Extracellular Heme Uptake and the Challenge of Bacterial Cell Membranes

Literature Cited

1. Dlouhy AC, Outten CE. 1.  2013. The iron metallome in eukaryotic organisms. Met. Ions Life Sci. 12:241–78 [Google Scholar]
2. Becker KW, Skaar EP. 2.  2014. Metal limitation and toxicity at the interface between host and pathogen. FEMS Microbiol. Rev. 38:1235–49 [Google Scholar]
3. Otto BR, Verweij-van Vught AM, MacLaren DM. 3.  1992. Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit. Rev. Microbiol. 18:217–33 [Google Scholar]
4. Barber MF, Elde NC. 4.  2014. Escape from bacterial iron piracy through rapid evolution of transferrin. Science 346:1362–66 [Google Scholar]
5. Schmidt PJ. 5.  2015. Regulation of iron metabolism by hepcidin under conditions of inflammation. J. Biol. Chem. 290:18975–83 [Google Scholar]
6. Clifton MC, Corrent C, Strong RK. 6.  2009. Siderocalins: siderophore-binding proteins of the innate immune system. Biometals 22:557–64 [Google Scholar]
7. Sia AK, Allred BE, Raymond KN. 7.  2013. Siderocalins: siderophore binding proteins evolved for primary pathogen host defense. Curr. Opin. Chem. Biol. 17:150–57 [Google Scholar]
8. Wessling-Resnick M. 8.  2015. Nramp1 and other transporters involved in metal withholding during infection. J. Biol. Chem. 290:18984–90 [Google Scholar]
9. Payne SM, Mey AR, Wyckoff EE. 9.  2016. Vibrio iron transport: evolutionary adaptation to life in multiple environments. Microbiol. Mol. Biol. Rev. 80:69–90 [Google Scholar]
10. Sheldon JR, Heinrichs DE. 10.  2015. Recent developments in understanding the iron acquisition strategies of gram positive pathogens. FEMS Microbiol. Rev. 39:592–630 [Google Scholar]
11. Smith AD, Wilks A. 11.  2012. Extracellular heme uptake and the challenges of bacterial cell membranes. Curr. Top. Membr. 69:359–92 [Google Scholar]
12. O'Neill MJ, Wilks A. 12.  2013. Extracellular heme uptake and metabolism in bacterial pathogenesis. Handbook of Porphyrin Science 26 G Ferreira 268–318 Singapore: World Scientific [Google Scholar]
13. Yukl ET, Jepkorir G, Alontaga AY, Pautsch L, Rodriguez JC. 13.  et al. 2010. Kinetic and spectroscopic studies of hemin acquisition in the hemophore HasAp from Pseudomonas aeruginosa. Biochemistry 49:6646–54 [Google Scholar]
14. Biville F, Cwerman H, Letoffe S, Rossi MS, Drouet V. 14.  et al. 2004. Haemophore-mediated signalling in Serratia marcescens: a new mode of regulation for an extra cytoplasmic function (ECF) σ factor involved in haem acquisition. Mol. Microbiol. 53:1267–77 [Google Scholar]
15. Ochsner UA, Johnson Z, Vasil ML. 15.  2000. Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146:185–98 [Google Scholar]
16. Ratliff M, Zhu W, Deshmukh R, Wilks A, Stojiljkovic I. 16.  2001. Homologues of neisserial heme oxygenase in gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J. Bacteriol. 183:6394–403 [Google Scholar]
17. Wilks A, Ikeda-Saito M. 17.  2014. Heme utilization by pathogenic bacteria: Not all pathways lead to biliverdin. Acc. Chem. Res. 47:2291–98 [Google Scholar]
18. Maresso AW, Schneewind O. 18.  2006. Iron acquisition and transport in Staphylococcus aureus. Biometals 19:193–203 [Google Scholar]
19. Grigg JC, Ukpabi G, Gaudin CF, Murphy ME. 19.  2010. Structural biology of heme binding in the Staphylococcus aureus Isd system. J. Inorg. Biochem. 104:341–48 [Google Scholar]
20. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P. 20.  et al. 2003. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906–9 [Google Scholar]
21. Sook BR, Block DR, Sumithran S, Montanez GE, Rodgers KR. 21.  et al. 2008. Characterization of SiaA, a streptococcal heme-binding protein associated with a heme ABC transport system. Biochemistry 47:2678–88 [Google Scholar]
