The Cysteine-rich Domain of Human ADAM 12 Supports Cell Adhesion Through Syndecans and Triggers Signaling Events that Lead to {beta}1 Integrin-dependent Cell Spreading

doi:10.1083/jcb.149.5.1143

This Article

	Full Text
	PDF (Full Text)
	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 Iba, K.
	Articles by Wewer, U. M.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Iba, K.
	Articles by Wewer, U. M.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2000/5/1143/ $5.00
The Journal of Cell Biology, Volume 149, Number 5, May 29, 2000 1143-1156

Original Article

The Cysteine-rich Domain of Human ADAM 12 Supports Cell Adhesion Through Syndecans and Triggers Signaling Events that Lead to ß1 Integrin–dependent Cell Spreading

Kousuke Iba^a, Reidar Albrechtsen^a, Brent Gilpin^a, Camilla Fröhlich^a, Frosty Loechel^a, Anna Zolkiewska^b, Kazuhiro Ishiguro^c, Tetsuhito Kojima^c, Wei Liu^d, J. Kevin Langford^d, Ralph D. Sanderson^d, Cord Brakebusch^e, Reinhard Fässler^e, and Ulla M. Wewer^a
^a The Institute of Molecular Pathology, University of Copenhagen, 2100 Copenhagen, Denmark
^b Department of Biochemistry, Kansas State University, Manhattan, Kansas 66506
^c Department of Medical Technology, School of Health Sciences, and First Department of Internal Medicine, Nagoya University, Nagoya 466-8550, Japan
^d The Department of Pathology, Arkansas Cancer Research Center, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205
^e Department of Experimental Pathology, Lund University, Lund 22185, Sweden

Correspondence to: Ulla M. Wewer, Institute of Molecular Pathology, University of Copenhagen, Frederik V's vej 11, 2100 Copenhagen, Denmark. Tel:45 3532 6056 Fax:45 3532 6081 E-mail:molera{at}inet.uni2.dk.

The ADAMs (a disintegrin and metalloprotease) family of proteinsis involved in a variety of cellular interactions, includingcell adhesion and ecto- domain shedding. Here we show that ADAM12 binds to cell surface syndecans. Three forms of recombinantADAM 12 were used in these experiments: the cys-teine-rich domainmade in Escherichia coli (rADAM 12-cys), the disintegrin-likeand cysteine-rich domain made in insect cells (rADAM 12-DC),and full-length human ADAM 12-S tagged with green fluorescentprotein made in mammalian cells (rADAM 12-GFP). Mesenchymalcells specifically and in a dose-dependent manner attach toADAM 12 via members of the syndecan family. After binding tosyndecans, mesenchymal cells spread and form focal adhesionsand actin stress fibers. Integrin ß1 was responsible forcell spreading because function-blocking monoclonal antibodiescompletely inhibited cell spreading, and chondroblasts lackingß1 integrin attached but did not spread. These data suggestthat mesenchymal cells use syndecans as the initial receptorfor the ADAM 12 cysteine-rich domain–mediated cell adhesion,and then the ß1 integrin to induce cell spreading. Interestingly,carcinoma cells attached but did not spread on ADAM 12. However,spreading could be efficiently induced by the addition of either1 mM Mn²⁺ or the ß1 integrin–activating monoclonalantibody 12G10, suggesting that in these carcinoma cells, theADAM 12–syndecan complex fails to modulate the functionof ß1 integrin.

Key Words: ADAM, syndecan, integrin, cell adhesion, receptor cross-talk

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:

