Polar residues in transmembrane helices can decrease electrophoretic mobility in polyacrylamide gels without causing helix dimerization

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 6, 2009, Pages 1321-1331

  Walkenhorst, William F ^b   Merzlyakov, Mikhail ^c   Hristova, Kalina ^c   Wimley, William C ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b LOYOLA UNIVERSITY   (United States)

^c Johns Hopkins University   (United States)

Author keywords

Asparagine; Dimerization; Membrane protein; MS1; SDS PAGE; Transmembrane

Indexed keywords

ASPARAGINE; DETERGENT; MEMBRANE PROTEIN;

ARTICLE; DIMERIZATION; ELECTROPHORETIC MOBILITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROPHILICITY; HYDROPHOBICITY; LIPID MEMBRANE; MOLECULAR WEIGHT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; DETERGENTS; DIMERIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLYCOPHORIN; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; SOLUBILITY; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 65549101578     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.02.017     Document Type: Article

References (51)

1. White S.H., and Wimley W.C. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struc. 28 (1999) 319-365
2. Popot J.-L., and Engelman D.M. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69 (2000) 881-922
3. Engelman D.M., Chen Y., Chin C.N., Curran A.R., Dixon A.M., Dupuy A.D., Lee A.S., Lehnert U., Matthews E.E., Reshetnyak Y.K., Senes A., and Popot J.L. Membrane protein folding: beyond the two stage model. FEBS Lett. 555 (2003) 122-125
4. White S.H., Ladokhin A.S., Jayasinghe S., and Hristova K. How membranes shape protein structure. J. Biol. Chem. 276 (2001) 32395-32398
5. 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 α-helices. J. Biol. Chem. 267 (1992) 7683-7689
6. 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
7. Russ W.P., and Engelman D.M. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 863-868
8. Fleming K.G., Ackerman A.L., and Engelman D.M. The effect of point mutations on the free energy of transmembrane α-helix dimerization. J. Mol. Biol. 272 (1997) 266-275
9. 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
10. Li E., You M., and Hristova K. FGFR3 dimer stabilization due to a single amino acid pathogenic mutation. J. Mol. Biol. 356 (2006) 600-612
11. Merzlyakov M., Chen L., and Hristova K. Studies of receptor tyrosine kinase transmembrane domain interactions: the EmEx-FRET method. J. Membr. Biol. 215 (2007) 93-103
12. Artemenko E.O., Egorova N.S., Arseniev A.S., and Feofanov A.V. Transmembrane domain of EphA1 receptor forms dimers in membrane-like environment. Biochim. Biophys. Acta 1778 (2008) 2361-2367
13. Choma C., Gratkowski H., Lear J.D., and DeGrado W.F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 7 (2000) 161-166
14. Therien A.G., Grant F.E.M., and Deber C.M. Interhelical hydrogen bonds in the CFTR membrane domain. Nat. Struct. Biol. 8 (2001) 597-601
15. Fisher L.E., Engelman D.M., and Sturgis J.N. Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 293 (1999) 639-651
16. Li E., You M., and Hristova K. SDS-PAGE and FRET suggest weak interactions between FGFR3 TM domains in the absence of extracellular domains and ligands. Biochemistry 44 (2005) 352-360
17. Lear J.D., Gratkowski H., Adamian L., Liang J., and DeGrado W.F. Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles. Biochemistry 42 (2003) 6400-6407
18. Gratkowski H., Dai Q.H., Wand A.J., DeGrado W.F., and Lear J.D. Cooperativity and specificity of association of a designed transmembrane peptide. Biophys. J. 83 (2002) 1613-1619
19. 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
20. 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
21. 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. Nat. Struct. Biol. 7 (2000) 154-160
22. Li E., and Hristova K. Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies. Biochemistry 45 (2006) 6241-6251
23. Partridge A.W., Melnyk R.A., and 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
24. Gratkowski H., Lear J.D., and DeGrado W.F. Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 880-885
