Structural analysis of the Na+/H+ exchanger isoform 1 (NHE1) using the divide and conquer approach

Biochemistry and Cell Biology

Volumn 89, Issue 2, 2011, Pages 189-199

  Lee, Brian L ^a   Sykes, Brian D ^a   Fliegel, Larry ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Membrane protein; Membrane protein topology; Na+ H+ exchanger; NhaA

Indexed keywords

DIVIDE-AND-CONQUER APPROACH; FUNCTIONAL DATAS; HEART DISEASE; HIGH RESOLUTION; INTRACELLULAR PH; ISOFORMS; LOW-RESOLUTION MOLECULAR ENVELOPE; MEMBRANE PROTEIN TOPOLOGY; MEMBRANE PROTEINS; MUTAGENESIS EXPERIMENT; NA+/H+ EXCHANGER; NHAA; PLASMA MEMBRANE PROTEIN; STRUCTURAL KNOWLEDGE; THERAPEUTIC TARGETS; TOPOLOGY MODEL; TRANSMEMBRANE HELICES; TRANSMEMBRANE SEGMENTS;

BACTERIOLOGY; BIOLOGICAL MEMBRANES; CELL MEMBRANES; CRYSTAL STRUCTURE; MEMBRANES; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RESONANCE; SODIUM; STRUCTURAL ANALYSIS; TOPOLOGY;

PROTEINS;

ALANINE; ARGININE; CYSTEINE; GLYCINE; MEMBRANE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 1; SODIUM PROTON EXCHANGE PROTEIN NHA2; SODIUM PROTON EXCHANGE PROTEIN NHAA; TRANSMEMBRANE 11 PROTEIN; TRANSMEMBRANE 2 PROTEIN; TRANSMEMBRANE 4 PROTEIN; TRANSMEMBRANE 5 PROTEIN; TRANSMEMBRANE 7 PROTEIN; TRANSMEMBRANE 9 PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; BILAYER MEMBRANE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYTOPLASM; DIMERIZATION; EXTRACELLULAR MATRIX; GENE MUTATION; HUMAN; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW;

ANIMALS; ESCHERICHIA COLI PROTEINS; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SODIUM-HYDROGEN ANTIPORTER;

BACTERIA (MICROORGANISMS);

EID: 79953753731     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O10-140     Document Type: Review

References (57)

