Boar seminal plasma: current insights on its potential role for assisted reproductive technologies in swine
Inmaculada Parrilla; Emilio Arsenio Martinez; Maria Antonia Gil; Cristina Cuello; Jordi Roca; Heriberto Rodriguez-Martinez; Cristina Alicia Martinez
Abstract
Keywords
References
Adhikari D, Zheng W, Shen Y, Gorre N, Ning Y, Halet G, Kaldis P, Liu K. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum Mol Genet. 2012;21(11):2476-84.
Alkmin DV, Pérez-Patiño C, Barranco I, Parrilla I, Vazquez JM, Martinez EA, Rodriguez-Martinez H, Roca J. Boar sperm cryosurvival is better after exposure to seminal plasma from selected fractions than to those from entire ejaculate. Cryobiology. 2014;69(2):203-10.
Almog T, Naor Z. The role of Mitogen Activated Protein Kinase (MAPK) in sperm functions. Mol Cell Endocrinol. 2010;314(2):239-43.
Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol. 2004;5(3):266-71.
Alvarez-Rodriguez M, Atikuzzaman M, Venhoranta H, Wright D, Rodriguez-Martinez H. Expression of immune regulatory genes in the porcine internal genital tract is differentially triggered by spermatozoa and seminal plasma. Int J Mol Sci. 2019;20(3):1-20.
Aumüller G, Riva A. Morphology and functions of the human seminal vesicle. Andrologia. 1992;24(4):183-96.
Awda BJ, Mackenzie-Bell M, Buhr MM. Reactive oxygen species and boar sperm function. Biol Reprod. 2009;81(3):553-61.
Barranco I, Padilla L, Pérez-Patiño C, Vazquez JM, Martinez EA, Rodriguez-Martinez EA, Roca J, Parrilla I. Seminal plasma cytokines are predictive of the outcome of boar sperm preservation. Front Vet Sci. 2019;6:436.
Barranco I, Roca J, Tvarijonaviciute A, Rubér M, Vicente-Carrillo A, Atikuzzaman M, Cerón JJ, Martínez EA, Rodríguez-Martínez H. Measurement of activity and concentration of paraoxonase 1 (PON-1) in seminal plasma and identification of PON-2 in the sperm of boar ejaculates. Mol Reprod Dev. 2015a;82(1):58-65.
Barranco I, Rubér M, Pérez-Patiño C, Atikuzzaman M, Martinez EA, Roca J, Rodriguez-Martinez H. The seminal plasma of the boar is rich in cytokines, with significant individual and intra-ejaculate variation. Am J Reprod Immunol. 2015b;74(6):523-32.
Barranco I, Tvarijonaviciute A, Pérez-Patiño C, Alkmin DV, Cerón JJ, Martínez EA, Rodríguez-Martínez H, Roca J. The activity of paraoxonase type 1 (PON-1) in boar seminal plasma and its relationship with sperm quality, functionality, and
Barranco I, Tvarijonaviciute A, Pérez-Patiño C, Vicente-Carrillo A, Parrilla I, Ceron JJ, Martinez EA, Rodriguez-Martinez H, Roca J. Glutathione peroxidase 5 is expressed by the entire pig male genital tract and once in the seminal plasma contributes to sperm survival and
Bazer FW, Johnson GA. Pig blastocyst-uterine interactions. Differentiation. 2014;87(1-2):52-65.
Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod. 2010;16(3):135-52.
Blitek A, Morawska E, Kiewisz J, Ziecik AJ. Effect of conceptus secretions on HOXA10 and PTGS2 gene expression, and PGE2 release in co-cultured luminal epithelial and stromal cells of the porcine endometrium at the time of early implantation. Theriogenology. 2011;76(5):954-66.
Boursnell JC, Baronos S, Briggs PA, Butler EJ. The concentration of Zinc in boar seminal plasma and vesicular secretion in relation to those of nitrgenous substances, citrate, galactose and fructose. J Reprod Fertil. 1972;29(2):215-27.
