The formate/nitrite transporter family of anion channels

Biological Chemistry

Volumn 394, Issue 6, 2013, Pages 715-727

  Lü, Wei ^a   Du, Juan ^a   Schwarzer, Nikola J ^a   Wacker, Tobias ^a   Andrade, Susana L A ^a   Einsle, Oliver ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Electrophysiology; Formate channel; Hydrosulfide channel; Membrane proteins; Nitrite channel; Protein crystallography

Indexed keywords

ACETIC ACID; ACETYL COENZYME A; ANION CHANNEL; BACTERIAL PROTEIN; CHLORIDE; FOCA CHANNEL; FORMATE NITRITE TRANSPORTER; FORMIC ACID; HSC CHANNEL; LACTIC ACID; MEMBRANE PROTEIN; NIRC CHANNEL; NITRITE; PYRUVIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CHANNEL GATING; ESCHERICHIA COLI; HUMAN; NITROGEN CYCLE; NITROGEN FIXATION; NONHUMAN; PASSIVE TRANSPORT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; REVIEW; SALMONELLA TYPHIMURIUM;

ANIMALS; ANIONS; FORMATES; HUMANS; ION CHANNELS; ION TRANSPORT; MODELS, MOLECULAR; NITRITES;

EID: 84881115596     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0339     Document Type: Review

References (44)

