The Expression of Free Oligosaccharides in Human Seminal Plasma

Abstract

Human seminal plasma is a complex mixture of proteins, glycoproteins, peptides, glycopeptides, and prostaglandins secreted by organs of the male reproductive tract. The components of this fluid have been implicated in the suppression of immune response, agonistic effects on sperm-egg binding, and promotion of successful implantation of the human embryo. Fractionation followed by biophysical analyses revealed that free oligosaccharides constitute a major component of the total glycoconjugates within seminal plasma. Significant findings of our analyses include the following: (i) the concentration of free oligosaccharides is 0.3–0.4 mg/ml; (ii) mono- and difucosylated forms of the disaccharide lactose are major components; (iii) many of the remaining oligosaccharides are also rich in fucose and carry Lewisx and/or Lewisyepitopes; (iv) a subset of the oligosaccharides express the reducing end sequence (GlcNAcβ1–3/4Glc) not reported in human milk oligosaccharides; (v) oligosaccharides in seminal plasma exclusively express type 2 (Galβ1–4GlcNAc) but not the type 1 sequences (Galβ1–3GlcNAc) that predominate in human milk glycans; and (vi) the structural diversity of seminal plasma oligosaccharides is far less than human milk oligosaccharides. The agonistic effect of both fucose and fucosylated glycoconjugates on human sperm-egg binding in vitro suggests that fucosylated oligosaccharides may also promote fertilization in the female reproductive tract. Human seminal plasma is a complex mixture of proteins, glycoproteins, peptides, glycopeptides, and prostaglandins secreted by organs of the male reproductive tract. The components of this fluid have been implicated in the suppression of immune response, agonistic effects on sperm-egg binding, and promotion of successful implantation of the human embryo. Fractionation followed by biophysical analyses revealed that free oligosaccharides constitute a major component of the total glycoconjugates within seminal plasma. Significant findings of our analyses include the following: (i) the concentration of free oligosaccharides is 0.3–0.4 mg/ml; (ii) mono- and difucosylated forms of the disaccharide lactose are major components; (iii) many of the remaining oligosaccharides are also rich in fucose and carry Lewisx and/or Lewisyepitopes; (iv) a subset of the oligosaccharides express the reducing end sequence (GlcNAcβ1–3/4Glc) not reported in human milk oligosaccharides; (v) oligosaccharides in seminal plasma exclusively express type 2 (Galβ1–4GlcNAc) but not the type 1 sequences (Galβ1–3GlcNAc) that predominate in human milk glycans; and (vi) the structural diversity of seminal plasma oligosaccharides is far less than human milk oligosaccharides. The agonistic effect of both fucose and fucosylated glycoconjugates on human sperm-egg binding in vitro suggests that fucosylated oligosaccharides may also promote fertilization in the female reproductive tract. human seminal plasma fast atom bombardment mass spectrometry electrospray gas chromatography mass spectrometry quadrupole orthogonal acceleration time of flight mass spectrometer collisionally activated decomposition prostaglandin Human semen contains a variety of different cell types including sperm, neutrophils, monocytes, and lymphocytes (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). If incubated for a brief period of time, semen undergoes a process known as liquefaction that leads to clearing of this fluid and a partial loss of its viscosity (2Sobrero A.J. MacLeod J.K. Fertil. Steril. 1962; 13: 184-189Abstract Full Text PDF PubMed Google Scholar). Centrifugation of partially liquefied semen leads to the separation of the cellular components from the viscous acellular fluid known as human seminal plasma (HSP).1HSP is more than simply a liquid medium for transporting sperm into the vagina. It is an extremely complex mixture of proteins, glycoproteins, peptides, glycopeptides, and prostaglandins secreted by the organs of the male reproductive tract (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). A plethora of different studies indicate that HSP supports sperm function, modulates maternal immune responses directed against sperm, and promotes successful implantation of the human embryo (reviewed in Refs. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar, 3Kelly R.W. Critchley H.O. Hum. Reprod. 1997; 12: 2200-2207Crossref PubMed Scopus (81) Google Scholar, and 4Robertson S.A. Sharkey D.J. Semin. Immunol. 