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6 - Seminal Plasma Plays Important Roles in Fertility

Published online by Cambridge University Press:  25 May 2017

By
Susan S. Suarez  and
Mariana F. Wolfner
Edited by
Christopher J. De Jonge  and
Christopher L. R. Barratt
Foreword by
Ryuzo Yanagimachi
Christopher J. De Jonge
Affiliation:
University of Minnesota
Christopher L. R. Barratt
Affiliation:
University of Dundee
Ryuzo Yanagimachi
Affiliation:
University of Hawaii, Manoa
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Type
Chapter
Information
The Sperm Cell
Production, Maturation, Fertilization, Regeneration
 , pp. 88 - 108
Publisher: Cambridge University Press
Print publication year: 2017

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References

Batruch, I, Lecker, I, Kagedan, D, Smith, CR, Mullen, BJ, Grober, E et al. 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 2011; 10: 941–53.CrossRefGoogle ScholarPubMed
Rolland, AD, Lavigne, R, Dauly, C, Calvel, P, Kervarrec, C, Freour, T et al. Identification of genital tract markers in the human seminal plasma using an integrative genomics approach. Hum Reprod 2013; 28: 199–209.CrossRefGoogle ScholarPubMed
Milardi, D, Grande, G, Vincenzoni, F, Messana, I, Pontecorvi, A, De Marinis, L et al. Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil Steril 2012; 97: 67–73 e1.CrossRefGoogle ScholarPubMed
Pilch, B, Mann, M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 2006; 7: R40.CrossRefGoogle ScholarPubMed
Rodriguez-Martinez, H, Kvist, U, Ernerudh, J, Sanz, L, Calvete, JJ. Seminal plasma proteins: What role do they play? Am J Reprod Immunol 2011; 66: 11–22.CrossRefGoogle ScholarPubMed
Poiani, A. Complexity of seminal fluid: A review. Behav Ecol Sociobiol 2006; 60: 289–310.CrossRefGoogle Scholar
Avila, FW, Sirot, LK, LaFlamme, BA, Rubinstein, CD, Wolfner, MF. Insect seminal fluid proteins: Identification and function. Annu Rev Entomol 2011; 56: 21–40.CrossRefGoogle ScholarPubMed
Mueller, JL, Ripoll, DR, Aquadro, CF, Wolfner, MF. Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. Proc Natl Acad Sci USA 2004; 101: 13,542–7.CrossRefGoogle ScholarPubMed
Bromfield, JJ, Schjenken, JE, Chin, PY, Care, AS, Jasper, MJ, Robertson, SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci USA 2014; 111: 2,200–5.CrossRefGoogle ScholarPubMed
Dean, MD. Genetic disruption of the copulatory plug in mice leads to severely reduced fertility. PLoS Genet 2013; 9: e1003185.CrossRefGoogle ScholarPubMed
Kalb, JM, DiBenedetto, AJ, Wolfner, MF. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc Natl Acad Sci USA 1993; 90: 8,093–7.CrossRefGoogle ScholarPubMed
Chow, CY, Avila, FW, Clark, AG, Wolfner, MF. Induction of excessive endoplasmic reticulum stress in the Drosophila male accessory gland results in infertility. PloS One 2015; 10: e0119386.CrossRefGoogle ScholarPubMed
Gillott, C. Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annu Rev Entomol 2003; 48: 163–84.CrossRefGoogle ScholarPubMed
Crawford, G, Ray, A, Gudi, A, Shah, A, Homburg, R. The role of seminal plasma for improved outcomes during in vitro fertilization treatment: Review of the literature and meta-analysis. Hum Reprod Update 2015; 21: 275–84.CrossRefGoogle ScholarPubMed
Odet, F, Gabel, S, London, RE, Goldberg, E, Eddy, EM. Glycolysis and mitochondrial respiration in mouse LDHC-null sperm. Biol Reprod 2013; 88: 95, 1–7.CrossRefGoogle ScholarPubMed
Wang, Z, Widgren, EE, Richardson, RT, O'Rand, MG. Characterization of an eppin protein complex from human semen and spermatozoa. Biol Reprod 2007; 77: 476–84.CrossRefGoogle ScholarPubMed
Sullivan, R. Epididymosomes: A heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian J Androl 2015; 17: 726–9.CrossRefGoogle ScholarPubMed
Owen, DH, Katz, DF. A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J Androl 2005; 26: 459–69.CrossRefGoogle ScholarPubMed
Prins, GS, Lindgren, M. Accessory sex glands in the male. In: Plant, TM, Zeleznik, A (Eds.), Knobil and Neill's Physiology of Reproduction (4th ed.), Vol. 1. Elsevier, 2015: 773–804.CrossRefGoogle Scholar
