Sugar-coated sperm: Unraveling the functions of the mammalian sperm glycocalyx

Molecular Reproduction and Development

Volumn 82, Issue 9, 2015, Pages 635-650

  Tecle, Eillen ^a   Gagneux, Pascal ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN; BETA DEFENSIN 126; CD52 ANTIGEN; GLYCAN; GLYCOPROTEIN; GLYCOSPHINGOLIPID; PLACENTA PROTEIN 14; SIALIC ACID DERIVATIVE; SUGAR; UNCLASSIFIED DRUG;

CELL FUNCTION; EPIDIDYMIS; FEMALE GENITAL SYSTEM; GLYCOCALYX; HUMAN; IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SPERM; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON CAPACITATION; SYNTHESIS; TESTIS; ANIMAL; CHEMISTRY; CYTOLOGY; FEMALE; MALE; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; FEMALE; GLYCOCALYX; HUMANS; MALE; MICE; SPERMATOZOA;

EID: 84941731922     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22500     Document Type: Review

References (125)

1. Akama TO, Nakagawa H, Sugihara K, Narisawa S, Ohyama C, Nishimura S, O'Brien DA, Moremen KW, Millan JL, Fukuda MN. 2002. Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 295:124- 127.
2. Akgul Y, Word RA, Ensign LM, Yamaguchi Y, Lydon J, Hanes J, Mahendroo M. 2014. Hyaluronan in cervical epithelia protects against infection-mediated preterm birth. J Clin Invest 124:5481-5489.
3. Alghamdi AS, Foster DN. 2005. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol Reprod 73:1174-1181.
4. Andersch-Bjorkman Y, Thomsson KA, Holmen Larsson JM, Ekerhovd E, Hansson GC. 2007. Large scale identification of proteins, mucins, and their O-glycosylation in the endocervical mucus during the menstrual cycle. Mol Cell Proteomics 6:708-716.
5. Arenas MI, de Miguel MP, Bethencourt FR, Fraile B, Royuela M, Paniagua R. 1996. Lectin histochemistry in the human epididymis. J Reprod Fertil 106:313-320.
6. Ariga T, Miyatake T, Yu RK. 2010. Role of proteoglycans and glycosaminoglycans in the pathogenesis of Alzheimer's disease and related disorders: Amyloidogenesis and therapeutic strategies-a review. J Neurosci Res 88:2303-2315.
7. Batista F, Lu L, Williams SA, Stanley P. 2012. Complex N-glycans are essential, but core 1 and 2 mucin O-glycans, O-fucose glycans, and NOTCH1 are dispensable, for mammalian spermatogenesis. Biol Reprod 86:179.
8. Bedford JM. 1983. Significance of the need for sperm capacitation before fertilization in eutherian mammals. Biol Reprod 28:108-120.
9. Belleannee C, Thimon V, Sullivan R. 2012. Region-specific gene expression in the epididymis. Cell Tissue Res 349:717-731.
10. Bernal A, Torres J, Reyes A, Rosado A. 1980. Presence and regional distribution of sialyl transferase in the epididymis of the rat. Biol Reprod 23:290- 293.
11. Bi J, Li Y, Sun F, Saalbach A, Klein C, Miller DJ, Hess R, Nowak RA. 2013. Basigin null mutant male mice are sterile and exhibit impaired interactions between germ cells and Sertoli cells. Dev Biol 380:145-156.
12. Bianchi PG, De Agostini A, Fournier J, Guidetti C, Tarozzi N, Bizzaro D, Manicardi GC. 2004. Human cervical mucus can act in vitro as a selective barrier against spermatozoa carrying fragmented DNA and chromatin structural abnormalities. J Assist Reprod Genet 21:97-102.
13. Bishop J, Gagneux P. 2007. Evolution of carbohydrate antigens-microbial forces shaping host glycomes? Glycobiology 17:23R-34R.
14. Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, Kataoka H, Nabeshima K. 1995. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 55:434-439.
15. Bulow HE, Hobert O. 2006. The molecular diversity of glycosaminoglycans shapes animal development. Annu Rev Cell Dev Biol 22:375-407.
