Skip to main content

Advertisement

Log in

Tetraspanins in mammalian reproduction: spermatozoa, oocytes and embryos

  • Review
  • Published:
Medical Microbiology and Immunology Aims and scope Submit manuscript

A Correction to this article was published on 20 June 2020

This article has been updated

Abstract

It is known that tetraspanin proteins are involved in many physiological somatic cell mechanisms. Additionally, research has indicated they also have a role in various infectious diseases and cancers. This review focuses on the molecular interactions underlying the tetraspanin web formation in gametes. Primarily, tetraspanins act in the reproductive tract as organizers of membrane complexes, which include the proteins involved in the contact and association of sperm and oocyte membranes. In addition, recent data shows that tetraspanins are likely to be involved in these processes in a complex way. In mammalian fertilization, an important role is attributed to CD molecules belonging to the tetraspanin superfamily, particularly CD9, CD81, CD151, and also CD63; mostly as part of extracellular vesicles, the significance of which and their potential in reproduction is being intensively investigated. In this article, we reviewed the existing knowledge regarding the expression of tetraspanins CD9, CD81, CD151, and CD63 in mammalian spermatozoa, oocytes, and embryos and their involvement in reproductive processes, including pathological events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Change history

References

  1. Rubinstein E, Ziyyat A, Wolf JP, Le Naour F, Boucheix C (2006) The molecular players of sperm–egg fusion in mammals. Semin Cell Dev Biol 17:254–263. https://doi.org/10.1016/j.semcdb.2006.02.012

    Article  CAS  PubMed  Google Scholar 

  2. Barraud-Lange V, Boucheix C (2013) The role of tetraspanin complexes in egg-sperm fusion. In: Berditchevski F, Rubinstein E (eds) Tetraspanins proteins and cell regulation 9. Springer, Dordrecht, pp 203–231

    Google Scholar 

  3. Machtinger R, Laurent LC, Baccarelli AA (2016) Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum Reprod Update 22:182–193. https://doi.org/10.1093/humupd/dmv055

    Article  CAS  PubMed  Google Scholar 

  4. Hemler ME (2001) Specific tetraspanin functions. J Cell Biol 155:1103–1108. https://doi.org/10.1083/jcb.200108061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Berditchevski F, Odintsova E, Sawada S, Gilbert E (2002) Expression of the palmitoylation-deficient CD151 weakens the association of α3β1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling. J Biol Chem 277:36991–37000. https://doi.org/10.1074/jbc.M205265200

    Article  CAS  PubMed  Google Scholar 

  6. Charrin S, Manié S, Oualid M, Billard M, Boucheix C, Rubinstein E (2002) Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Lett 516:139–144. https://doi.org/10.1016/S0014-5793(02)02522-X

    Article  CAS  PubMed  Google Scholar 

  7. Yang X, Claas C, Kraeft SK, Chen LB, Wang Z, Kreidberg JA, Hemler ME (2002) Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Mol Biol Cell 13:767–781. https://doi.org/10.1091/mbc.01-05-0275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci CMLS 58:1189–1205. https://doi.org/10.1007/PL00000933

    Article  CAS  PubMed  Google Scholar 

  9. Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y, Xie X, Yu Y, Yu X, Chen S, Zhang S, Pontarotti P, Xu A (2005) The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86:674–684. https://doi.org/10.1016/j.ygeno.2005.08.004

    Article  CAS  PubMed  Google Scholar 

  10. van Spriel AB, Figdor CG (2010) The role of tetraspanins in the pathogenesis of infectious diseases. Microbes Infect 12:106–112. https://doi.org/10.1016/j.micinf.2009.11.001

    Article  CAS  PubMed  Google Scholar 

  11. Martin F, Roth DM, Jans DA, Pouton CW, Partridge LJ, Monk PN, Moseley GW (2005) Tetraspanins in viral infections: a fundamental role in viral biology? J Virol 79:10839–10851. https://doi.org/10.1128/JVI.79.17.10839-10851.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Florin L, Lang T (2018) Tetraspanin assemblies in virus infection. Front Immunol 9:1140. https://doi.org/10.3389/fimmu.2018.01140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hemler ME (2014) Tetraspanin proteins promote multiple cancer stages. Nat Rev Cancer 14:49–60. https://doi.org/10.1038/nrc3640

    Article  CAS  PubMed  Google Scholar 

  14. Detchokul S, Williams ED, Parker MW, Frauman AG (2014) Tetraspanins as regulators of the tumour microenvironment: implications for metastasis and therapeutic strategies. Br J Pharmacol 171:5462–5490. https://doi.org/10.1111/bph.12260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Yanagimachi R (1994) Mammalian fertilization. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven Press, New York, pp 189–317

    Google Scholar 

  16. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N (2011) Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 108:4892–4896. https://doi.org/10.1073/pnas.1018202108

    Article  PubMed  PubMed Central  Google Scholar 

  17. Austin CR (1951) Observations on the penetration of the sperm into the mammalian egg. Aust J Biol Sci 4:581–596. https://doi.org/10.1071/bi9510581

    Article  CAS  Google Scholar 

  18. Chang MC (1951) Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697–698. https://doi.org/10.1038/168697b0

    Article  CAS  PubMed  Google Scholar 

  19. Chang H, Suarez SS (2011) Two distinct Ca2+ signaling pathways modulate sperm flagellar beating patterns in mice. Biol Reprod 85:296–305. https://doi.org/10.1095/biolreprod.110.089789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Florman HM, Fissore RA (2015) Fertilization in Mammals. In: Plant TM, Zeleznik AJ (eds) Knobil and Neill’s physiology of reproduction, 4th edn. Academic Press, San Diego, pp 149–196

    Chapter  Google Scholar 

  21. Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Mekada E (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287:321–324. https://doi.org/10.1126/science.287.5451.321

