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Research Article

Mechanisms of iron and haem transport by Listeria monocytogenes

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Pages 69-86 | Received 08 Apr 2012, Accepted 08 May 2012, Published online: 18 Jun 2012

References

  • Aboulwafa M, Chung YJ, Wai HH, Saier MH Jr. 2003. Studies on the Escherichia coli glucose-specific permease, PtsG, with a point mutation in its N-terminal amphipathic leader sequence. Microbiology 149:763–771.
  • Adams TJ, Vartivarian S, Cowart RE. 1990. Iron acquisition systems of Listeria monocytogenes. Infect Immun 58:2715–2718.
  • Aisen P, Leibman A, Zweier J. 1978. Stoichiometric and site characteristics of the binding of iron to human transferrin. J Biol Chem 253:1930–1937.
  • Anderson MT, Armstrong SK. 2008. Norepinephrine mediates acquisition of transferrin-iron in Bordetella bronchiseptica. J Bacteriol 190:3940–3947.
  • Andrade MA, Ciccarelli FD, Perez-Iratxeta C, Bork P. 2002. NEAT: A domain duplicated in genes near the components of a putative Fe3+ siderophore transporter from Gram-positive pathogenic bacteria. Genome Biol 3:Research 0047.
  • Annamalai R, Jin B, Cao Z, Newton SM, Klebba PE. 2004. Recognition of ferric catecholates by FepA. J Bacteriol 186:3578–3589.
  • Anzaldi LL, Skaar EP. 2010. Overcoming the heme paradox: Heme toxicity and tolerance in bacterial pathogens. Infect Immun 78:4977–4989.
  • Armstrong SK, Brickman TJ, Suhadolc RJ. 2012. Involvement of multiple distinct Bordetella receptor proteins in the utilization of iron liberated from transferrin by host catecholamine stress hormones. Mol Microbiol 84:446–462.
  • Arreguin S, Nelson P, Padway S, Shirazi M, Pierpont C. 2009. Dopamine complexes of iron in the etiology and pathogenesis of Parkinson's disease. J Inorg Biochem 103:87–93.
  • Ascenzi P, Bocedi A, Visca P, Altruda F, Tolosano E, Beringhelli T, 2005. Hemoglobin and heme scavenging. IUBMB Life 57:749–759.
  • Autret N, Dubail I, Trieu-Cuot P, Berche P, Charbit A. 2001. Identification of new genes involved in the virulence of Listeria monocytogenes by signature-tagged transposon mutagenesis. Infect Immun 69:2054–2065.
  • Barchini E, Cowart RE. 1996. Extracellular iron reductase activity produced by Listeria monocytogenes. Arch Microbiol 166:51–57.
  • Bates CS, Montanez GE, Woods CR, Vincent RM, Eichenbaum Z. 2003. Identification and characterization of a Streptococcus pyogenes operon involved in binding of hemoproteins and acquisition of iron. Infect Immun 71:1042–1055.
  • Bibb LA, Schmitt MP. 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 192:4606–4617.
  • Bierne H, Garandeau C, Pucciarelli MG, Sabet C, Newton SM, Del Portillo FG, 2004. Sortase B, a new class of sortase in Listeria monocytogenes. J Bacteriol 186:1972–1982.
  • Bierne H, Mazmanian SK, Trost M, Pucciarelli MG, Liu G, Dehoux P, 2002. Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence. Mol Microbiol 43:869–881.
  • Bluhm ME, Hay BP, Kim SS, Dertz EA, Raymond KN. 2002a. Corynebactin and a serine trilactone based analogue: Chirality and molecular modeling of ferric complexes. Inorg Chem 41:5475–5478.
  • Bluhm ME, Kim SS, Dertz EA, Raymond KN. 2002b. Corynebactin and enterobactin: Related siderophores of opposite chirality. J Am Chem Soc 124:2436–2437.
  • Bonnah RA, Schryvers AB. 1998. Preparation and characterization of Neisseria meningitidis mutants deficient in production of the human lactoferrin-binding proteins LbpA and LbpB. J Bacteriol 180:3080–3090.
  • Braun G, Cole ST. 1983. Molecular characterization of the gene coding for major outer membrane protein OmpA from Enterobacter aerogenes. Eur J Biochem 137:495–500.