Russo, CL, Spurr-Michaud, S, Tisdale, A, Pudney, J, Anderson, D, Gipson, IK. Mucin gene expression in human male urogenital tract epithelia. Hum Reprod 2006; 21: 2,783–93.CrossRefGoogle ScholarPubMed
Aalberts, M, Stout, TA, Stoorvogel, W. Prostasomes: Extracellular vesicles from the prostate. Reproduction 2014; 147: R1–14.CrossRefGoogle ScholarPubMed
Ross, M, Wojciech, P. Histology: A text and atlas: With correlated cell and molecular biology. Wolters Fluwer Health, 2016.Google Scholar
Abrahamsson, PA, Dizeyi, N, Alm, P, di Sant'Agnese, PA, Deftos, LJ, Aumuller, G. Calcitonin and calcitonin gene-related peptide in the human prostate gland. The Prostate 2000; 44: 181–6.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Finger, S, Schwieger, C, Arouri, A, Kerth, A, Blume, A. Interaction of linear polyamines with negatively charged phospholipids: The effect of polyamine charge distance. Biol Chem 2014; 395: 769–78.CrossRefGoogle ScholarPubMed
Lefevre, PL, Palin, MF, Murphy, BD. Polyamines on the reproductive landscape. Endocrine Rev 2011; 32: 694–712.CrossRefGoogle ScholarPubMed
Bouvet, JP, Gresenguet, G, Belec, L. Vaginal pH neutralization by semen as a cofactor of HIV transmission. Clin Microbiol Infect 1997; 3: 19–23.CrossRefGoogle ScholarPubMed
Kumar, V, Hassan, MI, Kashav, T, Singh, TP, Yadav, S. Heparin-binding proteins of human seminal plasma: Purification and characterization. Mol Reprod Dev 2008; 75: 1,767–74.CrossRefGoogle ScholarPubMed
Corrigan, L, Redhai, S, Leiblich, A, Fan, SJ, Perera, SM, Patel, R et al. BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior. J Cell Biol 2014; 206: 671–88.CrossRefGoogle ScholarPubMed
Bertram, M, Akerkar, GA, Ard, RL, Gonzalez, C, Wolfner, MF. Cell type specific gene expression in the Drosophila melanogaster male accessory gland. Mechs Dev 1992; 38: 33–40.CrossRefGoogle ScholarPubMed
Gligorov, D, Sitnik, JL, Maeda, RK, Wolfner, MF, Karch, F. A novel function for the Hox gene Abd-B in the male accessory gland regulates the long-term female post-mating response in Drosophila. PLoS Genet 2013; 9: e1003395.CrossRefGoogle ScholarPubMed
Iida, K, Cavener, DR. Glucose dehydrogenase is required for normal sperm storage and utilization in female Drosophila melanogaster. J Exp Biol 2004; 207: 675–81.CrossRefGoogle ScholarPubMed
Richmond, RC, Gilbert, DG, Sheehan, KB, Gromko, MH, Butterworth, FM. Esterase 6 and reproduction in Drosophila melanogaster. Science 1980; 207: 1,483–5.CrossRefGoogle ScholarPubMed
Avila, FW, Cohen, AB, Ameerudeen, FS, Duneau, D, Suresh, S, Mattei, AL et al. Retention of ejaculate by Drosophila melanogaster females requires the male-derived mating plug protein PEBme. Genetics 2015; 200: 1,171–9.CrossRefGoogle ScholarPubMed
Bretman, A, Lawniczak, MK, Boone, J, Chapman, T. A mating plug protein reduces early female remating in Drosophila melanogaster. J Insect Physiol 2010; 56: 107–13.CrossRefGoogle ScholarPubMed
Chin, JS, Ellis, SR, Pham, HT, Blanksby, SJ, Mori, K, Koh, QL et al. Sex-specific triacylglycerides are widely conserved in Drosophila and mediate mating behavior. eLife 2014; 3: e01751.CrossRefGoogle ScholarPubMed
Guiraudie-Capraz, G, Pho, DB, Jallon, JM. Role of the ejaculatory bulb in biosynthesis of the male pheromone cis-vaccenyl acetate in Drosophila melanogaster. Integrative Zool 2007; 2: 89–99.CrossRefGoogle ScholarPubMed
Ludwig, MZ, Uspensky, II, Ivanov, AI, Kopantseva, MR, Dianov, CM, Tamarina, NA et al. Genetic-control and expression of the major ejaculatory bulb protein (Peb-Me) in Drosophila-melanogaster. Biochem Genet 1991; 29: 215–39.CrossRefGoogle ScholarPubMed
Lung, O, Wolfner, MF. Drosophila seminal fluid proteins enter the circulatory system through the walls of the posterior vagina. Insect Biochem Mol Biol 1999; 29: 1,043–52.CrossRefGoogle Scholar
Laflamme, BA, Wolfner, MF. Identification and function of proteolysis regulators in seminal fluid. Mol Reprod Dev 2013; 80: 80–101.CrossRefGoogle ScholarPubMed
Monsma, SA, Wolfner, MF. Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor. Genes Dev 1988; 2: 1,063–73.CrossRefGoogle ScholarPubMed
