Sequence motifs, polar interactions and conformational changes in helical membrane proteins

Current Opinion in Structural Biology

Volumn 13, Issue 4, 2003, Pages 412-417

  Curran, A Rachael ^a   Engelman, Donald M ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; CONFORMATIONAL TRANSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW;

EID: 0042931286     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00102-7     Document Type: Review

References (50)

1. Schlessinger J. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell. 110:2002;669-672.
2. Moriki T., Maruyama H., Maruyama I.N. Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J Mol Biol. 311:2001;1011-1026.
3. Allen S.J., Kim J.M., Khorana H.G., Lu H., Booth P.J. Structure and function in bacteriorhodopsin: the effect of the interhelical loops on the protein folding kinetics. J Mol Biol. 308:2001;423-435.
4. Kim J.M., Booth P.J., Allen S.J., Khorana H.G. Structure and function in bacteriorhodopsin: the role of the interhelical loops in the folding and stability of bacteriorhodopsin. J Mol Biol. 308:2001;409-422.
5. Fleming K.G. Standardizing the free energy change of transmembrane helix-helix interactions. J Mol Biol. 323:2002;563-571.
6. Bowie J.U. Helix packing in membrane proteins. J Mol Biol. 272:1997;780-789.
7. Langosch D., Heringa J. Interaction of transmembrane helices by a knobs-into-holes packing characteristic of soluble coiled coils. Proteins. 31:1998;150-159.
8. Lemmon M.A., Flanagan J.M., Treutlein H.R., Zhang J., Engelman D.M. Sequence specificity in the dimerization of transmembrane alpha-helices. Biochemistry. 31:1992;12719-12725.
9. MacKenzie K.R., Prestegard J.H., Engelman D.M. A transmembrane helix dimer: structure and implications. Science. 276:1997;131-133.
10. Melnyk R.A., Partridge A.W., Deber C.M. Transmembrane domain mediated self-assembly of major coat protein subunits from Ff bacteriophage. J Mol Biol. 315:2002;63-72.
11. Deber C.M., Khan A.R., Li Z., Joensson C., Glibowicka M., Wang J. Val→Ala mutations selectively alter helix-helix packing in the transmembrane segment of phage M13 coat protein. Proc Natl Acad Sci USA. 90:1993;11648-11652.
12. Russ W.P., Engelman D.M. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol. 296:2000;911-919.
13. Senes A., Gerstein M., Engelman D.M. 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.
14. MacKenzie K.R., Engelman D.M. Structure-based prediction of the stability of transmembrane helix-helix interactions: the sequence dependence of glycophorin A dimerization. Proc Natl Acad Sci USA. 95:1998;3583-3590.
15. Eilers M., Patel A.B., Liu W., Smith S.O. Comparison of helix interactions in membrane and soluble alpha-bundle proteins. Biophys J. 82:2002;2720-2736.
16. Adamian L., Liang J. Helix-helix packing and interfacial pairwise interactions of residues in membrane proteins. J Mol Biol. 311:2001;891-907.
17. Adamian L., Jackups R. Jr., Binkowski T.A., Liang J. Higher-order interhelical spatial interactions in membrane proteins. J Mol Biol. 327:2003;251-272.
18. Liu Y, Engelman DM, Gerstein M: Genomic analysis of membrane protein families: abundance and conserved motifs. Genome Biol 2002, 3:research0054.
19. Senes A., Ubarretxena-Belandia I., Engelman D.M. The Calpha - H.O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions. Proc Natl Acad Sci USA. 98:2001;9056-9061 A study of the ability of polar residues to drive TM helix association in a polyleucine sequence context. The data show that asparagine, aspartic acid, glutamine, glutamine and histidine are capable of being both hydrogen-bond donors and acceptors, and suggest that interactions between polar residues in TM domains may provide structural stability and oligomerization specificity.
20. Loll B., Raszewski G., Saenger W., Biesiadka J. Functional role of C(alpha)-H.O hydrogen bonds between transmembrane alpha-helices in photosystem I. J Mol Biol. 328:2003;737-747.
21. Zhou F.X., Merianos H.J., Brunger A.T., Engelman D.M. Polar residues drive association of polyleucine transmembrane helices. Proc Natl Acad Sci USA. 98:2001;2250-2255.
22. Zhou F.X., Cocco M.J., Russ W.P., Brunger A.T., Engelman D.M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat Struct Biol. 7:2000;154-160 A study of the ability of polar residues to drive TM helix association in a polyleucine sequence context. The data show that asparagine, aspartic acid, glutamine, glutamine and histidine are capable of being both hydrogen-bond donors and acceptors, and suggest that interactions between polar residues in TM domains may provide structural stability and oligomerization specificity.
23. Gratkowski H., Lear J.D., DeGrado W.F. Polar side chains drive the association of model transmembrane peptides. Proc Natl Acad Sci USA. 98:2001;880-885 Analytical ultracentrifugation and gel electrophoresis were used to determine the tendency of different amino acids to direct the oligomerization of a model TM helix in a hydrophobic sequence context. The data show that variants with two polar atoms at the guest site (asparagine, glutamine, aspartic acid and glutamic acid) are able to oligomerize.
24. Bass R.B., Strop P., Barclay M., Rees D.C. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science. 298:2002;1582-1587.
25. Dawson J.P., Weinger J.S., Engelman D.M. Motifs of serine and threonine can drive association of transmembrane helices. J Mol Biol. 316:2002;799-805.
26. Adamian L., Liang J. Interhelical hydrogen bonds and spatial motifs in membrane proteins: polar clamps and serine zippers. Proteins. 47:2002;209-218.