    Article  CAS  PubMed  Google Scholar 

  22. Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C (2000) Severely reduced female fertility in CD9-deficient mice. Science 287:319–321. https://doi.org/10.1126/science.287.5451.319

    Article  PubMed  Google Scholar 

  23. Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A (2000) The gamete fusion process is defective in eggs of CD9-deficient mice. Nat Genet 24:279–282. https://doi.org/10.1038/73502

    Article  CAS  PubMed  Google Scholar 

  24. Kaji K, Oda S, Miyazaki S, Kudo A (2002) Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed for molecular analysis of sperm–egg fusion. Dev Biol 247:327–334. https://doi.org/10.1006/dbio.2002.0694

    Article  CAS  PubMed  Google Scholar 

  25. Zhu GZ, Miller BJ, Boucheix C, Rubinstein E, Liu CC, Hynes RO, Myles DG, Primakoff P (2002) Residues SFQ (173–175) in the large extracellular loop of CD9 are required for gamete fusion. Development 129:1995–2002

    Article  CAS  PubMed  Google Scholar 

  26. Chen MS, Tung KSK, Coonrod SA, Takahashi Y, Bigler D, Chang A, Yamashita Y, Kincade PW, Herr JC, Whiteet JM (1999) Role of the integrin-associated protein CD9 in binding between sperm ADAM 2 and the egg integrin α6β1: Implications for murine fertilization. Proc Natl Acad Sci 96:11830–11835. https://doi.org/10.1073/pnas.96.21.11830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Runge KE, Evans JE, He ZY, Gupta S, McDonald KL, Stahlberg H, Primakoff P, Mylesa DG (2007) Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 304:317–325. https://doi.org/10.1016/j.ydbio.2006.12.041

    Article  CAS  PubMed  Google Scholar 

  28. Coskun S, Elnour A, Hellani A, Gaafar T (2003) CD9 is expressed on human oocytes. Fertil Steril 80:268. https://doi.org/10.1016/S0015-0282(03)01678-9

    Article  Google Scholar 

  29. Ziyyat A, Rubinstein E, Monier-Gavelle F, Barraud V, Kulski O, Prenant M, Boucheix C, Bomsel M, Wolf JP (2006) CD9 controls the formation of clusters that contain tetraspanins and the integrin α6β1, which are involved in human and mouse gamete fusion. J Cell Sci 119:416–424. https://doi.org/10.1242/jcs.02730

    Article  CAS  PubMed  Google Scholar 

  30. Giacomini E, Vago R, Sanchez AM, Podini P, Zarovni N, Murdica V, Rizzo R, Bortolotti D, Candiani M, Viganò P (2017) Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-05549-w

    Article  CAS  Google Scholar 

  31. Vyas P, Balakier H, Librach CL (2019) Ultrastructural identification of CD9 positive extracellular vesicles released from human embryos and transported through the zona pellucida. Syst Biol Reprod Med. https://doi.org/10.1080/19396368.2019.1619858

    Article  PubMed  Google Scholar 

  32. Li YH, Hou Y, Ma W, Yuan JX, Zhang D, Sun QY, Wang WH (2004) Localization of CD9 in pig oocytes and its effects on sperm–egg interaction. Reproduction 127:151–157. https://doi.org/10.1530/rep.1.00006

    Article  CAS  PubMed  Google Scholar 

  33. Airuungowa WJ, Uyhan U, Shi Z, Zamgaa O, Enkhmaart YW, Wuri L, Cui Y, Nasanochir N, Feng JS (2016) Localization of CD9 on sheep oocytes and early embryos. Int J Clin Exp Me 9:7996–8004

    CAS  Google Scholar 

  34. Pan Y, Wang M, Baloch AR, Zhang Q, Wang J, Ma R, Xu G, Kashif J, Wang L, Fan J, Cui Y, Set Y (2019) FGF10 enhances yak oocyte fertilization competence and subsequent blastocyst quality and regulates the levels of CD9, CD81, DNMT1, and DNMT3B. J Cell Physiol 234:17677–17689. https://doi.org/10.1002/jcp.28394

    Article  CAS  PubMed  Google Scholar 

  35. Zhou GB, Liu GS, Meng QG, Liu Y, Hou YP, Wang XX, Li N, Zhu SE (2009) Tetraspanin CD9 in bovine oocytes and its role in rertilization. J Reprod Dev 55:305–308. https://doi.org/10.1262/jrd.20099

    Article  CAS  PubMed  Google Scholar 

  36. Jankovicova J, Secova P, Manaskova-Postlerova P, Simonik O, Frolikova M, Chmelikova E, Horovska L, Michalkova K, Dvorakova-Hortova K, Antalikova J (2019) Detection of CD9 and CD81 tetraspanins in bovine and porcine oocytes and embryos. Int J Biol Macromol 123:931–938. https://doi.org/10.1016/j.ijbiomac.2018.11.161

    Article  CAS  PubMed  Google Scholar 

  37. Dusinský R, Simon M, Nouzovská D (1988) Preparation of monoclonal antibodies against cell surface antigens in cattle. Vet Med (Praha) 33:135–142

    PubMed  Google Scholar 

  38. Zuidscherwoude M, Göttfert F, Dunlock VME, Figdor CG, van den Bogaart G, van Spriel AB (2015) The tetraspanin web revisited by super-resolution microscopy. Sci Rep 5:1–18. https://doi.org/10.1038/srep12201

    Article  CAS  Google Scholar 

  39. Dominguez R (2004) Actin-binding proteins—a unifying hypothesis. Trends Biochem Sci 29:572–578. https://doi.org/10.1016/j.tibs.2004.09.004

    Article  CAS  PubMed  Google Scholar 

  40. Macaulay AD, Gilbert I, Scantland S, Fournier E, Ashkar F, Bastien A, Saadi HAS, Gagné D, Sirard MA, Khandjian ÉW, Richard FJ, Hyttel P, Robert C (2016) Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation. Biol Reprod 94:16. https://doi.org/10.1095/biolreprod.114.127571

