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Cited by 30Bacterial Genetics and BiotechnologyIron Metabolism and DisordersEscherichia coli research studies

Iron Acquisition by Bacterial Pathogens: Beyond Tris‐Catecholate Complexes

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Zhang, Yifan, Sen, Sambuddha, Giedroc, David P.·2020·ChemBioChem
DOI 10.1002/cbic.201900778PMC PMC7367709
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Abstract

Sequestration of the essential nutrient iron from bacterial invaders that colonize the vertebrate host is a central feature of nutritional immunity and the “fight over transition metals” at the host‐pathogen interface. The iron quota for many bacterial pathogens is large, as iron enzymes often make up a significant share of the metalloproteome. Iron enzymes play critical roles in respiration, energy metabolism, and other cellular processes by catalyzing a wide range of oxidation‐reduction, electron transfer, and oxygen activation reactions. In this Concept article, we discuss recent insights into the diverse ways that bacterial pathogens acquire this essential nutrient, beyond the well‐characterized tris‐catecholate Fe III complexes, in competition and cooperation with significant host efforts to cripple these processes. We also discuss pathogen strategies to adapt their metabolism to less‐than‐optimal iron concentrations, and briefly speculate on what might be an integrated adaptive response to the concurrent limitation of both iron and zinc in the infected host.

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  • Iron is redox active and very poorly soluble in the oxidized Fe3+ form, which has led to the evolution of high affinity iron-binding siderophores synthesized by many bacteria and fungi.

    “Iron is redox active, and very poorly soluble in the oxidized Fe3+ (ferric) form, which has led to the evolution of high affinity iron-binding compounds (siderophores) synthesized by many bacteria and fungi.18,19”

    From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [19]

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  1. [1]Andreini C, Putignano V, Rosato A, Banci L, Metallomics 2018, 10, 1223– 1231. 30095136
  2. [2]Cvetkovic A, Menon AL, Thorgersen MP, Scott JW, Poole FL 2nd, Jenney FE Jr., Lancaster WA, Praissman JL, Shanmukh S, Vaccaro BJ, Trauger SA, Kalisiak E, Apon JV, Siuzdak G, Yannone SM, Tainer JA, Adams MW, Nature 2010, 466, 779– 782. 20639861
  3. [3]Waldron KJ, Rutherford JC, Ford D, and Robinson NJ, Nature 2009, 460, 823– 830. 19675642
  4. [4]a) Andreini C, Banci L, Bertini I, Rosato A, J Proteome Res 2006, 5, 3173– 3178; 17081069 b) Wang J, Lonergan ZR, Gonzalez-Gutierrez G, Nairn BL, Maxwell CN, Zhang Y, Andreini C, Karty JA, Chazin WJ, Trinidad JC, Skaar EP, Giedroc DP, Cell Chem Biol 2019, 26, 745– 755. 30905682 PMC6525019
  5. [5]Weinberg ED, JAMA 1975, 231, 39– 41. 1243565
  6. [6]a) Pi H, Helmann JD, Proc Natl Acad Sci U S A 2017, 114, 12785– 12790; 29133393 PMC5715773 b) Masse E, Gottesman S, Proc Natl Acad Sci U S A 2002, 99, 4620– 4625. 11917098 PMC123697
