Download PDF
Thromb Haemost 1995; 74(01): 352-359
DOI: 10.1055/s-0038-1642701
Symposium
Platler Glycoproteins and Genetic Disorders
Schattauer GmbH Stuttgart

Platelet lntegrins[§]

Mark H Ginsberg
Department of Vascular Biology, The Scripps Research Institute, La Jolla, CA, USA
,
Xiaoping Du
Department of Vascular Biology, The Scripps Research Institute, La Jolla, CA, USA
,
Timothy E O'Toole
Department of Vascular Biology, The Scripps Research Institute, La Jolla, CA, USA
,
Joseph C Loftus
Department of Vascular Biology, The Scripps Research Institute, La Jolla, CA, USA
› Author Affiliations
Further Information

Publication History

Publication Date:
09 July 2018 (online)

  PDF Download  Permissions and Reprints

§ Publication #9221 -VB from the Scripps Research Institute. Supported by grants from the NIH: HL-48728, HL-31950, AR-27214, and HL-16411.


 

  • References

  • 1 Ginsberg MH, Pierschbacher MD, Ruoslahti E, Marguerie G, Plow EF. Inhibition of fibronectin binding to platelets by proteolytic fragments and synthetic peptides which support fibroblast adhesion. J Biol Chem 1985; 260: 3931-3936
    PubMedGoogle Scholar
  • 2 Pytela RP, Pierschbacher MD, Ginsberg MH, Plow EF, Ruoslahti E. Platelet membrane glycoprotein Ilb/IIIa: Member of a family of Arg-Gly-Asp-specific adhesion receptors. Science 1986; 231: 1559-1562
    CrossrefPubMedGoogle Scholar
  • 3 Plow EF, Loftus J, Levin E, Fair D, Dixon D, Forsyth J, Ginsberg MH. Immunologic relationship between platelet membrane glycopro- tein GPIIb/IIIa and cell surface molecules expressed by a variety of cells. Proc Natl Acad Sci USA 1986; 83: 6002-6006
    CrossrefPubMedGoogle Scholar
  • 4 Ginsberg MH, Loftus JC, Ryckwaert J-J, Pierschbacher MD, Pytela R, Ruoslahti E, Plow EF. Immunochemical and amino-terminal sequence comparison of two cytoadhesins indicates they contain similar or identical beta subunits and distinct alpha subunits. J Biol Chem 1987; 262: 5437-5440
    PubMedGoogle Scholar
  • 5 Hynes RO. Integrins: A family of cell surface receptors. Cell 1987; 48: 549-554
    CrossrefPubMedGoogle Scholar
  • 6 O’Toole TE, Loftus JC, Plow EF, Glass A, Harper J, Ginsberg MH. Efficient surface expression of platelet GPIIb-IIIa requires both subunits. Blood 1989; 74: 14-18
    PubMedGoogle Scholar
  • 7 Ginsberg MH, Loftus JC, Plow EF. Cytoadhesins, integrins, and platelets. Thromb Haemostas 1988; 59: 1-6
    PubMedGoogle Scholar
  • 8 van Kuppevelt TH, Languino LR, Gailit JO, Suzuki S, Ruoslahti E. An alternative cytoplasmic domain of the integrin beta 3 subunit. Proc Natl Acad Sci USA 1989; 86: 5415-5418
    CrossrefPubMedGoogle Scholar
  • 9 Altruda F, Cervella P, Tarone G, Botta C, Balzac F, Stefanuto G, Silengo L. A human integrin beta 1 subunit with a unique cytoplasmic domain generated by alternative mRNA processing. Gene 1990; 95: 261-266
    CrossrefPubMedGoogle Scholar
  • 10 Languino LR, Ruoslahti E. An alternative form of the integrin beta 1 subunit with a variant cytoplasmic domain. J Biol Chem 1992; 267: 7116-7120
    PubMedGoogle Scholar
  • 11 Bray PF, Leung CS, Shuman MA. Human platelets and megakaryocytes contain alternately spliced glycoprotein lib mRNAs. J Biol Chem 1990; 265: 9587-9590
    PubMedGoogle Scholar
  • 12 Hogervorst F, Kuikman I, van Kessel A, Sonnenberg A. Molecular cloning of the human alpha 6 integrin subunit. Alternative splicing of alpha 6 mRNA and chromosomal localization of the alpha 6 and beta 4 genes. Eur J Biochem 1991; 199: 425-433
    CrossrefPubMedGoogle Scholar
  • 13 Solowska J, Guan J, Marcantonio E, Trevithick JE, Buck CA, Hynes RO. Expression of normal and mutant avian integrin subunits in rodent cells. J Cell Biol 1989; 109: 853-861
    CrossrefPubMedGoogle Scholar
  • 14 O’Toole TE, Mandelman D, Forsyth J, Shattil S, Plow EF, Ginsberg MH. Modulation of the affinity of integrin αllhβ3 (GPIIb- IHa) by the cytoplasmic domain of αII5 . Science 1991; 254: 845-847
    CrossrefPubMedGoogle Scholar
  • 15 Kolodziej MA, Vilaire G, Rifat S, Poncz M, Bennett JS. Effect of deletion of glycoprotein lib Exon 28 on the expression of the platelet glycoprotein Ilb/IIIa complex. Blood 1992; 78: 2344-2353
    PubMedGoogle Scholar
  • 16 Nurden AT, Caen JP. An abnormal platelet glycoprotein pattern in three cases of Glanzmann’s thrombasthenia. Br J Haematol 1974; 28: 253-260
    CrossrefPubMedGoogle Scholar
  • 17 Jennings LK, Phillips DR. Purification of glycoproteins lib and III from human platelet plasma membranes and characterization of a calcium-dependent glycoprotein Ilb-HI complex. J Biol Chem 1982; 257: 10458-10466
    PubMedGoogle Scholar
  • 18 Fitzgerald LA, Steiner B, Rail jr. S, Lo S-S, Phillips DR. Protein sequence of endothelial glycoprotein IHa derived from a cDNA clone. Identity with platelet glycoprotein ffla and similarity to “integrin” J Biol Chem 1987; 262: 3936-3939
    PubMedGoogle Scholar
  • 19 Loftus JC, Plow EF, Frelinger AL, III D’Souza SE, Dixon D, Lacy J, Sorge J, Ginsberg MH. Molecular cloning and chemical synthesis of a region of platelet GPIIb involved in adhesive function. Proc Natl Acad Sci USA 1987; 84: 7114-7118
