Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane

Oncotarget

Volumn 7, Issue 37, 2016, Pages 58832-58847

  Du, Jian ^a   Shen, Jian ^a   Wang, Yuanxian ^a   Pan, Chuanying ^a   Pang, Weijun ^a   Diao, Hua ^b   Dong, Wuzi ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

Boar sperm quality; Capacitation; Liquid storage; Pathology Section; Seminal plasma exosomes

Indexed keywords

ANTIOXIDANT; CD63 ANTIGEN; CD9 ANTIGEN; DILUENT; MALONALDEHYDE; MOLECULAR MARKER; NANOMATERIAL; PROTEIN AWN; PROTEIN PSP 1; SEMINAL PLASMA PROTEIN; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; PSPC1 PROTEIN, HUMAN; RNA BINDING PROTEIN; SPERMADHESIN;

ANIMAL CELL; ARTICLE; CELL INFILTRATION; EXOSOME; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; MALE; MALE GENITAL SYSTEM FUNCTION; MEMBRANE BINDING; NONHUMAN; PIG; PROTEIN CONTENT; PROTEIN TRANSPORT; SCANNING ELECTRON MICROSCOPY; SEMEN ANALYSIS; SEMINAL PLASMA; SPERM FUNCTION; SPERMATOZOON CAPACITATION; SPERMATOZOON HEAD; SPERMATOZOON MOTILITY; SURVIVAL TIME; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL MEMBRANE; CELL SURVIVAL; CYTOLOGY; FEMALE; FERTILITY; METABOLISM; SPERM; SPERMATOZOON;

ANIMALS; CELL MEMBRANE; CELL SURVIVAL; CELLS, CULTURED; EXOSOMES; FEMALE; MALE; NUCLEAR PROTEINS; RNA-BINDING PROTEINS; SEMEN; SEMEN ANALYSIS; SEMINAL PLASMA PROTEINS; SPERM CAPACITATION; SPERM MOTILITY; SPERM-OVUM INTERACTIONS; SPERMATOZOA; SWINE; TETRASPANIN 30; TETRASPANIN-29;

EID: 84991383932     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.11315     Document Type: Article

References (50)

