Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis
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Transition metal ions are essential micronutrients for all living organisms. In mammals, these ions are often protein-bound and sequestered within cells, limiting their availability to microbes. Moreover, in response to infection, mammalian hosts further reduce the availability of metal nutrients by activating epithelial cells and recruiting neutrophils, both of which release metal-binding proteins with antimicrobial function. Microorganisms, in turn, have evolved sophisticated systems to overcome these limitations and acquire the metal ions essential for their growth. Here we review some of the mechanisms employed by the host and by pathogenic microorganisms to compete for transition metal ions, with a discussion of how evading "nutritional immunity" benefits pathogens. Furthermore, we provide new insights on the mechanisms of host-microbe competition for metal ions in the mucosa, particularly in the inflamed gut.
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S100 proteins can be induced by IL-17 and IL-22, exert pro-inflammatory activity, and may promote chemotaxis of PMN.
“In addition, S100 proteins can be induced by IL-17 and IL-22, and S100 proteins exert pro-inflammatory activity and may promote chemotaxis of PMN (233, 244).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [244]
S100A8 and S100A9 form the heterodimeric complex calprotectin, which is mainly expressed by PMN.
“Two of these proteins, S100A8 and S100A9, form a heterodimeric complex named calprotectin and are mainly expressed by PMN.”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [244]
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Hepcidin Regulates Cellular Iron Efflux by Binding to Ferroportin and Inducing Its Internalization
Nemeth, E., Tuttle, M. S., Powelson, J., Vaughn, M. B., Donovan, A., Ward, D. M., Ganz, T., & Kaplan, J. (2004) · Science · doi:10.1126/science.1104742 · Cited by 4,803 · see citing works
Andrews, S. C., Robinson, A. K., & Rodríguez-Quiñones, F. (2003) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(03)00055-x · Cited by 2,702 · see citing works
Nemeth, E., Rivera, S., Gabayan, V., Keller, C., Taudorf, S., Pedersen, B. K., & Ganz, T. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200420945 · Cited by 2,650 · see citing works
Liang, S. C., Tan, X.-Y., Luxenberg, D. P., Karim, R., Dunussi-Joannopoulos, K., Collins, M., & Fouser, L. A. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20061308 · Cited by 2,330 · see citing works
Hepcidin, a urinary antimicrobial peptide synthesized in the liver
Park, C. H., Valore, E. V., Waring, A. J., & Ganz, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008922200 · Cited by 2,168 · see citing works
Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens
Zheng, Y., Valdez, P. A., Danilenko, D. M., Hu, Y., Susan, M. L., Gong, Q., Abbas, A. R., Modrusan, Z. D., Ghilardi, N., de Sauvage, F. J., et al. (2008) · Nature Medicine · doi:10.1038/nm1720 · Cited by 1,910 · see citing works
Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron
Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., & Aderem, A. (2004) · Nature · doi:10.1038/nature03104 · Cited by 1,877 · see citing works
Siderophore-Based Iron Acquisition and Pathogen Control
Miethke, M., & Marahiel, M. A. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00012-07 · Cited by 1,774 · see citing works
Urban, C. F., Ermert, D., Schmid, M., Abed, U. A., Goosmann, C., Nacken, W. K. F., Brinkmann, V., Jungblut, P. R., & Zychlinsky, A. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000639 · Cited by 1,677 · see citing works
Siderophores: Structure and Function of Microbial Iron Transport Compounds
Neilands, J. B. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.26723 · Cited by 1,652 · see citing works
Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein
Nemeth, E., Valore, E. V., Territo, M., Schiller, G., Lichtenstein, A., & Ganz, T. (2003) · Blood · doi:10.1182/blood-2002-10-3235 · Cited by 1,417 · see citing works
Goetz, D. H., Holmes, M. A., Borregaard, N., Bluhm, M. E., Raymond, K. N., & Strong, R. K. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00708-6 · Cited by 1,355 · see citing works
LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity
Krause, A., Neitz, S., Mägert, H.-J., Schulz, A., Forssmann, W.-G., Schulz-Knappe, P., & Adermann, K. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01920-7 · Cited by 1,324 · see citing works
Trace elements in human physiology and pathology: zinc and metallothioneins