Brewis IA, Gadella BM. Sperm surface proteomics: from protein list to biological function. Mol Hum Reprod. 2010;16(2):68-79.
Bromfield JJ, Roberts CT, Robertson SA. Seminal plasma programs uterine receptivity and pregnancy outcome. In: Proceedings of the 37th Annual Meeting of the Society for the Study of Reproduction; 2004 Aug 1-4; Vancouver, British Columbia, Canada. Madison: Society for the Study of Reproduction; 2004.
Bromfield JJ. Seminal fluid and reproduction: much more than previously thought. J Assist Reprod Genet. 2014;31(6):627-36.
Bromfield JJ. A role for seminal plasma in modulating pregnancy outcomes in domestic species. Reproduction. 2016;152(6):R223-32.
Bucci D, Isani G, Giaretta E, Spinaci M, Tamanini C, Ferlizza E, Galeati G. Alkaline phosphatase in boar sperm function. Andrology. 2014;2(1):100-6.
Caballero I, Parrilla I, Almiñana C, del Olmo D, Roca J, Martinez EA, Vázquez JM. Seminal plasma proteins as modulators of the sperm function and their application in sperm biotechnologies. Reprod Domest Anim. 2012;47(Suppl 3):12-21.
Carp HJ, Serr DM, Mashiach S, Nebel L. Influence of insemination on the implantation of transferred rat blastocysts. Gynecol Obstet Invest. 1984;18(4):194-8.
Chaouat G, Menu E, Clark DA, Dy M, Minkowski M, Wegmann TG. Control of fetal survival in CBA x DBA/2 mice by lymphokine therapy. J Reprod Fertil. 1990;89(2):447-58.
Choudhary KK, Kavya KM, Jerome A, Sharma RK. Advances in reproductive biotechnologies. Vet World. 2016;9(4):388-95.
Ciereszko A, Glogowski J, Strzezek J, Demianowicz W. Low stability of aspartate aminotransferase activity in boar semen. Theriogenology. 1992;37(6):1269-81.
Cooper TG. Function of the epididymis and its secretory products. In: Cooper TG, editor. The epididymis, sperm maturation and fertilisation. Berlin: Springer-Verlag; 1986. p. 174-272.
Druart X, Rickard JP, Mactier S, Kohnke PL, Kershaw-Young CM, Bathgate R, Gibb Z, Crossett B, Tsikis G, Labas V, Harichaux G, Grupen CG, de Graaf SP. Proteomic characterization and cross species comparison of mammalian seminal plasma. J Proteomics. 2013;91:13-22.
Dyck MK, Foxcroft GR, Novak S, Ruiz-Sanchez A, Patterson J, Dixon WT. Biological markers of boar fertility. Reprod Domest Anim. 2011;46(Suppl 2):55-8.
Edwards AK, van den Heuvel MJ, Wessels JM, Lamarre J, Croy BA, Tayade C. Expression of angiogenic basic fibroblast growth factor, platelet derived growth factor, thrombospondin-1 and their receptors at the porcine maternal-fetal interface. Reprod Biol Endocrinol. 2011;9(1):5.
Einer-Jensen N, Hunter RHF. Counter-current transfer in reproductive biology. Reproduction. 2005;129(1):9-18.
Food and Agriculture Organization of the United Nations – FAO, Organisation for Economic Co-operation and Development – OECD. Agricultural outlook 2018-2027 [Internet]. Rome: OECD-FAO; 2018 [cited 2020 Mar 10]. Available from:
Forejtek P, Návratil S. Relation between aspartate aminotrasnferase (AST) activity in the seminal fluid and indicators of boar ejaculate quality. Vet Med. 1984;29(4):217-22. PMid:6426132.
Fraczek M, Kurpisz M. Cytokines in the male reproductive tract and their role in infertility disorders. J Reprod Immunol. 2015;108:98-104.