    Article  CAS  PubMed  Google Scholar 

  41. Barraud-Lange V, Naud-Barriant N, Bomsel M, Wolf JP, Ziyyat A (2007) Transfer of oocyte membrane fragments to fertilizing spermatozoa. FASEB J 21:3446–3449. https://doi.org/10.1096/fj.06-8035hyp

    Article  CAS  PubMed  Google Scholar 

  42. Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M, Wang X, Miyamoto K, Akutsu H, Kondo T, Takahashi Y, Ban T, Ito Ch, Toshimori K, Nakamura A, Ito M, Miyado M, Mekada E, Umezawa A (2008) The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc Natl Acad Sci 105:12921–12926. https://doi.org/10.1073/pnas.0710608105

    Article  PubMed  PubMed Central  Google Scholar 

  43. Barraud-Lange V, Chalas Boissonnas C, Serres C, Auer J, Schmitt A, Lefèvre B, Wolf JP, Ziyyat A (2012) Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of Cd9-deleted oocytes. Reprod Camb Engl 144:53–66. https://doi.org/10.1530/REP-12-0040

    Article  CAS  Google Scholar 

  44. Miller BJ, Georges-Labouesse E, Primakoff P, Myles DG (2000) Normal fertilization occurs with eggs lacking the integrin α6β1 and is Cd9-dependent. J Cell Biol 149:1289–1296. https://doi.org/10.1083/jcb.149.6.1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Takahashi Y, Bigler D, Ito Y, White JM (2001) Sequence-specific interaction between the disintegrin domain of mouse ADAM 3 and murine eggs: role of beta1 integrin-associated proteins CD9, CD81, and CD98. Mol Biol Cell 12:809–820. https://doi.org/10.1091/mbc.12.4.809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Evans JP, Schultz RM, Kopf GS (1997) Characterization of the binding of recombinant mouse sperm fertilin α subunit to mouse eggs: evidence for function as a cell adhesion molecule in sperm–egg binding. Dev Biol 187:94–106. https://doi.org/10.1006/dbio.1997.8612

    Article  CAS  PubMed  Google Scholar 

  47. Evans JP, Kopf GS, Schultz RM (1997) Characterization of the binding of recombinant mouse sperm fertilin β subunit to mouse rggs: evidence for adhesive activity via an egg β1 integrin-mediated interaction. Dev Biol 187:79–93. https://doi.org/10.1006/dbio.1997.8611

    Article  CAS  PubMed  Google Scholar 

  48. Yamagata K, Nakanishi T, Ikawa M, Yamaguchi R, Moss SB, Okabe M et al (2002) Sperm from the calmegin-deficient mouse have normal abilities for binding and fusion to the egg plasma membrane. Dev Biol 250:348–357. https://doi.org/10.1006/dbio.2002.0803

    Article  CAS  PubMed  Google Scholar 

  49. Stein KK, Primakoff P, Myles D (2004) Sperm-egg fusion: events at the plasma membrane. J Cell Sci 117:6269–6274. https://doi.org/10.1242/jcs.01598

    Article  CAS  PubMed  Google Scholar 

  50. Jégou A, Ziyyat A, Barraud-Lange V, Perez E, Wolf JP, Pincet F, Gourier Ch (2011) CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. Proc Natl Acad Sci 108:10946–10951. https://doi.org/10.1073/pnas.1017400108

    Article  PubMed  PubMed Central  Google Scholar 

  51. Chalbi M, Barraud-Lange V, Ravaux B, Howan K, Rodriguez N, Soule P, Ndzoudi A, Boucheix C, Rubinstein E, Wolf JP, Ziyyat A, Perez E, Pincet F, Gourier Ch (2014) Binding of sperm protein Izumo1 and its egg receptor Juno drives CD9 accumulation in the intercellular contact area prior to fusion during mammalian fertilization. Development 141:3732–3739. https://doi.org/10.1242/dev.111534

    Article  CAS  PubMed  Google Scholar 

  52. Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234–238. https://doi.org/10.1038/nature03362

    Article  CAS  PubMed  Google Scholar 

  53. Ravaux B, Favier S, Perez E, Gourier C (2018) Egg CD9 protein tides correlated with sperm oscillations tune the gamete fusion ability in mammal. J Mol Cell Biol 10:494–502. https://doi.org/10.1093/jmcb/mjy005

    Article  CAS  PubMed  Google Scholar 

  54. Glazar AI, Evans JP (2009) Immunoglobulin superfamily member IgSF8 (EWI-2) and CD9 in fertilisation: Evidence of distinct functions for CD9 and a CD9-associated protein in mammalian sperm-egg interaction. Reprod Fertil Dev 21:293–303. https://doi.org/10.1071/rd08158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Sala-Valdés M, Ailane N, Greco C, Rubinstein E, Boucheix C (2012) Targeting tetraspanins in cancer. Expert Opin Ther Targets 16:985–997. https://doi.org/10.1517/14728222.2012.712688

    Article  CAS  PubMed  Google Scholar 

  56. Umeda R, Satouh Y, Takemoto M, Nakadu-Nakura Y, Liu K, Yokoyama T, Shirouzu M, Iwata S, Nomura N, Sato K, Ikawa M, Nishizawa T, Nureki O (2020) Structural insights into tetraspanin CD9 function. Nat Commun 11:1–11. https://doi.org/10.1038/s41467-020-15459-7

    Article  CAS  Google Scholar 

  57. Mellisho EA, Velásquez AE, Nuñez MJ, Cabezas JG, Cueto JA, Fader C, Castro FO, Rodríguez-Álvarezet L (2017) Identification and characteristics of extracellular vesicles from bovine blastocysts produced in vitro. PLoS ONE 12:e0178306. https://doi.org/10.1371/journal.pone.0178306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Marin D, Scott RT (2018) Extracellular vesicles: a promising tool for assessment of embryonic competence. Curr Opin Obstet Gynecol 30:171–178. https://doi.org/10.1097/GCO.0000000000000458