16. Cartwright EJ, Cowin A, Sharpe PT. 1991. Surface heterogeneity of bovine sperm revealed by aqueous two-phase partition. Biosci Rep 11:265-273.
17. Ceballos A, Remes Lenicov F, Sabatte J, Rodriguez Rodrigues C, Cabrini M, Jancic C, Raiden S, Donaldson M, Agustin Pasqualini RJ, Marin- Briggiler C, Vazquez-Levin M, Capani F, Amigorena S, Geffner J. 2009. Spermatozoa capture HIV-1 through heparan sulfate and efficiently transmit the virus to dendritic cells. J Exp Med 206:2717-2733.
18. Chen L, Bi J, Nakai M, Bunick D, Couse JF, Korach KS, Nowak RA. 2010. Expression of basigin in reproductive tissues of estrogen receptor-{alpha} or -{beta} null mice. Reproduction 139:1057-1066.
19. Chiu PC, Chung MK, Koistinen R, Koistinen H, Seppala M, Ho PC, Ng EH, Lee KF, Yeung WS. 2007a. Cumulus oophorus-associated glycodelin-C displaces sperm-bound glycodelin-A and -F and stimulates spermatozoa-zona pellucida binding. J Biol Chem 282:5378-5388.
20. Chiu PC, Chung MK, Koistinen R, Koistinen H, Seppala M, Ho PC, Ng EH, Lee KF, Yeung WS. 2007b. Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding. J Cell Sci 120:33-44.
21. Chou HH, Hayakawa T, Diaz S, Krings M, Indriati E, Leakey M, Paabo S, Satta Y, Takahata N, Varki A. 2002. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci USA 99:11736-11741.
22. Chou HH, Takematsu H, Diaz S, Iber J, Nickerson E, Wright KL, Muchmore EA, Nelson DL, Warren ST, Varki A. 1998. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA 95:11751-11756.
23. Chui D, Oh-Eda M, Liao YF, Panneerselvam K, Lal A, Marek KW, Freeze HH, Moremen KW, Fukuda MN, Marth JD. 1997. Alpha- mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 90:157-167.
24. Chui D, Sellakumar G, Green R, Sutton-Smith M, McQuistan T, Marek K, Morris H, Dell A, Marth J. 2001. Genetic remodeling of protein glycosylation in vivo induces autoimmune disease. Proc Natl Acad Sci U S A 98:1142-1147.
25. Cohen M, Varki A. 2010. The sialome-far more than the sum of its parts. OMICS 14:455-464.
26. Cornwall GA 2014. Role of posttranslational protein modifications in epididymal sperm maturation and extracellular quality control. Adv Exp Med Biol 759:159-180.
27. Dadoune JP, Siffroi JP, Alfonsi MF. 2004. Transcription in haploid male germ cells. Int Rev Cytol 237:1-56.
28. Diekman AB. 2003. Glycoconjugates in sperm function and gamete interactions: How much sugar does it take to sweet-talk the egg? Cell Mol Life Sci 60:298-308.
29. Diekman AB, Norton EJ, Klotz KL, Westbrook VA, Herr JC. 1999. Evidence for a unique N-linked glycan associated with human infertility on sperm C D52: a candidate contraceptive vaccinogen. Immunol Rev 171:203-211.
30. Dobrinski I, Ignotz GG, Thomas PG, Ball BA. 1996. Role of carbohydrates in the attachment of equine spermatozoa to uterine tubal (oviductal) epithelial cells in vitro. Am J Vet Res 57:1635-1639.
31. Dobrinski I, Smith TT, Suarez SS, Ball BA. 1997. Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro. Biol Reprod 56:861-869.
32. Drake PM, Nathan JK, Stock CM, Chang PV, Muench MO, Nakata D, Reader JR, Gip P, Golden KP, Weinhold B, Gerardy-Schahn R, Troy FA, Bertozzi CR. 2008. Polysialic acid, a glycan with highly restricted expression, is found on human and murine leukocytes and modulates immune responses. J Immunol 181:6850-6858.