22. Jin B, Newton SM, Shao Y, Jiang X, Charbit A, Klebba PE. 22.  2006. Iron acquisition systems for ferric hydroxamates, haemin and haemoglobin in Listeria monocytogenes. Mol. Microbiol. 59:1185–98 [Google Scholar]
23. Fabian M, Solomaha E, Olson JS, Maresso AW. 23.  2009. Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the gram-positive pathogen Bacillus anthracis. J. Biol. Chem. 284:32138–46 [Google Scholar]
24. Drazek ES, Hammack CA, Schmitt MP. 24.  2000. Corynebacterium diphtheriae genes required for acquisition of iron from haemin and haemoglobin are homologous to ABC haemin transporters. Mol. Microbiol. 36:68–84 [Google Scholar]
25. Tullius MV, Harmston CA, Owens CP, Chim N, Morse RP. 25.  et al. 2011. Discovery and characterization of a unique mycobacterial heme acquisition system. PNAS 108:5051–56 [Google Scholar]
26. Mazmanian SK, Ton-That H, Su K, Schneewind O. 26.  2002. An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. PNAS 99:2293–98 [Google Scholar]
27. Saederup KL, Stodkilde K, Graversen JH, Dickson CF, Etzerodt A. 27.  et al. 2016. The Staphylococcus aureus protein IsdH inhibits host hemoglobin scavenging to promote heme acquisition by the pathogen. J. Biol. Chem. 291:23989–98 [Google Scholar]
28. Skaar EP, Gaspar AH, Schneewind O. 28.  2004. IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J. Biol. Chem. 279:436–43 [Google Scholar]
29. Reniere ML, Ukpabi GN, Harry SR, Stec DF, Krull R. 29.  et al. 2010. The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Mol. Microbiol. 75:1529–38 [Google Scholar]
30. Matsui T, Nambu S, Ono Y, Goulding CW, Tsumoto K, Ikeda-Saito M. 30.  2013. Heme degradation by Staphylococcus aureus IsdG and IsdI liberates formaldehyde rather than carbon monoxide. Biochemistry 52:3025–27 [Google Scholar]
31. Llamas MA, Imperi F, Visca P, Lamont IL. 31.  2014. Cell-surface signaling in Pseudomonas: stress responses, iron transport, and pathogenicity. FEMS Microbiol. Rev. 38:569–97 [Google Scholar]
32. Campagne S, Allain FH, Vorholt JA. 32.  2015. Extra cytoplasmic function σ factors, recent structural insights into promoter recognition and regulation. Curr. Opin. Struct. Biol. 30:71–78 [Google Scholar]
33. Cescau S, Cwerman H, Letoffe S, Delepelaire P, Wandersman C, Biville F. 33.  2007. Heme acquisition by hemophores. Biometals 20:603–13 [Google Scholar]
34. Malki I, Simenel C, Wojtowicz H, de Amorim GC, Prochnicka-Chalufour A. 34.  et al. 2014. Interaction of a partially disordered anti-σ factor with its partner, the signaling domain of the TonB-dependent transporter HasR. PLOS ONE 9:e89502 [Google Scholar]
35. Cwerman H, Wandersman C, Biville F. 35.  2006. Heme and a five-amino-acid hemophore region form the bipartite stimulus triggering the has signaling cascade. J. Bacteriol. 188:3357–64 [Google Scholar]
36. Benevides-Matos N, Wandersman C, Biville F. 36.  2008. HasB, the Serratia marcescens TonB paralog, is specific to HasR. J. Bacteriol. 190:21–27 [Google Scholar]
37. Lefevre J, Delepelaire P, Delepierre M, Izadi-Pruneyre N. 37.  2008. Modulation by substrates of the interaction between the HasR outer membrane receptor and its specific TonB-like protein, HasB. J. Mol. Biol. 378:840–51 [Google Scholar]
38. de Amorim GC, Prochnicka-Chalufour A, Delepelaire P, Lefevre J, Simenel C. 38.  et al. 2013. The structure of HasB reveals a new class of TonB protein fold. PLOS ONE 8:e58964 [Google Scholar]
39. Wojtowicz H, Prochnicka-Chalufour A, de Amorim GC, Roudenko O, Simenel C. 39.  et al. 2016. Structural basis of the signalling through a bacterial membrane receptor HasR deciphered by an integrative approach. Biochem. J. 473:2239–48 [Google Scholar]