    Article  PubMed  Google Scholar 

  59. Kanatsu-Shinohara M, Toyokuni S, Shinohara T (2004) CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 70:70–75. https://doi.org/10.1095/biolreprod.103.020867

    Article  CAS  PubMed  Google Scholar 

  60. Kierszenbaum AL, Rosselot C, Rivkin E, Tres LL (2006) Role of integrins, tetraspanins, and ADAM proteins during the development of apoptotic bodies by spermatogenic cells. Mol Reprod Dev 73:906–917. https://doi.org/10.1002/mrd.20470

    Article  CAS  PubMed  Google Scholar 

  61. Ito C, Yamatoya K, Yoshida K, Maekawa M, Miyado K, Toshimori K (2010) Tetraspanin family protein CD9 in the mouse sperm: unique localization, appearance, behavior and fate during fertilization. Cell Tissue Res 340:583–594. https://doi.org/10.1007/s00441-010-0967-7

    Article  CAS  PubMed  Google Scholar 

  62. Frolikova M, Manaskova-Postlerova P, Cerny J, Jankovicova J, Simonik O, Pohlova A, Secova P, Antalikova J, Dvorakova-Hortova K (2018) CD9 and CD81 interactions and their structural modelling in sperm prior to fertilization. Int J Mol Sci 19:1236. https://doi.org/10.3390/ijms19041236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Antalíková J, Jankovičová J, Simon M, Cupperová P, Michalková K, Horovská Ľ (2015) Localization of CD9 molecule on bull spermatozoa: its involvement in the sperm–egg interaction. Reprod Domest Anim 50:423–430. https://doi.org/10.1111/rda.12508

    Article  CAS  PubMed  Google Scholar 

  64. Charrin S, Naour FL, Oualid M, Billard M, Faure G, Hanash SM, Boucheix C, Rubinstein E (2001) The major CD9 and CD81 molecular partner identification and characterization of complexes. J Biol Chem 276:14329–14337. https://doi.org/10.1074/jbc.M011297200

    Article  CAS  PubMed  Google Scholar 

  65. Sala-Valdés M, Ursa Á, Charrin S, Rubinstein E, Hemler ME, Sánchez-Madrid F, Yáñez-Mó M (2006) EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with Ezrin-Radixin-Moesin proteins. J Biol Chem 281:19665–19675. https://doi.org/10.1074/jbc.M602116200

    Article  CAS  PubMed  Google Scholar 

  66. Wang L, Chen W, Zhao C, Huo R, Guo XJ, Lin M, Huang XY, Mao YD, Zuo-Min Zhou ZM, Sha JH (2010) The role of ezrin-associated protein network in human sperm capacitation. Asian J Androl 12:667–676. https://doi.org/10.1038/aja.2010.79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Salvolini E, Buldreghini E, Lucarini G, Vignini A, Lenzi A, Di Primo R, Balercia G (2013) Involvement of sperm plasma membrane and cytoskeletal proteins in human male infertility. Fertil Steril 99:697–704. https://doi.org/10.1016/j.fertnstert.2012.10.042

    Article  CAS  PubMed  Google Scholar 

  68. The UniProt Consortium (2019) UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res 47:D506–D515. https://doi.org/10.1093/nar/gky1049

    Article  CAS  Google Scholar 

  69. Rubinstein E, Ziyyat A, Prenant M, Wrobel E, Wolf JF, Levy S, Le Naour F, Boucheix C (2006) Reduced fertility of female mice lacking CD81. Dev Biol 290:351–358. https://doi.org/10.1016/j.ydbio.2005.11.031

    Article  CAS  PubMed  Google Scholar 

  70. Ohnami N, Nakamura A, Miyado M, Sato M, Kawano N, Yoshida K, Harada Y, Takezawa Y, Kanai S, Ono Ch, Takahashi Y, Kimura K, Shida T, Miyado K, Umezawa A (2012) CD81 and CD9 work independently as extracellular components upon fusion of sperm and oocyte. Biol Open 1:640–647. https://doi.org/10.1242/bio.20121420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Jankovicova J, Frolikova M, Sebkova N, Simon M, Cupperova P, Lipcseyova D, Michalkova K, Horovska L, Sedlacek R, Stopka P, Dvorakova-Hortova AJK (2016) Characterization of tetraspanin protein CD81 in mouse spermatozoa and bovine gametes. Reproduction 152:785–793. https://doi.org/10.1530/REP-16-0304

    Article  CAS  PubMed  Google Scholar 

  72. Zimmerman B, Kelly B, McMillan BJ, Seegar TCM, Dror RO, Kruse AC, Blacklow SC (2016) Crystal structure of a full-length human tetraspanin reveals a cholesterol-binding pocket. Cell 167:1041–1051.e11. https://doi.org/10.1016/j.cell.2016.09.056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Gupta S, Primakoff P, Myles DG (2009) Can the presence of wild-type oocytes during insemination rescue the fusion defect of CD9 null oocytes? Mol Reprod Dev 76:602. https://doi.org/10.1002/mrd.21040

    Article  CAS  PubMed  Google Scholar 

  74. Wright MD, Geary SM, Fitter S, Moseley GW, Lau LM, Sheng KCh, Apostolopoulos V, Stanley EG, Jackson DE, Ashman LK (2004) Characterization of mice lacking the tetraspanin superfamily member CD151. Mol Cell Biol 24:5978–5988. https://doi.org/10.1128/MCB.24.13.5978-5988.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Talbot P, Dandekar P (2003) Perivitelline space: does it play a role in blocking polyspermy in mammals? Microsc Res Tech 61:349–357. https://doi.org/10.1002/jemt.10348

