A view into the blind spot: Solution NMR provides new insights into signal transduction across the lipid bilayer

Structure

Volumn 18, Issue 12, 2010, Pages 1559-1569

  Call, Matthew E ^a   Chou, James J ^b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; HOMODIMER; INTEGRIN; MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL COMMUNICATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CYTOLOGY; CYTOPLASM; GEOMETRY; LIPID BILAYER; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; SIGNAL TRANSDUCTION; SOLUTIONS;

EID: 78649794988     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.11.002     Document Type: Review

References (74)

1. D. Aivazian, and L.J. Stern Phosphorylation of T cell receptor zeta is regulated by a lipid dependent folding transition Nat. Struct. Biol. 7 2000 1023 1026
2. K.L. Arnett, S.C. Harrison, and D.C. Wiley Crystal structure of a human CD3-epsilon/delta dimer in complex with a UCHT1 single-chain antibody fragment Proc. Natl. Acad. Sci. USA 101 2004 16268 16273
3. J.D. Ashwell, and R.D. Klausner Genetic and mutational analysis of the T-cell antigen receptor Annu. Rev. Immunol. 8 1990 139 167
4. T.H. Bayburt, and S.G. Sligar Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers Protein Sci. 12 2003 2476 2481
5. E.V. Bocharov, K.S. Mineev, P.E. Volynsky, Y.S. Ermolyuk, E.N. Tkach, A.G. Sobol, V.V. Chupin, M.P. Kirpichnikov, R.G. Efremov, and A.S. Arseniev Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state J. Biol. Chem. 283 2008 6950 6956
6. A.W. Burgess, H.S. Cho, C. Eigenbrot, K.M. Ferguson, T.P. Garrett, D.J. Leahy, M.A. Lemmon, M.X. Sliwkowski, C.W. Ward, and S. Yokoyama An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors Mol. Cell 12 2003 541 552
7. M.E. Call, and K.W. Wucherpfennig The T cell receptor: critical role of the membrane environment in receptor assembly and function Annu. Rev. Immunol. 23 2005 101 125
8. M.E. Call, and K.W. Wucherpfennig Common themes in the assembly and architecture of activating immune receptors Nat. Rev. Immunol. 7 2007 841 850
9. M.E. Call, J. Pyrdol, and K.W. Wucherpfennig Stoichiometry of the T-cell receptor-CD3 complex and key intermediates assembled in the endoplasmic reticulum Embo J. 23 2004 2348 2357
10. M.E. Call, K.W. Wucherpfennig, and J.J. Chou The structural basis for intramembrane assembly of an activating immunoreceptor complex Nat. Immunol. 11 2010 1023 1029
11. M.E. Call, J. Pyrdol, M. Wiedmann, and K.W. Wucherpfennig The organizing principle in the formation of the T cell receptor-CD3 complex Cell 111 2002 967 979
12. M.E. Call, J.R. Schnell, C. Xu, R.A. Lutz, J.J. Chou, and K.W. Wucherpfennig The structure of the zetazeta transmembrane dimer reveals features essential for its assembly with the T cell receptor Cell 127 2006 355 368
13. T.J. Cammett, S.J. Jun, E.B. Cohen, F.N. Barrera, D.M. Engelman, and D. Dimaio Construction and genetic selection of small transmembrane proteins that activate the human erythropoietin receptor Proc. Natl. Acad. Sci. USA 107 2010 3447 3452
14. A. Chigaev, T. Buranda, D.C. Dwyer, E.R. Prossnitz, and L.A. Sklar FRET detection of cellular alpha4-integrin conformational activation Biophys. J. 85 2003 3951 3962
15. J.J. Chou, J.D. Kaufman, S.J. Stahl, P.T. Wingfield, and A. Bax Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel J. Am. Chem. Soc. 124 2002 2450 2451
