Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

Role of Seminal Plasma Proteins in Effective Zygote Formation- A Success Road to Pregnancy

Author(s): Archana Kumar, T.B. Sridharn* and Kamini A. Rao

Volume 26, Issue 4, 2019

Page: [238 - 250] Pages: 13

DOI: 10.2174/0929866526666190208112152

Price: $65

Abstract

Seminal plasma proteins contributed by secretions of accessory glands plays a copious role in fertilization. Their role is overlooked for decades and even now, as Artificial Reproduction Techniques (ART) excludes the plasma components in the procedures. Recent evidences suggest the importance of these proteins starting from imparting fertility status to men, fertilization and till successful implantation of the conceptus in the female uterus. Seminal plasma is rich in diverse proteins, but a major part of the seminal plasma is constituted by very lesser number of proteins. This makes isolation and further research on non abundant protein a tough task. With the advent of much advanced proteomic techniques and bio informatics tools, studying the protein component of seminal plasma has become easy and promising. This review is focused on the role of seminal plasma proteins on various walks of fertilization process and thus, the possible exploitation of seminal plasma proteins for understanding the etiology of male related infertility issues. In addition, a compilation of seminal plasma proteins and their functions has been done.

Keywords: Male infertility, seminar plasma, artificial reproduction techniques, accessory reproductive glands, immunomodulatory seminal proteins, fertilization.

Graphical Abstract

[1]
Beyler, S.A.; Zaneveld, L.J. The male accessory sex glands; Biochem. Mammal. Reprod, 1982, pp. 65-88.
[2]
Abdelbaki, S.A.; Sabry, J.H.; Al-Adl, A.M.; Sabry, H.H. The impact of coexisting sperm DNA fragmentation and seminal oxidative stress on the outcome of varicocelectomy in infertile patients: A prospective controlled study. Arab J. Urol., 2017, 15(2), 131-139.
[3]
Gilany, K.; Minai-Tehrani, A.; Savadi-Shiraz, E.; Rezadoost, H.; Lakpour, N. Exploring the human seminal plasma proteome: An unexplored gold mine of biomarker for male infertility and male reproduction disorder. J. Reprod. Infertil., 2015, 16(2), 61.
[4]
Jodar, M.; Soler-Ventura, A.; Oliva, R. Molecular biology of reproduction and development research group. semen proteomics and male infertility. J. Proteomics, 2017, 162, 125-134.
[5]
Philippov, O.; Radionchenko, A.; Bolotova, V.; Voronovskaya, N.; Potemkina, T. Estimation of the prevalence and causes of infertility in western Siberia. Bull. World Health Organ., 1998, 76(2), 183.
[6]
Dacheux, J.L.; Dacheux, F.; Druart, X. Epididymal protein markers and fertility. Anim. Reprod. Sci., 2016, 169, 76-87.
[7]
Ruiz‐Pesini, E.; Alvarez, E.; Enríquez, J.A.; López-Pérez, M.J. Association between seminal plasma carnitine and sperm mitochondrial enzymatic activities. Int. J. Androl., 2001, 24(6), 335-340.
[8]
Yeung, C.H.; Schröter, S.; Wagenfeld, A.; Kirchhoff, C.; Kliesch, S.; Poser, D.; Weinbauer, G.; Nieschlag, E.; Cooper, T. Interaction of the human epididymal protein CD52 (HE5) with epididymal spermatozoa from men and cynomolgus monkeys. Mol. Reprod. Develop. Incorporat. Gamete Res., 1997, 48(2), 267-275.
[9]
O’Bryan, M.; Baker, H.; Saunders, J.; Kirszbaum, L.; Walker, I.; Hudson, P.; Liu, D.; Glew, M.; d’Apice, A.; Murphy, B. Human seminal clusterin (SP-40, 40). Isolation and characterization. J. Clin. Invest., 1990, 85(5), 1477-1486.
[10]
Zalata, A.; El-Samanoudy, A.Z.; Shaalan, D.; El-Baiomy, Y.; Taymour, M.; Mostafa, T. Seminal clusterin gene expression associated with seminal variables in fertile and infertile men. J. Urol., 2012, 188(4), 1260-1264.
[11]
Wang, Z.; Widgren, E.E.; Richardson, R.T.; O’Rand, M.G. Characterization of an eppin protein complex from human semen and spermatozoa. Biol. Reprod., 2007, 77(3), 476-484.