    CrossrefPubMedGoogle Scholar
  • 20 Poncz M, Eisman R, Heidenreich R, Silver S, Vilaire G, Surrey S, Schwartz E, Bennett JS. Structure of the platelet membrane glycoprotein lib. Homology to the alpha subunits of the vitronectin and fibronectin membrane receptors. J Biol Chem 1987; 262: 8476-8482
    PubMedGoogle Scholar
  • 21 Rosa J-P, Bray PF, Gayet O, Johnston GI, Cook RG, Jackson KW, Shuman MA, McEver RP. Cloning of glycoprotein Ilia cDNA from human erythroleukemia cells and localization of the gene to chromosome 17. Blood 1988; 72: 593-600
    PubMedGoogle Scholar
  • 22 Weisel JW, Nagaswami C, Vilaire G, Bennett JS. Examination of the platelet membrane glycoprotein Ilb-IIIa complex and its interaction with fibrinogen and other ligands by electron microscopy. J Biol Chem 1992; 267: 16637-16643
    PubMedGoogle Scholar
  • 23 Nermut MV, Green NM, Eason P, Yamada S, Yamada KM. Electron microscopy and structural model of human fibronectin receptor. EMBO J 1988; 7: 4093-4099
    PubMedGoogle Scholar
  • 24 Carrell NA, Fitzgerald LA, Steiner B, Erickson H, Phillips DR. Structure of human platelet membrane glycoproteins lib and Ilia as determined by electron microscopy. J Biol Chem 1985; 260: 1743-1749
    PubMedGoogle Scholar
  • 25 Du X, Gu M, Weisel J, Nagaswami C, Bennett JS, Bowditch RD, Ginsberg MH. Long-range propagation of conformational changes in integrin aIIb/J3 . J Biol Chem 1993; 268: 23087-23092
    PubMedGoogle Scholar
  • 26 Parise LV, Phillips DR. Platelet membrane glycoprotein Ilb-IIIa complex incorporated into phospholipid vesicles. Preparation and morphology. J Biol Chem 1985; 260: 1750-1756
    PubMedGoogle Scholar
  • 27 Hantgan RR, Braaten JV, Rocco M. Dynamic light scattering studies of allbf33 solution conformation. Biochemistry. 1993 in press
    PubMedGoogle Scholar
  • 28 Calvete JJ, Henschen A, Gonzalez-Rodriguez J. Assignment of disulphide bonds in human platelet GPIIIa. A disulphide pattern for the beta-subunits of the integrin family. Biochem J 1991; 274: 63-71
    CrossrefPubMedGoogle Scholar
  • 29 Calvete JJ, Henschen A, Gonzalez-Rodriguez J. Complete localization of the intrachain disulphide bonds and the N-glycosylation points in the alpha-subunit of human platelet glycoprotein lib. Biochem J 1989; 261: 561-568
    CrossrefPubMedGoogle Scholar
  • 30 Calvete JJ, Arias J, Alvarez M, Lopez MM, Henschen A, Gonzalez-Rodriguez J. Further studies on the topography of human platelet glycoprotein lib. Biochem J 1991; 273: 767-775
    CrossrefPubMedGoogle Scholar
  • 31 Calvete JJ, Alvarez MV, Rivas G, Hew C, Henschen A, Gonzalez-Rodriguez J. Interchain and intrachain disulphide bonds in human platelet glycoprotein lib. Localization of the epitopes for several monoclonal antibodies. Biochem J 1989; 261: 551-560
    CrossrefPubMedGoogle Scholar
  • 32 Calvete JJ, Mann K, Alvarez M, Lopez MM, Gonzales-Rodriguez J. Proteolytic dissection of the isolated platelet fibrinogen receptor, integrin GPIIb/IIIa. Biochem J 1992; 282: 523-532
    CrossrefPubMedGoogle Scholar
  • 33 Calvete JJ, Mann K, Schafer W, Fernandez-Lafuente R, Guisan JM. Proteolytic degradation of the RGD-binding and non-RGD-binding conformers of human platelet integrin glycoprotein Ilb/IIIa: clues for identification of regions involved in the receptor’s activation. Biochem J 1994; 298: 1-7
    CrossrefPubMedGoogle Scholar
  • 34 Rocco M, Spotorno B, Hantgan RR. Modeling the cdIb/33 integrin solution conformation. Prot Sci 1993; 2: 2154-2166
    CrossrefPubMedGoogle Scholar
  • 35 Parise LV, Helgerson SL, Steiner B, Nannizzi L, Phillips DR. Synthetic peptides derived from fibrinogen and fibronectin change the conformation of purified platelet glycoprotein Ilb-IIIa. J Biol Chem 1987; 262: 12597-12602
    PubMedGoogle Scholar
  • 36 Steiner B, Parise L, Leung B, Phillips DR. Ca2+-dependent structural transitions of the platelet glycoprotein Ilb-IIIa complex. J Biol Chem 1991; 266: 14986-14991
    PubMedGoogle Scholar
  • 37 Frelinger III AL, Lam SC, Plow EF, Smith MA, Loftus JC, Ginsberg MH. Occupancy of an adhesive glycoprotein receptor modulates expression of an antigenic site involved in cell adhesion. J Biol Chem 1988; 263: 12397-12402
    PubMedGoogle Scholar
  • 38 Frelinger III AL, Cohen I, Plow EF, Smith MA, Roberts J, Lam SC-T, Ginsberg MH. Selective inhibition of integrin function by antibodies specific for ligand-occupied receptor conformers. J Biol Chem 1990; 265: 6346-6352
    PubMedGoogle Scholar
  • 39 Phillips DR, Agin PP. Platelet plasma membrane glycoproteins. Evidence for the presence of non-equivalent disulfide bonds using non-reduced-reduced two-dimensional gel electrophoresis. J Biol Chem 1977; 252: 2121-2126
    PubMedGoogle Scholar
  • 40 Lam SC T. Isolation and characterization of a chymotryptic fragment of platelet glycoprotein Ilb-IIIa retaining arg-gly-asp binding activity. J Biol Chem 1992; 267: 5649-5655
    PubMedGoogle Scholar