  • Braun V, Hantke K, Koster W. 1998. Bacterial iron transport: Mechanisms, genetics, and regulation. Met Ions Biol Syst 35:67–145.
  • Buchanan SK, Smith BS, Venkatramani L, Xia D, Esser L, Palnitkar M, 1999. Crystal structure of the outer membrane active transporter FepA from Escherichia coli [see comments]. Nat Struct Biol 6:56–63.
  • Bullen J, Griffiths E, Rogers H, Ward G. 2000. Sepsis: The critical role of iron. Microbes Infect 2:409–415.
  • Bullen JJ. 1974. Proceedings: Iron and infection. Br J Haematol 28:139–140.
  • Bullen JJ. 1981. The significance of iron in infection. Rev Infect Dis 3:1127–1138.
  • Bullen JJ. 1985. Iron and infection. Eur J Clin Microbiol 4:537–539.
  • Cao Z, Qi Z, Sprencel C, Newton SM, Klebba PE. 2000. Aromatic components of two ferric enterobactin binding sites in Escherichia coli fepA. Mol Microbiol 37:1306–1317.
  • Cho S, Wang Q, Swaminathan CP, Hesek D, Lee M, Boons GJ, 2007. Structural insights into the bactericidal mechanism of human peptidoglycan recognition proteins. Proc Natl Acad Sci USA 104:8761–8766.
  • Conte MP, Longhi C, Polidoro M, Petrone G, Buonfiglio V, Di Santo S, 1996. Iron availability affects entry of Listeria monocytogenes into the enterocytelike cell line Caco-2. Infect Immun 64:3925–3929.
  • Cornelissen CN, Kelley M, Hobbs MM, Anderson JE, Cannon JG, Cohen MS, 1998. The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers. Mol Microbiol 27:611–616.
  • Cornelissen CN, Sparling PF. 1994a. Identification of receptor-mediated transferrin-iron uptake mechanism in Neisseria gonorrhoeae. Methods Enzymol 235:356–363.
  • Cornelissen CN, Sparling PF. 1994b. Iron piracy: Acquisition of transferrin-bound iron by bacterial pathogens. Mol Microbiol 14:843–850.
  • Cossart P, Jonquieres R. 2000. Sortase, a universal target for therapeutic agents against gram-positive bacteria? Proc Natl Acad Sci USA 97:5013–5015.
  • Coulanges V, Andre P, Vidon DJ. 1996. Esculetin antagonizes iron-chelating agents and increases the virulence of Listeria monocytogenes. Res Microbiol 147:677–685.
  • Coulanges V, Andre P, Vidon DJ. 1998. Effect of siderophores, catecholamines, and catechol compounds on Listeria spp. Growth in iron-complexed medium. Biochem Biophys Res Commun 249:526–530.
  • Coulanges V, Andre P, Ziegler O, Buchheit L, Vidon DJ. 1997. Utilization of iron-catecholamine complexes involving ferric reductase activity in Listeria monocytogenes. Infect Immun 65:2778–2785.
  • Dassa E. 2011. Natural history of ABC systems: Not only transporters. Essays Biochem 50:19–42.
  • Dassa E, Bouige P. 2001. The ABC of ABCS: A phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152:211–229.
  • Demchick P, Koch AL. 1996. The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J Bacteriol 178:768–773.
  • Deneer HG, Healey V, Boychuk I. 1995. Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp. Microbiology 141:1985–1992.
  • Dhar G, Faull KF, Schneewind O. 2000. Anchor structure of cell wall surface proteins in Listeria monocytogenes. Biochemistry 39:3725–3733.
  • Dmitriev B, Toukach F, Ehlers S. 2005. Towards a comprehensive view of the bacterial cell wall. Trends Microbiol 13:569–574.
  • Dmitriev BA, Ehlers S, Rietschel ET. 1999. Layered murein revisited: A fundamentally new concept of bacterial cell wall structure, biogenesis and function. Med Microbiol Immunol (Berl) 187:173–181.
  • Dmitriev BA, Toukach FV, Schaper KJ, Holst O, Rietschel ET, Ehlers S. 2003. Tertiary structure of bacterial murein: The scaffold model. J Bacteriol 185:3458–3468.