García EM, Vazquez JM, Parrilla I, Calvete JJ, Sanz L, Caballero I, Roca J, Vazquez JL, Martinez EA. Improving the fertilizing ability of sex sorted boar spermatozoa. Theriogenology. 2007;68(5):771-8.
Gavet O, Pines J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell. 2010;18(4):533-43.
Ghiringhelli F, Ménard C, Terme M, Flament C, Taieb J, Chaput N, Puig PE, Novault S, Escudier B, Vivier E, Lecesne A, Robert C, Blay J-Y, Bernard J, Caillat-Zucman S, Freitas A, Tursz T, Wagner-Ballon O, Capron C, Vainchencker W, Martin F, Zitvogel L. CD4 + CD25 + regulatory T cells inhibit natural killer cell functions in a transforming growth factor–β–dependent manner. J Exp Med. 2005;202(8):1075-85.
Gou J, Jia J, Zhao X, Yi T, Li Z. Identification of stathmin 1 during peri-implantation period in mouse endometrium by a proteomics-based analysis. Biochem Biophys Res Commun. 2015;461(2):211-6.
Grasa P, Kaune H, Williams SA. Embryos generated from oocytes lacking complex N- and O-glycans have compromised development and implantation. Reproduction. 2012;144(4):455-65.
Guthrie HD, Welch GR, Long JA. Mitochondrial function and reactive oxygen species action in relation to boar motility. Theriogenology. 2008;70(8):1209-15.
Hamamah S, Gatti JL. Role of the ionic environment and internal pH on sperm activity. Hum Reprod. 1998;13(Suppl 4):20-30.
Hardy K, Spanos S. Growth factor expression and function in the human and mouse preimplantation embryo. J Endocrinol. 2002;172(2):221-36.
Hatano N, Mori Y, Oh-hora M, Kosugi A, Fujikawa T, Nakai N, Niwa H, Miyazaki J, Hamaoka T, Ogata M. Essential role for ERK2 mitogen- activated protein kinase in placental development. Genes Cells. 2003;8(11):847-56.
Jansen M, Ten Klooster JP, Offerhaus GJ, Clevers H. LKB1 and AMPK family signaling: the intimate link between cell polarity and energy metabolism. Physiol Rev. 2009;89(3):777-98.
Jeong W, Kim J, Bazer FW, Song G. Epidermal growth factor stimulates proliferation and migration of porcine trophectoderm cells through protooncogenic protein kinase 1 and extracellular-signal-regulated kinases 1/2 mitogen-activated protein kinase signal transduction cascades during early pregnancy. Mol Cell Endocrinol. 2013;381(1-2):302-11.
Jia J, Gou J, Zhao X, Yi T, Li Z. Apolipoprotein A1 and heterogeneous nuclear ribonucleoprotein E1 implicated in the regulation of embryo implantation by inhibiting lipid peroxidation. Reprod Biomed Online. 2016;33(5):635-45.
Jiang L, Zheng T, Huang J, Mo J, Zhou H, Liu M, Gao X, Yu B. Association of semen cytokines with reactive oxygen species and histone transition abnormalities. J Assist Reprod Genet. 2016;33(9):1239-46.
Johnson LA, Pursel VG, Gerrits RJ, Thomas CH. Free amino acid composition of porcine seminal, epididymal and seminal vesicle fluids. J Anim Sci. 1972;34(3):430-4.
Johnson LA, Weitze KF, Fiser P, Maxwell WM. Storage of boar semen. Anim Reprod Sci. 2000;62(1-3):143-72.
Juyena NS, Stelletta C. Seminal plasma: an essential attribute to spermatozoa. J Androl. 2012;33(4):536-51.
Kamp G, Lauterwein J. Multinuclear magnetic resonance studies of boar seminal plasma. Biochim Biophys Acta. 1995;1243(1):101-9.