[12]
Miranda, P.V.; González-Echeverría, F.; Blaquier, J.A.; Mahuran, D.J.; Tezón, J.G. Evidence for the participation of β-hexosaminidase in human sperm-zona pellucida interaction in vitro. Mol. Hum. Reprod., 2000, 6(8), 699-706.
[13]
Martin-DeLeon, P.A. Epididymal SPAM1 and its impact on sperm function. Mol. Cell. Endocrinol., 2006, 250(1-2), 114-121.
[14]
Sullivan, R. Epididymosomes: A heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian J. Androl., 2015, 17(5), 726.
[15]
Polak, B. AUNTER, B. Seminal plasma biochemistry. IV: Enzymes involved in the liquefaction of human seminal plasma. Int. J. Androl., 1989, 12(3), 187-194.
[16]
Özen, H.; Sözen, S. PSA isoforms in prostate cancer detection. Eur. Urol. Suppl., 2006, 5(6), 495-499.
[17]
Fung, K.Y.; Glode, L.M.; Green, S.; Duncan, M.W. A comprehensive characterization of the peptide and protein constituents of human seminal fluid. Prostate, 2004, 61(2), 171-181.
[18]
Piironen, T.; Villoutreix, B.O.; Becker, C.; Lilja, H.; Hollingsworth, K.; Vihinen, M.; Bridon, D.; Qiu, X.; Rapp, J.; Dowell, B. Determination and analysis of antigenic epitopes of Prostate Specific Antigen (PSA) and human glandular kallikrein 2 (hK2) using synthetic peptides and computer modeling. Protein Sci., 1998, 7(2), 259-269.
[19]
Tanaka, M.; Kishi, Y.; Takanezawa, Y.; Kakehi, Y.; Aoki, J.; Arai, H. Prostatic acid phosphatase degrades lysophosphatidic acid in seminal plasma. FEBS Lett., 2004, 571(1-3), 197-204.
[20]
Davis, N.S. Disant’Agnese, P.A.; Ewing, J.F.; Mooney, R.A. The neuroendocrine prostate: Characterization and quantitation of calcitonin in the human gland. J. Urol., 1989, 142(3), 884-888.
[21]
Charlesworth, M.C.; Young, C.Y.; Miller, V.M.; Tindall, D.J. Kininogenase activity of prostate‐derived human glandular kallikrein (hK2) purified from seminal fluid. J. Androl., 1999, 20(2), 220-229.
[22]
Yoshida, K.; Kawano, N.; Yoshiike, M.; Yoshida, M.; Iwamoto, T.; Morisawa, M. Physiological roles of semenogelin I and zinc in sperm motility and semen coagulation on ejaculation in humans. MHR: Basic Sci. Reprod. Med., 2008, 14(3), 151-156.
[23]
Subirán, N.; Agirregoitia, E.; Valdivia, A.; Ochoa, C.; Casis, L.; Irazusta, J. Expression of enkephalin-degrading enzymes in human semen and implications for sperm motility. Fertil. Steril., 2008, 89(5), 1571-1577.
[24]
Skidgel, R.A. Basic carboxypeptidases: Regulators of peptide hormone activity. Trends Pharmacol. Sci., 1988, 9(8), 299-304.
[25]
Vickers, C.; Hales, P.; Kaushik, V.; Dick, L.; Gavin, J.; Tang, J.; Godbout, K.; Parsons, T.; Baronas, E.; Hsieh, F. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase (ACE2). J. Biol. Chem., 2002, 277(17), 14838-14843.
[26]
Kumar, S.; Tomar, A.K.; Singh, S.; Gill, K.; Dey, S.; Singh, S.; Yadav, S. Heparin binding carboxypeptidase E protein exhibits antibacterial activity in human semen. Int. J. Biol. Macromol., 2014, 64, 319-327.
[27]
Marquínez, A.; Andreetta, A.; González, N.; Wolfenstein-Todel, C.; De Cerezo, J.S. Identification of gp17 glycoprotein and characterization of Prostatic Acid Phosphatase (PAP) and Carboxypeptidase E (CPE) fragments in a human seminal plasma fraction interacting with concanavalin A. J. Protein Chem., 2003, 22(5), 423-429.
[28]
Ronquist, G.; Brody, I. The prostasome: Its secretion and function in man. Biochim. Biophys. Acta, 1985, 822(2), 203-218.