40. Poole K, Zhao Q, Neshat S, Heinrichs DE, Dean CR. 40.  1996. The Pseudomonas aeruginosa tonB gene encodes a novel TonB protein. Microbiology 142:1449–58 [Google Scholar]
41. Zhao Q, Poole K. 41.  2000. A second tonB gene in Pseudomonas aeruginosa is linked to the exbB and exbD genes. FEMS Microbiol. Lett 184:127–32 [Google Scholar]
42. Draper RC, Martin LW, Beare PA, Lamont IL. 42.  2011. Differential proteolysis of σ regulators controls cell-surface signalling in Pseudomonas aeruginosa. Mol. Microbiol. 82:1444–53 [Google Scholar]
43. Kang JG, Paget MS, Seok YJ, Hahn MY, Bae JB. 43.  et al. 1999. RsrA, an anti-σ factor regulated by redox change. EMBO J 18:4292–98 [Google Scholar]
44. Chen CC, Lewis RJ, Harris R, Yudkin MD, Delumeau O. 44.  2003. A supramolecular complex in the environmental stress signalling pathway of Bacillus subtilis. Mol. Microbiol. 49:1657–69 [Google Scholar]
45. Bastiaansen KC, Otero-Asman JR, Luirink J, Bitter W, Llamas MA. 45.  2015. Processing of cell-surface signalling anti-σ factors prior to signal recognition is a conserved autoproteolytic mechanism that produces two functional domains. Environ. Microbiol. 17:3263–77 [Google Scholar]
46. Bastiaansen KC, van Ulsen P, Wijtmans M, Bitter W, Llamas MA. 46.  2015. Self-cleavage of the Pseudomonas aeruginosa cell-surface signaling anti-σ factor FoxR occurs through an N-O acyl rearrangement. J. Biol. Chem. 290:12237–46 [Google Scholar]
47. Mourino S, Giardina BJ, Reyes-Caballero H, Wilks A. 47.  2016. Metabolite-driven regulation of heme uptake by the biliverdin IXβ/δ-selective heme oxygenase (HemO) of Pseudomonas aeruginosa. J. Biol. Chem. 291:20503–15 [Google Scholar]
48. Perkins-Balding D, Baer MT, Stojiljkovic I. 48.  2003. Identification of functionally important regions of a haemoglobin receptor from Neisseria meningitidis. Microbiology 149:3423–35 [Google Scholar]
49. Wyckoff EE, Schmitt M, Wilks A, Payne SM. 49.  2004. HutZ is required for efficient heme utilization in Vibrio cholerae. J. Bacteriol. 186:4142–51 [Google Scholar]
50. Stojiljkovic I, Hwa V, de Saint Martin L, O'Gaora P, Nassif X. 50.  et al. 1995. The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol. Microbiol. 15:531–41 [Google Scholar]
51. Perkins-Balding D, Ratliff-Griffin M, Stojiljkovic I. 51.  2004. Iron transport systems in Neisseria meningitidis. Microbiol. Mol. Biol. Rev. 68:154–71 [Google Scholar]
52. Rohde KH, Dyer DW. 52.  2004. Analysis of haptoglobin and hemoglobin-haptoglobin interactions with the Neisseria meningitidis TonB-dependent receptor HpuAB by flow cytometry. Infect. Immun. 72:2494–506 [Google Scholar]
53. Wong CT, Xu Y, Gupta A, Garnett JA, Matthews SJ, Hare SA. 53.  2015. Structural analysis of haemoglobin binding by HpuA from the Neisseriaceae family. Nat. Commun. 6:10172 [Google Scholar]
54. Buscher AZ, Grass S, Heuser J, Roth R, St. Geme JW 3rd. 54.  2006. Surface anchoring of a bacterial adhesin secreted by the two-partner secretion pathway. Mol. Microbiol. 61:470–83 [Google Scholar]
55. Cope LD, Yogev R, Muller-Eberhard U, Hansen EJ. 55.  1995. A gene cluster involved in the utilization of both free heme and heme:hemopexin by Haemophilus influenzae type b. J. Bacteriol. 177:2644–53 [Google Scholar]
56. Fournier C, Smith A, Delepelaire P. 56.  2011. Haem release from haemopexin by HxuA allows Haemophilus influenzae to escape host nutritional immunity. Mol. Microbiol. 80:133–48 [Google Scholar]
57. Letoffe S, Ghigo JM, Wandersman C. 57.  1994. Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. PNAS 91:9876–80 [Google Scholar]
58. Rossi MS, Fetherston JD, Letoffe S, Carniel E, Perry RD, Ghigo JM. 58.  2001. Identification and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect. Immun. 69:6707–17 [Google Scholar]