  • Dramsi S, Dehoux P, Lebrun M, Goossens PL, Cossart P. 1997. Identification of four new members of the internalin multigene family of Listeria monocytogenes EGD. Infect Immun 65:1615–1625.
  • Elkins C, Chen CJ, Thomas CE. 1995. Characterization of the hgbA locus encoding a hemoglobin receptor from Haemophilus ducreyi. Infect Immun 63:2194–2200.
  • Elkins C, Totten PA, Olsen B, Thomas CE. 1998. Role of the Haemophilus ducreyi Ton system in internalization of heme from hemoglobin. Infect Immun 66:151–160.
  • Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W. 1998. Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide [see comments]. Science 282:2215–2220.
  • Fisher M, Huang YS, Li X, Mciver KS, Toukoki C, Eichenbaum Z. 2008. Shr is a broad-spectrum surface receptor that contributes to adherence and virulence in group A streptococcus. Infect Immun 76:5006–5015.
  • Furman M, Fica A, Saxena M, Di Fabio JL, Cabello FC. 1994. Salmonella typhi iron uptake mutants are attenuated in mice. Infect Immun 62:4091–4094.
  • Gan L, Chen S, Jensen GJ. 2008. Molecular organization of Gram-negative peptidoglycan. Proc Nat Acad Sci USA 105:18953–18957.
  • Ginalski K. 2006. Comparative modeling for protein structure prediction. Curr Opin Struct Biol 16:172–177.
  • Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, 2001. Comparative genomics of Listeria species. Science 294:849–852.
  • Gray-Owen SD, Schryvers AB. 1996. Bacterial transferrin and lactoferrin receptors. Trends Microbiol 4:185–191.
  • Griffiths E. 1993. Iron and infection: Better understanding at the molecular level but little progress on the clinical front [editorial]. J Med Microbiol 38:389–390.
  • Grigg JC, Ukpabi G, Gaudin CF, Murphy ME. 2010. Structural biology of heme binding in the Staphylococcus aureus Isd system. J Inorg Biochem 104:341–348.
  • Grigg JC, Vermeiren CL, Heinrichs DE, Murphy ME. 2007. Haem recognition by a Staphylococcus aureus NEAT domain. Mol Microbiol 63:139–149.
  • Hammer ND, Skaar EP. 2011. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 65:129–147.
  • Hartford T, O'Brien S, Andrew PW, Jones D, Roberts IS. 1993. Utilization of transferrin-bound iron by Listeria monocytogenes. FEMS Microbiol Lett 108:311–318.
  • Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. 2008. Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105:3963–3967.
  • Holtje JV. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203.
  • Jarosik GP, Maciver I, Hansen EJ. 1995. Utilization of transferrin-bound iron by Haemophilus influenzae requires an intact tonB gene. Infect Immun 63:710–713.
  • Jin B, Newton SM, Shao Y, Jiang X, Charbit A, Klebba PE. 2005. Iron acquisition systems for ferric hydroxamates, haemin and haemoglobin in Listeria monocytogenes. Mol Microbiol 59:1185–1198.
  • Kamisango K, Saiki I, Tanio Y, Okumura H, Araki Y, Sekikawa I, 1982. Structures and biological activities of peptidoglycans of Listeria monocytogenes and Propionibacterium acnes. J Biochem 92:23–33.
  • Kaserer WA, Jiang X, Xiao Q, Scott DC, Bauler M, Copeland D, 2008. Insight from TonB hybrid proteins into the mechanism of iron transport through the outer membrane. J Bacteriol 190:4001–4016.
  • Kaur AP, Wilks A. 2007. Heme inhibits the DNA binding properties of the cytoplasmic heme binding protein of Shigella dysenteriae (ShuS). Biochemistry 46:2994–3000.
  • Kharat AS, Tomasz A. 2003. Inactivation of the srtA gene affects localization of surface proteins and decreases adhesion of Streptococcus pneumoniae to human pharyngeal cells in vitro. Infect Immun 71:2758–2765.
  • Klebba PE. 2004. Transport biochemistry of FepA. Washington: DC: ASM Press.
  • Koch AL. 2000. Length distribution of the peptidoglycan chains in the sacculus of Escherichia coli. J Theor Biol 204:533–541.
