)

  • [12]Sullivan R, Saez F, Girouard J, Frenette G: Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis 35:1-10 (2005)

  • [13]Fabiani R, Johansson L, Lundkvist Ö, Ulmsten U, Ronquist G: Promotive effect by prostasomes on normal human spermatozoa exhibiting no forward motility due to buffer washings. Eur J Obstet Gynecol Reprod Biol 57:181-188 (1994)

  • [14]Thery C, Ostrowski, M Segura E: Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581-593 (2009)

  • [15]Thery C, Zitvogel L, Amigorena S: Exosomes: composition, biogenesis and function. Nat Rev Immunol 2:569-579 (2002)

  • [16]Masyuk AI, Huang BQ, Ward CJ, Gradilone SA, Banales JM, Masyuk TV, Radtke B, Splinter PL, LaRusso NF: Biliary exosomes influence cholangiocyte regulatory mechanisms and proliferation through interaction with primary cilia. Am J Physiol Gastrointest Liver Physiol 299: G990-999 (2010)

  • [17]Pisitkun T, Shen RF, Knepper MA: Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sc USA 101:13368-13373 (2004)

  • [18]AL-Dossary AA, Strehler EE, Martin-DeLeon PA: Expression and Secretion of Plasma Membrane Ca2+-ATPase4a (PMCA4a) during Murine Estrus: Association with Oviductal Exosomes and Uptake in Sperm. PLoS One 8: e80181 (2013)

  • [19]Griffiths GS, Miller KA, Galileo DS, Martin-DeLeon, PA: SPAM1 is secreted by the estrous murine uterus and oviduct in a form which can bind to sperm during capacitation: Acquisition enhances hyaluronic acid-binding ability and cumulus penetration efficiency. Reproduction 135:293-301 (2008)

  • [20]Habiba MA, James RF, Bell SC, and Al-Azzawi F: Identification of a cycle-modulated 200-kDa endometrial antigen by a monoclonal antibody LDS60. J Immunol Methods 227:65-73 (1999)

  • [21]Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, Salamonsen LA: Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One 8:e58502 (2013)

  • [22]Turturici G, Tinnirello R, Sconzo G, Geraci F: Extracellular membrane vesicles as a mechanism of cell-to-cell communication: advantages and disadvantages. Am J Physiol. Cell Physiol 306: C621-633 (2014)

  • [23]Meckes DG Jr, Raab-Traub N: Microvesicles and viral infection. J Virol 85:12844-54 (2011)

  • [24]Hermo L, Jacks D: Nature’s ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev 63:394-410 (2002)

  • [25]Nickel W: The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochemistry 270:2109-2119 (2003)

  • [26]Hermo L, Oko R, Morales CR: Secretion and endocytosis in the male reproductive tract: A role in sperm maturation. Int Rev Cytol 154:106-189 (1994)

  • [27]Patel R, AL-Dossary AA, Stabley DL, Barone C, Galileo D, Strehler EE, Martin-DeLeon PA: Plasma membrane Ca2+- ATPase in Murine Epididymis: Secretion of Splice variants in the luminal Fluid and a Role in Sperm maturation. Biol Reprod 89:1-11 (2013)

  • [28]Okunade GW, Miller ML, Pyne GJ, Sutliff RL, O’Connor KT, Neumann JC, Andringa A, Miller DA, Prasad V, Doetschman T, Paul RJ, Shull GE: 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 (2004)

  • [29]Schuh K, Cartwright EJ, Jankevics E, Bundschu K, Liebermann J, Williams JC, Armesilla AL, Emerson M, Oceandy D, Knobeloch KP, Neyses L: Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility. J Biol Chem 279:28220-28226 (2004)

  • [30]Griffiths GS, Miller KA, Galileo DS, Martin-DeLeon PA: SPAM1 is secreted by the estrous murine uterus and oviduct in a form which can bind to sperm during capacitation: Acquisition enhances hyaluronic acid-binding ability and cumulus penetration efficiency. Reproduction 135:293-301 (2008)

  • [31]Aalberts M, Stout TAE, Stoorvogel W: Prostasomes: extracellular vesicles from the prostate. Reproduction 147: R1-R14 (2014)

  • [32]Griffiths GS, Galileo DS, Aravindan RG, Martin-DeLeon PA: Clusterin facilitates exchange of glycosyl-phosphosphatidylinositol-linked SPAM1 between reproductive luminal fluids and mouse and human sperm membranes. Biol Reprod 81:562-570 (2009)

  • [33]Martin-DeLeon PA: Germ-cell hyaluronidases: Their Roles in Sperm Function. Intl J. Androl 34:306-318 (2010)

  • [34]Kirchoff C, Pera I, Derr P, Yeung CH, Cooper T: The molecular biology of the sperm surface: Post-testicular membrane remodeling. Adv Exp Med Biol 424:221-232 (1997)

  • [35]Wennemuth G, Babcock DF, Hille B: Calcium clearance mechanisms of mouse sperm J Gen Physiol 122:115-128 (2003)