33. Dravland E, Joshi MS. 1981. Sperm-coating antigens secreted by the epididymis and seminal vesicle of the rat. Biol Reprod 25:649-658.
34. Eberhard WL. 1996. Female control: Sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press. pp 147-148.
35. Familiari G, Motta PM. 1980. Morphological changes of mouse spermatozoa in uterus as revealed by scanning and transmission electron microscopy. Acta Biol Acad Sci Hung 31:57-67.
36. Flickinger CJ, Herr JC, McGee RS, Sigman M, Evans RJ, Sutherland WM, Summers TA, Spell DR, Conklin DJ. 1990. Dynamics of a human seminal vesicle specific protein. Andrologia 22:142-154.
37. Focarelli R, Rosati F, Terrana B. 1990. Sialyglycoconjugates release during in vitro capacitation of human spermatozoa. J Androl 11:97-104.
38. Foresta C, Patassini C, Bertoldo A, Menegazzo M, Francavilla F, Barzon L, Ferlin A. 2011. Mechanism of human papillomavirus binding to human spermatozoa and fertilizing ability of infected spermatozoa. PLoS One 6:e15036.
39. Franke FE, Kraus S, Eiermann C, Pauls K, Lalani EN, Bergmann M. 2001. MUC1 in normal and impaired spermatogenesis. Mol Hum Reprod 7:505-512.
40. Fujihara Y, Okabe M, Ikawa M. 2014. GPI-anchored protein complex, LY6K/TEX101, is required for sperm migration into the oviduct and male fertility in mice. Biol Reprod 90:60.
41. Fujisawa M, Kanai Y, Nam SY, Maeda S, Nakamuta N, Kano K, Kurohmaru M, Hayashi Y. 2004. Expression of Prnp mRNA (prion protein gene) in mouse spermatogenic cells. J Reprod Dev 50:565-570.
42. Fukuda MN, Akama TO. 2002. In vivo role of alpha-mannosidase IIx: Ineffective spermatogenesis resulting from targeted disruption of the Man2a2 in the mouse. Biochim Biophys Acta 1573:382-387.
43. Fukuda MN, Akama TO. 2003. The role of N-glycans in spermatogenesis. Cytogenet Genome Res 103:302-306.
44. Gagneux P, Varki A. 1999. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 9:747-755.
45. Galili U. 1993. Evolution and pathophysiology of the human natural anti-alpha-galactosyl IgG (anti-Gal) antibody. Springer Semin Immunopathol 15:155-171.
46. Ghaderi D, Springer SA, Ma F, Cohen M, Secrest P, Taylor RE, Varki A, Gagneux P. 2011. Sexual selection by female immunity against paternal antigens can fix loss of function alleles. Proc Natl Acad Sci USA 108:17743-17748.
47. Gilks CB, Reid PE, Clement PB, Owen DA. 1989. Histochemical changes in cervical mucus-secreting epithelium during the normal menstrual cycle. Fertil Steril 51:286-291.
48. Gmachl M, Sagan S, Ketter S, Kreil G. 1993. The human sperm protein PH-20 has hyaluronidase activity. FEBS Lett 336:545-548.
49. Hammond E, Khurana A, Shridhar V, Dredge K. 2014. The Role of heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics. Front Oncol 4:195.
50. Hao J, Chen M, Ji S, Wang X, Wang Y, Huang X, Yang L, Wang Y, Cui X, Lv L, Liu Y, Gao F. 2014. Equatorin is not essential for acrosome biogenesis but is required for the acrosome reaction. Biochem Biophys Res Commun 444:537-542.
51. Hardiyanto L, Hasegawa A, Komori S. 2012. The N-linked carbohydrate moiety of male reproductive tract CD52 (mrt-CD52) interferes with the complement system via binding to C1q. J Reprod Immunol 94:142-150.
52. Hasegawa A, Fu Y, Tsubamoto H, Tsuji Y, Sawai H, Komori S, Koyama K. 2003. Epitope analysis for human sperm- immobilizing monoclonal antibodies, MAb H6-3C4, 1G12 and campath-1. Mol Hum Reprod 9:337-343.
