The role of proline residues in the dynamics of transmembrane helices: the case of bacteriorhodopsin

References

• Bywater RP, Thomas D, Vriend G. A sequence and structural study of transmembrane helices. J Comput Aided Mol Des 2001; 15: 533–552
   PubMedGoogle Scholar
• Slepkov ER, Chow S, Lemieux MJ, Fliegel L. Proline residues in transmembrane segment IV are critical for activity, expression and targeting of the Na + /H+ exchanger isoform 1. Biochem J 2004; 379: 31–38
   Google Scholar
• Woolfson DN, Mortishire-Smith RJ, Williams DH. Conserved positioning of proline residues in membrane-spanning helices of ion-channel proteins. Biochem Biophys Res Commun 1991; 175: 733–737
   Google Scholar
• Cordes FS, Bright JN, Sansom MSP. Proline-induced distortions of transmembrane helices. J Mol Biol 2002; 323: 951–960
   PubMed Web of Science ®Google Scholar
• Sansom MS, Weinstein H. Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha-helices. Trends Pharmacol Sci 2000; 21: 445–451
   PubMed Web of Science ®Google Scholar
• von Heijne G. Proline kinks in transmembrane alpha-helices. J Mol Biol 1991; 218: 499–503
   PubMed Web of Science ®Google Scholar
• Reiersen H, Rees AR. The hunchback and its neighbours: proline as an environmental modulator. Trends Biochem Sci 2001; 26: 679–684
   PubMed Web of Science ®Google Scholar
• Bright JN, Sansom MSP. The flexing/twirling helix: exploring the flexibility about molecular hinges formed by proline and glycine motifs in transmembrane helices. J Phys Chem B 2003; 107: 627–636
   Google Scholar
• Chakrabarti P, Chakrabarti S. C–H · · · O hydrogen bond involving proline residues in alpha-helices. J Mol Biol 1998; 284: 867–873
   PubMed Web of Science ®Google Scholar
• Orzáez M, Salgado J, Giménez-Giner A, Pérez-Payá E, Mingarro I. Influence of proline residues in transmembrane helix packing. J Mol Biol 2004; 335: 631–640
   Google Scholar
• Bruns K, Fossen T, Wray V, Henklein P, Tessmer U, Schubert U. Structural characterization of the HIV-1 Vpr N terminus: evidence of cis/trans-proline isomerism. J Biol Chem 2003; 278: 43188–43201
   PubMed Web of Science ®Google Scholar
• Nilsson I, von Heijne G. Breaking the camel's back: proline-induced turns in a model transmembrane helix. J Mol Biol 1998; 284: 1185–1189
   Google Scholar
• Lu H, Marti T, Booth PJ. Proline residues in transmembrane alpha helices affect the folding of bacteriorhodopsin. J Mol Biol 2001; 308: 437–446
   Google Scholar
• Faham S, Yang D, Bare E, Yohannan S, Whitelegge JP, Bowie JU. Side-chain contributions to membrane protein structure and stability. J Mol Biol 2004; 335: 297–305
   Google Scholar
• Deupi X, Olivella M, Govaerts C, Ballesteros JA, Campillo M, Pardo L. Ser and Thr residues modulate the conformation of pro-kinked transmembrane alpha-helices. Biophys J 2004; 86: 105–115
   PubMed Web of Science ®Google Scholar
• Yohannan S, Faham S, Yang D, Whitelegge JP, Bowie JU. The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc Natl Acad Sci USA 2004; 101: 959–963
   PubMed Web of Science ®Google Scholar
• Ihara K, Umemura T, Katagiri I, Kitajima-Ihara T, Sugiyama Y, Kimura Y, Mukohata Y. Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J Mol Biol 1999; 285: 163–174
   Google Scholar
• Deber CM, Sorrell BJ, Xu GY. Conformation of proline residues in bacteriorhodopsin. Biochem Biophys Res Commun 1990; 172: 862–869
   Google Scholar
• Mogi T, Stern LJ, Chao BH, Khorana HG. Structure-function studies on bacteriorhodopsin. 8. Substitutions of the membrane-embedded proline-50, proline-91, and proline-186-the effects are determined by the substituting amino-acids. J Biol Chem 1989; 264: 14192–14196
   Google Scholar
• Zhang YN, El-Sayed MA, Stern LJ, Marti T, Mogi T, Khorana HG. Effects of mutagenetic substitution of prolines on the rate of deprotonation and reprotonation of the Schiff-base during the photocycle of bacteriorhodopsin. Photochem Photobiol 1993; 57: 1027–1031
   Google Scholar