1. Akabas, M.H., Stauffer, D.A., Xu, M., and Karlin, A. 1992. Acetyl-choline receptor channel structure probed in cysteine-substitution mutants. Science, 258(5080): 307-310. doi:10.1126/science. 1384130. PMID:1384130.
2. + exchanger from Escherichia coli, in the pH-activated and ion-translocating states. J. Mol. Biol. 388(3): 659-672. doi:10.1016/j.jmb.2009.03.010. PMID:19396973.
3. + antiporting. Science, 317(5839): 799-803. doi:10.1126/science.1142824. PMID:17690293. (Pubitemid 47257916)
4. Aurora, R., and Rose, G.D. 1998. Helix capping. Protein Sci. 7(1): 21-38. PMID:9514257. (Pubitemid 28133743)
5. Bordag, N., and Keller, S. 2010. Alpha-helical transmembrane peptides: a "divide and conquer" approach to membrane proteins. Chem. Phys. Lipids, 163(1): 1-26. doi:10.1016/j.chemphyslip. 2009.07.009. PMID:19682979.
6. Brett, C.L., Donowitz, M., and Rao, R. 2005. Evolutionary origins of eukaryotic sodium/proton exchangers. Am. J. Physiol. Cell Physiol. 288(2): C223-C239. doi:10.1152/ajpcell.00360.2004. PMID:15643048. (Pubitemid 40105332)
7. + exchanger in metastasis. Nat. Rev. Cancer, 5(10): 786-795. doi:10.1038/nrc1713. PMID: 16175178. (Pubitemid 41400778)
8. Cordes, F.S., Bright, J.N., and Sansom, M.S. 2002. Proline-induced distortions of transmembrane helices. J. Mol. Biol. 323(5): 951-960. doi:10.1016/S0022-2836(02)01006-9. PMID:12417206. (Pubitemid 35341067)
9. + exchanger NHE-1 possesses Nand O-linked glycosylation restricted to the first N-terminal extracellular domain. Biochemistry, 33(34): 10463-10469. doi:10.1021/bi00200a030. PMID: 8068684. (Pubitemid 24281815)
10. + exchanger isoform 1. J. Biol. Chem. 281(40): 29817-29829. doi:10.1074/jbc.M606152200. PMID: 16861220. (Pubitemid 44536991)
11. + exchanger. Can. J. Physiol. Pharmacol. 85(3-4): 319-325. doi:10.1139/Y06-081. PMID:17612640. (Pubitemid 47262236)
12. Engelman, D.M., Chen, Y., Chin, C.N., Curran, A.R., Dixon, A.M., Dupuy, A.D., et al. 2003. Membrane protein folding: beyond the two stage model. FEBS Lett. 555(1): 122-125. doi:10.1016/S0014-5793(03)01106-2. PMID:14630331. (Pubitemid 37431108)
13. + exchanger in the healthy and diseased myocardium. Expert Opin. Ther. Targets, 13(1): 55-68. doi:10.1517/14728220802600707. PMID:19063706.
14. + antiporter of Escherichia coli. J. Biol. Chem. 279(22): 23104-23113. doi:10.1074/jbc. M400288200. PMID:15039449. (Pubitemid 38685615)
15. + exchanger. Biochem. Cell Biol. 76(5): 837-842. doi:10.1139/bcb-76-5-837. PMID:10353718. (Pubitemid 29318181)
16. + exchange. CRC Press Inc., Boca Raton, Fla.
17. + antiporter lines the cation passage, and Asp65 is critical for pH activation of the antiporter. J. Biol. Chem. 285: 2211-2220. doi:10.1074/jbc.M109.047134. PMID:19923224.
18. + exchanger NHE1 revealed by symmetrical intermolecular cross-linking and selective co-immunoprecipitation. Biochemistry, 43(34): 11135-11143. doi:10.1021/bi049367x. PMID:15323573. (Pubitemid 39433702)
19. + exchanger NHE1. Biochemistry, 45(44): 13346-13355. doi:10. 1021/bi0608616. PMID:17073455. (Pubitemid 44707694)
20. + antiporter and insights into mechanism of action and regulation by pH. Nature, 435(7046): 1197-1202. doi:10.1038/nature03692. PMID: 15988517. (Pubitemid 40943079)
21. Kallick, D.A., Tessmer, M.R., Watts, C.R., and Li, C.Y. 1995. The use of dodecylphosphocholine micelles in solution NMR. J. Magn. Reson. B. 109(1): 60-65. doi:10.1006/jmrb.1995.1146. PMID:8581309.
22. + -H+ exchange. Am. J. Physiol. 255(3): H608-H615. PMID:2843057.
23. Katragadda, M., Alderfer, J.L., and Yeagle, P.L. 2001. Assembly of a polytopic membrane protein structure from the solution structures of overlapping peptide fragments of bacteriorhodopsin. Biophys. J. 81(2): 1029-1036. doi:10.1016/S0006-3495(01) 75760-8. PMID:11463644.
24. + exchanger isoform 1. Channels (Austin), 2(5): 329-336.
25. Kyte, J., and Doolittle, R.F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157(1): 105-132. doi:10.1016/0022-2836(82)90515-0. PMID:7108955.
26. + exchanger 1 (NHE1): functional and clinical implications. J. Biol. Chem. 282(52): 37854-37863. doi:10.1074/jbc.M705460200. PMID:17981808.
27. + exchanger family, regulates osteoclast differentiation and survival. Biochem. Biophys. Res. Commun. 369(2): 320-326. doi:10.1016/j.bbrc. 2008.01.168. PMID:18269914.
28. + exchanger. J. Biol. Chem. 284(17): 11546-11556. doi:10.1074/jbc.M809201200. PMID:19176522.
29. Lindhout, D.A., Thiessen, A., Schieve, D., and Sykes, B.D. 2003. High-yield expression of isotopically labeled peptides for use in NMR studies. Protein Sci. 12(8): 1786-1791. doi:10.1110/ps. 0376003. PMID:12876327. (Pubitemid 36910057)
30. 2+ overload. J. Cardiovasc. Pharmacol. 55(3): 227-233. doi:10.1097/FJC.0b013e3181cb599f.
31. + exchanger. Can. J. Physiol. Pharmacol. 84(11): 1081-1095. doi:10.1139/Y06-065. PMID:17218973. (Pubitemid 46465921)
