Normal Fertilization Occurs with Eggs Lacking the Integrin {alpha}6{beta}1 and Is CD9-dependent

doi:10.1083/jcb.149.6.1289

This Article

	Full Text
	Full Text (PDF, 236K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Miller, B. J.
	Articles by Myles, D. G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Miller, B. J.
	Articles by Myles, D. G.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2000/6/1289/ $5.00
The Journal of Cell Biology, Volume 149, Number 6, June 12, 2000 1289-1296

Original Article

Normal Fertilization Occurs with Eggs Lacking the Integrin ${alpha}$ 6ß1 and Is CD9-dependent

Brent J. Miller^a, Elisabeth Georges-Labouesse^c, Paul Primakoff^b, and Diana G. Myles^a
^a Department of Molecular and Cellular Biology, University of California Davis, Davis, California 95616
^b Department of Cell Biology and Human Anatomy, School of Medicine, University of California Davis, Davis, California 95616
^c Institut de Génétique et de Biologie Moléculaire et Cellulaire, Centre National de la Recherche Scientifique, Institut National de la Sante et de la Recherche Medicale, ULP, 67404 Illkirch, C.U. de Strasbourg, France

Correspondence to: Diana G. Myles, Department of Molecular and Cellular Biology, University of California Davis, One Shields Avenue, Davis, CA 96516. Tel:(530) 752-1553 Fax:(530) 752-7522 E-mail:dgmyles{at}ucdavis.edu.

Previous results, based on inhibition of fertilization by ananti– ${alpha}$ 6 integrin mAb (GoH3), suggest that the ${alpha}$ 6ß1integrin on mouse eggs functions as the receptor for sperm (Almeida,E.A., A.P. Huovila, A.E. Sutherland, L.E. Stephens, P.G. Calarco,L.M. Shaw, A.M. Mercurio, A. Sonnenberg, P. Primakoff, D.G.Myles, and J.M. White. 1995. Cell. 81:1095–1104). Becausethe egg surface tetraspanin CD9 is essential for gamete fusion(Kaji, K., S. Oda, T. Shikano, T. Ohnuki, Y. Uematsu, J. Sakagami,N. Tada, S. Miyazaki, and A. Kudo. 2000. Nat. Genet. 24:279–282;Le Naour, F., E. Rubinstein, C. Jasmin, M. Prenant, and C. Boucheix.2000. Science. 287:319–321; Miyado, K., G. Yamada, S.Yamada, H. Hasuwa, Y. Nakamura, F. Ryu, K. Suzuki, K. Kosai,K. Inoue, A. Ogura, M. Okabe, and E. Mekada. 2000. Science.287:321–324) and CD9 is known to associate with integrins,recent models of gamete fusion have posited that egg CD9 actsin association with ${alpha}$ 6ß1 in fusion (Chen, M.S., K.S. Tung,S.A. Coonrod, Y. Takahashi, D. Bigler, A. Chang, Y. Yamashita,P.W. Kincade, J.C. Herr, and J.M. White. 1999. Proc. Natl. Acad.Sci. USA. 96:11830–11835; Kaji, K., S. Oda, T. Shikano,T. Ohnuki, Y. Uematsu, J. Sakagami, N. Tada, S. Miyazaki, andA. Kudo. 2000. Nat. Genet. 24:279–282; Le Naour, F., E.Rubinstein, C. Jasmin, M. Prenant, and C. Boucheix. 2000. Science.287:319–321; Miyado, K., G. Yamada, S. Yamada, H. Hasuwa,Y. Nakamura, F. Ryu, K. Su- zuki, K. Kosai, K. Inoue, A. Ogura,M. Okabe, and E. Mekada. 2000. Science. 287:321–324).Using eggs from cultured ovaries of mice lacking the ${alpha}$ 6 integrinsubunit, we found that the fertilization rate, fertilizationindex, and sperm binding were not impaired compared with wild-typeor heterozygous controls. Furthermore, a reexamination of antibodyinhibition, using an assay that better simulates in vivo fertilizationconditions, revealed no inhibition of fusion by the GoH3 mAb.We also found that an anti-CD9 mAb completely blocks sperm fusionwith either wild-type eggs or eggs lacking ${alpha}$ 6ß1. Basedon these results, we conclude that the ${alpha}$ 6ß1 integrin isnot essential for sperm–egg fusion, and we suggest a newmodel in which CD9 acts by itself, or interacts with egg protein(s)other than ${alpha}$ 6ß1, to function in sperm–egg fusion.