Kiewisz J, Krawczynski K, Lisowski P, Blitek A, Zwierzchowski L, Ziecik AJ, Kaczmarek MM. Global gene expression profiling of porcine endometria on days 12 and 16 of the estrous cycle and pregnancy. Theriogenology. 2014;82(6):897-909.
Koziorowska-Gilun M, Koziorowski M, Fraser L, Strzeżek J. Antioxidant defence system of boar cauda epididymidal spermatozoa and reproductive tract fluids. Reprod Domest Anim. 2011;46(3):527-33.
Lee JH, Koh H, Kim M, Kim Y, Lee SY, Karess RE, Lee SH, Shong M, Kim JM, Kim J, Chung J. Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature. 2007;447(7147):1017-20.
Li J, Barranco I, Tvarijonaviciute A, Molina FM, Martinez EA, Rodriguez-Martinez H, Parrilla I, Roca J. Seminal plasma antioxidants are directly involved in boar sperm cryotolerance. Theriogenology. 2018;107:27-35.
Lim B, Sutherland RM, Zhan Y, Deliyannis G, Brown LE, Lew AM. Targeting CD45RB alters T cell migration and delays viral clearance. Int Immunol. 2006;18(2):291-300.
Lin H, Wang H, Wang Y, Liu C, Wang C, Guo J. Transcriptomic analysis of the porcine endometrium during embryo implantation. Genes. 2015;6(4):1330-46.
Liu L, Liu X, Ren X, Tian Y, Chen Z, Xu X, Du Y, Jiang C, Fang Y, Liu Z, Fan B, Zhang Q, Jin G, Yang X, Zhang X. Smad2 and Smad3 have differential sensitivity in relaying TGFβ signaling and inversely regulate early lineage specification. Sci Rep. 2016;6(1):21602.
López-Rodriguez A, Rijsselaere T, Beek J, Vyt P, Van Soom A, Maes D. Boar seminal plasma components and their relation with semen quality. Syst Biol Reprod Med. 2013;59(1):5-12.
Maegawa M, Kamada M, Irahara M, Yamamoto S, Yoshikawa S, Kasai Y, Ohmoto Y, Gima H, Thaler CJ, Aono T. A repertoire of cytokines in human seminal plasma. J Reprod Immunol. 2002;54(1-2):33-42.
Mains LM, Christenson L, Yang B, Sparks AE, Mathur S, Van Voorhis BJ. Identification of apolipoprotein A1 in the human embryonic secretome. Fertil Steril. 2011;96(2):422-7.e2.
Mann T, Leone E. Studies on the metabolism of semen. VIII. Ergothioneine as a normal constituent of boar seminal plasma; purification and crystallization; site of formation and function. Biochem J. 1953;53(1):140-8.
Mann T, Lutwak-Mann C. Biochemistry of seminal plasma and male accessory fluids; application to andrological problems. In: Mann T, Lutwak-Mann C, editors. Male reproductive function and semen. Berlin: Springer-Verlag; 1981. Chapter IX; p. 269-326.
Marin S, Chiang K, Bassilian S, Lee WN, Boros LG, Fernandez-Novell JM, Centelles JJ, Medrano A, Rodriguez-Gil JE, Cascante M. Metabolic strategy of boar spermatozoa revealed by a metabolomic characterization. FEBS Lett. 2003;554(3):342-6.
Martinez CA, Cambra JM, Nohalez A, Parrilla I, Roca J, Vazquez JL, Rodriguez-Martinez H, Gil MA, Martinez EA, Cuello C. Prevention of hatching of porcine morulae and blastocysts by liquid storage at 20 °C. Sci Rep. 2019a;9(1):6219.
Martinez CA, Cambra JM, Nohalez A, Parrilla I, Sanchez-Osorio J, Roca J, Rodriguez-Martinez H, Gil MA, Martinez EA, Cuello C. Porcine blastocyst viability and developmental potential is maintained for 48 h of liquid storage at 25 °C without CO2 gassing. Theriogenology. 2019b;135:46-55.
