Structural and functional characterization of an otopetrin family proton channel

eLife

Volumn 8, Issue , 2019, Pages

  Chen, Qingfeng ^a,b   Zeng, Weizhong ^a,b   She, Ji ^a,b   Bai, Xiao Chen ^b   Jiang, Youxing ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; ASPARTIC ACID; GLUTAMINE; HOMODIMER; OTOPETRIN; PROTEIN; PROTON; TYROSINE; UNCLASSIFIED DRUG; ION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DESENSITIZATION; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMAGE PROCESSING; INFORMATION PROCESSING; MUTAGENESIS; MUTATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTON TRANSPORT; VESTIBULAR SYSTEM; XENOPUS TROPICALIS; ANIMAL; CRYOELECTRON MICROSCOPY; DNA MUTATIONAL ANALYSIS; GENETICS; METABOLISM; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE; XENOPUS;

ANIMALS; CRYOELECTRON MICROSCOPY; DNA MUTATIONAL ANALYSIS; ION CHANNELS; MUTAGENESIS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; XENOPUS;

EID: 85065219757     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.46710     Document Type: Article

References (43)

1. Afonine PV, Poon BK, Read RJ, Sobolev OV, Terwilliger TC, Urzhumtsev A, Adams PD. Real-space refinement in PHENIX for cryo-EM and crystallography. Acta Crystallographica Section D Structural Biology. 2018a;74:531-544. DOI: Https://doi.org/10.1107/S2059798318006551.
2. Afonine PV, Klaholz BP, Moriarty NW, Poon BK, Sobolev OV, Terwilliger TC, Adams PD, Urzhumtsev A. New tools for the analysis and validation of cryo-EM maps and atomic models. Acta Crystallographica Section D Structural Biology. 2018b;74:814-840. DOI: Https://doi.org/10.1107/S2059798318009324.
3. Besson V, Nalesso V, Herpin A, Bizot JC, Messaddeq N, Romand R, Puech A, Blanquet V, Hérault Y. Training and aging modulate the loss-of-balance phenotype observed in a new ENU-induced allele of Otopetrin1. Biology of the Cell. 2005;97:787-798. DOI: Https://doi.org/10.1042/BC20040525.
4. Bron R, Kendal AP, Klenk HD, Wilschut J. Role of the M2 protein in influenza virus membrane fusion: Effects of amantadine and monensin on fusion kinetics. Virology. 1993;195:808-811. DOI: Https://doi.org/10.1006/viro.1993.1435.
5. Bushman JD, Ye W, Liman ER. A proton current associated with sour taste: Distribution and functional properties. The FASEB Journal. 2015;29:3014-3026. DOI: Https://doi.org/10.1096/fj.14-265694.
6. Chang RB, Waters H, Liman ER. A proton current drives action potentials in genetically identified sour taste cells. PNAS. 2010;107:22320-22325. DOI: Https://doi.org/10.1073/pnas.1013664107.
7. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D Biological Crystallography. 2010;66:12-21. DOI: Https://doi.org/10.1107/S0907444909042073.
8. Chovancova E, Pavelka A, Benes P, Strnad O, Brezovsky J, Kozlikova B, Gora A, Sustr V, Klvana M, Medek P, Biedermannova L, Sochor J, Damborsky J. CAVER 3.0: A tool for the analysis of transport pathways in dynamic protein structures. PLOS Computational Biology. 2012;8:e1002708. DOI: Https://doi.org/10.1371/journal.pcbi.1002708.
9. Decoursey TE. Voltage-gated proton channels and other proton transfer pathways. Physiological Reviews. 2003;83:475-579. DOI: Https://doi.org/10.1152/physrev.00028.2002.
10. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of coot. Acta Crystallographica. Section D, Biological Crystallography. 2010;66:486-501. DOI: Https://doi.org/10.1107/S0907444910007493.
11. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science. 2006;314:1458-1461. DOI: Https://doi.org/10.1126/science.1134389.
12. Heymann JB, Belnap DM. Bsoft: Image processing and molecular modeling for electron microscopy. Journal of Structural Biology. 2007;157:3-18. DOI: Https://doi.org/10.1016/j.jsb.2006.06.006.
13. Holm L, Rosenström P. Dali server: Conservation mapping in 3D. Nucleic Acids Research. 2010;38:W545-W549. DOI: Https://doi.org/10.1093/nar/gkq366.
14. Horio N, Yoshida R, Yasumatsu K, Yanagawa Y, Ishimaru Y, Matsunami H, Ninomiya Y. Sour taste responses in mice lacking PKD channels. PLOS ONE. 2011;6:e20007. DOI: Https://doi.org/10.1371/journal.pone.0020007.
15. Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Tränkner D, Ryba NJ, Zuker CS. The cells and logic for mammalian sour taste detection. Nature. 2006;442:934-938. DOI: Https://doi.org/10.1038/nature05084.
16. Hughes I, Blasiole B, Huss D, Warchol ME, Rath NP, Hurle B, Ignatova E, Dickman JD, Thalmann R, Levenson R, Ornitz DM. Otopetrin 1 is required for otolith formation in the zebrafish danio rerio. Developmental Biology. 2004;276:391-402. DOI: Https://doi.org/10.1016/j.ydbio.2004.09.001.
17. Hughes I, Thalmann I, Thalmann R, Ornitz DM. Mixing model systems: Using zebrafish and mouse inner ear mutants and other organ systems to unravel the mystery of otoconial development. Brain Research. 2006;1091:58-74. DOI: Https://doi.org/10.1016/j.brainres.2006.01.074.
18. Hughes I, Saito M, Schlesinger PH, Ornitz DM. Otopetrin 1 activation by purinergic nucleotides regulates intracellular calcium. PNAS. 2007;104:12023-12028. DOI: Https://doi.org/10.1073/pnas.0705182104.
19. Hughes I, Binkley J, Hurle B, Green ED, Sidow A, Ornitz DM, NISC Comparative Sequencing Program Identification of the otopetrin domain, a conserved domain in vertebrate otopetrins and invertebrate otopetrin-like family members. BMC Evolutionary Biology. 2008;8:41. DOI: Https://doi.org/10.1186/1471-2148-8-41.
20. Hurle B, Ignatova E, Massironi SM, Mashimo T, Rios X, Thalmann I, Thalmann R, Ornitz DM. Non-syndromic vestibular disorder with otoconial agenesis in tilted/mergulhador mice caused by mutations in otopetrin 1. Human Molecular Genetics. 2003;12:777-789. DOI: Https://doi.org/10.1093/hmg/ddg087.
21. Hurle B, Marques-Bonet T, Antonacci F, Hughes I, Ryan JF, Eichler EE, Ornitz DM, Green ED, NISC Comparative Sequencing Program Lineage-specific evolution of the vertebrate otopetrin gene family revealed by comparative genomic analyses. BMC Evolutionary Biology. 2011;11:23. DOI: Https://doi.org/10.1186/1471-2148-11-23.
22. Kim E, Hyrc KL, Speck J, Lundberg YW, Salles FT, Kachar B, Goldberg MP, Warchol ME, Ornitz DM. Regulation of cellular calcium in vestibular supporting cells by otopetrin 1. Journal of Neurophysiology. 2010;104:3439-3450. DOI: Https://doi.org/10.1152/jn.00525.2010.
23. Liman ER, Zhang YV, Montell C. Peripheral coding of taste. Neuron. 2014;81:984-1000. DOI: Https://doi.org/10.1016/j.neuron.2014.02.022.
24. Lishko PV, Botchkina IL, Fedorenko A, Kirichok Y. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell. 2010;140:327-337. DOI: Https://doi.org/10.1016/j.cell.2009.12.053.
25. Montell C. pHirst sour taste channels pHound? Science. 2018;359:991-992. DOI: Https://doi.org/10.1126/science.aas9772.
26. Morales-Perez CL, Noviello CM, Hibbs RE. Manipulation of subunit stoichiometry in heteromeric membrane proteins. Structure. 2016;24:797-805. DOI: Https://doi.org/10.1016/j.str.2016.03.004.