  7. [7]Reinhart AA, Nguyen AT, Brewer LK, Bevere J, Jones JW, Kane MA, Damron FH, Barbier M, Oglesby-Sherrouse AG, Infect Immun 2017, 85, e00764– 16 28289146 PMC5400841
  8. [8]Osman D, Martini MA, Foster AW, Chen J, Scott AJP, Morton RJ, Steed JW, Lurie-Luke E, Huggins TG, Lawrence AD, Deery E, Warren MJ, Chivers PT, Robinson NJ, Nat Chem Biol 2019, 15, 241– 249. 30692683 PMC6420079
  9. [9]Guan G, Pinochet-Barros A, Gaballa A, Patel SJ, Arguello JM, Helmann JD, Mol Microbiol 2015, 98, 787– 803. 26261021 PMC4648274
  10. [10]a) Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D, Arch Microbiol 2005, 183, 9– 18; 15549269 b) Sankari S, O’Brian MR, J Biol Chem 2014, 289, 16498– 16507; 24782310 PMC4047416 c) Pi H, Helmann JD, Metallomics 2017, 9, 840– 851. 28604884 PMC5675029
  11. [11]Lee JW, Helmann JD, Biometals 2007, 20, 485– 499. 17216355
  12. [12]Giel JL, Nesbit AD, Mettert EL, Fleischhacker AS, Wanta BT, Kiley PJ, Mol Microbiol 2013, 87, 478– 492. 23075318 PMC4108476
  13. [13]Verstraete MM, Morales LD, Kobylarz MJ, Loutet SA, Laakso HA, Pinter TB, Stillman MJ, Heinrichs DE, Murphy MEP, J Biol Chem 2019, 294, 11622– 11636. 31197035 PMC6663872
  14. [14]a) VanderWal AR, Makthal N, Pinochet-Barros A, Helmann JD, Olsen RJ, Kumaraswami M, Infect Immun 2017, 85; PMC5442632 28348051 b) Brenot A, Weston BF, Caparon MG, Mol Microbiol 2007, 63, 1185– 1196. 17238923
  15. [15]a) Turner AG, Djoko KY, Ong CY, Barnett TC, Walker MJ, McEwan AG, Biochem J 2019, 476, 595– 611; 30670571 b) Helmann JD, J Biol Chem 2014, 289, 28112– 28120. 25160631 PMC4192466
  16. [16]a) Sobota JM, Imlay JA, Proc Natl Acad Sci U S A 2011, 108, 5402– 5407; 21402925 PMC3069151 b) Anjem A, Imlay JA, J Biol Chem 2012, 287, 15544– 15556. 22411989 PMC3346116
  17. [17]a) Johnstone TC, Nolan EM, J Am Chem Soc 2017, 139, 15245– 15250; 28956921 PMC5748154 b) Raymond KN, Dertz EA, Kim SS, Proc Natl Acad Sci U S A 2003, 100, 3584– 3588. 12655062 PMC152965
  18. [18]Hider RC, Kong X, Nat Prod Rep 2010, 27, 637– 657. 20376388
  19. [19]Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K, Tsuji Y, Trends Mol Med 2016, 22, 1077– 1090. 27825668 PMC5135587
  20. [20]Martin RB, Savory J, Brown S, Bertholf RL, Wills MR, Clin Chem 1987, 33, 405– 407. 3815806
  21. [21]Gomez-Bombarelli R, Calle E, Casado J, J Org Chem 2013, 78, 6868– 6879. 23758295
  22. [22]a) Lavrrar JL, Christoffersen CA, McIntosh MA, J Mol Biol 2002, 322, 983– 995; 12367523 b) Brickman TJ, Ozenberger BA, McIntosh MA, J Mol Biol 1990, 212, 669– 682; 2139473 c) Hunt MD, Pettis GS, McIntosh MA, J Bacteriol 1994, 176, 3944– 3955. 8021177 PMC205592
  23. [23]a) Schalk IJ, Mislin GL, Brillet K, Curr Top Membr 2012, 69, 37– 66; 23046646 b) Celia H, Noinaj N, Zakharov SD, Bordignon E, Botos I, Santamaria M, Barnard TJ, Cramer WA, Lloubes R, Buchanan SK, Nature 2016, 538, 60– 65; 27654919 PMC5161667 c) Buchanan SK, Smith BS, Venkatramani L, Xia D, Esser L, Palnitkar M, Chakraborty R, van der Helm D, Deisenhofer J, Nat Struct Biol 1999, 6, 56– 63. 9886293
  24. [24]a) Zhu M, Valdebenito M, Winkelmann G, Hantke K, Microbiology 2005, 151, 2363– 2372; 16000726 b) Neumann W, Sassone-Corsi M, Raffatellu M, Nolan EM, J Am Chem Soc 2018, 140, 5193– 5201. 29578687 PMC5921047