Tapiero, H., & Tew, K. D. (2003) · Biomedicine & Pharmacotherapy · doi:10.1016/s0753-3322(03)00081-7 · Cited by 1,297 · see citing works
Metalloproteins and metal sensing
Waldron, K. J., Rutherford, J. C., Ford, D., & Robinson, N. J. (2009) · Nature · doi:10.1038/nature08300 · Cited by 1,269 · see citing works
Nicolas, G., Bennoun, M., Devaux, I., Beaumont, C., Grandchamp, B., Kahn, A., & Vaulont, S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.151179498 · Cited by 1,233 · see citing works
IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia
Aujla, S. J., Chan, Y. R., Zheng, M., Fei, M., Askew, D. J., Pociask, D. A., Reinhart, T. A., McAllister, F. M., Edeal, J., Gaus, K., et al. (2008) · Nature Medicine · doi:10.1038/nm1710 · Cited by 1,162 · see citing works
Manichanh, C., Borruel, N., Casellas, F., & Guarner, F. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.152 · Cited by 1,160 · see citing works
Metal ions in biological catalysis: from enzyme databases to general principles
Andreini, C., Bertini, I., Cavallaro, G., Holliday, G. L., & Thornton, J. M. (2008) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-008-0404-5 · Cited by 1,150 · see citing works
Severe iron deficiency anemia in transgenic mice expressing liver hepcidin
Nicolas, G., Bennoun, M., Porteu, A., Mativet, S., Beaumont, C., Grandchamp, B., Sirito, M., Sawadogo, M., Kahn, A., & Vaulont, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.072632499 · Cited by 880 · see citing works
Metal Chelation and Inhibition of Bacterial Growth in Tissue Abscesses
Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., Anderson, K. L., Dattilo, B. M., Dunman, P. M., Gerads, R., et al. (2008) · Science · doi:10.1126/science.1152449 · Cited by 857 · see citing works
The roles of iron in health and disease
Lieu, P. T., Heiskala, M. K., Peterson, P. A., & Yang, Y. M. (2001) · Molecular Aspects of Medicine · doi:10.1016/s0098-2997(00)00006-6 · Cited by 813 · see citing works
Chemistry and biology of eukaryotic iron metabolism
Aisen, P. (2001) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(01)00063-2 · Cited by 804 · see citing works
Genetics and Assembly Line Enzymology of Siderophore Biosynthesis in Bacteria
Crosa, J. H., & Walsh, C. T. (2002) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.66.2.223-249.2002 · Cited by 797 · see citing works
Tam, R., & Saier, M. H. (1993) · Microbiological Reviews · doi:10.1128/mr.57.2.320-346.1993 · Cited by 732 · see citing works
LACTOFERRIN, AN IRON-BINBING PROTEIN NI NEUTROPHILIC LEUKOCYTES
Masson, P. L., Heremans, J. F., & Schonne, E. (1969) · The Journal of Experimental Medicine · doi:10.1084/jem.130.3.643 · Cited by 700 · see citing works
Hepcidin and the iron-infection axis
Drakesmith, H., & Prentice, A. M. (2012) · Science · doi:10.1126/science.1224577 · Cited by 686 · see citing works
Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection
Gläser, R., Harder, J., Lange, H., Bartels, J., Christophers, E., & Schröder, J.-M. (2005) · Nature Immunology · doi:10.1038/ni1142 · Cited by 651 · see citing works
Zinc through the Three Domains of Life
Andreini, C., Banci, L., Bertini, I., & Rosato, A. (2006) · Journal of Proteome Research · doi:10.1021/pr0603699 · Cited by 648 · see citing works
Nutritional immunity beyond iron: a role for manganese and zinc
Kehl-Fie, T. E., & Skaar, E. P. (2010) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2009.11.008 · Cited by 634 · see citing works
Stoichiometric and site characteristics of the binding of iron to human transferrin
Aisen, P., Leibman, A., & Zweier, J. (1978) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)62337-9 · Cited by 601 · see citing works
Structural biology of bacterial iron uptake
Krewulak, K. D., & Vogel, H. J. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.07.026 · Cited by 552 · see citing works
Probiotic Bacteria Reduce Salmonella Typhimurium Intestinal Colonization by Competing for Iron
Deriu, E., Liu, J. Z., Pezeshki, M., Edwards, R. A., Ochoa, R. J., Contreras, H., Libby, S. J., Fang, F. C., & Raffatellu, M. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.06.007 · Cited by 550 · see citing works
Self-citationLack of a role for iron in the Lyme disease pathogen
Posey, J. E., & Gherardini, F. C. (2000) · Science · doi:10.1126/science.288.5471.1651 · Cited by 538 · see citing works
Raffatellu, M., George, M. D., Akiyama, Y., Hornsby, M. J., Nuccio, S.-P., Paixao, T. A., Butler, B. P., Chu, H., Santos, R. L., Berger, T., et al. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.03.011 · Cited by 525 · see citing works
Self-citationAntimicrobial actions of calcium binding leucocyte L1 protein, calprotectin