16. P. Cosson, S.P. Lankford, J.S. Bonifacino, and R.D. Klausner Membrane protein association by potential intramembrane charge pairs Nature 351 1991 414 416
17. L.M. Deford-Watts, T.C. Tassin, A.M. Becker, J.J. Medeiros, J.P. Albanesi, P.E. Love, C. Wulfing, and N.S. van Oers The cytoplasmic tail of the T cell receptor CD3 epsilon subunit contains a phospholipid-binding motif that regulates T cell functions J. Immunol. 183 2009 1055 1064
18. D.M. Engelman Electrostatic fasteners hold the T cell receptor-CD3 complex together Mol. Cell 11 2003 5 6
19. J. Feng, D. Garrity, M.E. Call, H. Moffett, and K.W. Wucherpfennig Convergence on a distinctive assembly mechanism by unrelated families of activating immune receptors Immunity 22 2005 427 438
20. B. Garcia-Alvarez, J.M. de Pereda, D.A. Calderwood, T.S. Ulmer, D. Critchley, I.D. Campbell, M.H. Ginsberg, and R.C. Liddington Structural determinants of integrin recognition by talin Mol. Cell 11 2003 49 58
21. K.H. Gardner, and L.E. Kay The use of 2H, 13C, 15N multidimensional NMR to study the structure and dynamics of proteins Annu. Rev. Biophys. Biomol. Struct. 27 1998 357 406
22. J.M. Gluck, M. Wittlich, S. Feuerstein, S. Hoffmann, D. Willbold, and B.W. Koenig Integral membrane proteins in nanodiscs can be studied by solution NMR spectroscopy J. Am. Chem. Soc. 131 2009 12060 12061
23. R.O. Hynes Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
24. N. Jura, N.F. Endres, K. Engel, S. Deindl, R. Das, M.H. Lamers, D.E. Wemmer, X. Zhang, and J. Kuriyan Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment Cell 137 2009 1293 1307
25. A.C. Kalli, K.L. Wegener, B.T. Goult, N.J. Anthis, I.D. Campbell, and M.S. Sansom The structure of the talin/integrin complex at a lipid bilayer: an NMR and MD simulation study Structure 18 2010 1280 1288
26. H.J. Kim, S.C. Howell, W.D. Van Horn, Y.H. Jeon, and C.R. Sanders Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins Prog. Nucl. Magn. Reson. Spectrosc. 55 2009 335 360
27. M. Kim, C.V. Carman, and T.A. Springer Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins Science 301 2003 1720 1725
28. L. Kjer-Nielsen, C.S. Clements, A.G. Brooks, A.W. Purcell, J. McCluskey, and J. Rossjohn The 1.5 A crystal structure of a highly selected antiviral T cell receptor provides evidence for a structural basis of immunodominance Structure 10 2002 1521 1532
29. L. Kjer-Nielsen, M.A. Dunstone, L. Kostenko, L.K. Ely, T. Beddoe, N.A. Mifsud, A.W. Purcell, A.G. Brooks, J. McCluskey, and J. Rossjohn Crystal structure of the human T cell receptor CD3 epsilon gamma heterodimer complexed to the therapeutic mAb OKT3 Proc. Natl. Acad. Sci. USA 101 2004 7675 7680
30. K.F. Kubatzky, W. Liu, K. Goldgraben, C. Simmerling, S.O. Smith, and S.N. Constantinescu Structural requirements of the extracellular to transmembrane domain junction for erythropoietin receptor function J. Biol. Chem. 280 2005 14844 14854
31. M.S. Kuhns, and M.M. Davis The safety on the TCR trigger Cell 135 2008 594 596
32. M.S. Kuhns, M.M. Davis, and K.C. Garcia Deconstructing the form and function of the TCR/CD3 complex Immunity 24 2006 133 139
33. L.L. Lanier DAP10- and DAP12-associated receptors in innate immunity Immunol. Rev. 227 2009 150 160
34. L.L. Lanier, B.C. Corliss, J. Wu, C. Leong, and J.H. Phillips Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells Nature 391 1998 703 707