    Article  CAS  PubMed  Google Scholar 

  76. Campbell S, Swann HR, Aplin JD, Seif MW, Kimber SJ, Elstein M (1995) CD44 is expressed throughout pre-implantation human embryo development. Hum Reprod Oxf Engl 10:425–430. https://doi.org/10.1093/oxfordjournals.humrep.a135955

    Article  CAS  Google Scholar 

  77. Jones PH, Bishop LA, Watt FM (1996) Functional significance of CD9 association with beta 1 integrins in human epidermal keratinocytes. Cell Adhes Commun 4:297–305. https://doi.org/10.3109/15419069609010773

    Article  CAS  PubMed  Google Scholar 

  78. Berditchevski F, Gilbert E, Griffiths MR, Fitter S, Ashman L, Jenner SJ (2001) Analysis of the CD151 α3β1 integrin and CD151 tetraspanin interactions by mutagenesis. J Biol Chem 276:41165–41174. https://doi.org/10.1074/jbc.M104041200

    Article  CAS  PubMed  Google Scholar 

  79. Yauch RL, Berditchevski F, Harler MB, Reichner J, Hemler ME (1998) Highly stoichiometric, stable, and specific association of integrin α3β1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol Biol Cell 9:2751–2765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Yauch RL, Kazarov AR, Desai B, Lee RT, Hemler ME (2000) Direct extracellular contact between integrin α3β1 and TM4SF protein CD151. J Biol Chem 275:9230–9238. https://doi.org/10.1074/jbc.275.13.9230

    Article  CAS  PubMed  Google Scholar 

  81. Serru V, Le Naour F, Billard M, Azorsa DO, Lanza F, Boucheix C, Rubinstein E (1999) Selective tetraspan-integrin complexes (CD81/alpha4beta1, CD151/alpha3beta1, CD151/alpha6beta1) under conditions disrupting tetraspan interactions. Biochem J 340:103–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Stipp CS, Kolesnikova TV, Hemler ME (2003) EWI-2 regulates α3β1 integrin–dependent cell functions on laminin-5. J Cell Biol 163:1167–1177. https://doi.org/10.1083/jcb.200309113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Charrin S, Manié S, Billard M, Ashman L, Gerlier D, Boucheix C, Rubinstein E (2003) Multiple levels of interactions within the tetraspanin web. Biochem Biophys Res Commun 304:107–112. https://doi.org/10.1016/S0006-291X(03)00545-X

    Article  CAS  PubMed  Google Scholar 

  84. Sabetian S, Shamsir MS, Naser MA (2014) Functional features and protein network of human sperm-egg interaction. Syst Biol Reprod Med 60:329–337. https://doi.org/10.3109/19396368.2014.955896

    Article  CAS  PubMed  Google Scholar 

  85. Frolikova M, Valaskova E, Cerny J, Lumeau A, Sebkova N, Palenikova V, Sanchez-Hernandez N, Pohlova A, Manaskova-Postlerova P, Dvorakova-Hortova K (2019) Addressing the compartmentalization of specific integrin heterodimers in mouse sperm. Int J Mol Sci 20:1004. https://doi.org/10.3390/ijms20051004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Jankovicova J, Frolikova M, Palenikova V, Valaskova E, Cerny J, Secova P, Bartokova M, Horovska L, Manaskova-Postlerova P, Antalikovaet J, Komrskova K (2020) Expression and distribution of CD151 as a partner of alpha6 integrin in male germ cells. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-61334-2

    Article  CAS  Google Scholar 

  87. Kierszenbaum AL, Rivkin E, Tres LL (2007) Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 65:33–43

    CAS  PubMed  Google Scholar 

  88. Pols MS, Klumperman J (2009) Trafficking and function of the tetraspanin CD63. Exp Cell Res 315:1584–1592. https://doi.org/10.1016/j.yexcr.2008.09.020

    Article  CAS  PubMed  Google Scholar 

  89. Latysheva N, Muratov G, Rajesh S, Padgett M, Hotchin NA, Overduin M, Berditchevski F (2006) Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol Cell Biol 26:7707–7718. https://doi.org/10.1128/MCB.00849-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Pan Y, Brown C, Wang X, Geisert EE (2007) The developmental regulation of CD81 in the rat retina. Mol Vis 13:181–189

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Lee H-J, Zheng JJ (2010) PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun Signal 8:8. https://doi.org/10.1186/1478-811X-8-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Schröder J, Lüllmann-Rauch R, Himmerkus N, Pleines I, Nieswandt B, Orinska Z, Koch-Nolte F, Schröder B, Bleich M, Saftig P (2009) Deficiency of the tetraspanin CD63 associated with kidney pathology but normal lysosomal function. Mol Cell Biol 29:1083–1094. https://doi.org/10.1128/MCB.01163-08

    Article  CAS  PubMed  Google Scholar 

  93. Yoshida K, Kawano N, Harada Y, Miyado K (2014) Role of CD9 in sperm–egg fusion and virus-induced cell fusion in mammals. In: Sawada H, Inoue N, Iwano M (eds) Sexual reproduction in animals and plants. Springer, Tokyo, pp 383–391

    Chapter  Google Scholar 

  94. Rana S, Yue S, Stadel D, Zöller M (2012) Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol 44:1574–1584. https://doi.org/10.1016/j.biocel.2012.06.018

    Article  CAS  PubMed  Google Scholar 

  95. Sullivan R, Saez F (2013) Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction 146:R21–R35. https://doi.org/10.1530/REP-13-0058

    Article  CAS  PubMed  Google Scholar 

  96. Du J, Shen J, Wang Y, Pan C, Pang W, Diao H, Dong W (2016) Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane. Oncotarget 7:58832–58847. https://doi.org/10.18632/oncotarget.11315

