CD9 controls the formation of clusters that contain tetraspanins and the intergrin α6β1, which are involved in human and mouse gamete fusion

Journal of Cell Science

Volumn 119, Issue 3, 2006, Pages 416-424

  Ziyyat, Ahmed ^a,d   Rubinstein, Eric ^b   Monier Gavelle, Frédérique ^a,d   Barraud, Virginie ^a,d   Kulski, Olivier ^a,d   Prenant, Michel ^b   Boucheix, Claude ^b   Bomsel, Morgane ^c   Wolf, Jean Philippe ^a,d  

^a UNIVERSITÉ PARIS 13   (France)

^b INSERM   (France)

^c INSTITUT COCHIN   (France)

^d HÔPITAL JEAN VERDIER   (France)

Author keywords

CD151; CD9; Fertilization; Human; Integrins; Tetraspanins

Indexed keywords

CD9 ANTIGEN; FLUORESCENT DYE; MONOCLONAL ANTIBODY; TETRASPANIN; VERY LATE ACTIVATION ANTIGEN 6;

ANIMAL CELL; ARTICLE; CELL FUSION; CONTROLLED STUDY; FERTILIZATION IN VITRO; GAMETE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; SPERM; ZONA PELLUCIDA;

ANIMALIA;

EID: 33644977667     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02730     Document Type: Article

References (63)

