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Holo- and apo-bound structures of bacterial periplasmic heme-binding proteins.

Ho WW, Li H, Eakanunkul S, Tong Y, Wilks A, Guo M, Poulos TL
J Biol Chem 282 35796-802 (2007)
Related entries: 2r7a, 2rg7

Cited: 45 times
EuropePMC logo PMID: 17925389

Abstract

An essential component of heme transport in Gram-negative bacterial pathogens is the periplasmic protein that shuttles heme between outer and inner membranes. We have solved the first crystal structures of two such proteins, ShuT from Shigella dysenteriae and PhuT from Pseudomonas aeruginosa. Both share a common architecture typical of Class III periplasmic binding proteins. The heme binds in a narrow cleft between the N- and C-terminal binding domains and is coordinated by a Tyr residue. A comparison of the heme-free (apo) and -bound (holo) structures indicates little change in structure other than minor alterations in the heme pocket and movement of the Tyr heme ligand from an "in" position where it can coordinate the heme iron to an "out" orientation where it points away from the heme pocket. The detailed architecture of the heme pocket is quite different in ShuT and PhuT. Although Arg(228) in PhuT H-bonds with a heme propionate, in ShuT a peptide loop partially takes up the space occupied by Arg(228), and there is no Lys or Arg H-bonding with the heme propionates. A comparison of PhuT/ShuT with the vitamin B(12)-binding protein BtuF and the hydroxamic-type siderophore-binding protein FhuD, the only two other structurally characterized Class III periplasmic binding proteins, demonstrates that PhuT/ShuT more closely resembles BtuF, which reflects the closer similarity in ligands, heme and B(12), compared with ligands for FhuD, a peptide siderophore.

Reviews - 2r79 mentioned but not cited (1)

  1. Iron Acquisition in Mycobacterium tuberculosis. Chao A, Sieminski PJ, Owens CP, Goulding CW. Chem. Rev. 119 1193-1220 (2019)

Articles - 2r79 mentioned but not cited (2)

  1. Characterization of a Bacillus subtilis transporter for petrobactin, an anthrax stealth siderophore. Zawadzka AM, Kim Y, Maltseva N, Nichiporuk R, Fan Y, Joachimiak A, Raymond KN. Proc. Natl. Acad. Sci. U.S.A. 106 21854-21859 (2009)
  2. Extracellular haem utilization by the opportunistic pathogen Pseudomonas aeruginosa and its role in virulence and pathogenesis. Mouriño S, Wilks A. Adv Microb Physiol 79 89-132 (2021)


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  1. Iron uptake and metabolism in pseudomonads. Cornelis P. Appl. Microbiol. Biotechnol. 86 1637-1645 (2010)
  2. Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. Eitinger T, Rodionov DA, Grote M, Schneider E. FEMS Microbiol. Rev. 35 3-67 (2011)
  3. Bacterial heme-transport proteins and their heme-coordination modes. Tong Y, Guo M. Arch. Biochem. Biophys. 481 1-15 (2009)
  4. Bacterial ATP-driven transporters of transition metals: physiological roles, mechanisms of action, and roles in bacterial virulence. Klein JS, Lewinson O. Metallomics 3 1098-1108 (2011)
  5. Role and regulation of heme iron acquisition in gram-negative pathogens. Runyen-Janecky LJ. Front Cell Infect Microbiol 3 55 (2013)
  6. Recent advances in bacterial heme protein biochemistry. Mayfield JA, Dehner CA, DuBois JL. Curr Opin Chem Biol 15 260-266 (2011)
  7. A structural and functional analysis of type III periplasmic and substrate binding proteins: their role in bacterial siderophore and heme transport. Chu BC, Vogel HJ. Biol. Chem. 392 39-52 (2011)
  8. Extracellular Heme Uptake and the Challenge of Bacterial Cell Membranes. Huang W, Wilks A. Annu. Rev. Biochem. 86 799-823 (2017)
  9. Heme Uptake and Utilization by Gram-Negative Bacterial Pathogens. Richard KL, Kelley BR, Johnson JG. Front Cell Infect Microbiol 9 81 (2019)
  10. Structures and coordination chemistry of transporters involved in manganese and iron homeostasis. Ray S, Gaudet R. Biochem Soc Trans 51 897-923 (2023)