2001; 13: 243-254Crossref PubMed Scopus (140) Google Scholar). The components of HSP may therefore profoundly impact male fertility in the female reproductive tract.Previous studies confirm that HSP contains a specific glycoprotein with immunomodulatory activities (5Bolton A.E. Pockley A.G. Clough K.J. Mowles E.A. Stoker R.J. Westwood O.M. Chapman M.G. Lancet. 1987; 1: 593-595Abstract PubMed Scopus (204) Google Scholar) now known as glycodelin-S (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). Glycodelin-S also promotes human sperm binding to homologous zona pellucida in the hemizona assay system (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). This intriguing combination of biological activities led us to investigate further the glycosylation of other components associated with HSP. By using fast atom bombardment (FAB) and electrospray (ES) mass spectrometry to screen HSP for novel glycoconjugates (7Dell A. Khoo K.-H. Panico M. McDowell R.A. Etienne A.T. Reason A.J. Morris H.R. Fukuda M. Kobata A. Glycobiology: A Practical Approach. Oxford University Press, Oxford1993: 187-222Google Scholar), we have made the surprising discovery that this fluid is also rich in free oligosaccharides. The only other human secretion known to contain a significant amount of free oligosaccharides is human milk (reviewed in Refs. 8Newburg D.S. Neubauer S.H. Jenson R.G. Handbook of Milk Composition. Academic Press, San Diego1995: 273-349Google Scholar and 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar). than human milk oligosaccharides have been structural is from and D.S. Neubauer S.H. Jenson R.G. Handbook of Milk Composition. Academic Press, San Diego1995: 273-349Google Scholar, 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google significant biological activities have been to human milk oligosaccharides. many and sequences associated with (reviewed in Ref. D.S. Chem. Google Scholar). human milk oligosaccharides may in by with and binding for and A more suggests that human milk oligosaccharides the binding of activated with to in vitro C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar) and may in this we the structural of of free oligosaccharides in HSP and that of the structural of human milk as as a of The are fucosylated and contain structural also in the of the oligosaccharides of The impact of free oligosaccharides on male reproductive is our this is the the of free oligosaccharides in HSP. both human milk and HSP are that contain free oligosaccharides. are significant milk and HSP oligosaccharides revealed by the structural (i) the concentration of free oligosaccharides is in human milk than HSP 0.3–0.4 C. Rudloff S. Baier W. Klein S. PubMed Scopus Google (ii) oligosaccharides are components in HSP not but of the total human milk PubMed Scopus Google (iii) the of complex HSP oligosaccharides are (iv) a subset of HSP oligosaccharides express the reducing end sequence (GlcNAcβ1–3/4Glc) not reported in human milk oligosaccharides; (v) HSP oligosaccharides exclusively express type 2 (Galβ1–4GlcNAc) but not the type 1 sequences (Galβ1–3GlcNAc) that predominate in human milk oligosaccharides C. Rudloff S. Baier W. Klein S. PubMed Scopus Google and (vi) the structural diversity of human milk oligosaccharides that of HSP oligosaccharides S. J. M. M. PubMed Scopus Google for the of HSP and human milk oligosaccharides may and activities associated with free are in human milk J. Full Text PDF PubMed Scopus Google Scholar, Kobata A. J. PubMed Scopus Google Scholar). activities are also in HSP PubMed Scopus Google Scholar, S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar). The of the include the following: (i) to S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar), a in milk J. Biol. Chem. Full Text PDF PubMed Google Scholar) that the of milk from to R.L. S. A. PubMed Scopus Google (ii) in the and PubMed Scopus Google Scholar, S. M. J. Reprod. Fertil. PubMed Scopus Google and (iii) S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar). A is the that human sperm is with this C. PubMed Scopus Google is that the of the in vitro 1987; PubMed Scopus Google Scholar). This is with the of fucosylated oligosaccharides in HSP. This in the and is also 12: PubMed Scopus Google is that other express free oligosaccharides in seminal plasma. are the of and associated in seminal plasma. a and an are in seminal plasma Biol. Reprod. PubMed Scopus Google Scholar). seminal plasma also contains of J. Reprod. Fertil. Scholar). are to in the of J. Reprod. Fertil. Scholar), but on the in free of HSP oligosaccharides in the male and/or the female reproductive is not semen into the sperm and