Correlating structure, dynamics, and function in transmembrane segment VII of the Na+/H+ exchanger isoform 1

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 2, 2010, Pages 94-104

  Reddy, Tyler ^a   Li, Xiuju ^c   Fliegel, Larry ^c   Sykes, Brian D ^c   Rainey, Jan K ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

15N relaxation; DPC; Model Free analysis; NMR; Peptide; Reduced spectral density mapping

Indexed keywords

ALANINE; DODECYLPHOSPHORYLCHOLINE; GLUTAMIC ACID; GLYCINE; ISOLEUCINE; PHENYLALANINE; SERINE; SODIUM PROTON EXCHANGE PROTEIN 1;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENE MUTATION; MATHEMATICAL MODEL; MICELLE; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS;

ANIMALS; CATION TRANSPORT PROTEINS; HUMANS; MICELLES; MODELS, MOLECULAR; PHOSPHORYLCHOLINE; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SODIUM-HYDROGEN ANTIPORTER; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 74249113935     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.06.025     Document Type: Article

References (64)

1. Riek R.P., Rigoutsos I., Novotny J., and Graham R.M. Non-[alpha]-helical elements modulate polytopic membrane protein architecture. J. Mol. Biol. 306 (2001) 349-362
2. Yohannan S., Faham S., Yang D., Whitelegge J.P., and Bowie J.U. The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 959-963
3. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., Trong I.L., Teller D.C., Okada T., Stenkamp R.E., Yamamoto M., and Miyano M. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 (2000) 739-745
4. Hunte C., Screpanti E., Venturi M., Rimon A., Padan E., and Michel H. Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435 (2005) 1197-1202
5. Takahashi M., Kondou Y., and Toyoshima C. Interdomain communication in calcium pump as revealed in the crystal structures with transmembrane inhibitors. Proc. Natl. Acad. Sci. 104 (2007) 5800-5805
6. Yamashita A., Singh S.K., Kawate T., Jin Y., and Gouaux E. Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437 (2005) 215-223
7. Jin T., Peng L., Mirshahi T., Rohacs T., Chan K.W., Sanchez R., and Logothetis D.E. The [beta][gamma] subunits of G proteins gate a K+ channel by pivoted bending of a transmembrane segment. Mol. Cell 10 (2002) 469-481
8. Liu L.P., and Deber C.M. Uncoupling hydrophobicity and helicity in transmembrane segments. Alpha-helical propensities of the amino acids in non-polar environments. J. Biol. Chem. 273 (1998) 23645-23648
9. Sadja R., Smadja K., Alagem N., and Reuveny E. Coupling G[beta][gamma]-dependent activation to channel opening via pore elements in inwardly rectifying potassium channels. Neuron 29 (2001) 669-680
10. Landau M., Herz K., Padan E., and Ben-Tal N. Model structure of the Na+/H+ exchanger 1 (NHE1): functional and clinical implications. J. Biol. Chem. 282 (2007) 37854-37863
11. Wakabayashi S., Pang T., Su X., and Shigekawa M. A novel topology model of the human Na+/H+ exchanger isoform 1. J. Biol. Chem. 275 (2000) 7942-7949
12. Ding J., Rainey J.K., Xu C., Sykes B.D., and Fliegel L. Structural and functional characterization of transmembrane segment VII of the Na+/H+ exchanger isoform 1. J. Biol. Chem. 281 (2006) 29817-29829
13. Lee B.L., Li X., Liu Y., Sykes B.D., and Fliegel L. Structural and functional analysis of TM XI of the nhe1 isoform of the NA+/H+ exchanger. J. Biol. Chem. (2009) M809201200
14. Reddy T., Ding J., Li X., Sykes B.D., Rainey J.K., and Fliegel L. Structural and functional characterization of transmembrane segment IX of the NHE1 isoform of the Na+/H+ exchanger. J. Biol. Chem. 283 (2008) 22018-22030
15. Slepkov E.R., Rainey J.K., Li X., Liu Y., Cheng F.J., Lindhout D.A., Sykes B.D., and Fliegel L. Structural and functional characterization of transmembrane segment IV of the NHE1 isoform of the Na+/H+ exchanger. J. Biol. Chem. 280 (2005) 17863-17872
16. Palmer III A.G. NMR probes of molecular dynamics: overview and comparison with other techniques. Annu. Rev. Biophys. Biomol. Struct. 30 (2001) 129-155
17. Palmer A.G., Williams J., and McDermott A. Nuclear magnetic resonance studies of biopolymer dynamics. J. Phys. Chem. 100 (1996) 13293-13310