1. Almeida, E. A., Huovila, A. P., Sutherland, A. E., Stephens, L. E., Calarco, P. G., Shaw, L. M., Mercurio, A. M., Sonnenberg, A., Primakoff, P. and Myles, D. G. (1995). Mouse egg integrin alpha 6 beta 1 functions as a sperm receptor. Cell 81, 1095-1104.
2. Azorsa, D. O., Moog, S., Cazenave, J. P. and Lanza, F. (1999). A general approach to the generation of monoclonal antibodies against members of the tetraspanin superfamily using recombinant GST fusion proteins. J. Immunol. Methods 229, 35-48.
3. Bazzoni, G. and Hemler, M. E. (1998). Are changes in integrin affinity and conformation overemphasized? Trends Biochem. Sci. 23, 30-34.
4. Berditchevski, F. (2001). Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 114, 4143-4151.
5. Berditchevski, F., Odintsova, E., Sawada, S. and Gilbert, E. (2002). Expression of the palmitoylation-deficient CD151 weakens the association of alpha 3 beta 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling. J. Biol. Chem. 277, 36991-37000.
6. Boucheix, C. and Rubinstein, E. (2001). Tetraspanins. Cell Mol. Life Sci. 58, 1189-1205.
7. Bronson, R. A., Fusi, F. M., Calzi, F., Doldi, N. and Ferrari, A. (1999). Evidence that a functional fertilin-like ADAM plays a role in human sperm-oolemmal interactions. Mol. Hum. Reprod. 5, 433-440.
8. Campbell, S., Swann, H. R., Aplin, J. D., Seif, M. W., Kimber, S. J. and Elstein, M. (1995a). CD44 is expressed throughout pre-implantation human embryo development. Hum. Reprod. 10, 425-430.
9. Campbell, S., Swann, H. R., Seif, M. W., Kimber, S. J. and Aplin, J. D. (1995b). Cell adhesion molecules on the oocyte and preimplantation human embryo. Hum. Reprod. 10, 1571-1578.
10. Capmany, G., Mart, M., Santalo, J. and Bolton, V. N. (1998). Distribution of alpha3, alphas and alpha(v) integrin subunits in mature and immature human oocytes. Mol. Hum. Reprod. 4, 951-956.
11. Charrin, S., le Naour, F., Oualid, M., Billard, M., Faure, G., Hanash, S. M., Boucheix, C. and Rubinstein, E. (2001). The major CD9 and CD81 molecular partner: Identification and characterization of the complexes. J. Biol. Chem. 276, 14329-14337.
12. Charrin, S., Manie, S., Billard, M., Ashman, L., Gerlier, D., Boucheix, C. and Rubinstein, E. (2003). Multiple levels of interactions within the tetraspanin web. Biochem. Biophys. Res. Commun. 304, 107-112.
13. Chen, H. and Sampson, N. S. (1999). Mediation of sperm-egg fusion: evidence that mouse egg alpha6beta1 integrin is the receptor for sperm ferfilin beta. Chem. Biol. 6, 1-10.
14. Chen, M. S., Tung, K. S., Coonrod, S. A., Takahashi, Y., Bigler, D., Chang, A., Yamashita, Y., Kincade, P. W., Herr, J. C. and White, J. M. (1999). Role of the integrin-associated protein CD9 in binding between sperm ADAM 2 and the egg integrin alpha6beta1: implications for marine fertilization. Proc. Natl. Acad. Sci. USA 96, 11830-11835.
15. 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.
16. Cowan, A. E., Myles, D. G. and Koppel, D. E. (1991). Migration of the guinea pig sperm membrane protein PH-20 from one localized surface domain to another does not occur by a simple diffusion-trapping mechanism. Dev. Biol. 144, 189-198.
17. Davies, T. J. and Gardner, R. L. (2002). The plane of first cleavage is not related to the distribution of sperm components in the mouse. Hum. Reprod. 17, 2368-2379.
18. Evans, J. P. (1999). Sperm disintegrins, egg integrins, and other cell adhesion molecules of mammalian gamete plasma membrane interactions. Front. Biosci. 4, D114-D131.
19. Evans, J. P., Kopf, G. S. and Schultz, R. M. (1997). Characterization of the binding of recombinant mouse sperm fertilin beta subunit to mouse eggs: evidence for adhesive activity via an egg beta1 integrin-mediated interaction. Dev. Biol. 187, 79-93.
20. Feigelson, S. W., Grabovsky, V., Shamri, R., Levy, S. and Alon, R. (2003). The CD81 tetraspanin facilitates instantaneous leukocyte VLA-4 adhesion strengthening to vascular cell adhesion molecule 1 (VCAM-1) under shear flow. J. Biol. Chem. 278, 51203-51212.