other seminal plasma components the to this (reviewed in Ref. 2001; PubMed Google Scholar). It may for components free oligosaccharides to this to within the and the of sperm in the and the sperm in human a in the of the fertilization (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). a is fertilization in the of of sperm with for successful in vitro fertilization sperm binding The is that male and female within the and this effects of free oligosaccharides on sperm include the following: (i) sperm by (ii) sperm that and (iii) sperm binding to sperm and to human vitro E. Fertil. Steril. Full Text Full Text PDF PubMed Scopus Google Scholar). The major associated with human are with Lewisx and sequences J. Biol. Chem. Full Text PDF PubMed Google Scholar), as are HSP oligosaccharides. Human sperm binding to the zona pellucida is by in the hemizona assay in the of fucose but not other S. A. Fertil. Steril. Full Text PDF PubMed Google Scholar). a HSP glycoprotein also with Lewisx and sperm binding in the hemizona assay by (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). The of fucosylated sequences on free and may promote sperm-egg binding in the human oligosaccharides associated with HSP also a in cell in the male and female reproductive for sperm, are the cell type in HSP from are neutrophils, with of and (reviewed in Ref. H. Fertil. Steril. Full Text PDF PubMed Google Scholar). is a by of in semen (reviewed in Ref. R.J. Hum. Reprod. PubMed Scopus Google Scholar). in a is associated with male H. Fertil. Steril. Full Text PDF PubMed Google Scholar). is also a of into the and an to as the A.E. J. Reprod. Immunol. PubMed Scopus Google Scholar). The of the are neutrophils, with of and A.E. J. Reprod. Immunol. PubMed Scopus Google Scholar). Human sperm express sequences that are by M.S. Oehninger S. Dell A. Morris H. Seppala M. Clark G.F. Hum. Reprod. 1997; PubMed Scopus Google Scholar), are from this type of the sperm from other immune and cell types in semen and the are not is that in HSP by and C. Hum. Reprod. PubMed Scopus Google Scholar). may sperm from the of that prostaglandins and in HSP a in the suppression of R.W. Critchley H.O. Hum. Reprod. 1997; 12: 2200-2207Crossref PubMed Scopus (81) Google Scholar). of the cell with a seminal plasma in and effect on the of the the concentration of the seminal plasma R.W. Hum. Reprod. PubMed Scopus Google Scholar). By of with HSP to the from R.W. Hum. Reprod. PubMed Scopus Google Scholar). This that other components within HSP are for the major effect of this implicated in this is a glycoprotein that Lewisx and sequences with the HSP oligosaccharides (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google milk oligosaccharides the binding of many to in vitro (reviewed in Refs. 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar and D.S. Chem. Google Scholar). of are by fucosylated oligosaccharides in this HSP oligosaccharides also with for tract have been implicated in with human type and human 1997; PubMed Scopus Google Scholar, H. S. E. PubMed Scopus Google Scholar). to HSP oligosaccharides effect against in the male and/or female reproductive free oligosaccharides of sequence are in the HSP of The of a of the complex suggests to in the human to the of free oligosaccharides in human Human semen contains a variety of different cell types including sperm, neutrophils, monocytes, and lymphocytes (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). If incubated for a brief period of time, semen undergoes a process known as liquefaction that leads to clearing of this fluid and a partial loss of its viscosity (2Sobrero A.J. MacLeod J.K. Fertil. Steril. 1962; 13: 184-189Abstract Full Text PDF PubMed Google Scholar). Centrifugation of partially liquefied semen leads to the separation of the cellular components from the viscous acellular fluid known as human seminal plasma HSP is more than simply a liquid medium for transporting sperm into the vagina. It is an extremely complex mixture of proteins, glycoproteins, peptides, glycopeptides, and prostaglandins secreted by the organs of the male reproductive tract (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). A plethora of different studies indicate that HSP supports sperm function, modulates maternal immune responses directed against sperm, and promotes successful implantation of the human embryo (reviewed in Refs. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar, 3Kelly R.W. Critchley H.O. Hum. Reprod. 1997; 12: 2200-2207Crossref PubMed Scopus (81) Google Scholar, and 4Robertson S.A. Sharkey D.J. Semin. Immunol. 