Crystal structure of a phosphorylation-coupled saccharide transporter

Nature

Volumn 473, Issue 7345, 2011, Pages 50-54

  Cao, Yu ^a   Jin, Xiangshu ^b   Levin, Elena J ^a   Huang, Hua ^a   Zong, Yinong ^c   Quick, Matthias ^d,e   Weng, Jun ^a   Pan, Yaping ^a   Love, James ^f   Punta, Marco ^f,g   Rost, Burkhard ^f,g   Hendrickson, Wayne A ^d,f   Javitch, Jonathan A ^d,e   Rajashankar, Kanagalaghatta R ^h   Zhou, Ming ^a  

^a Columbia University ^*  (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c BURNHAM INSTITUTE   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^f NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^g TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^h Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHITOBIOSE; N,N' DIACETYLCHITOBIOSE; PROTEIN CHBC; UNCLASSIFIED DRUG;

AMINO ACID; CRYSTAL STRUCTURE; ENZYME ACTIVITY; MEMBRANE; PHYLOGENETICS; PROTEIN; SUBSTRATE; SUGAR; TRANSLOCATION;

ARTICLE; BACILLUS CEREUS; BINDING SITE; CARBOHYDRATE TRANSPORT; CRYSTAL STRUCTURE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

BACILLUS CEREUS; BINDING SITES; CARBOHYDRATE METABOLISM; CRYSTALLIZATION; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

BACILLUS CEREUS;

EID: 79955593495     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09939     Document Type: Article

References (50)

