Selection for higher fertility reflects in the seminal fluid proteome of modern domestic chicken

Agostini, 2001, CXCR3 and its ligand CXCL10 are expressed by inflammatory cells infiltrating lung allografts and mediate chemotaxis of T cells at site of rejection, Am. J. Pathol., 158, 1703, 10.1016/S0002-9440(10)64126-0 Atikuzzaman, 2015, Spermatozoa rather than seminal fluid drives immune-modulation in the sperm storage tubuli of Red Junglefowl hens, Reprod. Domest. Anim., 50, 44 Atikuzzaman, 2015, Mating induces the expression of immune- and pH-regulatory genes in the utero-vaginal junction containing mucosal sperm-storage tubuli of hens, Reproduction, 150, 473, 10.1530/REP-15-0253 Ayroles, 2011, Funtional genome annotation of Drosophila seminal fluid proteins using transcriptional genetic networks, Genet. Res., 93, 387, 10.1017/S0016672311000346 Bakst, 1992, Effect of bovine serum albumin on motility and fecundity of turkey spermatozoa before and after storage, J. Reprod. Fertil., 94, 287, 10.1530/jrf.0.0940287 Baron, 2014, Ovotransferrin plays a major role in the strong bactericidal effect of egg white against the Bacillus cereus group, J. Food Prot., 77, 955, 10.4315/0362-028X.JFP-13-473 Barranco, 2015, The seminal plasma of the boar is rich in cytokines, with significant individual and intra-ejaculate variation, Am. J. Reprod. Immunol., 74, 523, 10.1111/aji.12432 Batruch, 2011, Proteomic analysis of seminal plasma from normal volunteers and post-vasectomy patients identifies over 2000 proteins and candidate biomarkers of the urogenital system, J. Proteome Res., 10, 941, 10.1021/pr100745u Bharshankar, 2000, Relationship of seminal plasma transferrin with seminal parameters in male infertility, Indian J. Physiol. Pharmacol., 44, 456 Blesbois, 1990, Effects of high-density lipoproteins on storage at 4°C of fowl spermatozoa, J. Reprod. Fertil., 90, 473, 10.1530/jrf.0.0900473 Bromfield, 2014, Maternal factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring, Proc. Natl. Acad. Sci., 111, 2200, 10.1073/pnas.1305609111 Caballero, 2012, Seminal plasma proteins as modulators of the sperm function and their application in sperm biotechnologies, Reprod. Domest. Anim., 47, 12, 10.1111/j.1439-0531.2012.02028.x Calvete, 1994, Isolation and biochemical characterization of stallion seminal-plasma proteins, Reprod. Domest. Anim., 29, 411, 10.1111/j.1439-0531.1994.tb00588.x Calvete, 2009, Exploring the venom proteome of the western diamondback rattlesnake, Crotalus atrox, via snake venomics and combinatorial peptide ligand library approaches, J. Proteome Res., 8, 3055, 10.1021/pr900249q Castillo, 2011, Ovotransferrin and Gallinacin-9 Found in Seminal Plasma Rooster Crawford, 2015, The role of seminal plasma for improved outcomes during in vitro fertilization treatment: review of the literature and meta-analysis, Hum. Reprod. Update, 21, 275, 10.1093/humupd/dmu052 Das, 2006, Expression of TGFβ-isoforms and their receptors in utero-vaginal junction of hen oviduct in presence or absence of resident sperm with reference to sperm storage, Reproduction, 132, 781, 10.1530/rep.1.01177 Das, 2008, Mechanisms of prolonged sperm storage and sperm survivality in hen oviduct: a review, Reprod. Immunol., 60, 477, 10.1111/j.1600-0897.2008.00651.x Das, 2009, Changes in the expression of interleukin-1β and lipopolysaccharide-induced TNF factor in the oviduct of laying hens in response to artificial insemination, Reproduction, 137, 527, 10.1530/REP-08-0175 Das, 2011, Expression of toll-like receptors and avian b-defensins and their changes in response to bacterial components in chicken sperm, Poult. Sci., 90, 417, 10.3382/ps.2010-00850 Dietz, 1969, Metabolism of bovine semen. XX. Role of ammonia in interactions between the citric acid and urea cycles, Biol. Reprod., 1, 200, 10.1095/biolreprod1.2.200 DiScipio, 1978, Activation of human factor IX (Christmas factor), J. Clin. Invest., 61, 1528, 10.1172/JCI109073 Douard, 2005, Role of seminal plasma in damage to Turkey spermatozoa during in vitro storage, Theriogenology, 63, 126, 10.1016/j.theriogenology.2004.03.020 Druart, 2013, Proteomic characterization and cross species comparison of mammalian seminal plasma, J. Proteome, 91, 13, 10.1016/j.jprot.2013.05.029 