  25. [25]a) Subashchandrabose S, Smith S, DeOrnellas V, Crepin S, Kole M, Zahdeh C, Mobley HL, mSphere 2016, 1; PMC4863628 27303682 b) Cornelis P, Dingemans J, Front Cell Infect Microbiol 2013, 3, 75. 24294593 PMC3827675
  26. [26]a) Moynie L, Milenkovic S, Mislin GLA, Gasser V, Malloci G, Baco E, McCaughan RP, Page MGP, Schalk IJ, Ceccarelli M, Naismith JH, Nat Commun 2019, 10, 3673; 31413254 PMC6694100 b) Zarate-Bonilla LJ, Del Portillo P, Saenz-Suarez H, Gonzales-Santos J, Barreto-Sampaio GE, Poutou-Pinales RA, Rey AF, Rey JG, Poult Sci 2014, 93, 221– 230; 24570443 c) Smallwood CR, Jordan L, Trinh V, Schuerch DW, Gala A, Hanson M, Shipelskiy Y, Majumdar A, Newton SM, Klebba PE, J Gen Physiol 2014, 144, 71– 80. 24981231 PMC4076525
  27. [27]a) Braun V, Hantke K, Koster W, Met Ions Biol Syst 1998, 35, 67– 145; 9444760 b) Hantke K, FEMS Microbiol Lett 1990, 55, 5– 8. 2139424
  28. [28]Grinter R, Lithgow T, J Biol Chem 2019, 294, 19523– 19534. 31712312 PMC6926462
  29. [29]Delepelaire P, Res Microbiol 2019, 170, 345– 355. 31678562
  30. [30]Cooper JD, Hannauer M, Marolda CL, Briere LA, Heinrichs DE, Biochemistry 2014, 53, 5060– 5069. 25050909
  31. [31]a) Grigg JC, Cheung J, Heinrichs DE, Murphy ME, J Biol Chem 2010, 285, 34579– 34588; 20810662 PMC2966073 b) Beasley FC, Marolda CL, Cheung J, Buac S, Heinrichs DE, Infect Immun 2011, 79, 2345– 2355; 21402762 PMC3125851 c) Madsen JL, Johnstone TC, Nolan EM, J Am Chem Soc 2015, 137, 9117– 9127. 26030732
  32. [32]Grigg JC, Cooper JD, Cheung J, Heinrichs DE, Murphy ME, J Biol Chem 2010, 285, 11162– 11171. 20147287 PMC2856993
  33. [33]de Boer M, Gouridis G, Vietrov R, Begg SL, Schuurman-Wolters GK, Husada F, Eleftheriadis N, Poolman B, McDevitt CA, Cordes T, Elife 2019, 8. PMC6450668 30900991
  34. [34]Stephens DL, Choe MD, Earhart CF, Microbiology 1995, 141, 1647– 1654. 7551033
  35. [35]Sprencel C, Cao Z, Qi Z, Scott DC, Montague MA, Ivanoff N, Xu J, Raymond KM, Newton SM, Klebba PE, J Bacteriol 2000, 182, 5359– 5364. 10986237 PMC110977
  36. [36]Mademidis A, Koster W, Mol Gen Genet 1998, 258, 156– 165. 9613584
  37. [37]Moynie L, Serra I, Scorciapino MA, Oueis E, Page MG, Ceccarelli M, Naismith JH, Elife 2018, 7, e42270. 30558715 PMC6300358
  38. [38]Bailey DC, Bohac TJ, Shapiro JA, Giblin DE, Wencewicz TA, Gulick AM, Biochemistry 2018, 57, 6653– 6661. 30406986 PMC6474793
  39. [39]Lin H, Fischbach MA, Liu DR, Walsh CT, J Am Chem Soc 2005, 127, 11075– 11084. 16076215 PMC2536649
  40. [40]Kobylarz MJ, Heieis GA, Loutet SA, Murphy MEP, ACS Chem Biol 2017, 12, 1778– 1786. 28463500
  41. [41]Miethke M, Hou J, Marahiel MA, Biochemistry 2011, 50, 10951– 10964. 22098718
  42. [42]Wang S, Wu Y, Outten FW, J Bacteriol 2011, 193, 563– 574. 21097627 PMC3019823
  43. [43]Matzanke BF, Anemuller S, Schunemann V, Trautwein AX, Hantke K, Biochemistry 2004, 43, 1386– 1392. 14756576
  44. [44]Hartmann A, Braun V, J Bacteriol 1980, 143, 246– 255. 6995431 PMC294220
  45. [45]Meyer JM, Hohnadel D, Halle F, J Gen Microbiol 1989, 135, 1479– 1487. 2533244
  46. [46]Noinaj N, Easley NC, Oke M, Mizuno N, Gumbart J, Boura E, Steere AN, Zak O, Aisen P, Tajkhorshid E, Evans RW, Gorringe AR, Mason AB, Steven AC, Buchanan SK, Nature 2012, 483, 53– 58. 22327295 PMC3292680