  • 41 Wippler J, Kouns W, Schlaeger EJ, Kuhn H, Hadvary P, Steiner B. The integrin αIIbβ3, platelet glycoprotein Ilb-IIIa, can form a functionally active heterodimer complex without the cysteine-rich repeats of the β3 subunit. J Biol Chem 1994; 269: 8754-8761
    PubMedGoogle Scholar
  • 42 Santoro SA, Lawing Jr. WJ. Competition for related but nonidentical binding sites on the glycoprotein Ilb-IIIa complex by peptides derived from platelet adhesive proteins. Cell 1987; 48: 867-873
    CrossrefPubMedGoogle Scholar
  • 43 Smith JW, Cheresh DA. Integrin (αvβ3)-ligand interaction. Identification of a heterodimeric RGD binding site on the vitronectin receptor. J Biol Chem 1990; 265: 2168-2172
    PubMedGoogle Scholar
  • 44 Smith JW, Cheresh DA. The Arg-Gly-Asp binding domain of the vitronectin receptor. Photoaffmity cross-linking implicates amino acid residues 61-203 of the (3 subunit. J Biol Chem 1988; 263: 18726-18731
    PubMedGoogle Scholar
  • 45 D’Souza SE, Ginsberg MH, Burke TA, Lam SC, Plow EF. Localization of an Arg-Gly-Asp recognition site within an integrin adhesion receptor. Science 1988; 242: 91-93
    CrossrefPubMedGoogle Scholar
  • 46 Fitzgerald LA, Phillips DR. Calcium regulation of the platelet membrane glycoprotein Ilb-IIIa complex. J Biol Chem 1985; 260: 11366-11374
    PubMedGoogle Scholar
  • 47 Pidard D, Didry D, Kunicki T, Nurden AT. Temperature-depen- dent effects of EDTA on the membrane glycoprotein Ilb-IIIa complex and platelet aggregability. Blood 1986; 67: 604-611
    PubMedGoogle Scholar
  • 48 Brass LF, Shattil SJ, Kunicki TJ, Bennett JS. Effect of calcium on the stability of the platelet membrane glycoprotein Ilb-IIIa complex. J Biol Chem 1985; 260: 7875-7881
    PubMedGoogle Scholar
  • 49 Kunicki TJ, Pidard D, Rosa J, Nurden AT. The formation of Ca+ +-dependent complexes of platelet membrane glycoproteins lib and Hla in solution as determined by crossed immunoelectro- phoresis. Blood 1981; 58: 268-277
    PubMedGoogle Scholar
  • 50 Shattil SJ, Brass LF, Bennett JS, Pandhi P. Biochemical and functional consequences of dissociation of the platelet membrane glycoprotein Ilb-IIIa complex. Blood 1985; 66: 92-98
    PubMedGoogle Scholar
  • 51 Buck CA, Shea E, Duggan K, Horwitz AF. Integrin (The CSAT antigen): Functionality requires oligomeric integrity. J Cell Biol 1986; 103: 2421-2428
    CrossrefPubMedGoogle Scholar
  • 52 Loftus JC, O’Toole TE, Plow EF, Glass A, Frelinger A, III Ginsberg MH. A (β3 integrin mutation abolishes ligand binding and alters divalent cation-dependent conformation. Science 1990; 249: 915-918
    CrossrefPubMedGoogle Scholar
  • 53 Bennett BD, Cowley S, Jiang S, London R, Deng B, Grabarek J, Groopman JE, Goeddel DV, Avraham H. Identification and characterization of a novel tyrosine kinase from megakaryocytes. J Biol Chem 1994; 269: 1068-1074
    PubMedGoogle Scholar
  • 54 Andrieux A, Rabiet M, Chapel A, Concord E, Marguerie G. A highly conserved sequence of the Arg-Gly-Asp-binding domain of the integrin beta 3 subunit is sensitive to stimulation. J Biol Chem 1991; 266: 14202-14207
    PubMedGoogle Scholar
  • 55 Calvete JJ, Arias J, Alvarez M, Lopez MM, Henschen A, Gonzalez-Rodriguez J. Further studies on the topography of the N-terminal region of human platelet glycoprotein Ilia. Localization of monoclonal antibody epitopes and the putative fibrinogen-binding sites. Biochem J 1991; 274: 457-463
    CrossrefPubMedGoogle Scholar
  • 56 Wang R, Furihata K, McFarland J, Friedman K, Aster RH, Newman PJ. An amino acid polymorphism within the RGD binding domain of platelet membrane glycoprotein Ilia is responsible for the formation of the pen-a/pen-b alloantigen system. J Clin Invest 1992; 90: 2038-2043
    CrossrefPubMedGoogle Scholar
  • 57 D’Souza SE, Haas TA, Piotrowicz RS, Byers-Ward V, McGrath D, Soule HR, Cierniewski C, Plow E, Smith JW. Ligand and cation binding are dual functions of a discrete segment of the integrin (β3 subunit: Cation displacement is involved in ligand binding. Cell 1994; 79: 659-667
    CrossrefPubMedGoogle Scholar
  • 58 Bajt ML, Loftus JC, Gawaz MP, Ginsberg MH. Characterization of a gain of function mutation of integrin cdIb/33 (platelet (GPIIb-IIIa). J Biol Chem 1992; 267: 22211-22216
    PubMedGoogle Scholar
  • 59 Takada Y, Ylanne J, Mandelman D, Puzon W, Ginsberg MH. A point mutation of integrin β3 subunit blocks binding of α5(βX to fibronectin and invasin but not recruitment to adhesion plaques. J Cell Biol 1992; 119: 913-921
    CrossrefPubMedGoogle Scholar
  • 60 Bajt ML, Goodman T, McGuire SL. β2 (CD 18) is involved in ligand recognition by I domain integrins, LFA-1 (αLβ2 CDlla/ CD 18) and MAC-1 αmβ2 CDllb/CD18). J Biol Chem 1995; 270-270
    PubMedGoogle Scholar
  • 61 Ginsberg MH, Lightsey A, Kunicki T, Kaufman A, Marguerie GA, Plow EF. Divalent cation regulation of the surface orientation of platelet membrane glycoprotein lib: Correlation with fibrinogen binding function and definition of a novel variant of Glanzmann’s thrombasthenia. J Clin Invest 1986; 78: 1103-1111
    CrossrefPubMedGoogle Scholar
  • 62 Kretsinger RH. Structure and evolution of calcium-modulated proteins. CRC Crit Rev Biochem 1980; 8: 119-174
    PubMedGoogle Scholar