Bertram, MJ, Neubaum, DM, Wolfner, MF. Localization of the Drosophila accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem Mol Biol 1996; 26: 971–80.CrossRefGoogle ScholarPubMed
LaFlamme, BA, Ram, KR, Wolfner, MF. The Drosophila melanogaster seminal fluid protease “seminase” regulates proteolytic and post-mating reproductive processes. PLoS Genet 2012; 8: e1002435.CrossRefGoogle ScholarPubMed
Laflamme, BA, Avila, FW, Michalski, K, Wolfner, MF. A Drosophila protease cascade member, seminal metalloprotease-1, is activated stepwise by male factors and requires female factors for full activity. Genetics 2014; 196: 1,117–29.CrossRefGoogle ScholarPubMed
Carlson, AE, Hille, B, Babcock, DF. External Ca2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. Dev Biol 2007; 312: 183–92.CrossRefGoogle ScholarPubMed
Luconi, M, Porazzi, I, Ferruzzi, P, Marchiani, S, Forti, G, Baldi, E. Tyrosine phosphorylation of the a kinase anchoring protein 3 (AKAP3) and soluble adenylate cyclase are involved in the increase of human sperm motility by bicarbonate. Biol Reprod 2005; 72: 22–32.CrossRefGoogle ScholarPubMed
Visconti, PE. Understanding the molecular basis of sperm capacitation through kinase design. Proc Natl Acad Sci USA 2009; 106: 667–8.CrossRefGoogle ScholarPubMed
Rogers, DW, Baldini, F, Battaglia, F, Panico, M, Dell, A, Morris, HR et al. Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol 2009; 7: e1000272.CrossRefGoogle ScholarPubMed
Mitchell, SN, Kakani, EG, South, A, Howell, PI, Waterhouse, RM, Catteruccia, F. Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes. Science 2015; 347: 985–8.CrossRefGoogle ScholarPubMed
Polak, M, Starmer, WT, Barker, JSF. A mating plug and male mate choice in Drosophila hibisci Bock. Anim Behav 1998; 56: 919–26.CrossRefGoogle Scholar
Lilja, H, Abrahamsson, PA, Lundwall, A. Semenogelin, the predominant protein in human semen. Primary structure and identification of closely related proteins in the male accessory sex glands and on the spermatozoa. J Biol Chem 1989; 264: 1,894–90.CrossRefGoogle ScholarPubMed
Silva, EJ, Hamil, KG, O'Rand, MG. Interacting proteins on human spermatozoa: Adaptive evolution of the binding of semenogelin I to EPPIN. PloS One 2013; 8: e82014.CrossRefGoogle ScholarPubMed
Sobrero, AJ, Macleod, J. The immediate postcoital test. Fertil Steril 1962; 13: 184–9.CrossRefGoogle ScholarPubMed
Tollner, TL, Yudin, AI, Treece, CA, Overstreet, JW, Cherr, GN. Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus. Hum Reprod 2008; 23: 2,523–34.CrossRefGoogle ScholarPubMed
Tollner, TL, Venners, SA, Hollox, EJ, Yudin, AI, Liu, X, Tang, G et al. A common mutation in the defensin DEFB126 causes impaired sperm function and subfertility. Sci Transl Med 2011; 3: 92ra65.CrossRefGoogle ScholarPubMed
Salois, D, Menard, M, Paquette, Y, Manjunath, P. Complementary deoxyribonucleic acid cloning and tissue expression of BSP-A3 and BSP-30-kDa: Phosphatidylcholine and heparin-binding proteins of bovine seminal plasma. Biol Reprod 1999; 61: 288–97.CrossRefGoogle ScholarPubMed
Desnoyers, L, Manjunath, P. Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J Biol Chem 1992; 267: 10,149–55.CrossRefGoogle ScholarPubMed
Muller, P, Erlemann, KR, Muller, K, Calvete, JJ, Topfer-Petersen, E, Marienfeld, K et al. Biophysical characterization of the interaction of bovine seminal plasma protein PDC-109 with phospholipid vesicles. Eur Biophys J: EBJ 1998; 27 33–41.Google ScholarPubMed
Gwathmey, TM, Ignotz, GG, Mueller, JL, Manjunath, P, Suarez, SS. Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct. Biol Reprod 2006; 75: 501–7.CrossRefGoogle ScholarPubMed
Greube, A, Muller, K, Topfer-Petersen, E, Herrmann, A, Muller, P. Influence of the bovine seminal plasma protein PDC-109 on the physical state of membranes. Biochemistry 2001; 40: 8,326–34.CrossRefGoogle ScholarPubMed
Muller, P, Greube, A, Topfer-Petersen, E, Herrmann, A. Influence of the bovine seminal plasma protein PDC-109 on cholesterol in the presence of phospholipids. Eur Biophys J 2002; 31: 438–47.Google ScholarPubMed
Soubeyrand, S, Manjunath, P. Novel seminal phospholipase A2 is inhibited by the major proteins of bovine seminal plasma. Biochim Biophys Acta 1997; 1,341: 183–8.Google Scholar