Steinbakk, M., Naess-Andresen, C. F., Fagerhol, M. K., Lingaas, E., Dale, I., & Brandtzaeg, P. (1990) · The Lancet · doi:10.1016/0140-6736(90)93237-j · Cited by 512 · see citing works
The ZnuABC high‐affinity zinc uptake system and its regulator Zur in <i>Escherichia coli</i>
Patzer, S. I., & Hantke, K. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00883.x · Cited by 490 · see citing works
Andoh, A., Zhang, Z., Inatomi, O., Fujino, S., Deguchi, Y., Araki, Y., Tsujikawa, T., Kitoh, K., Kim‐Mitsuyama, S., Takayanagi, A., et al. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.06.071 · Cited by 480 · see citing works
Berger, T., Togawa, A., Duncan, G. S., Elia, A. J., You-Ten, A., Wakeham, A., Fong, H. E. H., Cheung, C. C., & Mak, T. W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510847103 · Cited by 460 · see citing works
Enterobactin, an iron transport compound from Salmonella typhimurium
Pollack, J. R., & Neilands, J. B. (1970) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(70)90819-3 · Cited by 433 · see citing works
Divalent-metal transport by NRAMP proteins at the interface of host–pathogen interactions
Forbes, J. R., & Gros, P. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02098-4 · Cited by 424 · see citing works
Kehl-Fie, T. E., Chitayat, S., Hood, M. I., Damo, S., Restrepo, N., Garcia, C., Munro, K. A., Chazin, W. J., & Skaar, E. P. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.07.004 · Cited by 419 · see citing works
Iron homeostasis: insights from genetics and animal models
Andrews, N. C. (2000) · Nature Reviews Genetics · doi:10.1038/35042073 · Cited by 418 · see citing works
Zinc: an essential but elusive nutrient
King, J. C. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.005744 · Cited by 399 · see citing works
McAllister, F. M., Henry, A. C., Kreindler, J. L., Dubin, P. J., Ulrich, L., Steele, C. H., Finder, J. D., Pilewski, J. M., Carreno, B. M., Goldman, S. J., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.1.404 · Cited by 398 · see citing works
MRP-8 and MRP-14, two abundant Ca2+-binding proteins of neutrophils and monocytes
Hessian, P. A., Edgeworth, J. D., & Hogg, N. (1993) · Journal of Leukocyte Biology · doi:10.1002/jlb.53.2.197 · Cited by 396 · see citing works
Damo, S. M., Kehl-Fie, T. E., Sugitani, N., Holt, M. E., Rathi, S., Murphy, W. J., Zhang, Y., Betz, C., Hench, L., Fritz, G., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220341110 · Cited by 388 · see citing works
Dintilhac, A., Alloing, G., Granadel, C., & Claverys, J. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.5111879.x · Cited by 380 · see citing works
TLR4-dependent hepcidin expression by myeloid cells in response to bacterial pathogens
Peyssonnaux, C., Zinkernagel, A. S., Datta, V., Lauth, X., Johnson, R. S., & Nizet, V. (2006) · Blood · doi:10.1182/blood-2005-06-2259 · Cited by 379 · see citing works
“Blooming” in the gut: how dysbiosis might contribute to pathogen evolution.
Stecher, B., Maier, L., & Hardt, W.-D. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2989 · Cited by 378 · see citing works
Lipoproteins of gram-positive bacteria
Sutcliffe, I. C., & Russell, R. R. B. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.5.1123-1128.1995 · Cited by 377 · see citing works
Natural Resistance to Intracellular Infections
Jabado, N., Jankowski, A., Dougaparsad, S., Picard, V., Grinstein, S., & Gros, P. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.9.1237 · Cited by 372 · see citing works
The structure of enterochelin and related 2,3-dihydroxy-N-benzoyne conjugates from Eschericha Coli
O'Brien, I. G., & Gibson, F. (1970) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(70)90038-3 · Cited by 366 · see citing works
Hantke, K., Nicholson, G., Rabsch, W., & Winkelmann, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0737682100 · Cited by 359 · see citing works
Raymond, K. N., Müller, G., & Matzanke, B. F. (1984) · Topics in Current Chemistry · doi:10.1007/3-540-13099-3_2 · Cited by 357 · see citing works
Zindl, C., Lai, J., Lee, Y., Maynard, C. L., Harbour, S. N., Ouyang, W., Chaplin, D., & Weaver, C. (2013) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1300318110 · Cited by 347 · see citing works
A High-Affinity Iron Permease Essential for <i>Candida albicans</i> Virulence
Ramanan, N., & Wang, Y. (2000) · Science · doi:10.1126/science.288.5468.1062 · Cited by 336 · cited 1× · see citing works
“In the case of Candida albicans, uptake of unbound iron via the high-affinity iron permease FTR1 is critical for establishing systemic infection in mice (Ramanan and Wang, 2000).”