21. Fitter, S., Sincock, P. M., Jolliffe, C. N. and Ashman, L. K. (1999). Transmembrane 4 superfamily protein CD151 (PETA-3) associates with beta 1 and alpha IIb beta 3 integrins in haemopoietic cell lines and modulates cell-cell adhesion. Biochem. J. 338, 61-70.
22. Fusi, F. M., Vignali, M., Busacca, M. and Bronson, R. A. (1992). Evidence for the presence of an integrin cell adhesion receptor on the oolemma of unfertilized human oocytes. Mol. Reprod. Dev. 31, 215-222.
23. He, Z. Y., Brakebusch, C., Fassler, R., Kreidberg, J. A., Primakoff, P. and Myles, D. G. (2003). None of the integrins known to be present on the mouse egg or to be ADAM receptors are essential for sperm-egg binding and fusion. Dev. Biol. 254, 226-237.
24. Hemler, M. E. (2003). Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 19, 397-422.
25. Higginbottom, A., Quinn, E. R., Kuo, C. C., Flint, M., Wilson, L. H., Bianchi, E., Nicosia, A., Monk, P. N., McKeating, J. A. and Levy, S. (2000). Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J. Virol. 74, 3642-3649.
26. Horvath, P. M., Kellom, T., Caulfield, J. and Boldt, J. (1993). Mechanistic studies of the plasma membrane block to polyspermy in mouse eggs. Mol. Reprod. Dev. 34, 65-72.
27. Ito, Y., Yoshida, H., Uruno, T., Nakano, K., Takamura, Y., Miya, A., Kobayashi, K., Yokozawa, T., Matsuzuka, F., Kuma, K. et al. (2003). KAI1 expression in thyroid neoplasms: its linkage with clinicopathologic features in papillary carcinoma. Pathol. Res. Pract. 199, 79-83.
28. Ji, Y. Z., Wolf, J. P., Jouannet, P. and Bomsel, M. (1998). Human gamete fusion can bypass beta1 integrin requirement. Hum. Reprod. 13, 682-689.
29. Jones, P. H., Bishop, L. A. and Watt, F. M. (1996). Functional significance of CD9 association with β1 integrins in human epidermal keratinocytes. Cell Adh. Comm. 4, 297-305.
30. Kaji, K., Oda, S., Shikano, T., Ohnuki, T., Uematsu, Y., Sakagami, J., Tada, N., Miyazaki, S. and Kudo, A. (2000). The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat. Genet. 24, 279-282.
31. Kaji, K., Oda, S., Miyazaki, S. and 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.
32. Karamatic Crew, V., Burton, N., Kagan, A., Green, C. A., Levene, C., Flinter, F., Brady, R. L., Daniels, G. and Anstee, D. J. (2004). CD151, the first member of the tetraspanin (TM4) superfamily detected on erythrocytes, is essential for the correct assembly of human basement membranes in kidney and skin. Blood 104, 2217-2223.
33. Kellom, T., Vick, A. and Boldt, J. (1992). Recovery of penetration ability in protease-treated zona-free mouse eggs occurs coincident with recovery of a cell surface 94 kD protein. Mol. Reprod Dev. 33, 46-52.
34. Kinn, S. R. and Allen, T. D. (1981). Conversion of blebs to microvilli: cell surface reorganisation after trypsin. Differentiation 20, 168-173.
35. Lammerding, J., Kazarov, A. R., Huang, H., Lee, R. T. and Hemler, M. E. (2003). Tetraspanin CD151 regulates {alpha}6(beta}1 integrin adhesion strengthening. Proc. Natl. Acad. Sci. USA 100, 7616-7621.
36. Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M. and Boucheix, C. (2000). Severely reduced female fertility in CD9-deficient mice. Science 287, 319-321.
37. Liddington, R. C. and Ginsberg, M. H. (2002). Integrin activation takes shape. J. Cell Biol. 158, 833-839.
38. Maro, B., Johnson, M. H., Pickering, S. J. and Flach, G. (1984). Changes in actin distribution during fertilization of the mouse egg. J. Embryol. Exp. Morphol. 81, 211-237.
39. Miller, B. J., Georges-Labouesse, E., Primakoff, P. and Myles, D. G. (2000). Normal fertilization occurs with eggs lacking the integrin alpha6beta1 and is CD9-dependent. J. Cell Biol. 149, 1289-1296.
40. Miyado, K., Yamada, G., Yamada, S., Hasuwa, H., Nakamura, Y., Ryu, F., Suzuki, K., Kosai, K., Inoue, K., Ogura, A., Okabe, M. and Mekada, E. (2000). Requirement of CD9 on the egg plasma membrane for fertilization. Science 287, 321-324.
41. Noguchi, T. and Mabuchi, I. (2001). Reorganization of actin cytoskeleton at the growing end of the cleavage furrow of Xenopus egg during cytokinesis. J. Cell Sci. 114, 401-412.
42. Primakoff, P. and Myles, D. G. (2002). Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science 296, 2183-2185.