[29]
Kelly, R.; Holland, P.; Skibinski, G.; Harrison, C.; McMillan, L.; Hargreave, T.; James, K. Extracellular organelles (prostasomes) are immunosuppressive components of human semen. Clin. Exp. Immunol., 1991, 86(3), 550-556.
[30]
Jarvis, G.A.; Li, J.; Hakulinen, J.; Brady, K.A.; Nordling, S.; Dahiya, R.; Meri, S. Expression and function of the complement membrane attack complex inhibitor protectin (CD59) in human prostate cancer. Int. J. Cancer, 1997, 71(6), 1049-1055.
[31]
Tanase, C.P.; Codrici, E.; Popescu, I.D.; Mihai, S.; Enciu, A.M.; Necula, L.G.; Preda, A.; Ismail, G.; Albulescu, R. Prostate cancer proteomics: Current trends and future perspectives for biomarker discovery. Oncotarget, 2017, 8(11), 18497.
[32]
Aalberts, M.; Stout, T.A.; Stoorvogel, W. Prostasomes: Extracellular vesicles from the prostate. Reproduction, 2014, 147(1), R1-R14.
[33]
Huggins, C.; Scott, W.W.; Heinen, J.H. Chemical composition of human semen and of the secretions of the prostate and seminal vesicles. Am. J. Physiol., 1942, 136(3), 467-473.
[34]
Robert, M.; Gagnon, C. Sperm motility inhibitor from human seminal plasma: Presence of a precursor molecule in seminal vesicle fluid and its molecular processing after ejaculation. Int. J. Androl., 1994, 17(5), 232-240.
[35]
Zhao, H.; Lee, W.H.; Shen, J.H.; Li, H.; Zhang, Y. Identification of novel semenogelin I-derived antimicrobial peptide from liquefied human seminal plasma. Peptides, 2008, 29(4), 505-511.
[36]
Tomar, A.K.; Sooch, B.S.; Raj, I.; Singh, S.; Yadav, S. Interaction analysis identifies semenogelin I fragments as new binding partners of PIP in human seminal plasma. Int. J. Biol. Macromol., 2013, 52, 296-299.
[37]
Lilja, H.; Oldbring, J.; Rannevik, G.; Laurell, C. Seminal vesicle-secreted proteins and their reactions during gelation and liquefaction of human semen. J. Clin. Invest., 1987, 80(2), 281-285.
[38]
Brock, J.H. The physiology of lactoferrin. Biochem. Cell Biol., 2002, 80(1), 1-6.
[39]
Sanocka, D.; Kurpisz, M. Reactive oxygen species and sperm cells. Reprod. Biol. Endocrinol., 2004, 2(1), 12.
[40]
Geva, E.; Lessing, J.B.; Lerner-Geva, L.; Amit, A. Free radicals, antioxidants and human spermatozoa: Clinical implications. Hum. Reprod., 1998, 13(6), 1422-1424.
[41]
Foresta, C.; Manoni, F.; Businaro, V.; Donadel, C.; Indino, M.; Scandellari, C. Possible significance of transferrin levels in seminal plasma of fertile and infertile men. J. Androl., 1986, 7(2), 77-82.
[42]
Kosar, A.; Sarica, K.; Özdiler, E. Effect of varicocelectomy on seminal plasma transferrin values: A comparative clinical trial. Andrologia, 2000, 32(1), 19-22.
[43]
Robert, M.; Gagnon, C.; Semenogelin, I. A coagulum forming, multifunctional seminal vesicle protein. Cell. Mol. Life Sci. CMLS, 1999, 55(6-7), 944-960.
[44]
Erdös, E.; Schulz, W.; Gafford, J.; Defendini, R. Neutral metalloendopeptidase in human male genital tract. Comparison to angiotensin I-converting enzyme. Lab. Invest J. Tech. Method Pathol., 1985, 52(4), 437-447.
[45]
Miller, D.J.; Ax, R.L. Proceeding 12th Tech. Conf. Art. Insem. Reprod, 1988, pp. 97-107.
[46]
Therien, I.; Bleau, G.; Manjunath, P. Phosphatidylcholine-binding proteins of bovine seminal plasma modulate capacitation of spermatozoa by heparin. Biol. Reprod., 1995, 52(6), 1372-1379.