  47. [47]a) Field LH, Headley VL, Payne SM, Berry LJ, Infect Immun 1986, 54, 126– 132; 2944843 PMC260126 b) Naikare H, Butcher J, Flint A, Xu J, Raymond KN, Stintzi A, Metallomics 2013, 5, 988– 996. 23702883 PMC3754778
  48. [48]Cheng W, Li Q, Jiang YL, Zhou CZ, Chen Y, PLoS One 2013, 8, e71451. 23951167 PMC3741162
  49. [49]a) Knosp O, von Tigerstrom M, Page WJ, J Bacteriol 1984, 159, 341– 347; 6429124 PMC215635 b) Palanche T, Blanc S, Hennard C, Abdallah MA, Albrecht-Gary AM, Inorg Chem 2004, 43, 1137– 1152. 14753838
  50. [50]Brandel J, Humbert N, Elhabiri M, Schalk IJ, Mislin GL, Albrecht-Gary AM, Dalton Trans 2012, 41, 2820– 2834. 22261733
  51. [51]a) Balado M, Souto A, Vences A, Careaga VP, Valderrama K, Segade Y, Rodriguez J, Osorio CR, Jimenez C, Lemos ML, ACS chemical biology 2015, 10, 2850– 2860; 26463084 b) Barghouthi S, Young R, Olson MO, Arceneaux JE, Clem LW, Byers BR, J Bacteriol 1989, 171, 1811– 1816. 2522922 PMC209826
  52. [52]Perry WJ, Spraggins JM, Sheldon JR, Grunenwald CM, Heinrichs DE, Cassat JE, Skaar EP, Caprioli RM, Proc Natl Acad Sci U S A 2019, 116, 21980– 21982. 31611408 PMC6825271
  53. [53]a) Wyckoff EE, Allred BE, Raymond KN, Payne SM, J Bacteriol 2015, 197, 2840– 2849; 26100039 PMC4524036 b) Wilkins TD, Lankford CE, J Infect Dis 1970, 121, 129– 136; 4905647 c) Wang CC, Newton A, J Bacteriol 1969, 98, 1142– 1150; 4892368 PMC315307 d) Rabsch W, Methner U, Voigt W, Tschape H, Reissbrodt R, Williams PH, Infect Immun 2003, 71, 6953– 6961; 14638784 PMC308886 e) Hancock RE, Hantke K, Braun V, Arch Microbiol 1977, 114, 231– 239; 143918 f) Berner I, Greiner M, Metzger J, Jung G, Winkelmann G, Biol Met 1991, 4, 113– 118. 1831634
  54. [54]Freestone PPE, Sandrini SM, Haigh RD, Lyte M, Trends Microbiol 2008, 16, 55– 64. 18191570
  55. [55]a) Eisenhofer G, Kopin IJ, Goldstein DS, Pharmacol Rev 2004, 56, 331– 349; 15317907 b) Esler M, Jennings G, Korner P, Blombery P, Sacharias N, Leonard P, Am J Physiol 1984, 247, E21– 28. 6742187
  56. [56]a) Zeng X, Xu F, Lin J, Infect Immun 2009, 77, 5437– 5448; 19737895 PMC2786435 b) Xu F, Zeng X, Haigh RD, Ketley JM, Lin J, J Bacteriol 2010, 192, 4425– 4435; 20585060 PMC2937379 c) Raines DJ, Moroz OV, Blagova EV, Turkenburg JP, Wilson KS, Duhme-Klair AK, Proc Natl Acad Sci U S A 2016, 113, 5850– 5855. 27162326 PMC4889360
  57. [57]a) Neal CP, Freestone PP, Maggs AF, Haigh RD, Williams PH, Lyte M, FEMS Microbiol Lett 2001, 194, 163– 169; 11164302 b) Gonzales XF, Castillo-Rojas G, Castillo-Rodal AI, Tuomanen E, Lopez-Vidal Y, Microbiology 2013, 159, 2333– 2341; 23963302 c) Graziano TS, Closs P, Poppi T, Franco GC, Cortelli JR, Groppo FC, Cogo K, J Periodontal Res 2014, 49, 660– 669; 24251763 d) O’Donnell PM, Aviles H, Lyte M, Sonnenfeld G, Appl Environ Microbiol 2006, 72, 5097– 5099. 16820514 PMC1489335
  58. [58]Barber MF, Elde NC, Science 2014, 346, 1362– 1366. 25504720 PMC4455941
  59. [59]Sandrini SM, Shergill R, Woodward J, Muralikuttan R, Haigh RD, Lyte M, Freestone PP, J Bacteriol 2010, 192, 587– 594. 19820086 PMC2805316
  60. [60]Jewett SL, Eggling S, Geller L, J Inorg Biochem 1997, 66, 165– 173.