Martinez CA, Cambra JM, Parrilla I, Roca J, Ferreira-Dias G, Pallares FJ, Lucas X, Vazquez JM, Martinez EA, Gil MA, Rodriguez-Martinez H, Cuello C, Alvarez-Rodriguez M. Seminal plasma modifies the transcriptional pattern of the endometrium and advances embryo development in pigs. Front Vet Sci. 2019c;6:465.
Martinez EA, Angel MA, Cuello C, Sanchez-Osorio J, Gomis J, Parrilla I, Vila J, Colina I, Diaz M, Reixach J, Vazquez JL, Vazquez JM, Roca J, Gil MA. Successful non-surgical deep uterine transfer of porcine morulae after 24 hour culture in a chemically defined medium. PLoS One. 2014;9(8):e104696.
Martinez EA, Martinez CA, Cambra JM, Maside C, Lucas X, Vazquez JL, Vazquez JM, Roca J, Rodriguez-Martinez H, Gil MA, Parrilla I, Cuello C. Achievements and future perspectives of embryo transfer technology in pigs. Reprod Domest Anim. 2019d;54(Suppl 4):4-13.
Martinez EA, Martinez CA, Nohalez A, Sanchez-Osorio J, Vazquez JM, Roca J, Parrilla I, Gil MA, Cuello C. Nonsurgical deep uterine transfer of vitrified,
Maxwell WM, Johnson LA. Physiology of spermatozoa at high dilution rates: the influence of seminal plasma. Theriogenology. 1999;52(8):1353-62.
McBride A, Ghilagaber S, Nikolaev A, Hardie DG. The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell Metab. 2009;9(1):23-34.
Ming Q, Roske Y, Schuetz A, Walentin K, Ibraimi I, Schmidt-Ott KM, Heinemann U. Structural basis of gene regulation by the Grainyhead/CP2 transcription factor family. Nucleic Acids Res. 2018;46(4):2082-95.
Mogielnicka-Brzozowska M, Kordan W. Characteristics of selected seminal plasma proteins and their application in the improvement of the reproductive processes in mammals. Pol J Vet Sci. 2011;14(3):489-99.
Morris D, Diskin M. Effect of progesterone on embryo survival. Animal. 2008;2(8):1112-9.
Murer V, Spetz JF, Hengst U, Altrogge LM, de Agostini A, Monard D. Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1. Proc Natl Acad Sci USA. 2001;98(6):3029-33.
Nayeem SB, Arfuso F, Dharmarajan A, Keelan JA. Role of Wnt signalling in early pregnancy. Reprod Fertil Dev. 2016;28(5):525-44.
Nikodemus D, Lazic D, Bach M, Bauer T, Pfeiffer C, Wiltzer L, Lain E, Schömig E, Gründemann D. Paramount levels of ergothioneine transporter SLC22A4 mRNA in boar seminal vesicles and cross-species analysis of ergothioneine and glutathione in seminal plasma. J Physiol Pharmacol. 2011;62(4):411-9. PMid:22100842.
Novak S, Ruiz-Sanchez A, Dixon WT, Foxcroft GR, Dyck MK. Seminal plasma proteins as potential markers of relative fertility in boars. J Androl. 2010;31(2):188-200.
O WS, Chen HQ, Chow PH. Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J Reprod Fertil. 1988;84(1):341-4.
O’Leary S, Jasper MJ, Robertson SA, Armstrong DT. Seminal plasma regulates ovarian progesterone production, leukocyte recruitment and follicular cell responses in the pig. Reproduction. 2006;132(1):147-58.
O’Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA. Seminal plasma regulates endometrial cytokine expression leukocyte recruitment and embryo development in the pig. Reproduction. 2004;128(2):237-47.