[47]
Moreau, R.; Frank, P.G.; Perreault, C.; Marcel, Y.L.; Manjunath, P. Seminal plasma choline phospholipid-binding proteins stimulate cellular cholesterol and phospholipid efflux. Biochim. Biophys. Acta (BBA)-. Mol. Cell Biol. Lipid, 1999, 1438(1), 38-46.
[48]
Davis, B.; Niwa, K. Inhibition of mammalian fertilization in vitro by membrane vesicles from seminal plasma. Proc. Soc. Exp. Biol. Med., 1974, 146(1), 11-16.
[49]
Austin, C. Observations on the penetration of the sperm into the mammalian egg. Aust. J. Biol. Sci., 1951, 4(4), 581-596.
[50]
Manjunath, P.; Thérien, I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J. Reprod. Immunol., 2002, 53(1-2), 109-119.
[51]
Chiu, W.; Chamley, L. Human seminal plasma antibody‐binding proteins. Am. J. Reprod. Immunol., 2003, 50(3), 196-201.
[52]
Gaubin, M.; Autiero, M.; Basmaciogullari, S.; Métivier, D.; Misëhal, Z.; Culerrier, R.; Oudin, A.; Guardiola, J.; Piatier-Tonneau, D. Potent inhibition of CD4/TCR-mediated T cell apoptosis by a CD4-binding glycoprotein secreted from breast tumor and seminal vesicle cells. J. Immunol., 1999, 162(5), 2631-2638.
[53]
Bergamo, P.; Balestrieri, M.; Cammarota, G.; Guardiola, J.; Abrescia, P. CD4-mediated anchoring of the seminal antigen gp17 onto the spermatozoon surface. Hum. Immunol., 1997, 58(1), 30-41.
[54]
Meuleman, T.; Snaterse, G.; van Beelen, E.; Anholts, J.D.; Pilgram, G.S.; van der Westerlaken, L.A.; Eikmans, M.; Claas, F.H. The immunomodulating effect of seminal plasma on T cells. J. Reprod. Immunol., 2015, 110, 109-116.
[55]
Lu, N.Q.; Zha, S.W. Inhibitory effects of human seminal plasma on an ELISA used to detect anti-sperm antibodies: Implications for the determination of sperm quality. J. Reprod. Immunol., 2000, 47(1), 33-40.
[56]
Robertson, S.A.; Guerin, L.R.; Moldenhauer, L.M.; Hayball, J.D. Activating T regulatory cells for tolerance in early pregnancy the contribution of seminal fluid. J. Reprod. Immunol., 2009, 83(1-2), 109-116.
[57]
Robertson, S.A.; Ingman, W.V.; O’Leary, S.; Sharkey, D.J.; Tremellen, K.P. Transforming growth factor β a mediator of immune deviation in seminal plasma. J. Reprod. Immunol., 2002, 57(1-2), 109-128.
[58]
Sharkey, D.J.; Macpherson, A.M.; Tremellen, K.P.; Robertson, S.A. Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol. Hum. Reprod., 2007, 13(7), 491-501.
[59]
Prakash, C. Etiology of immune infertility. Prog. Clin. Biol. Res., 1981, 70, 403-412.
[60]
Thaler, C.J. Immunological role for seminal plasma in insemination and pregnancy. Am. J. Reprod. Immunol., 1989, 21(3‐4), 147-150.
[61]
Coulam, C.; Stern, J. Effect of seminal plasma on implantation rates. Early Pregnancy: Biol. Med. Official J. Soc. Invest. Early Pregnancy, 1995, 1(1), 33-36.
[62]
Need, J.A.; Bell, B.; Meffin, E.; Jones, W. Pre-eclampsia in pregnancies from donor inseminations. J. Reprod. Immunol., 1983, 5(6), 329-338.
[63]
Serhal, P.; Craft, I. Oocyte donation in 61 patients. The Lancet, 1989, 333(8648), 1185-1187.
[64]
Sharkey, D.J.; Tremellen, K.P.; Jasper, M.J.; Gemzell-Danielsson, K.; Robertson, S.A. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J. Immunol., 2012, 188(5), 2445-2454.
[65]
Pandya, I.J.; Cohen, J. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil. Steril., 1985, 43(3), 417-421.
[66]
Sharkey, D.J.; Schjenken, J.E.; Mottershead, D.G.; Robertson, S.A. Seminal fluid factors regulate activin A and follistatin synthesis in female cervical epithelial cells. Mol. Cell. Endocrinol., 2015, 417, 178-190.