  • Konopka K, Bindereif A, Neilands JB. 1982. Aerobactin-mediated utilization of transferrin iron. Biochemistry 21:6503–6508.
  • Konopka K, Neilands JB. 1984. Effect of serum albumin on siderophore-mediated utilization of transferrin iron. Biochemistry 23:2122–2127.
  • Kuan G, Dassa E, Saurin W, Hofnung M, Saier MH Jr. 1995. Phylogenetic analyses of the ATP-binding constituents of bacterial extracytoplasmic receptor-dependent ABC-type nutrient uptake permeases. Res Microbiol 146:271–278.
  • Labischinski H, Goodell EW, Goodell A, Hochberg ML. 1991. Direct proof of a ‘more-than-single-layered' peptidoglycan architecture of Escherichia coli W7: A neutron small-angle scattering study. J Bacteriol 173:751–756.
  • Lebrun M, Mengaud J, Ohayon H, Nato F, Cossart P. 1996. Internalin must be on the bacterial surface to mediate entry of Listeria monocytogenes into epithelial cells. Mol Microbiol 21:579–592.
  • Lechardeur D, Cesselin B, Liebl U, Vos MH, Fernandez A, Brun C, 2012. Discovery of intracellular heme-binding protein HrtR, which controls heme efflux by the conserved HrtB-HrtA transporter in Lactococcus lactis. J Biol Chem 287:4752–4758.
  • Lee SF, Boran TL. 2003. Roles of sortase in surface expression of the major protein adhesin P1, saliva-induced aggregation and adherence, and cariogenicity of Streptococcus mutans. Infect Immun 71:676–681.
  • Lei B, Smoot LM, Menning HM, Voyich JM, Kala SV, Deleo FR, 2002. Identification and characterization of a novel heme-associated cell surface protein made by Streptococcus pyogenes. Infect Immun 70:4494–4500.
  • Letoffe S, Deniau C, Wolff N, Dassa E, Delepelaire P, Lecroisey A, 2001. Haemophore-mediated bacterial haem transport: Evidence for a common or overlapping site for haem-free and haem-loaded haemophore on its specific outer membrane receptor. Mol Microbiol 41:439–450.
  • Liu M, Lei B. 2005. Heme transfer from streptococcal cell surface protein Shp to HtsA of transporter HtsABC. Infect Immun 73:5086–5092.
  • Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, 1998. Transmembrane signaling across the ligand-gated FhuA receptor: Crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771–778.
  • Lopez-Goni I, Moriyon I, Neilands JB. 1992. Identification of 2,3-dihydroxybenzoic acid as a Brucella abortus siderophore. Infect Immun 60:4496–4503.
  • Marchand CH, Salmeron C, Raad RB, Meniche X, Chami M, Masi M, 2012. Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. J Bacteriol 194:587–597.
  • Maresso AW, Garufi G, Schneewind O. 2008. Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLoS Pathog 4:e1000132.
  • Maresso AW, Schneewind O. 2006. Iron acquisition and transport in Staphylococcus aureus. Biometals 19:193–203.
  • Mariscotti JF, Garcia-Del Portillo F, Pucciarelli MG. 2009. The Listeria monocytogenes sortase-B recognizes varied amino acids at position 2 of the sorting motif. J Biol Chem 284:6140–6146.
  • Matias VR, Al-Amoudi A, Dubochet J, Beveridge TJ. 2003. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185:6112–6118.
  • Matias VR, Beveridge TJ. 2007. Cryo-electron microscopy of cell division in Staphylococcus aureus reveals a mid-zone between nascent cross walls. Mol Microbiol 64:195–206.
  • Mazmanian SK, Liu G, Jensen ER, Lenoy E, Schneewind O. 2000. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc Natl Acad Sci USA 97:5510–5515.
  • Mazmanian SK, Liu G, Ton-That H, Schneewind O. 1999. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760–763.
  • Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, 2003. Passage of heme-iron across the envelope of Staphylococcus aureus.. Science 299:906–909.
  • Mazmanian SK, Ton-That H, Su K, Schneewind O. 2002. An iron-regulated sortase anchors a class of surface protien during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci USA 99:2293–2298.
  • Mazurier J, Spik G. 1980. Comparative study of the iron-binding properties of human transferrins. I. Complete and sequential iron saturation and desaturation of the lactotransferrin. Biochim Biophys Acta 629:399–408.