25. Lear J.D., Gratkowski H., and DeGrado W.F. De novo design, synthesis and characterization of membrane-active peptides. Biochem. Soc. Trans. 29 (2001) 559-564
26. Rausch J.M., Marks J.R., and Wimley W.C. Rational combinatorial design of pore-forming beta-sheet peptides. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10511-10515
27. Grant G.A. Synthetic peptides: A user's guide (1992), WH Freeman and Company, New York
28. You M., Li E., Wimley W.C., and Hristova K. FRET in liposomes: measurements of TM helix dimerization in the native bilayer environment. Anal. Biochem. 340 (2005) 154-164
29. Johnson W.C. Protein secondary structure and circular dichroism: a practical guide. Proteins 7 (1990) 205-214
30. Ashish, and Wimley W.C. Visual detection of specific, native interactions between soluble and microbead-tethered α-helices from membrane proteins. Biochemistry 40 (2001) 13753-13759
31. Mohanty A.K., Bishop C.M., Bishop T.C., Wimley W.C., and Wiener M.C. Enzymatic E-colicins bind to their target receptor BtuB by presentation of a small binding epitope on a coiled-coil scaffold. J. Biol. Chem. 278 (2003) 40953-40958
32. 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
33. Johnson R.M., Heslop C.L., and Deber C.M. Hydrophobic helical hairpins: design and packing interactions in membrane environments. Biochemistry 43 (2004) 14361-14369
34. Iwamoto T., You M., Li E., Spangler J., Tomich J.M., and Hristova K. Synthesis and initial characterization of FGFR3 transmembrane domain: consequences of sequence modifications. Biochim. Biophys. Acta 1668 (2005) 240-247
35. Wu P.G., and Brand L. Resonance energy transfer: methods and applications. Anal. Biochem. 218 (1994) 1-13
36. Reither S., and Jeltsch A. Specificity of DNA triple helix formation analyzed by a FRET assay. BMC Biochem. 3 (2002) 27
37. Fisher L.E., and Engelman D.M. High-yield synthesis and purification of an α-helical transmembrane domain. Anal. Biochem. 293 (2001) 102-108
38. Wimley W.C., Selsted M.E., and White S.H. Interactions between human defensins and lipid bilayers: evidence for the formation of multimeric pores. Protein Sci. 3 (1994) 1362-1373
39. Ladokhin A.S., Wimley W.C., and White S.H. Leakage of membrane vesicle contents: determination of mechanism using fluorescence requenching. Biophys. J. 69 (1995) 1964-1971
40. Lakowicz J.R. Principles of Fluorescence Spectroscopy (1983), Plenum Press, New York
41. Wolber P.K., and Hudson B.S. An analytic solution to the Förster energy transfer problem in two dimensions. Biophys. J. 28 (1979) 197-210
42. You M., Spangler J., Li E., Han X., Ghosh P., and Hristova K. Effect of pathogenic cysteine mutations on FGFR3 transmembrane domain dimerization in detergents and lipid bilayers. Biochemistry 46 (2007) 11039-11046
43. Therien A.G., and Deber C.M. Oligomerization of a peptide derived from the transmembrane region of the sodium pump gamma subunit: effect of the pathological mutation G41R. J. Mol. Biol. 322 (2002) 583-590
44. Merzlyakov M., Li E., Casas R., and Hristova K. Spectral Forster resonance energy transfer detection of protein interactions in surface-supported bilayers. Langmuir 22 (2006) 6986-6992
45. 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. U. S. A. 100 (2003) 14772-14777
46. Gerber D., Sal-Man N., and Shai Y. Two motifs within a transmembrane domain, one for homodimerization and the other for heterodimerization. J. Biol. Chem. 279 (2004) 21177-21182
47. Hessa T., White S.H., and von Heijne G. Membrane insertion of a potassium-channel voltage sensor. Science 307 (2005) 1427
48. Wimley W.C., and White S.H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3 (1996) 842-848
49. Dawson J.P., Weinger J.S., and Engelman D.M. Motifs of serine and threonine can drive association of transmembrane helices. J. Mol. Biol. 316 (2002) 799-805
50. Han X., Mihailescu M., and Hristova K. Neutron diffraction studies of fluid bilayers with transmembrane proteins: structural consequences of the achondroplasia mutation. Biophys. J. 91 (2006) 3736-3747
51. MacKenzie K.R. Folding and stability of alpha-helical integral membrane proteins. Chem. Rev. 106 (2006) 1931-1977