Racey, PA, Uchida, TA, Mori, T, Avery, MI, Fenton, MB. Sperm-epithelium relationships in relation to the time of insemination in little brown bats (Myotis lucifugus). J Reprod Fertil 1987; 80: 445–54.Google Scholar
Wilcox, AJ, Weinberg, CR, Baird, DD. Timing of sexual intercourse in relation to ovulation. Effects on the probability of conception, survival of the pregnancy, and sex of the baby. N Engl J Med 1995; 333: 1,517–21.CrossRefGoogle ScholarPubMed
Baillie, HS, Pacey, AA, Warren, MA, Scudamore, IW, Barratt, CL. Greater numbers of human spermatozoa associate with endosalpingeal cells derived from the isthmus compared with those from the ampulla. Hum Reprod 1997; 12: 1,985–92.CrossRefGoogle ScholarPubMed
Nauc, V, Manjunath, P. Radioimmunoassays for bull seminal plasma proteins (BSP-A1/-A2, BSP-A3, and BSP-30-Kilodaltons), and their quantification in seminal plasma and sperm. Biol Reprod 2000; 63: 1,058–66.CrossRefGoogle Scholar
Lefebvre, J, Fan, J, Chevalier, S, Sullivan, R, Carmona, E, Manjunath, P. Genomic structure and tissue-specific expression of human and mouse genes encoding homologues of the major bovine seminal plasma proteins. Mol Hum Reprod 2007; 13: 45–53.CrossRefGoogle ScholarPubMed
Lefebvre, J, Boileau, G, Manjunath, P. Recombinant expression and affinity purification of a novel epididymal human sperm-binding protein, BSPH1. Mol Hum Reprod 2009; 15: 105–14.Google ScholarPubMed
Tollner, TL, Yudin, AI, Tarantula, AF, Greece, CA, Overstreet, JA, Cherr, GN. Beta-defensin 126 on the surface of macaque sperm mediates attachment of sperm to oviductal epithelia. Biol Reprod 2008; 78: 400–12.CrossRefGoogle ScholarPubMed
Adams, EM, Wolfner, MF. Seminal proteins but not sperm induce morphological changes in the Drosophila melanogaster female reproductive tract during sperm storage. J Insect Physiol 2007; 53: 319–31.CrossRefGoogle Scholar
Mattei, AL, Riccio, ML, Avila, FW, Wolfner, MF. Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning. Proc Natl Acad Sci USA 2015; 112: 8,475–80.CrossRefGoogle ScholarPubMed
Avila, FW, Wolfner, MF. Acp36DE is required for uterine conformational changes in mated Drosophila females. Proc Natl Acad Sci USA 2009; 106: 15,796–680.CrossRefGoogle ScholarPubMed
Hung, PH, Suarez, SS. Alterations to the bull sperm surface proteins that bind sperm to oviductal epithelium. Biol Reprod 2012; 87: 88.Google Scholar
Gromko, MH, Gilbert, DG, Richmond, RC. Sperm transfer and use in the multiple mating system of Drosophila. In: Smith, RL (Ed.), Sperm Competition and the Evolution of Mating Systems. Academic Press, 1984: 371–426.CrossRefGoogle Scholar
Avila, FW, Ravi Ram, K, Bloch Qazi, MC, Wolfner, MF. Sex peptide is required for the efficient release of stored sperm in mated Drosophila females. Genetics 2010; 186: 595–600.CrossRefGoogle ScholarPubMed
Yapici, N, Kim, YJ, Ribeiro, C, Dickson, BJ. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 2008; 451: 33–7.CrossRefGoogle ScholarPubMed
Avila, FW, Mattei, AL, Wolfner, MF. Sex peptide receptor is required for the release of stored sperm by mated Drosophila melanogaster females. J Insect Physiol 2015; 76: 1–6.CrossRefGoogle ScholarPubMed
Heifetz, Y, Lindner, M, Garini, Y, Wolfner, MF. Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract. Curr Biol 2014; 24: 731–7.CrossRefGoogle ScholarPubMed
Rezaval, C, Nojima, T, Neville, MC, Lin, AC, Goodwin, SF. Sexually dimorphic octopaminergic neurons modulate female postmating behaviors in Drosophila. Curr Biol 2014; 24: 725–30.CrossRefGoogle ScholarPubMed
Peng, J, Chen, S, Busser, S, Liu, H, Honegger, T, Kubli, E. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr Biol 2005; 15: 207–13.CrossRefGoogle ScholarPubMed
Araki, N, Trencsenyi, G, Krasznai, ZT, Nizsaloczki, E, Sakamoto, A, Kawano, N et al. Seminal vesicle secretion 2 acts as a protectant of sperm sterols and prevents ectopic sperm capacitation in mice. Biol Reprod 2015; 92: 8.CrossRefGoogle ScholarPubMed
de Lamirande, E, Lamothe, G. Levels of semenogelin in human spermatozoa decrease during capacitation: Involvement of reactive oxygen species and zinc. Hum Reprod 2010; 25: 1,619–30.CrossRefGoogle ScholarPubMed