O’Neill C. The potential roles for embryotrophic ligands in preimplantation embryo development. Hum Reprod Update. 2008;14(3):275-88.
Pang SF, Chow PH, Wong TM. The role of the seminal vesicle, coagulating glands and prostate glands on the fertility and fecundity of mice. J Reprod Fertil. 1979;56(1):129-32.
Parrilla I, Pérez-Patiño C, Li J, Barranco I, Padilla L, Rodriguez-Martinez H, Martinez EA, Roca J. Boar semen proteomics and sperm preservation. Theriogenology. 2019;137:23-9.
Parrilla I, Vazquez JM, Caballero I, Gil MA, Hernandez M, Roca J, Lucas X, Martinez EA. Optimal characteristics of spermatozoa for semen technologies in pigs. In: Rodriguez-Martinez H, Vallet JL, Ziecik AJ, editors. Control of pig reproduction VIII. Nottingham: Nottingham University Press; 2009. p. 37-50.
Pérez-Patiño C, Barranco I, Parrilla I, Valero ML, Martinez EA, Rodriguez-Martinez H, Roca J. Characterization of the porcine seminal plasma proteome comparing ejaculate portions. J Proteomics. 2016;142:15-23.
Peitz B, Olds Clarke P. Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol Reprod. 1986;35(3):608-17.
Pérez-Patiño C, Parrilla I, Li J, Barranco I, Martinez EA, Rodriguez-Martinez H, Roca J. The proteome of pig spermatozoa is remodeled during ejaculation. Mol Cell Proteomics. 2019;18(1):41-50.
Petrof G, Nanda A, Howden J, Takeichi T, McMillan JR, Aristodemou S, Ozoemena L, Liu L, South AP, Pourreyron C, Dafou D, Proudfoot LE, Al-Ajmi H, Akiyama M, McLean WH, Simpson MA, Parsons M, McGrath JA. Mutations in GRHL2 result in an autosomal-recessive ectodermal dysplasia syndrome. Am J Hum Genet. 2014;95(3):308-14.
Pipan MZ, Mrkun J, Strajn BJ, Vrtač KP, Kos J, Pišlar A, Zrimšek P. The influence of macro- and microelements in seminal plasma on diluted boar sperm quality. Acta Vet Scand. 2017;59(1):11.
Pursel VG, Johnson LA. Freezing of boar spermatozoa: fertilizing capacity with concentrated semen and a new thawing procedure. J Anim Sci. 1975;40(1):99-102.
Qazi IH, Angel C, Yang H, Zoidis E, Pan B, Wu Z, Ming Z, Zeng CJ, Meng Q, Han H, Zhou G. Role of selenium and selenoproteins in male reproductive function: a review of past and present evidences. Antioxidants. 2019;8(8):268.
Qiu Q, Yang M, Tsang BK, Gruslin A. EGF-induced trophoblast secretion of MMP-9 and TIMP-1 involves activation of both PI3K and MAPK signalling pathways. Reproduction. 2004;128(3):355-63.
Queen K, Dhabuwala CB, Pierrepoint CG. The effect of removal of the various accessory sex glands on the fertility of male rats. J Reprod Fertil. 1981;62(2):423-6.
Radomil L, Pettitt MJ, Merkies KM, Hickey KD, Buhr MM. Stress and dietary factors modify boar sperm for processing. Reprod Domest Anim. 2011;46(Suppl 2):39-44.
Robertson SA, Moldenhauer LM. Immunological determinants of implantation success. Int J Dev Biol. 2014;58(2-4):205-17.
Robertson SA. GM-CSF regulation of embryo development and pregnancy. Cytokine Growth Factor Rev. 2007;18(3-4):287-98.
Robertson SA. Immune regulation of conception and embryo implantation-all about quality control? J Reprod Immunol. 2010;85(1):51-7.
Robertson SA. Seminal plasma and male factor signaling in the female reproductive tract. Cell Tissue Res. 2005;322(1):43-52.