Bourd-Boittin, K., Le Pabic, H., Bonnier, D., L'Helgoualc'h, A., Theret, N. (2008). RACK1, a New ADAM12 Interacting Protein: CONTRIBUTION TO LIVER FIBROGENESIS. J. Biol. Chem. 283: 26000-26009 [Abstract] [Full Text]
Frohlich, C., Albrechtsen, R., Dyrskjot, L., Rudkjaer, L., Orntoft, T. F., Wewer, U. M. (2006). Molecular Profiling of ADAM12 in Human Bladder Cancer. Clin. Cancer Res. 12: 7359-7368 [Abstract] [Full Text]
Hozumi, K., Suzuki, N., Nielsen, P. K., Nomizu, M., Yamada, Y. (2006). Laminin {alpha}1 Chain LG4 Module Promotes Cell Attachment through Syndecans and Cell Spreading through Integrin {alpha}2beta1. J. Biol. Chem. 281: 32929-32940 [Abstract] [Full Text]
Werner, E., Kowalczyk, A. P., Faundez, V. (2006). Anthrax Toxin Receptor 1/Tumor Endothelium Marker 8 Mediates Cell Spreading by Coupling Extracellular Ligands to the Actin Cytoskeleton. J. Biol. Chem. 281: 23227-23236 [Abstract] [Full Text]
Ohtsu, H., Dempsey, P. J., Eguchi, S. (2006). ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 291: C1-C10 [Abstract] [Full Text]
Ma, G.-F., Liljestrom, M., Ainola, M., Chen, T., Tiainen, V.-M., Lappalainen, R., Konttinen, Y. T., Salo, J. (2006). Expression of ADAM9 (meltrin-{gamma}) around aseptically loosened total hip replacement implants. Rheumatology (Oxford) 45: 808-814 [Abstract] [Full Text]
McQuade, K. J., Beauvais, D. M., Burbach, B. J., Rapraeger, A. C. (2006). Syndecan-1 regulates {alpha}v{beta}5 integrin activity in B82L fibroblasts. J. Cell Sci. 119: 2445-2456 [Abstract] [Full Text]
Laigaard, J., Sorensen, T., Placing, S., Holck, P., Frohlich, C., Wojdemann, K. R., Sundberg, K., Shalmi, A.-C., Tabor, A., Norgaard-Pedersen, B., Ottesen, B., Christiansen, M., Wewer, U. M. (2005). Reduction of the Disintegrin and Metalloprotease ADAM12 in Preeclampsia. Obstet Gynecol 106: 144-149 [Abstract] [Full Text]
Yi, H., Gruszczynska-Biegala, J., Wood, D., Zhao, Z., Zolkiewska, A. (2005). Cooperation of the Metalloprotease, Disintegrin, and Cysteine-rich Domains of ADAM12 during Inhibition of Myogenic Differentiation. J. Biol. Chem. 280: 23475-23483 [Abstract] [Full Text]
Wang, H.-X., Zhao, Y.-G., Wang, H.-M., Yang, Q., Lin, H.-Y., Sang, Q.-X. A., Zhu, C. (2005). Expression of adamalysin 19/ADAM19 in the endometrium and placenta of rhesus monkey (Macaca mulatta) during early pregnancy. Mol Hum Reprod 11: 429-435 [Abstract] [Full Text]
Lafuste, P., Sonnet, C., Chazaud, B., Dreyfus, P. A., Gherardi, R. K., Wewer, U. M., Authier, F.-J. (2005). ADAM12 and {alpha}9{beta}1 Integrin Are Instrumental in Human Myogenic Cell Differentiation. Mol. Biol. Cell 16: 861-870 [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]
Roy, R., Wewer, U. M., Zurakowski, D., Pories, S. E., Moses, M. A. (2004). ADAM 12 Cleaves Extracellular Matrix Proteins and Correlates with Cancer Status and Stage. J. Biol. Chem. 279: 51323-51330 [Abstract] [Full Text]
Sundberg, C., Thodeti, C. K., Kveiborg, M., Larsson, C., Parker, P., Albrechtsen, R., Wewer, U. M. (2004). Regulation of ADAM12 Cell-surface Expression by Protein Kinase C {epsilon}. J. Biol. Chem. 279: 51601-51611 [Abstract] [Full Text]
Kodama, T., Ikeda, E., Okada, A., Ohtsuka, T., Shimoda, M., Shiomi, T., Yoshida, K., Nakada, M., Ohuchi, E., Okada, Y. (2004). ADAM12 Is Selectively Overexpressed in Human Glioblastomas and Is Associated with Glioblastoma Cell Proliferation and Shedding of Heparin-Binding Epidermal Growth Factor. Am. J. Pathol. 165: 1743-1753 [Abstract] [Full Text]
Kamimura, K., Rhodes, J. M., Ueda, R., McNeely, M., Shukla, D., Kimata, K., Spear, P. G., Shworak, N. W., Nakato, H. (2004). Regulation of Notch signaling by Drosophila heparan sulfate 3-O sulfotransferase. J. Cell Biol. 166: 1069-1079 [Abstract] [Full Text]