  61. [62]Zeng X, Xu F, Lin J, FEMS Microbiol Lett 2013, 347, 83– 91. 23905838 PMC3774156
  62. [63]Zeng X, Mo Y, Xu F, Lin J, Mol Microbiol 2013, 87, 594– 608. 23278903 PMC3556234
  63. [64]Palyada K, Threadgill D, Stintzi A, J Bacteriol 2004, 186, 4714– 4729. 15231804 PMC438614
  64. [65]Wilde EJ, Hughes A, Blagova EV, Moroz OV, Thomas RP, Turkenburg JP, Raines DJ, Duhme-Klair AK, Wilson KS, Sci Rep 2017, 7, 45941. 28383577 PMC5382913
  65. [66]Wilde EJ, Blagova EV, Sanderson TJ, Raines DJ, Thomas RP, Routledge A, Duhme-Klair AK, Wilson KS, J Inorg Biochem 2019, 190, 75– 84. 30384009
  66. [67]Aron AT, Heffern MC, Lonergan ZR, Vander Wal MN, Blank BR, Spangler B, Zhang Y, Park HM, Stahl A, Renslo AR, Skaar EP, Chang CJ, Proc Natl Acad Sci U S A 2017, 114, 12669– 12674. 29138321 PMC5715752
  67. [68]a) Hunter RC, Asfour F, Dingemans J, Osuna BL, Samad T, Malfroot A, Cornelis P, Newman DK, mBio 2013, 4, e00557– 13; PMC3753050 23963183 b) Blank BR, Talukder P, Muir RK, Green ER, Skaar EP, Renslo AR, ACS Infect Dis 2019, 5, 1366– 1375. 31140267 PMC6880962
  68. [69]Cox CD, Infection and immunity 1986, 52, 263– 270. 2937736 PMC262229
  69. [70]a) Peng ED, Payne SM, J Bacteriol 2017, 199, e00874– 16; 28348025 PMC5446626 b) Small SK, O’Brian MR, J Bacteriol 2011, 193, 4088– 4094. 21705608 PMC3147698
  70. [71]Deneer HG, Healey V, Boychuk I, Microbiology 1995, 141, 1985– 1992. 7551061
  71. [72]Abeyrathna SS, Abeyrathna NS, Thai NK, Sarkar P, D’Arcy S, Meloni G, Biochemistry 2019, 58, 4337– 4342. 31589416 PMC7231427
  72. [73]Lau CK, Krewulak KD, Vogel HJ, FEMS Microbiol Rev 2016, 40, 273– 298. 26684538
  73. [74]Sestok AE, Linkous RO, Smith AT, Metallomics 2018, 10, 887– 898. 29953152 PMC6051883
  74. [75]Smith AT, Linkous RO, Max NJ, Sestok AE, Szalai VA, Chacon KN, Biochemistry 2019, 58, 4935– 4949. 31713418 PMC6904521
  75. [76]Hantke K, FEMS <icrobiol Lett 1987, 44, 53– 57.
