A simple method for modeling transmembrane helix oligomers

Journal of Molecular Biology

Volumn 329, Issue 4, 2003, Pages 831-840

  Kim, Sanguk ^a   Chamberlain, Aaron K ^a   Bowie, James U ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Glycophorin A, neu, erbB 2, M2, phospholamban; Membrane protein; Modeling; Monte Carlo optimization; Structure prediction

Indexed keywords

GLYCOPHORIN A; MEMBRANE PROTEIN; OLIGOMER; PHOSPHOLAMBAN; PROTEIN;

ANALYTIC METHOD; ARTICLE; CELL HETEROGENEITY; CHEMICAL MODEL; DATA ANALYSIS; DNA HELIX; EXPERIMENTAL TEST; PARTICLE SIZE; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE;

HOMO;

EID: 0038730774     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00521-7     Document Type: Article

References (54)

1. White S.H., Wimley W.C. Hydrophobic interactions of peptides with membrane interface. Biochim. Biphys. Acta. 1376:1998;339-352.
2. White S.H., Wimley W.C. Membrane protein folding and stability: physical priciples. Annu. Rev. Biophys. Biomol. Struct. 28:1999;319-365.
3. Kim S., Cross T.A. Uniformity, ideality and hydrogen bonds in transmembrane α helices. Biophys. J. 83:2002;2084-2095.
4. Bowie J.U. Helix-bundle membrane protein fold temPlate. Protein Sci. 8:1999;2711-2719.
5. Popot J.-L., Engelman D.M. Membrane protein folding and oligomerization: the two-stage model. Biochemistry. 29:1990;4037-4041.
6. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., et al. Structural determinants of water permeation through aquaporin-1. Nature. 407:2000;599-605.
7. Dutzler R., Campbell E.B., Cadene M., Chait B.T., MacKinnon R. X-ray structure of a CIC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature. 415:2002;287-294.
8. Pappu R.V., Marshall G.R., Ponder J.W. A potential smoothing algorithm accurately predict transmembrane helix packing. Nature Struct. Biol. 6:1999;50-55.
9. Adams P.D., Engelman D.M., Brunger A.T. Improved prediction for the structure of the dimeriic transmembrane domain of glycophorin A obtained through global searching. Proteins: Struct. Funct. Genet. 26:1995;257-261.
10. + channel. J. Mol. Biol. 286:1999;951-962.
11. Adams P.D., Arkin I.T., Engelman D.M., Brunger A.T. Computational searching and mutagenesis suggest a structure for the pentameric transmembrane domain of phospholamban. Nature Struct. Biol. 2:1996;154-162.
12. Shortle D., Simons K.T., Baker D. Clustering of low-energy conformations near the native structures of small proteins. Proc. Natl Acad. Sci. USA. 95:1998;11158-11162.
13. Tomita M., Furthmaryr H., Marchesi V.T. Primary structure of human erythrocyte glycophorin A. Isolation and characterization of peptide and complete amino acid sequence. Biochemistry. 17:1978;4756-4770.
14. MacKenzi K.R., Prestegard J.H., Engelman D.M. A transmembrane helix dimer: structure and implication. Science. 276:1997;131-133.
15. Smith S.O., Song D., Shekar S., Groesbeek M., Ziliox M., Aimoto S. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry. 40:2001;6553-6558.
16. Dunbrack R.L., Karplus M. Backbone-dependent rotamer library for proteins: application to side-chain prediction. J. Mol. Biol. 230:1993;543-574.
17. Bargmann C.I., Weinberg R.A. Oncogenic activation of the neu-encoded receptor protein by point mutation and deletion. EMBO J. 7:1988;2043-2052.
18. Stern D.F., Kamps M.P., Cao H. Oncogenic activation of p185neu stimulates tyrosine phosphorylation in vivo. Mol. Cell. Biol. 8:1988;3969-3973.
19. * activation. EMBO J. 11:1992;923-932.
20. Smith S.O., Smith C.S., Bormann B.J. Strong hydrogen bonding interactions involving a buried glutamic acid in the transmembrane sequence of the neu/erbB-2 receptor. Nature Struct. Biol. 3:1996;252-258.
21. Smith S.O., Smith C., Shekar S., Peersen O., Ziliox M., Aimoto S. Transmembrane interactions in the activation of the neu receptor tyrosine kinase. Biochemistry. 41:2002;9321-9332.
22. Segatto O., King C.R., Pierce J.H., Di fiore P.P., Aaronson S.A. Different structural alterations upregulated in vivo tyrosine kinase activity and transforming potency of erbB-2 gene. Mol. Cell. Biol. 8:1988;5570-5574.
23. Mendrola J.M., Berger M.B., King M.C., Lemmon M.A. The single transmembrane domains of erbB receptors self-associate in cell membranes. J. Biol. Chem. 277:2002;4704-4712.
24. Lemoine N.R., Staddon S., Dickson C., Barnes D.M., Gullick W.J. Absence of activating transmembrane mutations in the c-erbB-2 proto-oncogene in human breast cancer. Oncogene. 5:1990;237-239.
25. Burke C.L., Stern D.F. Activation of Neu (ErbB-2) mediated by disulfide bond-induced dimerization reveals a receptor tyrosine kinase dimer interface. Mol. Cell. Biol. 18:1998;5371-5379.