    Article  PubMed  PubMed Central  Google Scholar 

  97. Alvarez-Rodriguez M, Ljunggren SA, Karlsson H, Rodriguez-Martinez H (2019) Exosomes in specific fractions of the boar ejaculate contain CD44: a marker for epididymosomes? Theriogenology 140:143–152. https://doi.org/10.1016/j.theriogenology.2019.08.023

    Article  CAS  PubMed  Google Scholar 

  98. Barranco I, Padilla L, Parrilla I, Álvarez-Barrientos A, Pérez-Patiño C, Peña FJ, Martínez EA, Rodriguez-Martínez H, Jordi Rocaet J (2019) Extracellular vesicles isolated from porcine seminal plasma exhibit different tetraspanin expression profiles. Sci Rep. https://doi.org/10.1038/s41598-019-48095-3

    Article  PubMed  PubMed Central  Google Scholar 

  99. Pagano N, Kosior MA, Gasparrini B, Longobardi V, De Canditiis C, Albero G, Deregibus MC, Bosi G, Idda A, Consiglioet AL (2020) 148 Bull spermatozoa uptake of extracellular vesicles from bovine seminal plasma. Reprod Fertil Dev 32:200–200. https://doi.org/10.1071/RDv32n2Ab148

    Article  Google Scholar 

  100. da Silveira JC, Veeramachaneni DNR, Winger QA, Carnevale EM, Bouma GJ (2012) Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol Reprod 86:71. https://doi.org/10.1095/biolreprod.111.093252

    Article  CAS  PubMed  Google Scholar 

  101. Sohel MH, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft Ch, Rings F, Uddin MJ, Spencere TE, Schellander K, Tesfaye D (2013) Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS ONE 8:e78505. https://doi.org/10.1371/journal.pone.0078505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Santonocito M, Vento M, Guglielmino MR, Battaglia R, Wahlgren J, Ragusa M, Barbagallo D, Borzi P, Rizzari S, Maugeri M, Scollo P, Tatone C, Valadi H, Purrello M, Di Pietro C (2014) Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil Steril 102:1751–1761.e1. https://doi.org/10.1016/j.fertnstert.2014.08.005

    Article  CAS  PubMed  Google Scholar 

  103. Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, Salamonsen LA (2013) Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS ONE 8:e58502. https://doi.org/10.1371/journal.pone.0058502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE (2014) Extracellular vesicles in luminal fluid of the ovine uterus. PLoS ONE 9:e90913. https://doi.org/10.1371/journal.pone.0090913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Battaglia R, Palini S, Vento ME, La Ferlita A, Lo Faro MJ, Caroppo E, Borzì P, Falzone L, Barbagallo D, Ragusa M, Scalia M, D’Amato G, Scollo P, Musumeci P, Purrello M, Gravotta E, Di Pietro C (2019) Identification of extracellular vesicles and characterization of miRNA expression profiles in human blastocoel fluid. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-018-36452-7

    Article  CAS  Google Scholar 

  106. Tarique I, Haseeb A, Bai X, Li W, Yang P, Huang Y, Yang S, Xu M, Zhang Y, Vistro WA, Fazlani SA, Chen Q (2019) Cellular evidence of CD63-enriched exosomes and multivesicular bodies within the seminiferous tubule during the spermatogenesis of turtles. Microsc Microanal 26:148–156. https://doi.org/10.1017/S1431927619015149

    Article  CAS  Google Scholar 

  107. Tarique I, Liu Y, Bai X, Haseeb A, Yang P, Huang Y, Qu W, Wu R, Vistro WA, Chen Q (2019) Characterization of extracellular vesicles from cilia and epithelial cells of ductuli efferentes in a turtle (Pelodiscus sinensis). Animals 9:888. https://doi.org/10.3390/ani9110888

    Article  PubMed  PubMed Central  Google Scholar 

  108. Huang A, Isobe N, Yoshimura Y (2017) Changes in localization and density of CD63-positive exosome-like substances in the hen oviduct with artificial insemination and their effect on sperm viability. Theriogenology 101:135–143. https://doi.org/10.1016/j.theriogenology.2017.06.028

    Article  CAS  PubMed  Google Scholar 

  109. Robertson SA, Sharkey DJ (2016) Seminal fluid and fertility in women. Fertil Steril 106:511–519. https://doi.org/10.1016/j.fertnstert.2016.07.1101

    Article  PubMed  Google Scholar 

  110. Caballero JN, Frenette G, Belleannée C, Sullivan R (2013) CD9-positive microvesicles mediate the transfer of molecules to bovine spermatozoa during epididymal maturation. PLoS ONE 8:e65364. https://doi.org/10.1371/journal.pone.0065364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Jankovičová J, Bartóková M, Horovská Ľ et al (2019) Poster: detection of cluster of differentiation molecule 63 in bull sperm. Reprod Dom Anim 54:110–111

    Google Scholar 

  112. Liu WM, Cao YJ, Yang YJ, Hu Z, Duan EK (2006) Tetraspanin CD9 regulates invasion during mouse embryo implantation. J Mol Endocrinol 36:121–130. https://doi.org/10.1677/jme.1.01910

    Article  CAS  PubMed  Google Scholar 

  113. Yubero N, Jiménez-Marín Á, Lucena C, Barbancho M, Garrido JJ (2010) Immunohistochemical distribution of the tetraspanin CD9 in normal porcine tissues. Mol Biol Rep 38:1021–1028. https://doi.org/10.1007/s11033-010-0198-8

    Article  CAS  PubMed  Google Scholar 

  114. Saadeldin IM, Kim SJ, Choi YB, Lee BC (2014) Improvement of cloned embryos development by co-culturing with parthenotes: a possible role of exosomes/microvesicles for embryos paracrine communication. Cell Reprogr 16:223–234. https://doi.org/10.1089/cell.2014.0003

    Article  CAS  Google Scholar 

  115. Zhou GB, Zeng Y, Meng QG, Liu Y, Dai YP, Zhu SE, Bunch TD, Hou YP (2013) Decreased expression of CD9 in bovine oocytes after cryopreservation and the relationship to fertilization capacity. Mol Reprod Dev 80:451–459. https://doi.org/10.1002/mrd.22181