59. Nelson KE, Fleischmann RD, DeBoy RT, Paulsen IT, Fouts DE. 59.  et al. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J. Bacteriol. 185:5591–601 [Google Scholar]
60. Benevides-Matos N, Biville F. 60.  2010. The Hem and Has haem uptake systems in Serratia marcescens. Microbiology 156:1749–57 [Google Scholar]
61. Ghigo JM, Letoffe S, Wandersman C. 61.  1997. A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J. Bacteriol. 179:3572–79 [Google Scholar]
62. Alontaga AY, Rodriguez JC, Schonbrunn E, Becker A, Funke T. 62.  et al. 2009. Structural characterization of the hemophore HasAp from Pseudomonas aeruginosa: NMR spectroscopy reveals protein-protein interactions between Holo-HasAp and hemoglobin. Biochemistry 48:96–109 [Google Scholar]
63. Deniau C, Gilli R, Izadi-Pruneyre N, Letoffe S, Delepierre M. 63.  et al. 2003. Thermodynamics of heme binding to the HasA(SM) hemophore: effect of mutations at three key residues for heme uptake. Biochemistry 42:10627–33 [Google Scholar]
64. Kumar R, Qi Y, Matsumura H, Lovell S, Yao H. 64.  et al. 2016. Replacing arginine 33 for alanine in the hemophore HasA from Pseudomonas aeruginosa causes closure of the H32 loop in the apo-protein. Biochemistry 55:2622–31 [Google Scholar]
65. Izadi-Pruneyre N, Huche F, Lukat-Rodgers GS, Lecroisey A, Gilli R. 65.  et al. 2006. The heme transfer from the soluble HasA hemophore to its membrane-bound receptor HasR is driven by protein-protein interaction from a high to a lower affinity binding site. J. Biol. Chem. 281:25541–50 [Google Scholar]
66. Barjon C, Wecker K, Izadi-Pruneyre N, Delepelaire P. 66.  2007. Mutagenesis and molecular modeling reveal three key extracellular loops of the membrane receptor HasR that are involved in hemophore HasA binding. J. Bacteriol. 189:5379–82 [Google Scholar]
67. Caillet-Saguy C, Piccioli M, Turano P, Izadi-Pruneyre N, Delepierre M. 67.  et al. 2009. Mapping the interaction between the hemophore HasA and its outer membrane receptor HasR using CRINEPT-TROSY NMR spectroscopy. J. Am. Chem. Soc. 131:1736–44 [Google Scholar]
68. Smith AD, Modi AR, Sun S, Dawson JH, Wilks A. 68.  2015. Spectroscopic determination of distinct heme ligands in outer-membrane receptors PhuR and HasR of Pseudomonas aeruginosa. Biochemistry 54:2601–12 [Google Scholar]
69. Mokry DZ, Nadia-Albete A, Johnson MK, Lukat-Rodgers GS, Rodgers KR, Lanzilotta WN. 69.  2014. Spectroscopic evidence for a 5-coordinate oxygenic ligated high spin ferric heme moiety in the Neisseria meningitidis hemoglobin binding receptor. Biochim. Biophys. Acta 1840:3058–66 [Google Scholar]
70. Burkhard KA, Wilks A. 70.  2007. Characterization of the outer membrane receptor ShuA from the heme uptake system of Shigella dysenteriae. Substrate specificity and identification of the heme protein ligands. J. Biol. Chem. 282:15126–36 [Google Scholar]
71. Letoffe S, Nato F, Goldberg ME, Wandersman C. 71.  1999. Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol. Microbiol. 33:546–55 [Google Scholar]
72. Krieg S, Huche F, Diederichs K, Izadi-Pruneyre N, Lecroisey A. 72.  et al. 2009. Heme uptake across the outer membrane as revealed by crystal structures of the receptor-hemophore complex. PNAS 106:1045–50 [Google Scholar]
73. Cobessi D, Meksem A, Brillet K. 73.  2010. Structure of the heme/hemoglobin outer membrane receptor ShuA from Shigella dysenteriae: heme binding by an induced fit mechanism. Proteins 78:286–94 [Google Scholar]
74. Liu X, Olczak T, Guo HC, Dixon DW, Genco CA. 74.  2006. Identification of amino acid residues involved in heme binding and hemoprotein utilization in the Porphyromonas gingivalis heme receptor HmuR. Infect. Immun. 74:1222–32 [Google Scholar]