de Lamirande, E, Yoshida, K, Yoshiike, TM, Iwamoto, T, Gagnon, C. Semenogelin, the main protein of semen coagulum, inhibits human sperm capacitation by interfering with the superoxide anion generated during this process. J Androl 2001; 22: 672–9.CrossRefGoogle ScholarPubMed
Manjunath, P, Therien, I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 2002; 53: 109–19.CrossRefGoogle ScholarPubMed
Parrish, JJ, Susko-Parrish, J, Winer, MA, First, NL. Capacitation of bovine sperm by heparin. Biol Reprod 1988; 38: 1,171–80.CrossRefGoogle ScholarPubMed
Mann, T, Lutwak-Mann, C. Male reproductive function and semen. Springer Verlag, 1981.CrossRefGoogle Scholar
Popat, A, Crankshaw, DJ. Variable responses to prostaglandin E(2) in human non-pregnant myometrium. Eur J Pharmacology 2001; 416: 145–52.CrossRefGoogle ScholarPubMed
Sasanami, T, Izumi, S, Sakurai, N, Hirata, T, Mizushima, S, Matsuzaki, M et al. A unique mechanism of successful fertilization in a domestic bird. Sci Rep 2015; 5: 7,700.CrossRefGoogle Scholar
Overstreet, JW, Cooper, GW. Sperm transport in the reproductive tract of the female rabbit: I. The rapid transit phase of transport. Biol Reprod 1978; 19: 101–14.Google ScholarPubMed
de Araujo Pereira, RR, Bruschi, ML. Vaginal mucoadhesive drug delivery systems. Drug Dev Ind Pharm 2012; 38: 643–52.CrossRefGoogle ScholarPubMed
Loher, W, Ganjian, I, Kubo, I, Stanley-Samuelson, D, Tobe, SS. Prostaglandins: Their role in egg-laying of the cricket Teleogryllus commodus. Proc Natl Acad Sci USA 1981; 78: 7,835–8.CrossRefGoogle ScholarPubMed
Dubrovsky, EB, Dubrovskaya, VA, Berger, EM. Juvenile hormone signaling during oogenesis in Drosophila melanogaster. Insect Biochem Mol Biol 2002; 32: 1,555–65.CrossRefGoogle ScholarPubMed
Audit-Lamour, C, Busson, D. Oogenesis defects in the ecd-1 mutant of Drosophila melanogaster, deficient in ecdysteroid at high temperature. J Insect Physiol 1981; 27: 829–37.CrossRefGoogle Scholar
Riddiford, LM. How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocrinol 2012; 179: 477–84.CrossRefGoogle Scholar
Gabrieli, P, Kakani, EG, Mitchell, SN, Mameli, E, Want, EJ, Mariezcurrena Anton, A et al. Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae. Proc Natl Acad Sci USA 2014; 111: 16,353–8.CrossRefGoogle ScholarPubMed
Borovsky, D, Carlson, DA, Hancock, RG, Rembold, H, van Handel, E. De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito. Insect Biochem Mol Biol 1994; 24: 437–44.CrossRefGoogle ScholarPubMed
Clifton, ME, Correa, S, Rivera-Perez, C, Nouzova, M, Noriega, FG. Male Aedes aegypti mosquitoes use JH III transferred during copulation to influence previtellogenic ovary physiology and affect the reproductive output of female mosquitoes. J Insect Physiol 2014; 64: 40–7.CrossRefGoogle ScholarPubMed
Moshitzky, P, Fleischmann, I, Chaimov, N, Saudan, P, Klauser, S, Kubli, E et al. Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch Insect Biochem Physiol 1996; 32: 363–74.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Reiff, T, Jacobson, J, Cognigni, P, Antonello, Z, Ballesta, E, Tan, KJ et al. Endocrine remodelling of the adult intestine sustains reproduction in Drosophila. eLife 2015; 4: e06930.CrossRefGoogle ScholarPubMed
Soller, M, Bownes, M, Kubli, E. Control of oocyte maturation in sexually mature Drosophila females. Dev Biol 1999; 208: 337–51.CrossRefGoogle ScholarPubMed
Bontonou, G, Shaik, HA, Denis, B, Wicker-Thomas, C. Acp70A regulates Drosophila pheromones through juvenile hormone induction. Insect Biochem Mol Biol 2015; 56: 36–49.CrossRefGoogle ScholarPubMed
Kamimura, Y. Copulation anatomy of Drosophila melanogaster (Diptera: Drosophilidae): Wound-making organs and their possible roles. Zoomorphology 2010; 129: 163–74.CrossRefGoogle Scholar
McGraw, LA, Gibson, G, Clark, AG, Wolfner, MF. Genes regulated by mating, sperm or seminal proteins in mated female Drosophila melanogaster. Curr Biol 2004; 14: 1,509–14.CrossRefGoogle ScholarPubMed
Lawniczak, MK, Begun, DJ. A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 2004; 47: 900–10.CrossRefGoogle ScholarPubMed