    Article  CAS  PubMed  Google Scholar 

  116. Qu P, Qing S, Liu R, Qin H, Wang W, Qiao F, Ge H, Liu J, Zhang Y, Cui W, Wang Y (2017) Effects of embryo-derived exosomes on the development of bovine cloned embryos. PLoS ONE 12:e0174535. https://doi.org/10.1371/journal.pone.0174535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Tanigawa M, Miyamoto K, Kobayashi S, Sato M, Akutsu H, Okabe M, Mekada E, Sakakibara K, Miyado M, Umezawa A, Miyado K (2008) Possible involvement of CD81 in acrosome reaction of sperm in mice. Mol Reprod Dev 75:150–155. https://doi.org/10.1002/mrd.20709

    Article  CAS  PubMed  Google Scholar 

  118. Tres LL, Kierszenbaum AL (2005) The ADAM-integrin-tetraspanin complex in fetal and postnatal testicular cords. Birth Defects Res Part C Embryo Today Rev 75:130–141. https://doi.org/10.1002/bdrc.20041

    Article  CAS  Google Scholar 

  119. Kaewmala K, Uddin MJ, Cinar MU, Große-Brinkhaus Ch, Jonas E, Tesfaye D, Phatsara Ch, Tholen E, Looft Ch, Schellander K (2011) Association study and expression analysis of CD9 as candidate gene for boar sperm quality and fertility traits. Anim Reprod Sci 125:170–179. https://doi.org/10.1016/j.anireprosci.2011.02.017

    Article  CAS  PubMed  Google Scholar 

  120. Custer MC, Risinger JI, Hoover S, Simpson RM, Patterson T, Barrett JC (2006) Characterization of an antibody that can detect the Kai1/CD82 murine metastasis suppressor. Prostate 66:567–577. https://doi.org/10.1002/pros.20386

    Article  CAS  PubMed  Google Scholar 

  121. Risinger JI, Custer M, Feigenbaum L, Simpson RM, Hoover SB, Webster JD, Chandramouli GVR, Tessarollo L, Barrett JC (2014) Normal viability of Kai1/Cd82 deficient mice. Mol Carcinog 53:610–624. https://doi.org/10.1002/mc.22009

    Article  CAS  PubMed  Google Scholar 

  122. García-Herrero S, Meseguer M, Martínez-Conejero JA, José Remohí J, Pellicer A, Garrido N (2010) The transcriptome of spermatozoa used in homologous intrauterine insemination varies considerably between samples that achieve pregnancy and those that do not. Fertil Steril 94:1360–1373. https://doi.org/10.1016/j.fertnstert.2009.07.1671

    Article  CAS  PubMed  Google Scholar 

  123. Todd SC, Doctor VS, Levy S (1998) Sequences and expression of six new members of the tetraspanin/TM4SF family. Biochim Biophys Acta 1399:101–104. https://doi.org/10.1016/s0167-4781(98)00087-6

    Article  CAS  PubMed  Google Scholar 

  124. Bansal SK, Gupta N, Sankhwar SN, Rajender S (2015) Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis. PLoS ONE 10:e0127007. https://doi.org/10.1371/journal.pone.0127007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S (2006) The human cumulus–oocyte complex gene-expression profile. Hum Reprod 21:1705–1719. https://doi.org/10.1093/humrep/del065

    Article  CAS  PubMed  Google Scholar 

  126. Liao Y, Chang HC, Liang FX, Chung PJ, Wei Y, Nguyen TP, Zhou G, Talebian S, Lewis C, Krey LC, Fang-Ming Deng FM, Wong TW, Chicote JU, Grifo JA, Keefe DL, Shapiro E, Lepor H, Wu XR, DeSalle R, Garcia-España A, Kim SY, Sun TT (2018) Uroplakins play conserved roles in egg fertilization and acquired additional urothelial functions during mammalian divergence. Mol Biol Cell 29:3128–3143. https://doi.org/10.1091/mbc.E18-08-0496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Garcia-España A, Chung P-J, Zhao X, Lee A, Pellicer A, Yu J, Sun TT, DeSalle R (2006) Origin of the tetraspanin uroplakins and their co-evolution with associated proteins: implications for uroplakin structure and function. Mol Phylogenet Evol 41:355–367. https://doi.org/10.1016/j.ympev.2006.04.023

    Article  CAS  PubMed  Google Scholar 

  128. Schuster A, Tang C, Xie Y, Ortogero N, Yuan S, Yan W (2016) SpermBase: a database for sperm-borne RNA contents. Biol Reprod 95:1–12. https://doi.org/10.1095/biolreprod.116.142190

    Article  CAS  Google Scholar 

  129. Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma Ch, Kazarov AR, Andzelm SJL, Brown M, Hemler ME (2008) CD151 accelerates breast cancer by regulating α6 integrin function, signaling, and molecular organization. Cancer Res 68:3204–3213. https://doi.org/10.1158/0008-5472.CAN-07-2949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Sadej R, Romanska H, Baldwin G, Gkirtzimanaki K, Novitskaya V, Filer AD, Krcova Z, Kusinska R, Ehrmann J, Buckley ChD, Kordek R, Potemski P, Eliopoulos AG, Lalani EN, Berditchevski F (2009) CD151 regulates tumorigenesis by modulating the communication between tumor cells and endothelium. Mol Cancer Res 7:787–798. https://doi.org/10.1158/1541-7786.MCR-08-0574

    Article  CAS  PubMed  Google Scholar 

  131. Scheffer KD, Berditchevski F, Florin L (2014) The tetraspanin CD151 in papillomavirus infection. Viruses 6:893–908. https://doi.org/10.3390/v6020893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Ang J, Lijovic M, Ashman LK, Ang J, Lijovic M, Ashman LK, Kan K, Frauman AG (2004) CD151 protein expression predicts the clinical outcome of low-grade primary prostate cancer better than histologic grading: a new prognostic indicator? Cancer Epidemiol Prev Biomark 13:1717–1721