18. Ma D., Tillman T.S., Tang P., Meirovitch E., Eckenhoff R., Carnini A., and Xu Y. NMR studies of a channel protein without membranes: structure and dynamics of water-solubilized KcsA. Proc. Natl. Acad. Sci. 105 (2008) 16537-16542
19. Slovic A.M., Kono H., Lear J.D., Saven J.G., and DeGrado W.F. Computational design of water-soluble analogues of the potassium channel KcsA. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 1828-1833
20. Andronesi O.C., Becker S., Seidel K., Heise H., Young H.S., and Baldus M. Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy and #x2020. J. Am. Chem. Soc. 127 (2005) 12965-12974
21. Heise H., Hoyer W., Becker S., Andronesi O.C., Riedel D., and Baldus M. Molecular-level secondary structure, polymorphism, and dynamics of full-length Œ ± -synuclein fibrils studied by solid-state NMR. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 15871-15876
22. Durr U.H., Waskell L., and Ramamoorthy A. The cytochromes P450 and b5 and their reductases-promising targets for structural studies by advanced solid-state NMR spectroscopy. Biochim. Biophys. Acta 1768 (2007) 3235-3259
23. Xu J., Durr U.H., Im S.C., Gan Z., Waskell L., and Ramamoorthy A. Bicelle-enabled structural studies on a membrane-associated cytochrome B5 by solid-state MAS NMR spectroscopy. Angew. Chem., Int. Ed. Engl. 47 (2008) 7864-7867
24. Arseniev A.S., Barsukov I.L., Bystrov V.F., Lomize A.L., and Ovchinnikov Yu A. 1H-NMR study of gramicidin A transmembrane ion channel. Head-to-head right-handed, single-stranded helices. FEBS Lett. 186 (1985) 168-174
25. Franzin C.M., Teriete P., and Marassi F.M. Structural similarity of a membrane protein in micelles and membranes. J. Am. Chem. Soc. 129 (2007) 8078-8079
26. Ketchem R.R., Hu W., and Cross T.A. High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science 261 (1993) 1457-1460
27. Opella S.J., Marassi F.M., Gesell J.J., Valente A.P., Kim Y., Oblatt-Montal M., and Montal M. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol. 6 (1999) 374-379
28. Katragadda M., Alderfer J.L., and Yeagle P.L. Assembly of a polytopic membrane protein structure from the solution structures of overlapping peptide fragments of bacteriorhodopsin. Biophys. J. 81 (2001) 1029-1036
29. Katragadda M., Chopra A., Bennett M., Alderfer J.L., Yeagle P.L., and Albert A.D. Structures of the transmembrane helices of the G-protein coupled receptor, rhodopsin. J. Pept. Res. 58 (2001) 79-89
30. Almeida F.C.L., and Opella S.J. fd coat protein structure in membrane environments: structural dynamics of the loop between the hydrophobic trans-membrane helix and the amphipathic in-plane helix. J. Mol. Biol. 270 (1997) 481-495
31. Orekhov V.Y., Pervushin K.V., Korzhnev D.M., and Arseniev A.S. Backbone dynamics of (1-71)-and (1-36)bacterioopsin studied by two-dimensional 1H-15N NMR spectroscopy. J. Biomol. NMR 6 (1995) 113-122
32. Orekhov V.Y., Korzhnev D.M., Diercks T., Kessler H., and Arseniev A.S. 1H-15N NMR dynamic study of an isolated α-helical peptide (1-36)-bacteriorhodopsin reveals the equilibrium helix-coil transitions. J. Biomol. NMR 14 (1999) 345-356
33. Orlowski J., and Grinstein S. Na+/H+ exchangers of mammalian cells. J. Biol. Chem. 272 (1997) 22373-22376
34. Grinstein S., Rotin D., and Mason M.J. Na+/H+ exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation. Biochim. Biophys. Acta (BBA)-Rev. Biomembr. 988 (1989) 73-97
35. Shrode L., Cabado A., Goss G., and Grinstein S. In: Fliegel L. (Ed). The Na+/H+ Exchanger (1996), R.G. Landes Co., Austin, TX 101-122
36. Fliegel L. Regulation of myocardial Na+/H+ exchanger activity. Basic Res. Cardiol. 96 (2001) 301-305
37. Karmazyn M., Liu Q., Gan X.T., Brix B.J., and Fliegel L. Aldosterone increases NHE-1 expression and induces NHE-1-dependent hypertrophy in neonatal rat ventricular myocytes. Hypertension 42 (2003) 1171-1176
38. Jones D.T., Taylor W.R., and Thornton J.M. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33 (1994) 3038-3049
39. Murtazina R., Booth B.J., Bullis B.L., Singh D.N., and Fliegel L. Functional analysis of polar amino-acid residues in membrane associated regions of the NHE1 isoform of the mammalian Na+/H+ exchanger. Eur. J. Biochem. 268 (2001) 4674-4685