75. Nepluev I, Afonina G, Fusco WG, Leduc I, Olsen B. 75.  et al. 2009. An immunogenic, surface-exposed domain of Haemophilus ducreyi outer membrane protein HgbA is involved in hemoglobin binding. Infect. Immun. 77:3065–74 [Google Scholar]
76. Smith AD, Wilks A. 76.  2015. Differential contributions of the outer membrane receptors PhuR and HasR to heme acquisition in Pseudomonas aeruginosa. J. Biol. Chem. 290:7756–66 [Google Scholar]
77. Marvig RL, Damkiaer S, Khademi SM, Markussen TM, Molin S, Jelsbak L. 77.  2014. Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin. mBio 5:e00966–14 [Google Scholar]
78. Nguyen AT, O'Neill MJ, Watts AM, Robson CL, Lamont IL. 78.  et al. 2014. Adaptation of iron homeostasis pathways by a Pseudomonas aeruginosa pyoverdine mutant in the cystic fibrosis lung. J. Bacteriol. 196:2265–76 [Google Scholar]
79. Damron FH, Barbier M, Oglesby-Sherrouse AG, Wilks A. 79.  2016. Dual-seq transcriptomics reveals the battle for iron during Pseudomonas aeruginosa acute murine pneumonia. Sci. Rep. 6:39172 [Google Scholar]
80. Grigg JC, Mao CX, Murphy ME. 80.  2011. Iron-coordinating tyrosine is a key determinant of NEAT domain heme transfer. J. Mol. Biol. 413:684–98 [Google Scholar]
81. Ho WW, Li H, Eakanunkul S, Tong Y, Wilks A. 81.  et al. 2007. Holo- and apo-bound structures of bacterial periplasmic heme-binding proteins. J. Biol. Chem. 282:35796–802 [Google Scholar]
82. Kumar R, Matsumura H, Lovell S, Yao H, Rodriguez JC. 82.  et al. 2014. Replacing the axial ligand tyrosine 75 or its hydrogen bond partner histidine 83 minimally affects hemin acquisition by the hemophore HasAp from Pseudomonas aeruginosa. Biochemistry 53:2112–25 [Google Scholar]
83. Khursigara CM, De Crescenzo G, Pawelek PD, Coulton JW. 83.  2005. Kinetic analyses reveal multiple steps in forming TonB–FhuA complexes from Escherichia coli. Biochemistry 44:3441–53 [Google Scholar]
84. Shultis DD, Purdy MD, Banchs CN, Wiener MC. 84.  2006. Outer membrane active transport: structure of the BtuB:TonB complex. Science 312:1396–99 [Google Scholar]
85. Chimento DP, Kadner RJ, Wiener MC. 85.  2005. Comparative structural analysis of TonB-dependent outer membrane transporters: implications for the transport cycle. Proteins 59:240–51 [Google Scholar]
86. Krewulak KD, Vogel HJ. 86.  2008. Structural biology of bacterial iron uptake. Biochim. Biophys. Acta 1778:1781–804 [Google Scholar]
87. Carter DM, Miousse IR, Gagnon JN, Martinez E, Clements A. 87.  et al. 2006. Interactions between TonB from Escherichia coli and the periplasmic protein FhuD. J. Biol. Chem. 281:35413–24 [Google Scholar]
88. Dwyer MA, Hellinga HW. 88.  2004. Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr. Opin. Struct. Biol. 14:495–504 [Google Scholar]
89. Borths EL, Locher KP, Lee AT, Rees DC. 89.  2002. The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. PNAS 99:16642–47 [Google Scholar]
90. Eakanunkul S, Lukat-Rodgers GS, Sumithran S, Ghosh A, Rodgers KR. 90.  et al. 2005. Characterization of the periplasmic heme-binding protein ShuT from the heme uptake system of Shigella dysenteriae. Biochemistry 44:13179–91 [Google Scholar]
91. Higgins CF. 91.  1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67–113 [Google Scholar]
92. Higgins CF. 92.  2001. ABC transporters: physiology, structure and mechanism—an overview. Res. Microbiol. 152:205–10 [Google Scholar]
93. Walker JE, Saraste M, Gay NJ. 93.  1982. E. coli F1-ATPase interacts with a membrane protein component of a proton channel. Nature 298:867–69 [Google Scholar]