BackgroundHaas, H. (2003) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-003-1335-2 · Cited by 334 · see citing works
Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., Restrepo, N. A., Hosking, M. P., Edwards, R. A., Battistoni, A., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.01.017 · Cited by 328 · see citing works
Self-citationPetsko, G. A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.2.538 · Cited by 327 · see citing works
Touch and go: tying TonB to transport
Postle, K., & Kadner, R. J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03629.x · Cited by 321 · see citing works
How pathogenic bacteria evade mammalian sabotage in the battle for iron
Fischbach, M. A., Lin, H., Liu, D. R., & Walsh, C. T. (2006) · Nature Chemical Biology · doi:10.1038/nchembio771 · Cited by 321 · see citing works
Bacterial zinc uptake and regulators
Hantke, K. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.02.001 · Cited by 319 · see citing works
Bachman, M. A., Oyler, J. E., Burns, S. H., Caza, M., Lepine, F. L., Dozois, C. M., & Weiser, J. N. (2011) · Infection and Immunity · doi:10.1128/iai.05114-11 · Cited by 308 · see citing works
Battles with Iron: Manganese in Oxidative Stress Protection
Aguirre, J. D., & Culotta, V. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.312181 · Cited by 304 · see citing works
TonB‐dependent iron acquisition: mechanisms of siderophore‐mediated active transport†
Moeck, G., & Coulton, J. W. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00817.x · Cited by 302 · see citing works
Hepcidin regulation by innate immune and infectious stimuli
Armitage, A. E., Eddowes, L. A., Gileadi, U., Cole, S., Spottiswoode, N., Selvakumar, T. A., Ho, L.-P., Townsend, A. R. M., & Drakesmith, H. (2011) · Blood · doi:10.1182/blood-2011-04-351957 · Cited by 294 · see citing works
Kehres, D. G., Zaharik, M. L., Finlay, B. B., & Maguire, M. E. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01922.x · Cited by 292 · see citing works
Iron uptake in fungi: a system for every source
Philpott, C. C. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.05.008 · Cited by 289 · see citing works
Forbes, J. R., & Gros, P. (2003) · Blood · doi:10.1182/blood-2003-02-0425 · Cited by 288 · see citing works
Awane, M., Andres, P. G., Li, D. J., & Reinecker, H. (1999) · PubMed · Cited by 288 · see citing works
Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria
Kehres, D. G., & Maguire, M. E. (2003) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(03)00052-4 · Cited by 284 · see citing works
Panina, E. M., Mironov, A. A., & Gelfand, M. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1733691100 · Cited by 284 · see citing works
Que, Q., & Helmann, J. D. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01811.x · Cited by 282 · see citing works
Manganese Transport and the Role of Manganese in Virulence
Papp‐Wallace, K. M., & Maguire, M. E. (2006) · Annual Review of Microbiology · doi:10.1146/annurev.micro.60.080805.142149 · Cited by 273 · see citing works
Recent insights into iron import by bacteria
Braun, V., & Hantke, K. (2011) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2011.01.005 · Cited by 264 · see citing works
Hood, M. I., Mortensen, B. L., Moore, J. L., Zhang, Y., Kehl-Fie, T. E., Sugitani, N., Chazin, W. J., Caprioli, R. M., & Skaar, E. P. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003068 · Cited by 255 · see citing works
ABC transporter architecture and regulatory roles of accessory domains
Biemans‐Oldehinkel, E., Doeven, M. K., & Poolman, B. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.11.079 · Cited by 250 · see citing works
Ammendola, S., Pasquali, P., Pistoia, C., Petrucci, P., Petrarca, P., Rotilio, G., & Battistoni, A. (2007) · Infection and Immunity · doi:10.1128/iai.00559-07 · Cited by 248 · see citing works