  • Mclaughlin H, Xiao Q, Rea RB, Pi H, Casey PG, Darby T, 2012. A putative P-type ATPase required for virulence and resistance to haem toxicity in Listeria monocytogenes. PLoS One 7:e30928.
  • Meroueh SO, Bencze KZ, Hesek D, Lee M, Fisher JF, Stemmler TL, 2006. Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc Natl Acad Sci USA 103:4404–4409.
  • Morton DJ, Whitby PW, Jin H, Ren Z, Stull TL. 1999. Effect of multiple mutations in the hemoglobin- and hemoglobin-haptoglobin-binding proteins, HgpA, HgpB, and HgpC, of Haemophilus influenzae type b. Infect Immun 67:2729–2739.
  • Navarre WW, Schneewind O. 1994. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria. Mol Microbiol 14:115–121.
  • Navarre WW, Schneewind O. 1999. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229.
  • Negari S, Sulpher J, Pacello F, Ingrey K, Battistoni A, Lee BC. 2008. A role for Haemophilus ducreyi Cu, ZnSOD in resistance to heme toxicity. Biometals 21:249–258.
  • Newton SM, Igo JD, Scott DC, Klebba PE. 1999. Effect of loop deletions on the binding and transport of ferric enterobactin by FepA. Mol Microbiol 32:1153–1165.
  • Newton SM, Klebba PE, Raynaud C, Shao Y, Jiang X, Dubail I, 2005. The svpA-srtB locus of Listeria monocytogenes: Fur-mediated iron regulation and effect on virulence. Mol Microbiol 55:927–940.
  • Newton SM, Trinh V, Pi H, Klebba PE. 2010. Direct measurements of the outer membrane stage of ferric enterobactin transport: Postuptake binding. J Biol Chem 285:17488–17497.
  • Nhien NT, Huy NT, Naito M, Oida T, Uyen DT, Huang M, 2010. Neutralization of toxic haem by Porphyromonas gingivalis haemoglobin receptor. J Biochem 147:317–325.
  • Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H. 2010. Mycobacterial outer membranes: In search of proteins. Trends Microbiol 18:109–116.
  • Nikaido H, Vaara M. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49:1–32.
  • Nobles CL, Maresso AW. 2011. The theft of host heme by Gram-positive pathogenic bacteria. Metallomics 3:788–796.
  • Nygaard TK, Blouin GC, Liu M, Fukumura M, Olson JS, Fabian M, 2006. The mechanism of direct heme transfer from the streptococcal cell surface protein Shp to HtsA of the HtsABC transporter. J Biol Chem 281:20761–20771.
  • Perez-Dorado I, Campillo NE, Monterroso B, Hesek D, Lee M, Paez JA, 2007. Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin CPL-1. J Biol Chem 282:24990–24999.
  • Perez-Dorado I, Gonzalez A, Morales M, Sanles R, Striker W, Vollmer W, 2010. Insights into pneumococcal fratricide from the crystal structures of the modular killing factor LytC. Nat Struct Mol Biol 17:576–581.
  • Pilpa RM, Robson SA, Villareal VA, Wong ML, Phillips M, Clubb RT. 2009. Functionally distinct NEAT (NEAr Transporter) domains within the Staphylococcus aureus IsdH/HarA protein extract heme from methemoglobin. J Biol Chem 284:1166–1176.
  • Popowska M. 2004. Analysis of the peptidoglycan hydrolases of Listeria monocytogenes: Multiple enzymes with multiple functions. Pol J Microbiol 53(Suppl):29–34.
  • Porter J, Arreguin S, Pierpont CG. 2010. Ferric iron complexes of dopamine and 5,6-dihydroxyindole with nta, edda, and edta as ancillary ligands. Inorg Chim Acta 363:2800–2803.
  • Raymond KN, Carrano CJ. 1979. Coordination chemistry and microbial iron transport. Accts Chem Res 12:183–190.
  • Ren Z, Jin H, Morton DJ, Stull TL. 1998. hgpB, a gene encoding a second Haemophilus influenzae hemoglobin- and hemoglobin-haptoglobin-binding protein. Infect Immun 66:4733–4741.