1. Koch S, Acebron SP, Herbst J, Hatiboglu G, Niehrs C. Posttranscriptional Wnt Signaling Governs Epididymal Sperm Maturation. Cell. 2015; 163:1225-1236
2. Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. The Prostate. 2009; 69:159-167
3. Suzuki K, Asano A, Eriksson B, Niwa K, Nagai T, Rodriguez-Martinez H. Capacitation status and in vitro fertility of boar spermatozoa: effects of seminal plasma, cumulus-oocyte-complexes-conditioned medium and hyaluronan. International journal of andrology. 2002; 25:84-93
4. Abney TO, Williams WL. Inhibition of sperm capacitation by intrauterine deposition of seminal plasma decapacitation factor. Biology of reproduction. 1970; 2:14-17
5. Mendoza N, Casao A, Perez-Pe R, Cebrian-Perez JA, Muino-Blanco T. New insights into the mechanisms of ram sperm protection by seminal plasma proteins. Biology of reproduction. 2013; 88:149
6. Huo LJ, Yue KZ, Yang ZM. Characterization of viability, mitochondrial activity, acrosomal integrity and capacitation status in boar sperm during in vitro storage at different ambient temperatures. Reproduction, fertility, and development. 2002; 14:509-514
7. Kovak MR, Saraswati S, Schoen DJ, Diekman AB. Investigation of galectin-3 function in the reproductive tract by identification of binding ligands in human seminal plasma. Am J Reprod Immunol. 2014; 72:403-412
8. Sullivan R, Saez F, Girouard J, Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood cells, molecules & diseases. 2005; 35:1-10
9. Gatti JL, Metayer S, Belghazi M, Dacheux F, Dacheux JL. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biology of reproduction. 2005; 72:1452-1465
10. Piehl LL, Fischman ML, Hellman U, Cisale H, Miranda PV. Boar seminal plasma exosomes: effect on sperm function and protein identification by sequencing. Theriogenology. 2013; 79:1071-1082
11. Park KH, Kim BJ, Kang J, Nam TS, Lim JM, Kim HT, Park JK, Kim YG, Chae SW, Kim UH. Ca2+ signaling tools acquired from prostasomes are required for progesteroneinduced sperm motility. Sci Signa.l 2011; 4: ra31
12. Aalberts M, Stout TA, Stoorvogel W. Prostasomes: extracellular vesicles from the prostate. Reproduction. 2014; 147:1-14
13. Berruti G, Paiardi C. Acrosome biogenesis: Revisiting old questions to yield new insights. Spermatogenesis. 2011; 1:95-98
14. Zhang HG, Cao P, Teng Y, Hu X, Wang Q, Yeri AS, Zhuang X, Samykutty A, Mu J, Deng ZB et al. Isolation, identification, and characterization of novel nanovesicles. Oncotarget. 2016; 7:41364-41362. doi: 10.18632/oncotarget.9325
15. Royo F, Zuniga-Garcia P, Sanchez-Mosquera P, Egia A, Perez A, Loizaga A, Arceo R, Lacasa I, Rabade A, Arrieta E et al. Different EV enrichment methods suitable for clinical settings yield different subpopulations of urinary extracellular vesicles from human samples. Journal of extracellular vesicles. 2016; 5: 1-11
16. Sanz L, Calvete JJ, Mann K, Schafer W, Schmid ER, Amselgruber W, Sinowatz F, Ehrhard M, Topfer-Petersen E. The complete primary structure of the spermadhesin AWN, a zona pellucida-binding protein isolated from boar spermatozoa. FEBS letters. 1992; 300:213-218
17. Petrunkina AM, Harrison RA, Topfer-Petersen E. Only low levels of spermadhesin AWN are detectable on the surface of live ejaculated boar spermatozoa. Reproduction, fertility, and development. 2000; 12:361-371
18. Caballero I, Vazquez JM, Garcia EM, Roca J, Martinez EA, Calvete JJ, Sanz L, Ekwall H, Rodriguez-Martinez H. Immunolocalization and possible functional role of PSP-I/PSP-II heterodimer in highly extended boar spermatozoa. Journal of andrology. 2006; 27:766-773
19. Saez F, Sullivan R. Prostasomes, post-testicular sperm maturation and fertility. Front Biosci (Landmark Ed.) 2016; 21:1464-1473
20. Higgins SJ, Burchell JM, Mainwaring WI. Androgendependent synthesis of basic secretory proteins by the rat seminal vesicle. The Biochemical journal. 1976; 158:271-282
21. Davis BK. Decapacitation and recapacitation of rabbit spermatozoa treated with membrane vesicles from seminal plasma. J Reprod Fertil. 1974; 41:241-244
22. Breitbart H, Rubinstein S. Characterization of Mg2+-and Ca2+-ATPase activity in membrane vesicles from ejaculated ram seminal plasma. Arch Androl. 1982; 9:147-157
23. Killian GJ, Chapman DA, Rogowski LA: Fertilityassociated proteins in Holstein bull seminal plasma. Biology of reproduction. 1993; 49:1202-1207
24. Sostaric E, Aalberts M, Gadella BM, Stout TA: The roles of the epididymis and prostasomes in the attainment of fertilizing capacity by stallion sperm. Anim Reprod Sci. 2008; 107:237-248
25. Simons M, Raposo G: Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009, 21:575-581