Makui, H., Roig, E. A., Cole, S. T., Helmann, J. D., Gros, P., & Cellier, M. F. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01774.x · Cited by 237 · see citing works
Calcium-dependent complex assembly of the myeloic differentiation proteins MRP-8 and MRP-14
Teigelkamp, S., Bhardwaj, R. S., Roth, J., Meinardus‐Hager, G., Karas, M., & Sorg, C. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)98862-9 · Cited by 229 · see citing works
Horsburgh, M. J., Wharton, S. J., Cox, A. G., Ingham, E., Peacock, S., & Foster, S. J. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02944.x · Cited by 228 · see citing works
Heymann, P., Gerads, M., Schaller, M., Dromer, F., Winkelmann, G., & Ernst, J. F. (2002) · Infection and Immunity · doi:10.1128/iai.70.9.5246-5255.2002 · Cited by 226 · see citing works
The Metal Permease ZupT from Escherichia coli Is a Transporter with a Broad Substrate Spectrum
Grass, G., Franke, S., Taudte, N., Nies, D. H., Kucharski, L. M., Maguire, M. E., & Rensing, C. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.5.1604-1611.2005 · Cited by 218 · see citing works
Kehl-Fie, T. E., Zhang, Y., Moore, J. L., Farrand, A. J., Hood, M. I., Rathi, S., Chazin, W. J., Caprioli, R. M., & Skaar, E. P. (2013) · Infection and Immunity · doi:10.1128/iai.00420-13 · Cited by 213 · see citing works
Gilson, É., Alloing, G., Schmidt, T., Claverys, J., Dudler, R., & Hofnung, M. J. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb03284.x · Cited by 205 · see citing works
Nramp1 phagocyte intracellular metal withdrawal defense
Cellier, M. F., Courville, P., & Campion, C. (2007) · Microbes and Infection · doi:10.1016/j.micinf.2007.09.006 · Cited by 203 · see citing works
ZupT Is a Zn(II) Uptake System in <i>Escherichia coli</i>
Grass, G., Wong, M. D., Rosen, B. P., Smith, R. L., & Rensing, C. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.3.864-866.2002 · Cited by 197 · see citing works
Active transport of iron and siderophore antibiotics
Braun, V (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00298-9 · Cited by 188 · see citing works
Crouch, M. V., Castor, M., Karlinsey, J. E., Kalhorn, T., & Fang, F. C. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06089.x · Cited by 187 · see citing works
Bachman, M. A., Miller, V. L., & Weiser, J. N. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000622 · Cited by 186 · see citing works
Zhou, D., Hardt, W.-D., & Galán, J. E. (1999) · Infection and Immunity · doi:10.1128/iai.67.4.1974-1981.1999 · Cited by 182 · see citing works
SitABCD Is the Alkaline Mn<sup>2+</sup>Transporter of<i>Salmonella enterica</i>Serovar Typhimurium
Kehres, D. G., Janakiraman, A., Slauch, J. M., & Maguire, M. E. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.12.3159-3166.2002 · Cited by 177 · see citing works
Kao, C., Huang, F., Chen, Y. M., Thai, P., Wachi, S., Kim, C., Tam, L., & Wu, R. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.10.6676 · Cited by 176 · see citing works
Anti-Infective Protective Properties of S100 Calgranulins
Hsu, K., Champaiboon, C., Guenther, B. D., Sorenson, B. S., Khammanivong, A., Ross, K. F., Geczy, C. L., & Herzberg, M. C. (2009) · Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry · doi:10.2174/187152309789838975 · Cited by 173 · see citing works
A new family of high-affinity ABC manganese and zinc permeases
Claverys, J. (2001) · Research in Microbiology · doi:10.1016/s0923-2508(01)01195-0 · Cited by 169 · see citing works
Nramp1 promotes efficient macrophage recycling of iron following erythrophagocytosis in vivo
Soe-Lin, S., Apte, S. S., Andriopoulos, B., Andrews, M. C., Schranzhofer, M., Kahawita, T., Garcia-Santos, D., & Ponka, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900808106 · Cited by 167 · see citing works