94. Woo JS, Zeltina A, Goetz BA, Locher KP. 94.  2012. X-ray structure of the Yersinia pestis heme transporter HmuUV. Nat. Struct. Mol. Biol. 19:1310–15 [Google Scholar]
95. Naoe Y, Nakamura N, Doi A, Sawabe M, Nakamura H. 95.  et al. 2016. Crystal structure of bacterial haem importer complex in the inward-facing conformation. Nat. Commun. 7:13411 [Google Scholar]
96. Hvorup RN, Goetz BA, Niederer M, Hollenstein K, Perozo E, Locher KP. 96.  2007. Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 317:1387–90 [Google Scholar]
97. Korkhov VM, Mireku SA, Locher KP. 97.  2012. Structure of AMP-PNP-bound vitamin B12 transporter BtuCD-F. Nature 490:367–72 [Google Scholar]
98. Korkhov VM, Mireku SA, Veprintsev DB, Locher KP. 98.  2014. Structure of AMP-PNP-bound BtuCD and mechanism of ATP-powered vitamin B12 transport by BtuCD-F. Nat. Struct. Mol. Biol. 21:1097–99 [Google Scholar]
99. Burkhard KA, Wilks A. 99.  2008. Functional characterization of the Shigella dysenteriae heme ABC transporter. Biochemistry 47:7977–79 [Google Scholar]
100. O'Neill MJ, Wilks A. 100.  2013. The P. aeruginosa heme binding protein PhuS is a heme oxygenase titratable regulator of heme uptake. ACS Chem. Biol. 8:1794–802 [Google Scholar]
101. Andrade MA, Ciccarelli FD, Perez-Iratxeta C, Bork P. 101.  2002. NEAT: a domain duplicated in genes near the components of a putative Fe³⁺ siderophore transporter from gram-positive pathogenic bacteria. Genome Biol 3:RESEARCH0047 [Google Scholar]
102. Dickson CF, Kumar KK, Jacques DA, Malmirchegini GR, Spirig T. 102.  et al. 2014. Structure of the hemoglobin-IsdH complex reveals the molecular basis of iron capture by Staphylococcus aureus. J. Biol. Chem. 289:6728–38 [Google Scholar]
103. Grigg JC, Vermeiren CL, Heinrichs DE, Murphy ME. 103.  2007. Heme coordination by Staphylococcus aureus IsdE. J. Biol. Chem. 282:28815–22 [Google Scholar]
104. Sharp KH, Schneider S, Cockayne A, Paoli M. 104.  2007. Crystal structure of the heme-IsdC complex, the central conduit of the Isd iron/heme uptake system in Staphylococcus aureus. J. Biol. Chem. 282:10625–31 [Google Scholar]
105. Pilpa RM, Fadeev EA, Villareal VA, Wong ML, Phillips M, Clubb RT. 105.  2006. Solution structure of the NEAT (NEAr Transporter) domain from IsdH/HarA: the human hemoglobin receptor in Staphylococcus aureus. J. Mol. Biol. 360:435–47 [Google Scholar]
106. Gaudin CF, Grigg JC, Arrieta AL, Murphy ME. 106.  2011. Unique heme-iron coordination by the hemoglobin receptor IsdB of Staphylococcus aureus. Biochemistry 50:5443–52 [Google Scholar]
107. Tiedemann MT, Muryoi N, Heinrichs DE, Stillman MJ. 107.  2008. Iron acquisition by the haem-binding Isd proteins in Staphylococcus aureus: studies of the mechanism using magnetic circular dichroism. Biochem. Soc. Trans. 36:1138–43 [Google Scholar]
108. Spirig T, Malmirchegini GR, Zhang J, Robson SA, Sjodt M. 108.  et al. 2013. Staphylococcus aureus uses a novel multidomain receptor to break apart human hemoglobin and steal its heme. J. Biol. Chem. 288:1065–78 [Google Scholar]
109. Bowden CF, Verstraete MM, Eltis LD, Murphy ME. 109.  2014. Hemoglobin binding and catalytic heme extraction by IsdB near iron transporter domains. Biochemistry 53:2286–94 [Google Scholar]
110. Sjodt M, Macdonald R, Spirig T, Chan AH, Dickson CF. 110.  et al. 2016. The PRE-derived NMR model of the 38.8-kDa tri-domain IsdH protein from Staphylococcus aureus suggests that it adaptively recognizes human hemoglobin. J. Mol. Biol. 428:1107–29 [Google Scholar]
111. Zhu H, Xie G, Liu M, Olson JS, Fabian M. 111.  et al. 2008. Pathway for heme uptake from human methemoglobin by the iron-regulated surface determinants system of Staphylococcus aureus. J. Biol. Chem. 283:18450–60 [Google Scholar]
