Potential role for ADAM15 in pathological neovascularization in mice

Molecular and Cellular Biology

Volumn 23, Issue 16, 2003, Pages 5614-5624

  Horiuchi, Keisuke ^a   Weskamp, Gisela ^a   Lum, Lawrence ^a   Hammes, Hans Peter ^d   Cai, Hui ^a,c   Brodie, Thomas A ⁱ   Ludwig, Thomas ^g   Chiusaroli, Riccardo ^f,h   Baron, Roland ^f,h   Preissner, Klaus T ^e   Manova, Katia ^b   Blobel, Carl P ^a,b  

^a Cell Biochem and Biophys Program   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c Weill Cornell Graduate School of Biomedical Sciences   (United States)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e JUSTUS LIEBIG UNIVERSITY   (Germany)

^f GLAXOSMITHKLINE   (United States)

^g Och Spine at New York Presbyterian Hospitals   (United States)

^h YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ Mem Sloan Kettering Cancer Center ^*

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CD31 ANTIGEN; DISINTEGRIN; MEMBRANE PROTEIN; METALLOPROTEINASE; METARGIDIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INTERACTION; CELL SURVIVAL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IN SITU HYBRIDIZATION; MELANOMA CELL; MOUSE; MUSCLE DEVELOPMENT; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; TARGET CELL;

ADAM PROTEINS; ALLELES; ANIMALS; BLOTTING, WESTERN; BRAIN; CELL MEMBRANE; CELLS, CULTURED; DNA, COMPLEMENTARY; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; GENE DELETION; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, GENETIC; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; RETINAL DISEASES; RNA, MESSENGER; TIME FACTORS; TISSUE DISTRIBUTION; TUMOR CELLS, CULTURED; UMBILICAL VEINS;

ANIMALIA;

EID: 0041631044     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.16.5614-5624.2003     Document Type: Article

References (80)