[67]
Bellinge, B.S.; Copeland, C.M.; Thomas, T.D.; Mazzucchelli, R.E.; O’Neil, G.; Cohen, M.J. The influence of patient insemination on the implantation rate in an in vitro fertilization and embryo transfer program. Fertil. Steril., 1986, 46(2), 252-256.
[68]
James, K.; Hargreave, T.B. Immunosuppression by seminal plasma and its possible clinical significance. Immunol. Today, 1984, 5(12), 357-363.
[69]
Légaré, C.; Cloutier, F.; Makosso-Kallyth, S.; Laflamme, N.; Jarvi, K.; Tremblay, R.R.; Sullivan, R. Cysteine-rich secretory protein 1 in seminal plasma: Potential biomarker for the distinction between obstructive and nonobstructive azoospermia. Fertil. Steril., 2013, 100(5), 1253-1260.
[70]
Davalieva, K.; Kiprijanovska, S.; Noveski, P.; Plaseski, T.; Kocevska, B.; Broussard, C.; Plaseska‐Karanfilska, D. Proteomic analysis of seminal plasma in men with different spermatogenic impairment. Andrologia, 2012, 44(4), 256-264.
[71]
Crabbe, M. The development of a qualitative assay for male infertility from a study of enzymes in human semen. J. Reprod. Fertil., 1977, 51(1), 73-76.
[72]
Aafjes, J.; Cohen, J.; Vreeburg, J.; Oort, H.W.V. Fumarase activity in human ejaculate relationship to sperm-motility or-penetration of zona‐free hamster eggs. Andrologia, 1981, 13(6), 578-582.
[73]
Sharma, R.; Agarwal, A.; Mohanty, G.; Jesudasan, R.; Gopalan, B.; Willard, B.; Yadav, S.P.; Sabanegh, E. Functional proteomic analysis of seminal plasma proteins in men with various semen parameters. Reprod. Biol. Endocrinol., 2013, 11(1), 38.
[74]
Michaelis, M.; Gralla, O.; Behrends, T.; Scharpf, M.; Endermann, T.; Rijntjes, E.; Pietschmann, N.; Hollenbach, B.; Schomburg, L. Selenoprotein P in seminal fluid is a novel biomarker of sperm quality. Biochem. Biophys. Res. Commun., 2014, 443(3), 905-910.
[75]
Giacomini, E.; Ura, B.; Giolo, E.; Luppi, S.; Martinelli, M.; Garcia, R.C.; Ricci, G. Comparative analysis of the seminal plasma proteomes of oligoasthenozoospermic and normozoospermic men. Reprod. Biomed. Online, 2015, 30(5), 522-531.
[76]
Du, J.W.; Xu, K.Y.; Fang, L.Y.; Qi, X.L. Detection and analysis of MMP-2 and MMP-9 in seminal plasma. J. Men’s Health, 2012, 9(4), 216-219.
[77]
Baka, S.; Zourla, K.; Kouskouni, E.; Makrakis, E.; Demeridou, S.; Tzanakaki, D.; Hassiakos, D.; Creatsas, G. Matrix metalloproteinases 2 and 9 and their tissue inhibitors in the follicular fluid of patients with polycystic ovaries undergoing in vitro fertilisation. In Vivo, 2010, 24(3), 293-296.
[78]
Fernandez-Encinas, A.; García-Peiró, A.; Ribas-Maynou, J.; Abad, C.; Amengual, M.J.; Navarro, J.; Benet, J. Characterization of nuclease activity in human seminal plasma and its relationship to semen parameters, sperm DNA fragmentation and male infertility. J. Urol., 2016, 195(1), 213-219.
[79]
Milardi, D.; Grande, G.; Vincenzoni, F.; Messana, I.; Pontecorvi, A.; De Marinis, L.; Castagnola, M.; Marana, R. Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil. Steril., 2012, 97(1), 67-73.
[80]
Maxwell, W.; Johnson, L. Physiology of spermatozoa at high dilution rates: The influence of seminal plasma. Theriogenology, 1999, 52(8), 1353-1362.
[81]
Nelson, W.O. In: Some factors involved in the control of the gametogenic and endocrine functions of the testis,, Cold Spring Harbor Symposia on Quantitative Biology, Cold Spring Harbor Laboratory Press: New York, USA. 1937, pp 123-135.