112. Tiedemann MT, Heinrichs DE, Stillman MJ. 112.  2012. Multiprotein heme shuttle pathway in Staphylococcus aureus: iron-regulated surface determinant cog-wheel kinetics. J. Am. Chem. Soc. 134:16578–85 [Google Scholar]
113. Abe R, Caaveiro JM, Kozuka-Hata H, Oyama M, Tsumoto K. 113.  2012. Mapping ultra-weak protein-protein interactions between heme transporters of Staphylococcus aureus. J. Biol. Chem. 287:16477–87 [Google Scholar]
114. Moriwaki Y, Terada T, Tsumoto K, Shimizu K. 114.  2015. Rapid heme transfer reactions between NEAr transporter domains of Staphylococcus aureus: a theoretical study using QM/MM and MD simulations. PLOS ONE 10:e0145125 [Google Scholar]
115. Dale SE, Sebulsky MT, Heinrichs DE. 115.  2004. Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J. Bacteriol. 186:8356–62 [Google Scholar]
116. Speziali CD, Dale SE, Henderson JA, Vines ED, Heinrichs DE. 116.  2006. Requirement of Staphylococcus aureus ATP-binding cassette-ATPase FhuC for iron-restricted growth and evidence that it functions with more than one iron transporter. J. Bacteriol. 188:2048–55 [Google Scholar]
117. Bibb LA, Kunkle CA, Schmitt MP. 117.  2007. The ChrA-ChrS and HrrA-HrrS signal transduction systems are required for activation of the hmuO promoter and repression of the hemA promoter in Corynebacterium diphtheriae. Infect. Immun. 75:2421–31 [Google Scholar]
118. Stauff DL, Bagaley D, Torres VJ, Joyce R, Anderson KL. 118.  et al. 2008. Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J. Bacteriol. 190:3588–96 [Google Scholar]
119. Bibb LA, Schmitt MP. 119.  2010. The ABC transporter HrtAB confers resistance to hemin toxicity and is regulated in a hemin-dependent manner by the ChrAS two-component system in Corynebacterium diphtheriae. J. Bacteriol. 192:4606–17 [Google Scholar]
120. Stauff DL, Skaar EP. 120.  2009. The heme sensor system of Staphylococcus aureus. Contrib. Microbiol. 16:120–35 [Google Scholar]
121. Ferris HU, Dunin-Horkawicz S, Mondejar LG, Hulko M, Hantke K. 121.  et al. 2011. The mechanisms of HAMP-mediated signaling in transmembrane receptors. Structure 19:378–85 [Google Scholar]
122. Routh MD, Zalucki Y, Su CC, Zhang Q, Shafer WM, Yu EW. 122.  2011. Efflux pumps of the resistance-nodulation-division family: a perspective of their structure, function, and regulation in gram-negative bacteria. Adv. Enzymol. Relat. Areas Mol. Biol. 77:109–46 [Google Scholar]
123. Rohde KH, Dyer DW. 123.  2003. Mechanisms of iron acquisition by the human pathogens Neisseriameningitidis and Neisseria gonorrhoeae. Front. Biosci. 8:d1186–218 [Google Scholar]
124. Holland J, Parsons TR, Hasan AA, Cook SM, Stevenson P. 124.  et al. 1996. Conservation and antigenic cross-reactivity of the transferrin-binding proteins of Haemophilus influenzae, Actinobacilluspleuropneumoniae and Neisseria meningitidis. Microbiology 142:3505–13 [Google Scholar]
125. Richardson AR, Stojiljkovic I. 125.  1999. HmbR, a hemoglobin-binding outer membrane protein of Neisseria meningitidis, undergoes phase variation. J. Bacteriol. 181:2067–74 [Google Scholar]
126. Ekins A, Bahrami F, Sijercic A, Maret D, Niven DF. 126.  2004. Haemophilus somnus possesses two systems for acquisition of transferrin-bound iron. J. Bacteriol. 186:4407–11 [Google Scholar]
127. Chen CJ, Elkins C, Sparling PF. 127.  1998. Phase variation of hemoglobin utilization in Neisseria gonorrhoeae. Infect. Immun. 66:987–93 [Google Scholar]
128. Cornelissen CN, Anderson JE, Boulton IC, Sparling PF. 128.  2000. Antigenic and sequence diversity in gonococcal transferrin-binding protein A. Infect. Immun. 68:4725–35 [Google Scholar]
129. Cornelissen CN. 129.  2008. Identification and characterization of gonococcal iron transport systems as potential vaccine antigens. Future Microbiol 3:287–98 [Google Scholar]