2001; 13: 243-254Crossref PubMed Scopus (140) Google Scholar). The components of HSP may therefore profoundly impact male fertility in the female reproductive tract. studies confirm that HSP contains a specific glycoprotein with immunomodulatory activities (5Bolton A.E. Pockley A.G. Clough K.J. Mowles E.A. Stoker R.J. Westwood O.M. Chapman M.G. Lancet. 1987; 1: 593-595Abstract PubMed Scopus (204) Google Scholar) now known as glycodelin-S (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). Glycodelin-S also promotes human sperm binding to homologous zona pellucida in the hemizona assay system (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). This intriguing combination of biological activities led us to investigate further the glycosylation of other components associated with HSP. By using fast atom bombardment (FAB) and electrospray (ES) mass spectrometry to screen HSP for novel glycoconjugates (7Dell A. Khoo K.-H. Panico M. McDowell R.A. Etienne A.T. Reason A.J. Morris H.R. Fukuda M. Kobata A. Glycobiology: A Practical Approach. Oxford University Press, Oxford1993: 187-222Google Scholar), we have made the surprising discovery that this fluid is also rich in free oligosaccharides. The only other human secretion known to contain a significant amount of free oligosaccharides is human milk (reviewed in Refs. 8Newburg D.S. Neubauer S.H. Jenson R.G. Handbook of Milk Composition. Academic Press, San Diego1995: 273-349Google Scholar and 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar). than human milk oligosaccharides have been structural is from and D.S. Neubauer S.H. Jenson R.G. Handbook of Milk Composition. Academic Press, San Diego1995: 273-349Google Scholar, 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar). significant biological activities have been to human milk oligosaccharides. many and sequences associated with (reviewed in Ref. D.S. Chem. Google Scholar). human milk oligosaccharides may in by with and binding for and A more suggests that human milk oligosaccharides the binding of activated with to in vitro C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar) and may in this we the structural of of free oligosaccharides in HSP and that of the structural of human milk as as a of The are fucosylated and contain structural also in the of the oligosaccharides of The impact of free oligosaccharides on male reproductive is our this is the the of free oligosaccharides in HSP. both human milk and HSP are that contain free oligosaccharides. are significant milk and HSP oligosaccharides revealed by the structural (i) the concentration of free oligosaccharides is in human milk than HSP 0.3–0.4 C. Rudloff S. Baier W. Klein S. PubMed Scopus Google (ii) oligosaccharides are components in HSP not but of the total human milk PubMed Scopus Google (iii) the of complex HSP oligosaccharides are (iv) a subset of HSP oligosaccharides express the reducing end sequence (GlcNAcβ1–3/4Glc) not reported in human milk oligosaccharides; (v) HSP oligosaccharides exclusively express type 2 (Galβ1–4GlcNAc) but not the type 1 sequences (Galβ1–3GlcNAc) that predominate in human milk oligosaccharides C. Rudloff S. Baier W. Klein S. PubMed Scopus Google and (vi) the structural diversity of human milk oligosaccharides that of HSP oligosaccharides S. J. M. M. PubMed Scopus Google for the of HSP and human milk oligosaccharides may and activities associated with free are in human milk J. Full Text PDF PubMed Scopus Google Scholar, Kobata A. J. PubMed Scopus Google Scholar). activities are also in HSP PubMed Scopus Google Scholar, S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar). The of the include the following: (i) to S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar), a in milk J. Biol. Chem. Full Text PDF PubMed Google Scholar) that the of milk from to R.L. S. A. PubMed Scopus Google (ii) in the and PubMed Scopus Google Scholar, S. M. J. Reprod. Fertil. PubMed Scopus Google and (iii) S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar). A is the that human sperm is with this C. PubMed Scopus Google is that the of the in vitro 1987; PubMed Scopus Google Scholar). This is with the of fucosylated oligosaccharides in HSP. This in the and is also 12: PubMed Scopus Google is that other express free oligosaccharides in seminal plasma. are the of and associated in seminal plasma. a and an are in seminal plasma Biol. Reprod. PubMed Scopus Google Scholar). seminal plasma also contains of J. Reprod. Fertil. Scholar). are to in the of J. Reprod. Fertil. Scholar), but on the in free of HSP oligosaccharides in the male and/or the female