  • 63 Pierschbacher MD. Ruoslahti: Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 1984; 309: 30-33
    CrossrefPubMedGoogle Scholar
  • 64 Pierschbacher MD, Ruoslahti E. Variants of the cell recognition site of fibronectin that retain attachment-promoting activity (cell adhe- sion/extracellular matrices/collagen/synthetic peptides). Proc Natl Acad Sci USA 1984; 81: 5985-5988
    CrossrefPubMedGoogle Scholar
  • 65 Ruggeri ZM, Houghten RA, Russell SR, Zimmerman TS. Inhibition of platelet function with synthetic peptides designed to be high- affinity antagonists of fibrinogen binding to platelets (platelet receptors/platelet aggregation/thrombosis). Proc Natl Acad Sci USA 1986; 83: 5708-5712
    CrossrefPubMedGoogle Scholar
  • 66 Humphries MJ, Akiyama SK, Komoriya A, Olden K, Yamada KM. Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion. J Cell Biol 1986; 103: 2637-2647
    CrossrefPubMedGoogle Scholar
  • 67 Komoriya A, Green L, Mervic M, Yamada SS, Yamada KM, Humphries MJ. The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced Type III connecting segment domain of fibronectin is leucine-aspartic acid-valine. J Biol Chem 1991; 266: 15075-15079
    PubMedGoogle Scholar
  • 68 Vonderheide RH, Tedder TF, Springer TA, Staunton DE. Residues within a conserved amino acid motif of domains 1 and 4 of VCAM-1 are required for binding to VLA-4. J Cell Biol 1994; 125: 215-222
    CrossrefPubMedGoogle Scholar
  • 69 Osborn L, Vassallo C, Browning B, Tizard R, Haskard DO, Benjamin CD, Dougas I, Kirchhausen T. Arrangement of domains,and amino acid residues required for binding of vascular cell adhesion molecule-1 to its counter-receptor VLA-4α4β1). J Cell Biol 1994; 124: 601-608
    CrossrefPubMedGoogle Scholar
  • 70 Berendt AR, McDowall A, Craig A, Bates PA, Sternberg MJ E, Marsh K, Newbold Cl, Hogg N. The binding site on ICAM-1 for plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1-binding site. Cell 1992; 68: 71-81
    CrossrefPubMedGoogle Scholar
  • 71 Charo IF, Nannizzi L, Phillips D, Hsu MA, Scarborough RM. Inhibition of fibrinogen binding to GPIIb-IIIa by a GP Ilia peptide. J Biol Chem 1991; 266: 1414-1421
    PubMedGoogle Scholar
  • 72 Steiner B, Trzeciak A, Pfenninger G, Kouns WC. Peptides derived from a sequence within (33 integrin bind to platelet aIIb/J3 (GPIIb- Ila) and inhibit ligand binding. J Biol Chem 1993; 268: 6870-6873
    PubMedGoogle Scholar
  • 73 Bajt ML, Ginsberg MH, Frelinger AL, III Berndt MC, Loftus JC. A spontaneous mutation of integrin cdIb/33 (platelet glycoprotein Ilb-IIIa) helps define a ligand binding site. J Biol Chem 1992; 267: 3789-3794
    PubMedGoogle Scholar
  • 74 Lanza F, Stierle A, Fournier D, Morales M, Andre G, Nurden A, Cazenave J-P. A new variant of Glanzmann’s thrombasthenia (Strasbourg I). Platelets with functionally defective glycoprotein Ilb-IIIa complexes and a glycoprotein Ilia 214Arg^-2i4Trp mutation. J Clin Invest 1992; 89: 1995-2004
    CrossrefPubMedGoogle Scholar
  • 75 Fournier DJ, Kabral A, Castaldi P, Berndt MC. A variant of Glanzmann’s thrombasthenia characterized by abnormal glycoprotein Ilb/IIIa complex formation. Thromb Haemostas 1989; 62: 977-983
    PubMedGoogle Scholar
  • 76 D’Souza SE, Ginsberg MH, Burke TA, Plow EF. The ligand binding site of the platelet integrin receptor GPIIb-IIIa is proximal to the second calcium binding domain of its aloha subunit. J Biol Chem 1990; 265: 3440-3446
    PubMedGoogle Scholar
  • 77 D’Souza SE, Ginsberg MH, Matsueda GR, Plow EF. A discrete sequence in a platelet integrin is involved in ligand recognition. Nature 1991; 350: 66-68
    CrossrefPubMedGoogle Scholar
  • 78 Taylor DB, Gartner T. A peptide corresponding to GPIIba 300-312, a presumptive fibrinogen gamma-chain binding site on the platelet integrin GPIIb/IIIa, inhibits the adhesion of platelets to at least four adhesive ligands. J Biol Chem 1992; 267: 11729-11733
    PubMedGoogle Scholar
  • 79 Gulino D, Boudignon C, Zhang L, Concord E, Rabiet Ml, Marguerie G. Ca(2+)-binding properties of the platelet glycoprotein lib ligand-interacting domain. J Biol Chem 1992; 267: 1001-1007
    PubMedGoogle Scholar
  • 80 Hemler ME. VLA proteins in the integrin family: Structures, functions, and their role on leukocytes. Annu Rev Immunol 1990; 8: 365-400
    CrossrefPubMedGoogle Scholar
  • 81 Shaw SK, Cepek KL, Murphy EA, Russell GJ, Brenner MB, Parker CM. Molecular cloning of the human mucosal lymphocyte integrin aE subunit. Unusual structure and restricted RNA distribution. J Biol Chem 1994; 269: 6016-6025
    PubMedGoogle Scholar
  • 82 Fleming JC, Pahl HL, Gonzalez DA, Smith TF, Tenen DG. Structural analysis of the CD1 lb gene and phylogenetic analysis of the X alpha-integrin gene family demonstrate remarkable conservation of genomic X organization and suggest early diversification during evolution. J Immunol 1993; 150: 480-490
    PubMedGoogle Scholar
  • 83 Hughes AL. Coevolution of the vertebrate integrin alpha- and beta-chain genes. Mol. Biol. Evolution 1992; 9: 216-234
    PubMedGoogle Scholar