1. Agre, P., King, L.S., Yasui, M., Guggino, W.B., Ottersen, O.P., Fujiyoshi, Y., Engel, A., and Nielsen, S. (2002). Aquaporin water channels - from atomic structure to clinical medicine. J. Physiol. 542, 3-16. (Pubitemid 35190266)
2. Berks, B.C., Ferguson, S.J., Moir, J.W.B., and Richardson, D.J. (1995). Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim. Biophys. Acta 1232, 97-173.
3. Brett, P.J., Burtnick, M.N., Su, H., Nair, V., and Gherardini, F.C. (2008). iNOS activity is critical for the clearance of Burkholderia mallei from infected RAW 264.7 murine macrophages. Cell Microbiol. 10, 487-498.
4. Chakravortty, D. and Hensel, M. (2003). Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microb. Infect. 5, 621-627. (Pubitemid 36645122)
5. Clegg, S., Yu, F., Griffiths, L., and Cole, J.A. (2002). The roles of the polytopic membrane proteins NarK, NarU and NirC in Escherichia coli K-12: two nitrate and three nitrite transporters. Mol. Microbiol. 44, 143-155. (Pubitemid 34429771)
6. Cole, J. (1996). Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol. Lett. 136, 1-11. (Pubitemid 26063443)
7. Czyzewski, B.K. and Wang, D.N. (2012). Identification and characterization of a bacterial hydrosulphide ion channel. Nature 483, 494-497.
8. Das, P., Lahiri, A., Lahiri, A., and Chakravortty, D. (2009). Novel role of the nitrite transporter NirC in Salmonella pathogenesis: SPI2-dependent suppression of inducible nitric oxide synthase in activated macrophages. Microbiology 155, 2476-2489.
9. Delomenie, C., Foti, E., Floch, E., Diderot, V., Porquet, D., Dupuy, C., and Bonaly, J. (2007). A new homolog of FocA transporters identified in cadmium-resistant Euglena gracilis. Biochem. Biophys. Res. Commun. 358, 455-461. (Pubitemid 46755726)
10. Einsle, O. (2011). Structure and function of formate-dependent cytochrome c nitrite reductase, NrfA. Methods Enzymol. 496, 399-422.
11. Einsle, O. and Kroneck, P.M.H. (2004). Structural basis of denitrification. Biol. Chem. 385, 875-883. (Pubitemid 39481134)
12. Eisenman, G. and Horn, R. (1983). Ionic selectivity revisited - the role of kinetic and equilibrium processes in ion permeation through channels. J. Membr. Biol. 76, 197-225. (Pubitemid 14201481)
13. Falke, D., Schulz, K., Doberenz, C., Beyer, L., Lilie, H., Thiemer, B., and Sawers, R.G. (2010). Unexpected oligomeric structure of the FocA formate channel of Escherichia coli: a paradigm for the formate-nitrite transporter family of integral membrane proteins. FEMS Microbiol. Lett. 303, 69-75.
14. Feng, Z., Hou, T., and Li, Y. (2012). Concerted movement in pH-dependent gating of FocA from molecular dynamics simulations. J. Chem. Inf. Model. 52, 2119-2131.
15. Hille, B. (2001). Ion Channels of Excitable Membranes, 3rd edition. (Sunderland, MA: Sinauer Associates).
16. Jia, W.J., Tovell, N., Clegg, S., Trimmer, M., and Cole, J. (2009). A single channel for nitrate uptake, nitrite export and nitrite uptake by Escherichia coli NarU and a role for NirC in nitrite export and uptake. Biochem. J. 417, 297-304.
17. Kaback, H.R. (1974). Transport studies in bacterial-membrane vesicles. Science 186, 882-892.
18. Knappe, J. and Sawers, G. (1990). A radical-chemical route to acetyl-CoA - the anaerobically induced pyruvate formate-lyase system of Escherichia coli. FEMS Microbiol. Rev. 75, 383-398. (Pubitemid 20281612)
19. Latorre, R. and Miller, C. (1983). Conduction and selectivity in potassium channels. J. Membr. Biol. 71, 11-30. (Pubitemid 13156990)
20. Leonhartsberger, S., Korsa, I., and Böck, A. (2002). The molecular biology of formate metabolism in enterobacteria. J. Mol. Microb. Biotechnol. 4, 269-276. (Pubitemid 34256702)
21. Lü, W., Du, J., Wacker, T., Gerbig-Smentek, E., Andrade, S.L.A., and Einsle, O. (2011). pH-Dependent gating in a FocA formate channel. Science 332, 352-354.
22. L ü, W., Du, J., Schwarzer, N.J., Gerbig-Smentek, E., Einsle, O., and Andrade, S.L. (2012a). The formate channel FocA exports the products of mixed-acid fermentation. Proc. Natl. Acad. Sci. USA 109, 13254-13259.
23. L ü, W., Schwarzer, N.J., Du, J., Gerbig-Smentek, E., Andrade, S.L.A., and Einsle, O. (2012b). Structural and functional characterization of the nitrite channel NirC from Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 109, 18395-18400.
24. Martinez-Espinosa, R.M., Cole, J.A., Richardson, D.J., and Watmough, N.J. (2011). Enzymology and ecology of the nitrogen cycle. Biochem. Soc. Trans. 39, 175-178.
25. Miller, C. (2006). CIC chloride channels viewed through a transporter lens. Nature 440, 484-489.
26. Moir, J.W.B. and Wood, N.J. (2001). Nitrate and nitrite transport in bacteria. Cell. Mol. Life Sci. 58, 215-224. (Pubitemid 32217353)
27. Peakman, T., Crouzet, J., Mayaux, J.F., Busby, S., Mohan, S., Harborne, N., Wootton, J., Nicolson, R., and Cole, J.A. (1990). Nucleotide sequence, organisation and structural analysis of the products of genes in the nirB-cysG region of the Escherichia coli K-12 chromosome. Eur. J. Biochem. 191, 315-323. (Pubitemid 20233744)
28. Rosen, B.P. (1986). Ion extrusion systems in Escherichia coli. Methods Enzymol. 125, 328-336. (Pubitemid 16072648)
29. Rycovska, A., Hatahet, L., Fendler, K., and Michel, H. (2012). The nitrite transport protein NirC from Salmonella typhimurium is a nitrite/proton antiporter. Biochim. Biophys. Acta 1818, 1342-1350.
30. Saier, M.H. Jr., Eng, B.H., Fard, S., Garg, J., Haggerty, D.A., Hutchinson, W.J., Jack, D.L., Lai, E.C., Liu, H.J., Nusinew, D.P., et al. (1999). Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim. Biophys. Acta 1422, 1-56. (Pubitemid 29114906)
31. Sawers, G. (1998). Biochemistry, physiology and molecular biology of glycyl radical enzymes. FEMS Microbiol. Rev. 22, 543-551. (Pubitemid 29074352)
32. Sawers, R.G. (2005). Formate and its role in hydrogen production in Escherichia coli. Biochem. Soc. Trans. 33, 42-46. (Pubitemid 40313757)
33. Singer, S.J. (1990). The structure and insertion of integral proteins in membranes. Annu. Rev. Cell. Biol. 6, 247-296.
34. Singer, S.J. and Nicolson, G.L. (1972). Fluid mosaic model of structure of cell membranes. Science 175, 720-731.
35. Slater, E.C., Skulache,V.P., Azzone, G.F., Crofts, A.R., Pressman, B.C., Ernster, L., Harold, F.M., Kaback, H.R., Hinkle, P., Weber, M., et al. (1974). Mechanisms of active-transport - general discussion. Ann. NY Acad. Sci. 227, 348-354.
36. Smart, O.S., Neduvelil, J.G., Wang, X., Wallace, B.A., and Sansom, M.S. (1996). HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14, 354-360. (Pubitemid 27302826)
37. Suppmann, B. and Sawers, G. (1994). Isolation and characterization of hypophosphite-resistant mutants of Escherichia coli - identification of the FocA protein, encoded by the pfl operon, as a putative formate transporter. Mol. Microbiol. 11, 965-982. (Pubitemid 24199664)
38. Tsien, R.W., Hess, P., Mccleskey, E.W., and Rosenberg, R.L. (1987). Calcium channels - mechanisms of selectivity, permeation, and block. Annu. Rev. Biophys. Biol. 16, 265-290.
39. von Heijne, G. and Gavel, Y. (1988). Topogenic signals in integral membrane proteins. Eur. J. Biochem. 174, 671-678.
40. Waight, A.B., Love, J., and Wang, D.N. (2010). Structure and mechanism of a pentameric formate channel. Nat. Struct. Mol. Biol. 17, 31-37.
41. Wang, Y., Huang, Y.J., Wang, J.W., Cheng, C., Huang, W.J., Lu, P.L., Xu, Y.N., Wang, P.Y., Yan, N., and Shi, Y.G. (2009). Structure of the formate transporter FocA reveals a pentameric aquaporin-like channel. Nature 462, 467-472.
42. White, W.B. and Ferry, J.G. (1992). Identification of formate dehydrogenase-specific messenger-RNA species and nucleotide-sequence of the fdhC gene of Methanobacterium formicicum. J. Bacteriol. 174, 4997-5004.
43. Xie, Q. and Nathan, C. (1994). The high-output nitric oxide pathway: role and regulation. J. Leukoc. Biol. 56, 576-582. (Pubitemid 24348815)
44. Yang, Y.T., Bennett, G.N., and San, K.Y. (2001). The effects of feed and intracellular pyruvate levels on the redistribution of metabolic fluxes in Escherichia coli. Metab. Eng. 3, 115-123. (Pubitemid 32930967)