26. Bell C.A., Tynan J.A., Hart K.C., Meyer A.N., Roberson S.C., Donoghue D.J. Rotational coupling of the transmembrane and kinase domain of the Neu receptor tyrosine kinase. Mol. Biol. Cell. 11:2000;3589-3599.
27. Fleishman S.J., Schlessinger J., Ben-Tal N. A putative molecular-activation switch in the transmembrane domain of erbB2. Proc. Natl Acad. Sci. USA. 99:2002;15937-15940.
28. Sakaguchi T., Tu Q., Pinto L.H., Lamb R.A. The active oligomeric state of the minimalistic influenza virus M2 ion channel is a tetramer. Proc. Natl Acad. Sci. USA. 94:1997;5000-5005.
29. Bauer C.M., Pinto L.H., Cross T.A., Lamb R.A. The influenza virus M2 ion channel protein probing the structure of the transmembrane domain in intact cells by using engineered disulfide cross-linking. Virology. 254:1999;196-209.
30. Lamb R.A., Zebedee S.L., Richardson C.D. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell. 40:1985;627-633.
31. Lamb R.A., Holsinger L.J., Pinto L.H. The influenza A virus M2 ion channel protein and its role in the influenza virus life cycle. Wemmer E. Receptor-mediated Virus Entry into Cell. 1994;303-321 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Pinto L.H., Dieckmann G.R., Gandhi C.S., Papworth C.G., Braman J., Shaughnessy M.A., et al. A functionally defined model for the M2 proton channel of Influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl Acad. Sci. USA. 94:1997;11301-11306.
33. + channel. Protein Sci. 10:2001;2241-2250.
34. Holsinger L.J., Nichani D., Pinto L.H., Lamb R.A. Influenza-A virus M2 ion-channel protein - a structure-function analysis. Virology. 68:1994;1551-1563.
35. Grambas S., Bennett M., Hay A. Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A virus. Virology. 191:1992;541-549.
36. Wang C., Takeuchi K., Pinto L.H., Lamb R.A. Ion channel activity of the influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67:1993;5585-5594.
37. Wang C., Lamb R.A., Pinto L.H. Activation of the M2 ion-channel of influenza virus - a role for the transmembrane domain histidine residue. Biophys. J. 69:1995;1363-1371.
38. Tang Y., Zaitseva F., Lamb R.A., Pinto L.H. The gate of the influenza virus M2 proton channel is formed by a single tryptophan residue. J. Biol. Chem. 277:2002;39880-39886.
39. Kirchberger M.A., Tada M., Katz A.M. Phopholamban: a regulatory protein of the cardiac sarcoplasmic reticulum. Recent Advan. Stud. Cardiac Struct. Metal. 5:1975;103-115.
40. 2+ pump of sarcoplasimic reticulum. Nature. 342:1989;90-92.
41. Arkin I.T., Adams P.D., MacKenzie K.R., Lemmon M.A., Brunger A.T., Engelman D.M. Structural organization of the pentameric transmembrane alpha-helices of phospholamban, a cardiac ion channel. EMBO J. 13:1994;4757-4764.
42. Simmerman H.K., Kobayashi Y.M., Autry J.M., Jones L.R. A leucine zipper stabilizes the pentameric membrane domain of phospholamban and forms a coiled-coil pore structure. J. Biol. Chem. 271:1996;5941-5946.
43. Herzyk P., Hubbard R.E. Using experimental information to produce a model of the transmembrane domain of the ion channel phospholamban. Biophys. J. 74:1998;1203-1214.
44. Adamian L., Liang J. Helix-helix packing and interfacial pairwise interactions of residues in membrane proteins. J. Mol. Biol. 311:2001;891-907.
45. 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 β-branched residues at neighboring positions. J. Mol. Biol. 296:2000;921-936.
46. Jiang S., Vakser I.A. Side-chains in transmembrane helices are shorter at helix-helix interfaces. Proteins: Struct. Funct. Genet. 40:2000;429-435.
47. Fleishman S.J., Ben-Tal N. A novel scoring function for predicting the conformations of tightly packed pairs of transmembrane α-helices. J. Mol. Biol. 321:2002;363-378.
48. Luecke H., Schobert B., Richter H.T., Cartailler J.-P., Lanyi J.K. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:1999;899-911.
49. Sansom M.S.P., Weinstein H. Hinges, swivels and switches: the role of pralines in signaling via transmembrane α-helices. Trends Pharmacol. Sci. 21:2000;445-451.
50. Riek R.P., Rigoutsos I., Novotny J., Graham R.M. Non-α-helical elements modulate polytopic membrane protein architecture. J. Mol. Biol. 306:2001;349-362.
51. 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 β-branched residues at neighboring positions. J. Mol. Biol. 296:2000;921-936.
52. Bower M.J., Cohen F.E., Dunbrack R.L. Prediction of protein side-chain rotamers from a backbone-dependent rotamer library: a new homology modeling tool. J. Mol. Biol. 267:1997;1268-1282.
53. Kelly L.A., Gardner S.P., Sutcliffe M.J. An automated approach for clustering an ensemble of NMR-derived protein structures into conformationally-related subfamilies. Protein Eng. 9:1996;1063-1065.
54. Brunger A.T., Adams P.D., Clore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system. Acta Crystallog. sect. D. 54:1998;905-921.