Changes in Apparent Free Energy of Helix-Helix Dimerization in a Biological Membrane Due to Point Mutations

Journal of Molecular Biology

Volumn 371, Issue 2, 2007, Pages 422-434

  Duong, Mylinh T ^a   Jaszewski, Todd M ^a   Fleming, Karen G ^b   MacKenzie, Kevin R ^a  

^a RICE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

dimerization; glycophorin A; thermodynamics; TOXCAT; transmembrane domain

Indexed keywords

GLYCOPHORIN A; MEMBRANE PROTEIN; THREONINE;

AMINO ACID SEQUENCE; ARTICLE; DIMERIZATION; ENERGY BALANCE; GENE EXPRESSION; MEMBRANE BIOLOGY; MEMBRANE POTENTIAL; MUTATION; PRIORITY JOURNAL; PROTEIN STABILITY; SEDIMENTATION; THERMODYNAMICS; WILD TYPE;

EID: 34447271539     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.05.026     Document Type: Article

References (52)

1. MacKenzie K.R. Folding and stability of alpha-helical integral membrane proteins. Chem. Rev. 106 (2006) 1931-1977
2. Fleming K.G., Ackerman A.L., and Engelman D.M. The effect of point mutations on the free energy of transmembrane alpha-helix dimerization. J. Mol. Biol. 272 (1997) 266-275
3. Fleming K.G. Probing stability of helical transmembrane proteins. Methods Enzymol. 323 (2000) 63-77
4. Fleming K.G. Standardizing the free energy change of transmembrane helix-helix interactions. J. Mol. Biol. 323 (2002) 563-571
5. Cristian L., Lear J.D., and DeGrado W.F. Determination of membrane protein stability via thermodynamic coupling of folding to thiol-disulfide interchange. Protein Sci. 12 (2003) 1732-1740
6. Cristian L., Lear J.D., and DeGrado W.F. Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers. Proc. Natl Acad. Sci. USA 100 (2003) 14772-14777
7. You M., Li E., Wimley W.C., and Hristova K. Forster resonance energy transfer in liposomes: measurements of transmembrane helix dimerization in the native bilayer environment. Anal. Biochem. 340 (2005) 154-164
8. Fleming K.G., and Engelman D.M. Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants. Proc. Natl Acad. Sci. USA 98 (2001) 14340-14344
9. Doura A.K., and Fleming K.G. Complex interactions at the helix-helix interface stabilize the glycophorin A transmembrane dimer. J. Mol. Biol. 343 (2004) 1487-1497
10. Doura A.K., Kobus F.J., Dubrovsky L., Hibbard E., and Fleming K.G. Sequence context modulates the stability of a GxxxG-mediated transmembrane helix-helix dimer. J. Mol. Biol. 341 (2004) 991-998
11. Stouffer A.L., Nanda V., Lear J.D., and DeGrado W.F. Sequence determinants of a transmembrane proton channel: an inverse relationship between stability and function. J. Mol. Biol. 347 (2005) 169-179
12. Langosch D., Brosig B., Kolmar H., and Fritz H.J. Dimerisation of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator. J. Mol. Biol. 263 (1996) 525-530
13. Brosig B., and Langosch D. The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci. 7 (1998) 1052-1056
14. Russ W.P., and Engelman D.M. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl Acad. Sci. USA 96 (1999) 863-868
15. Leeds J.A., Boyd D., Huber D.R., Sonoda G.K., Luu H.T., Engelman D.M., and Beckwith J. Genetic selection for and molecular dynamic modeling of a protein transmembrane domain multimerization motif from a random Escherichia coli genomic library. J. Mol. Biol. 313 (2001) 181-195
16. Gurezka R., and Langosch D. In vitro selection of membrane-spanning leucine zipper protein-protein interaction motifs using POSSYCCAT. J. Biol. Chem. 276 (2001) 45580-45587
17. Schneider D., and Engelman D.M. GALLEX, a measurement of heterologous association of transmembrane helices in a biological membrane. J. Biol. Chem. 278 (2003) 3105-3111
18. Laage R., and Langosch D. Dimerization of the synaptic vesicle protein synaptobrevin (vesicle-associated membrane protein) II depends on specific residues within the transmembrane segment. Eur. J. Biochem. 249 (1997) 540-546
19. Gurezka R., Laage R., Brosig B., and Langosch D. A heptad motif of leucine residues found in membrane proteins can drive self-assembly of artificial transmembrane segments. J. Biol. Chem. 274 (1999) 9265-9270
20. Laage R., Rohde J., Brosig B., and Langosch D. A conserved membrane-spanning amino acid motif drives homomeric and supports heteromeric assembly of presynaptic SNARE proteins. J. Biol. Chem. 275 (2000) 17481-17487
21. Mendrola J.M., Berger M.B., King M.C., and Lemmon M.A. The single transmembrane domains of ErbB receptors self-associate in cell membranes. J. Biol. Chem. 277 (2002) 4704-4712
22. Bowen M.E., Engelman D.M., and Brunger A.T. Mutational analysis of synaptobrevin transmembrane domain oligomerization. Biochemistry 41 (2002) 15861-15866
23. McClain M.S., Iwamoto H., Cao P., Vinion-Dubiel A.D., Li Y., Szabo G., Shao Z., and Cover T.L. Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J. Biol. Chem. 278 (2003) 12101-12108