1. Abe, M., and Y. Sato. 2001. cDNA microarray analysis of the gene expression profile of VEGF-activated human umbilical vein endothelial cells. Angiogenesis 4:289-298.
2. Alfandari, D., H. Cousin, A. Gaultier, K. Smith, J. M. White, T. Darribere, and D. W. DeSimone. 2001. Xenopus ADAM 13 is a metalloprotease required for cranial neural crest-cell migration. Curr. Biol. 11:918-930.
3. Asakura, M., M. Kitakaze, S. Takashima, Y. Liao, F. Ishikura, T. Yoshinaka, H. Ohmoto, K. Node, K. Yoshino, H. Ishiguro, H. Asanuma, S. Sanada, Y. Matsumura, H. Takeda, S. Beppu, M. Tada, M. Hori, and S. Higashiyama. 2002. Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat. Med. 8:35-40.
4. Black, R. A., C. T. Rauch, C. J. Kozlosky, J. J. Peschon, J. L. Slack, M. F. Wolfson, B. J. Castner, K. L. Stocking, P. Reddy, S. Srinivasan, N. Nelson, N. Boiani, K. A. Schooley, M. Gerhart, R. Davis, J. N. Fitzner, R. S. Johnson, R. J. Paxton, C. J. March, and D. P. Cerretti. 1997. A metalloproteinase disintegrin that releases tumour-necrosis factor-α from cells. Nature 385:729-733.
5. Black, R. A., and J. M. White. 1998. ADAMs: focus on the protease domain. Curr. Opin. Cell Biol. 10:654-659.
6. Blobel, C. P. 1997. Metalloprotease-disintegrins: links to cell adhesion and cleavage of TNF α and Notch. Cell 90:589-592.
7. Bosse, F., G. Petzold, R. Greiner-Petter, U. Pippirs, C. Gillen, and H. W. Muller. 2000. Cellular localization of the disintegrin CRII-7/rMDC15 mRNA in rat PNS and CNS and regulated expression in postnatal development and after nerve injury. Glia 32:313-327.
8. Buxbaum, J. D., K. N. Liu, Y. Luo, J. L. Slack, K. L. Stocking, J. J. Peschon, R. S. Johnson, B. J. Castner, D. P. Cerretti, and R. A. Black. 1998. Evidence that tumor necrosis factor α converting enzyme is involved in regulated α-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 273:27765-27767.
9. Cal, S., J. M. Freije, J. M. Lopez, Y. Takada, and C. Lopez-Otin. 2000. ADAM 23/MDC3, a human disintegrin that promotes cell adhesion via interaction with the αvβ3 integrin through an RGD-independent mechanism. Mol. Biol. Cell 11:1457-1469.
10. Carmeliet, P., and R. K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature 407:249-257.
11. Chavakis, E., B. Riecke, J. Lin, T. Linn, R. G. Bretzel, K. T. Preissner, M. Brownlee, and H. P. Hammes. 2002. Kinetics of integrin expression in the mouse model of proliferative retinopathy and success of secondary intervention with cyclic RGD peptides. Diabetologia 45:262-267.
12. Cho, C., D. O. Bunch, J. E. Faure, E. H. Goulding, E. M. Eddy, P. Primakoff, and D. G. Myles. 1998. Fertilization defects in sperm from mice lacking fertilin β. Science 281:1857-1859.
13. -/- sperm: evidence for C-terminal modification, alpha/beta dimerization, and lack of essential role of fertilin α in sperm-egg fusion. Dev. Biol. 222:289-295.
14. Condon, T. P., S. Flournoy, G. J. Sawyer, B. F. Baker, T. K. Kishimoto, and C. F. Bennett. 2001. ADAM17 but not ADAM10 mediates tumor necrosis factor-alpha and L-selectin shedding from leukocyte membranes. Antisense Nucleic Acid Drug Dev. 11:107-116.
15. Eliceiri, B. P., and D. A. Cheresh. 1999. The role of αv integrins during angiogenesis: insights into potential mechanisms of action and clinical development. J. Clin. Investig. 103:1227-1230.
16. Eliceiri, B. P., R. Paul, P. L. Schwartzberg, J. D. Hood, J. Leng, and D. A. Cheresh. 1999. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol. Cell 4:915-924.
17. Eto, K., C. Huet, T. Tarui, S. Kupriyanov, H. Z. Liu, W. Puzon-McLaughlin, X. P. Zhang, D. Sheppard, E. Engvall, and Y. Takada. 2002. Functional classification of ADAMs based on a conserved motif for binding to integrin α9β1: implications for sperm-egg binding and other cell interactions. J. Biol. Chem. 277:17804-17810.
18. Eto, K., W. Puzon-McLaughlin, D. Sheppard, A. Sehara-Fujisawa, X. P. Zhang, and Y. Takada. 2000. RGD-independent binding of integrin α9β1 to the ADAM-12 and -15 disintegrin domains mediates cell-cell interaction. J. Biol. Chem. 275:34922-34930.
19. Fambrough, D., D. Pan, G. M. Rubin, and C. S. Goodman. 1996. The cell surface metalloprotease/disintegrin Kuzbanian is required for axonal extension in Drosophila. Proc. Natl. Acad. Sci. USA 93:13233-13238.