  • 84 Larson RS, Corbi AL, Berman L, Springer TA. Primary structure of the leukocyte function-associated molecule-1 a subunit: An integrin with an embedded domain defining a protein superfamily. J Cell Biol 1989; 108: 703-712
    CrossrefPubMedGoogle Scholar
  • 85 Springer TA. Adhesion receptors of the immune system. Nature 1990; 346: 425-434
    CrossrefPubMedGoogle Scholar
  • 86 Bonthron D, Orr E, Mitsock LM, Ginsburg D, Handin R, Orkin SH. Nucleotide sequence of pre-pro-von Willebrand factor cDNA. Nucleic Acids Res 1986; 14: 7125-7127
    CrossrefPubMedGoogle Scholar
  • 87 Shelton-Inloes BB, Titani K, Sadler JE. cDNA sequences for human von Willebrand factor reveal five types of repeated domains and five possible protein sequence polymorphisms. Biochemistry 1986; 25: 3164-3171
    CrossrefPubMedGoogle Scholar
  • 88 Titani K, Kumar S, Takio K, Ericsson L, Wade RD, Ashida K, Walsh K, Chopek MW, Sadler JE, Fujikawa K. Amino acid sequence of human von Willebrand factor. Biochemistry 1986; 25: 3171-3184
    CrossrefPubMedGoogle Scholar
  • 89 Verweij CL, Diergaarde PJ, Hart M, Pannekoek H. Full-length von Willebrand factor (vWF) cDNA encodes a highly repetitive protein considerably larger than the mature vWF subunit. EMBO J 1986; 5: 1839-1847
    PubMedGoogle Scholar
  • 90 Corbi AL, Kishimoto TK, Miller LJ, Springer TA. The human leukocyte adhesion glycoprotein Mac-1 (complement receptor type 3, CDllb) a subunit: Cloning, primary structure, and relation to the integrins, von Willebrand factor and factor B. J Biol Chem 1988; 263: 12403-12411
    PubMedGoogle Scholar
  • 91 Diamond MS, Garcia-Aguilar J, Bickford J, Corbi AL, Springer TA. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CDllb/CD18) for four distinct adhesion ligands. J Cell Biol 1993; 120: 1031-1043
    CrossrefPubMedGoogle Scholar
  • 92 Michishita M, Videm V, Arnaout MA. A novel divalent cationbinding site in the A domain of the α2 integrin CR3 (Cdl lb/CD18) is essential for ligand binding. Cell 1993; 72: 857-867
    CrossrefPubMedGoogle Scholar
  • 93 Kern A, Briesewitz R, Bank I, Marcantonio EE. The role of the I domain in ligand binding of the human integrin ax(3v . J Biol Chem 1994; 269: 22811-22816
    PubMedGoogle Scholar
  • 94 Randi AM, Hogg N. I domain of beta 2 integrin lymphocyte function-associated antigen-1 contains a binding site for ligand intercellular adhesion molecule-1. J Biol Chem 1994; 269: 12395-12398
    PubMedGoogle Scholar
  • 95 Kamata T, Puzon W, Takada Y. Identification of putative ligand binding sites within I domain of integrin α1β2(VLA-2, CD49b/ CD29). J Biol Chem 1994; 269: 9659-9663
    PubMedGoogle Scholar
  • 96 Perkins SJ, Smith KF, Williams SC, Haris PI, Chapman D, Sim RB. The secondary structure of the von Willebrand factor type A domain in factor B of human complement by Fourier transform infrared spectroscopy. Its occurrence in collagen types VI, VII, XII and XIV, the integrins and other proteins by averaged structure predictions. J Mol Biol 1994 238: 104-119
    PubMedGoogle Scholar
  • 97 Kamata T, Takada Y. Collagen directly binds to the I domain of integrin a2(31 (VLA-2, CD49b/CD29) in a divalent cation-independent manner. J Biol Chem. 1994 in press
    PubMedGoogle Scholar
  • 98 Rieu P, Ueda T, Haruta I, Sharma C, Arnaout MA. The a- domain of β2 integrin CR3 (CD22b/DC18) is a receptor for the hookworm-derived neutrophil adhesion inhibition NIF. J Cell Biol 1994; 127: 2081-2091
    CrossrefPubMedGoogle Scholar
  • 99 Kamata T, Takada Y. Direct binding of collagen to the I domain of integrin alpha 2 beta 1 (VLA-2, CD49b/CD29) in a divalent cation-independent manner. J Biol Chem 1994; 269: 26006-26010
    PubMedGoogle Scholar
  • 100 Muchowski PJ, Zhang L, Chang E, Soule HR, Plow EF, Moyle M. Functional interaction between the integrin antagonist neutrophil inhibitory factor and the I domain of CDllb/CD18. J Biol Chem 1994; 269: 26419-26423
    PubMedGoogle Scholar
  • 101 Loftus JC, Smith JW, Ginsberg MH. Integrin-mediated cell adhesion: the extracellular face. J Biol Chem 1994; 269: 25235-25238
    PubMedGoogle Scholar
  • 102 Dransfield I, Cabanas C, Craig A, Hogg N. Divalent cation regulation of the function of the leukocyte integrin LFA-1. J Cell Biol 1992; 116: 219-226
    CrossrefPubMedGoogle Scholar
  • 103 Staatz WD, Rajpara SM, Wayner EA, Carter WG, Santoro SA. The membrane glycoprotein Ia-IIa (VLA-2) complex mediates the Mg++-dependent adhesion of platelets to collagen. J Cell Biol 1989; 108: 1917-1924
    CrossrefPubMedGoogle Scholar
  • 104 Staatz WD, Peters KJ, Santoro SA. Divalent cation-dependent structure in the platelet membrane glycoprotein Ia-IIa (VLA-2) complex. Biochem Biophys Res Commun 1990; 168: 107-113
    CrossrefPubMedGoogle Scholar
  • 105 Shadle PJ, Barondes SH. Adhesion of human platelets to immobilized trimeric collagen. J Cell Biol 1982; 95: 361-365
    CrossrefPubMedGoogle Scholar
  • 106 Li R, Nortamo P, Kantor C, Kovanen P, Timonen T, Gahmberg CG. A leukocyte integrin binding peptide from intercellular adhesion molecule-2 stimulates T cell adhesion and natural killer cell activity. J Biol Chem 1993; 268: 21474-21477