Innocenti, P, Morrow, EH. Immunogenic males: A genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females. J Evol Biol 2009; 22: 964–73.CrossRefGoogle Scholar
Short, SM, Wolfner, MF, Lazzaro, BP. Female Drosophila melanogaster suffer reduced defense against infection due to seminal fluid components. J Insect Physiol 2012; 58: 1,192–201.CrossRefGoogle ScholarPubMed
Gioti, A, Wigby, S, Wertheim, B, Schuster, E, Martinez, P, Pennington, CJ et al. Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proc Biol Sci 2012; 279: 4,423–32.Google ScholarPubMed
Kapelnikov, A, Zelinger, E, Gottlieb, Y, Rhrissorrakrai, K, Gunsalus, KC, Heifetz, Y. Mating induces an immune response and developmental switch in the Drosophila oviduct. Proc Natl Acad Sci USA 2008; 105: 13,912–7.CrossRefGoogle ScholarPubMed
Mack, PD, Kapelnikov, A, Heifetz, Y, Bender, M. Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. Proc Natl Acad Sci USA 2006; 103: 10,358–63.CrossRefGoogle ScholarPubMed
Peng, J, Zipperlen, P, Kubli, E. Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr Biol 2005; 15: 1,690–4.CrossRefGoogle ScholarPubMed
McGraw, LA, Clark, AG, Wolfner, MF. Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 2008; 179: 1,395–408.CrossRefGoogle ScholarPubMed
Heifetz, Y, Wolfner, MF. Seminal fluid and mating mediate changes in nerve termini innervating the Drosophila reproductive tract. Proc Natl Acad Sci USA 2004; 101: 6,261–6.CrossRefGoogle Scholar
Neubaum, DM, Wolfner, MF. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 1999; 153: 845–57.CrossRefGoogle ScholarPubMed
Bloch Qazi, MC, Wolfner, MF. An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. J Exp Biol 2003; 206: 3,521–8.Google ScholarPubMed
Staples, RE. Behavioural induction of ovulation in the oestrous rabbit. J Reprod Fertil 1967; 13: 429–35.Google ScholarPubMed
Ratto, MH, Leduc, YA, Valderrama, XP, van Straaten, KE, Delbaere, LT, Pierson, RA et al. The nerve of ovulation-inducing factor in semen. Proc Natl Acad Sci USA 2012; 109: 15,042–7.CrossRefGoogle ScholarPubMed
Adams, GP, Ratto, MH. Ovulation-inducing factor in seminal plasma: A review. Anim Reprod Sci 2013; 136: 148–56.CrossRefGoogle ScholarPubMed
Pan, G, Chen, Z, Liu, X, Li, D, Xie, Q, Ling, F et al. Isolation and purification of the ovulation-inducing factor from seminal plasma in the Bactrian camel (Camelus bactrianus). Theriogenology 2001; 55: 1,863–79.CrossRefGoogle ScholarPubMed
Bogle, OA, Ratto, MH, Adams, GP. Ovulation-inducing factor (OIF) induces LH secretion from pituitary cells. Anim Reprod Sci 2012; 133: 117–22.CrossRefGoogle ScholarPubMed
Tanco, VM, Van Steelandt, MD, Ratto, MH, Adams, GP. Effect of purified llama ovulation-inducing factor (OIF) on ovarian function in cattle. Theriogenology 2012; 78: 1,030–9.CrossRefGoogle ScholarPubMed
Tribulo, P, Bogle, O, Mapletoft, RJ, Adams, GP. Bioactivity of ovulation inducing factor (or nerve growth factor) in bovine seminal plasma and its effects on ovarian function in cattle. Theriogenology 2015; 83: 1,394–401.CrossRefGoogle ScholarPubMed
Waberski, D, Claassen, R, Hahn, T, Jungblut, PW, Parvizi, N, Kallweit, E et al. LH profile and advancement of ovulation after transcervical infusion of seminal plasma at different stages of oestrus in gilts. J Reprod Fertil 1997; 109: 29–34.CrossRefGoogle ScholarPubMed
Waberski, D, Sudhoff, H, Hahn, T, Jungblut, PW, Kallweit, E, Calvete, JJ et al. Advanced ovulation in gilts by the intrauterine application of a low molecular mass pronase-sensitive fraction of boar seminal plasma. J Reprod Fertil 1995; 105: 247–52.Google ScholarPubMed
Chapman, T, Bangham, J, Vinti, G, Seifried, B, Lung, O, Wolfner, MF et al. The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference. Proc Natl Acad Sci USA 2003; 100: 9,923–8.CrossRefGoogle ScholarPubMed
Liu, H, Kubli, E. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc Natl Acad Sci USA 2003; 100: 9,929–33.CrossRefGoogle ScholarPubMed
Chapman, T, Herndon, LA, Heifetz, Y, Partridge, L, Wolfner, MF. The Acp26Aa seminal fluid protein is a modulator of early egg hatchability in Drosophila melanogaster. Proc Biol Sci 2001; 268: 1,647–54.CrossRefGoogle ScholarPubMed
