Complex interactions at the helix-helix interface stabilize the glycophorin A transmembrane dimer

Journal of Molecular Biology

Volumn 343, Issue 5, 2004, Pages 1487-1497

  Doura, Abigail K ^a   Fleming, Karen G ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

dimerization motif; glycophorin A; GxxxG; helix helix interface; transmembrane helices

Indexed keywords

ALANINE; DIMER; GLYCINE; GLYCOPHORIN A; MUTANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DIMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STABILITY;

EID: 6344236852     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.09.011     Document Type: Article

References (38)

1. G.K. Ackers, and F.R. Smith Effects of site-specific amino acid modification on protein interactions and biological function Annu. Rev. Biochem. 54 1985 597 629
2. J.L. Popot, and D.M. Engelman Membrane protein folding and oligomerization: the two-stage model Biochemistry 29 1990 4031 4037
3. T.P. Creamer, R. Srinivasan, and G.D. Rose Modeling unfolded states of peptides and proteins Biochemistry 34 1995 16245 16250
4. D. Shortle The denatured state (the other half of the folding equation) and its role in protein stability FASEB J. 10 1996 27 34
5. M.A. Lemmon, J.M. Flanagan, J.F. Hunt, B.D. Adair, B.J. Bormann, C.E. Dempsey, and D.M. Engelman Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices J. Biol. Chem. 267 1992 7683 7689
6. W.P. Russ, and D.M. Engelman TOXCAT: a measure of transmembrane helix association in a biological membrane Proc. Natl Acad. Sci. USA 96 1999 863 868
7. K.G. Fleming, A.L. Ackerman, and D.M. Engelman The effect of point mutations on the free energy of transmembrane alpha-helix dimerization J. Mol. Biol. 272 1997 266 275
8. M.A. Lemmon, J.M. Flanagan, H.R. Treutlein, J. Zhang, and D.M. Engelman Sequence specificity in the dimerization of transmembrane alpha-helices Biochemistry 31 1992 12719 12725
9. K.R. MacKenzie, J.H. Prestegard, and D.M. Engelman A transmembrane helix dimer: structure and implications Science 276 1997 131 133
10. D. Langosch, B. Brosig, H. Kolmar, and H.J. Fritz Dimerisation of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator J. Mol. Biol. 263 1996 525 530
11. W.P. Russ, and D.M. Engelman The GxxxG motif: a framework for transmembrane helix-helix association J. Mol. Biol. 296 2000 911 919
12. A. Senes, M. Gerstein, and D.M. Engelman Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions J. Mol. Biol. 296 2000 921 936
13. A.K. Doura, F.J. Kobus, L. Dubrovsky, E. Hibbard, and K.G. Fleming Sequence context modulates the stability of a GxxxG mediated transmembrane helix-helix dimer J. Mol. Biol. 341 2004 991 998
14. W. Liu, M. Eilers, A.B. Patel, and S.O. Smith Helix packing moments reveal diversity and conservation in membrane protein structure J. Mol. Biol. 337 2004 713 729
15. S. Jiang, and I.A. Vakser Shorter side chains optimize helix-helix packing Protein Sci. 13 2004 1426 1429
16. J. Chen, and W.E. Stites Energetics of side chain packing in staphylococcal nuclease assessed by systematic double mutant cycles Biochemistry 40 2001 14004 14011
17. A. Horovitz, and A.R. Fersht Co-operative interactions during protein folding J. Mol. Biol. 224 1992 733 740
18. A.S. Mildvan, D.J. Weber, and A. Kuliopulos Quantitative interpretations of double mutations of enzymes Arch. Biochem. Biophys. 294 1992 327 340
19. J. Wells Additivity of mutational effects in proteins Biochemistry 29 1990 8509 8517
20. K.M. Perry, J.J. Onuffer, M.S. Gittelman, L. Barmat, and C.R. Matthews Long-range electrostatic interactions can influence the folding, stability, and cooperativity of dihydrofolate reductase Biochemistry 28 1989 7961 7968
21. V.J. LiCata, P.M. Dalessio, and G.K. Ackers Single-site modifications of half-ligated hemoglobin reveal autonomous dimer cooperativity within a quaternary T tetramer Proteins: Struct. Funct. Genet. 17 1993 279 296
22. A.A. Fodor, and R.W. Aldrich On evolutionary conservation of thermodynamic coupling in proteins J. Biol. Chem. 279 2004 19046 19050
23. S.M. Green, and D. Shortle Patterns of nonadditivity between pairs of stability mutations in staphylococcal nuclease Biochemistry 32 1993 10131 10139
24. S.M. Green, A.K. Meeker, and D. Shortle Contributions of the polar, uncharged amino acids to the stability of staphylococcal nuclease: evidence for mutational effects on the free energy of the denatured state Biochemistry 31 1992 5717 5728
25. G. Kleiger, R. Grothe, P. Mallick, and D. Eisenberg GXXXG and AXXXA common alpha-helical interaction motifs in proteins, particularly in extremophiles Biochemistry 41 2002 5990 5997
26. K.G. Fleming, and D.M. Engelman Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants Proc. Natl Acad. Sci. USA 98 2001 14340 14344
27. R.A. Melnyk, S. Kim, A.R. Curran, D.M. Engelman, J.U. Bowie, and C.M. Deber The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication J. Biol. Chem. 279 2004 16591 16597
28. J.U. Bowie Helix packing in membrane proteins J. Mol. Biol. 272 1997 780 789
29. J.U. Bowie Helix packing angle preferences Nature Struct. Biol. 4 1997 915 917
30. B.M. Baker, and K.P. Murphy Prediction of binding energetics from structure using empirical parameterization Methods Enzymol. 295 1998 294 315
31. K.P. Murphy Predicting binding energetics from structure: looking beyond DeltaG degrees Med. Res. Rev. 19 1999 333 339
32. S. Faham, D. Yang, E. Bare, S. Yohannan, J.P. Whitelegge, and J.U. Bowie Side-chain contributions to membrane protein structure and stability J. Mol. Biol. 335 2004 297 305
33. M.L. Johnson, J.J. Correia, D.A. Yphantis, and H.R. Halvorson Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques Biophys. J. 36 1981 575 588
34. T.M. Laue, B. Shah, T.M. Ridgeway, and S.L. Pelletier Computer-aided interpretation of analytical sedimentation data for proteins S.E. Harding A.J. Rowe J.C. Horton Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992 Royal Society of Chemistry Cambridge 90 125
35. K.G. Fleming Standardizing the free energy change of transmembrane helix-helix interactions J. Mol. Biol. 323 2002 563 571
36. G. Vriend WHAT IF: a molecular modeling and drug design program J. Mol. Graph. 8 1990 52 56 see also page 29
37. N. Pattabiraman, K.B. Ward, and P.J. Fleming Occluded molecular surface: analysis of protein packing J. Mol. Recogn. 8 1995 334 344
38. K.H. Lee, D. Xie, E. Freire, and L.M. Amzel Estimation of changes in side chain configurational entropy in binding and folding: general methods and application to helix formation Proteins: Struct. Funct. Genet. 20 1994 68 84