27. Partridge A.W., Therien A.G., Deber C.M. Polar mutations in membrane proteins as a biophysical basis for disease. Biopolymers. 66:2002;350-358.
28. Therien A.G., Grant F.E., Deber C.M. Interhelical hydrogen bonds in the CFTR membrane domain. Nat Struct Biol. 8:2001;597-601 Helix-loop-helix constructs corresponding to TM helices from CFTR were studied. It was determined that a polar cystic fibrosis phenotypic mutant was able to form a non-native hydrogen bond with a neighboring helix. The formation of such a hydrogen bond is suggested to compromise the effectiveness of CFTR as a chloride channel.
29. Partridge A.W., Melnyk R.A., Deber C.M. Polar residues in membrane domains of proteins: molecular basis for helix-helix association in a mutant CFTR transmembrane segment. Biochemistry. 41:2002;3647-3653.
30. DiMaio D., Lai C.C., Mattoon D. The platelet-derived growth factor beta receptor as a target of the bovine papillomavirus E5 protein. Cytokine Growth Factor Rev. 11:2000;283-293.
31. Constantinescu S.N., Liu X., Beyer W., Fallon A., Shekar S., Henis Y.I., Smith S.O., Lodish H.F. Activation of the erythropoietin receptor by the gp55-P viral envelope protein is determined by a single amino acid in its transmembrane domain. EMBO J. 18:1999;3334-3347.
32. Petti L.M., Reddy V., Smith S.O., DiMaio D. Identification of amino acids in the transmembrane and juxtamembrane domains of the platelet-derived growth factor receptor required for productive interaction with the bovine papillomavirus E5 protein. J Virol. 71:1997;7318-7327.
33. Nilson L.A., Gottlieb R.L., Polack G.W., DiMaio D. Mutational analysis of the interaction between the bovine papillomavirus E5 transforming protein and the endogenous beta receptor for platelet-derived growth factor in mouse C127 cells. J Virol. 69:1995;5869-5874.
34. Nappi V.M., Schaefer J.A., Petti L.M. Molecular examination of the transmembrane requirements of the platelet-derived growth factor beta receptor for a productive interaction with the bovine papillomavirus E5 oncoprotein. J Biol Chem. 277:2002;47149-47159.
35. Nappi V.M., Petti L.M. Multiple transmembrane amino acid requirements suggest a highly specific interaction between the bovine papillomavirus E5 oncoprotein and the platelet-derived growth factor beta receptor. J Virol. 76:2002;7976-7986.
36. Spencer R.H., Rees D.C. The alpha-helix and the organization and gating of channels. Annu Rev Biophys Biomol Struct. 31:2002;207-233 A useful review focusing on the orientation and packing of α helices in membrane proteins. The paper focuses on channel proteins whose structures have recently been determined.
37. Subramaniam S., Lindahl M., Bullough P., Faruqi A.R., Tittor J., Oesterhelt D., Brown L., Lanyi J., Henderson R. Protein conformational changes in the bacteriorhodopsin photocycle. J Mol Biol. 287:1999;145-161.
38. Lanyi J.K., Schobert B. Mechanism of proton transport in bacteriorhodopsin from crystallographic structures of the K, L, M1, M2, and M2′ intermediates of the photocycle. J Mol Biol. 328:2003;439-450.
39. Lanyi J., Schobert B. Crystallographic structure of the retinal and the protein after deprotonation of the Schiff base: the switch in the bacteriorhodopsin photocycle. J Mol Biol. 321:2002;727-737.
40. + conduction and selectivity. Science. 280:1998;69-77.
41. 2+-ATPase structure in the E1 and E2 conformations: mechanism, helix-helix and helix-lipid interactions. Biochim Biophys Acta. 1565:2002;246-266.
42. + channel: tryptophan scanning and complementation analysis lead to mutants with altered gating. Biochemistry. 41:2002;13653-13662.
43. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:2002;515-522.
44. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., MacKinnon R. The open pore conformation of potassium channels. Nature. 417:2002;523-526 This paper provides a structural comparison of the closed and open states of the potassium channel. The analysis suggests a common structural basis for gating among potassium channels and provides an explanation for the high conduction rates of the channels.
45. Toyoshima C., Nakasako M., Nomura H., Ogawa H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature. 405:2000;647-655.
46. Toyoshima C., Nomura H. Structural changes in the calcium pump accompanying the dissociation of calcium. Nature. 418:2002;605-611.
47. Perozo E., Cortes D.M., Sompornpisut P., Kloda A., Martinac B. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 418:2002;942-948 Electron paramagnetic resonance spectroscopy and site-directed spin labeling have been used to investigate the structural rearrangements that underlie the opening and gating of MscL. A model for the transition from the closed to open states of the channel includes large structural rearrangements of the TM helices.
48. Strop P., Bass R., Rees D.C. Prokaryotic mechanosensitive channels. Adv Protein Chem. 63:2003;177-209.
49. Breyton C., Haase W., Rapoport T.A., Kuhlbrandt W., Collinson I. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature. 418:2002;662-665 A three-dimensional projection map of SecYEG at a resolution of 8 Å is reported. The complex is a dimer, with each monomer containing 15 TM helices. These data represent the highest resolution structure currently available of the bacterial protein translocation complex and provide important insights into how membrane proteins fold.
50. Kuo A., Gulbis J.M., Antcliff J.F., Rahman T., Lowe E.D., Zimmer J., Cuthbertson J., Ashcroft F.M., Ezaki T., Doyle D.A. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science. 300:2003;1922-1926.