Roca J, Broekhuijse MLWJ, Parrilla I, Rodriguez-Martinez H, Martinez EA, Bolarin A. Boar differences in artificial insemination outcomes: can they be minimized. Reprod Domest Anim. 2015;50(Suppl 2):48-55.
Roca J, Pérez-Patiño C, Barranco I, Padilla LC, Martinez EA, Rodriguez-Martinez H, Parrilla I. Proteomics in fresh and preserved pig semen: recent achievements and future challenges. Theriogenology. 2020. In press.
Roca J, Rodríguez MJ, Gil MA, Carvajal G, Garcia EM, Cuello C, Vazquez JM, Martinez EA. Survival and in vitro fertility of boar spermatozoa frozen in the presence of superoxide dismutase and/or catalase. J Androl. 2005;26(1):15-24.
Rodríguez-Gil JE. Energy management of mature mammalian spermatozoa. In: Lemma A, editor. Success in artificial insemination: quality of semen and diagnostics employed. Croatia: IntechOpen; 2013.
Rodriguez-Martinez H, Kvist U, Saravia F, Wallgren M, Johannisson A, Sanz L, Peña FJ, Martinez EA, Roca J, Vazquez JM, Calvete JJ. The physiological roles of the boar ejaculate. In: Rodriguez-Martinez H, Vallet JL, Ziecik AJ, editors. Control of pig reproduction VIII. Nottingham: Nottingham University Press; 2009. p. 1-21.
Rodríguez-Martínez, Kvist U, Ernerudh J, Sanz L, Calvete JJ. Seminal plasma proteins: what role do they play? Am J Reprod Immunol. 2011;66(Suppl 1):11-22.
Rudensky AY. Regulatory T cells and Foxp3. Immunol Rev. 2011;241(1):260-8.
Saba-El-Leil MK, Vella FD, Vernay B, Voisin L, Chen L, Labrecque N, Ang SL, Meloche S. An essential function of the mitogen-activated protein kinase Erk2 in mouse trophoblast development. EMBO Rep. 2003;4(10):964-8.
Samborski A, Graf A, Krebs S, Kessler B, Bauersachs S. Deep sequencing of the porcine endometrial transcriptome on day 14 of pregnancy. Biol Reprod. 2013;88(4):84.
Santamaría D, Barrière C, Cerqueira A, Hunt S, Tardy C, Newton K, Cáceres JF, Dubus P, Malumbres M, Barbacid M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature. 2007;448(7155):811-5.
Saravia F, Wallgren M, Johannisson A, Calvete JJ, Sanz L, Peña FJ, Roca J, Rodriguez-Martinez H. Exposure to the seminal plasma of different portions of the boar ejaculate modulates the survival of spermatozoa cryopreserved in MiniFlatPacks. Theriogenology. 2009;71(4):662-75.
Schjenken JE, Robertson SA. Seminal fluid and immune adaptation for pregnancy – comparative biology in mammalian species. Reprod Domest Anim. 2014;49(Suppl 3):27-36.
Schuberth HJ, Taylor U, Zerbe H, Waberski D, Hunter R, Rath D. Immunological responses to semen in the female genital tract. Theriogenology. 2008;70(8):1174-81.
Scott MP, Carroll SB. The segmentation and homeotic gene network in early Drosophila development. Cell. 1987;51(5):689-98.
Setchell BP, Brooks DE. Anatomy, vasculature, innervation and fluids of the male reproductive tract. In: Knobil E, Neil J, editors. The physiology of reproduction. New York: Raven Press; 1988. p. 753-836. (vol. 2).
Shevach EM. CD4+CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol. 2002;2(6):389-400.
Shiota C, Woo J-T, Lindner J, Shelton KD, Magnuson MA. Multiallelic disruption of the Rictor gene in mice reveals that mTOR complex 2 is essential for fetal growth and viability. Dev Cell. 2006;11(4):583-9.