Heifetz, Y, Lung, O, Frongillo, EA Jr., Wolfner, MF. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol 2000; 10: 99–102.CrossRefGoogle ScholarPubMed
Herndon, LA, Wolfner, MF. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc Natl Acad Sci USA 1995; 92: 10,114–8.CrossRefGoogle ScholarPubMed
Rubinstein, CD, Wolfner, MF. Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. Proc Natl Aca Sci USA 2013; 110: 17,420–5.CrossRefGoogle ScholarPubMed
Roeder, T. Octopamine in invertebrates. Prog Neurobiol 1999; 59: 533–61.CrossRefGoogle ScholarPubMed
Monastirioti, M. Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev Biol 2003; 264: 38–49.CrossRefGoogle ScholarPubMed
Monastirioti, M, Linn, CE, White, K. Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 1996; 16: 3,900–11.CrossRefGoogle ScholarPubMed
Lee, HG, Seong, CS, Kim, YC, Davis, RL, Han, KA. Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. Dev Biol 2003; 264: 179–90.CrossRefGoogle ScholarPubMed
Lim, J, Sabandal, PR, Fernandez, A, Sabandal, JM, Lee, HG, Evans, P et al. The octopamine receptor Octbeta2R regulates ovulation in Drosophila melanogaster. PloS One 2014; 9: e104441.CrossRefGoogle ScholarPubMed
Li, Y, Fink, C, El-Kholy, S, Roeder, T. The octopamine receptor octss2R is essential for ovulation and fertilization in the fruit fly Drosophila melanogaster. Arch Insect Biochem Physiol 2015; 88: 168–78.CrossRefGoogle ScholarPubMed
Middleton, CA, Nongthomba, U, Parry, K, Sweeney, ST, Sparrow, JC, Elliott, CJ. Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary. BMC Biol 2006; 4: 17.CrossRefGoogle ScholarPubMed
Schjenken, JE, Robertson, SA. Seminal fluid signalling in the female reproductive tract: Implications for reproductive success and offspring health. Adv Exp Med Biol 2015; 868: 127–58.CrossRefGoogle ScholarPubMed
Guerin, LR, Prins, JR, Robertson, SA. Regulatory T-cells and immune tolerance in pregnancy: A new target for infertility treatment? Hum Reprod Update 2009; 15: 517–35.CrossRefGoogle ScholarPubMed
Robertson, SA, Guerin, LR, Bromfield, JJ, Branson, KM, Ahlstrom, AC, Care, AS. Seminal fluid drives expansion of the CD4+CD25+T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol Reprod 2009; 80: 1,036–45.CrossRefGoogle ScholarPubMed
Robertson, SA, Mau, VJ, Tremellen, KP, Seamark, RF. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil 1996; 107: 265–77.Google ScholarPubMed
Schjenken, JE, Glynn, DJ, Sharkey, DJ, Robertson, SA. TLR4 signaling is a major mediator of the female tract response to seminal fluid in mice. Biol Reprod 2015; 93: 68.CrossRefGoogle Scholar
Sharkey, DJ, Tremellen, KP, Jasper, MJ, Gemzell-Danielsson, K, Robertson, SA. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol 2012; 188: 2,445–54.CrossRefGoogle ScholarPubMed
Gutsche, S, von Wolff, M, Strowitzki, T, Thaler, CJ. Seminal plasma induces mRNA expression of IL-1beta, IL-6 and LIF in endometrial epithelial cells in vitro. Mol Hum Reprod 2003; 9: 785–91.CrossRefGoogle ScholarPubMed
Saftlas, AF, Rubenstein, L, Prater, K, Harland, KK, Field, E, Triche, EW. Cumulative exposure to paternal seminal fluid prior to conception and subsequent risk of preeclampsia. J Reprod Immunol 2014; 101–2: 104–10.Google Scholar
Rooney, IA, Heuser, JE, Atkinson, JP. GPI-anchored complement regulatory proteins in seminal plasma. An analysis of their physical condition and the mechanisms of their binding to exogenous cells. J Clin Invest 1996; 97: 1,675–86.CrossRefGoogle ScholarPubMed
Tecle, E, Gagneux, P. Sugar-coated sperm: Unraveling the functions of the mammalian sperm glycocalyx. Mol Reprod Dev 2015; 82: 635–50.CrossRefGoogle ScholarPubMed
Yudin, AI, Generao, SE, Tollner, TL, Treece, CA, Overstreet, JW, Cherr, GN. Beta-defensin 126 on the cell surface protects sperm from immunorecognition and binding of anti-sperm antibodies. Biol Reprod 2005; 73: 1,243–52.CrossRefGoogle ScholarPubMed
Fedorka, KM, Linder, JE, Winterhalter, W, Promislow, D. Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc Biol Sci 2007; 274: 1,211–7.Google ScholarPubMed
