The glycophorin A transmembrane sequence within integrin αvβ3 creates a non-signaling integrin with low basal affinity that is strongly adhesive under force

Journal of Molecular Biology

Volumn 425, Issue 16, 2013, Pages 2988-3006

  Müller, Martina A ^a   Opfer, Jan ^b   Brunie, Leonora ^a   Volkhardt, Lilli A ^a   Sinner, Eva Kathrin ^c   Boettiger, David ^d   Bochen, Alexander ^a   Kessler, Horst ^a,e   Gottschalk, Kay Eberhard ^b   Reuning, Ute ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF ULM   (Germany)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

cell adhesion; cell migration and signaling; integrin activation; integrin conformation; integrin transmembrane domain

Indexed keywords

GLYCOPHORIN A; LIGAND; VITRONECTIN RECEPTOR;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL MOTILITY; CHIMERA; CONTROLLED STUDY; FOCAL ADHESION; FORCE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR AFFINITY; RECEPTOR BINDING; WILD TYPE;

EID: 84880917957     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.05.020     Document Type: Article

References (55)

1. M.J. Humphries Integrin structure Biochem. Soc. Trans. 28 2000 311 339
2. R.O. Hynes Integrins: bidirectional, allosteric signaling machines Cell 110 2002 673 687 (Pubitemid 35283958)
3. S. Tadokoro, S.J. Shattil, K. Eto, V. Tai, R.C. Liddington, and J.M. de Pereda Talin binding to integrin β-tails: a final common step in integrin activation Science 302 2003 103 106 (Pubitemid 37210697)
4. D.S. Harburger, and D.A. Calderwood Integrin signalling at a glance J. Cell Sci. 122 2009 159 163
5. K.E. Gottschalk, P.D. Adams, A.T. Brunger, and H. Kessler Transmembrane signal transduction of the alpha(IIb)beta(3) integrin Protein Sci. 11 2002 1800 1812 (Pubitemid 34663559)
6. M. Hoefling, H. Kessler, and K.E. Gottschalk The transmembrane structure of integrin αIIbβ3: significance for signal transduction Angew. Chem. Int. Ed Engl. 48 2009 6590 6593
7. T.L. Lau, C. Kim, M.H. Ginsberg, and T.S. Ulmer The structure of the integrin αIIbβ3 transmembrane complex explains integrin transmembrane signalling EMBO J. 28 2009 1351 1361
8. R.R. Hantgan, C. Paumi, M. Rocco, and J.W. Weisel Effects of ligand-mimetic peptides Arg-Gly-Asp-X (X = Phe, Trp, Ser) on αIIbβ3 integrin conformation and oligomerization Biochemistry 38 1999 14461 14474
9. T. Xiao, J. Takagi, B.S. Coller, J.H. Wang, and T.A. Springer Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics Nature 432 2004 59 67 (Pubitemid 39490825)
10. J. Zhu, B.H. Luo, P. Barth, J. Schonbrun, D. Baker, and T.A. Springer The structure of a receptor with two associating transmembrane domains on the cell surface: integrin αIIbβ3 Mol. Cell 34 2009 234 249
11. M.A. Lemmon, J.M. Flanagan, J.F. Hunt, B.D. Adair, B.J. Bormann, and C.E. Dempsey Glycophorin A dimerization is driven by specific interactions between transmembrane α-helices J. Biol. Chem. 267 1992 7683 7689
12. A. Senes, D.E. Engel, and W.F. DeGrado Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs Curr. Opin. Struct. Biol. 14 2004 465 479 (Pubitemid 39094354)
13. D. Lössner, C. Abou-Ajram, A. Benge, M. Aumercier, M. Schmitt, and U. Reuning Integrin αvβ3 upregulates integrin-linked kinase expression in human ovarian cancer cells via enhancement of ILK gene transcription J. Cell. Physiol. 220 2009 367 375
14. S. Hapke, H. Kessler, B. Luber, A. Benge, P. Hutzler, and H. Höfler Ovarian cancer cell proliferation and motility is induced by engagement of integrin αvβ3/vitronectin interaction Biol. Chem. 384 2003 1073 1083 (Pubitemid 37062968)
15. D. Lössner, C. Abou-Ajram, A. Benge, and U. Reuning Integrin αvβ3 mediates upregulation of epidermal growth-factor receptor expression and activity in human ovarian cancer cells Int. J. Biochem. Cell Biol. 40 2008 2746 2761