43. Rubinstein, E., le Naour, F., Lagaudrière, C., Billard, M., Conjeaud, H. and Boucheix, C. (1996). CD9, CD63, CD81 and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur. J. Immunol. 26, 2657-2665.
44. Sanchez-Mateos, P., Cabanas, C. and Sanchez-Madrid, F. (1996). Regulation of integrin function. Semin. Cancer Biol. 7, 99-109.
45. Santella, L., Alikani, M., Talansky, B. E., Cohen, J. and Dale, B. (1992). Is the human oocyte plasma membrane polarized? Hum. Reprod. 7, 999-1003.
46. Schwartz, M. A. (1992). Transmembrane signalling by integrins. Trends Cell Biol. 2, 304-308.
47. Serru, V., le Naour, F., Billard, M., Azorsa, D. O., Lanza, F., Boucheix, C. and Rubinstein, E. (1999). Selective Tetraspan/integrin complexes (CD81/α4β1, CD151/α3β1, CD151 /α6β1) under conditions disrupting tetraspan interactions. Biochem. J. 340, 103-111.
48. Sonnenberg, A., Linders, C. J., Modderman, P. W., Damsky, C. H., Aumailley, M. and Timpl, R. (1990). Integrin recognition of different cell-binding fragments of laminin (P1, E3, E8) and evidence that alpha 6 beta 1 but not alpha 6 beta 4 functions as a major receptor for fragment E8. J. Cell Biol. 110, 2145-2155.
49. Suzuki, K., Eriksson, B., Shimizu, H., Nagai, T. and Rodriguez-Martinez, H. (2000). Effect of hyaluronan on monospermic penetration of porcine oocytes fertilized in vitro. Int. J. Androl. 23, 13-21.
50. Takahashi, Y., Yamakawa, N., Matsumoto, K., Toyoda, Y., Furukawa, K. and Sato, E. (2000). Analysis of the role of egg integrins in sperm-egg binding and fusion. Mol. Reprod. Dev. 56, 412-423.
51. Takahashi, Y., Bigler, D., Ito, Y. and White, J. M. (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.
52. Talbot, P. and Dandekar, P. (2003). Perivitelline space: does it play a role in blocking polyspermy in mammals? Microsc. Res. Tech. 61, 349-357.
53. Tarone, G., Russo, M. A., Hirsch, E., Odorisio, T., Altruda, F., Silengo, L. and Siracusa, G. (1993). Expression of beta 1 integrin complexes on the surface of unfertilized mouse oocyte. Development 117, 1369-1375.
54. Tesarik, J. and Kopecny, V. (1989). Developmental control of the human male pronucleus by ooplasmic factors. Hum. Reprod. 4, 962-968.
55. Tomczuk, M., Takahashi, Y., Huang, J., Murase, S., Mistretta, M., Klaffky, E., Sutherland, A., Bolling, L., Coonrod, S., Marcinkiewicz, C. et al. (2003). Role of multiple beta1 integrins in cell adhesion to the disintegrin domains of ADAMS 2 and 3. Exp. Cell Res. 290, 68-81.
56. Wassarman, P. M., Jovine, L. and Litscher, E. S. (2001). A profile of fertilization in mammals. Nat. Cell Biol. 3, E59-E64.
57. Whittingham, D. G. (1971). Culture of mouse ova. J. Reprod. Fertil. Suppl. 14, 7-21.
58. Wolf, J. P., Ducot, B., Aymar, C., Rodrigues, D., Desjardin, S., Jardin, A. and Jouannet, P. (1997). Absence of block to polyspermy at the human oolemma. Fertil. Steril. 67, 1095-1102.
59. Wright, M. D., Geary, S. M., Fitter, S., Moseley, G. W., Lau, L. M., Sheng, K. C., Apostolopoulos, V., Stanley, E. G., Jackson, D. E. and Ashman, L. K. (2004). Characterization of mice lacking the tetraspanin superfamily member CD151. Mol. Cell. Biol. 24, 5978-5988.
60. Yauch, R. L., Berditchevski, F., Harler, M. B., Reichner, J. and Hemler, M. E. (1998). Highly stoichiometric, stable, and specific association of integrin alpha3beta1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol. Biol. Cell 9, 2751-2765.
61. Zhang, X. A., Kazarov, A. R., Yang, X., Bontrager, A. L., Stipp, C. S. and Hemler, M. E. (2002). Function of the Tetraspanin CD151-alpha6beta1 integrin Complex during Cellular Morphogenesis. Mol. Biol. Cell 13, 1-11.
62. Zhu, G. Z., Miller, B. J., Boucheix, C., Rubinstein, E., Liu, C. C., Hynes, R. O., Myles, D. G. and Primakoff, P. (2002). Residues SFQ (173-175) in the large extracellular loop of CD9 are required for gamete fusion. Development 129, 1995-2002.
63. Zhu, X. and Evans, J. P. (2002). Analysis of the roles of RGD-binding integrins, alpha(4)/alpha(9) integrins, alpha(6) integrins, and CD9 in the interaction of the fertilin beta (ADAM2) disintegrin domain with the mouse egg membrane. Biol. Reprod. 66, 1193-1202.