Campos, L. S., Leone, D. P., Relvas, J. B., Brakebusch, C., Fassler, R., Suter, U., ffrench-Constant, C. (2004). {beta}1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131: 3433-3444 [Abstract] [Full Text]
Powell, R. M., Wicks, J., Holloway, J. W., Holgate, S. T., Davies, D. E. (2004). The Splicing and Fate of ADAM33 Transcripts in Primary Human Airways Fibroblasts. Am. J. Respir. Cell Mol. Bio. 31: 13-21 [Abstract] [Full Text]
Hathaway, H. J., Evans, S. C., Dubois, D. H., Foote, C. I., Elder, B. H., Shur, B. D. (2003). Mutational analysis of the cytoplasmic domain of {beta}1,4-galactosyltransferase I: influence of phosphorylation on cell surface expression. J. Cell Sci. 116: 4319-4330 [Abstract] [Full Text]
Stacey, M., Chang, G.-W., Davies, J. Q., Kwakkenbos, M. J., Sanderson, R. D., Hamann, J., Gordon, S., Lin, H.-H. (2003). The epidermal growth factor-like domains of the human EMR2 receptor mediate cell attachment through chondroitin sulfate glycosaminoglycans. Blood 102: 2916-2924 [Abstract] [Full Text]
Cao, Y., Zhao, Z., Gruszczynska-Biegala, J., Zolkiewska, A. (2003). Role of Metalloprotease Disintegrin ADAM12 in Determination of Quiescent Reserve Cells during Myogenic Differentiation In Vitro. Mol. Cell. Biol. 23: 6725-6738 [Abstract] [Full Text]
Moghadaszadeh, B., Albrechtsen, R., Guo, L. T., Zaik, M., Kawaguchi, N., Borup, R. H., Kronqvist, P., Schroder, H. D., Davies, K. E., Voit, T., Nielsen, F. C., Engvall, E., Wewer, U. M. (2003). Compensation for dystrophin-deficiency: ADAM12 overexpression in skeletal muscle results in increased {alpha}7 integrin, utrophin and associated glycoproteins. Hum Mol Genet 12: 2467-2479 [Abstract] [Full Text]
Kawaguchi, N., Sundberg, C., Kveiborg, M., Moghadaszadeh, B., Asmar, M., Dietrich, N., Thodeti, C. K., Nielsen, F. C., Moller, P., Mercurio, A. M., Albrechtsen, R., Wewer, U. M. (2003). ADAM12 induces actin cytoskeleton and extracellular matrix reorganization during early adipocyte differentiation by regulating {beta}1 integrin function. J. Cell Sci. 116: 3893-3904 [Abstract] [Full Text]
ENGVALL, E., WEWER, U. M. (2003). The new frontier in muscular dystrophy research: booster genes. FASEB J. 17: 1579-1584 [Abstract] [Full Text]
Horiuchi, K., Weskamp, G., Lum, L., Hammes, H.-P., Cai, H., Brodie, T. A., Ludwig, T., Chiusaroli, R., Baron, R., Preissner, K. T., Manova, K., Blobel, C. P. (2003). Potential Role for ADAM15 in Pathological Neovascularization in Mice. Mol. Cell. Biol. 23: 5614-5624 [Abstract] [Full Text]
Holgate, S T, Davies, D E, Murphy, G, Powell, R M, Holloway, J W (2003). ADAM 33: just another asthma gene or a breakthrough in understanding the origins of bronchial hyperresponsiveness?. Thorax 58: 466-469 [Full Text]
Peiretti, F., Deprez-Beauclair, P., Bonardo, B., Aubert, H., Juhan-Vague, I., Nalbone, G. (2003). Identification of SAP97 as an intracellular binding partner of TACE. J. Cell Sci. 116: 1949-1957 [Abstract] [Full Text]
Thodeti, C. K., Albrechtsen, R., Grauslund, M., Asmar, M., Larsson, C., Takada, Y., Mercurio, A. M., Couchman, J. R., Wewer, U. M. (2003). ADAM12/Syndecan-4 Signaling Promotes beta 1 Integrin-dependent Cell Spreading through Protein Kinase Calpha and RhoA. J. Biol. Chem. 278: 9576-9584 [Abstract] [Full Text]
Kurisaki, T., Masuda, A., Sudo, K., Sakagami, J., Higashiyama, S., Matsuda, Y., Nagabukuro, A., Tsuji, A., Nabeshima, Y., Asano, M., Iwakura, Y., Sehara-Fujisawa, A. (2003). Phenotypic Analysis of Meltrin {alpha} (ADAM12)-Deficient Mice: Involvement of Meltrin {alpha} in Adipogenesis and Myogenesis. Mol. Cell. Biol. 23: 55-61 [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]
