Advertisement

Siderophores: A Novel Approach to Fight Antimicrobial Resistance

  • Marta Ribeiro
  • Manuel SimõesEmail author
Chapter
Part of the Environmental Chemistry for a Sustainable World book series (ECSW, volume 28)

Abstract

The increasing bacterial resistance subsequent to antibiotic use has instigated the development of new and effective antimicrobial strategies. Bacterial iron uptake systems are novel therapeutic agents since iron is crucial for the growth and development of microorganisms as well as a main virulence factor during the establishment of an infection. The method commonly used for iron assimilation is based on the production of siderophores, which are low molecular weight iron chelators produced by bacteria, fungi, and plants to facilitate iron uptake and crucial for bacterial pathogenicity. Therefore, in recent year’s siderophore iron uptake, systems have received much attention as novel targets for antimicrobial approaches.

Here we review siderophores in the antimicrobial field. We first outline the problematic of bacterial resistance to available marketed antibacterial drugs and, consequently, the current needs to contrast with the emergence of bacterial resistance. After, we emphasize the critical role of iron for bacterial growth and development and how pathogens compete with the host for iron. The biosynthesis, regulation, and transport of siderophores are also discussed. Lastly, we review work done with siderophores in the antimicrobial field. Such work has generally been done using three essential approaches: siderophore-mediated drug delivery, inhibition of siderophores biosynthesis, and iron starvation via competitive chelation.

Keywords

Antimicrobial resistance Bacterial infections Biofilm Drug delivery Iron Siderophores Trojan Horse approach 

Notes

Acknowledgements

This work was supported by projects: POCI-01-0145-FEDER-030219; POCI-01-0145-FEDER-007274; POCI-01-0145-FEDER-029777; POCI-01-0145-FEDER-006939 – Laboratory for Process Engineering, Environment, Biotechnology and Energy (LEPABE) – funded by Fundo Europeu de Desenvolvimento Regional (FEDER) funds through COMPETE2020 – Programa Operacional Competitividade e Internacionalização (POCI); by national funds through Fundação para a Ciência e a Tecnologia (FCT) and the post-doc grant awarded to Anabela Borges (SFRH/BPD/98684/2013); and project NORTE-01-0145-FEDER-000005 – LEPABE-2-ECO-INNOVATION, funded by Fundo Europeu de Desenvolvimento Regional (FEDER) through COMPETE2020 – Programa Operacional Competitividade e Internacionalização (POCI) and Programa Operacional Regional do Norte (NORTE2020).

References

  1. Ahmed E, Holmstrom SJ (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208.  https://doi.org/10.1111/1751-7915.12117 CrossRefGoogle Scholar
  2. Alanis AJ (2005) Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res 36:697–705.  https://doi.org/10.1016/j.arcmed.2005.06.009 CrossRefGoogle Scholar
  3. Andersson DI, Hughes D (2011) Persistence of antibiotic resistance in bacterial populations. FEMS Microbiol Rev 35:901–911.  https://doi.org/10.1111/j.1574-6976.2011.00289.x CrossRefGoogle Scholar
  4. Antunes LC, Imperi F, Minandri F, Visca P (2012) In vitro and in vivo antimicrobial activities of gallium nitrate against multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 56:5961–5970.  https://doi.org/10.1128/AAC.01519-12 CrossRefGoogle Scholar
  5. Auletta S, Galli F, Lauri C, Martinelli D, Santino I, Signore A (2016) Imaging bacteria with radiolabelled quinolones, cephalosporins and siderophores for imaging infection: a systematic review. Clin Transl Imag 4:229–252.  https://doi.org/10.1007/s40336-016-0185-8 CrossRefGoogle Scholar
  6. Azevedo AS, Almeida C, Melo LF, Azevedo NF (2017) Impact of polymicrobial biofilms in catheter-associated urinary tract infections. Crit Rev Microbiol 43:423–439.  https://doi.org/10.1080/1040841X.2016.1240656 CrossRefGoogle Scholar
  7. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102:11076–11081.  https://doi.org/10.1073/pnas.0504266102 CrossRefGoogle Scholar
  8. Banin E, Brady KM, Greenberg EP (2006) Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol 72:2064–2069.  https://doi.org/10.1128/AEM.72.3.2064-2069.2006 CrossRefGoogle Scholar
  9. Banin E, Lozinski A, Brady KM, Berenshtein E, Butterfield PW, Moshe M, Chevion M, Greenberg EP, Banin E (2008) The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc Natl Acad Sci U S A 105:16761–16766.  https://doi.org/10.1073/pnas.0808608105 CrossRefGoogle Scholar
  10. Beasley FC, Marolda CL, Cheung J, Buac S, Heinrichs DE (2011) Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79:2345–2355.  https://doi.org/10.1128/IAI.00117-11 CrossRefGoogle Scholar
  11. Behnsen J, Raffatellu M (2016) Siderophores: more than stealing iron. MBio 7:e01906–e01916.  https://doi.org/10.1128/mBio.01906-16 CrossRefGoogle Scholar
  12. Blackledge MS, Worthington RJ, Melander C (2013) Biologically inspired strategies for combating bacterial biofilms. Curr Opin Pharmacol 13:699–706.  https://doi.org/10.1016/j.coph.2013.07.004 CrossRefGoogle Scholar
  13. Bonchi C, Imperi F, Minandri F, Visca P, Frangipani E (2014) Repurposing of gallium-based drugs for antibacterial therapy. Biofactors 40:303–312.  https://doi.org/10.1002/biof.1159 CrossRefGoogle Scholar
  14. Braun V, Pramanik A, Gwinner T, Köberle M, Bohn E (2009) Sideromycins: tools and antibiotics. Biometals 22:3.  https://doi.org/10.1007/s10534-008-9199-7 CrossRefGoogle Scholar
  15. Bunet R, Brock A, Rexer HU, Takano E (2006) Identification of genes involved in siderophore transport in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 262:57–64.  https://doi.org/10.1111/j.1574-6968.2006.00362.x CrossRefGoogle Scholar
  16. Cabral DJ, Wurster JI, Belenky P (2018) Antibiotic persistence as a metabolic adaptation: stress, metabolism, the host, and new directions. Pharmaceuticals 11:1–19.  https://doi.org/10.3390/ph11010014 CrossRefGoogle Scholar
  17. Cai S, Qiao X, Feng L, Shi N, Wang H, Yang H, Guo Z, Wang M, Chen Y, Wang Y (2018) Python cathelicidin CATHPb1 protects against multidrug-resistant staphylococcal infections by antimicrobial-immunomodulatory duality. J Med Chem 61:2075–2086.  https://doi.org/10.1021/acs.jmedchem.8b00036 CrossRefGoogle Scholar
  18. Chatterjee A, O’Brian MR (2018) Rapid evolution of a bacterial iron acquisition system. Mol Microbiol.  https://doi.org/10.1111/mmi.13918 CrossRefGoogle Scholar
  19. Cheung J, Beasley FC, Liu S, Lajoie GA, Heinrichs DE (2009) Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol Microbiol 74:594–608.  https://doi.org/10.1111/j.1365-2958.2009.06880.x CrossRefGoogle Scholar
  20. Cheung J, Murphy ME, Heinrichs DE (2012) Discovery of an iron-regulated citrate synthase in Staphylococcus aureus. Chem Biol 19:1568–1578.  https://doi.org/10.1016/j.chembiol.2012.10.003 CrossRefGoogle Scholar
  21. Chitambar CR (2016) Gallium and its competing roles with iron in biological systems. Biochim Biophys Acta 1863:2044–2053.  https://doi.org/10.1016/j.bbamcr.2016.04.027 CrossRefGoogle Scholar
  22. Chitambar CR (2017) The therapeutic potential of iron-targeting gallium compounds in human disease: from basic research to clinical application. Pharmacol Res 115:56–64.  https://doi.org/10.1016/j.phrs.2016.11.009 CrossRefGoogle Scholar
  23. Chu BC, Garcia-Herrero A, Johanson TH, Krewulak KD, Lau CK, Peacock RS, Slavinskaya Z, Vogel HJ (2010) Siderophore uptake in bacteria and the battle for iron with the host; a bird’s eye view. Biometals 23:601–611.  https://doi.org/10.1007/s10534-010-9361-x CrossRefGoogle Scholar
  24. Coll F, Phelan J, Hill-Cawthorne GA, Nair MB, Mallard K, Ali S, Abdallah AM, Alghamdi S, Alsomali M, Ahmed AO (2018) Genome-wide analysis of multi-and extensively drug-resistant mycobacterium tuberculosis. Nat Genet 50:307–316.  https://doi.org/10.1038/s41588-017-0029-0 CrossRefGoogle Scholar
  25. Cornelis P (2010) Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol 86:1637–1645.  https://doi.org/10.1007/s00253-010-2550-2 CrossRefGoogle Scholar
  26. Dale SE, Doherty-Kirby A, Lajoie G, Heinrichs DE (2004) Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect Immun 72:29–37.  https://doi.org/10.1128/IAI.72.1.29-37.2004 CrossRefGoogle Scholar
  27. Dave BP, Anshuman K, Hajela P (2006) Siderophores of halophilic archaea and their chemical characterization. Indian J Exp Biol 44:340–344Google Scholar
  28. Ding P, Schous CE, Miller MJ (2008) Design and synthesis of a novel protected mixed ligand siderophore. Tetrahedron Lett 49:2306–2310.  https://doi.org/10.1016/j.tetlet.2008.02.007 CrossRefGoogle Scholar
  29. Drechsel H, Tschierske M, Thieken A, Jung G, Zähner H, Winkelmann G (1995) The carboxylate type siderophore rhizoferrin and its analogs produced by directed fermentation. J Ind Microbiol 14:105–112CrossRefGoogle Scholar
  30. Driscoll JA, Brody SL, Kollef MH (2007) The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 67:351–368.  https://doi.org/10.2165/00003495-200767030-00003 CrossRefGoogle Scholar
  31. Dumas Z, Ross-Gillespie A, Kümmerli R (2013) Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc Biol Sci 280:20131055.  https://doi.org/10.1098/rspb.2013.1055 CrossRefGoogle Scholar
  32. Eby G (2005) Elimination of arthritis pain and inflammation for over 2 years with a single 90 min, topical 14% gallium nitrate treatment: case reports and review of actions of gallium III. Med Hypotheses 65:1136–1141.  https://doi.org/10.1016/j.mehy.2005.06.021 CrossRefGoogle Scholar
  33. Ellermann M, Arthur JC (2017) Siderophore-mediated iron acquisition and modulation of host-bacterial interactions. Free Radic Biol Med 105:68–78.  https://doi.org/10.1016/j.freeradbiomed.2016.10.489 CrossRefGoogle Scholar
  34. Faraldo-Gomez JD, Sansom MS (2003) Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4:105–116.  https://doi.org/10.1038/nrm1015 CrossRefGoogle Scholar
  35. Ferguson AD, Braun V, Fiedler HP, Coulton JW, Diederichs K, Welte W (2000) Crystal structure of the antibiotic albomycin in complex with the outer membrane transporter FhuA. Protein Sci 9:956–963.  https://doi.org/10.1110/ps.9.5.956 CrossRefGoogle Scholar
  36. Ferreras JA, Ryu J-S, Di Lello F, Tan DS, Quadri LEN (2005) Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat Chem Biol 1:29–32.  https://doi.org/10.1038/nchembio706 CrossRefGoogle Scholar
  37. Finking R, Marahiel MA (2004) Biosynthesis of nonribosomal peptides1. Annu Rev Microbiol 58:453–488.  https://doi.org/10.1146/annurev.micro.58.030603.123615 CrossRefGoogle Scholar
  38. Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325:1089–1093.  https://doi.org/10.1126/science.1176667 CrossRefGoogle Scholar
  39. Fukushima T, Allred BE, Sia AK, Nichiporuk R, Andersen UN, Raymond KN (2013) Gram-positive siderophore-shuttle with iron-exchange from Fe-siderophore to apo-siderophore by Bacillus cereus YxeB. Proc Natl Acad Sci U S A 110:13821–13826.  https://doi.org/10.1073/pnas.1304235110 CrossRefGoogle Scholar
  40. Ganz T (2018) Iron and infection. Int J Hematol 107:7–15.  https://doi.org/10.1007/s12185-017-2366-2 CrossRefGoogle Scholar
  41. Garenaux A, Caza M, Dozois CM (2011) The ins and outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli. Vet Microbiol 153:89–98.  https://doi.org/10.1016/j.vetmic.2011.05.023 CrossRefGoogle Scholar
  42. Ghosh A, Ghosh M, Niu C, Malouin F, Moellmann U, Miller MJ (1996) Iron transport-mediated drug delivery using mixed-ligand siderophore-beta-lactam conjugates. Chem Biol 3:1011–1019.  https://doi.org/10.1016/S1074-5521(96)90167-2 CrossRefGoogle Scholar
  43. Glick R, Gilmour C, Tremblay J, Satanower S, Avidan O, Deziel E, Greenberg EP, Poole K, Banin E (2010) Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 192:2973–2980.  https://doi.org/10.1128/JB.01601-09 CrossRefGoogle Scholar
  44. Granato ET, Kümmerli R (2017) The path to re-evolve cooperation is constrained in Pseudomonas aeruginosa. BMC Evol Biol 17:214.  https://doi.org/10.1186/s12862-017-1060-6 CrossRefGoogle Scholar
  45. Grobelak A, Hiller J (2017) Bacterial siderophores promote plant growth: screening of catechol and hydroxamate siderophores. Int J Phytoremediation 19:825–833.  https://doi.org/10.1080/15226514.2017.1290581 CrossRefGoogle Scholar
  46. Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657.  https://doi.org/10.1039/b906679a CrossRefGoogle Scholar
  47. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332.  https://doi.org/10.1016/j.ijantimicag.2009.12.011 CrossRefGoogle Scholar
  48. Holden VI, Lenio S, Kuick R, Ramakrishnan SK, Shah YM, Bachman MA (2014) Bacterial siderophores that evade or overwhelm lipocalin 2 induce hypoxia inducible factor 1α and proinflammatory cytokine secretion in cultured respiratory epithelial cells. Infect Immun 82:3826–3836.  https://doi.org/10.1128/IAI.01849-14 CrossRefGoogle Scholar
  49. Holden VI, Breen P, Houle S, Dozois CM, Bachman MA (2016) Klebsiella pneumoniae siderophores induce inflammation, bacterial dissemination, and HIF-1α stabilization during pneumonia. MBio 7:e01397–e01316.  https://doi.org/10.1128/mBio.01397-16 CrossRefGoogle Scholar
  50. Imperi F, Massai F, Facchini M, Frangipani E, Visaggio D, Leoni L, Bragonzi A, Visca P (2013) Repurposing the antimycotic drug flucytosine for suppression of Pseudomonas aeruginosa pathogenicity. Proc Natl Acad Sci U S A 110:7458–7463.  https://doi.org/10.1073/pnas.1222706110 CrossRefGoogle Scholar
  51. Ivanova A, Ivanova K, Hoyo J, Heinze T, Sanchez-Gomez S, Tzanov T (2018) Layer-by-layer decorated nanoparticles with uunable antibacterial and antibiofilm properties against both Gram-Positive and Gram-Negative bacteria. ACS Appl Mater Interfaces 10:3314–3323.  https://doi.org/10.1021/acsami.7b16508 CrossRefGoogle Scholar
  52. Javvadi S, Pandey SS, Mishra A, Pradhan BB, Chatterjee S (2018) Bacterial cyclic β-(1,2)-glucans sequester iron to protect against iron-induced toxicity. EMBO Rep 19:172–186.  https://doi.org/10.15252/embr.201744650 CrossRefGoogle Scholar
  53. Ji C, Juarez-Hernandez RE, Miller MJ (2012) Exploiting bacterial iron acquisition: siderophore conjugates. Future Med Chem 4:297–313.  https://doi.org/10.4155/fmc.11.191 CrossRefGoogle Scholar
  54. Juan C, Peña C, Oliver A (2017) Host and pathogen biomarkers for severe Pseudomonas aeruginosa infections. J Infect Dis 215:S44–S51.  https://doi.org/10.1093/infdis/jiw299 CrossRefGoogle Scholar
  55. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117:877–888.  https://doi.org/10.1172/JCI30783 CrossRefGoogle Scholar
  56. Kang D, Kirienko NV (2017) High-throughput genetic screen reveals that early attachment and biofilm formation are necessary for full Pyoverdine production by Pseudomonas aeruginosa. Front Microbiol 8:1–15.  https://doi.org/10.3389/fmicb.2017.01707 CrossRefGoogle Scholar
  57. Kohli RM, Trauger JW, Schwarzer D, Marahiel MA, Walsh CT (2001) Generality of peptide cyclization catalyzed by isolated thioesterase domains of nonribosomal peptide synthetases. Biochemist 40:7099–7108.  https://doi.org/10.1021/bi010036j CrossRefGoogle Scholar
  58. Koo H, Allan RN, Howlin RP, Stoodley P, Hall-Stoodley L (2017) Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 15:740–755.  https://doi.org/10.1038/nrmicro.2017.99 CrossRefGoogle Scholar
  59. Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta 1778:1781–1804.  https://doi.org/10.1016/j.bbamem.2007.07.026 CrossRefGoogle Scholar
  60. Kurtjak M, Vukomanovic M, Kramer L, Suvorov D (2016) Biocompatible nano-gallium/hydroxyapatite nanocomposite with antimicrobial activity. J Mater Sci Mater Med 27:170.  https://doi.org/10.1007/s10856-016-5777-3 CrossRefGoogle Scholar
  61. Lamb AL (2015) Breaking a pathogen’s iron will: inhibiting siderophore production as an antimicrobial strategy. Biochim Biophys Acta 1854:1054–1070.  https://doi.org/10.1016/j.bbapap.2015.05.001 CrossRefGoogle Scholar
  62. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 99:7072–7077.  https://doi.org/10.1073/pnas.092016999 CrossRefGoogle Scholar
  63. Lamont IL, Konings AF, Reid DW (2009) Iron acquisition by Pseudomonas aeruginosa in the lungs of patients with cystic fibrosis. Biometals 22:53–60.  https://doi.org/10.1007/s10534-008-9197-9 CrossRefGoogle Scholar
  64. de Leseleuc L, Harris G, KuoLee R, Chen W (2012) In vitro and in vivo biological activities of iron chelators and gallium nitrate against Acinetobacter baumannii. Antimicrob Agents Chemother 56:5397–5400.  https://doi.org/10.1128/AAC.00778-12 CrossRefGoogle Scholar
  65. Matzanke BF, Anemüller S, Schünemann V, Trautwein AX, Hantke K (2004) FhuF, part of a siderophore−reductase system. Biochemist 43:1386–1392.  https://doi.org/10.1021/bi0357661 CrossRefGoogle Scholar
  66. May JJ, Wendrich TM, Marahiel MA (2001) The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276:7209–7217.  https://doi.org/10.1074/jbc.M009140200 CrossRefGoogle Scholar
  67. Meneely KM, Lamb AL (2007) Biochemical characterization of a flavin adenine dinucleotide-dependent monooxygenase, ornithine hydroxylase from Pseudomonas aeruginosa, suggests a novel reaction mechanism. Biochemistry 46:11930–11937.  https://doi.org/10.1021/bi700932q CrossRefGoogle Scholar
  68. Miao J, Chen L, Wang J, Wang W, Chen D, Li L, Li B, Deng Y, Xu Z (2017) Current methodologies on genotyping for nosocomial pathogen methicillin-resistant Staphylococcus aureus (MRSA). Microb Pathog 107:17–28.  https://doi.org/10.1016/j.micpath.2017.03.010 CrossRefGoogle Scholar
  69. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451.  https://doi.org/10.1128/MMBR.00012-07 CrossRefGoogle Scholar
  70. Miller MJ et al (2009) Utilization of microbial iron assimilation processes for the development of new antibiotics and inspiration for the design of new anticancer agents. Biometals 22:61–75.  https://doi.org/10.1007/s10534-008-9185-0 CrossRefGoogle Scholar
  71. Mills B, Bradley M, Dhaliwal K (2016) Optical imaging of bacterial infections. Clin Transl Imag 4:163–174.  https://doi.org/10.1007/s40336-016-0180-0 CrossRefGoogle Scholar
  72. Milner SJ, Seve A, Snelling AM, Thomas GH, Kerr KG, Routledge A, Duhme-Klair AK (2013) Staphyloferrin A as siderophore-component in fluoroquinolone-based Trojan horse antibiotics. Org Biomol Chem 11:3461–3468.  https://doi.org/10.1039/c3ob40162f CrossRefGoogle Scholar
  73. Mollmann U, Heinisch L, Bauernfeind A, Kohler T, Ankel-Fuchs D (2009) Siderophores as drug delivery agents: application of the “Trojan Horse” strategy. Biometals 22:615–624.  https://doi.org/10.1007/s10534-009-9219-2 CrossRefGoogle Scholar
  74. Moreau-Marquis S, O’Toole GA, Stanton BA (2009) Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am J Respir Cell Mol Biol 41:305–313.  https://doi.org/10.1165/rcmb.2008-0299OC CrossRefGoogle Scholar
  75. Murray J, Muruko T, Gill CI, Kearney MP, Farren D, Scott MG, McMullan G, Ternan NG (2017) Evaluation of bactericidal and anti-biofilm properties of a novel surface-active organosilane biocide against healthcare associated pathogens and Pseudomonas aeruginosa biolfilm. PLoS One 12:e0182624.  https://doi.org/10.1371/journal.pone.0182624 CrossRefGoogle Scholar
  76. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726.  https://doi.org/10.1074/jbc.270.45.26723 CrossRefGoogle Scholar
  77. Noël S, Guillon L, Schalk IJ, Mislin GLA (2011) Synthesis of fluorescent probes based on the Pyochelin siderophore scaffold. Org Lett 13:844–847.  https://doi.org/10.1021/ol1028173 CrossRefGoogle Scholar
  78. Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60.  https://doi.org/10.1146/annurev.micro.112408.134247 CrossRefGoogle Scholar
  79. O’Driscoll NH, Cushnie TPT, Matthews KH, Lamb AJ (2018) Colistin causes profound morphological alteration but minimal cytoplasmic membrane perforation in populations of Escherichia coli and Pseudomonas aeruginosa. Arch Microbiol.  https://doi.org/10.1007/s00203-018-1485-3 CrossRefGoogle Scholar
  80. Ouchetto H, Dias M, Mornet R, Lesuisse E, Camadro JM (2005) A new route to trihydroxamate-containing artificial siderophores and synthesis of a new fluorescent probe. Bioorg Med Chem 13:1799–1803.  https://doi.org/10.1016/j.bmc.2004.11.053 CrossRefGoogle Scholar
  81. Page MGP (2013) Siderophore conjugates. Ann N Y Acad Sci 1277:115–126.  https://doi.org/10.1111/nyas.12024 CrossRefGoogle Scholar
  82. Page MGP, Heim J (2009) Prospects for the next anti-Pseudomonas drug. Curr Opin Pharmacol 9:558–565.  https://doi.org/10.1016/j.coph.2009.08.006 CrossRefGoogle Scholar
  83. Page MGP, Dantier C, Desarbre E (2010) In vitro properties of BAL30072, a novel siderophore sulfactam with activity against multiresistant gram-negative bacilli. Antimicrob Agents Chemother 54:2291–2302.  https://doi.org/10.1128/AAC.01525-09 CrossRefGoogle Scholar
  84. Peek ME, Bhatnagar A, McCarty NA, Zughaier SM (2012) Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Interdisc Perspect Infect Dis 2012:843509.  https://doi.org/10.1155/2012/843509 CrossRefGoogle Scholar
  85. Peleg AY, Hooper DC (2010) Hospital-acquired infections due to gram-negative bacteria. N Engl J Med 362:1804–1813.  https://doi.org/10.1056/NEJMra0904124 CrossRefGoogle Scholar
  86. Petrik M, Zhai C, Haas H, Decristoforo C (2017) Siderophores for molecular imaging applications. ClinTransl Imag 5:15–27.  https://doi.org/10.1007/s40336-016-0211-x CrossRefGoogle Scholar
  87. Pitts NB, Zero DT, Marsh PD, Ekstrand K, Weintraub JA, Ramos-Gomez F, Tagami J, Twetman S, Tsakos G, Ismail A (2017) Dental caries. Nat Rev Dis Prim 3:17030.  https://doi.org/10.1038/nrdp.2017.30 CrossRefGoogle Scholar
  88. Pramanik A, Braun V (2006) Albomycin uptake via a ferric hydroxamate transport system of Streptococcus pneumoniae R6. J Bacteriol 188:3878–3886.  https://doi.org/10.1128/JB.00205-06 CrossRefGoogle Scholar
  89. Qiu KJ, Lin WJ, Zhou FY, Nan HQ, Wang BL, Li L, Lin JP, Zheng YF, Liu YH (2014) Ti-Ga binary alloys developed as potential dental materials. Mater Sci Eng C Mater Biol Appl 34:474–483.  https://doi.org/10.1016/j.msec.2013.10.004 CrossRefGoogle Scholar
  90. Raad I, Chatzinikolaou I, Chaiban G, Hanna H, Hachem R, Dvorak T, Cook G, Costerton W (2003) In vitro and ex vivo activities of minocycline and EDTA against microorganisms embedded in biofilm on catheter surfaces. Antimicrob Agents Chemother 47:3580–3585.  https://doi.org/10.1128/AAC.47.11.3580-3585.2003 CrossRefGoogle Scholar
  91. Raymond KN, Dertz EA, Kim SS (2003) Enterobactin: an archetype for microbial iron transport. Proc Natl Acad Sci U S A 100:3584–3588.  https://doi.org/10.1073/pnas.0630018100 CrossRefGoogle Scholar
  92. Roosenberg JM 2nd, Lin YM, Lu Y, Miller MJ (2000) Studies and syntheses of siderophores, microbial iron chelators, and analogs as potential drug delivery agents. Curr Med Chem 7:159–197.  https://doi.org/10.2174/0929867003375353 CrossRefGoogle Scholar
  93. Russo TA, Page MG, Beanan JM, Olson R, Hujer AM, Hujer KM, Jacobs M, Bajaksouzian S, Endimiani A, Bonomo RA (2011) In vivo and in vitro activity of the siderophore monosulfactam BAL30072 against Acinetobacter baumannii. J Antimicrob Chemother 66:867–873.  https://doi.org/10.1093/jac/dkr013 CrossRefGoogle Scholar
  94. Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53:303–317.  https://doi.org/10.1002/jobm.201100552 CrossRefGoogle Scholar
  95. Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int 23:3984–3999.  https://doi.org/10.1007/s11356-015-4294-0 CrossRefGoogle Scholar
  96. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854.  https://doi.org/10.1111/j.1462-2920.2011.02556.x CrossRefGoogle Scholar
  97. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56.  https://doi.org/10.1016/0003-2697(87)90612-9 CrossRefGoogle Scholar
  98. Shukla M, Soni I, Matsuyama K, Tran T, Tanga M, Gong L, Chopra S (2018) Identification and bio-evaluation of SRI-12742 as a antimicrobial agent against multi-drug resistant Acinetobacter baumannii. Int J Antimicrob Agents.  https://doi.org/10.1016/j.ijantimicag.2018.02.018 CrossRefGoogle Scholar
  99. Signore A, Glaudemans AW (2011) The molecular imaging approach to image infections and inflammation by nuclear medicine techniques. Ann Nucl Med 25:681–700.  https://doi.org/10.1007/s12149-011-0521-z CrossRefGoogle Scholar
  100. Simões M (2011) Antimicrobial strategies effective against infectious bacterial biofilms. Curr Med Chem 18:2129–2145.  https://doi.org/10.2174/092986711795656216 CrossRefGoogle Scholar
  101. Singh PK, Parsek MR, Greenberg EP, Welsh MJ (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417:552–555.  https://doi.org/10.1038/417552a CrossRefGoogle Scholar
  102. Singh S, Kalia NP, Joshi P, Kumar A, Sharma PR, Kumar A, Bharate SB, Khan IA (2017) Boeravinone B, A novel dual inhibitor of NorA bacterial efflux pump of Staphylococcus aureus and human P-glycoprotein, reduces the biofilm formation and intracellular invasion of bacteria. Front Microbiol 8:1868.  https://doi.org/10.3389/fmicb.2017.01868 CrossRefGoogle Scholar
  103. Smith I (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev 16:463–496.  https://doi.org/10.1128/CMR.16.3.463-496.2003 CrossRefGoogle Scholar
  104. Struve C, Krogfelt KA (2004) Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ Microbiol 6:584–590.  https://doi.org/10.1111/j.1462-2920.2004.00590.x CrossRefGoogle Scholar
  105. Swarupa V, Chaudhury A, Sarma P (2018) Iron enhances the peptidyl deformylase activity and biofilm formation in Staphylococcus aureus. 3 Biotech 8:32.  https://doi.org/10.1007/s13205-017-1050-9 CrossRefGoogle Scholar
  106. Szebesczyk A, Olshvang E, Shanzer A, Carver PL, Gumienna-Kontecka E (2016) Harnessing the power of fungal siderophores for the imaging and treatment of human diseases. Coord Chem Rev 327–328:84–109.  https://doi.org/10.1016/j.ccr.2016.05.001 CrossRefGoogle Scholar
  107. Thet NT, Wallace L, Wibaux A, Boote N, Jenkins ATA (2018) Development of a mixed-species biofilm model and its virulence implications in device related infections. J Biomed Mater Res B.  https://doi.org/10.1002/jbm.b.34103 CrossRefGoogle Scholar
  108. Tripathi A et al (2014) Baulamycins A and B, broad-spectrum antibiotics identified as inhibitors of siderophore biosynthesis in Staphylococcus aureus and Bacillus anthracis. J Am Chem Soc 136:1579–1586.  https://doi.org/10.1021/ja4115924 CrossRefGoogle Scholar
  109. Verron E, Bouler JM, Scimeca JC (2012) Gallium as a potential candidate for treatment of osteoporosis. Drug Discov Today 17:1127–1132.  https://doi.org/10.1016/j.drudis.2012.06.007 CrossRefGoogle Scholar
  110. Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30.  https://doi.org/10.1016/j.tim.2006.11.004 CrossRefGoogle Scholar
  111. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647.  https://doi.org/10.1146/annurev.micro.58.030603.123811 CrossRefGoogle Scholar
  112. Wang J, He M, Wang G, Fu Q (2017) Organic gallium treatment improves osteoporotic fracture healing through affecting the OPG/RANKL ratio and expression of serum inflammatory cytokines in ovariectomized rats. Biol Trace Elem Res.  https://doi.org/10.1007/s12011-017-1123-y CrossRefGoogle Scholar
  113. Wilson MK, Abergel RJ, Raymond KN, Arceneaux JE, Byers BR (2006) Siderophores of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Biochem Biophys Res Commun 348:320–325.  https://doi.org/10.1016/j.bbrc.2006.07.055 CrossRefGoogle Scholar
  114. Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K, Tsuji Y (2016) Siderophores in iron metabolism: from mechanism to therapy potential. Trends Mol Med 22:1077–1090.  https://doi.org/10.1016/j.molmed.2016.10.005 CrossRefGoogle Scholar
  115. Youard ZA, Wenner N, Reimmann C (2011) Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 24:513–522.  https://doi.org/10.1007/s10534-010-9399-9 CrossRefGoogle Scholar
  116. Zheng T, Nolan EM (2014) Enterobactin-mediated delivery of β-lactam antibiotics enhances antibacterial activity against pathogenic Escherichia coli. J Am Chem Soc 136:9677–9691.  https://doi.org/10.1021/ja503911p CrossRefGoogle Scholar
  117. Zimbler DL, Penwell WF, Gaddy JA, Menke SM, Tomaras AP, Connerly PL, Actis LA (2009) Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals 22:23–32.  https://doi.org/10.1007/s10534-008-9202-3 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.LEPABE – Laboratório de Engenharia de Processos, Ambiente, Biotecnologia e EnergiaFaculdade de Engenharia da Universidade do PortoPortoPortugal

Personalised recommendations