Key Words: sperm–egg fusion, tetraspanin, membrane adhesion, oocyte,ovarian cultare

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Miyado, K., Yoshida, K., Yamagata, K., Sakakibara, K., Okabe, M., Wang, X., Miyamoto, K., Akutsu, H., Kondo, T., Takahashi, Y., Ban, T., Ito, C., 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. USA 105: 12921-12926 [Abstract] [Full Text]
Swain, J. E., Pool, T. B. (2008). ART failure: oocyte contributions to unsuccessful fertilization. Hum Reprod Update 14: 431-446 [Abstract] [Full Text]
Lin, Y.-N., Roy, A., Yan, W., Burns, K. H., Matzuk, M. M. (2007). Loss of Zona Pellucida Binding Proteins in the Acrosomal Matrix Disrupts Acrosome Biogenesis and Sperm Morphogenesis. Mol. Cell. Biol. 27: 6794-6805 [Abstract] [Full Text]
Qian, H., Georges-Labouesse, E., Nystrom, A., Domogatskaya, A., Tryggvason, K., Jacobsen, S. E. W., Ekblom, M. (2007). Distinct roles of integrins {alpha}6 and {alpha}4 in homing of fetal liver hematopoietic stem and progenitor cells. Blood 110: 2399-2407 [Abstract] [Full Text]
Mahbub Hasan, A.K.M., Ou, Z., Sakakibara, K., Hirahara, S., Iwasaki, T., Sato, K.-i., Fukami, Y. (2007). Characterization of Xenopus egg membrane microdomains containing uroplakin Ib/III complex: roles of their molecular interactions for subcellular localization and signal transduction.. GENES CELLS 12: 251-267 [Abstract] [Full Text]
Ziyyat, A., Rubinstein, E., Monier-Gavelle, F., Barraud, V., Kulski, O., Prenant, M., Boucheix, C., Bomsel, M., Wolf, J.-P. (2006). CD9 controls the formation of clusters that contain tetraspanins and the integrin {alpha}6{beta}1, which are involved in human and mouse gamete fusion. J. Cell Sci. 119: 416-424 [Abstract] [Full Text]
Whitaker, M. (2006). Calcium at Fertilization and in Early Development. Physiol. Rev. 86: 25-88 [Abstract] [Full Text]
Ziyyat, A., Naud-Barriant, N., Barraud-Lange, V., Chevalier, F., Kulski, O., Lemkecher, T., Bomsel, M., Wolf, J.P. (2005). Cyclic FEE peptide increases human gamete fusion and potentiates its RGD-induced inhibition. Hum Reprod 20: 3452-3458 [Abstract] [Full Text]
Barreiro, O., Yanez-Mo, M., Sala-Valdes, M., Gutierrez-Lopez, M. D., Ovalle, S., Higginbottom, A., Monk, P. N., Cabanas, C., Sanchez-Madrid, F. (2005). Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation. Blood 105: 2852-2861 [Abstract] [Full Text]
Stein, K. K., Primakoff, P., Myles, D. (2004). Sperm-egg fusion: events at the plasma membrane. J. Cell Sci. 117: 6269-6274 [Abstract] [Full Text]
Carroll, J (2004). EDITORIAL. Reproduction 127: 407-408 [Full Text]
Sengoku, K., Takuma, N., Miyamoto, T., Horikawa, M., Ishikawa, M. (2004). Integrins are not involved in the process of human sperm-oolemmal fusion. Hum Reprod 19: 639-644 [Abstract] [Full Text]
Zhang, J., Randall, G., Higginbottom, A., Monk, P., Rice, C. M., McKeating, J. A. (2004). CD81 Is Required for Hepatitis C Virus Glycoprotein-Mediated Viral Infection. J. Virol. 78: 1448-1455 [Abstract] [Full Text]
Li, Y.-H., Hou, Y., Ma, W., Yuan, J.-X., Zhang, D., Sun, Q.-Y., Wang, W.-H. (2004). Localization of CD9 in pig oocytes and its effects on sperm-egg interaction. Reproduction 127: 151-157 [Abstract] [Full Text]
Murk, J. L. A. N., Humbel, B. M., Ziese, U., Griffith, J. M., Posthuma, G., Slot, J. W., Koster, A. J., Verkleij, A. J., Geuze, H. J., Kleijmeer, M. J. (2003). Endosomal compartmentalization in three dimensions: Implications for membrane fusion. Proc. Natl. Acad. Sci. USA 100: 13332-13337 [Abstract] [Full Text]
Sato, K.-i., Tokmakov, A. A., He, C.-L., Kurokawa, M., Iwasaki, T., Shirouzu, M., Fissore, R. A., Yokoyama, S., Fukami, Y. (2003). Reconstitution of Src-dependent Phospholipase C{gamma} Phosphorylation and Transient Calcium Release by Using Membrane Rafts and Cell-free Extracts from Xenopus Eggs. J. Biol. Chem. 278: 38413-38420 [Abstract] [Full Text]