16. C. Mas-Moruno, F. Rechenmacher, and H. Kessler Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation Anticancer Agents Med Chem. 10 2010 753 768
17. A. Capes-Davis, G. Theodosopoulos, I. Atkin, H.G. Drexler, A. Kohara, and R.A. MacLeod Check your cultures! A list of cross-contaminated or misidentified cell lines Int. J. Cancer 127 2010 1 8
18. M.A. Lemmon, J.M. Flanagan, H.R. Treutlein, J. Zhang, and D.M. Engelman Sequence specificity in the dimerization of transmembrane α-helices Biochemistry 31 1992 12719 12725 (Pubitemid 23027049)
19. U.J. Landegren Measurement of cell numbers by means of the endogenous enzyme hexosaminidase. Applications to detection of lymphokines and cell surface antigens Immunol. Methods 67 1984 379 388
20. S. Hapke, H. Kessler, N. Arroyo de Prada, A. Benge, M. Schmitt, E. Lengyel, and U. Reuning Integrin αvβ3/vitronectin interaction affects expression of the urokinase system in human ovarian cancer cells J. Biol. Chem. 276 2001 26340 26348
21. J. Helenius, C.P. Heisenberg, H.E. Gaub, and D.J. Muller Single-cell force spectroscopy J. Cell Sci. 121 2008 1785 1791 (Pubitemid 351943371)
22. J. Schmitz, M. Benoit, and K.E. Gottschalk The viscoelasticity of membrane tethers and its importance for cell adhesion Biophys. J. 95 2008 1448 1459
23. D. Boettiger Quantitative measurements of integrin-mediated adhesion to extracellular matrix Methods Enzymol. 426 2007 1 25
24. A.J. Garcia, P. Ducheyne, and D. Boettiger Quantification of cell adhesion using a spinning disc device and application to surface-reactive materials Biomaterials 18 1997 1091 1098 (Pubitemid 27342984)
25. D. Boettiger, F. Huber, L. Lynch, and S. Blystone Activation of αvβ3-vitronectin binding is a multistage process in which increases in bond strength are dependent on Y747 and Y759 in the cytoplasmic domain of beta3 Mol. Biol. Cell 12 2001 1227 1237 (Pubitemid 33044407)
26. Q. Shi, and D. Boettiger A novel mode for integrin-mediated signaling: tethering is required for phosphorylation of FAK Y397 Mol. Biol. Cell 14 2003 4306 4315 (Pubitemid 37186330)
27. A.J. Engler, M. Chan, D. Boettiger, and J.E. Schwarzbauer A novel mode of cell detachment from fibrillar fibronectin matrix under shear J. Cell Sci. 122 2009 1647 1653
28. R.K. Assoian, and X. Zhu Cell anchorage and the cytoskeleton as partners in growth factor dependent cell cycle progression Curr. Opin. Cell Biol. 9 1997 93 98 (Pubitemid 27065114)
29. L. Moro, M. Venturino, C. Bozzo, L. Silengo, F. Altruda, and L. Beguinot Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival EMBO J. 17 1998 6622 6632 (Pubitemid 28521796)
30. B. Dummler, and B.A. Hemmings Physiological roles of PKB/Akt isoforms in development and disease Biochem. Soc. Trans. 35 2007 231 235 (Pubitemid 46596476)
31. K.A. Higgins, J.R. Perez, T.A. Coleman, K. Dorshkind, W.A. McComas, and U.M. Sarmiento Antisense inhibition of the p65 subunit of NF-kappa B blocks tumorigenicity and causes tumor regression Proc. Natl Acad. Sci USA 90 1993 9901 9905 (Pubitemid 23328218)
32. J.A. Sokoloski, A.C. Sartorelli, C.A. Rosen, and R. Narayanan Antisense oligonucleotides to the p65 subunit of NF-kappa B block CD11b expression and alter adhesion properties of differentiated HL-60 granulocytes Blood 82 1993 625 632 (Pubitemid 23206131)
33. M. Yebra, E.J. Filardo, E.M. Bayna, E. Kawahara, J.C. Becker, and D.A. Cheresh Induction of carcinoma cell migration on vitronectin by NF-κB-dependent gene expression Mol. Biol. Cell 6 1995 841 850
34. M. Fuortes, W.W. Jin, and C. Nathan Beta 2 integrin-dependent tyrosine phosphorylation of paxillin in human neutrophils treated with tumor necrosis factor J. Cell Biol. 127 1994 1477 1483 (Pubitemid 24362577)