27. Morgan D, Capasso M, Musset B, Cherny VV, Rios E, Dyer MJS, DeCoursey TE. Voltage-gated proton channels maintain pH in human neutrophils during phagocytosis. PNAS. 2009;106:18022-18027. DOI: Https://doi.org/10.1073/pnas.0905565106.
28. Ornitz DM, Bohne BA, Thalmann I, Harding GW, Thalmann R. Otoconial agenesis in tilted mutant mice. Hearing Research. 1998;122:60-70. DOI: Https://doi.org/10.1016/S0378-5955(98)00080-X.
29. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF chimera--a visualization system for exploratory research and analysis. Journal of Computational Chemistry. 2004;25:1605-1612. DOI: Https://doi.org/10.1002/jcc.20084.
30. Pinto LH, Holsinger LJ, Lamb RA. Influenza virus M2 protein has ion channel activity. Cell. 1992;69:517-528. DOI: Https://doi.org/10.1016/0092-8674(92)90452-I.
31. Ramsey IS, Moran MM, Chong JA, Clapham DE. A voltage-gated proton-selective channel lacking the pore domain. Nature. 2006;440:1213-1216. DOI: Https://doi.org/10.1038/nature04700.
32. Ramsey IS, DeSimone JA. Otopetrin-1: A sour-tasting proton channel. The Journal of General Physiology. 2018;150:379-382. DOI: Https://doi.org/10.1085/jgp.201812003.
33. Sasaki M, Takagi M, Okamura Y. A voltage sensor-domain protein is a voltage-gated proton channel. Science. 2006;312:589-592. DOI: Https://doi.org/10.1126/science.1122352.
34. Scheres SH. RELION: Implementation of a bayesian approach to cryo-EM structure determination. Journal of Structural Biology. 2012;180:519-530. DOI: Https://doi.org/10.1016/j.jsb.2012.09.006.
35. Söllner C, Schwarz H, Geisler R, Nicolson T. Mutated otopetrin 1 affects the genesis of otoliths and the localization of starmaker in zebrafish. Development Genes and Evolution. 2004;214:582-590. DOI: Https://doi.org/10.1007/s00427-004-0440-2.
36. Tu YH, Cooper AJ, Teng B, Chang RB, Artiga DJ, Turner HN, Mulhall EM, Ye W, Smith AD, Liman ER. An evolutionarily conserved gene family encodes proton-selective ion channels. Science. 2018;359:1047-1050. DOI: Https://doi.org/10.1126/science.aao3264.
37. Waldner C, Roose M, Ryffel GU. Red fluorescent Xenopus laevis: A new tool for grafting analysis. BMC Developmental Biology. 2009;9:37. DOI: Https://doi.org/10.1186/1471-213X-9-37.
38. Walker JE. The ATP synthase: The understood, the uncertain and the unknown. Biochemical Society Transactions. 2013;41:1-16. DOI: Https://doi.org/10.1042/BST20110773.
39. White C, Nixon A, Bradbury NA. Determining membrane protein topology using fluorescence protease protection (FPP) Journal of Visualized Experiments. 2015;20:e52509. DOI: Https://doi.org/10.3791/52509.
40. Yarmolinsky DA, Zuker CS, Ryba NJ. Common sense about taste: From mammals to insects. Cell. 2009;139:234-244. DOI: Https://doi.org/10.1016/j.cell.2009.10.001.
41. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ. Coding of sweet, bitter, and umami tastes: Different receptor cells sharing similar signaling pathways. Cell. 2003;112:293-301. DOI: Https://doi.org/10.1016/s0092-8674(03)00071-0.
42. Zhang K. Gctf: Real-time CTF determination and correction. Journal of Structural Biology. 2016;193:1-12. DOI: Https://doi.org/10.1016/j.jsb.2015.11.003.
43. Zheng SQ, Palovcak E, Armache J-P, Verba KA, Cheng Y, Agard DA. MotionCor2: Anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nature Methods. 2017;14:331-332. DOI: Https://doi.org/10.1038/nmeth.4193.