53. Hasegawa A, Koyama K. 2005. Antigenic epitope for sperm-immobilizing antibody detected in infertile women. J Reprod Immunol 67:77- 86.
54. Holt CE, Dickson BJ. 2005. Sugar codes for axons? Neuron 46:169-172.
55. Huang HH, Stanley P. 2010. A testis-specific regulator of complex and hybrid N-glycan synthesis. J Cell Biol 190:893-910.
56. Igakura T, Kadomatsu K, Kaname T, Muramatsu H, Fan QW, Miyauchi T, Toyama Y, Kuno N, Yuasa S, Takahashi M, Senda T, Taguchi O, Yamamura K, Arimura K, Muramatsu T. 1998. A null mutation in basigin, an immunoglobulin superfamily member, indicates its important roles in peri-implantation development and spermatogenesis. Dev Biol 194:152-165.
57. Ikawa M, Tokuhiro K, Yamaguchi R, Benham AM, Tamura T, Wada I, Satouh Y, Inoue N, Okabe M. 2011. Calsperin is a testis-specific chaperone required for sperm fertility. J Biol Chem 286:5639-5646.
58. Ioffe E, Stanley P. 1994. Mice lacking N-acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc Natl Acad Sci USA 91:728-732.
59. Katila T. 2012. Post-mating inflammatory responses of the uterus. Reprod Domest Anim 47:31-41.
60. Kirchhoff C, Hale G. 1996. Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Mol Hum Reprod 2:177-184.
61. Koistinen H, Koistinen R, Dell A, Morris HR, Easton RL, Patankar MS, Oehninger S, Clark GF, Seppala M. 1996. Glycodelin from seminal plasma is a differentially glycosylated form of contraceptive glycodelin-A. Mol Hum Reprod 2:759-765.
62. Koyama K, Hasegawa A, Komori S. 2009. Functional aspects of CD52 in reproduction. J Reprod Immunol 83:56-59.
63. Kratz E, Poland DC, van DW, Katnik-Prastowska I. 2003. Alterations of branching and differential expression of sialic acid on alpha-1-acid glycoprotein in human seminal plasma. Clin Chim Acta 331:87-95.
64. Kraushaar DC, Dalton S, Wang L. 2013. Heparan sulfate: A key regulator of embryonic stem cell fate. Biol Chem 394:741-751.
65. Langsdorf A, Schumacher V, Shi X, Tran T, Zaia J, Jain S, Taglienti M, Kreidberg JA, Fine A, Ai X. 2011. Expression regulation and function of heparan sulfate 6-O-endosulfatases in the spermatogonial stem cell niche. Glycobiology 21:152-161.
66. Lee MC, Damjanov I. 1984. Anatomic distribution of lectin-binding sites in mouse testis and epididymis. Differentiation 27:74-81.
67. Lemaire L, Heinlein UA. 1992. Stage-specific mouse testis cell surface alterations detected by fluorescence-labeled lectins. Cell Biol Int Rep 16:675-677.
68. Lohr M, Kaltner H, Schwartz-Albiez R, Sinowatz F, Gabius HJ. 2010. Towards functional glycomics by lectin histochemistry: strategic probe selection to monitor core and branch-end substitutions and detection of cell-type and regional selectivity in adult mouse testis and epididymis. Anat Histol Embryol 39:481-493.
69. Ma F, Wu D, Deng L, Secrest P, Zhao J, Varki N, Lindheim S, Gagneux P. 2012. Sialidases on mammalian sperm mediate deciduous sialylation during capacitation. J Biol Chem 287:38073-38079.
70. Marth JD. 2008. A unified vision of the building blocks of life. Nat Cell Biol 10:1015-1016.
71. Mori S, Kadokawa Y, Hoshinaga K, Marunouchi T. 2003. Sequential activation of Notch family receptors during mouse spermatogenesis. Dev Growth Differ 45:7-13.
72. Morrow EH, Innocenti P. 2012. Female postmating immune responses, immune system evolution and immunogenic males. Biol Rev Camb Philos Soc 87:631-638.