35. L.L. Lanier, B. Corliss, J. Wu, and J.H. Phillips Association of DAP12 with activating CD94/NKG2C NK cell receptors Immunity 8 1998 693 701
36. T.L. Lau, V. Dua, and T.S. Ulmer Structure of the integrin alphaIIb transmembrane segment J. Biol. Chem. 283 2008 16162 16168
37. T.L. Lau, A.W. Partridge, M.H. Ginsberg, and T.S. Ulmer Structure of the integrin beta3 transmembrane segment in phospholipid bicelles and detergent micelles Biochemistry 47 2008 4008 4016
38. T.L. Lau, C. Kim, M.H. Ginsberg, and T.S. Ulmer The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling EMBO J. 28 2009 1351 1361
39. M.A. Lemmon, and J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 141 2010 1117 1134
40. P.E. Love, and S.M. Hayes ITAM-mediated signaling by the T-cell antigen receptor Cold Spring Harb. Perspect. Biol. 2 2010 a002485
41. C. Lu, J. Takagi, and T.A. Springer Association of the membrane proximal regions of the alpha and beta subunit cytoplasmic domains constrains an integrin in the inactive state J. Biol. Chem. 276 2001 14642 14648
42. B.H. Luo, T.A. Springer, and J. Takagi A specific interface between integrin transmembrane helices and affinity for ligand PLoS Biol. 2 2004 e153
43. B.H. Luo, C.V. Carman, and T.A. Springer Structural basis of integrin regulation and signaling Annu. Rev. Immunol. 25 2007 619 647
44. K.R. Mackenzie Folding and stability of α-helical integral membrane proteins Chem. Rev. 106 2006 1931 1977
45. K.R. MacKenzie, J.H. Prestegard, and D.M. Engelman A transmembrane helix dimer: structure and implications Science 276 1997 131 133
46. N. Manolios, J.S. Bonifacino, and R.D. Klausner Transmembrane helical interactions and the assembly of the T cell receptor complex Science 249 1990 274 277
47. T. Otomo, N. Ito, Y. Kyogoku, and T. Yamazaki NMR observation of selected segments in a larger protein: central-segment isotope labeling through intein-mediated ligation Biochemistry 38 1999 16040 16044
48. K. Pervushin, R. Riek, G. Wider, and K. Wuthrich Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution Proc. Natl. Acad. Sci. USA 94 1997 12366 12371
49. R.M. Pielak, and J.J. Chou Solution NMR structure of the V27A drug resistant mutant of influenza A M2 channel Biochem. Biophys. Res. Commun. 401 2010 58 63
50. T. Raschle, S. Hiller, T.Y. Yu, A.J. Rice, T. Walz, and G. Wagner Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs J. Am. Chem. Soc. 131 2009 17777 17779
51. T. Raschle, S. Hiller, M. Etzkorn, and G. Wagner Nonmicellar systems for solution NMR spectroscopy of membrane proteins Curr. Opin. Struct. Biol. 20 2010 471 479
52. M. Red Brewer, S.H. Choi, D. Alvarado, K. Moravcevic, A. Pozzi, M.A. Lemmon, and G. Carpenter The juxtamembrane region of the EGF receptor functions as an activation domain Mol. Cell 34 2009 641 651
53. L.E. Samelson, J.B. Harford, and R.D. Klausner Identification of the components of the murine T cell antigen receptor complex Cell 43 1985 223 231
54. C.R. Sanders, and R.S. Prosser Bicelles: a model membrane system for all seasons? Struct. Fold. Des. 6 1998 1227 1234
55. J. Schlessinger Ligand-induced, receptor-mediated dimerization and activation of EGF receptor Cell 110 2002 669 672
56. J.R. Schnell, and J.J. Chou Structure and mechanism of the M2 proton channel of influenza A virus Nature 451 2008 591 595
57. S.J. Shattil, C. Kim, and M.H. Ginsberg The final steps of integrin activation: the end game Nat. Rev. Mol. Cell. Biol. 11 2010 288 300