Manganese Metabolism in Animals and Humans Including the Toxicity of Manganese
Keen, C. L., Ensunsa, J. L., & Clegg, M. S. (2000) · CRC Press eBooks · doi:10.1201/9781482289893-14 · Cited by 158 · see citing works
Carrano, C. J., & Raymond, K. N. (1979) · Journal of the American Chemical Society · doi:10.1021/ja00512a047 · Cited by 155 · see citing works
S100 Calgranulins in inflammatory arthritis
Perera, C., McNeil, H. P., & Geczy, C. L. (2009) · Immunology and Cell Biology · doi:10.1038/icb.2009.88 · Cited by 152 · see citing works
Campoy, S., Jara, M., Busquets, N., de Rozas, A. M. P., Badiola, I., & Barbé, J. (2002) · Infection and Immunity · doi:10.1128/iai.70.8.4721-4725.2002 · Cited by 148 · see citing works
Ross, S. L., Tran, L., Winters, A., Lee, K.-J., Plewa, C., Foltz, I., King, C., Miranda, L. P., Allen, J., Beckman, H., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.03.017 · Cited by 145 · see citing works
Mycobactin-mediated iron acquisition within macrophages
Luo, M., Fadeev, E. A., & Groves, J. T. (2005) · Nature Chemical Biology · doi:10.1038/nchembio717 · Cited by 141 · see citing works
Lipocalin 2 Deficiency Dysregulates Iron Homeostasis and Exacerbates Endotoxin-Induced Sepsis
Srinivasan, G., Aitken, J. D., Zhang, B., Carvalho, F. A., Chassaing, B., Shashidharamurthy, R., Borregaard, N., Jones, D. P., Gewirtz, A. T., & Vijay–Kumar, M. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200892 · Cited by 137 · see citing works
Rodriguez, R., Jung, C.-L., Gabayan, V., Deng, J. C., Ganz, T., Nemeth, E., & Bulut, Y. (2014) · Infection and Immunity · doi:10.1128/iai.00983-13 · Cited by 127 · see citing works
Kolenbrander, P. E., Andersen, R. N., Baker, R. A., & Jenkinson, H. F. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.2.290-295.1998 · Cited by 124 · see citing works
Novel insights into the role of S 100 A 8/ A 9 in skin biology
Kerkhoff, C., Voß, A., Scholzen, T. E., Averill, M. M., Zänker, K. S., & Bornfeldt, K. (2012) · Experimental Dermatology · doi:10.1111/j.1600-0625.2012.01571.x · Cited by 122 · see citing works
Davis, L. M., Kakuda, T., & DiRita, V. J. (2008) · Journal of Bacteriology · doi:10.1128/jb.01394-08 · Cited by 118 · see citing works
The Diversity of Microbial Responses to Nitric Oxide and Agents of Nitrosative Stress
Bowman, L. A. H., McLean, S., Poole, R. K., & Fukuto, J. M. (2011) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/b978-0-12-387661-4.00006-9 · Cited by 117 · see citing works
Aerobactin genes in Shigella spp
Lawlor, K. M., & Payne, S. M. (1984) · Journal of Bacteriology · doi:10.1128/jb.160.1.266-272.1984 · Cited by 117 · see citing works
Mammalian Siderophores, Siderophore-binding Lipocalins, and the Labile Iron Pool
Correnti, C., & Strong, R. K. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.311829 · Cited by 115 · see citing works
Expression and role of superoxide dismutases (SOD) in pathogenic bacteria
Lynch, M. C., & Kuramitsu, H. K. (2000) · Microbes and Infection · doi:10.1016/s1286-4579(00)01278-8 · Cited by 113 · see citing works
Debrunner, P. G. (1983) · Science · doi:10.1126/science.220.4603.1266 · Cited by 110 · see citing works
Calcitermin, a novel antimicrobial peptide isolated from human airway secretions
Cole, A. M., Kim, Y., Tahk, S., Hong, T., Weis, P., Waring, A. J., & Ganz, T. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02731-4 · Cited by 104 · see citing works
Karlinsey, J. E., Maguire, M. E., Becker, L. A., Crouch, M. V., & Fang, F. C. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07357.x · Cited by 102 · see citing works
Manganese in natural waters and earth's crust: its availability to organisms.