[82]
McCullagh, R.D.; Walsh, E.L. Experimental hypertrophy and atrophy of the prostate gland. Endocrinology, 1935, 19(4), 466-470.
[83]
McCullagh, E.P.; Schneider, R.W.; Bowman, W.; Smith, M. Adrenal and testicular deficiency: A comparison based on similarities in androgen deficiency, androgen and 17-ketosteroid excretion, and on differences in their effects upon pituitary activity. J. Clin. Endocrinol., 1948, 8(4), 275-294.
[84]
Howard, R.P.; Sniffen, R.C.; Simmons, F.A.; Albright, F. Testicular deficiency: A clinical and pathologic study. J. Clin. Endocrinol., 1950, 10(2), 121-186.
[85]
McCullagh, E.P.; Schaffenburg, C. The role of the seminiferous tubules in the production of hormones. Ann. N. Y. Acad. Sci., 1952, 55(4), 674-684.
[86]
Howard, R.P.; Simmons, F.A.; Sniffen, R.C. Differential diagnosis in male sterility: With consideration of the role of endocrine therapy. Fertil. Steril., 1951, 2(2), 95-114.
[87]
Taira, A.; Tarkhan, A. The role of the testis in the release of gonadotrophins from the hypophysis. Acta Endocrinol., 1962, 40(2), 175-187.
[88]
Sheth, A.R.; Arabatti, N.; Carlquist, M.; Jörnvall, H. Characterization of a polypeptide from human seminal plasma with inhibin (inhibition of FSH secretion) like activity. FEBS Lett., 1984, 165(1), 11-15.
[89]
Dubé, J.Y.; Frenette, G.; Paquin, R.; Chapdelaine, P.; Tremblay, J.; Tremblay, R.R.; Lazure, C.; Seidah, N.; Chrétien, M. Isolation from human seminal plasma of an abundant 16 kDa protein originating from the prostate, its identification with a 94-residue peptide originally described as β‐inhibin. J. Androl., 1987, 8(3), 182-189.
[90]
Iwamoto, T.; Gagnon, C. A human seminal plasma protein blocks the motility of human spermatozoa. J. Urol., 1988, 140(5), 1045-1048.
[91]
Orlando, C.; Caldini, A.L.; Barni, T.; Wood, W.G.; Strasburger, C.J.; Natali, A.; Maver, A.; Forti, G.; Serio, M. Ceruloplasmin and transferrin in human seminal plasma: Are they an index of seminiferous tubular function? Fertil. Steril., 1985, 43(2), 290-294.
[92]
Forrester, I.T.; Bradley, M.P. Identification of calmodulin-like activity in human seminal plasma. Biochem. Biophys. Res. Commun., 1980, 92(3), 994-1001.
[93]
Krassnigg, F.; Niederhauser, H.; Fink, E.; Frick, J.; Schill, W.B. Angiotensin converting enzyme in human seminal plasma is synthesized by the testis, epididymis and prostate. Int. J. Androl., 1989, 12(1), 22-28.
[94]
O’Bryan, M.; Baker, H.; Saunders, J.; Kirszbaum, L.; Walker, I.; Hudson, P.; Liu, D.; Glew, M.; d’Apice, A.; Murphy, B. Human seminal clusterin (SP-40, 40). Isolation and characterization. J. Clin. Invest., 1990, 85(5), 1477-1486.
[95]
Ding, Z.; Qu, F.; Guo, W.; Ying, X.; Wu, M.; Zhang, Y. Identification of sperm forward motility-related proteins in human seminal plasma. Mol. Reprod. Dev., 2007, 74(9), 1124-1131.
[96]
Glander, H.J.; Kratzsch, J.; Weisbrich, C.; Birkenmeier, G. Andrology: Insulin-like growth factor-I and α2-macroglobulin in seminal plasma correlate with semen quality. Hum. Reprod., 1996, 11(11), 2454-2460.
[97]
Euler, U.V. To the knowledge of the pharmacological effects of native secretions and extracts of male accessory glands. Naunyn Schmiedebergs Arch. Exp. Pathol. Pharmakol., 1934, 175(1), 78-84.
[98]
Goldblatt, M. Properties of human seminal plasma. J. Physiol., 1935, 84(2), 208-218.
[99]
Ganguli, N.C. Seemingly silent seminal plasma. Indian Dairym., 1979, 31, 879-882.
[100]
Jeulin, C.; Soufir, J.; Weber, P.; Laval-Martin, D.; Calvayrac, R. Catalase activity in human spermatozoa and seminal plasma. Gamete Res., 1989, 24(2), 185-196.