73. Nakanishi T, Isotani A, Yamaguchi R, Ikawa M, Baba T, Suarez SS, Okabe M. 2004. Selective passage through the uterotubal junction of sperm from a mixed population produced by chimeras of calmegin-knockout and wild-type male mice. Biol Reprod 71:959-965.
74. Netzel-Arnett S, Bugge TH, Hess RA, Carnes K, Stringer BW, Scarman AL, Hooper JD, Tonks ID, Kay GF, Antalis TM. 2009. The glycosylphosphatidylinositol-anchored serine protease PRSS21 (testisin) imparts murine epididymal sperm cell maturation and fertilizing ability. Biol Reprod 81:921-932.
75. Osheroff JE, Visconti PE, Valenzuela JP, Travis AJ, Alvarez J, Kopf GS. 1999. Regulation of human sperm capacitation by a cholesterol efflux-stimulated signal transduction pathway leading to protein kinase A-mediated up-regulation of protein tyrosine phosphorylation. Mol Hum Reprod 5:1017-1026.
76. Padler-Karavani V, Yu H, Cao H, Chokhawala H, Karp F, Varki N, Chen X, Varki A. 2008. Diversity in specificity, abundance, and composition of anti-Neu5Gc antibodies in normal humans: Potential implications for disease. Glycobiology 18:818-830.
77. Pandya IJ, Cohen J. 1985. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil Steril 43:417-421.
78. Pang PC, Tissot B, Drobnis EZ, Sutovsky P, Morris HR, Clark GF, Dell A. 2007. Expression of bisecting type and Lewisx/Lewisy terminated N-glycans on human sperm. J Biol Chem 282:36593-36602.
79. Parry S, Wong NK, Easton RL, Panico M, Haslam SM, Morris HR, Anderson P, Klotz KL, Herr JC, Diekman AB, Dell A. 2007. The sperm agglutination antigen-1 (SAGA-1) glycoforms of CD52 are O-glycosylated. Glycobiology 17:1120-1126.
80. Pollard JW, Plante C, King WA, Hansen PJ, Betteridge KJ, Suarez SS. 1991. Fertilizing capacity of bovine sperm may be maintained by binding of oviductal epithelial cells. Biol Reprod 44:102-107.
81. Rabionet M, van der Spoel AC, Chuang CC, von Tumpling-Radosta B, Litjens M, Bouwmeester D, Hellbusch CC, Korner C, Wiegandt H, Gorgas K, Platt FM, Grone HJ, Sandhoff R. 2008. Male germ cells require polyenoic sphingolipids with complex glycosylation for completion of meiosis: a link to ceramide synthase-3. J Biol Chem 283:13357-13369.
82. Rooney IA, Atkinson JP, Krul ES, Schonfeld G, Polakoski K, Saffitz JE, Morgan BP. 1993. Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J Exp Med 177:1409-1420.
83. Ruddock LW, Molinari M. 2006. N-glycan processing in ER quality control. J Cell Sci 119:4373-4380.
84. Russo CL, Spurr-Michaud S, Tisdale A, Pudney J, Anderson D, Gipson IK. 2006. Mucin gene expression in human male urogenital tract epithelia. Hum Reprod 21:2783-2793.
85. Sandhoff R, Geyer R, Jennemann R, Paret C, Kiss E, Yamashita T, Gorgas K, Sijmonsma TP, Iwamori M, Finaz C, Proia RL, Wiegandt H, Grone HJ. 2005. Novel class of glycosphingolipids involved in male fertility. J Biol Chem 280:27310-27318.
86. Sandler L, Novitski E. 1957. Meiotic drive as an evolutionary force. Am Nat XCI, 857:105-110.
87. Saxena DK, Oh-Oka T, Kadomatsu K, Muramatsu T, Toshimori K. 2002. Behaviour of a sperm surface transmembrane glycoprotein basigin during epididymal maturation and its role in fertilization in mice. Reproduction 123:435-444.
88. Schnaar RL, Suzuki A, Stanley P. 2009. Glycosphingolipids. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of Glycobiology. 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009. Chapter 10, pp 129-142.