reproductive is not semen into the sperm and other seminal plasma components the to this (reviewed in Ref. 2001; PubMed Google Scholar). It may for components free oligosaccharides to this to within the and the of sperm in the and the sperm in human a in the of the fertilization (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). a is fertilization in the of of sperm with for successful in vitro fertilization sperm binding The is that male and female within the and this effects of free oligosaccharides on sperm include the following: (i) sperm by (ii) sperm that and (iii) sperm binding to sperm and to human vitro E. Fertil. Steril. Full Text Full Text PDF PubMed Scopus Google Scholar). The major associated with human are with Lewisx and sequences J. Biol. Chem. Full Text PDF PubMed Google Scholar), as are HSP oligosaccharides. Human sperm binding to the zona pellucida is by in the hemizona assay in the of fucose but not other S. A. Fertil. Steril. Full Text PDF PubMed Google Scholar). a HSP glycoprotein also with Lewisx and sperm binding in the hemizona assay by (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). The of fucosylated sequences on free and may promote sperm-egg binding in the human oligosaccharides associated with HSP also a in cell in the male and female reproductive for sperm, are the cell type in HSP from are neutrophils, with of and (reviewed in Ref. H. Fertil. Steril. Full Text PDF PubMed Google Scholar). is a by of in semen (reviewed in Ref. R.J. Hum. Reprod. PubMed Scopus Google Scholar). in a is associated with male H. Fertil. Steril. Full Text PDF PubMed Google Scholar). is also a of into the and an to as the A.E. J. Reprod. Immunol. PubMed Scopus Google Scholar). The of the are neutrophils, with of and A.E. J. Reprod. Immunol. PubMed Scopus Google Scholar). Human sperm express sequences that are by M.S. Oehninger S. Dell A. Morris H. Seppala M. Clark G.F. Hum. Reprod. 1997; PubMed Scopus Google Scholar), are from this type of the sperm from other immune and cell types in semen and the are not is that in HSP by and C. Hum. Reprod. PubMed Scopus Google Scholar). may sperm from the of that prostaglandins and in HSP a in the suppression of R.W. Critchley H.O. Hum. Reprod. 1997; 12: 2200-2207Crossref PubMed Scopus (81) Google Scholar). of the cell with a seminal plasma in and effect on the of the the concentration of the seminal plasma R.W. Hum. Reprod. PubMed Scopus Google Scholar). By of with HSP to the from R.W. Hum. Reprod. PubMed Scopus Google Scholar). This that other components within HSP are for the major effect of this implicated in this is a glycoprotein that Lewisx and sequences with the HSP oligosaccharides (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google milk oligosaccharides the binding of many to in vitro (reviewed in Refs. 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar and D.S. Chem. Google Scholar). of are by fucosylated oligosaccharides in this HSP oligosaccharides also with for tract have been implicated in with human type and human 1997; PubMed Scopus Google Scholar, H. S. E. PubMed Scopus Google Scholar). to HSP oligosaccharides effect against in the male and/or female reproductive free oligosaccharides of sequence are in the HSP of The of a of the complex suggests to in the human to the of free oligosaccharides in human our this is the the of free oligosaccharides in HSP. both human milk and HSP are that contain free oligosaccharides. are significant milk and HSP oligosaccharides revealed by the structural (i) the concentration of free oligosaccharides is in human milk than HSP 0.3–0.4 C. Rudloff S. Baier W. Klein S. PubMed Scopus Google (ii) oligosaccharides are components in HSP not but of the total human milk PubMed Scopus Google (iii) the of complex HSP oligosaccharides are (iv) a subset of HSP oligosaccharides express the reducing end sequence (GlcNAcβ1–3/4Glc) not reported in human milk oligosaccharides; (v) HSP oligosaccharides exclusively express type 2 (Galβ1–4GlcNAc) but not the type 1 sequences (Galβ1–3GlcNAc) that predominate in human milk oligosaccharides C. Rudloff S. Baier W. Klein S. PubMed Scopus Google and (vi) the structural diversity of human milk oligosaccharides that of HSP oligosaccharides S. J. M. M. PubMed Scopus Google Scholar). The for the of HSP and human milk oligosaccharides may and activities associated with free are in human milk J. Full Text PDF PubMed Scopus Google Scholar, Kobata A. J. PubMed Scopus Google Scholar). activities are also in HSP PubMed Scopus Google Scholar, S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar). The