DOI QR코드

DOI QR Code

ADAM7 Is Associated with Epididymosomes and Integrated into Sperm Plasma Membrane

  • Oh, Jeong Su (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Han, Cecil (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Cho, Chunghee (Department of Life Science, Gwangju Institute of Science and Technology)
  • Received : 2009.07.06
  • Accepted : 2009.09.01
  • Published : 2009.11.30

Abstract

During epididymal transit, mammalian sperm acquire selected proteins secreted by the epididymis. We previously showed that a disintegrin and metalloprotease (ADAM) 7 is expressed specifically in the epididymis and transferred to the sperm surface during epididymal transit. Here, we show that mouse ADAM7 secreted to the epididymal lumen is associated with membranous vesicles known as epididymosomes. Furthermore, we found that ADAM7 can be transferred directly from epididymal vesicles to sperm and that it is an integral plasma membrane protein in sperm. Thus, our study provides new information regarding the unique mode of secretion and interaction of ADAM7 during the epididymis-to-sperm transfer process.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation, Korea Research Foundation, Gwangju Institute of Science and Technology

References

  1. Arienti, G., Carlini, E., De Cosmo, A.M., Di Profio, P., and Palmerini, C.A. (1998). Prostasome-like particles in stallion semen. Biol. Reprod. 59, 309-313 https://doi.org/10.1095/biolreprod59.2.309
  2. Aumuller, G., Renneberg, H., Schiemann, P.J., Wilhelm, B., Seitz, J., Konrad, L., and Wennemuth, G. (1997). The role of apocrine released proteins in the post-testicular regulation of human sperm function. Adv. Exp. Med. Biol. 424, 193-219
  3. Aumuller, G., Wilhelm, B., and Seitz, J. (1999). Apocrine secretion--fact or artifact? Ann. Anat. 181, 437-446 https://doi.org/10.1016/S0940-9602(99)80020-X
  4. Brown, D.A., and London, E. (2000). Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224 https://doi.org/10.1074/jbc.R000005200
  5. Cho, C., Bunch, D.O., Faure, J.E., Goulding, E.H., Eddy, E.M., Primakoff, P., and Myles, D.G. (1998). Fertilization defects in sperm from mice lacking fertilin beta. Science 281, 1857-1859 https://doi.org/10.1126/science.281.5384.1857
  6. Cho, C. (2005). Mammalian ADAMs with testis-specific or -predominant expression. In The ADAM Family of Proteases, Vol. 4 in the Proteases in Biology and Disease series, N.M. Hoopers, and U. Lendekel, eds., (Netherlands: Springer), pp. 239-259
  7. Cho, C. (2005). Mammalian ADAMs with testis-specific or -predominant expression. In The ADAM Family of Proteases, Vol. 4 in the Proteases in Biology and Disease series, N.M. Hoopers, and U. Lendekel, eds., (Netherlands: Springer), pp. 239-259
  8. Cooper, T.G. (1998). Interactions between epididymal secretions and spermatozoa. J. Reprod. Fertil. Suppl. 53, 119-136
  9. Cornwall, G.A., and Hsia, N. (1997). ADAM7, a member of the ADAM (a disintegrin and metalloprotease) gene family is specifically expressed in the mouse anterior pituitary and epididymis. Endocrinology 138, 4262-4272 https://doi.org/10.1210/en.138.10.4262
  10. Edidin, M. (2003). The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32, 257-283 https://doi.org/10.1146/annurev.biophys.32.110601.142439