Smith, K. M., Gaultier, A., Cousin, H., Alfandari, D., White, J. M., DeSimone, D. W. (2002). The cysteine-rich domain regulates ADAM protease function in vivo. J. Cell Biol. 159: 893-902 [Abstract] [Full Text]
Kronqvist, P., Kawaguchi, N., Albrechtsen, R., Xu, X., Schroder, H. D., Moghadaszadeh, B., Nielsen, F. C., Frohlich, C., Engvall, E., Wewer, U. M. (2002). ADAM12 Alleviates the Skeletal Muscle Pathology in mdx Dystrophic Mice. Am. J. Pathol. 161: 1535-1540 [Abstract] [Full Text]
Cao, Y., Kang, Q., Zhao, Z., Zolkiewska, A. (2002). Intracellular Processing of Metalloprotease Disintegrin ADAM12. J. Biol. Chem. 277: 26403-26411 [Abstract] [Full Text]
Gaultier, A., Cousin, H., Darribere, T., Alfandari, D. (2002). ADAM13 Disintegrin and Cysteine-rich Domains Bind to the Second Heparin-binding Domain of Fibronectin. J. Biol. Chem. 277: 23336-23344 [Abstract] [Full Text]
Stevens, A., Jacobs, J. R. (2002). Integrins Regulate Responsiveness to Slit Repellent Signals. J. Neurosci. 22: 4448-4455 [Abstract] [Full Text]
Lilla, J., Stickens, D., Werb, Z. (2002). Metalloproteases and Adipogenesis: A Weighty Subject. Am. J. Pathol. 160: 1551-1554 [Full Text]
Kawaguchi, N., Xu, X., Tajima, R., Kronqvist, P., Sundberg, C., Loechel, F., Albrechtsen, R., Wewer, U. M. (2002). ADAM 12 Protease Induces Adipogenesis in Transgenic Mice. Am. J. Pathol. 160: 1895-1903 [Abstract] [Full Text]
Herren, B. (2002). ADAM-Mediated Shedding and Adhesion: a Vascular Perspective. Physiology 17: 73-76 [Abstract] [Full Text]
Wang, Z., Liu, Y., Mori, M., Kulesz-Martin, M. (2002). Gene expression profiling of initiated epidermal cells with benign or malignant tumor fates. Carcinogenesis 23: 635-643 [Abstract] [Full Text]
Weskamp, G., Cai, H., Brodie, T. A., Higashyama, S., Manova, K., Ludwig, T., Blobel, C. P. (2002). Mice Lacking the Metalloprotease-Disintegrin MDC9 (ADAM9) Have No Evident Major Abnormalities during Development or Adult Life. Mol. Cell. Biol. 22: 1537-1544 [Abstract] [Full Text]
Stepp, M. A., Gibson, H. E., Gala, P. H., Iglesia, D. D. Sta., Pajoohesh-Ganji, A., Pal-Ghosh, S., Brown, M., Aquino, C., Schwartz, A. M., Goldberger, O., Hinkes, M. T., Bernfield, M. (2002). Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115: 4517-4531 [Abstract] [Full Text]
Moiseeva, E. P. (2001). Adhesion receptors of vascular smooth muscle cells and their functions. Cardiovasc Res 52: 372-386 [Abstract] [Full Text]
Iba, K., Durkin, M. E., Johnsen, L., Hunziker, E., Damgaard-Pedersen, K., Zhang, H., Engvall, E., Albrechtsen, R., Wewer, U. M. (2001). Mice with a Targeted Deletion of the Tetranectin Gene Exhibit a Spinal Deformity. Mol. Cell. Biol. 21: 7817-7825 [Abstract] [Full Text]
Rapraeger, A. C. (2000). Syndecan-regulated Receptor Signaling. J. Cell Biol. 149: 995-998 [Abstract] [Full Text]
Iida, J., Pei, D., Kang, T., Simpson, M. A., Herlyn, M., Furcht, L. T., McCarthy, J. B. (2001). Melanoma Chondroitin Sulfate Proteoglycan Regulates Matrix Metalloproteinase-dependent Human Melanoma Invasion into Type I Collagen. J. Biol. Chem. 276: 18786-18794 [Abstract] [Full Text]
Kang, Q., Cao, Y., Zolkiewska, A. (2001). Direct Interaction between the Cytoplasmic Tail of ADAM 12 and the Src Homology 3 Domain of p85alpha Activates Phosphatidylinositol 3-Kinase in C2C12 Cells. J. Biol. Chem. 276: 24466-24472 [Abstract] [Full Text]
Utani, A., Nomizu, M., Matsuura, H., Kato, K., Kobayashi, T., Takeda, U., Aota, S., Nielsen, P. K., Shinkai, H. (2001). A Unique Sequence of the Laminin alpha 3 G Domain Binds to Heparin and Promotes Cell Adhesion through Syndecan-2 and -4. J. Biol. Chem. 276: 28779-28788 [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]