89. Schröter S, Osterhoff C, McArdle W, Ivell R. 1999. The glycocalyx of the sperm surface. Hum Reprod Update 5:302-313.
90. Schultz N, Hamra FK, Garbers DL. 2003. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci USA 100:12201-12206.
91. Seo JT, Lee JS, Jun JH, Yang MH. 2005. Expression of mucin genes in the human testis and its relationship to spermatogenesis. Yonsei Med J 46:667-672.
92. Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, Robertson SA. 2012. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol 188:2445-2454.
93. Simon P, Baumner S, Busch O, Rohrich R, Kaese M, Richterich P, Wehrend A, Muller K, Gerardy- Schahn R, Muhlenhoff M, Geyer H, Geyer R, Middendorff R, Galuska SP. 2013. Polysialic acid is present in mammalian semen as a post-translational modification of the neural cell adhesion molecule NCAM and the polysialyltransferase ST8SiaII. J Biol Chem 288:18825-18833.
94. Skudlarek MD, 1993. Beta-D-galactosidase of rat spermatozoa: Subcellular distribution, substrate specificity, and molecular changes during epididymal maturation. Biol Reprod 49:204-213.
95. Springer SA, Tulsiani DR, Nagdas SK, Orgebin-Crist MC. 2013. Glycan evolution in response to collaboration, conflict, and constraint. J Biol Chem 288:6904-6911.
96. Stanley P, Schachter H, Taniguchi N. 2009. N- Glycans. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of glycobiology. 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009. Chapter 13, pp 175-198.
97. Suarez SS. 2008. Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol 52:455-462.
98. Suarez SS, Pacey AA. 2006a. Sperm transport in the female reproductive tract. Hum Reprod Update 12:23-37.
99. Suarez SS, Pacey AA. 2006b. Sperm transport in the female reproductive tract. Hum Reprod Update 12:23-37.
100. Sullivan R, Frenette G, Girouard J. 2007. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 9:483-491.
101. Takamiya K, Yamamoto A, Furukawa K, Zhao J, Fukumoto S, Yamashiro S, Okada M, Haraguchi M, Shin M, Kishikawa M, Shiku H, Aizawa S, Furukawa K. 1998. Complex gangliosides are essential in spermatogenesis of mice: Possible roles in the transport of testosterone. Proc Natl Acad Sci USA 95:12147-12152.
102. Tang W, Chang SB, Hemler ME. 2004. Links between CD147 function, glycosylation, and caveolin-1. Mol Biol Cell 15:4043-4050.
103. Tateno H, Krapf D, Hino T, Sanchez-Cardenas C, Darszon A, Yanagimachi R, Visconti PE. 2013. Ca2+ ionophore A23187 can make mouse spermatozoa capable of fertilizing in vitro without activation of cAMP-dependent phosphorylation pathways. Proc Natl Acad Sci USA 110:18543-18548.
104. Taylor RE, Gregg CJ, Padler-Karavani V, Ghaderi D, Yu H, Huang S, Sorensen RU, Chen X, Inostroza J, Nizet V, Varki A. 2010. Novel mechanism for the generation of human xeno-autoantibodies against the nonhuman sialic acid N-glycolylneuraminic acid. J Exp Med 20:1637-1646.
105. Thompson LA, Barratt CL, Bolton AE, Cooke ID. 1992. The leukocytic reaction of the human uterine cervix. Am J Reprod Immunol 28:85-89.
106. Tollner TL, Bevins CL, Cherr GN. 2012. Multifunctional glycoprotein DEFB126-a curious story of defensin-clad spermatozoa. Nat Rev Urol 9:365-375.
107. Tollner TL, Venners SA, Hollox EJ, Yudin AI, Liu X, Tang G, Xing H, Kays RJ, Lau T, Overstreet JW, Xu X, Bevins CL, Cherr GN. 2011. A common mutation in the defensin DEFB126 causes impaired sperm function and subfertility. Sci Transl Med 3:92ra65.
108. Tollner TL, Yudin AI, Tarantal AF, Treece CA, Overstreet JW, Cherr GN. 2008a. Beta-defensin 126 on the surface of macaque sperm mediates attachment of sperm to oviductal epithelia. Biol Reprod 78:400-412.