    Article  CAS  Google Scholar 

  133. Wang JC, Bégin LR, Bérubé NG, Chevalier S, Aprikian AG, Gourdeau H, Chevrette M (2007) Down-regulation of CD9 expression during prostate carcinoma progression is associated with CD9 mRNA modifications. Clin Cancer Res 13:2354–2361. https://doi.org/10.1158/1078-0432.CCR-06-1692

    Article  CAS  PubMed  Google Scholar 

  134. Brzozowski JS, Bond DR, Jankowski H et al (2018) Extracellular vesicles with altered tetraspanin CD9 and CD151 levels confer increased prostate cell motility and invasion. Sci Rep 8:1–13. https://doi.org/10.1038/s41598-018-27180-z

    Article  CAS  Google Scholar 

  135. Logozzi M, Angelini DF, Iessi E, Mizzoni D, Raimo RD, Federici C, Lugini L, Borsellino G, Gentilucci A, Pierella F, Marzio V, Sciarra A, Battistini L, Fais S (2017) Increased PSA expression on prostate cancer exosomes in in vitro condition and in cancer patients. Cancer Lett 403:318–329. https://doi.org/10.1016/j.canlet.2017.06.036

    Article  CAS  PubMed  Google Scholar 

  136. Padda RS, Deng FK, Brett SI, Biggs CN, Durfee PN, Brinker ChJ, Williams KC, Leong HS (2019) Nanoscale flow cytometry to distinguish subpopulations of prostate extracellular vesicles in patient plasma. Prostate 79:592–603. https://doi.org/10.1002/pros.23764

    Article  CAS  PubMed  Google Scholar 

  137. Goyal SM (1993) Porcine reproductive and respiratory syndrome. J Vet Diagn Investig Off Publ Am Assoc Vet Lab Diagn Inc 5:656–664. https://doi.org/10.1177/104063879300500435

    Article  CAS  Google Scholar 

  138. de Jong M, Cromvijk W, Cromvijk P (1991) The new pig dis-ease-epidemiology and production losses in the Netherlands. Comm Eur Commun 1:9–19

    Google Scholar 

  139. Shanmukhappa K, Kim JK, Kapil S (2007) Role of CD151, a tetraspanin, in porcine reproductive and respiratory syndrome virus infection. Virol J 4:62. https://doi.org/10.1186/1743-422X-4-62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Kreutz LC, Ackermann MR (1996) Porcine reproductive and respiratory syndrome virus enters cells through a low pH-dependent endocytic pathway. Virus Res 42:137–147. https://doi.org/10.1016/0168-1702(96)01313-5

    Article  CAS  PubMed  Google Scholar 

  141. Sincock PM, Fitter S, Parton RG, Berndt MC, Gamble JR, Ashman LK (1999) PETA-3/CD151, a member of the transmembrane 4 superfamily, is localised to the plasma membrane and endocytic system of endothelial cells, associates with multiple integrins and modulates cell function. J Cell Sci 112:833–844

    Article  CAS  PubMed  Google Scholar 

  142. Fast LA, Lieber D, Lang T, Florin L (2017) Tetraspanins in infections by human cytomegalo- and papillomaviruses. Biochem Soc Trans 45:489–497. https://doi.org/10.1042/BST20160295

    Article  CAS  PubMed  Google Scholar 

  143. Gomes VA, de Moraes BC, Rosa-e-Silva JC, de Paz CCP, Ferriani RA, Meola J (2018) The apoptotic, angiogenic and cell proliferation genes CD63, S100A6 e GNB2L1 are altered in patients with endometriosis. Rev Bras Ginecol E Obstetrícia RBGO Gynecol Obstet 40:606–613. https://doi.org/10.1055/s-0038-1673364

    Article  Google Scholar 

  144. Menon R, Dixon CL, Sheller-Miller S, Fortunato SJ, Saade GR, Palma C, Lai A, Guanzon D, Salomon C (2019) Quantitative proteomics by SWATH-MS of maternal plasma exosomes determine pathways associated with term and preterm birth. Endocrinology 160:639–650. https://doi.org/10.1210/en.2018-00820

    Article  PubMed  PubMed Central  Google Scholar 

  145. Zhao S, Qi W, Zheng J, Tian Y, Qi X, Kong D, Zhang J, Huang X (2020) Exosomes derived from adipose mesenchymal stem cells restore functional endometrium in a rat model of intrauterine adhesions. Reprod Sci. https://doi.org/10.1007/s43032-019-00112-6

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Scientific Grant Agency of the Ministry of Education, Science, Research, and Sport of the Slovak Republic and the Slovak Academy of Sciences (VEGA-2/0027/20), by the Slovak Research and Development Agency (APVV-15-0196), bilateral project SAS-CAS (18-17); by the Internal Grant Agency of Czech University of Life Sciences in Prague (SV18-08-21230); by the CellFit COST Action CA16119, Ministry of Education, Youth and Sports, Czech Republic INTER-COST LTC 18059; by the Grant Agency of the Czech Republic No. GA-18-11275S; by the project BIOCEV (CZ.1.05/1.1.00/02.0109) from the ERDF; and by the Institutional support of the Institute of Biotechnology RVO: 86652036.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jana Antalíková.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Edited by Charlotte M de Winde.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Special Issue on Tetraspanins in Infection and Immunity.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jankovičová, J., Neuerová, Z., Sečová, P. et al. Tetraspanins in mammalian reproduction: spermatozoa, oocytes and embryos. Med Microbiol Immunol 209, 407–425 (2020). https://doi.org/10.1007/s00430-020-00676-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00430-020-00676-0

Keywords

Navigation