  11. Edwards, D.R., Handsley, M.M., and Pennington, C.J. (2008). The ADAM metalloproteinases. Mol. Aspects Med. 29, 258-289 https://doi.org/10.1016/j.mam.2008.08.001
  12. Frenette, G., and Sullivan, R. (2001). Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol. Reprod. Dev. 59, 115-121 https://doi.org/10.1002/mrd.1013
  13. Frenette, G., Lessard, C., and Sullivan, R. (2002). Selected proteins of 'prostasome-like particles' from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol. Reprod. 67, 308-313 https://doi.org/10.1095/biolreprod67.1.308
  14. Frenette, G., Lessard, C., Madore, E., Fortier, M.A., and Sullivan, R. (2003). Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol. Reprod. 69, 1586-1592 https://doi.org/10.1095/biolreprod.103.019216
  15. Frenette, G., Legare, C., Saez, F., and Sullivan, R. (2005). Macrophage migration inhibitory factor in the human epididymis and semen. Mol. Hum. Reprod. 11, 575-582 https://doi.org/10.1093/molehr/gah197
  16. Frenette, G., Thabet, M., and Sullivan, R. (2006). Polyol pathway in human epididymis and semen. J. Androl. 27, 233-239 https://doi.org/10.2164/jandrol.05108
  17. Frohlich, O., and Young, L.G. (1996). Molecular cloning and characterization of EPI-1, the major protein in chimpanzee (Pan troglodytes) cauda epididymal fluid. Biol. Reprod. 54, 857-864 https://doi.org/10.1095/biolreprod54.4.857
  18. Gatti, J.L., Metayer, S., Belghazi, M., Dacheux, F., and Dacheux, J.L. (2005). Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol. Reprod. 72, 1452-1465 https://doi.org/10.1095/biolreprod.104.036426
  19. Gesase, A.P., and Satoh,Y. (2003). Apocrine secretory mechanism: recent findings and unresolved problems. Histol. Histopathol. 18, 597-608
  20. Hermo, L., and Jacks, D. (2002). Nature’s ingenuity: bypassing the classical secretory route via apocrine secretion. Mol. Reprod. Dev. 63, 394-410 https://doi.org/10.1002/mrd.90023
  21. Jin, E.J., Choi, Y.A., Sonn, J.K., and Kang, S.S. (2007). Suppression of ADAM 10-induced Delta-1 shedding inhibits cell proliferation during the chondro-inhibitory action of TGF-beta3. Mol. Cells 23, 139-147
  22. Kim, T., Oh, J., Woo, J.M., Choi, E., Im, S.H., Yoo, Y.J., Kim, D.H., Nishimura, H., and Cho, C. (2006). Expression and relationship of male reproductive ADAMs in mouse. Biol. Reprod. 74, 744-750 https://doi.org/10.1095/biolreprod.105.048892
  23. Kirchhoff, C., and Hale, G. (1996). Cell-to-cell transfer of glycosylphosphatidylinositol- anchored membrane proteins during sperm maturation. Mol. Hum. Reprod. 2, 177-184 https://doi.org/10.1093/molehr/2.3.177
  24. Kravets, F.G., Lee, J., Singh, B., Trocchia, A., Pentyala, S.N., and Khan, S.A. (2000). Prostasomes: current concepts. Prostate 43, 169-174 https://doi.org/10.1002/(SICI)1097-0045(20000515)43:3<169::AID-PROS2>3.0.CO;2-D
  25. Legare, C., Berube, B., Boue, F., Lefievre, L., Morales, C.R., El-Alfy, M., and Sullivan, R. (1999). Hamster sperm antigen P26h is a phosphatidylinositol-anchored protein. Mol. Reprod. Dev. 52, 225-233 https://doi.org/10.1002/(SICI)1098-2795(199902)52:2<225::AID-MRD14>3.0.CO;2-M
  26. Lin, Y.C., Sun, G.H., Lee, Y.M., Guo, Y.W., and Liu, H.W. (2001). Cloning and characterization of a complementary DNA encoding a human epididymis-associated disintegrin and metalloprotease 7 protein. Biol. Reprod. 65, 944-950 https://doi.org/10.1095/biolreprod65.3.944