32. McDermott, A. 2009. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu Rev Bio-phys, 38(1): 385-403. doi:10.1146/annurev.biophys.050708. 133719. PMID:19245337.
33. Melnyk, R.A., Partridge, A.W., Yip, J., Wu, Y., Goto, N.K., and Deber, C.M. 2003. Polar residue tagging of transmembrane pep-tides. Biopolymers, 71(6): 675-685. doi:10.1002/bip.10595. PMID:14991677. (Pubitemid 38325778)
34. + exchanger isoform 1 overproduced in Saccharomyces cerevisiae. J. Biol. Chem. 283(7): 4145-4154. doi:10.1074/jbc.M704844200. PMID:18077454.
35. Murphy, E., and Allen, D.G. 2009. Why did the NHE inhibitor clinical trials fail? J. Mol. Cell. Cardiol. 46(2): 137-141. doi:10. 1016/j.yjmcc.2008. 09.715. PMID:19027021.
36. + exchanger. Eur. J. Biochem. 268(17): 4674-4685. doi:10.1046/j.1432-1327.2001. 02391.x. PMID:11532004. (Pubitemid 34203416)
37. + and the interaction with amiloride derivatives. Biochemistry, 42(51): 15361-15368. doi:10.1021/bi035296a. PMID:14690446. (Pubitemid 38031735)
38. Padan, E., Kozachkov, L., Herz, K., and Rimon, A. 2009. NhaA crystal structure: functional-structural insights. J. Exp. Biol. 212(11): 1593-1603. doi:10.1242/jeb.026708. PMID:19448069.
39. Pedersen, S.F., King, S.A., Nygaard, E.B., Rigor, R.R., and Cala, P.M. 2007. NHE1 inhibition by amilorideand benzoylguanidine-type compounds. Inhibitor binding loci deduced from chimeras of NHE1 homologues with endogenous differences in inhibitor sensitivity. J. Biol. Chem. 282(27): 19716-19727. doi:10.1074/jbc.M701637200. PMID:17493937. (Pubitemid 47100094)
40. Popot, J.L., and Engelman, D.M. 1990. Membrane protein folding and oligomerization: the two-stage model. Biochemistry, 29(17): 4031-4037. doi:10.1021/bi00469a001. PMID:1694455. (Pubitemid 20145635)
41. Rainey, J.K., Fliegel, L., and Sykes, B.D. 2006. Strategies for dealing with conformational sampling in structural calculations of flexible or kinked transmembrane peptides. Biochem. Cell Biol. 84(6): 918-929. doi:10.1139/O06-178. PMID:17215879. (Pubitemid 46450692)
42. + exchanger. J. Biol. Chem. 283(32): 22018-22030. doi:10.1074/jbc. M803447200. PMID:18508767.
43. + exchanger isoform 1. Biochim. Bio-phys. Acta, 1798(2): 94-104. doi:10.1016/j.bbamem.2009.06. 025. PMID:19595986.
44. Sanders, C.R., and Sonnichsen, F. 2006. Solution NMR of membrane proteins: practice and challenges. Magn. Reson. Chem. 44(S1): S24-S40. doi:10.1002/mrc.1816. PMID:16826539. (Pubitemid 44090388)
45. + exchanger family. J. Biochem. 138(4): 425-431. doi:10.1093/jb/mvi132. PMID: 16272136. (Pubitemid 41703694)
46. Sato, Y., Ariyoshi, N., Mihara, K., and Sakaguchi, M. 2004. Topogenesis of NHE1: direct insertion of the membrane loop and sequestration of cryptic glycosylation and processing sites just after TM9. Biochem. Biophys. Res. Commun. 324(1): 281-287. doi:10.1016/j.bbrc.2004.09.054. PMID:15465015. (Pubitemid 39311491)
47. Schushan, M., Xiang, M., Bogomiakov, P., Padan, E., Rao, R., and Ben-Tal, N. 2010. Model-guided mutagenesis drives functional studies of human NHA2, implicated in hypertension. J. Mol. Biol. 396(5): 1181-1196. doi:10.1016/j.jmb.2009.12.055. PMID: 20053353.
48. Screpanti, E., and Hunte, C. 2007. Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159(2): 261-267. doi:10.1016/j.jsb.2007.01.011. PMID:17350860. (Pubitemid 47095395)
49. + exchanger isoform 1. Biochem. J. 379(1): 31-38. doi:10.1042/BJ20030884. PMID:14680478. (Pubitemid 38491356)
50. + exchanger. J. Biol. Chem. 280(18): 17863-17872. doi:10.1074/jbc.M409608200. PMID:15677483. (Pubitemid 41389027)
51. + exchanger. Bio-chem. J. 401(3): 623-633. doi:10.1042/BJ20061062. PMID: 17209804. (Pubitemid 46219256)
52. + exchanger isoform 1. J. Biol. Chem. 275(11): 7942-7949. doi:10.1074/jbc.275.11.7942. PMID:10713111. (Pubitemid 30159703)
53. + /H+ exchanger. Am. J. Physiol. 269(2 Pt. 1): C392-C402. PMID:7653521.
54. White, S.H., and Wimley, W.C. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28(1): 319-365. doi:10.1146/annurev.biophys.28.1.319. PMID:10410805. (Pubitemid 29319262)
55. White, S.H., Ladokhin, A.S., Jayasinghe, S., and Hristova, K. 2001. How membranes shape protein structure. J. Biol. Chem. 276(35): 32395-32398. doi:10.1074/jbc.R100008200. PMID: 11432876.
56. + /H antiporter sharing evolutionary origins with bacterial NhaA may be a candidate gene for essential hypertension. Proc. Natl. Acad. Sci. U.S.A. 104(47): 18677-18681. doi:10.1073/pnas. 0707120104. PMID:18000046. (Pubitemid 350210756)
57. Zerbini, G., Maestroni, A., Breviario, D., Mangili, R., and Casari, G. 2003. Alternative splicing of NHE-1 mediates Na-Li countertransport and associates with activity rate. Diabetes, 52(6): 1511-1518. doi:10.2337/diabetes. 52.6.1511. PMID:12765964. (Pubitemid 36666208)