35. I.L. Graham, D.C. Anderson, V.M. Holers, and E.J. Brown Complement receptor 3 (CR3, Mac-1, integrin αMβ2, CD11b/CD18) is required for tyrosine phosphorylation of paxillin in adherent and nonadherent neutrophils J. Cell Biol. 127 1994 1139 1147
36. X. Zhou, J. Li, and D.F. Kucik The microtubule cytoskeleton participates in control of β2-integrin avidity J. Biol. Chem. 276 2001 44762 44769
37. B.D. Adair, and M. Yeager Three-dimensional model of the human platelet integrin αIIbβ3 based on electron cryomicroscopy and x-ray crystallography Proc. Natl Acad. Sci. USA 99 2002 14059 14064 (Pubitemid 35257624)
38. K.E. Gottschalk, and H. Kessler A computational model of transmembrane integrin clustering Structure 12 2004 1109 1116 (Pubitemid 38748782)
39. R. Li, R. Gorelik, V. Nanda, P.B. Law, J.D. Lear, and W.F. DeGrado Dimerization of the transmembrane domain of integrin αIIb subunit in cell membranes J. Biol. Chem. 279 2004 26666 26673 (Pubitemid 38798824)
40. D. Schneider, and D.M. Engelman Involvement of transmembrane domain interactions in signal transduction by alpha/beta integrins J. Biol. Chem. 279 2004 9840 9846 (Pubitemid 38372582)
41. P.E. Hughes, F. Diaz-Gonzalez, L. Leong, C. Wu, J.A. McDonald, and S.J. Shattil Breaking the integrin hinge. A defined structural constraint regulates integrin signaling J. Biol. Chem. 271 1996 6571 6574
42. C. Kim, F. Ye, and M.H. Ginsberg Regulation of integrin activation Annu. Rev. Cell Dev. Biol. 27 2011 321 345
43. R. Li, N. Mitra, H. Gratkowski, G. Vilaire, R. Litvinov, and C. Nagasami Activation of integrin αIIbβ3 by modulation of transmembrane helix associations Science 300 2003 795 798 (Pubitemid 36532114)
44. B.H. Luo, C.V. Carman, J. Takagi, and T.A. Springer Disrupting integrin transmembrane domain heterodimerization increases ligand binding affinity, not valency or clustering Proc. Natl Acad. Sci. USA 102 2005 3679 3684 (Pubitemid 40354671)
45. J.P. Xiong, T. Stehle, R. Zhang, A. Joachimiak, M. Frech, S.L. Goodman, and M.A. Arnaout Crystal structure of the extracellular segment of integrin alphaVbeta3 in complex with an Arg-Gly-Asp ligand Science 296 2002 151 155 (Pubitemid 34280076)
46. M. Moser, K.R. Legate, R. Zent, and R. Fässler The tail of integrins, talin, and kindlins Science 324 2009 895 899
47. J. Zhu, B.H. Luo, T. Xiao, C. Zhang, N. Nishida, and T.A. Springer Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces Mol. Cell 32 2008 849 861
48. G.I. Bell Models for the specific adhesion of cells to cells Science 200 1978 618 627
49. E. Evans, and K. Ritchie Dynamic strength of molecular adhesion bonds Biophys. J. 72 1997 1541 1555 (Pubitemid 27133095)
50. J. Schmitz, and K.E. Gottschalk Mechanical regulation of cell adhesion Soft Matter 4 2008 1373 1387 (Pubitemid 351875590)
51. A. Huttenlocher, and A.R. Horwitz Integrins in cell migration Cold Spring Harb. Perspect. Biol. 3 2011 a005074
52. R. Alon, and M.L. Dustin Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells Immunity 26 2007 17 27 (Pubitemid 46109349)
53. D.M. Rose, R. Alon, and M.H. Ginsberg Integrin modulation and signaling in leukocyte adhesion and migration Immunol. Rev. 218 2007 126 134 (Pubitemid 47052306)
54. V. Beck, H. Herold, A. Benge, B. Luber, P. Hutzler, and H. Tschesche ADAM15 decreases integrin αvβ3/vitronectin-mediated ovarian cancer cell adhesion and motility in an RGD-dependent fashion Int. J. Biochem. Cell. Biol. 37 2005 590 603 (Pubitemid 40022936)
55. J. Opfer, and K.E. Gottschalk Identifying discrete states of a biological system using a novel step detection algorithm PLoS One 7 2012 e45896