40. Zhang Y.P., Lewis R.N., Hodges R.S., and McElhaney R.N. Interaction of a peptide model of a hydrophobic transmembrane alpha-helical segment of a membrane protein with phosphatidylethanolamine bilayers: differential scanning calorimetric and Fourier transform infrared spectroscopic studies. Biophys. J. 68 (1995) 847-857
41. Kay L., Keifer P., and Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114 (1992) 10663-10665
42. Taylor J.R. An Introduction To Error Analysis, 2nd ed., University Science Books, Sausalito, CA (1997)
43. d'Auvergne E.J., and Gooley P.R. Optimisation of NMR dynamic models II. A new methodology for the dual optimisation of the model-free parameters and the Brownian rotational diffusion tensor. J. Biomol. NMR 40 (2008) 121-133
44. d'Auvergne E.J., and Gooley P.R. Optimisation of NMR dynamic models I. Minimisation algorithms and their performance within the model-free and Brownian rotational diffusion spaces. J. Biomol. NMR 40 (2008) 107-119
45. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., Shoelson S.E., Pawson T., Forman-Kay J.D., and Kay L.E. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
46. Abragam A. The Principles of Nuclear Magnetism, Clarendon Press, Oxford (1961)
47. Farrow N.A., Zhang O., Szabo A., Torchia D.A., and Kay L.E. Spectral density function mapping using 15N relaxation data exclusively. J. Biomol. NMR 6 (1995) 153-162
48. Hiyama Y., Niu C.H., Silverton J.V., Bavoso A., and Torchia D.A. Determination of 15N chemical shift tensor via 15N-2H dipolar coupling in Boc-glycylglycyl[15N glycine]benzyl ester. J. Am. Chem. Soc. 110 (1988) 2378-2383
49. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104 (1982) 4546-4559
50. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104 (1982) 4559-4570
51. Spyracopoulos L. A suite of Mathematica notebooks for the analysis of protein main chain 15N NMR relaxation data. J. Biomol. NMR 36 (2006) 215-224
52. Mandel A.M., Akke M., and Palmer III A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246 (1995) 144-163
53. d'Auvergne E.J., and Gooley P.R. The use of model selection in the model-free analysis of protein dynamics. J. Biomol. NMR 25 (2003) 25-39
54. Palmer A.G., Rance M., and Wright P.E. Intramolecular motions of a zinc finger DNA-binding domain from Xfin characterized by proton-detected natural abundance carbon-13 heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113 (1991) 4371-4380
55. Lefevre J.F., Dayie K.T., Peng J.W., and Wagner G. Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry 35 (1996) 2674-2686
56. Ropars V., Bouguet-Bonnet S., Auguin D., Barthe P., Canet D., and Roumestand C. Unraveling protein dynamics through fast spectral density mapping. J. Biomol. NMR 37 (2007) 159-177
57. Slepkov E.R., Chow S., Lemieux M.J., and Fliegel L. Proline residues in transmembrane segment IV are critical for activity, expression and targeting of the Na+/H+ exchanger isoform 1. Biochem. J. 379 (2004) 31-38
58. Peng J.W., and Wagner G. Frequency spectrum of NH bonds in eglin c from spectral density mapping at multiple fields. Biochemistry 34 (1995) 16733-16752
59. Mulder F.A., Mittermaier A., Hon B., Dahlquist F.W., and Kay L.E. Studying excited states of proteins by NMR spectroscopy. Nat. Struct. Biol. 8 (2001) 932-935
60. Li X., Ding J., Liu Y., Brix B.J., and Fliegel L. Functional analysis of acidic amino acids in the cytosolic tail of the Na+/H+ exchanger. Biochemistry 43 (2004) 16477-16486
61. Slupsky C.M., Spyracopoulos L., Booth V.K., Sykes B.D., and Crump M.P. Probing nascent structures in peptides using natural abundance 13C NMR relaxation and reduced spectral density mapping. Proteins 67 (2007) 18-30
62. Ding J., Ng R.W., and Fliegel L. Functional characterization of the transmembrane segment VII of the NHE1 isoform of the Na+/H+ exchanger. Can. J. Physiol. Pharm. 85 (2007) 319-325
63. Rainey J.K., Fliegel L., and Sykes B.D. Strategies for dealing with conformational sampling in structural calculations of flexible or kinked transmembrane peptides. Biochem. Cell Biol. 84 (2006) 918-929
64. Langelaan D.N., Bebbington E.M., Reddy T., and Rainey J.K. Structural insight into G-protein coupled receptor binding by apelin. Biochemistry 48 (2009) 537-548