26. Thery C, Zitvogel L, Amigorena S: Exosomes: composition, biogenesis and function. Nature reviews Immunology. 2002, 2:569-579
27. Ronquist G, Frithz GG: Prostasomes in human semen contain ADP and GDP. Acta Europaea fertilitatis. 1986; 17:273-276
28. Pons-Rejraji H, Artonne C, Sion B, Brugnon F, Canis M, Janny L, Grizard G. Prostasomes: inhibitors of capacitation and modulators of cellular signalling in human sperm. International journal of andrology. 2011; 34:568-580
29. Hernandez M, Roca J, Calvete JJ, Sanz L, Muino-Blanco T, Cebrian-Perez JA, Vazquez JM, Martinez EA. Cryosurvival and in vitro fertilizing capacity postthaw is improved when boar spermatozoa are frozen in the presence of seminal plasma from good freezer boars. Journal of andrology. 2007; 28:689-697
30. Kareskoski AM, del Alamo MM, Guvenc K, Reilas T, Calvete JJ, Rodriguez-Martinez H, Andersson M, Katila T. Protein composition of seminal plasma in fractionated stallion ejaculates. Reprod Domest Anim. 2011; 46:e79-84
31. Burden HP, Holmes CH, Persad R, Whittington K. Prostasomes-their effects on human male reproduction and fertility. Hum Reprod Update. 2006; 12:283-292
32. Neild DM, Gadella BM, Chaves MG, Miragaya MH, Colenbrander B, Aguero A. Membrane changes during different stages of a freeze-thaw protocol for equine semen cryopreservation. Theriogenology. 2003; 59:1693-1705
33. Johnson LA, Weitze KF, Fiser P, Maxwell WM. Storage of boar semen. Anim Reprod Sci. 2000; 62:143-172
34. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol. 2008; 59:2-11
35. Sariozkan S, Turk G, Canturk F, Yay A, Eken A, Akcay A. The effect of bovine serum albumin and fetal calf serum on sperm quality, DNA fragmentation and lipid peroxidation of the liquid stored rabbit semen. Cryobiology. 2013; 67:1-6
36. Aitken RJ. Sperm function tests and fertility. International journal of andrology. 2006; 29:69-75
37. Zhang XG, Yan GJ, Hong JY, Su ZZ, Yang GS, Li QW, Hu JH. Effects of bovine serum albumin on boar sperm quality during liquid storage at 17 degrees C. Reprod Domest. Anim 2015; 50:263-269
38. Yamazaki D, Funato Y, Miyata H, Ikawa M, Miki H. Complementary role of CNNM2 in sperm motility and Ca(2+) influx during capacitation. Biochemical and biophysical research communications. 2016; 474:441-446
39. Cisneros-Mejorado A, Hernandez-Soberanis L, Islas-Carbajal MC, Sanchez D. Capacitation and Ca(2+) influx in spermatozoa: role of CNG channels and protein kinase G. Andrology. 2014; 2:145-154
40. Kawakami E, Nishizono Y, Miyata C, Hirano T, Hori T, Tsutsui T. Effects of hyaluronic acid on Ca(2+) influx, lactate dehydrogenase activity, and cyclic AMP synthesis in canine ejaculated sperm during In Vitro capacitation. J Vet Med Sci. 2006; 68:119-123
41. Kaul G, Sharma GS, Singh B, Gandhi KK. Capacitation and acrosome reaction in buffalo bull spermatozoa assessed by chlortetracycline and Pisum sativum agglutinin fluorescence assay. Theriogenology. 2001; 55:1457-1468
42. DasGupta S, Mills CL, Fraser LR. Ca(2+)-related changes in the capacitation state of human spermatozoa assessed by a chlortetracycline fluorescence assay. J Reprod Fertil. 1993; 99:135-143
43. Ward CR, Storey BT: Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev Biol. 1984; 104:287-296
44. Fabiani R, Johansson L, Lundkvist O, Ronquist G. Prolongation and improvement of prostasome promotive effect on sperm forward motility. European journal of obstetrics, gynecology, and reproductive biology. 1995; 58:191-198
45. Davis BK. Timing of fertilization in mammals: sperm cholesterol/phospholipid ratio as a determinant of the capacitation interval. Proceedings of the National Academy of Sciences of the United States of America. 1981; 78:7560-7564
46. Cohen R, Mukai C, Travis AJ. Lipid Regulation of Acrosome Exocytosis. Advances in anatomy, embryology, and cell biology. 2016; 220:107-127
47. Hu JH, Li QW, Jiang ZL, Yang H, Zhang SS, Zhao HW. The cryoprotective effect of trehalose supplementation on boar spermatozoa quality. Reprod Domest Anim. 2009; 44:571-575
48. Estienne MJ, Harper AF, Day JL. Characteristics of sperm motility in boar semen diluted in different extenders and stored for seven days at 18 degrees C. Reprod Biol. 2007; 7:221-231
49. Nagy S, Jansen J, Topper EK, Gadella BM. A triple-stain flow cytometric method to assess plasma-and acrosomemembrane integrity of cryopreserved bovine sperm immediately after thawing in presence of egg-yolk particles. Biology of reproduction. 2003; 68:1828-1835
50. Flesch FM, Colenbrander B, van Golde LM, Gadella BM. Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane. Biochemical and biophysical research communications. 1999; 262:787-792