20. Fassler, R., and M. Meyer. 1995. Consequences of lack of β1 integrin gene expression in mice. Genes Dev. 9:1896-1908.
21. Gutwein, P., S. Mechtersheimer, S. Riedle, A. Stoeck, D. Gast, S. Joumaa, H. Zentgraf, M. Fogel, and P. Altevogt. 2002. ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB J. 3:292-294.
22. Ham, C., B. Levkau, E. W. Raines, and B. Herren. 2002. ADAM15 is an adherens junction molecule whose surface expression can be driven by VE-cadherin. Exp. Cell Res. 279:239-247.
23. Hammes, H. P., M. Brownlee, A. Jonczyk, A. Sutter, and K. T. Preissner. 1996. Subcutaneous injection of a cyclic peptide antagonist of vitronectin receptor-type integrins inhibits retinal neovascularization. Nat. Med. 2:529-533.
24. Hartmann, D., B. de Strooper, L. Serneels, K. Craessaerts, A. Herreman, W. Annaert, L. Umans, T. Lubke, A. Lena Illert, K. von Figura, and P. Saftig. 2002. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for α-secretase activity in fibroblasts. Hum. Mol. Genet. 11:2615-2624.
25. Heissig, B., K. Hattori, S. Dias, M. Friedrich, B. Ferris, N. R. Hackett, R. G. Crystal, P. Besmer, D. Lyden, M. A. Moore, Z. Werb, and S. Rafii. 2002. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of Kit-ligand. Cell 109:625-637.
26. Hernandez-Barrantes, S., M. Toth, M. M. Bernardo, M. Yurkova, D. C. Gervasi, Y. Raz, Q. A. Sang, and R. Fridman. 2000. Binding of active (57 kDa) membrane type 1-matrix metalloproteinase (MT1-MMP) to tissue inhibitor of metalloproteinase (TIMP)-2 regulates MT1-MMP processing and pro-MMP-2 activation. J. Biol. Chem. 275:12080-12089.
27. Herren, B., B. Levkau, E. W. Raines, and R. Ross. 1998. Cleavage of β-catenin and plakoglobin and shedding of VE-cadherin during endothelial apoptosis: evidence for a role for caspases and metalloproteinases. Mol. Biol. Cell 9:1589-1601.
28. Herren, B., E. W. Raines, and R. Ross. 1997. Expression of a disintegrin-like protein in cultured human vascular cells and in vivo. FASEB J. 11:173-180.
29. Hiraoka, N., E. Allen, I. J. Apel, M. R. Gyetko, and S. J. Weiss. 1998. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95:365-377.
30. Howard, L., K. K. Nelson, R. A. Maciewicz, and C. P. Blobel. 1999. Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J. Biol. Chem. 274:31693-31699.
31. Huang, X. Z., J. F. Wu, R. Ferrando, J. H. Lee, Y. L. Wang, R. V. Farese, Jr., and D. Sheppard. 2000. Fatal bilateral chylothorax in mice lacking the integrin α9β1. Mol. Cell. Biol. 20:5208-5215.
32. Iba, K., R. Albrechtsen, B. Gilpin, C. Frohlich, F. Loechel, A. Zolkiewska, K. Ishiguro, T. Kojima, W. Liu, J. K. Langford, R. D. Sanderson, C. Brakebusch, R. Fassler, and U. M. Wewer. 2000. The cysteine-rich domain of human ADAM 12 supports cell adhesion through syndecans and triggers signaling events that lead to β1 integrin-dependent cell spreading. J. Cell Biol. 149:1143-1156.
33. Ilan, N., A. Mohsenin, L. Cheung, and J. A. Madri. 2001. PECAM-1 shedding during apoptosis generates a membrane-anchored truncated molecule with unique signaling characteristics. FASEB J. 15:362-372.
34. Kawaguchi, N., X. Xu, R. Tajima, P. Kronqvist, C. Sundberg, F. Loechel, R. Albrechtsen, and U. M. Wewer. 2002. ADAM 12 protease induces adipogenesis in transgenic mice. Am. J. Pathol. 160:1895-1903.
35. Kim, S., K. Bell, S. A. Mousa, and J. A. Varner. 2000. Regulation of angiogenesis in vivo by ligation of integrin α1β5 with the central cell-binding domain of fibronectin. Am. J. Pathol. 156:1345-1362.
36. Klagsbrun, M., and P. A. D'Amore. 1996. Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev. 7:259-270.
37. Kratzschmar, J., L. Lum, and C. P. Blobel. 1996. Metargidin, a membrane-anchored metalloprotease-disintegrin protein with an RGD integrin binding sequence. J. Biol. Chem. 271:4593-4596.
38. Kronqvist, P., N. Kawaguchi, R. Albrechtsen, X. Xu, H. D. Schroder, B. Moghadaszadeh, F. C. Nielsen, C. Frohlich, E. Engvall, and U. M. Wewer. 2002. ADAM12 alleviates the skeletal muscle pathology in mdx dystrophic mice. Am. J. Pathol. 161:1535-1540.