  76. [77]Wyckoff EE, Mey AR, Leimbach A, Fisher CF, Payne SM, J Bacteriiol 2006, 188, 6515– 6523. PMC1595488 16952942
  77. [78]a) Dashper SG, Butler CA, Lissel JP, Paolini RA, Hoffmann B, Veith PD, O’Brien-Simpson NM, Snelgrove SL, Tsiros JT, Reynolds EC, J Biol Chem 2005, 280, 28095– 28102; 15901729 b) Awad MM, Cheung JK, Tan JE, McEwan AG, Lyras D, Rood JI, Anaerobe 2016, 41, 10– 17. 27178230
  78. [79]a) Naikare H, Palyada K, Panciera R, Marlow D, Stintzi A, Infect Immun 2006, 74, 5433– 5444; 16988218 PMC1594910 b) Velayudhan J, Hughes NJ, McColm AA, Bagshaw J, Clayton CL, Andrews SC, Kelly DJ, Mol Microbiol 2000, 37, 274– 286. 10931324
  79. [80]Nagy TA, Moreland SM, Detweiler CS, Mol Microbiol 2014, 93, 1314– 1326. 25081030 PMC4160465
  80. [81]a) Perry RD, Mier I Jr., Fetherston JD, Biometals 2007, 20, 699– 703; 17206386 b) Perez N, Johnson R, Sen B, Ramakrishnan G, MicrobiologyOpen 2016, 5, 453– 468. 26918301 PMC4905997
  81. [82]a) Weaver EA, Wyckoff EE, Mey AR, Morrison R, Payne SM, J Bacteriol 2013, 195, 4826– 4835; 23955009 PMC3807486 b) Kim H, Lee H, Shin D, Biochem Biophys Res Commun 2012, 423, 733– 738; 22705302 c) Alvarez-Fraga L, Vazquez-Ucha JC, Martinez-Guitian M, Vallejo JA, Bou G, Beceiro A, Poza M, Virulence 2018, 9, 496– 509. 29334313 PMC5955439
  82. [83]Dauner M, Skerra A, Chembiochem 2019, in the press.
  83. [84]a) Sia AK, Allred BE, Raymond KN, Curr Opin Chem Biol 2013, 17, 150– 157; 23265976 PMC3634885 b) Huang X, Slavkovic S, Song E, Botta A, Mehrazma B, Lento C, Johnson PE, Sweeney G, Wilson DJ, ACS Chem Biol 2019, in the press. 31613081
  84. [85]Moura-Alves P, Puyskens A, Stinn A, Klemm M, Guhlich-Bornhof U, Dorhoi A, Furkert J, Kreuchwig A, Protze J, Lozza L, Pei G, Saikali P, Perdomo C, Mollenkopf HJ, Hurwitz R, Kirschhoefer F, Brenner-Weiss G, Weiner J 3rd, Oschkinat H, Kolbe M, Krause G, Kaufmann SHE, Science 2019, 366. 31857448
  85. [86]a) Corbin BD, Seeley EH, Raab A, Feldmann J, Miller MR, Torres VJ, Anderson KL, Dattilo BM, Dunman PM, Gerads R, Caprioli RM, Nacken W, Chazin WJ, Skaar EP, Science 2008, 319, 962– 965; 18276893 b) Clohessy PA, Golden BE, Scand J Immunol 1995, 42, 551– 556. 7481561
  86. [87]Nakashige TG, Zhang B, Krebs C, Nolan EM, Nat Chem Biol 2015, 11, 765– 771. 26302479 PMC4575267
  87. [88]Zygiel EM, Nelson CE, Brewer LK, Oglesby-Sherrouse AG, Nolan EM, J Biol Chem 2019, 294, 3549– 3562. 30622135 PMC6416435
  88. [89]Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, Zhang Y, Betz C, Hench L, Fritz G, Skaar EP, Chazin WJ, Proc Natl Acad Sci U S A 2013, 110, 3841– 3846. 23431180 PMC3593839
  89. [90]a) Brophy MB, Hayden JA, Nolan EM, J Am Chem Soc 2012, 134, 18089– 18100; 23082970 PMC3579771 b) Hayden JA, Brophy MB, Cunden LS, Nolan EM, J Am Chem Soc 2013, 135, 775– 787. 23276281 PMC3575579
  90. [91]Baker TM, Nakashige TG, Nolan EM, Neidig ML, Chem Sci 2017, 8, 1369– 1377. 28451278 PMC5361872
  91. [92]Zygiel EM, Nolan EM, Acc Chem Res 2019, 52, 2301– 2308. 31381301 PMC6702060