    PubMedGoogle Scholar
  • 107 Ross L, Hassman F, Molony L. Inhibition of Molt-4-endothelial adherence by synthetic peptides from the sequence of ICAM-1. J Biol Chem 1992; 267: 8537-8543
    PubMedGoogle Scholar
  • 108 Staatz WD, Fok KF, Zutter MM, Adams SP, Rodriguez BA, Santoro SA. Identification of a tetrapeptide recognition sequence for the alpha-2 beta-1 integrin in collagen. J Biol Chem 1991; 266: 7363-7367
    PubMedGoogle Scholar
  • 109 Cheng S, Craig W, Mullen D, Tschopp JF, Dixon D, Piersch-bacher MD. Design and synthesis of novel cyclic RGD-containing peptides as highly potent and selective integrin αllhβ3 antagonists. J Med Chem 1994; 37: 1-8
    CrossrefPubMedGoogle Scholar
  • 110 Barbas CF, Languino LR, Smith JW. High-affinity self-reactive human antibodies by design and selection: targeting the integrin ligand binding site. Proc Natl Acad Sci USA 1993; 90: 10003-10007
    CrossrefPubMedGoogle Scholar
  • 111 Greenspoon N, Hershkoviz R, Alon R, Varon D, Shenkman B, Marx G, Federman S, Kapustina G, Lider O. Structural analysis of integrin recognition and the inhibition of integrin-mediated cell functions by novel nonpeptidic surrogates of the Arg-Gly-Asp sequence. Biochemistry 1993; 32: 1001-1008
    CrossrefPubMedGoogle Scholar
  • 112 Horton MA, Dorey EL, Nesbitt SA, Samanen J, Ali F, Stadel JM, Nichols A, Greig R, Helfrich MH. Modulation of vitronectin receptor-mediated osteoclast adhesion by Arg-Gly-Asp peptide analogs: a structure-function analysis. J Bone Miner Res 1993; 8: 239-247
    PubMedGoogle Scholar
  • 113 Koivunen E, Gay D, Ruoslahti E. Selection of peptides binding of the a5 (3{ integrin from phage display library. J Biol Chem 1993; 268: 20205-20210
    PubMedGoogle Scholar
  • 114 Nowlin DM, Gorcsan F, Moscinski M, Chiang S, Lobl TJ, Cardarelli PM. A novel cyclic pentapeptide inhibits alpha 4 beta 1 and alpha 5 beta 1 integrin-mediated cell adhesion. J Biol Chem 1993; 268: 20352-20359
    PubMedGoogle Scholar
  • 115 Alig L, Edenhofer A, Hadvary P, Hurzeler M, Knopp D, Muller M, Steiner B, Trzeciak A, Weller T. Low molecular weight, non-peptide fibrinogen receptor antagonists. J Med Chem 1992; 35: 4393-4407
    CrossrefPubMedGoogle Scholar
  • 116 Bajt ML, Loftus JC. Mutation of a ligand binding domain of integrin. Integral role of oxygenated residues in αllhβ3 (GPIIb-IIIa) receptor function. J Biol Chem 1994; 269: 20913-20919
    PubMedGoogle Scholar
  • 117 Bennett JS, Vilaire G. Exposure of platelet fibrinogen receptors by ADP and epinephrine. J Clin Invest 1979; 64: 1393-1401
    CrossrefPubMedGoogle Scholar
  • 118 Sims PJ, Ginsberg MH, Plow EF, Shattil SJ. Effect of platelet activation on the conformation of the plasma membrane glycoprotein Ilb-IIIa complex. J Biol Chem 1991; 266: 7345-7352
    PubMedGoogle Scholar
  • 119 O’Toole TE, Loftus JC, Du X, Glass A, Ruggeri ZM, Shattil SJ, Plow EF, Ginsberg MH. Affinity modulation of the αllhβ3 integrin (platelet GPIIb-IIIa) is an intrinsic property of the receptor. Cell Reg 1990; 1: 883-893
    PubMedGoogle Scholar
  • 120 Peerschke El, Zucker MB, Grant RA, Egan JJ, Johnson MM. Correlation between fibrinogen binding to human platelets and platelet aggregability. Blood 1980; 55: 841-847
    PubMedGoogle Scholar
  • 121 Marguerie GA, Plow EF, Edgington TS. Human platelets possess an inducible and saturable receptor specific for fibrinogen. J Biol Chem 1979; 254: 5357-5363
    PubMedGoogle Scholar
  • 122 Dustin ML, Springer T. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 1989; 341: 619-624
    CrossrefPubMedGoogle Scholar
  • 123 Fujimoto T, Ohara S, Hawiger J. Thrombin-induced exposure and prostacyclin inhibition of the receptor for factor VUI/von Wille- brand factor on human platelets. J Clin Invest 1982; 69: 1212-1222
    CrossrefPubMedGoogle Scholar
  • 124 Shattil SJ, Brass LF. Induction of the fibrinogen receptor on human platelets by intracellular mediators. J Biol Chem 1987; 262: 992-1000
    PubMedGoogle Scholar
  • 125 Hillery CA, Smyth SS, Parise LV. Phosphorylation of human platelet glycoprotein Ilia (GPIHa). J Biol Chem 1991; 266: 14663-14669
    PubMedGoogle Scholar
  • 126 Shaw LM, Messier JM, Mercurio AM. The activation dependent adhesion of macrophages to laminin involves cytoskeletal anchoring and phosphorylation of the alpha 6 beta 1 integrin. J Cell Biol 1990; 110: 2167-2174
    CrossrefPubMedGoogle Scholar
  • 127 Hogervorst F, Kuikman I, Noteboom E, Sonnenberg A. The role of phosphorylation in activation of the alpha 6A beta 1 laminin receptor. J Biol Chem 1993; 268: 18427-18430
    PubMedGoogle Scholar
  • 128 Shaw LM, Mercurio AM. Regulation of alpha 6 beta 1 integrin laminin receptor function by the cytoplasmic domain of the alpha 6 subunit. J Cell Biol 1993; 123: 1017-1025
    CrossrefPubMedGoogle Scholar
  • 129 Hemler ME, Weitzman JB, Pasqualini R, Kawaguchi S, Kassner P, Berdichevsky FB. Structure, biochemical properties, and biological functions of integrin cytoplasmic domains. In: Integrins: The Biological Problem. Takada Y. ed CRC Press; Boca Raton: 1994. pp. 1-36