Schwenke, RA, Lazzaro, BP, Wolfner, MF. Reproduction–immunity trade-offs in insects. Annu Rev Entomol 2016; 61: 239–56.CrossRefGoogle ScholarPubMed
Otti, O. Genitalia-associated microbes in insects. Insect Sci 2015; 22: 325–39.CrossRefGoogle ScholarPubMed
Knell, RJ, Webberley, KM. Sexually transmitted diseases of insects: Distribution, evolution, ecology and host behaviour. Biol Rev Cambridge Philos Soc 2004; 79: 557–81.CrossRefGoogle ScholarPubMed
Cognigni, P, Bailey, AP, Miguel-Aliaga, I. Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab 2011; 13: 92–104.CrossRefGoogle ScholarPubMed
Apger-McGlaughon, J, Wolfner, MF. Post-mating change in excretion by mated Drosophila melanogaster females is a long-term response that depends on sex peptide and sperm. J Insect Physiol 2013; 59: 1,024–30.CrossRefGoogle ScholarPubMed
Edman, JD. Rate of digestion of vertebrate blood in Aedes aegypti (L.). Effect of age, mating, and parity. Am J Trop Med Hyg 1970; 1970: 1,031–3.Google Scholar
Carvalho, GB, Kapahi, P, Anderson, DJ, Benzer, S. Allocrine modulation of appetite by the sex peptide of Drosophila. Curr Biol: CB 2006; 16: 692–6.CrossRefGoogle Scholar
Ribeiro, C, Dickson, BJ. Sex peptide receptor and neuronal TOR/S6K signalling modulate nutrient balancing in Drosophila. Curr Biol 2010; 20: 1,000–5.CrossRefGoogle ScholarPubMed
Isaac, RE, Li, C, Leedale, AE, Shirras, AD. Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female. Proc Biol Sci 2010; 277: 65–70.Google ScholarPubMed
Eliyahu, D, Nagalakshmi, V, Applebaum, SW, Kubli, E, Choffat, Y, Rafaeli, A. Inhibition of pheromone biosynthesis in Helicoverpa armigera by pheromonostatic peptides. J Insect Physiol 2003; 49: 569–74.CrossRefGoogle ScholarPubMed
Kingan, TG, Thomas-Laemont, PA, Raina, AK. Male accessory gland factors elicit change from “virgin” to “mated” behaviour in the female corn earworm moth Helicoverpa zea. J Exp Biol 1993; 183: 61–76.CrossRefGoogle Scholar
Hasemeyer, M, Yapici, N, Heberlein, U, Dickson, BJ. Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 2009; 61: 511–8.CrossRefGoogle ScholarPubMed
Yang, CH, Rumpf, S, Xiang, Y, Gordon, MD, Song, W, Jan, LY et al. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 2009; 61: 519–26.CrossRefGoogle ScholarPubMed
Rezaval, C, Pavlou, HJ, Dornan, AJ, Chan, YB, Kravitz, EA, Goodwin, SF. Neural circuitry underlying Drosophila female postmating behavioral responses. Curr Biol 2012; 22: 1,155–65.CrossRefGoogle ScholarPubMed
Scott, D. Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females. Proc Natl Acad Sci USA 1986; 83: 8,429–33.CrossRefGoogle ScholarPubMed
Ejima, A, Smith, BP, Luca, C, van der Boes van, Naters W, MIller, CJ, Carlson, JR et al. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 2007; 17: 599–605.CrossRefGoogle ScholarPubMed
Kawano, N, Araki, N, Yoshida, K, Hibino, T, Ohnami, N, Makino, M et al. Seminal vesicla protein SVS2 is required for sperm survival in the uterus. Proc Natl Acad Sci USA 2014; 111: 4,145–50.CrossRefGoogle Scholar
Sirot, LK, Findlay, GD, Sitnik, JL, Frasheri, D, Avila, FW, Wolfner, MF. Molecular characterization and evolution of a gene family encoding both female- and male-specific reproductive proteins in Drosophila. Mol Biol Evol 2014; 31: 1,554–67.CrossRefGoogle ScholarPubMed
Clark, NL, Swanson, WJ. Pervasive adaptive evolution in primate seminal proteins. PLoS Genet 2005; 1: e35.CrossRefGoogle ScholarPubMed
Panhuis, TM, Clark, NL, Swanson, WJ. Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc London B Biol Sci 2006; 361: 261–8.CrossRefGoogle ScholarPubMed
Swanson, WJ, Vacquier, VD. The rapid evolution of reproductive proteins. Nat Rev Genet 2002; 3: 137–44.CrossRefGoogle ScholarPubMed
Parker, GA. Sperm competition and its evolutionary consequences in the insects. Biol Rev 1970; 45: 525–67.CrossRefGoogle Scholar
Dorus, S, Evans, PD, Wyckoff, GJ, Choi, SS, Lahn, BT. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 2004; 36: 1,326–9.CrossRefGoogle ScholarPubMed
Chapman, T, Arnqvist, G, Bangham, J, Rowe, L. Sexual conflict. Trends Ecol Evol 2003; 18: 41–7.CrossRefGoogle Scholar

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