  92. [93]Nakashige TG, Nolan EM, Metallomics 2017, 9, 1086– 1095. 28561859 PMC5559331
  93. [94]Masse E, Salvail H, Desnoyers G, Arguin M, Cur Opin Microbiol 2007, 10, 140– 145. 17383226
  94. [95]da Silva Neto JF, Lourenco RF, Marques MV, BMC Genomics 2013, 14, 549. 23941329 PMC3751524
  95. [96]Eijkelkamp BA, Hassan KA, Paulsen IT, Brown MH, BMC Genomics 2011, 12, 126. 21342532 PMC3055841
  96. [97]Thamer W, Cirpus I, Hans M, Pierik AJ, Selmer T, Bill E, Linder D, Buckel W, Arch Microbiol 2003, 179, 197– 204. 12610725
  97. [98]a) Chazarreta-Cifre L, Martiarena L, de Mendoza D, Altabe SG, J Bacteriol 2011, 193, 4043– 4048; 21665975 PMC3147679 b) Yoch DC, Valentine RC, Ann Rev Microbiol 1972, 26, 139– 162; 4562807 c) Sandmann G, Peleato ML, Fillat MF, Lazaro MC, Gomez-Moreno C, Photosynth Res 1990, 26, 119– 125. 24420464
  98. [99]Vasileva D, Janssen H, Honicke D, Ehrenreich A, Bahl H, Microbiology 2012, 158, 1918– 1929. 22556358
  99. [100]Hastie JL, Hanna PC, Carlson PE, Pathog Dis 2018, 76. PMC6251574 29390127
  100. [101]Erdner DL, Price NM, Doucette GJ, Peleato ML, Anderson DM, Mar Ecol Progr Ser 1999, 184, 43– 53.
  101. [102]Worst DJ, Gerrits MM, Vandenbroucke-Grauls CM, Kusters JG, J Bacteriol 1998, 180, 1473– 1479. 9515916 PMC107047
  102. [103]a) Baichoo N, Wang T, Ye R, Helmann JD, Mol Microbiol 2002, 45, 1613– 1629; 12354229 b) Crossley RA, Gaskin DJ, Holmes K, Mulholland F, Wells JM, Kelly DJ, van Vliet AH, Walton NJ, Appl Environ Microbiol 2007, 73, 7819– 7825. 17965203 PMC2168145
  103. [104]a) Sepulveda Cisternas I, Salazar JC, Garcia-Angulo VA, Frontiers in microbiology 2018, 9, 1478; 30026736 PMC6041382 b) Pajuelo D, Hernandez-Cabanyero C, Sanjuan E, Lee CT, Silva-Hernandez FX, Hor LI, MacKenzie S, Amaro C, Environ Microbiol 2016, 18, 4005– 4022. 27348505
  104. [105]Mortensen BL, Rathi S, Chazin WJ, Skaar EP, J Bacteriol 2014, 196, 2616– 2626. 24816603 PMC4097591
  105. [106]a) Nairn BL, Lonergan ZR, Wang J, Braymer JJ, Zhang Y, Calcutt MW, Lisher JP, Gilston BA, Chazin WJ, de Crecy-Lagard V, Giedroc DP, Skaar EP, Cell Host Microbe 2016, 19, 826– 836; 27281572 PMC4901392 b) Jordan MR, Wang J, Weiss A, Skaar EP, Capdevila DA, Giedroc DP, Inorg Chem 2019, 58, 13661– 13672. 31247880 PMC7005846
  106. [107]Chandrangsu P, Huang X, Gaballa A, Helmann JD, Mol Microbiol 2019. PMC6736736 31132310
  107. [108]Fojcik C, Arnoux P, Ouerdane L, Aigle M, Alfonsi L, Borezee-Durant E, Mol Microbiol 2018, 108, 159– 177. 29431891
  108. [109]Peng ED, Oram DM, Battistel MD, Lyman LR, Freedberg DI, Schmitt MP, J Bacteriol 2018, 200, e00051– 18. 29507090 PMC5915790
  109. [110]a) Ghssein G, Brutesco C, Ouerdane L, Fojcik C, Izaute A, Wang S, Hajjar C, Lobinski R, Lemaire D, Richaud P, Voulhoux R, Espaillat A, Cava F, Pignol D, Borezee-Durant E, Arnoux P, Science 2016, 352, 1105– 1109; 27230378 b) Lhospice S, Gomez NO, Ouerdane L, Brutesco C, Ghssein G, Hajjar C, Liratni A, Wang S, Richaud P, Bleves S, Ball G, Borezee-Durant E, Lobinski R, Pignol D, Arnoux P, Voulhoux R, Sci Rep 2017, 7, 17132. 29214991 PMC5719457