of the include the following: (i) to S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar), a in milk J. Biol. Chem. Full Text PDF PubMed Google Scholar) that the of milk from to R.L. S. A. PubMed Scopus Google (ii) in the and PubMed Scopus Google Scholar, S. M. J. Reprod. Fertil. PubMed Scopus Google and (iii) S. M. J. Reprod. Fertil. PubMed Scopus Google Scholar). A is the that human sperm is with this C. PubMed Scopus Google Scholar). is that the of the in vitro 1987; PubMed Scopus Google Scholar). This is with the of fucosylated oligosaccharides in HSP. This in the and is also 12: PubMed Scopus Google Scholar). is that other express free oligosaccharides in seminal plasma. are the of and associated in seminal plasma. a and an are in seminal plasma Biol. Reprod. PubMed Scopus Google Scholar). seminal plasma also contains of J. Reprod. Fertil. Scholar). are to in the of J. Reprod. Fertil. Scholar), but on the in free The of HSP oligosaccharides in the male and/or the female reproductive is not semen into the sperm and other seminal plasma components the to this (reviewed in Ref. 2001; PubMed Google Scholar). It may for components free oligosaccharides to this to within the and the of sperm in the and the sperm in human a in the of the fertilization (reviewed in Ref. 1Setchell B.P. Brooks D.E. Knobil E. Neill J.D. Perspectives in Male Reproduction. Raven Press, Ltd., New York1980: 753-856Google Scholar). a is fertilization in the of of sperm with for successful in vitro fertilization sperm binding The is that male and female within the and this effects of free oligosaccharides on sperm include the following: (i) sperm by (ii) sperm that and (iii) sperm binding to Human sperm and to human vitro E. Fertil. Steril. Full Text Full Text PDF PubMed Scopus Google Scholar). The major associated with human are with Lewisx and sequences J. Biol. Chem. Full Text PDF PubMed Google Scholar), as are HSP oligosaccharides. Human sperm binding to the zona pellucida is by in the hemizona assay in the of fucose but not other S. A. Fertil. Steril. Full Text PDF PubMed Google Scholar). a HSP glycoprotein also with Lewisx and sperm binding in the hemizona assay by (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). The of fucosylated sequences on free and may promote sperm-egg binding in the human The oligosaccharides associated with HSP also a in cell in the male and female reproductive for sperm, are the cell type in HSP from are neutrophils, with of and (reviewed in Ref. H. Fertil. Steril. Full Text PDF PubMed Google Scholar). is a by of in semen (reviewed in Ref. R.J. Hum. Reprod. PubMed Scopus Google Scholar). in a is associated with male H. Fertil. Steril. Full Text PDF PubMed Google Scholar). is also a of into the and an to as the A.E. J. Reprod. Immunol. PubMed Scopus Google Scholar). The of the are neutrophils, with of and A.E. J. Reprod. Immunol. PubMed Scopus Google Scholar). Human sperm express sequences that are by M.S. Oehninger S. Dell A. Morris H. Seppala M. Clark G.F. Hum. Reprod. 1997; PubMed Scopus Google Scholar), are from this type of the sperm from other immune and cell types in semen and the are not is that in HSP by and C. Hum. Reprod. PubMed Scopus Google Scholar). may sperm from the of that prostaglandins and in HSP a in the suppression of R.W. Critchley H.O. Hum. Reprod. 1997; 12: 2200-2207Crossref PubMed Scopus (81) Google Scholar). of the cell with a seminal plasma in and effect on the of the the concentration of the seminal plasma R.W. Hum. Reprod. PubMed Scopus Google Scholar). By of with HSP to the from R.W. Hum. Reprod. PubMed Scopus Google Scholar). This that other components within HSP are for the major effect of this implicated in this is a glycoprotein that Lewisx and sequences with the HSP oligosaccharides (6Morris H.R. Dell A. Easton R.L. Panico M. Koistinen H. Koistinen R. Oehninger S. Patankar M.S. Seppala M. Clark G.F. J. Biol. Chem. 1996; 271: 32159-32167Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). Human milk oligosaccharides the binding of many to in vitro (reviewed in Refs. 9Kunz C. Rudloff S. Baier W. Klein S. PubMed Scopus Google Scholar and D.S. Chem. Google Scholar). of are by fucosylated oligosaccharides in this HSP oligosaccharides also with for tract have been implicated in with human type and human 1997; PubMed Scopus Google Scholar, H. S. E. PubMed Scopus Google Scholar). to HSP oligosaccharides effect against in the male and/or female reproductive free oligosaccharides of sequence are in the HSP of The of a of the complex suggests to in the human to the of free oligosaccharides in human