    Google Scholar
  • 130 Juliano R. Signal transduction by integrins and its role in the regulation of tumor growth. Cancer Metastasis Rev 1994; 13: 2530-2530
    PubMedGoogle Scholar
  • 131 Sastry SK, Horwitz AF. Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signaling. Curr Opin Cell Biol 1993; 5: 819-831
    CrossrefPubMedGoogle Scholar
  • 132 Damsky C, Werb Z. Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr Biol 1992; 4: 772-781
    CrossrefPubMedGoogle Scholar
  • 133 Ginsberg MH, Du X, Plow EF. Inside-out integrin signalling. Curr Opin Cell Biol 1992; 4: 766-771
    CrossrefPubMedGoogle Scholar
  • 134 Schwartz MA. Transmembrane signalling by integrins. Trends Cell Biol 1992; 2: 304-308
    CrossrefPubMedGoogle Scholar
  • 135 O’Toole TE, Katagiri Y, Faull R, Peter K, Tamura RN, Quaranta V, Loftus JC, Shattil SJ, Ginsberg MH. Integrin cytoplasmic domains mediate inside-out signal transduction. J Cell Biol 1994; 124: 1047-1059
    CrossrefPubMedGoogle Scholar
  • 136 Chen Y, O’Toole T, Ylanne J, Rosa J, Ginsberg MH. A point mutation in the integrin β3 cytoplasmic domain (S752-P) impairs bidirectional signaling through cdIb/33 (platelet glycoprotein Ilb-IIIa). Blood 1994; 84: 1857-1865
    PubMedGoogle Scholar
  • 137 Chen Y, Djaffar I, Pidard D, Steiner B, Cieutat A, Caen JP, Rosa JP. Ser-752 — Pro-mutation in the cytoplasmic domain of integrin β3 subunit and defective activation of platelet integrin cdIb/33 (glycoprotein Ilb-IIIa) in a variant of Glanzmann thrombasthenia. Proc Natl Acad Sci USA 1992; 89: 10169-10173
    CrossrefPubMedGoogle Scholar
  • 138 Chen Y, O’Toole T, Shipley T, Forsyth J, LaFlamme S, Yamada KM, Shattil SJ, Ginsberg MH. “Inside-out” signal transduction inhibited by isolated integrin cytoplasmic domains. J Biol Chem 1994; 269: 18307-18310
    PubMedGoogle Scholar
  • 139 Rojiani MV, Finlay BB, Gray V, Dedhar S. In vitro interaction of a polypeptide homologous to human Ro/SS-A antigen (calreticulin) with a highly conserved amino acid sequence in the cytoplasmic domain of integrin alpha subunits. Biochemistry 1991; 30: 9859-9866
    CrossrefPubMedGoogle Scholar
  • 140 Horwitz A, Duggan K, Buck C, Beckerle MC, Burridge K. Interaction of plasma membrane fibronectin receptor with talin - a transmembrane linkage. Nature 1986; 320: 531-533
    CrossrefPubMedGoogle Scholar
  • 141 Otey CA, Pavalko FM, Burridge K. An interaction between alpha actinin and the beta 1 integrin subunit in vitro. J Cell Biol 1990; 111: 721-729
    CrossrefPubMedGoogle Scholar
  • 142 Schaller MD, Otey CA, Hildebrand JD, Parsons JT. Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domains. Submitted.
    PubMedGoogle Scholar
  • 143 Williams MJ, Hughes PE, O’Toole TE, Ginsberg MH. The inner world of cell adhesion: integrin cytoplasmic domains. Trends Cell Biol 1994; 4: 109-112
    CrossrefPubMedGoogle Scholar
  • 144 Crowe DT, Chiu H, Fong S, Weissman IL. Regulation of the avidity of integrin α7 by the β7 cytoplasmic domain. J Biol Chem 1994; 269: 14411-14418
    PubMedGoogle Scholar
  • 145 Hughes PE, O’Toole TE, Ylanne J, Shattil S, Ginsberg MH. A conserved membrane-proximal region of an integrin cytoplasmic domain specified ligand binding affinity. Submitted.
    PubMedGoogle Scholar
  • 146 Dedbar S. Novel functions for calreticulin: interaction with integrins and modulation of gene expression. Trends Biochem Sci 1994; 19: 269-271
    CrossrefPubMedGoogle Scholar
  • 147 Leung-Hagesteijn CY, Milankov K, Michalak M, Wilkins J, Dedhar S. Cell attachment to extracellular matrix substrates is inhibited upon downregulation of expression of calreticulin, an intracellular integrin a-subunit-binding protein. J Cell Sci 1994; 107: 589-600
    PubMedGoogle Scholar
  • 148 Lenter M, Vestweber D. The integrin chains β{ and α6 associate with the chaperone calnexin prior to integrin assembly. J Biol Chem 1994; 269: 12263-12268
    PubMedGoogle Scholar
  • 149 Otey CA, Schaller MD, Parsons JT. Characterization of the binding site for focal adhesion kinase on the 0j integrin subunit. Mol Biol Cell 1995; (Suppl. 05) Suppl 66 a
    PubMedGoogle Scholar
  • 150 Cobb BS, Schaller MD, Leu T, Parsons JT. Stable association of pp60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, ppl25FAK. Mol Cell Biol 1994; 14: 147-155
    CrossrefPubMedGoogle Scholar
  • 151 Chen H, Guan J. Association of focal adhesion kinase with its potential substrate phosphatidyl inositol 3-kinase. Proc Natl Acad Sci USA 1994; 91: 10148-10152
    CrossrefPubMedGoogle Scholar
  • 152 Schlaepfer DD, Hanks SK, Hunter T, van der Geer P. Integrin- mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 1994; 372: 786-791
    CrossrefPubMedGoogle Scholar
  • 153 Muir TW, Williams MJ, Ginsberg MH, Kent SB H. Design and chemical synthesis of a neoprotein structural model for the cytoplasmic domain of a multisubunit cell-surface receptor: integrin cdIb/J3 (platelet GPIIb-IIIa). Biochemistry 1994; 33: 7701-7708
    CrossrefPubMedGoogle Scholar
  • 154 LaFlamme SE, Akiyama SK, Yamada KM. Regulation of fibro- nectin receptor distribution. J Cell Biol 1992; 117: 437-447