24. Roy R., Laage R., and Langosch D. Synaptobrevin transmembrane domain dimerization-revisited. Biochemistry 43 (2004) 4964-4970
25. Ruan W., Lindner E., and Langosch D. The interface of a membrane-spanning leucine zipper mapped by asparagine-scanning mutagenesis. Protein Sci. 13 (2004) 555-559
26. Melnyk R.A., Kim S., Curran A.R., Engelman D.M., Bowie J.U., and Deber C.M. The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication. J. Biol. Chem. 279 (2004) 16591-16597
27. Schneider D., and Engelman D.M. Motifs of two small residues can assist but are not sufficient to mediate transmembrane helix interactions. J. Mol. Biol. 343 (2004) 799-804
28. Schneider D., and Engelman D.M. Involvement of transmembrane domain interactions in signal transduction by alpha/beta integrins. J. Biol. Chem. 279 (2004) 9840-9846
29. Li R., Gorelik R., Nanda V., Law P.B., Lear J.D., DeGrado W.F., and Bennett J.S. Dimerization of the transmembrane domain of Integrin alphaIIb subunit in cell membranes. J. Biol. Chem. 279 (2004) 26666-26673
30. Chin C.N., Sachs J.N., and Engelman D.M. Transmembrane homodimerization of receptor-like protein tyrosine phosphatases. FEBS Letters 579 (2005) 3855-3858
31. Zhou F.X., Merianos H.J., Brunger A.T., and Engelman D.M. Polar residues drive association of polyleucine transmembrane helices. Proc. Natl Acad. Sci. USA 98 (2001) 2250-2255
32. Zhou F.X., Cocco M.J., Russ W.P., Brunger A.T., and Engelman D.M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nature Struct. Biol. 7 (2000) 154-160
33. Lemmon M.A., Flanagan J.M., Hunt J.F., Adair B.D., Bormann B.J., Dempsey C.E., and Engelman D.M. Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices. J. Biol. Chem. 267 (1992) 7683-7689
34. Lemmon M.A., Treutlein H.R., Adams P.D., Brunger A.T., and Engelman D.M. A dimerization motif for transmembrane alpha-helices. Nature Struct. Biol. 1 (1994) 157-163
35. Fleming K.G., Ren C.C., Doura A.K., Eisley M.E., Kobus F.J., and Stanley A.M. Thermodynamics of glycophorin A transmembrane helix dimerization in C14 betaine micelles. Biophys. Chem. 108 (2004) 43-49
36. Lemmon M.A., Flanagan J.M., Treutlein H.R., Zhang J., and Engelman D.M. Sequence specificity in the dimerization of transmembrane alpha-helices. Biochemistry 31 (1992) 12719-12725
37. Shaw W.V. Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria. Methods Enzymol. 43 (1975) 737-755
38. Sulistijo E.S., Jaszewski T.M., and MacKenzie K.R. Sequence-specific dimerization of the transmembrane domain of the "BH3-only" protein BNIP3 in membranes and detergent. J. Biol. Chem. 278 (2003) 51950-51956
39. Gorman C.M., Moffat L.F., and Howard B.H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2 (1982) 1044-1051
40. Young S.L., Barbera L., Kaynard A.H., Haugland R.P., Kang H.C., Brinkley M., and Melner M.H. A nonradioactive assay for transfected chloramphenicol acetyltransferase activity using fluorescent substrates. Anal. Biochem. 197 (1991) 401-407
41. Hessa T., Kim H., Bihlmaier K., Lundin C., Boekel J., Andersson H., et al. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433 (2005) 377-381
42. Miller V.L., and Mekalanos J.J. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc. Natl Acad. Sci. USA 81 (1984) 3471-3475
43. Miller V.L., Taylor R.K., and Mekalanos J.J. Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell 48 (1987) 271-279
44. MacKenzie K.R., Prestegard J.H., and Engelman D.M. A transmembrane helix dimer: structure and implications. Science 276 (1997) 131-133
45. Smith S.O., Eilers M., Song D., Crocker E., Ying W., Groesbeek M., et al. Implications of threonine hydrogen bonding in the glycophorin A transmembrane helix dimer. Biophys. J. 82 (2002) 2476-2486
46. Sulistijo E.S., and Mackenzie K.R. Sequence dependence of BNIP3 transmembrane domain dimerization implicates side-chain hydrogen bonding and a tandem GxxxG motif in specific helix-helix interactions. J. Mol. Biol. 364 (2006) 974-990
47. Popot J.L., and Engelman D.M. Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29 (1990) 4031-4037
48. Li S.C., and Deber C.M. A measure of helical propensity for amino acids in membrane environments. Nature Struct. Biol. 1 (1994) 558
49. White S.H., and Wimley W.C. Hydrophobic interactions of peptides with membrane interfaces. Biochim. Biophys. Acta 1376 (1998) 339-352
50. Wimley W.C., and White S.H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3 (1996) 842-848
51. Wimley W.C., Creamer T.P., and White S.H. Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 35 (1996) 5109-5124
52. Finger C., Volkmer T., Prodohl A., Otzen D.E., Engelman D.M., and Schneider D. The stability of transmembrane helix interactions measured in a biological membrane. J. Mol. Biol. 358 (2006) 1221-1228