  • Richardson AR, Stojiljkovic I. 1999. HmbR, a hemoglobin-binding outer membrane protein of Neisseria meningitidis, undergoes phase variation. J Bacteriol 181:2067–2074.
  • Roche TE, Hiromasa Y. 2007. Pyruvate dehydrogenase kinase regulatory mechanisms and inhibition in treating diabetes, heart ischemia, and cancer. Cell Mol Life Sci 64:830–849.
  • Roden JA, Wells DH, Chomel BB, Kasten RW, Koehler JE. 2012. Hemin binding protein C is found in outer membrane vesicles and protects Bartonella henselae against toxic concentrations of hemin. Infect Immun 80:929–942.
  • Rouquette C, Bolla JM, Berche P. 1995. An iron-dependent mutant of Listeria monocytogenes of attenuated virulence. FEMS Microbiol Lett 133:77–83.
  • Rozalska B, Lisiecki P, Sadowska B, Mikucki J, Rudnicka W. 1998. The virulence of Staphylococcus aureus isolates differing by siderophore production. Acta Microbiol Pol 47:185–194.
  • Saier MH Jr. 2000. Families of proteins forming transmembrane channels. J Membr Biol 175:165–180.
  • Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, 1999. The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279.
  • Sanders JD, Cope LD, Hansen EJ. 1994. Identification of a locus involved in the utilization of iron by Haemophilus influenzae.. Infect Immun 62:4515–4525.
  • Scheurwater EM, Burrows LL. 2011. Maintaining network security: How macromolecular structures cross the peptidoglycan layer. FEMS Microbiol Lett 318:1–9.
  • Schiffler B, Barth E, Daffe M, Benz R. 2007. Corynebacterium diphtheriae: Identification and characterization of a channel-forming protein in the cell wall. J Bacteriol 189:7709–7719.
  • Schneewind O, Mihaylova-Petkov D, Model P. 1993. Cell wall sorting signals in surface proteins of Gram-positive bacteria. EMBO J 12:4803–4811.
  • Schryvers AB, Stojiljkovic I. 1999. Iron acquisition systems in the pathogenic Neisseria. Mol Microbiol 32:1117–1123.
  • Schwarzenbach G, Schwarzenbach K. 1963. Hydroxamatkomplexe I. Die stabilitat der Eisen (III)-komplexe einfacher hydroxamsauren und des ferroxamins B. Helv Chim Acta 46:1390–1400.
  • Schwyn B, Neilands JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56.
  • Scott DC, Cao Z, Qi Z, Bauler M, Igo JD, Newton SM, 2001. Exchangeability of N termini in the ligand-gated porins of Escherichia coli.. J Biol Chem 276:13025–13033.
  • Sebulsky MT, Hohnstein D, Hunter MD, Heinrichs DE. 2000. Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus.. J Bacteriol 182:4394–4400.
  • Sharp KH, Schneider S, Cockayne A, Paoli M. 2007. Crystal structure of the heme-IsdC complex, the central conduit of the Isd iron/heme uptake system in Staphylococcus aureus.. J Biol Chem 282:10625–10631.
  • Spirig T, Weiner EM, Clubb RT. 2011. Sortase enzymes in Gram-positive bacteria. Mol Microbiol 82:1044–1059.
  • Sprencel C, Cao Z, Qi Z, Scott DC, Montague MA, Ivanoff N, 2000. Binding of ferric enterobactin by the Escherichia coli periplasmic protein fepB. J Bacteriol 182:5359–5364.
  • Stauff DL, Bagaley D, Torres VJ, Joyce R, Anderson KL, Kuechenmeister L, 2008. Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J Bacteriol 190:3588–3596.
  • Stauff DL, Skaar EP. 2009. The heme sensor system of Staphylococcus aureus.. Contrib Microbiol 16:120–135.
  • Stevens MK, Porcella S, Klesney-Tait J, Lumbley S, Thomas SE, Norgard MV, 1996. A hemoglobin-binding outer membrane protein is involved in virulence expression by Haemophilus ducreyi in an animal model. Infect Immun 64:1724–1735.
  • Stojiljkovic I, Hwa V, Larson J, Lin L, So M, Nassif X. 1997. Cloning and characterization of the Neisseria meningitidis rfaC gene encoding alpha-1,5 heptosyltransferase I. FEMS Microbiol Lett 151:41–49.
  • Tai SS, Lee CJ, Winter RE. 1993. Hemin utilization is related to virulence of Streptococcus pneumoniae.. Infect Immun 61:5401–5405.
  • Thomas KL, Leduc I, Olsen B, Thomas CE, Cameron DW, Elkins C. 2001. Cloning, overexpression, purification, and immunobiology of an 85-kilodalton outer membrane protein from Haemophilus ducreyi.. Infect Immun 69:4438–4446.
  • Tidmarsh GF, Klebba PE, Rosenberg LT. 1983. Rapid release of iron from ferritin by siderophores. J Inorg Biochem 18:161–168.
  • Tomasz A. 1979. From penicillin-binding proteins to the lysis and death of bacteria: A 1979 view. Rev Infect Dis 1:434–467.
  • Ton-That H, Liu G, Mazmanian SK, Faull KF, Schneewind O. 1999. Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc Natl Acad Sci USA 96:12424–12429.
  • Ton-That H, Mazmanian SK, Faull KF, Schneewind O. 2000. Anchoring of surface proteins to the cell wall of Staphylococcus aureus. Sortase catalyzed in vitro transpeptidation reaction using LPXTG peptide and NH(2)-Gly(3) substrates. J Biol Chem 275:9876–9881.
  • Torres VJ, Pishchany G, Humayun M, Schneewind O, Skaar EP. 2006. Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J Bacteriol 188:8421–8429.
  • Touhami A, Jericho MH, Beveridge TJ. 2004. Atomic force microscopy of cell growth and division in Staphylococcus aureus.. J Bacteriol 186:3286–3295.
  • Trias J, Jarlier V, Benz R. 1992. Porins in the cell wall of mycobacteria. Science 258:1479–1481.
  • Tsolis RM, Baumler AJ, Heffron F, Stojiljkovic I. 1996. Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect Immun 64:4549–4556.
  • Vollmer W, Blanot D, De Pedro MA. 2008. Peptidoglycan structure and architecture. FEMS Microbiol Rev 32:149–167.
  • Vollmer W, Seligman SJ. 2010. Architecture of peptidoglycan: More data and more models. Trends Microbiol 18:59–66.
  • Ward CG, Bullen JJ, Rogers HJ. 1996. Iron and infection: New developments and their implications. J Trauma 41:356–364.
  • Wayne R, Neilands JB. 1975. Evidence for common binding sites for ferrichrome compounds and bacteriophage phi 80 in the cell envelope of Escherichia coli.. J Bacteriol 121:497–503.
  • Weiss WJ, Lenoy E, Murphy T, Tardio L, Burgio P, Projan SJ, 2004. Effect of srtA and srtB gene expression on the virulence of Staphylococcus aureus in animal models of infection. The structure of sortase B, a cysteine transpeptidase that tethers surface protein to the Staphylococcus aureus cell wall IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Antimicrob Chemother 4:4.
  • Xiao Q, Jiang X, Moore KJ, Shao Y, Pi H, Dubail I, 2011. Sortase independent and dependent systems for acquisition of haem and haemoglobin in Listeria monocytogenes. Mol Microbiol 80:1581–1597.
  • Yem DW, Wu HC. 1978. Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. J Bacteriol 133:1419–1426.
  • Young KD. 2006. Too many strictures on structure. Trends Microbiol 14:155–156.
  • Zhang Z, Aboulwafa M, Smith MH, Saier MH Jr. 2003. The ascorbate transporter of Escherichia coli.. J Bacteriol 185:2243–2250.
  • Zhu H, Liu M, Lei B. 2008a. The. surface protein Shr of Streptococcus pyogenes binds heme and transfers it to the streptococcal heme-binding protein Shp. BMC Microbiol 8:15.
  • Zhu H, Xie G, Liu M, Olson JS, Fabian M, Dooley DM, 2008b. Pathway for heme uptake from human methemoglobin by the iron-regulated surface determinants system of Staphylococcus aureus.. J Biol Chem 283:18450–18460.
  • Zhu W, Hunt DJ, Richardson AR, Stojiljkovic I. 2000. Use of heme compounds as iron sources by pathogenic neisseriae requires the product of the hemO gene. J Bacteriol 182:439–447.
  • Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffe M. 2008. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 190:5672–5680.

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