Jj, M. (2000) · PubMed · Cited by 93 · see citing works
Kim, S., Watanabe, K., Shirahata, T., & Watarai, M. (2004) · Journal of Veterinary Medical Science · doi:10.1292/jvms.66.1059 · Cited by 92 · see citing works
Lusitani, D., Malawista, S. E., & Montgomery, R. R. (2003) · Infection and Immunity · doi:10.1128/iai.71.8.4711-4716.2003 · Cited by 91 · see citing works
Lee, M. J., Lee, J., Choi, J., Lee, C. S., Sim, J. H., Cho, C., Lee, K. H., Cho, I., Chung, M.-H., Kim, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038801 · Cited by 89 · see citing works
Role of prokaryotic Cu,Zn superoxide dismutase in pathogenesis
Battistoni, A. (2003) · Biochemical Society Transactions · doi:10.1042/bst0311326 · Cited by 89 · see citing works
Siderophore synthesis in Klebsiella pneumoniae and Shigella sonnei during iron deficiency
Perry, R. D., & Clemente, C. L. S. (1979) · Journal of Bacteriology · doi:10.1128/jb.140.3.1129-1132.1979 · Cited by 86 · see citing works
Fritsche, G., Dlaska, M., Barton, H., Theurl, I., Garimorth, K., & Weiss, G. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.4.1994 · Cited by 86 · see citing works
Chakraborty, R., Storey, E. P., & der Helm, D. V. (2006) · BioMetals · doi:10.1007/s10534-006-9060-9 · Cited by 86 · see citing works
FhuA (TonA), the Career of a Protein
Braun, V. (2009) · Journal of Bacteriology · doi:10.1128/jb.00106-09 · Cited by 81 · see citing works
Fritsche, G., Nairz, M., Libby, S. J., Fang, F. C., & Weiss, G. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1111554 · Cited by 72 · see citing works
Calgranulin C Has Filariacidal and Filariastatic Activity
Gottsch, J. D., Eisinger, S. W., Liu, S. H., & Scott, A. L. (1999) · Infection and Immunity · doi:10.1128/iai.67.12.6631-6636.1999 · Cited by 72 · see citing works
The theft of host heme by Gram-positive pathogenic bacteria
Nobles, C. L., & Maresso, A. W. (2011) · Metallomics · doi:10.1039/c1mt00047k · Cited by 69 · see citing works
Point mutations change specificity and kinetics of metal uptake by ZupT from Escherichia coli
Taudte, N., & Grass, G. (2010) · BioMetals · doi:10.1007/s10534-010-9319-z · Cited by 66 · see citing works
<i>Nramp1</i>‐functionality increases iNOS expression <i>via</i> repression of IL‐10 formation
Fritsche, G., Nairz, M., Werner, E. R., Barton, H. C., & Weiss, G. (2008) · European Journal of Immunology · doi:10.1002/eji.200838449 · Cited by 57 · see citing works
Østvik, A. E., Granlund, A. V. B., TORP, S. H., Flatberg, A., Beisvåg, V., Waldum, H. L., Flo, T. H., Espevik, T., Damås, J. K., & Sandvik, A. K. (2013) · Clinical & Experimental Immunology · doi:10.1111/cei.12136 · Cited by 56 · see citing works
Biomarkers of Therapeutic Response in the IL-23 Pathway in Inflammatory Bowel Disease
Cayatte, C., Joyce-Shaikh, B., Vega, F., Boniface, K., Grein, J., Murphy, E., Blumenschein, W. M., Chen, S., Malinao, M.-C., Basham, B., et al. (2012) · Clinical and Translational Gastroenterology · doi:10.1038/ctg.2012.2 · Cited by 52 · see citing works
Garrido, M. E. B., Bosch, M., Medina, R., Llagostera, M., de Rozas, A. M. P., Badiola, I., & Barbé, J. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00131-9 · Cited by 52 · see citing works
Boniface, K., Lecron, J., Bernard, F., Dagrégorio, G., Guillet, G., Nau, F., & Morel, F. (2005) · PubMed · Cited by 52 · see citing works
Moore, J. L., Becker, K. W., Nicklay, J. J., Boyd, K. L., Skaar, E. P., & Caprioli, R. M. (2013) · PROTEOMICS · doi:10.1002/pmic.201300046 · Cited by 49 · see citing works
A Comparison of Human S100A12 with MRP-14 (S100A9)
Robinson, M. J., & Hogg, N. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3407 · Cited by 49 · see citing works
Increased ferritin synthesis and iron uptake in inflammatory mouse macrophages
Birgegård, G., & Caro, J. (1984) · Scandinavian Journal of Haematology · doi:10.1111/j.1600-0609.1984.tb02208.x · Cited by 44 · see citing works
Manganese in Natural Waters and Earth’s Crust: Its Availability to Organisms
(2000) · CRC Press eBooks · doi:10.1201/9781482289893-11 · Cited by 43 · see citing works
Production of enterochelin by Escherichia coli 0111
Rogers, H. J., Synge, C., Kimber, B. J., & Bayley, P. M. (1977) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(77)90211-2 · Cited by 39 · see citing works
Negative Interactions with the Microbiota: IBD
Salzman, N. H., & Bevins, C. L. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-09550-9_6 · Cited by 38 · see citing works
Faecal calprotectin concentrations in gastrointestinal diseases
Wang, S., Wang, Z., Shi, H., Lu, H., Wei, J., Yuan, B., Wu, X., & Wang, F. (2013) · Journal of International Medical Research · doi:10.1177/0300060513488499 · Cited by 31 · see citing works
Bando, M., Zou, X., Hiroshima, Y., Kataoka, M., Ross, K. F., Shinohara, Y., Nagata, T., Herzberg, M. C., & Kido, J.-I. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.03.010 · Cited by 27 · see citing works
(2005) · Van Nostrand's Scientific Encyclopedia · doi:10.1002/0471743984.vse4298 · Cited by 9 · see citing works
(1984) · Topics in current chemistry · doi:10.1007/3-540-13099-3 · Cited by 2 · see citing works
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Macrophage defense mechanisms against intracellular bacteria
Weiss, G., & Schaible, U. E. (2015) · Immunological Reviews · doi:10.1111/imr.12266 · Cited by 989 · see citing works
Resolution of Inflammation: What Controls Its Onset?