  27. Liu, H.W., Lin, Y.C., Chao, C.F., Chang, S.Y., and Sun, G.H. (2000). GP-83 and GP-39, two glycoproteins secreted by human epididymis are conjugated to spermatozoa during maturation. Mol. Hum. Reprod. 6, 422-428 https://doi.org/10.1093/molehr/6.5.422
  28. Llorente, A., de Marco, M.C., and Alonso, M.A. (2004). Caveolin-1 and MAL are located on prostasomes secreted by the prostate cancer PC-3 cell line. J. Cell Sci. 117, 5343-5351 https://doi.org/10.1242/jcs.01420
  29. Nishimura, H., Cho, C., Branciforte, D.R., Myles, D.G., and Primakoff, P. (2001). Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin beta. Dev. Biol. 233, 204-213 https://doi.org/10.1006/dbio.2001.0166
  30. Nishimura, H., Kim, E., Nakanishi, T., and Baba, T. (2004). Possible function of the ADAM1a/ADAM2 Fertilin complex in the appearance of ADAM3 on the sperm surface. J. Biol. Chem. 279, 34957-34962 https://doi.org/10.1074/jbc.M314249200
  31. Oh, J., Woo, J.M., Choi, E., Kim, T., Cho, B.N., Park, Z.Y., Kim, Y.C., Kim, D.H., and Cho, C. (2005). Molecular, biochemical, and cellular characterization of epididymal ADAMs, ADAM7 and ADAM28. Biochem. Biophys. Res. Commun. 331, 1374-1383 https://doi.org/10.1016/j.bbrc.2005.04.067
  32. Perry, A.C., Jones, R., Barker, P.J., and Hall, L. (1992). A mammalian epididymal protein with remarkable sequence similarity to snake venom haemorrhagic peptides. Biochem. J. 286, 671-675 https://doi.org/10.1042/bj2860671
  33. Primakoff, P., and Myles, D.G. (2000). The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet. 16, 83-87 https://doi.org/10.1016/S0168-9525(99)01926-5
  34. Rejraji, H., Vernet, P., and Drevet, J.R. (2002). GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Mol. Reprod. Dev. 63, 96-103 https://doi.org/10.1002/mrd.10136
  35. Rejraji, H., Sion, B., Prensier, G., Carreras, M., Motta, C., Frenoux, J.M., Vericel, E., Grizard, G., Vernet, P., and Drevet, J.R. (2006). Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol. Reprod. 74, 1104-1113 https://doi.org/10.1095/biolreprod.105.049304
  36. Saez, F., Frenette, G., and Sullivan, R. (2003). Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J. Androl. 24, 149-154 https://doi.org/10.1002/j.1939-4640.2003.tb02653.x
  37. Seals, D.F., and Courtneidge, S.A. (2003). The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17, 7-30 https://doi.org/10.1101/gad.1039703
  38. Sullivan, R., Saez, F., Girouard, J., and Frenette, G. (2005). Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol. Dis. 35, 1-10 https://doi.org/10.1016/j.bcmd.2005.03.005
  39. Sun, G.H., Lin, Y.C., Guo, Y.W., Chang, S.Y., and Liu, H.W. (2000). Purification of GP-83, a glycoprotein secreted by the human epididymis and conjugated to mature spermatozoa. Mol. Hum. Reprod. 6, 429-434 https://doi.org/10.1093/molehr/6.5.429
  40. Udenfriend, S., and Kodukula, K. (1995) How glycosylphosphatidylinositol- anchored membrane proteins are made. Annu. Rev. Biochem. 64, 563-591 https://doi.org/10.1146/annurev.bi.64.070195.003023
  41. Weininger, R.B., Fisher, S., Rifkin, J., and Bedford, J.M. (1982). Experimental studies on the passage of specific IgG to the lumen of the rabbit epididymis. J. Reprod. Fertil. 66, 251-258 https://doi.org/10.1530/jrf.0.0660251