[101]
Kunze, H.; Nahas, N.; Wurl, M. Phospholipases in human seminal plasma. Biochim. Biophys. Acta, 1974, 348(1), 35-44.
[102]
Hölttä, E.; Pulkkinen, P.; Elfving, K.; Jänne, J. Oxidation of polymines by diamine oxidase from human seminal plasma. Biochem. J., 1975, 145(2), 373-378.
[103]
CasslEn. B.; Åstedt, B. Occurrence of both urokinase and tissue plasminogen activator in the human endometrium. Contraception, 1983, 28(6), 553-564.
[104]
Depierre, D.; Bargetzi, J.P.; Roth, M. Dipeptidyl carboxypeptidase from human seminal plasma. Biochim. Biophys. Acta (BBA)-. Enzymol., 1978, 523(2), 469-476.
[105]
Nissen, H.; Kreysel, H. Superoxide dismutase in human semen. Klin. Wochenschr., 1983, 61(1), 63-65.
[106]
Skidgel, R.A.; Deddish, P.A.; Davis, R.M. Isolation and characterization of a basic carboxypeptidase from human seminal plasma. Arch. Biochem. Biophys., 1988, 267(2), 660-667.
[107]
Zini, A.; O’Bryan, M.K.; Schlegel, P.N. Nitric oxide synthase activity in human seminal plasma. Urology, 2001, 58(1), 85-89.
[108]
Pullar, J.; Carr, A.; Bozonet, S.; Rosengrave, P.; Kettle, A.; Vissers, M. Elevated seminal plasma myeloperoxidase is associated with a decreased sperm concentration in young men. Andrology, 2017, 5(3), 431-438.
[109]
Lilja, H.; Weiber, H. γ-Glutamyltransferase bound to prostatic subcellular organelles and in free form in human seminal plasma. Scand. J. Clin. Lab. Invest., 1983, 43(4), 307-312.
[110]
Cooper, T.; Yeung, C.; Nashan, D.; Jockenhövel, F.; Nieschlag, E. Improvement in the assessment of human epididymal function by the use of inhibitors in the assay of α-glucosidase in seminal plasma. Int. J. Androl., 1990, 13(4), 297-305.
[111]
Tokugawa, Y.; Kunishige, I.; Kubota, Y.; Shimoya, K.; Nobunaga, T.; Kimura, T.; Saji, F.; Murata, Y.; Eguchi, N.; Oda, H. Lipocalin-type prostaglandin D synthase in human male reproductive organs and seminal plasma. Biol. Reprod., 1998, 58(2), 600-607.
[112]
Polak, B.; Aunter, B. Seminal plasma biochemistry. IV: Enzymes involved in the liquefaction of human seminal plasma. Int. J. Androl., 1989, 12(3), 187-194.
[113]
Lord, E.M.; Sensabaugh, G.F.; Stites, D.P. Immunosuppressive activity of human seminal plasma: I. Inhibition of in vitro lymphocyte activation. J. Immunol., 1977, 118(5), 1704-1711.
[114]
James, K.; Hargreave, T.B. Immunosuppression by seminal plasma and its possible clinical significance. Immunol. Today, 1984, 5(12), 357-363.
[115]
Li, T.S.; Behrman, S. The sperm-and seminal plasma-specific antigens of human semen. Fertil. Steril., 1970, 21(7), 565-573.
[116]
Loumaye, E.; de Cooman, S.; Thomas, K. Immunoreactive relaxin-like substance in human seminal plasma. J. Clin. Endocrinol. Metab., 1980, 50(6), 1142-1143.
[117]
Nocera, M.; Chu, T.M. Transforming growth factor β as an immunosuppressive protein in human seminal plasma. Am. J. Reprod. Immunol., 1993, 30(1), 1-8.
[118]
Malm, J.; Sørensen, O.; Persson, T.; Frohm-Nilsson, M.; Johansson, B.; Bjartell, A.; Lilja, H.; Ståhle-Bäckdahl, M.; Borregaard, N.; Egesten, A. The human cationic antimicrobial protein (hCAP-18) is expressed in the epithelium of human epididymis, is present in seminal plasma at high concentrations, and is attached to spermatozoa. Infect. Immun., 2000, 68(7), 4297-4302.