109. Tollner TL, Yudin AI, Treece CA, Overstreet JW, Cherr GN. 2008b. Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus. Hum Reprod 23:2523-2534.
110. Toole BP. 2003. Emmprin (CD147), a cell surface regulator of matrix metalloproteinase production and function. Curr Top Dev Biol 54:371-389.
111. Toshimori K, Araki S, Oura C, Eddy EM. 1991. Loss of sperm surface sialic acid induces phagocytosis: An assay with a monoclonal antibody T21, which recognizes a 54K sialoglycoprotein. Arch Androl 27:79-86.
112. Tulsiani DR. 2003. Glycan modifying enzymes in luminal fluid of rat epididymis: Are they involved in altering sperm surface glycoproteins during maturation? Microsc Res Tech 61:18-27.
113. Tulsiani DR. 2006. Glycan-modifying enzymes in luminal fluid of the mammalian epididymis: An overview of their potential role in sperm maturation. Mol Cell Endocrinol 250:58-65.
114. Tulsiani DR, Orgebin-Crist MC, Skudlarek MD. 1998. Role of luminal fluid glycosyltransferases and glycosidases in the modification of rat sperm plasma membrane glycoproteins during epididymal maturation. J Reprod Fertil Suppl 53:85-97.
115. Tulsiani DR, Skudlarek MD, Holland MK, Orgebin-Crist MC. 1993. Glycosylation of rat sperm plasma membrane during epididymal maturation. Biol Reprod 48:417-428.
116. Varki A. 2011. Since there are PAMPs and DAMPs, there must be SAMPs? Glycan "self-associated molecular patterns" dampen innate immunity, but pathogens can mimic them. Glycobiology 21:1121- 1124.
117. Varki A, Esko JD, Colley KJ. 2009. Cellular organization of glycosylation. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of glycobiology. 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009. Chapter 3, pp 37-46.
118. Ventela S, Toppari J, Parvinen M. 2003. Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: Mechanisms of haploid gene product sharing. Mol Biol Cell 14:2768-2780.
119. Vives RR, Seffouh A, Lortat-Jacob H. 2014. Post-synthetic regulation of HS structure: The Yin and Yang of the sulfs in sancer. Front Oncol 3:331.
120. Wang Y, Tan J, Sutton-Smith M, Ditto D, Panico M, Campbell RM, Varki NM, Long JM, Jaeken J, Levinson SR, Wynshaw-Boris A, Morris HR, Le D, Dell A, Schachter H, Marth JD. 2001. Modeling human congenital disorder of glycosylation type IIa in the mouse: Conservation of asparagine-linked glycan-dependent functions in mammalian physiology and insights into disease pathogenesis. Glycobiology 11:1051-1070.
121. Watanabe H, Takeo T, Tojo H, Sakoh K, Berger T, Nakagata N, Mak TW, Kondoh G. 2014. Lipocalin 2 binds to membrane phosphatidylethanolamine to induce lipid raft movement in a PKA-dependent manner and modulates sperm maturation. Development 141:2157-2164.
122. Yamaguchi R, Yamagata K, Ikawa M, Moss SB, Okabe M. 2006. Aberrant distribution of ADAM3 in sperm from both angiotensin-converting enzyme (Ace)- and calmegin (Clgn)-deficient mice. Biol Reprod 75:760-766.
123. Yeung WS, Lee KF, Koistinen R, Koistinen H, Seppala M, Ho PC, Chiu PC. 2006. Roles of glycodelin in modulating sperm function. Mol Cell Endocrinol 250:149-156.
124. Yeung WS, Lee KF, Koistinen R, Koistinen H, Seppala M, Ho PC, Chiu PC. 2007. Glycodelin: A molecule with multi-functions on spermatozoa. Soc Reprod Fertil Suppl 63:143-151.
125. Yudin AI, Generao SE, Tollner TL, Treece CA, Overstreet JW, Cherr GN. 2005. Beta-defensin 126 on the cell surface protects sperm from immunorecognition and binding of anti-sperm antibodies. Biol Reprod 73:1243-1252.