Cited by

  1. Egg hull formation in Callochiton dentatus (Mollusca, Polyplacophora): the contribution of microapocrine secretion : Egg hull formation in Callochiton vol.129, pp.4, 2009, https://doi.org/10.1111/j.1744-7410.2010.00208.x
  2. Extracellular Domain of V-Set and Immunoglobulin Domain Containing 1 (VSIG1) Interacts with Sertoli Cell Membrane Protein, while Its PDZ-Binding Motif Forms a Complex with ZO-1 vol.30, pp.5, 2009, https://doi.org/10.1007/s10059-010-0138-4
  3. Post Testicular Sperm Maturational Changes in the Bull: Important Role of the Epididymosomes and Prostasomes vol.2011, pp.None, 2009, https://doi.org/10.4061/2011/757194
  4. The emerging role of matrix metalloproteases of the ADAM family in male germ cell apoptosis vol.1, pp.3, 2009, https://doi.org/10.4161/spmg.1.3.17894
  5. On the ancestral recruitment of metalloproteinases into the venom of snakes vol.60, pp.4, 2012, https://doi.org/10.1016/j.toxicon.2012.02.006
  6. Testicular and epididymal ADAMs: expression and function during fertilization vol.9, pp.10, 2009, https://doi.org/10.1038/nrurol.2012.167
  7. Cell-Free Seminal mRNA and MicroRNA Exist in Different Forms vol.7, pp.4, 2009, https://doi.org/10.1371/journal.pone.0034566
  8. Expression and function of the testis-predominant protein LYAR in mice vol.35, pp.1, 2009, https://doi.org/10.1007/s10059-013-2271-3
  9. The function of chaperone proteins in the assemblage of protein complexes involved in gamete adhesion and fusion processes. vol.145, pp.2, 2009, https://doi.org/10.1530/rep-12-0316
  10. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology vol.146, pp.1, 2009, https://doi.org/10.1530/rep-13-0058
  11. Comparative Transcriptome Analysis of the Accessory Sex Gland and Testis from the Chinese Mitten Crab ( Eriocheir sinensis ) vol.8, pp.1, 2009, https://doi.org/10.1371/journal.pone.0053915
  12. CLCAs - A Family of Metalloproteases of Intriguing Phylogenetic Distribution and with Cases of Substituted Catalytic Sites vol.8, pp.5, 2009, https://doi.org/10.1371/journal.pone.0062272
  13. Vesicular transfer of membrane components to bovine epididymal spermatozoa vol.353, pp.3, 2013, https://doi.org/10.1007/s00441-013-1633-7
  14. High-resolution helium ion microscopy of epididymal epithelial cells and their interaction with spermatozoa vol.20, pp.10, 2009, https://doi.org/10.1093/molehr/gau052
  15. Prostasomes: extracellular vesicles from the prostate vol.147, pp.1, 2014, https://doi.org/10.1530/rep-13-0358
  16. Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane vol.29, pp.2, 2009, https://doi.org/10.1096/fj.14-259382
  17. Development of Apical Blebbing in the Boar Epididymis vol.10, pp.5, 2009, https://doi.org/10.1371/journal.pone.0126848
  18. Extracellular vesicle-mediated delivery of molecular compounds into gametes and embryos: learning from nature vol.21, pp.5, 2015, https://doi.org/10.1093/humupd/dmv027
  19. Reduced Fertility and Altered Epididymal and Sperm Integrity in Mice Lacking ADAM71 vol.93, pp.3, 2015, https://doi.org/10.1095/biolreprod.115.130252
  20. Roll over Weismann: extracellular vesicles in the transgenerational transmission of environmental effects vol.7, pp.7, 2009, https://doi.org/10.2217/epi.15.58
  21. Sperm Proteome Maturation in the Mouse Epididymis vol.10, pp.11, 2015, https://doi.org/10.1371/journal.pone.0140650
  22. Quantitative Glycopeptide Changes in Rat Sperm During Epididymal Transit1 vol.94, pp.4, 2009, https://doi.org/10.1095/biolreprod.115.134114
  23. PLAG1 deficiency impairs spermatogenesis and sperm motility in mice vol.7, pp.None, 2009, https://doi.org/10.1038/s41598-017-05676-4
  24. Preclinical evaluation of a TEX101 protein ELISA test for the differential diagnosis of male infertility vol.15, pp.1, 2009, https://doi.org/10.1186/s12916-017-0817-5
  25. Validating Missing Proteins in Human Sperm Cells by Targeted Mass-Spectrometry- and Antibody-based Methods vol.16, pp.12, 2009, https://doi.org/10.1021/acs.jproteome.7b00374
  26. Extracellular Vesicles in Human Reproduction in Health and Disease vol.39, pp.3, 2009, https://doi.org/10.1210/er.2017-00229
  27. Proteomic analysis of seminal extracellular vesicle proteins involved in asthenozoospermia by iTRAQ vol.86, pp.9, 2019, https://doi.org/10.1002/mrd.23224
  28. Weighted single-step GWAS identified candidate genes associated with semen traits in a Duroc boar population vol.20, pp.1, 2009, https://doi.org/10.1186/s12864-019-6164-5
  29. ANDROGENIC FUNCTION OF TESTES AND STATE OF SPERMS IN YOUNG AND AGING RATS AFTER LONG INHIBITION OF STEROID AROMATASE FOLLOWED BY ITS WITHDRAWAL vol.65, pp.6, 2009, https://doi.org/10.15407/fz65.06.003
  30. Quantitative Proteomic Analysis of Seminal Plasma, Sperm Membrane Proteins, and Seminal Extracellular Vesicles Suggests Vesicular Mechanisms Aid in the Removal and Addition of Proteins to the Ram Sper vol.20, pp.12, 2009, https://doi.org/10.1002/pmic.201900289
  31. Roles of male reproductive tract extracellular vesicles in reproduction vol.85, pp.2, 2009, https://doi.org/10.1111/aji.13338