Dufour, 2002, IFN-γ-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking, J. Immunol., 168, 3195, 10.4049/jimmunol.168.7.3195 Elzanaty, 2007, Seminal plasma albumin: origin and relation to the male reproductive parameters, Andrologia, 39, 60, 10.1111/j.1439-0272.2007.00764.x Etches, 1996, The Male, 208 Fazeli, 2004, Sperm-induced modification of the oviductal gene expression profile after natural insemination in mice, Biol. Reprod., 71, 60, 10.1095/biolreprod.103.026815 Finkelstein, 2010, Role and regulation of sperm gelsolin prior to fertilization, J. Biol. Chem., 285, 39702, 10.1074/jbc.M110.170951 Frankham, 1972, Semen characteristics of lines selected for increased part-record egg production, Poult. Sci., 51, 1468, 10.3382/ps.0511468 Froman, 2011, A proteome-based model for sperm mobility phenotype, J. Anim. Sci., 89, 1330, 10.2527/jas.2010-3367 Fujihara, 1992, Accessory reproductive fluids and organs in male domestic birds, Worlds Poult. Sci. J., 48, 39, 10.1079/WPS19920005 Fukui, 2007, Fertility of ewes inseminated intrauterinally with frozen semen using extender containing bovine serum albumin, J. Reprod. Dev., 53, 959, 10.1262/jrd.19017 Gilmont, 1990, Seminal transferrin and spermatogenic capability in the bull, Biol. Reprod., 43, 151, 10.1095/biolreprod43.1.151 Harris, 1971, Changes in the protein concentration of chicken seminal plasma after rapid freeze–thaw, Cryobiology, 7, 209, 10.1016/0011-2240(70)90023-4 Holmes, 1982, Transferrin and gonadal dysfunction in man, Fertil. Steril., 38, 600, 10.1016/S0015-0282(16)46641-0 Hossain, 2007, Effect of fatty acids bound to bovine serum albumin-V on acrosome reaction and utilization of glucose in boar spermatozoa, Reprod. Med. Biol., 6, 109, 10.1111/j.1447-0578.2007.00173.x Johnsson, 2012, A sexual ornament in chickens is affected by pleiotropic alleles at HAO1 and BMP2, selected during domestication, PLoS Genet., 8, 10.1371/journal.pgen.1002914 Kareskoski, 2011, Protein composition of seminal plasma in fractionated stallion ejaculates, Reprod. Domest. Anim., 46, e79, 10.1111/j.1439-0531.2010.01641.x Katayama, 1979, Comparison of amino acid sequence of bovine coagulation factor IX (Christmas factor) with that of other vitamin K-dependant plasma proteins, Proc. Natl. Acad. Sci., 76, 4990, 10.1073/pnas.76.10.4990 Kelly, 2006, Characterization of bovine seminal plasma by proteomics, Proteomics, 6, 5826, 10.1002/pmic.200500830 Labas, 2015, Qualitative and quantitative peptidomic and proteomic approaches to phenotyping chicken semen, J. Proteome, 112, 313, 10.1016/j.jprot.2014.07.024 Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 LaFlamme, 2012, The Drosophila melanogaster seminal fluid protease “seminase” regulates proteolytic and post-mating reproductive process, PLoS Genet., 8, 10.1371/journal.pgen.1002435 Lwaleed, 2005, Quantitation of seminal factor IX and factor IXa in fertile, nonfertile, and vasectomy subjects: a step closer toward identifying a functional clotting system in human semen, J. Androl., 26, 146 Malik, 2013, Evaluation of the ejaculate quality of the red jungle fowl, domestic chicken, and bantam chicken in Malaysia, Turkish J. Vet. Anim. Sci., 37, 564, 10.3906/vet-1107-26 Mann, 1982, Passage of chemicals into human and animal semen: mechanisms and significance, Crit. Rev. Toxicol., 11, 1, 10.3109/10408448209089846 Marzoni, 2013, A proteomic approach to identify seminal plasma proteins in roosters (Gallus gallus domesticus), Anim. Reprod. Sci., 140, 216, 10.1016/j.anireprosci.2013.06.009 Matsuoka, 2006, Effects of bovine serum albumin and trehalose in semen diluents for improvement of frozen-thawed ram spermatozoa, J. Reprod. Dev., 52, 675, 10.1262/jrd.18033 Mi, 2016, PANTHER version10: expanded protein families and functions, and analysis tools, Nucleic Acids Res., 44, D336, 10.1093/nar/gkv1194 Michailidis, 2014, Activation of innate immune system in response to lipopolysaccharide in chicken sertoli cells, Reproduction, 148, 259, 10.1530/REP-14-0064 Milardi, 2013, Proteomics of human seminal plasma: identification of biomarkers candidates for fertility and infertility and the evolution of technology, Mol. Reprod. Dev., 80, 350, 10.1002/mrd.22178 Murugesan, 2013, Semen quality in white leghorn chicken