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  2. Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Beasley FC, Vinés ED, Grigg JC, Zheng Q, Liu S, Lajoie GA, Murphy ME, Heinrichs DE. Mol Microbiol 72 947-963 (2009)
  3. A distinct mechanism for the ABC transporter BtuCD-BtuF revealed by the dynamics of complex formation. Lewinson O, Lee AT, Locher KP, Rees DC. Nat. Struct. Mol. Biol. 17 332-338 (2010)
  4. The Staphylococcus aureus siderophore receptor HtsA undergoes localized conformational changes to enclose staphyloferrin A in an arginine-rich binding pocket. Grigg JC, Cooper JD, Cheung J, Heinrichs DE, Murphy ME. J. Biol. Chem. 285 11162-11171 (2010)
  5. Characterization of heme ligation properties of Rv0203, a secreted heme binding protein involved in Mycobacterium tuberculosis heme uptake. Owens CP, Du J, Dawson JH, Goulding CW. Biochemistry 51 1518-1531 (2012)
  6. Mapping ultra-weak protein-protein interactions between heme transporters of Staphylococcus aureus. Abe R, Caaveiro JM, Kozuka-Hata H, Oyama M, Tsumoto K. J. Biol. Chem. 287 16477-16487 (2012)
  7. Specificity of Staphyloferrin B recognition by the SirA receptor from Staphylococcus aureus. Grigg JC, Cheung J, Heinrichs DE, Murphy ME. J. Biol. Chem. 285 34579-34588 (2010)
  8. Functional characterization of the Shigella dysenteriae heme ABC transporter. Burkhard KA, Wilks A. Biochemistry 47 7977-7979 (2008)
  9. Induced fit on heme binding to the Pseudomonas aeruginosa cytoplasmic protein (PhuS) drives interaction with heme oxygenase (HemO). O'Neill MJ, Bhakta MN, Fleming KG, Wilks A. Proc. Natl. Acad. Sci. U.S.A. 109 5639-5644 (2012)
  10. Product release rather than chelation determines metal specificity for ferrochelatase. Medlock AE, Carter M, Dailey TA, Dailey HA, Lanzilotta WN. J. Mol. Biol. 393 308-319 (2009)
  11. Spectroscopic and mutagenesis studies of human PGRMC1. Kaluka D, Batabyal D, Chiang BY, Poulos TL, Yeh SR. Biochemistry 54 1638-1647 (2015)
  12. Differential contributions of the outer membrane receptors PhuR and HasR to heme acquisition in Pseudomonas aeruginosa. Smith AD, Wilks A. J. Biol. Chem. 290 7756-7766 (2015)
  13. Helicobacter pylori periplasmic receptor CeuE (HP1561) modulates its nickel affinity via organic metallophores. Shaik MM, Cendron L, Salamina M, Ruzzene M, Zanotti G. Mol. Microbiol. 91 724-735 (2014)
  14. Molecular dynamics simulations of the bacterial periplasmic heme binding proteins ShuT and PhuT. Liu M, Su JG, Kong R, Sun TG, Tan JJ, Chen WZ, Wang CX. Biophys. Chem. 138 42-49 (2008)
  15. Replacing the axial ligand tyrosine 75 or its hydrogen bond partner histidine 83 minimally affects hemin acquisition by the hemophore HasAp from Pseudomonas aeruginosa. Kumar R, Matsumura H, Lovell S, Yao H, Rodríguez JC, Battaile KP, Moënne-Loccoz P, Rivera M. Biochemistry 53 2112-2125 (2014)
  16. Extracellular heme uptake and the challenges of bacterial cell membranes. Smith AD, Wilks A. Curr Top Membr 69 359-392 (2012)
  17. FecB, a periplasmic ferric-citrate transporter from E. coli, can bind different forms of ferric-citrate as well as a wide variety of metal-free and metal-loaded tricarboxylic acids. Banerjee S, Paul S, Nguyen LT, Chu BC, Vogel HJ. Metallomics 8 125-133 (2016)