58. A.B. Sigalov, D.A. Aivazian, V.N. Uversky, and L.J. Stern Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling subunits Biochemistry 45 2006 15731 15739
59. L.C. Sullivan, C.S. Clements, T. Beddoe, D. Johnson, H.L. Hoare, J. Lin, T. Huyton, E.J. Hopkins, H.H. Reid, and M.C. Wilce The heterodimeric assembly of the CD94-NKG2 receptor family and implications for human leukocyte antigen-E recognition Immunity 27 2007 900 911
60. J.J. Sussman, J.S. Bonifacino, J. Lippincott-Schwartz, A.M. Weissman, T. Saito, R.D. Klausner, and J.D. Ashwell Failure to synthesize the T cell CD3-zeta chain: structure and function of a partial T cell receptor complex Cell 52 1988 85 95
61. J. Takagi, B.M. Petre, T. Walz, and T.A. Springer Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling Cell 110 2002 599 611
62. E. Tomasello, L. Olcese, F. Vely, C. Geourgeon, M. Blery, A. Moqrich, D. Gautheret, M. Djabali, M.G. Mattei, and E. Vivier Gene structure, expression pattern, and biological activity of mouse killer cell activating receptor-associated protein (KARAP)/DAP-12 J. Biol. Chem. 273 1998 34115 34119
63. A. van Agthoven, C. Terhorst, E. Reinherz, and S. Schlossman Characterization of T cell surface glycoproteins T 1 and T 3 present on all human peripheral T lymphocytes and functionally mature thymocytes Eur. J. Immunol. 11 1981 18 21
64. O. Vinogradova, A. Velyvis, A. Velyviene, B. Hu, T. Haas, E. Plow, and J. Qin A structural mechanism of integrin alpha(IIb)beta(3) "inside-out" activation as regulated by its cytoplasmic face Cell 110 2002 587 597
65. R.R. Vold, R.S. Prosser, and A.J. Deese Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides J. Biomol. NMR 9 1997 329 335
66. A.M. Weljie, P.M. Hwang, and H.J. Vogel Solution structures of the cytoplasmic tail complex from platelet integrin alpha IIb- and beta 3-subunits Proc. Natl. Acad. Sci. USA 99 2002 5878 5883
67. C. Xie, J. Zhu, X. Chen, L. Mi, N. Nishida, and T.A. Springer Structure of an integrin with an alphaI domain, complement receptor type 4 Embo J. 29 2010 666 679
68. J.P. Xiong, T. Stehle, B. Diefenbach, R. Zhang, R. Dunker, D.L. Scott, A. Joachimiak, S.L. Goodman, and M.A. Arnaout Crystal structure of the extracellular segment of integrin alpha Vbeta3 Science 294 2001 339 345
69. C. Xu, E. Gagnon, M.E. Call, J.R. Schnell, C.D. Schwieters, C.V. Carman, J.J. Chou, and K.W. Wucherpfennig Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif Cell 135 2008 702 713
70. J. Yang, Y.Q. Ma, R.C. Page, S. Misra, E.F. Plow, and J. Qin Structure of an integrin alphaIIb beta3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation Proc. Natl. Acad. Sci. USA 106 2009 17729 17734
71. X. Yu, K.D. Sharma, T. Takahashi, R. Iwamoto, and E. Mekada Ligand-independent dimer formation of epidermal growth factor receptor (EGFR) is a step separable from ligand-induced EGFR signaling Mol. Biol. Cell 13 2002 2547 2557
72. X. Zhang, J. Gureasko, K. Shen, P.A. Cole, and J. Kuriyan An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor Cell 125 2006 1137 1149 (Pubitemid 43866200)
73. J. Zhu, C.V. Carman, M. Kim, M. Shimaoka, T.A. Springer, and B.H. Luo Requirement of alpha and beta subunit transmembrane helix separation for integrin outside-in signaling Blood 110 2007 2475 2483
74. 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 alphaIIbbeta3 Mol. Cell 34 2009 234 249