[119]
Maegawa, M.; Kamada, M.; Irahara, M.; Yamamoto, S.; Yoshikawa, S.; Kasai, Y.; Ohmoto, Y.; Gima, H.; Thaler, C.J.; Aono, T. A repertoire of cytokines in human seminal plasma. J. Reprod. Immunol., 2002, 54(1-2), 33-42.
[120]
Julkunen, M.; Wahlström, T.; Seppälä, M.; Koistinen, R.; Koskimies, A.; Stenman, U.; Bohn, H. Detection and localization of placental protein 14-like protein in human seminal plasma and in the male genital tract. Arch. Androl., 1984, 12, 59-67.
[121]
Bischof, P.; Martin-Du-Pan, R.; Lauber, K.; Girard, J.; Herrmann, W.; Sizonenko, P. Human seminal plasma contains a protein that shares physicochemical, immunochemical, and immunosuppressive properties with pregnancy-associated plasma protein-A. J. Clin. Endocrinol. Metab., 1983, 56(2), 359-362.
[122]
Khunsook, S.; Alhadeff, J.A.; Bean, B.S. Purification and characterization of human seminal plasma α-L-fucosidase. MHR: Basic Sci. Reprod. Med., 2002, 8(3), 221-227.
[123]
Ronquist, G.; Brody, I.; Gottfries, A.; Stegmayr, B. An Mg2+ and Ca2+‐stimulated adenosine triphosphatase in human prostatic fluid: Part I. Andrologia, 1978, 10(4), 261-272.
[124]
Stegmayr, B.; Brody, I.; Ronquist, G. A biochemical and ultrastructural study on the endogenous protein kinase activity of secretory granule membranes of prostatic origin in human seminal plasma. J. Ultrastruct. Res., 1982, 78(2), 206-214.
[125]
Van der Ven, H.; Bhattacharyya, A.K.; Binor, Z.; Leto, S.; Zaneveld, L.J. Inhibition of human sperm capacitation by a high-molecular-weight factor from human seminal plasma. Fertil. Steril., 1982, 38(6), 753-755.
[126]
Foresta, C.; Caretto, A.; Indino, M.; Betterle, C.; Scandellari, C. Calcitonin in human seminal plasma and its localization on human spermatozoa. Andrologia, 1986, 18(5), 470-473.
[127]
Chiu, W.; Chamley, L. Human seminal plasma antibody‐binding proteins. Am. J. Reprod. Immunol., 2003, 50(3), 196-201.
[128]
Zaneveld, L.; Schumacher, G.; Fritz, H.; Fink, E.; Jaumann, E. Interaction of human sperm acrosomal proteinase with human seminal plasma proteinase inhibitors. J. Reprod. Fertil., 1973, 32(3), 525-529.
[129]
Han, H.L.; Mack, S.R.; De, C.J.; Zaneveld, L. Inhibition of the human sperm acrosome reaction by a high molecular weight factor from human seminal plasma. Fertil. Steril., 1990, 54(6), 1177-1179.
[130]
Ross, V.; Moore, D.H.; Miller, E.G. Proteins of human seminal plasma. J. Biol. Chem., 1942, 144(3), 667-677.
[131]
Sensabaugh, G. Isolation and characterization of a semen-specific protein from human seminal plasma: A potential new marker for semen identification. J. Forensic Sci., 1978, 23(1), 106-115.
[132]
Edwards, J.J.; Tollaksen, S.L.; Anderson, N.G. Proteins of human semen. I. Two-dimensional mapping of human seminal fluid. Clin. Chem., 1981, 27(8), 1335-1340.
[133]
Rui, H.; Mevåg, B.; Purvis, K. Two‐dimensional electrophoresis of proteins in various fractions of the human split ejaculate. Int. J. Androl., 1984, 7(6), 509-520.
[134]
Starita‐Geribaldi, M.; Roux, F.; Garin, J.; Chevallier, D.; Fénichel, P.; Pointis, G. Development of narrow immobilized pH gradients covering one pH unit for human seminal plasma proteomic analysis. Proteomics: Int. Ed., 2003, 3(8), 1611-1619.
[135]
Pilch, B.; Mann, M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol., 2006, 7(5), R40.
[136]
Batruch, I.; Lecker, I.; Kagedan, D.; Smith, C.R.; Mullen, B.J.; Grober, E.; Lo, K.C.; Diamandis, E.P.; Jarvi, K.A. 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(3), 941-953.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy