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Abstract

Antimicrobial resistance (AMR) is one of the greatest global health challenges of modern times and its prevalence is rising worldwide. AMR within bacteria reduces the efficacy of antibiotics and increases both the morbidity and the mortality associated with bacterial infections. Despite this growing risk, few antibiotics with a novel mode of action are being produced, leading to a lack of antibiotics that can effectively treat bacterial infections with AMR. Metals have a history of antibacterial use but upon the discovery of antibiotics, often became overlooked as antibacterial agents. Meanwhile, metal-based complexes have been used as treatments for other diseases, such as the gold-containing drug auranofin, used to treat rheumatoid arthritis. Metal-based antibacterial compounds have novel modes of action that provide an advantage for the treatment of bacterial infections with resistance to conventional antibiotics. In this review, the antibacterial activity, mode of action, and potential for systemic use of a number of metal-based antibacterial complexes are discussed. The current limitations of these compounds are highlighted to determine if metal-based agents are a potential solution for the treatment of bacterial infections, especially those resistant to conventional antibiotics.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-05-07
2022-01-24
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References

  1. CDC Antibiotic resistance threats in the United States, 2019. Report; 2019
  2. ECDPC Surveillance of antimicrobial resistance in Europe 2018: Stockholm: European centre for disease prevention and control; 2019
  3. WHO Antimicrobial Resistance: Global Report on Surveillance World Health Organization; 2014
    [Google Scholar]
  4. Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL et al. Antibiotic resistance-the need for global solutions. Lancet Infect Dis 2013; 13:1057–1098 [View Article][PubMed]
    [Google Scholar]
  5. Brown ED, Wright GD. Antibacterial drug discovery in the resistance era. Nature 2016; 529:336–343 [View Article]
    [Google Scholar]
  6. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 2019; 17:203–218 [View Article][PubMed]
    [Google Scholar]
  7. Harkins CP, Pichon B, Doumith M, Parkhill J, Westh H. Methicillin-resistant Staphylococcus aureus emerged long before the introduction of methicillin into clinical practice. Genome Biol 2017; 18:130
    [Google Scholar]
  8. Hameed HMA, Islam MM, Chhotaray C, Wang C, Liu Y et al. Molecular targets related drug resistance mechanisms in MDR-, XDR-, and TDR-Mycobacterium tuberculosis strains. Front Cell Infect Microbiol 2018; 8:114 [View Article][PubMed]
    [Google Scholar]
  9. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article][PubMed]
    [Google Scholar]
  10. Zare EN, Makvandi P, Ashtari B, Rossi F, Motahari A et al. Progress in conductive polyaniline-based nanocomposites for biomedical applications: a review. J Med Chem 2020; 63:1–22 [View Article][PubMed]
    [Google Scholar]
  11. Zare EN, Jamaledin R, Naserzadeh P, Afjeh-Dana E, Ashtari B et al. Metal-based nanostructures/PLGA nanocomposites: antimicrobial activity, cytotoxicity, and their biomedical applications. ACS Appl Mater Interfaces 2020; 12:3279–3300 [View Article][PubMed]
    [Google Scholar]
  12. Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 2015; 13:42–51 [View Article][PubMed]
    [Google Scholar]
  13. Ikuma K, Decho AW, Lau BL. When nanoparticles meet biofilms-interactions guiding the environmental fate and accumulation of nanoparticles. Front Microbiol 2015; 6:591 [View Article][PubMed]
    [Google Scholar]
  14. Exner M, Bhattacharya S, Christiansen B, Gebel J, Goroncy-Bermes P. Antibiotic resistance: what is so special about multidrug-resistant Gram-negative bacteria?. GMS Hyg Infect Control 2017; 12:Doc05
    [Google Scholar]
  15. Ghai I, Ghai S. Understanding antibiotic resistance via outer membrane permeability. Infect Drug Resist 2018; 11:523–530 [View Article]
    [Google Scholar]
  16. Pachori P, Gothalwal R, Gandhi P. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis 2019; 6:109–119
    [Google Scholar]
  17. Beceiro A, Tomás M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world?. Clin Microbiol Rev 2013; 26:185–230 [View Article][PubMed]
    [Google Scholar]
  18. PEW Trusts Antibiotics currently in global clinical development; 2020
  19. Alexander JW. History of the medical use of silver. Surg Infect 2009; 10:289–292 [View Article][PubMed]
    [Google Scholar]
  20. Gasser G. Metal complexes and medicine: a successful combination. CHIMIA Int J Chem 2015; 69:442–446 [View Article]
    [Google Scholar]
  21. Haldar AK, Sen P, Roy S. Use of antimony in the treatment of leishmaniasis: current status and future directions. Mol Biol Int 2011; 2011:571242–23 [View Article][PubMed]
    [Google Scholar]
  22. Domingos S, André V, Quaresma S, Martins ICB, Minas da Piedade MF et al. New forms of old drugs: improving without changing. J Pharm Pharmacol 2015; 67:830–846 [View Article][PubMed]
    [Google Scholar]
  23. Simpson PV, Desai NM, Casari I, Massi M, Falasca M. Metal-Based antitumor compounds: beyond cisplatin. Future Med Chem 2019; 11:119–135 [View Article][PubMed]
    [Google Scholar]
  24. Holm RH, Kennepohl P, Solomon EI. Structural and functional aspects of metal sites in biology. Chem Rev 1996; 96:2239–2314 [View Article][PubMed]
    [Google Scholar]
  25. Frei A, Zuegg J, Elliott AG, Baker M, Braese S et al. Metal complexes as a promising source for new antibiotics. Chem Sci 2020; 11:2627–2639 [View Article][PubMed]
    [Google Scholar]
  26. Frei A. Metal complexes, an Untapped source of antibiotic potential?. Antibiotics 2020; 9:90
    [Google Scholar]
  27. Klasen HJ. Historical review of the use of silver in the treatment of burns. I. early uses. Burns 2000; 26:117–130 [View Article][PubMed]
    [Google Scholar]
  28. Chernousova S, Epple M. Silver as antibacterial agent: ion, nanoparticle, and metal. Angew Chem Int Ed Engl 2013; 52:1636–1653 [View Article][PubMed]
    [Google Scholar]
  29. Nowack B, Krug HF, Height M. 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 2011; 45:1177–1183 [View Article][PubMed]
    [Google Scholar]
  30. Brett DW. A discussion of silver as an antimicrobial agent: alleviating the confusion. Ostomy Wound Manage 2006; 52:34–41[PubMed]
    [Google Scholar]
  31. Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF et al. Nanotechnology in the real world: Redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 2015; 6:1769–1780 [View Article][PubMed]
    [Google Scholar]
  32. Morsi NM, Abdelbary GA, Ahmed MA. Silver sulfadiazine based cubosome hydrogels for topical treatment of burns: development and in vitro/in vivo characterization. Eur J Pharm Biopharm 2014; 86:178–189 [View Article][PubMed]
    [Google Scholar]
  33. Sierra MA, Casarrubios L, de la Torre MC. Bio-Organometallic derivatives of antibacterial drugs. Chemistry 2019; 25:7232–7242 [View Article][PubMed]
    [Google Scholar]
  34. Aziz Z, Abu SF, Chong NJ. A systematic review of silver-containing dressings and topical silver agents (used with dressings) for burn wounds. Burns 2012; 38:307–318
    [Google Scholar]
  35. Vasilev K, Cook J, Griesser HJ. Antibacterial surfaces for biomedical devices. Expert Rev Med Devices 2009; 6:553–567 [View Article][PubMed]
    [Google Scholar]
  36. U.S National library of medicine. https://www.clinicaltrials.gov/ June 8, 2020
  37. Barras F, Aussel L, Ezraty B. Silver and antibiotic, new facts to an old story. Antibiotics 2018; 7:79
    [Google Scholar]
  38. Arakawa H, Neault JF, Tajmir-Riahi HA. Silver(I) complexes with DNA and RNA studied by Fourier transform infrared spectroscopy and capillary electrophoresis. Biophys J 2001; 81:1580–1587
    [Google Scholar]
  39. Lansdown A. Silver in health care: antimicrobial effects and safety in use. Karger 2006; 33:17–34
    [Google Scholar]
  40. Russell AD, Hugo WB. Antimicrobial activity and action of silver. Prog Med Chem 1994; 31:351–370
    [Google Scholar]
  41. Morones-Ramirez JR, Winkler JA, Spina CS, Collins JJ. Silver enhances antibiotic activity against gram-negative bacteria. Sci Transl Med 2013; 5:190ra181
    [Google Scholar]
  42. Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN et al. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus . J Biomed Mater Res 2000; 52:662–668 [View Article][PubMed]
    [Google Scholar]
  43. Wang H, Yan A, Liu Z, Yang X, Xu Z. Deciphering molecular mechanism of silver by integrated omic approaches enables enhancing its antimicrobial efficacy in E. coli . PLoS Biol 2019; 17:e3000292
    [Google Scholar]
  44. Wang H, Wang M, Yang X, Xu X, Hao Q et al. Antimicrobial silver targets glyceraldehyde-3-phosphate dehydrogenase in glycolysis of E. coli . Chem Sci 2019; 10:7193–7199 [View Article][PubMed]
    [Google Scholar]
  45. Vila Domínguez A, Ayerbe Algaba R, Miró Canturri A, Á RV, Smani Y. Antibacterial activity of colloidal silver against gram-negative and Gram-positive bacteria. Antibiotics 2020; 9:36
    [Google Scholar]
  46. Kascatan-Nebioglu A, Panzner MJ, Tessier CA, Cannon CL, Youngs WJ. N-Heterocyclic carbene–silver complexes: a new class of antibiotics. Coord Chem Rev 2007; 251:884–895 [View Article]
    [Google Scholar]
  47. Johnson NA, Southerland MR, Youngs WJ. Recent developments in the medicinal applications of Silver-NHC complexes and imidazolium salts. Molecules 2017; 22:1263
    [Google Scholar]
  48. Medici S, Peana M, Crisponi G, Nurchi VM, Lachowicz JI et al. Silver coordination compounds: a new horizon in medicine. Coord Chem Rev 2016; 327-328:349–359 [View Article]
    [Google Scholar]
  49. Crudden CM, Allen DP. Stability and reactivity of N-heterocyclic carbene complexes. Coord Chem Rev 2004; 248:2247–2273 [View Article]
    [Google Scholar]
  50. Patil S, Deally A, Gleeson B, Müller-Bunz H, Paradisi F. Novel benzyl-substituted N-heterocyclic carbene–silver acetate complexes: synthesis, cytotoxicity and antibacterial studies. Metallomics 2011; 3:74–88
    [Google Scholar]
  51. Sharkey MA, Gara JP, Gordon SV, Hackenberg F, Healy C. Investigations into the antibacterial activity of the Silver-Based antibiotic drug candidate SBC3. Antibiotics 2012; 1:25–28
    [Google Scholar]
  52. Browne N, Hackenberg F, Streciwilk W, Tacke M, Kavanagh K. Assessment of in vivo antimicrobial activity of the carbene silver(I) acetate derivative SBC3 using Galleria mellonella larvae. BioMetals 2014; 27:745–752
    [Google Scholar]
  53. Junqueira JC. Galleria mellonella as a model host for human pathogens. Virulence 2012; 3:474–476
    [Google Scholar]
  54. Tsai CJ-Y, JMS L, Proft T. Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence 2016; 7:214–229
    [Google Scholar]
  55. O'Beirne C, Alhamad NF, Ma Q, Müller-Bunz H, Kavanagh K et al. Synthesis, structures and antimicrobial activity of novel NHC∗- and Ph3P-Ag(I)-Benzoate derivatives. Inorganica Chim Acta 2019; 486:294–303 [View Article]
    [Google Scholar]
  56. Patil SA, Patil SA, Patil R, Keri RS, Budagumpi S et al. N-Heterocyclic carbene metal complexes as bio-organometallic antimicrobial and anticancer drugs. Future Med Chem 2015; 7:1305–1333 [View Article][PubMed]
    [Google Scholar]
  57. Gulbranson SH, Hud JA, Hansen RC. Argyria following the use of dietary supplements containing colloidal silver protein. Cutis 2000; 66:373–374
    [Google Scholar]
  58. Rosenman KD, Moss A, Kon S. Argyria: clinical implications of exposure to silver nitrate and silver oxide. J Occup Med 1979; 21:430–435
    [Google Scholar]
  59. Weir FW. Health hazard from occupational exposure to metallic copper and silver dust. Am Ind Hyg Assoc J 1979; 40:245–247
    [Google Scholar]
  60. Pricker SP. Medical uses of gold compounds: past, present and future. Gold Bulletin 1996; 29:53–60
    [Google Scholar]
  61. Koch R. Ueber bakteriologische forschung; 1890
  62. Bertrand B, Casini A. A golden future in medicinal inorganic chemistry: the promise of anticancer gold organometallic compounds. Dalton Trans 2014; 43:4209–4219 [View Article][PubMed]
    [Google Scholar]
  63. Glišić Biljana Đ, Djuran MI. Gold complexes as antimicrobial agents: an overview of different biological activities in relation to the oxidation state of the gold ion and the ligand structure. Dalton Trans 2014; 43:5950–5969 [View Article][PubMed]
    [Google Scholar]
  64. Tiekink ERT. Gold derivatives for the treatment of cancer. Crit Rev Oncol Hematol 2002; 42:225–248 [View Article][PubMed]
    [Google Scholar]
  65. Liu W, Gust R. Update on metal N-heterocyclic carbene complexes as potential anti-tumor metallodrugs. Coord Chem Rev 2016; 329:191–213 [View Article]
    [Google Scholar]
  66. Berners-Price SJ, Filipovska A. Gold compounds as therapeutic agents for human diseases. Metallomics 2011; 3:863–873 [View Article][PubMed]
    [Google Scholar]
  67. Rackham O, Shearwood A-MJ, Thyer R, McNamara E, Davies SMK et al. Substrate and inhibitor specificities differ between human cytosolic and mitochondrial thioredoxin reductases: implications for development of specific inhibitors. Free Radic Biol Med 2011; 50:689–699 [View Article][PubMed]
    [Google Scholar]
  68. Bindoli A, Rigobello MP, Scutari G, Gabbiani C, Casini A et al. Thioredoxin reductase: a target for gold compounds acting as potential anticancer drugs. Coord Chem Rev 2009; 253:1692–1707 [View Article]
    [Google Scholar]
  69. Arnér ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 2000; 267:6102–6109 [View Article][PubMed]
    [Google Scholar]
  70. Gustafsson TN, Sahlin M, Lu J, Sjöberg B-M, Holmgren A. Bacillus anthracis thioredoxin systems, characterization and role as electron donors for ribonucleotide reductase. J Biol Chem 2012; 287:39686–39697 [View Article][PubMed]
    [Google Scholar]
  71. Rocha ER, Tzianabos AO, Smith CJ. Thioredoxin reductase is essential for thiol/disulfide redox control and oxidative stress survival of the anaerobe Bacteroides fragilis . J Bacteriol 2007; 189:8015–8023 [View Article][PubMed]
    [Google Scholar]
  72. Comtois SL, Gidley MD, Kelly DJ. Role of the thioredoxin system and the thiol-peroxidases Tpx and BCP in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori . Microbiology 2003; 149:121–129
    [Google Scholar]
  73. Scharf C, Riethdorf S, Ernst H, Engelmann S, Völker U et al. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis . J Bacteriol 1998; 180:1869–1877 [View Article][PubMed]
    [Google Scholar]
  74. Roder C, Thomson MJ. Auranofin: repurposing an old drug for a golden new age. Drugs in R&D 2015; 15:13–20
    [Google Scholar]
  75. Harbut MB, Vilchèze C, Luo X, Hensler ME, Guo H et al. Auranofin exerts broad-spectrum bactericidal activities by targeting thiol-redox homeostasis. Proc Natl Acad Sci U S A 2015; 112:4453–4458 [View Article][PubMed]
    [Google Scholar]
  76. Marzo T, Cirri D, Pollini S, Prato M, Fallani S. Auranofin and its analogues show potent antimicrobial activity against multidrug-resistant pathogens: Structure–Activity relationships. ChemMedChem 2018; 13:2448–2454
    [Google Scholar]
  77. Thangamani S, Mohammad H, Abushahba MFN, Sobreira TJP, Hedrick VE. Antibacterial activity and mechanism of action of auranofin against multi-drug resistant bacterial pathogens. Scientific Reports 2016; 6:22571
    [Google Scholar]
  78. Wu B, Yang X, Yan M. Synthesis and structure-activity relationship study of antimicrobial auranofin against ESKAPE pathogens. J Med Chem 2019; 62:7751–7768 [View Article][PubMed]
    [Google Scholar]
  79. Tharmalingam N, Ribeiro NQ, da Silva DL, Naik MT, Cruz LI et al. Auranofin is an effective agent against clinical isolates of Staphylococcus aureus . Future Med Chem 2019; 11:1417–1425 [View Article][PubMed]
    [Google Scholar]
  80. She P, Zhou L, Li S, Liu Y, Xu L et al. Synergistic microbicidal effect of auranofin and antibiotics against planktonic and biofilm-encased S. aureus and E. faecalis . Front Microbiol 2019; 10:2453 [View Article][PubMed]
    [Google Scholar]
  81. Hopkinson MN, Richter C, Schedler M, Glorius F. An overview of N-heterocyclic carbenes. Nature 2014; 510:485–496
    [Google Scholar]
  82. Dominelli B, Correia JDG, Kühn FE. Medicinal applications of gold(I/III)-based complexes bearing N-heterocyclic carbene and phosphine ligands. J Organomet Chem 2018; 866:153–164 [View Article]
    [Google Scholar]
  83. Rubbiani R, Salassa L, de Almeida A, Casini A, Ott I. Cytotoxic gold(I) n-heterocyclic carbene complexes with phosphane ligands as potent enzyme inhibitors. Chem Med Chem 2014; 9:1205–1210
    [Google Scholar]
  84. Holenya P, Can S, Rubbiani R, Alborzinia H, Jünger A. Detailed analysis of pro-apoptotic signaling and metabolic adaptation triggered by a N-heterocyclic carbene–gold(i) complex. Metallomics 2014; 6:1591–1601
    [Google Scholar]
  85. Cheng X, Holenya P, Can S, Alborzinia H, Rubbiani R. A TrxR inhibiting gold(I) NHC complex induces apoptosis through ASK1-p38-MAPK signaling in pancreatic cancer cells. Molecular Cancer 2014; 13:221
    [Google Scholar]
  86. Hickey JL, Ruhayel RA, Barnard PJ, Baker MV, Berners-Price SJ et al. Mitochondria-targeted chemotherapeutics: the rational design of gold(I) N-heterocyclic carbene complexes that are selectively toxic to cancer cells and target protein selenols in preference to thiols. J Am Chem Soc 2008; 130:12570–12571 [View Article][PubMed]
    [Google Scholar]
  87. Baker MV, Barnard PJ, Berners-Price SJ, Brayshaw SK, Hickey JL et al. Cationic, linear Au(I) N-heterocyclic carbene complexes: synthesis, structure and anti-mitochondrial activity. Dalton Trans 2006; 30:3708–3715 [View Article][PubMed]
    [Google Scholar]
  88. Rubbiani R, Kitanovic I, Alborzinia H, Can S, Kitanovic A et al. Benzimidazol-2-ylidene gold(I) complexes are thioredoxin reductase inhibitors with multiple antitumor properties. J Med Chem 2010; 53:8608–8618 [View Article][PubMed]
    [Google Scholar]
  89. Pratesi A, Gabbiani C, Michelucci E, Ginanneschi M, Papini AM et al. Insights on the mechanism of thioredoxin reductase inhibition by gold N-heterocyclic carbene compounds using the synthetic linear selenocysteine containing C-terminal peptide hTrxR(488-499): an ESI-MS investigation. J Inorg Biochem 2014; 136:161–169 [View Article][PubMed]
    [Google Scholar]
  90. Bertrand B, Stefan L, Pirrotta M, Monchaud D, Bodio E et al. Caffeine-based gold(I) N-heterocyclic carbenes as possible anticancer agents: synthesis and biological properties. Inorg Chem 2014; 53:2296–2303 [View Article][PubMed]
    [Google Scholar]
  91. Zou T, Lum CT, Chui SS-Y, Che C-M. Gold(III) complexes containing N-heterocyclic carbene ligands: thiol "switch-on" fluorescent probes and anti-cancer agents. Angew Chem Int Ed Engl 2013; 52:2930–2933 [View Article][PubMed]
    [Google Scholar]
  92. Schmidt C, Karge B, Misgeld R, Prokop A, Franke R et al. Gold(I) NHC complexes: antiproliferative activity, cellular uptake, inhibition of mammalian and bacterial thioredoxin reductases, and Gram-positive directed antibacterial effects. Chemistry 2017; 23:1869–1880 [View Article][PubMed]
    [Google Scholar]
  93. Blodgett RC, Pietrusko RG. Long-term efficacy and safety of auranofin: a review of clinical experience. Scand J Rheumatol Suppl 1986; 63:67–78[PubMed]
    [Google Scholar]
  94. Levaditi C, Bardet J, Tchakirian A, Vaisman A. Le gallium, propriétés thérapeutiques dans La syphilis et les trypanosomiases expérimentales. CR Hebd Seances Acad Sci Ser D Sci Nat 1931; 192:1142–1143
    [Google Scholar]
  95. Hart MM, Smith CF, Yancey ST, Adamson RH. Toxicity and antitumor activity of gallium nitrate and periodically related metal salts. J Natl Cancer Inst 1971; 47:1121–1127
    [Google Scholar]
  96. Edwards CL, Hayes RL. Tumor scanning with 67GA citrate. J Nucl Med 1969; 10:103–105
    [Google Scholar]
  97. Thadepalli H, Rambhatla K, Mishkin FS, Khurana MM, Niden AH. Correlation of microbiologic findings and 67Gallium scans in patients with pulmonary infections. Chest 1977; 72:442–448
    [Google Scholar]
  98. Lavender JP, Lowe J, Barker JR, Burn JI, Chaudhri MA. Gallium 67 citrate scanning in neoplastic and inflammatory lesions. Br J Radiol 1971; 44:361–366 [View Article][PubMed]
    [Google Scholar]
  99. Hayes RL. The medical use of gallium radionuclides: a brief history with some comments. Semin Nucl Med 1978; 8:183–191 [View Article][PubMed]
    [Google Scholar]
  100. Chitambar CR. Gallium-containing anticancer compounds. Future Med Chem 2012; 4:1257–1272 [View Article][PubMed]
    [Google Scholar]
  101. Timerbaev AR. Advances in developing tris(8-quinolinolato)gallium(iii) as an anticancer drug: critical appraisal and prospects. Metallomics 2009; 1:193–198
    [Google Scholar]
  102. Foster BJ, Clagett-Carr K, Hoth D, Leyland-Jones B. Gallium nitrate: the second metal with clinical activity. Cancer Treat Rep 1986; 70:1311–1319
    [Google Scholar]
  103. Kubista B, Schoefl T, Mayr L, van Schoonhoven S, Heffeter P et al. Distinct activity of the bone-targeted gallium compound KP46 against osteosarcoma cells - synergism with autophagy inhibition. J Exp Clin Cancer Res 2017; 36:52 [View Article][PubMed]
    [Google Scholar]
  104. Hara T. On the binding of gallium to transferrin. Int J Nucl Med Biol 1974; 1:152–IN1 [View Article][PubMed]
    [Google Scholar]
  105. Sephton RG, Harris AW. Brief communication: gallium-67 citrate uptake by cultured tumor cells, stimulated by serum Transferrin234. JNCI 1975; 54:1263–1266 [View Article]
    [Google Scholar]
  106. Chitambar CR, Wereley JP, Matsuyama S. Gallium-induced cell death in lymphoma: role of transferrin receptor cycling, involvement of Bax and the mitochondria, and effects of proteasome inhibition. Mol Cancer Ther 2006; 5:2834–2843 [View Article][PubMed]
    [Google Scholar]
  107. Skaar EP. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 2010; 6:e1000949 [View Article][PubMed]
    [Google Scholar]
  108. Ganz T, Nemeth E. Regulation of iron acquisition and iron distribution in mammals. Biochim Biophys Acta 2006; 1763:690–699 [View Article][PubMed]
    [Google Scholar]
  109. Puig S, Ramos-Alonso L, Romero AM, Martínez-Pastor MT. The elemental role of iron in DNA synthesis and repair. Metallomics 2017; 9:1483–1500
    [Google Scholar]
  110. Weinberg ED. Microbial pathogens with impaired ability to acquire host iron. Biometals 2000; 13:85–89
    [Google Scholar]
  111. Cornelis P, Dingemans J. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol 2013; 3:75 [View Article][PubMed]
    [Google Scholar]
  112. DeLeon K, Balldin F, Watters C, Hamood A, Griswold J et al. Gallium maltolate treatment eradicates Pseudomonas aeruginosa infection in thermally injured mice. Antimicrob Agents Chemother 2009; 53:1331–1337 [View Article][PubMed]
    [Google Scholar]
  113. Chitambar CR. The therapeutic potential of iron-targeting gallium compounds in human disease: from basic research to clinical application. Pharmacol Res 2017; 115:56–64 [View Article][PubMed]
    [Google Scholar]
  114. Schröder I, Johnson E, de Vries S. Microbial ferric iron reductases. FEMS Microbiol Rev 2003; 27:427–447 [View Article][PubMed]
    [Google Scholar]
  115. Goss CH, Kaneko Y, Khuu L, Anderson GD, Ravishankar S et al. Gallium disrupts bacterial iron metabolism and has therapeutic effects in mice and humans with lung infections. Sci Transl Med 2018; 10:eaat7520 [View Article][PubMed]
    [Google Scholar]
  116. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 2007; 117:877–888 [View Article][PubMed]
    [Google Scholar]
  117. Wooldridge KG, Williams PH. Iron uptake mechanisms of pathogenic bacteria. FEMS Microbiol Rev 1993; 12:325–348 [View Article][PubMed]
    [Google Scholar]
  118. Cornelissen CN, Sparling PF. Iron piracy: acquisition of transferrin-bound iron by bacterial pathogens. Mol Microbiol 1994; 14:843–850 [View Article][PubMed]
    [Google Scholar]
  119. Bonchi C, Imperi F, Minandri F, Visca P, Frangipani E. Repurposing of gallium-based drugs for antibacterial therapy. Biofactors 2014; 40:303–312
    [Google Scholar]
  120. Antunes LCS, Imperi F, Minandri F, Visca P. In vitro and in vivo antimicrobial activities of gallium nitrate against multidrug-resistant Acinetobacter baumannii . Antimicrob Agents Chemother 2012; 56:5961–5970 [View Article][PubMed]
    [Google Scholar]
  121. de Léséleuc L, Harris G, KuoLee R, Chen W. In vitro and in vivo biological activities of iron chelators and gallium nitrate against Acinetobacter baumannii . Antimicrob Agents Chemother 2012; 56:5397–5400 [View Article][PubMed]
    [Google Scholar]
  122. Imperi F, Tiburzi F, Fimia GM, Visca P. Transcriptional control of the pvdS iron starvation sigma factor gene by the master regulator of sulfur metabolism CysB in Pseudomonas aeruginosa . Environ Microbiol 2010; 12:1630–1642
    [Google Scholar]
  123. Yang L, Liu Y, Wu H, Song Z, Høiby N et al. Combating biofilms. FEMS Immunol Med Microbiol 2012; 65:146–157 [View Article][PubMed]
    [Google Scholar]
  124. Høiby N, Ciofu O, Johansen HK, Song ZJ, Moser C. The clinical impact of bacterial biofilms. Int J Oral Sci 2011; 3:55–65
    [Google Scholar]
  125. Fothergill JL, Winstanley C, James CE. Novel therapeutic strategies to counter Pseudomonas aeruginosa infections. Expert Rev Anti Infect Ther 2012; 10:219–235 [View Article][PubMed]
    [Google Scholar]
  126. Rzhepishevska O, Ekstrand-Hammarström B, Popp M, Björn E, Bucht A et al. The antibacterial activity of Ga3+ is influenced by ligand complexation as well as the bacterial carbon source. Antimicrob Agents Chemother 2011; 55:5568–5580 [View Article][PubMed]
    [Google Scholar]
  127. Banin E, Lozinski A, Brady KM, Berenshtein E, Butterfield PW et al. The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc Natl Acad Sci U S A 2008; 105:16761–16766 [View Article][PubMed]
    [Google Scholar]
  128. Secor PR, Michaels LA, Ratjen A, Jennings LK, Singh PK. Entropically driven aggregation of bacteria by host polymers promotes antibiotic tolerance in Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 2018; 115:10780–10785 [View Article][PubMed]
    [Google Scholar]
  129. Reichhardt C, Jacobs HM, Matwichuk M, Wong C, Wozniak DJ et al. The versatile Pseudomonas aeruginosa biofilm matrix protein CdrA promotes aggregation through different extracellular exopolysaccharide interactions. J Bacteriol 2020; 202:e00216–00220 [View Article][PubMed]
    [Google Scholar]
  130. Alhede M, Kragh KN, Qvortrup K, Allesen-Holm M, van Gennip M. Phenotypes of non-attached Pseudomonas aeruginosa aggregates resemble surface attached biofilm. PLoS One 2011; 6:e27943
    [Google Scholar]
  131. Martin I, Waters V, Grasemann H. Approaches to targeting bacterial biofilms in cystic fibrosis airways. Int J Mol Sci 2021; 22:2155 [View Article][PubMed]
    [Google Scholar]
  132. Baldoni D, Steinhuber A, Zimmerli W, Trampuz A. In vitro activity of gallium maltolate against staphylococci in logarithmic, stationary, and biofilm growth phases: comparison of conventional and calorimetric susceptibility testing methods. Antimicrob Agents Chemother 2010; 54:157–163 [View Article][PubMed]
    [Google Scholar]
  133. Martens RJ, Mealey K, Cohen ND, Harrington JR, Chaffin MK et al. Pharmacokinetics of gallium maltolate after intragastric administration in neonatal foals. Am J Vet Res 2007; 68:1041–1044 [View Article][PubMed]
    [Google Scholar]
  134. Martens RJ, Miller NA, Cohen ND, Harrington JR, Bernstein LR. Chemoprophylactic antimicrobial activity of gallium maltolate against intracellular Rhodococcus equi . J Equine Vet Sci 2007; 27:341–345 [View Article]
    [Google Scholar]
  135. Nerren JR, Edrington TS, Bernstein LR, Farrow RL, Genovese KG. Evaluation of the effect of gallium maltolate on fecal Salmonella shedding in cattle. Journal of Food Protection 2011; 74:524–530
    [Google Scholar]
  136. Fecteau M-E, Aceto HW, Bernstein LR, Sweeney RW. Comparison of the antimicrobial activities of gallium nitrate and gallium maltolate against Mycobacterium avium subsp. paratuberculosis in vitro . Vet J 2014; 202:195–197 [View Article][PubMed]
    [Google Scholar]
  137. Arnold CE, Bordin A, Lawhon SD, Libal MC, Bernstein LR et al. Antimicrobial activity of gallium maltolate against Staphylococcus aureus and methicillin-resistant S. aureus and Staphylococcus pseudintermedius: an in vitro study. Vet Microbiol 2012; 155:389–394 [View Article][PubMed]
    [Google Scholar]
  138. Bernstein LR. Mechanisms of therapeutic activity for gallium. Pharmacol Rev 1998; 50:665–682[PubMed]
    [Google Scholar]
  139. Hopkins A. Determination that GANITE (Gallium nitrate) injectable and five other drug products were not withdrawn from sale for reasons of safety or effectiveness. office of the federal register, National Archives and records administration; 20149225
  140. Giacani L, Bernstein LR, Haynes AM, Godornes BC, Ciccarese G et al. Topical treatment with gallium maltolate reduces Treponema pallidum subsp. pertenue burden in primary experimental lesions in a rabbit model of yaws. PLoS Negl Trop Dis 2019; 13:e0007076 [View Article][PubMed]
    [Google Scholar]
  141. Bernstein LR, Tanner T, Godfrey C, Noll B. Chemistry and pharmacokinetics of gallium maltolate, a compound with high oral gallium bioavailability. Met Based Drugs 2000; 7:33–47 [View Article][PubMed]
    [Google Scholar]
  142. Bernstein LR. 31Ga Therapeutic Gallium Compounds. In Gielen M, Tiekink ERT. (editors) Metallotherapeutic Drugs and Metal‐Based Diagnostic Agents 2005 pp 259–277
    [Google Scholar]
  143. Bernstein L. Gallium, therapeutic effects. Encyclopedia of metalloproteins 2013823–835
    [Google Scholar]
  144. Borkow G, Copper GJ. An ancient remedy returning to fight microbial, fungal and viral infections. Curr Chem Biol 2009; 3:272–278
    [Google Scholar]
  145. Arendsen LP, Thakar R, Sultan AH. The use of copper as an antimicrobial agent in health care, including obstetrics and gynecology. Clin Microbiol Rev 2019; 32:e00125–00118 [View Article][PubMed]
    [Google Scholar]
  146. Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M et al. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 2013; 87:1181–1200 [View Article][PubMed]
    [Google Scholar]
  147. Forman TE. Synergistic Relationship Between Copper and Ribosome-Targeting Antibiotics in Close Relatives of B. subtilis ssp. spizizenii Wesleyan University; 2019
    [Google Scholar]
  148. Huh AJ, Kwon YJ. "Nanoantibiotics": a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Control Release 2011; 156:128–145 [View Article][PubMed]
    [Google Scholar]
  149. Drewry JA, Gunning PT. Recent advances in biosensory and medicinal therapeutic applications of zinc(II) and copper(II) coordination complexes. Coord Chem Rev 2011; 255:459–472 [View Article]
    [Google Scholar]
  150. Sorenson JRJ. 6 copper complexes offer a physiological approach to treatment of chronic diseases. In Ellis GP, West GB. (editors) Progress in Medicinal Chemistry: Elsevier; 1989 pp 437–568
  151. Mello Filho AC, Hoffmann ME, Meneghini R. Cell killing and DNA damage by hydrogen peroxide are mediated by intracellular iron. Biochem J 1984; 218:273–275
    [Google Scholar]
  152. Imlay J, Chin S, Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro . Science 1988; 240:640–642
    [Google Scholar]
  153. Thurman RB, Gerba CP, Bitton G. The molecular mechanisms of copper and silver ion disinfection of bacteria and viruses. Crit Rev Environ Sci 1989; 18:295–315
    [Google Scholar]
  154. Macomber L, Imlay JA. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci U S A 2009; 106:8344–8349 [View Article][PubMed]
    [Google Scholar]
  155. Fein JB, Yu Q, Nam J, Yee N. Bacterial cell envelope and extracellular sulfhydryl binding sites: their roles in metal binding and bioavailability. Chemical Geology 2019; 521:28–38
    [Google Scholar]
  156. Pokrovsky OS, Pokrovski GS, Shirokova LS, Gonzalez AG, Emnova EE. Chemical and structural status of copper associated with oxygenic and anoxygenic phototrophs and heterotrophs: possible evolutionary consequences. Geobiology 2012; 10:130–149
    [Google Scholar]
  157. Chandraleka S, Ramya K, Chandramohan G, Dhanasekaran D, Priyadharshini A et al. Antimicrobial mechanism of copper (II) 1,10-phenanthroline and 2,2′-bipyridyl complex on bacterial and fungal pathogens. J Saudi Chem Soc 2014; 18:953–962 [View Article]
    [Google Scholar]
  158. Mohindru A, Fisher JM, Rabinovitz M. 2,9-Dimethyl-1,10-phenanthroline (neocuproine): a potent, copper-dependent cytotoxin with anti-tumor activity. Biochem Pharmacol 1983; 32:3627–3632 [View Article][PubMed]
    [Google Scholar]
  159. Ainscough EW, Brodie AM, Denny WA, Finlay GJ, Ranford JD. Nitrogen, sulfur and oxygen donor adducts with copper(II) complexes of antitumor 2-formylpyridinethiosemicarbazone analogs: physicochemical and cytotoxic studies. J Inorg Biochem 1998; 70:175–185 [View Article][PubMed]
    [Google Scholar]
  160. Sorenson JR. Copper chelates as possible active forms of the antiarthritic agents. J Med Chem 1976; 19:135–148 [View Article][PubMed]
    [Google Scholar]
  161. Ruiz-Ramírez L, de la Rosa ME, Gracia-Mora I, Mendoza A, Pérez G et al. Casiopeinas, metal-based drugs a new class of antineoplastic and genotoxic compounds. J Inorg Biochem 1995; 59:207 [View Article]
    [Google Scholar]
  162. Brown DH, Smith WE, Teape JW, Lewis AJ. Antiinflammatory effects of some copper complexes. J Med Chem 1980; 23:729–734 [View Article][PubMed]
    [Google Scholar]
  163. Ude Z, Kavanagh K, Twamley B, Pour M, Gathergood N. A new class of prophylactic metallo-antibiotic possessing potent anti-cancer and anti-microbial properties. Dalton Transactions 2019; 48:
    [Google Scholar]
  164. Uivarosi V. Metal complexes of quinolone antibiotics and their applications: an update. Molecules 2013; 18:11153–11197
    [Google Scholar]
  165. Tuma J, Connors WH, Stitelman DH, Richert C. On the effect of covalently appended quinolones on termini of DNA duplexes. J Am Chem Soc 2002; 124:4236–4246 [View Article][PubMed]
    [Google Scholar]
  166. Kathiravan MK, Khilare MM, Nikoomanesh K, Chothe AS, Jain KS. Topoisomerase as target for antibacterial and anticancer drug discovery. J Enzyme Inhib Med Chem 2013; 28:419–435 [View Article][PubMed]
    [Google Scholar]
  167. Kumar M, Mogha NK, Kumar G, Hussain F, Masram DT. Biological evaluation of copper(II) complex with nalidixic acid and 2,2′-bipyridine (bpy). Inorganica Chimica Acta 2019; 490:144–154
    [Google Scholar]
  168. Debnath A, Mogha NK, Masram DT. Metal complex of the first-generation quinolone antimicrobial drug nalidixic acid: structure and its biological evaluation. Appl Biochem Biotechnol 2015; 175:2659–2667 [View Article][PubMed]
    [Google Scholar]
  169. Tweedy BG. Plant extracts with metal ions as potential antimicrobial agents. Pathophysiology 1964; 55:910–918
    [Google Scholar]
  170. Levinson W, Jawetz E. Medical Microbiology and Immunology: Examination and Board Review Appleton & Lange; 1996
    [Google Scholar]
  171. Crisponi G, Nurchi VM, Fanni D, Gerosa C, Nemolato S et al. Copper-related diseases: from chemistry to molecular pathology. Coord Chem Rev 2010; 254:876–889 [View Article]
    [Google Scholar]
  172. Dimiza F, Fountoulaki S, Papadopoulos AN, Kontogiorgis CA, Tangoulis V. Non-steroidal antiinflammatory drug–copper(ii) complexes: Structure and biological perspectives. Dalton Transactions 2011; 40:8555–8568
    [Google Scholar]
  173. Pohanka M. Copper and copper nanoparticles toxicity and their impact on basic functions in the body. Bratisl Lek Listy 2019; 120:397–409
    [Google Scholar]
  174. Gaetke LM, Chow CK. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 2003; 189:147–163
    [Google Scholar]
  175. Braymer JJ, Giedroc DP. Recent developments in copper and zinc homeostasis in bacterial pathogens. Curr Opin Chem Biol 2014; 19:59–66 [View Article][PubMed]
    [Google Scholar]
  176. Neyrolles O, Wolschendorf F, Mitra A, Niederweis M. Mycobacteria, metals, and the macrophage. Immunol Rev 2015; 264:249–263 [View Article][PubMed]
    [Google Scholar]
  177. McCarron P, McCann M, Devereux M, Kavanagh K, Skerry C et al. Unprecedented in vitro antitubercular activitiy of manganese(II) complexes containing 1,10-phenanthroline and dicarboxylate ligands: increased activity, superior selectivity, and lower toxicity in comparison to their copper(II) analogs. Front Microbiol 2018; 9:1432 [View Article][PubMed]
    [Google Scholar]
  178. Simpson PV, Nagel C, Bruhn H, Schatzschneider U. Antibacterial and antiparasitic activity of manganese(I) tricarbonyl complexes with ketoconazole, miconazole, and clotrimazole ligands. Organometallics 2015; 34:3809–3815
    [Google Scholar]
  179. Paul P, Bhowmik KRN, Roy S, Deb D, Das N. Synthesis, structural features, antibacterial behaviour and theoretical investigation of two new manganese(III) Schiff base complexes. Polyhedron 2018; 151:407–416
    [Google Scholar]
  180. Rani N, Sharma A, Singh R, Nidhi R, Ajay S. Imidazoles as promising scaffolds for antibacterial activity: a review. Mini Rev Med Chem 2013; 13:1812–1835 [View Article][PubMed]
    [Google Scholar]
  181. Glans L, Hu W, Jöst C, de Kock C, Smith PJ et al. Synthesis and biological activity of cymantrene and cyrhetrene 4-aminoquinoline conjugates against malaria, leishmaniasis, and trypanosomiasis. Dalton Trans 2012; 41:6443–6450 [View Article][PubMed]
    [Google Scholar]
  182. Simpson PV, Schmidt C, Ott I, Bruhn H, Schatzschneider U. Synthesis, cellular uptake and biological activity against pathogenic microorganisms and cancer cells of rhodium and iridium N-heterocyclic carbene complexes bearing charged substituents. Eur J Inorg Chem 2013; 2013:5547–5554 [View Article]
    [Google Scholar]
  183. Ross AC, Caballero BH, Cousins RJ, Tucker KL, Ziegler TR. Modern Nutrition in Health and Disease Wolters Kluwer Health Adis (ESP); 2012
    [Google Scholar]
  184. Erdman JW, MacDonald IA, Zeisel SH. Manganese, Molybdenum, Boron, Chromium, and Other Trace Elements Present Knowledge in Nutrition: Wiley-Blackwell; 2012 pp 586–607
    [Google Scholar]
  185. Institute of Medicine (US) Panel on Micronutrients Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc Washington, DC: The National Academies Press; 2001
    [Google Scholar]
  186. Li L, Yang X. The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxid Med Cell Longev 2018; 2018:7580707
    [Google Scholar]
  187. Chen P, Bornhorst J, Aschner M. Manganese metabolism in humans. Front Biosci 2018; 23:1655–1679
    [Google Scholar]
  188. Palacios C. The role of nutrients in bone health, from A to Z. Crit Rev Food Sci Nutr 2006; 46:621–628
    [Google Scholar]
  189. Aschner JL, Aschner M. Nutritional aspects of manganese homeostasis. Mol Aspects Med 2005; 26:353–362
    [Google Scholar]
  190. Dwyer FP, Gyarfas EC, Rogers WP, Koch JH. Biological activity of complex ions. Nature 1952; 170:190–191
    [Google Scholar]
  191. Wang Y, Hu L, Xu F, Quan Q, Lai Y-T et al. Integrative approach for the analysis of the proteome-wide response to bismuth drugs in Helicobacter pylori . Chem Sci 2017; 8:4626–4633 [View Article][PubMed]
    [Google Scholar]
  192. Chen F, Moat J, McFeely D, Clarkson G, Hands-Portman IJ et al. Biguanide iridium(III) complexes with potent antimicrobial activity. J Med Chem 2018; 61:7330–7344 [View Article][PubMed]
    [Google Scholar]
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