  • [36]de Lamirande E, Leclerc P, Gagnon C: Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 3:175-194 (1997)

  • [37]Fraser LR: Minimum and maximum extracellular Ca2+ requirements during mouse sperm capacitation and fertilization J Reprod Fertil 81:77-89 (1987)

  • [38]Oliphant G, Reynolds AB, Thomas TS: Sperm surface components involved in the control of the acrosome reaction. Am J Anat 174:269-283 (1985)

  • [39]Schwarz A, Wennemuth G, Post H, Brandenburger T, Aumüller G, Wilhelm B: Vesicular transfer of membrane components to bovine epididymal spermatozoa. Cell Tissue Res 353:549-561 (2013)

  • [40]Fraser LR: Ca+ requirements for capacitation and acrosomal exocytosis in mammalian sperm. Intl. Rev Cytol 149:1-46 (1994)

  • [41]Adeoya-Osiguwa SA, Fraser LR: Evidence for Ca2+-Dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm. Mol Reprod Dev 44; 111-120 (1996)

  • [42]Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE: Extracellular vesicles in luminal fluid of the ovine uterus. PLoS One 9:e90913 (2014)

  • [43]Center for Disease Control (CDC) 2012 Preliminary ART data.

  • [44]Caballero J, Frenette G, Sullivan R: Post testicular sperm maturational changes in the bull: important role of the epididymosomes and prostasomes. Vet Med Intl 2011:757194 13 pages, (2011)

  • [45]Arienti G, Carlini E, Palmerini CA: Fusion of human sperm to prostasomes at acidic pH. J Memb Biol 155:89-94 (1997)

  • [46]Carlini E, Palminerini CA, Cosmi EV, Arenti G: Fusion of sperm with prostasomes: Effects on membrane fluidity. Arch Biochem Biophys 343:6-12 (1997)

  • [47]AL-Dossary AA, Caplan JL, Martin-DeLeon PA: The Contribution of Exosomes/Microvesicles to the Sperm Proteome. Mol Reprod Dev 82:79 (2015)

  • [48]Thimon V, Frenette G, Saez F, Thabet M, Sullivan R: Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum Reprod 23:1698-1707 (2008)

  • [49]Girouard J, Frenette G, Sullivan R: Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymis. Intl J Androl 34: e475-486 (2011)

  • [50]Hemler ME: Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Ann Review Cell Dev Biol 19:397-422 (2003)

  • [51]Al-Dossary AA, Bathala P, Caplan JL, Martin-DeLeon PA: Oviductosome-Sperm Membrane Interaction in Cargo Delivery: Detection of Fusion and Underlying Molecular Players using 3D Super-Resolution Structured Illumination Microscopy (SR-SIM) J Biol Chem 290:

  • [52]Ilangumaran S, Robinson PJ, Hossali DC: Transfer of exogenous glycosyl-phosphatidylinositol (GPI)-linked molecules to plasma membranes. Trends Cell Biol 6:163-167 (1996)

  • [53]Tian T, Zhu Y-L, Zhou Y-Y, Liang G-F, Wang Y-Y, Hu F-H, Xiao, Z-D: Exosome uptake through Clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem 289:22258-22267 (2014)

  • [54]Oko R, Hermo L, Chan PT, Fazel A, Bergeron JJ: The cytoplasmic droplet of rat epididymal spermatozoa contains macular elements with Golgi characteristics. J Cell Biol 123:809-821 (1993)

Article Metrics

  • Information

  • Download

  • Contents

Frontiers in Bioscience-Scholar (FBS) is published by IMR Press from Volume 13 Issue 1 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.

1 Jan 2016Review

Uterosomes: Exosomal cargo during the estrus cycle and interaction with sperm

Patricia A. Martin-DeLeon 1,*
Affiliation
Article Info

1 219 Mckinly Lab, Department of Biological Sciences, University of Delaware, Newark, DE 19701

*Author to whom correspondence should be addressed.

 

Abstract

The term “uterosomes” was first used to classify extracellular membrane vesicles released into the uterine luminal fluid. These extracellular vesicles (EVs), varying in sizes, fit the classification of exosomes and microvesicles on the basis of size, the presence of the CD9 biochemical marker, and lateral orientation of the membrane. Uterosomes appear to be formed by the apocrine pathway, similar to other reproductive EVs. In the murine system, the protein cargo carried by uterosomes includes glycosyl phosphatidylinositol (GPI)-linked and transmembrane proteins and these are hormonally regulated, appearing at high levels during proestrus/estrus and only marginally present at diestrus/metestrus. Uterosomes have been shown to deliver proteins in their cargo to sperm, with a functional impact, and are thought to participate in promoting sperm capacitation. Further studies are warranted, particularly those aimed at identifying the contents of their cargo during the estrus and menstrual cycle and the role they play n sperm maturation.

Keywords

  • Capacitation
  • Sperm Proteome
  • Vesicular Protein Transfer
  • Review

References