Sjöblom C, Roberts CT, Wikland M, Robertson SA. Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology. 2005;146(5):2142-53.
Sjöblom C, Wikland M, Robertson SA. Granulocyte-macrophage colony-stimulating factor (GM-CSF) acts independently of the beta common subunit of the GM-CSF receptor to prevent inner cell mass apoptosis in human embryos. Biol Reprod. 2002;67(6):1817-23.
Songyang Z, Baltimore D, Cantley LC, Kaplan DR, Franke TF. Interleukin 3-dependent survival by the Akt protein kinase. Proc Natl Acad Sci USA. 1997;94(21):11345-50.
Sopkova D, Andrejcakova Z, Vlckova R, Danisova O, Supuka P, Ondrasovicova S, Petrilla V. Lactate dehydrogenase as a possible indicator of reproductive capacity of boars. Indian J Anim Sci. 2015;85(2):143-7.
Sun R, Lei L, Liu S, Xue B, Wang J, Wang J, Shen J, Duan L, Shen X, Cong Y, Gu Y, Hu K, Jin L, Liu ZH. Morphological changes and germ layer formation in the porcine embryos from days 7-13 of development. Zygote. 2015;23(2):266-76.
Syriou V, Papanikolaou D, Kozyraki A, Goulis DG. Cytokines and Male Infertility. Eur Cytokine Netw. 2018;29(3):73-82.
Taams LS, Akbar AN. Peripheral generation and function of CD4+CD25+ regulatory T cells. Curr Top Microbiol Immunol. 2005;293:115-31.
Troedsson MH, Desvousges A, Alghamdi AS, Dahms B, Dow CA, Hayna J, Valesco R, Collahan PT, Macpherson ML, Pozor M, Buhi WC. Components in seminal plasma regulating sperm transport and elimination. Anim Reprod Sci. 2005;89(1-4):171-86.
Vilagran I, Yeste M, Sancho S, Casas I, Rivera del Álamo MM, Bonet S. Relationship of sperm small heat-shock protein 10 and voltage-dependent anion channel 2 with semen freezability in boars. Theriogenology. 2014;82(3):418-26.
Waberski D, Claassen R, Hahn T, Jungblut PW, Parvizi N, Kallweit E, Weitze KF. LH profile and advancement of ovulation after transcervical infusion of seminal plasma at different stages of oestrus in gilts. J Reprod Fertil. 1997;109(1):29-34.
Waberski D, Schäfer J, Bölling A, Scheld M, Henning H, Hambruch N, Schuberth H-J, Pfarrer C, Wrenzycki C, Hunter RHF. Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles. PLoS One. 2018;13(8):e0202654.
Waclawik A, Kaczmarek M, Blitek A, Kaczynski P, Ziecik AJ. Embryo-maternal dialogue during pregnancy establishment and implantation in the pig. Mol Reprod Dev. 2017;84(9):842-55.
Watson JG, Carroll J, Chaykin S. Reproduction in mice: the fate of spermatozoa not involved in fertilization. Gamete Res. 1983;7(1):75-84.
Wysocki P, Strzezek J. Molecular forms of acid phosphatase of boar seminal plasma. Anim Sci Pap Rep. 2000;18(2):99-106.
Yao Y, Li W, Wu J, Germann UA, Su MS, Kuida K, Boucher DM. Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation. Proc Natl Acad Sci USA. 2003;100(22):12759-64.
Yeste M, Rodriguez-Gil JE, Bonet S. Artificial insemination with frozen-thawed boar sperm. Mol Reprod Dev. 2017;84(9):802-13.
Yong HEJ, Murthi P, Kalionis B, Keogh RJ, Brennecke SP. Decidual ACVR2A regulates extravillous trophoblast functions of adhesion, proliferation, migration and invasion
Submitted date:
03/10/2020
Accepted date:
04/14/2020
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email