  18. Study on the mechanism of the BtuF periplasmic-binding protein for vitamin B12. Liu M, Sun T, Hu J, Chen W, Wang C. Biophys. Chem. 135 19-24 (2008)
  19. The solution structure, binding properties, and dynamics of the bacterial siderophore-binding protein FepB. Chu BC, Otten R, Krewulak KD, Mulder FA, Vogel HJ. J. Biol. Chem. 289 29219-29234 (2014)
  20. Crystal structure of the Pseudomonas aeruginosa cytoplasmic heme binding protein, Apo-PhuS. Tripathi S, O'Neill MJ, Wilks A, Poulos TL. J. Inorg. Biochem. 128 131-136 (2013)
  21. Spectroscopic Determination of Distinct Heme Ligands in Outer-Membrane Receptors PhuR and HasR of Pseudomonas aeruginosa. Smith AD, Modi AR, Sun S, Dawson JH, Wilks A. Biochemistry 54 2601-2612 (2015)
  22. Heme Binding by Corynebacterium diphtheriae HmuT: Function and Heme Environment. Draganova EB, Akbas N, Adrian SA, Lukat-Rodgers GS, Collins DP, Dawson JH, Allen CE, Schmitt MP, Rodgers KR, Dixon DW. Biochemistry 54 6598-6609 (2015)
  23. Corynebacterium diphtheriae HmuT: dissecting the roles of conserved residues in heme pocket stabilization. Draganova EB, Adrian SA, Lukat-Rodgers GS, Keutcha CS, Schmitt MP, Rodgers KR, Dixon DW. J. Biol. Inorg. Chem. 21 875-886 (2016)
  24. Designating ligand specificities to metal uptake ABC transporters in Thermus thermophilus HB8. Mandal SK, Adhikari R, Sharma A, Chandravanshi M, Gogoi P, Kanaujia SP. Metallomics 11 597-612 (2019)
  25. Ligand binding specificity of the Escherichia coli periplasmic histidine binding protein, HisJ. Paul S, Banerjee S, Vogel HJ. Protein Sci. 26 268-279 (2017)
  26. Structural Characterization of Heme Environmental Mutants of CgHmuT that Shuttles Heme Molecules to Heme Transporters. Muraki N, Kitatsuji C, Ogura M, Uchida T, Ishimori K, Aono S. Int J Mol Sci 17 (2016)
  27. Structural basis for binding and transfer of heme in bacterial heme-acquisition systems. Naoe Y, Nakamura N, Rahman MM, Tosha T, Nagatoishi S, Tsumoto K, Shiro Y, Sugimoto H. Proteins 85 2217-2230 (2017)
  28. Structure and functional analysis of the siderophore periplasmic binding protein from the fuscachelin gene cluster of Thermobifida fusca. Li K, Bruner SD. Proteins 84 118-128 (2016)
  29. Characterization of the second conserved domain in the heme uptake protein HtaA from Corynebacterium diphtheriae. Uluisik RC, Akbas N, Lukat-Rodgers GS, Adrian SA, Allen CE, Schmitt MP, Rodgers KR, Dixon DW. J. Inorg. Biochem. 167 124-133 (2017)
  30. Differentiating the roles of Mycobacterium tuberculosis substrate binding proteins, FecB and FecB2, in iron uptake. de Miranda R, Cuthbert BJ, Klevorn T, Chao A, Mendoza J, Arbing M, Sieminski PJ, Papavinasasundaram K, Abdul-Hafiz S, Chan S, Sassetti CM, Ehrt S, Goulding CW. PLoS Pathog 19 e1011650 (2023)
  31. Genome scale identification, structural analysis, and classification of periplasmic binding proteins from Mycobacterium tuberculosis. Sandhu P, Kumari M, Naini K, Akhter Y. Curr. Genet. 63 553-576 (2017)
  32. Structure and dynamics of Type III periplasmic proteins VcFhuD and VcHutB reveal molecular basis of their distinctive ligand binding properties. Agarwal S, Dey S, Ghosh B, Biswas M, Dasgupta J. Sci Rep 7 42812 (2017)


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