130. Leduc I, Banks KE, Fortney KR, Patterson KB, Billings SD. 130.  et al. 2008. Evaluation of the repertoire of the TonB-dependent receptors of Haemophilus ducreyi for their role in virulence in humans. J. Infect. Dis. 197:1103–9 [Google Scholar]
131. Afonina G, Leduc I, Nepluev I, Jeter C, Routh P. 131.  et al. 2006. Immunization with the Haemophilus ducreyi hemoglobin receptor HgbA protects against infection in the swine model of chancroid. Infect. Immun. 74:2224–32 [Google Scholar]
132. Leduc I, Fusco WG, Choudhary N, Routh PA, Cholon DM. 132.  et al. 2011. Passive immunization with a polyclonal antiserum to the hemoglobin receptor of Haemophilus ducreyi confers protection against a homologous challenge in the experimental swine model of chancroid. Infect. Immun. 79:3168–77 [Google Scholar]
133. Allard M, Moisan H, Brouillette E, Gervais AL, Jacques M. 133.  et al. 2006. Transcriptional modulation of some Staphylococcus aureus iron-regulated genes during growth in vitro and in a tissue cage model in vivo. Microbes Infect 8:1679–90 [Google Scholar]
134. Ster C, Beaudoin F, Diarra MS, Jacques M, Malouin F, Lacasse P. 134.  2010. Evaluation of some Staphylococcus aureus iron-regulated proteins as vaccine targets. Vet. Immunol. Immunopathol. 136:311–18 [Google Scholar]
135. Kim HK, DeDent A, Cheng AG, McAdow M, Bagnoli F. 135.  et al. 2010. IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28:6382–92 [Google Scholar]
136. Pancari G, Fan H, Smith S, Joshi A, Haimbach R. 136.  et al. 2012. Characterization of the mechanism of protection mediated by CS-D7, a monoclonal antibody to Staphylococcus aureus iron regulated surface determinant B (IsdB). Front. Cell Infect. Microbiol. 2:36 [Google Scholar]
137. Ferreira D, Seca AM, Diana CG, Silva AM. 137.  2016. Targeting human pathogenic bacteria by siderophores: a proteomics review. J. Proteom. 145:153–66 [Google Scholar]
138. Hampton-Marcell JT, Moormann SM, Owens SM, Gilbert JA. 138.  2013. Preparation and metatranscriptomic analyses of host-microbe systems. Methods Enzymol 531:169–85 [Google Scholar]
139. Bozja J, Yi K, Shafer WM, Stojiljkovic I. 139.  2004. Porphyrin-based compounds exert antibacterial action against the sexually transmitted pathogens Neisseriagonorrhoeae and Haemophilus ducreyi. Int. J. Antimicrob. Agents 24:578–84 [Google Scholar]
140. Olczak T, Maszczak-Seneczko D, Smalley JW, Olczak M. 140.  2012. Gallium(III), cobalt(III) and copper(II) protoporphyrin IX exhibit antimicrobial activity against Porphyromonas gingivalis by reducing planktonic and biofilm growth and invasion of host epithelial cells. Arch. Microbiol. 194:719–24 [Google Scholar]
141. Stojiljkovic I, Kumar V, Srinivasan N. 141.  1999. Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol. Microbiol. 31:429–42 [Google Scholar]
142. Stojiljkovic I, Evavold BD, Kumar V. 142.  2001. Antimicrobial properties of porphyrins. Expert Opin. Investig. Drugs 10:309–20 [Google Scholar]
143. Shirataki C, Shoji O, Terada M, Ozaki S, Sugimoto H. 143.  et al. 2014. Inhibition of heme uptake in Pseudomonas aeruginosa by its hemophore (HasA_p) bound to synthetic metal complexes. Angew. Chem. Int. Ed. Engl. 53:2862–66 [Google Scholar]
144. Mislin GL, Schalk IJ. 144.  2014. Siderophore-dependent iron uptake systems as gates for antibiotic Trojan horse strategies against Pseudomonas aeruginosa. Metallomics 6:408–20 [Google Scholar]
145. Fardeau S, Dassonville-Klimpt A, Audic N, Sasaki A, Pillon M. 145.  et al. 2014. Synthesis and antibacterial activity of catecholate-ciprofloxacin conjugates. Bioorg. Med. Chem 22:4049–60 [Google Scholar]