39. Kurisaki, T., A. Masuda, K. Sudo, J. Sakagami, S. Higashiyama, Y. Matsuda, A. Nagabukuro, A. Tsuji, Y. Nabeshima, M. Asano, Y. Iwakura, and A. Sehara-Fujisawa. 2003. Phenotypic analysis of Meltrin α (ADAM12)-deficient mice: involvement of Meltrin a in adipogenesis and myogenesis. Mol. Cell. Biol. 23:55-61.
40. Leong, K. G., X. Hu, L. Li, M. Noseda, B. Larrivee, C. Hull, L. Hood, F. Wong, and A. Karsan. 2002. Activated Notch4 inhibits angiogenesis: role of β1-integrin activation. Mol. Cell. Biol. 22:2830-2841.
41. Lieber, T., S. Kidd, and M. W. Young. 2002. kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev. 16:209-221.
42. Lum, L., M. S. Reid, and C. P. Blobel. 1998. Intracellular maturation of the mouse metalloprotease disintegrin MDC15. J. Biol. Chem. 273:26236-26247.
43. Manova, K., K. Nocka, P. Besmer, and R. F. Bachvarova. 1990. Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110:1057-1069.
44. Martin, J., L. V. Eynstone, M. Davies, J. D. Williams, and R. Steadman. 2002. The role of ADAM 15 in glomerular mesangial cell migration. J. Biol. Chem. 277:33683-33689.
45. Merlos-Suarez, A., S. Ruiz-Paz, J. Baselga, and J. Arribas. 2001. Metalloprotease-dependent protransforming growth factor-α ectodomain shedding in the absence of tumor necrosis factor-α-converting enzyme. J. Biol. Chem. 276:48510-48517.
46. Mitchell, K. J., K. I. Pinson, O. G. Kelly, J. Brennan, J. Zupicich, P. Scherz, P. A. Leighton, L. V. Goodrich, X. Lu, B. J. Avery, P. Tate, K. Dill, E. Pangilinan, P. Wakenight, M. Tessier- Lavigne, and W. C. Skarnes. 2001. Functional analysis of secreted and transmembrane proteins critical to mouse development. Nat. Genet. 28:241-249.
47. Moss, M. L., S. L. Jin, M. E. Milla, D. M. Bickett, W. Burkhart, H. L. Carter, W. J. Chen, W. C. Clay, J. R. Didsbury, D. Hassler, C. R. Hoffman, T. A. Kost, M. H. Lambert, M. A. Leesnitzer, P. McCauley, G. McGeehan, J. Mitchell, M. Moyer, G. Pahel, W. Rocque, L. K. Overton, F. Schoenen, T. Seaton, J. L. Su, J. D. Becherer, et al. 1997. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-α. Nature 385:733-736.
48. Nath, D., P. M. Slocombe, P. E. Stephens, A. Warn, G. R. Hutchinson, K. M. Yamada, A. J. Docherty, and G. Murphy. 1999. Interaction of metargidin (ADAM-15) with αvβ3 and α5β1 integrins on different haemopoietic cells. J. Cell Sci. 112:579-587.
49. 1 integrin, leading to a marked induction of fibroblast cell motility. J. Cell Sci. 113:2319-2328.
50. Nishimura, H., C. Cho, D. R. Branciforte, D. G. Myles, and P. Primakoff. 2001. Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin β. Dev. Biol. 233:204-213.
51. Pan, D., and G. M. Rubin. 1997. Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90:271-280.
52. Peschon, J. J., J. L. Slack, P. Reddy, K. L. Stocking, S. W. Sunnarborg, D. C. Lee, W. E. Russell, B. J. Castner, R. S. Johnson, J. N. Fitzner, R. W. Boyce, N. Nelson, C. J. Kozlosky, M. F. Wolfson, C. T. Rauch, D. P. Cerretti, R. J. Paxton, C. J. March, and R. A. Black. 1998. An essential role for ectodomain shedding in mammalian development. Science 282:1281-1284.
53. Pierce, E. A., R. L. Avery, E. D. Foley, L. P. Aiello, and L. E. Smith. 1995. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc. Natl. Acad. Sci. USA 92:905-909.
54. Poghosyan, Z., S. M. Robbins, M. D. Houslay, A. Webster, G. Murphy, and D. R. Edwards. 2002. Phosphorylation-dependent interactions between ADAM15 cytoplasmic domain and Src family protein-tyrosine kinases. J. Biol. Chem. 277:4999-5007.
55. Primakoff, P., and D. G. Myles. 2000. The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet. 16:83-87.
56. Qi, H., M. D. Rand, X. Wu, N. Sestan, W. Wang, P. Rakic, T. Xu, and S. Artavanis-Tsakonas. 1999. Processing of the notch ligand delta by the metalloprotease Kuzbanian. Science 283:91-94.
57. Reusch, P., B. Barleon, K. Weindel, G. Martiny-Baron, A. Godde, G. Siemeister, and D. Marme. 2001. Identification of a soluble form of the angiopoietin receptor TIE-2 relased from endothelial cells and present in human blood. Angiogenesis 4:123-131.
58. Robertson, E. J. 1987. Emryo derived stem cell lines, p. 71-112. In E. J. Robertson (ed.), Teratocarcinomas and embryonic stem cells: a practical approach. IRL Press, Oxford, United Kingdom.