    CrossrefPubMedGoogle Scholar
  • 155 Lukashev ME, Sheppard D, Pytela R. Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed 01 integrin cytoplasmic domain. J Biol Chem 1994; 269: 18311-18314
    PubMedGoogle Scholar
  • 156 Akiyama SK, Yamada SS, Yamada KM, LaFlamme SE. Trans-membrane signal transduction by integrin cytoplasmic domains expressed in single-subunit chimeras. J Biol Chem 1994; 269: 15961-15964
    PubMedGoogle Scholar
  • 157 Ylanne J, Chen Y, O’Toole T, Loftus JC, Takada Y, Ginsberg MH. Distinct functions of integrin α and β subunit cytoplasmic domains in cell spreading and formation of focal adhesions. J Cell Biol 1993; 122: 223-233
    CrossrefPubMedGoogle Scholar
  • 158 Briesewitz R, Kern A, Marcantonio EE. Ligand-dependent and independent integrin focal contact localization: the role of the a chain cytoplasmic domain. Mol Biol Cell 1993; 4: 593-604
    CrossrefPubMedGoogle Scholar
  • 159 Du X, Plow E, Frelinger AL, III O’Toole TE, Loftus JC, Ginsberg MH. Ligands “activate” integrin αIIbβ3 (platelet GPIIb- IIIa). Cell 1991; 65: 409-416
    CrossrefPubMedGoogle Scholar
  • 160 Smyth SS, Parise LV. Regulation of ligand binding to glycoprotein Ilb-IIIa (integrin allb03) in isolated platelet membranes. Biochem J 1993; 292: 749-758
    CrossrefPubMedGoogle Scholar
  • 161 Frelinger AL, III Du X, Plow EF, Ginsberg MH. Monoclonal antibodies to ligand-occupied conformers of integrin αIIbβ3 (Glyco protein Ilb-IIIa) alter receptor affinity, specificity, and function. J Biol Chem 1991; 266: 17106-17111
    PubMedGoogle Scholar
  • 162 Neugebauer KM, Reichardt LF. Cell-surface regulation of B1 integrin activity on developing retinal neurons. Nature 1991; 350: 68-71
    CrossrefPubMedGoogle Scholar
  • 163 Kovach NL, Carlos TM, Yee E, Harlan JM. A monoclonal antibody to β1 integrin (CD29) stimulates VLA-dependent adherence of leukocytes to human umbilical vein endothelial cells and matrix components. J Cell Biol 1992; 116: 499-509
    CrossrefPubMedGoogle Scholar
  • 164 van de Wiel-van Kemenade E, van Kooyk Y, de Boer A, Huijbens RJ F, Weder P, van de Kasteele W, Melief CJ M, Figdor CG. Adhesion of T and B lymphocytes to extracellular matrix and endothelial cells can be regulated through the beta subunit of VLA. J Cell Biol 1992; 117: 461-470
    CrossrefPubMedGoogle Scholar
  • 165 Faull RJ, Kovach NL, Harlan JM, Ginsberg MH. Affinity modulation of integrin α5β1 regulation of the functional response by soluble fibronectin. J Cell Biol 1993; 121: 155-162
    CrossrefPubMedGoogle Scholar
  • 166 Conforti G, Zanetti A, Pasquali-Ronchetti I, Quaglino jr. D, Neyroz P, Dejana E. Modulation of vitronectin receptor binding by membrane lipid composition. J Biol Chem 1990; 265: 4011-4019
    PubMedGoogle Scholar
  • 167 Smyth SS, Hillery CA, Parise LV. Fibrinogen binding to purified platelet glycoprotein Ilb-IIIa (integrin αIIbβ3) is modulated by lipids. J Biol Chem 1992; 287: 15588-15577
    PubMedGoogle Scholar
  • 168 Lam SC, Plow EF, D’Souza SE, Cheresh DA, Frelinger AL, III Ginsberg MH. Isolation and characterization of a platelet mem-brane protein related to the vitronectin receptor. J Biol Chem 1989; 264: 3742-3749
    PubMedGoogle Scholar
  • 169 Coller BS, Seligsohn U, West S, Scudder LE, Norton KJ. Platelet fibrinogen and vitronectin in Glanzmann thrombasthenia: evidence consistent with specific roles for glycoprotein Ilb/IIIA and alpha v beta 3 integrins in platelet protein trafficking. Blood 1991; 78: 2603-2610
    PubMedGoogle Scholar
  • 170 Schwartz MA, Denninghoff K. αv integrins mediate the rise in intracellular calcium in endothelial cells on fibronectin even though they play a minor role in adhesion. J Biol Chem 1994; 269: 11133-11137
    PubMedGoogle Scholar
  • 171 Kunicki TJ, Nugent DJ, Staats SJ, Orchekowski RP, Wayner EA, Carter WG. The human fibroblast class II extracellular matrix receptor mediates platelet adhesion to collagen and is identical to the platelet glycoprotein Ia-IIa complex. J Biol Chem 1988; 263: 4516-4519
    PubMedGoogle Scholar
  • 172 Sonnenberg A, Modderman P, Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature 1988; 336: 487-489
    CrossrefPubMedGoogle Scholar
  • 173 Piotrowicz RS, Orchekowski RP, Nugent DJ, Yamada KY, Kunicki TJ. Glycoprotein Ic-IIa functions as an activation- independent fibronectin receptor on human platelets. J Cell Biol 1988; 106: 1359-1364
    CrossrefPubMedGoogle Scholar
  • 174 Lipfert L, Haimovich B, Schaller M, Cobb BS, Parsons JT, Brugge JS. Integrin-dependent phosphorylation and activation of the protein tyrosine kinase ppl25FAK in platelets. J Cell Biol 1992; 119: 905-912
    CrossrefPubMedGoogle Scholar
  • 175 Kim S, Prive G, Yeh J, Scott WG, Milburn MV. A model for transmembrane signaling in a bacterial chemotaxis receptor. Cold Spring Harbor Symposium 1992; 57: 17-24
    CrossrefPubMedGoogle Scholar
  • 176 Stoddard BL, Biemann H-P, Koshland jr DE. Receptors and transmembrane signalling. Cold Spring Harbor Symposium 1992; 57: 1-15
    CrossrefPubMedGoogle Scholar