  110. [111]a) Grim KP, San Francisco B, Radin JN, Brazel EB, Kelliher JL, Parraga Solorzano PK, Kim PC, McDevitt CA, Kehl-Fie TE, MBio 2017, 8; PMC5666155 29089427 b) Song L, Zhang Y, Chen W, Gu T, Zhang SY, Ji Q, Proc Natl Acad Sci U S A 2018, 115, 3942– 3947. 29581261 PMC5899449
  111. [112]Peng H, Shen J, Edmonds KA, Luebke JL, Hickey AK, Palmer LD, Chang FJ, Bruce KA, Kehl-Fie TE, Skaar EP, Giedroc DP, mSphere 2017, 2, e00082– 00017. 28656172 PMC5480029
  112. [113]Stork M, Grijpstra J, Bos MP, Manas Torres C, Devos N, Poolman JT, Chazin WJ, Tommassen J, PLoS Pathog 2013, 9, e1003733. 24204275 PMC3814407
  113. [114]a) Wakeman CA, Moore JL, Noto MJ, Zhang Y, Singleton MD, Prentice BM, Gilston BA, Doster RS, Gaddy JA, Chazin WJ, Caprioli RM, Skaar EP, Nat Commun 2016, 7, 11951; 27301800 PMC4912628 b) Ohlemacher SI, Giblin DE, d’Avignon DA, Stapleton AE, Trautner BW, Henderson JP, J Clin Invest 2017, 127, 4018– 4030. 28945201 PMC5663353
  114. [115]Moore JL, Becker KW, Nicklay JJ, Boyd KL, Skaar EP, Caprioli RM, Proteomics 2013, 14, 820– 828. 23754577 PMC3883928
  115. [116]a) Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP, Nat Chem Biol 2012, 8, 731– 736; 22772152 PMC3600419 b) Robinson AE, Lowe JE, Koh EI, Henderson JP, J Biol Chem 2018, 293, 14953– 14961; 30108176 PMC6166729 c) Koh EI, Hung CS, Parker KS, Crowley JR, Giblin DE, Henderson JP, Metallomics 2015, 7, 1011– 1022. 25824627 PMC4809022
  116. [117]Bleuel C, Grosse C, Taudte N, Scherer J, Wesenberg D, Krauss GJ, Nies DH, Grass G, J Bacteriol 2005, 187, 6701– 6707. 16166532 PMC1251586
  117. [118]Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK, Mol Cell 2002, 10, 1033– 1043. 12453412
  118. [119]Hoette TM, Abergel RJ, Xu J, Strong RK, Raymond KN, J Am Chem Soc 2008, 130, 17584– 17592. 19053425 PMC2778733

Cited by

Sorted by citations

Authors
Zhang, Y., Sen, S., & Giedroc, D. P.
Affiliations
Indiana University Bloomington (US)
Corresponding author
Giedroc, David P.
ORCID
Venue
ChemBioChem
Publisher
Wiley
Published
2020-04-14
Volume
21
Issue
14
Pages
1955-1967
ISSN
  • 1439-4227 (ISSN-L)
  • 1439-7633
DOI
10.1002/cbic.201900778
PMC
PMC7367709
OpenAlex
W3011622131
Cited by
30
References
23
Citations by year
2026: 4 · 2025: 5 · 2024: 6 · 2023: 5 · 2022: 3 · 2021: 3 · 2020: 4
FWCI
0.54
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • ChemBioChem (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (R35 GM118157, R01 AI101171)
  • Indiana University
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Keywords
iron acquisition, pathogenic bacteria, nutritional immunity, iron-containing enzymes, host-pathogen interaction, iron limitation, zinc limitation, metalloproteome
MeSH terms
Bacteria, Ferric Compounds, Host-Pathogen Interactions

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