selected for egg production traits, Turk. J. Vet. Anim. Sci., 37, 747, 10.3906/vet-1304-59 Nang, 2012, Bovine serum albumin: survival and osmolarity effect in bovine spermatozoa stored above freezing point, Andrologia, 44, 447, 10.1111/j.1439-0272.2011.01203.x Niranjan, 2001, Semen quality studies in two White Leghorn lines maintained at Tripura, Indian J. Poult. Sci., 36, 287 Nocera, 1995, Characterization of latent transforming growth factor-beta from human seminal plasma, Am. J. Reprod. Immunol., 33, 282, 10.1111/j.1600-0897.1995.tb00897.x Novak, 2010, Seminal plasma proteins as potential markers of relative fertility in boars, J. Androl., 31, 188, 10.2164/jandrol.109.007583 Ocón-Grove, 2010, NAMPT (visfatin) in the chicken testis: influence of sexual maturation on cellular localization, plasma levels and gene and protein expression, Reproduction, 139, 217, 10.1530/REP-08-0377 Perez-Patiño, 2016, Characterization of the porcine seminal plasma proteome comparing ejaculate portions, J. Proteome, 142, 15, 10.1016/j.jprot.2016.04.026 Pilch, 2006, Large-scale and high-confidence proteomic analysis of human seminal plasma, Genome Biol., 7, R40, 10.1186/gb-2006-7-5-r40 Ram, 2006, Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster, Proc. Natl. Acad. Sci., 103, 18674, 10.1073/pnas.0606228103 Robertson, 2005, Seminal plasma and male factor signaling in the female reproductive tract, Cell Tissue Res., 322, 43, 10.1007/s00441-005-1127-3 Robertson, 2002, Transforming growth factor β-a mediator of immune deviation in seminal plasma, J. Reprod. Immunol., 57, 109, 10.1016/S0165-0378(02)00015-3 Rodrigues, 2013, Seminal plasma proteins and their relationship with sperm motility in Santa Ines rams, Small Rumin. Res., 109, 94, 10.1016/j.smallrumres.2012.07.032 Rodríguez-Martínez, 1998, Immunoelectroscopic imaging of speradhesin AWN epitopes on boar spermatozoa bound in vivo to the zona pellucida, Reprod. Fertil. Dev., 10, 491, 10.1071/RD98111 Rodríguez-Martínez, 2008, Influence of seminal plasma on kinematics of boar spermatozoa during freezing, Theriogenology, 70, 1242, 10.1016/j.theriogenology.2008.06.007 Rodríguez-Martínez, 2011, Seminal plasma proteins: what role do they play?, Am. J. Reprod. Immunol., 66, 11, 10.1111/j.1600-0897.2011.01033.x Salvolini, 2013, Involvement of sperm plasma membrane and cytoskeletal proteins in human male infertility, Fertil. Steril., 99, 697, 10.1016/j.fertnstert.2012.10.042 Schjenken, 2014, Seminal fluid and immune adaptation for pregnancy-comparative biology in maternal species, Reprod. Domest. Anim., 49, 27, 10.1111/rda.12383 Sharma, 2013, Functional proteomic analysis of seminal plasma proteins in men with various semen parameters, Reprod. Biol. Endocrinol., 11, 38, 10.1186/1477-7827-11-38 Sirot, 2009, Molecular social interactions: Drosophila melanogaster seminal fluid proteins as a case study, Adv. Genet., 68, 23, 10.1016/S0065-2660(09)68002-0 Slowinska, 2015, Proteomic analysis of white and yellow seminal plasma in turkeys, J. Anim. Sci., 93, 2785, 10.2527/jas.2015-8912 Slowin'ska, 2014, Isolation of an ovoinhibitor, a multidomain kazal-like inhibitor from turkey (Meleagris gallopavo) seminal plasma, Biol. Reprod., 91, 108 Soggiu, 2013, Unravelling the bull fertility proteome, Mol. BioSyst., 9, 1188, 10.1039/c3mb25494a Soleilhavoup, 2014, Ram seminal plasma proteome and its impact on liquid preservation of spermatozoa, J. Proteome, 109, 245, 10.1016/j.jprot.2014.07.007 Soler, 2016, Intact cell MALDI-TOF MS on sperm: a molecular test for male fertility, Mol. Cell. Proteomics, 15, 1998, 10.1074/mcp.M116.058289 Song, 2016, Seminal plasma induces inflammation in the uterus through the γδT/IL-17 pathway, Sci. Rep., 6, 25118, 10.1038/srep25118 Srivastava, 1996, Cytokines of the human reproductive tract, Am. J. Reprod. Immunol., 36, 157, 10.1111/j.1600-0897.1996.tb00157.x Thurston, 1982, Elevated seminal plasma protein: a characteristic of yellow Turkey semen, Poult. Sci., 61, 1905, 10.3382/ps.0611905 Valenti, 1983, Studies of the antimicrobial activity of ovotransferrin, Int. J. Tissue React., 5, 97 Xia, 2009, The BSA-induced Ca(2+) influx during sperm capacitation is CATSPERM channel-dependent, Reprod. Biol. Endocrinol., 7, 119, 10.1186/1477-7827-7-119