1. Kundig, W., Ghosh, S. & Roseman, S. Phosphate bound to histidine in a protein as an intermediate in a novel phospho-transferase system. Proc. Natl Acad. Sci. USA 52, 1067-1074 (1964).
2. Postma, P. W., Lengeler, J. W. & Jacobson, G. R. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57, 543-594 (1993). (Pubitemid 23262509)
3. Postma, P. W. & Lengeler, J. W. Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. Microbiol. Rev. 49, 232-269 (1985).
4. Siebold, C., Flü kiger, K., Beutler, R. & Erni, B. Carbohydrate transporters of the bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS). FEBS Lett. 504, 104-111 (2001). (Pubitemid 32787057)
5. Robillard, G. T. & Broos, J. Structure/function studies on the bacterial carbohydrate transporters, enzymes II, of the phosphoenolpyruvate- dependent phosphotransferase system. Biochim. Biophys. Acta 1422, 73-104 (1999). (Pubitemid 29313326)
6. Nguyen, T. X., Yen, M. R., Barabote, R. D.& Saier, M. H. Jr. Topological predictions for integral membrane permeases of the phosphoenolpyruvate:sugar phosphotransferase system. J. Mol. Microbiol. Biotechnol. 11, 345-360 (2006).
7. Meadow, N. D., Fox, D. K. & Roseman, S. The bacterial phosphoenolpyruvate: glycose phosphotransferase system. Annu. Rev. Biochem. 59, 497-542 (1990).
8. Rees, D. C., Johnson, E. & Lewinson, O. ABC transporters: the power to change. Nature Rev. Mol. Cell Biol. 10, 218-227 (2009).
9. Davidson, A. L., Dassa, E., Orelle, C. & Chen, J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364 (2008). (Pubitemid 351822295)
10. Krishnamurthy, H., Piscitelli, C. L. & Gouaux, E. Unlocking the molecular secrets of sodium-coupled transporters. Nature 459, 347-355 (2009).
11. Lemieux, M. J., Huang, Y. & Wang, D. N. The structural basis of substrate translocation by the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily. Curr. Opin. Struct. Biol. 14, 405-412 (2004). (Pubitemid 39099284)
12. Abramson, J., Kaback, H. R. & Iwata, S. Structural comparison of lactose permease and the glycerol-3-phosphate antiporter: members of the major facilitator superfamily. Curr. Opin. Struct. Biol. 14, 413-419 (2004). (Pubitemid 39099285)
13. Rephaeli, A. W. & Saier, M. H. Jr. Regulation of genes coding for enzyme constituents of the bacterial phosphotransferase system. J. Bacteriol. 141, 658-663 (1980). (Pubitemid 10110856)
14. Deutscher, J., Francke, C. & Postma, P. W.Howphosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70, 939-1031 (2006). (Pubitemid 44958262)
15. Saier, M. H., Hvorup, R. N. & Barabote, R. D. Evolution of the bacterial phosphotransferase system: from carriers and enzymes to group translocators. Biochem. Soc. Trans. 33, 220-224 (2005). (Pubitemid 40313807)
16. Saraceni-Richards, C. A. & Jacobson, G. R. Subunit and amino acid interactions in the Escherichia coli mannitol permease: a functional complementation study of coexpressed mutant permease proteins. J. Bacteriol. 179, 5171-5177 (1997). (Pubitemid 27340553)
17. Saraceni-Richards, C. A. & Jacobson, G. R. A conserved glutamate residue, Glu- 257, is important for substrate binding and transport by the Escherichia coli mannitol permease. J. Bacteriol. 179, 1135-1142 (1997). (Pubitemid 27076576)
18. Keyhani, N. O. & Roseman, S. Wild-type Escherichia coli grows on the chitin disaccharide, N,N9-diacetylchitobiose, by expressing the cel operon. Proc. Natl Acad. Sci. USA 94, 14367-14371 (1997).
19. Keyhani, N. O., Wang, L. X., Lee, Y. C. & Roseman, S. The chitin disaccharide, N,N9- diacetylchitobiose, is catabolized by Escherichia coli and is transported/ phosphorylated by the phosphoenolpyruvate:glycose phosphotransferase system. J. Biol. Chem. 275, 33084-33090 (2000).
20. van Montfort, B. A. et al. Mapping of the dimer interface of the Escherichia coli mannitol permease by cysteine cross-linking. J. Biol. Chem. 277, 14717-14723 (2002). (Pubitemid 34952542)
21. Erni, B. Glucose-specific permease of the bacterial phosphotransferase system: phosphorylation and oligomeric structure of the glucose-specific IIGlc-IIIGlc complex of Salmonella typhimurium. Biochemistry 25, 305-312 (1986). (Pubitemid 16053789)
22. Pas, H. H., Ellory, J. C.& Robillard, G. T. Bacterial phosphoenolpyruvate-dependent phosphotransferase system: association state of membrane-bound mannitolspecific enzyme II demonstrated by inactivation. Biochemistry 26, 6689-6696 (1987).
23. Khandekar, S. S. & Jacobson, G. R. Evidence for two distinct conformations of the Escherichia coli mannitol permease that are important for its transport and phosphorylation functions. J. Cell. Biochem. 39, 207-216 (1989). (Pubitemid 19062786)
24. Chen, Q. & Amster-Choder, O. BglF, the sensor of the bgl system and the b-glucosides permease of Escherichia coli: evidence for dimerization and intersubunit phosphotransfer. Biochemistry 37, 8714-8723 (1998). (Pubitemid 28299609)
25. von Heijne, G. & Gavel, Y. Topogenic signals in integral membrane proteins. Eur. J. Biochem. 174, 671-678 (1988).
26. Daley, D. O. et al. Global topology analysis of the Escherichia coli inner membrane proteome. Science 308, 1321-1323 (2005). (Pubitemid 40746130)
27. Sugiyama, J. E., Mahmoodian, S. & Jacobson, G. R. Membrane topology analysis of Escherichia coli mannitol permease by using a nested-deletion method to create mtlA-phoA fusions. Proc. Natl Acad. Sci. USA 88, 9603-9607 (1991). (Pubitemid 21915679)
28. Buhr, A. & Erni, B. Membrane topology of the glucose transporter of Escherichia coli. J. Biol. Chem. 268, 11599-11603 (1993). (Pubitemid 23168106)
29. Yagur-Kroll, S. & Amster-Choder, O. Dynamic membrane topology of the Escherichia coli b-glucoside transporter BglF. J. Biol. Chem. 280, 19306-19318 (2005). (Pubitemid 41379638)
30. Koning, R. I. et al. The 5 A projection structure of the transmembrane domain of the mannitol transporter enzyme II. J. Mol. Biol. 287, 845-851 (1999). (Pubitemid 29188871)
31. Yernool, D., Boudker, O., Jin, Y. & Gouaux, E. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431, 811-818 (2004). (Pubitemid 39434071)
32. Weng, Q. P. & Jacobson, G. R. Role of a conserved histidine residue, His-195, in the activities of the Escherichia coli mannitol permease. Biochemistry 32, 11211-11216 (1993). (Pubitemid 23332030)
33. Weng, Q. P., Elder, J. & Jacobson, G. R. Site-specific mutagenesis of residues in the Escherichia coli mannitol permease that have been suggested to be important for its phosphorylation and chemoreception functions. J. Biol. Chem. 267, 19529-19535 (1992).
34. Opacić, M., Vos, E. P., Hesp, B. H. & Broos, J. Localization of the substrate-binding site in the homodimeric mannitol transporter, EIImtl, of Escherichia coli. J. Biol. Chem. 285, 25324-25331 (2010).
35. Widdas, W. F. Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer. J. Physiol. (Lond.) 118, 23-39 (1952).
36. Yamashita, A. et al. Crystal structure of a bacterial homologue of Na1/Cl2- dependent neurotransmitter transporters. Nature 437, 215-223 (2005). (Pubitemid 41294479)
37. Reyes, N., Ginter, C. & Boudker, O. Transportmechanismof a bacterial homologue of glutamate transporters. Nature 462, 880-885 (2009).
38. Shi, L. et al. The mechanism of a neurotransmitter:sodium symporter-inward release ofNa1 and substrate is triggered by substrate in a secondbinding site.Mol. Cell 30, 667-677 (2008). (Pubitemid 351815131)
39. Love, J. et al. The New York Consortium on Membrane Protein Structure (NYCOMPS): a high-throughput platform for structural genomics of integral membrane proteins. J. Struct. Funct. Genomics 11, 191-199 (2010).
40. Zhou, M. & MacKinnon, R. A mutant KcsA K1 channel with altered conduction properties and selectivity filter ion distribution. J. Mol. Biol. 338, 839-846 (2004). (Pubitemid 38507426)
41. Rocchia, W. et al. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects. J. Comput. Chem. 23, 128-137 (2002). (Pubitemid 34063137)
42. Punta, M. et al. Structural genomics target selection for the New York Consortium on Membrane Protein Structure. J. Struct. Funct. Genomics 10, 255-268 (2009).
43. Levin, E. J., Quick, M. & Zhou, M. Crystal structure of a bacterial homologue of the kidney urea transporter. Nature 462, 757-761 (2009).
44. Schaffner, W. & Weissmann, C. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56, 502-514 (1973).
45. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
46. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
47. de La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494 (1997). (Pubitemid 27085618)
48. Cowtan, K. Error estimation and bias correction in phase-improvement calculations. Acta Crystallogr. D 55, 1555-1567 (1999). (Pubitemid 29449865)
49. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004). (Pubitemid 41742764)
50. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).