• Edman K, Royant A, Larsson G, Jacobson F, Taylor T, van der Spoel D, Landau EM, Pebay-Peyroula E, Neutze R. Deformation of helix C in the low temperature L-intermediate of bacteriorhodopsin. J Biol Chem 2004; 279: 2147–2158
   PubMedGoogle Scholar
• Kouyama T, Nishikawa T, Tokuhisa T, Okumura H. Crystal structure of the L intermediate of bacteriorhodopsin: evidence for vertical translocation of a water molecule during the proton pumping cycle. J Mol Biol 2004; 335: 531–546
   PubMedGoogle Scholar
• Subramaniam S, Henderson R. Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature 2000; 406: 653–657
   PubMed Web of Science ®Google Scholar
• Gerwert K, Hess B, Engelhard M. Proline residues undergo structural-changes during proton pumping in bacteriorhodopsin. FEBS Lett 1990; 261: 449–454
   Google Scholar
• Needleman R, Chang M, Ni BF, Varo G, Fornes J, White SH, Lanyi JK. Properties of Asp212→Asn bacteriorhodopsin suggest that Asp212 and Asp85 both participate in a counterion and proton acceptor complex near the Schiff-base. J Biol Chem 1991; 266: 11478–11484
   Google Scholar
• Ahl PL, Stern LJ, During D, Mogi T, Khorana HG, Rothschild KJ. Effects of amino-acid substitutions in the F-helix of bacteriorhodopsin. Low-temperature ultraviolet – visible difference spectroscopy. J Biol Chem 1988; 263: 13594–13601
   PubMed Web of Science ®Google Scholar
• Rothschild KJ, He YW, Mogi T, Marti T, Stern LJ, Khorana HG. Vibrational spectroscopy of bacteriorhodopsin mutants .4. Evidence for the interaction of proline-186 with the retinylidene chromophore. Biochemistry 1990; 29: 5954–5960
   Google Scholar
• Sanz C, Lazarova T, Sepulcre F, González-Moreno R, Bourdelande JL, Querol E, Padrós E. Opening the Schiff base moiety of bacteriorhodopsin by mutation of the four extracellular Glu side chains. FEBS Lett 1999; 456: 191–195
   Google Scholar
• Oesterhelt D, Stoeckenius W. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol 1974; 31: 667–678
   PubMedGoogle Scholar
• Perálvarez A, Barnadas R, Sabés M, Querol E, Padrós E. Thr90 is a key residue of the bacteriorhodopsin proton pumping mechanism. FEBS Lett 2001; 508: 399–402
   Google Scholar
• Lazarova T, Padrós E. Helical and reverse turn changes in the BR→N transition of bacteriorhodopsin. Biochemistry 1996; 35: 8354–8358
   Google Scholar
• Perálvarez-Marín A, Márquez M, Bourdelande JL, Querol E, Padrós E. Thr-90 plays a vital role in the structure and function of bacteriorhodopsin. J Biol Chem 2004; 279: 16403–16409
   Google Scholar
• Dioumaev AK, Brown LS, Needleman R, Lanyi JK. Coupling of the reisomerization of the retinal, proton uptake, and reprotonation of Asp-96 in the N photointermediate of bacteriorhodopsin. Biochemistry 2001; 40: 11308–11317
   Google Scholar
• Bright JN, Shrivastava IH, Cordes FS, Sansom MSP. Conformational dynamics of helix S6 from Shaker potassium channel: Simulation studies. Biopolymers 2002; 64: 303–313
   PubMed Web of Science ®Google Scholar
• Ludlam CFC, Sonar S, Lee CP, Coleman M, Herzfeld J, Rajbhandary UL, Rothschild KJ. Site-directed isotope labeling and ATR-FTIR difference spectroscopy of bacteriorhodopsin: the peptide carbonyl group of Tyr-185 is structurally active during the Br→N-transition. Biochemistry 1995; 34: 2–6
   Google Scholar
• Kira A, Tanio M, Tuzi S, Saito H. Significance of low-frequency local fluctuation motions in the transmembrane B and C alpha-helices of bacteriorhodopsin, to facilitate efficient proton uptake from the cytoplasmic surface, as revealed by site-directed solid-state 13C NMR. Eur Biophys J 2004; 33: 580–588
   Google Scholar
• Takeda K, Matsui Y, Kamiya N, Adachi S, Okumura H, Kouyama T. Crystal structure of the M intermediate of bacteriorhodopsin: Allosteric structural changes mediated by sliding movement of a transmembrane helix. J Mol Biol 2004; 341: 1023–1037
   Google Scholar
• Gether U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr Rev 2000; 21: 90–113
   PubMed Web of Science ®Google Scholar
• Stitham J, Martin KA, Hwa J. The critical role of transmembrane prolines in human prostacyclin receptor activation. Mol Pharmacol 2002; 61: 1202–1210
   Google Scholar