59. Rooke, J., D. Pan, T. Xu, and G. M. Rubin. 1996. KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science 273:1227-1231.
60. Sato, H., T. Kinoshita, T. Takino, K. Nakayama, and M. Seiki. 1996. Activation of a recombinant membrane type 1-matrix metalloproteinase (MT1-MMP) by furin and its interaction with tissue inhibitor of metalloproteinases (TIMP)-2. FEBS Lett. 393:101-104.
61. Sato, H., T. Takino, Y. Okada, J. Cao, A. Shinagawa, E. Yamamoto, and M. Seiki. 1994. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370:61-65.
62. Schlondorff, J., and C. P. Blobel. 1999. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J. Cell Sci. 112:3603-3617.
63. Seals, D. F., and S. A. Courtneidge. 2003. The ADAMs familiy of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17:7-30.
64. Shamsadin, R., I. M. Adham, K. Nayernia, U. A. Heinlein, H. Oberwinkler, and W. Engel. 1999. Male mice deficient for germ-cell cyritestin are infertile. Biol. Reprod. 61:1445-1451.
65. Shirakabe, K., S. Wakatsuki, T. Kurisaki, and A. Fujisawa-Sehara. 2001. Roles of Meltrin β/ADAM19 in the processing of neuregulin. J. Biol. Chem. 276:9352-9358.
66. Shirayoshi, Y., Y. Yuasa, T. Suzuki, K. Sugaya, E. Kawase, T. Ikemura, and N. Nakatsuji. 1997. Proto-oncogene of int-3, a mouse Notch homologue, is expressed in endothelial cells during early embryogenesis. Genes Cells 2:213-224.
67. Smith, L. E., E. Wesolowski, A. McLellan, S. K. Kostyk, R. D'Amato, R. Sullivan, and P. A. D'Amore. 1994. Oxygen-induced retinopathy in the mouse. Investig. Ophthalmol. Vis. Sci. 35:101-111.
68. Sotillos, S., F. Roch, and S. Campuzano. 1997. The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs. Development 124:4769-4779.
69. Stephens, L. E., A. E. Sutherland, I. V. Klimanskaya, A. Andrieux, J. Meneses, R. A. Pedersen, and C. H. Damsky. 1995. Deletion of β1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9:1883-1895.
70. Sunnarborg, S. W., C. L. Hinkle, M. Stevenson, W. E. Russell, C. S. Raska, J. J. Peschon, B. J. Castner, M. J. Gerhart, R. J. Paxton, R. A. Black, and D. C. Lee. 2002. Tumor necrosis factor-α converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J. Biol. Chem. 277:12838-12845.
71. Thodeti, C. K., R. Albrechtsen, M. Grauslund, M. Asmar, C. Larsson, Y. Takada, A. M. Mercurio, J. R. Couchman, and U. M. Wewer. 2002. ADAM12/syndecan-4 signaling promotes β 1 integrin-dependent cell spreading through PKCα and RhoA. J. Biol. Chem. 31:9576-9584.
72. Toth, M., S. Hernandez-Barrantes, P. Osenkowski, M. M. Bernardo, D. C. Gervasi, Y. Shimura, O. Meroueh, L. P. Kotra, B. G. Galvez, A. G. Arroyo, S. Mobashery, and R. Fridman. 2002. Complex pattern of membrane type 1 matrix metalloproteinase shedding: regulation by autocatalytic cells surface inactivation of active enzyme. J. Biol. Chem. 277:26340-26350.
73. Uyttendaele, H., J. Ho, J. Rossant, and J. Kitajewski. 2001. Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc. Natl. Acad. Sci. USA 98:5643-5648.
74. Uyttendaele, H., G. Marazzi, G. Wu, Q. Yan, D. Sassoon, and J. Kitajewski. 1996. Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene. Development 122:2251-2259.
75. Wen, C., M. M. Metzstein, and I. Greenwald. 1997. SUP-17, a Caenorhabditis elegans ADAM protein related to Drosophila KUZBANIAN, and its role in LIN-12/NOTCH signalling. Development 124:4759-4767.
76. Weskamp, G., H. Cai, T. A. Brodie, S. Higashyama, K. Manova, T. Ludwig, and C. P. Blobel. 2002. Mice lacking the metalloprotease-disintegrin MDC9 (ADAM9) have no evident major abnormalities during development or adult life. Mol. Cell. Biol. 22:1537-1544.
77. Weskamp, G., J. Kratzschmar, M. S. Reid, and C. P. Blobel. 1996. MDC9, a widely expressed cellular disintegrin containing cytoplasmic SH3 ligand domains. J. Cell Biol. 132:717-726.
78. Yagi, T., Y. Ikawa, K. Yoshida, Y. Shigetani, N. Takeda, I. Mabuchi, T. Yamamoto, and S. Aizawa. 1990. Homologous recombination at c-fyn locus of mouse embryonic stem cells with use of diphtheria toxin A-fragment gene in negative selection. Proc. Natl. Acad. Sci. USA 87:9918-9922.
79. 5 integrin-deficient mice. Development 119:1093-1105.
80. 3. J. Biol. Chem. 273:7345-7350.