Alfieri, J. A., Martin, A. D., Takeda, J., Kondoh, G., Myles, D. G., Primakoff, P. (2003). Infertility in female mice with an oocyte-specific knockout of GPI-anchored proteins. J. Cell Sci. 116: 2149-2155 [Abstract] [Full Text]
Misamore, M. J., Gupta, S., Snell, W. J. (2003). The Chlamydomonas Fus1 Protein Is Present on the Mating Type plus Fusion Organelle and Required for a Critical Membrane Adhesion Event during Fusion with minus Gametes. Mol. Biol. Cell 14: 2530-2542 [Abstract] [Full Text]
Zhu, G.-Z., Miller, B. J., Boucheix, C., Rubinstein, E., Liu, C. C., Hynes, R. O., Myles, D. G., Primakoff, P. (2003). Residues SFQ (173-175) in the large extracellular loop of CD9 are required for gamete fusion. Development 129: 1995-2002 [Abstract] [Full Text]
Seals, D. F., Courtneidge, S. A. (2003). The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17: 7-30 [Full Text]
Talbot, P., Shur, B. D., Myles, D. G. (2003). Cell Adhesion and Fertilization: Steps in Oocyte Transport, Sperm-Zona Pellucida Interactions, and Sperm-Egg Fusion. Biol. Reprod. 68: 1-9 [Abstract] [Full Text]
Primakoff, P., Myles, D. G. (2002). Penetration, Adhesion, and Fusion in Mammalian Sperm-Egg Interaction. Science 296: 2183-2185 [Abstract] [Full Text]
Xiang, W., MacLaren, L. A. (2002). Expression of Fertilin and CD9 in Bovine Trophoblast and Endometrium During Implantation. Biol. Reprod. 66: 1790-1796 [Abstract] [Full Text]
Eto, K., Huet, C., Tarui, T., Kupriyanov, S., Liu, H.-Z., Puzon-McLaughlin, W., Zhang, X.-P., Sheppard, D., Engvall, E., Takada, Y. (2002). Functional Classification of ADAMs Based on a Conserved Motif for Binding to Integrin alpha 9beta 1. IMPLICATIONS FOR SPERM-EGG BINDING AND OTHER CELL INTERACTIONS. J. Biol. Chem. 277: 17804-17810 [Abstract] [Full Text]
Zhu, X., 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 [Abstract] [Full Text]
Miller, D. J., Shi, X., Burkin, H. (2002). Molecular Basis of Mammalian Gamete Binding. Recent Prog Horm Res 57: 37-73 [Abstract] [Full Text]
Stanton, J.L., Green, D.P.L. (2001). A set of 840 mouse oocyte genes with well-matched human homologues. Mol Hum Reprod 7: 521-543 [Abstract] [Full Text]
Wu, H., Smyth, J., Luzzi, V., Fukami, K., Takenawa, T., Black, S. L., Allbritton, N. L., Fissore, R. A. (2001). Sperm Factor Induces Intracellular Free Calcium Oscillations by Stimulating the Phosphoinositide Pathway. Biol. Reprod. 64: 1338-1349 [Abstract] [Full Text]
Takahashi, Y., Bigler, D., Ito, Y., White, J. M. (2001). Sequence-Specific Interaction between the Disintegrin Domain of Mouse ADAM 3 and Murine Eggs: Role of {beta}1 Integrin-associated Proteins CD9, CD81, and CD98. Mol. Biol. Cell 12: 809-820 [Abstract] [Full Text]
Eto, K., Puzon-McLaughlin, W., Sheppard, D., Sehara-Fujisawa, A., Zhang, X.-P., Takada, Y. (2000). RGD-independent Binding of Integrin alpha 9beta 1 to the ADAM-12 and -15 Disintegrin Domains Mediates Cell-Cell Interaction. J. Biol. Chem. 275: 34922-34930 [Abstract] [Full Text]
Wong, G. E., Zhu, X., Prater, C. E., Oh, E., Evans, J. P. (2001). Analysis of Fertilin alpha (ADAM1)-mediated Sperm-Egg Cell Adhesion during Fertilization and Identification of an Adhesion-mediating Sequence in the Disintegrin-like Domain. J. Biol. Chem. 276: 24937-24945 [Abstract] [Full Text]
Hemler, M. E. (2001). Specific tetraspanin functions. JCB 155: 1103-1108 [Abstract] [Full Text]

Original Article

Normal Fertilization Occurs with Eggs Lacking the Integrin 6ß1 and Is CD9-dependent

Normal Fertilization Occurs with Eggs Lacking the Integrin ${alpha}$ 6ß1 and Is CD9-dependent