Sugimoto, M. A., Sousa, L. P., Pinho, V., Perretti, M., & Teixeira, M. M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00160 · Cited by 638 · see citing works
Iron at the interface of immunity and infection
Nairz, M., Haschka, D., Demetz, E., & Weiss, G. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00152 · Cited by 325 · see citing works
“…effect against such infections via acidification of the microbe containing phagosome, but also by altering the cellular distribution of divalent metals such as zinc, manganese or iron which all play decisive role in host–pathogen interaction (Hood and Skaar, 2012; Diaz-Ochoa et al., 2014).”
BackgroundDiverging roles of bacterial siderophores during infection
Holden, V. I., & Bachman, M. A. (2015) · Metallomics · doi:10.1039/c4mt00333k · Cited by 274 · see citing works
Human calprotectin is an iron-sequestering host-defense protein
Nakashige, T. G., Zhang, B., Krebs, C., & Nolan, E. M. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1891 · Cited by 291 · see citing works
Nutritional iron turned inside out: intestinal stress from a gut microbial perspective
Kortman, G. A. M., Raffatellu, M., Swinkels, D. W., & Tjalsma, H. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12086 · Cited by 291 · see citing works
Self-citationThe Iron age of host–microbe interactions
Soares, M. P., & Weiss, G. (2015) · The EMBO Reports · doi:10.15252/embr.201540558 · Cited by 227 · see citing works
Constante, M., Fragoso, G., Calvé, A., Samba-Mondonga, M., & Santos, M. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01809 · Cited by 161 · see citing works
Manganese homeostasis and utilization in pathogenic bacteria
Juttukonda, L. J., & Skaar, E. P. (2015) · Molecular Microbiology · doi:10.1111/mmi.13034 · Cited by 121 · see citing works
Role of divalent metals in infectious disease susceptibility and outcome
Weiss, G., & Carver, P. L. (2018) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2017.01.018 · Cited by 123 · see citing works
Nickel Sequestration by the Host-Defense Protein Human Calprotectin
Nakashige, T. G., Zygiel, E. M., Drennan, C. L., & Nolan, E. M. (2017) · Journal of the American Chemical Society · doi:10.1021/jacs.7b01212 · Cited by 125 · see citing works
Kapetanovic, R., Bokil, N. J., Achard, M. E. S., Ong, C. Y., Peters, K. M., Stocks, C. J., Phan, M., Monteleone, M., Schroder, K., Irvine, K. M., et al. (2016) · The FASEB Journal · doi:10.1096/fj.201500061 · Cited by 86 · see citing works
Gaddy, J. A., Radin, J. N., Loh, J. T., Piazuelo, M. B., Kehl-Fie, T. E., Delgado, A. G., Ilca, F. T., Peek, R. M., Cover, T. L., Chazin, W. J., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004450 · Cited by 87 · see citing works
Haley, K. P., Delgado, A. G., Piazuelo, M. B., Mortensen, B. L., Correa, P., Damo, S. M., Chazin, W. J., Skaar, E. P., & Gaddy, J. A. (2015) · Infection and Immunity · doi:10.1128/iai.00544-15 · Cited by 68 · see citing works
Gaddy, J. A., Radin, J. N., Cullen, T. W., Chazin, W. J., Skaar, E. P., Trent, M. S., & Algood, H. M. S. (2015) · mBio · doi:10.1128/mbio.01349-15 · Cited by 59 · see citing works
Price, S. L., Vadyvaloo, V., DeMarco, J. K., Brady, A., Gray, P. A., Kehl-Fie, T. E., Garneau-Tsodikova, S., Perry, R. D., & Lawrenz, M. B. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2104073118 · Cited by 49 · see citing works
Competition for Manganese at the Host–Pathogen Interface
Kelliher, J. L., & Kehl-Fie, T. E. (2016) · Progress in Molecular Biology and Translational Science · doi:10.1016/bs.pmbts.2016.05.002 · Cited by 34 · see citing works
Haschka, D., Nairz, M., Demetz, E., Wienerroither, S., Decker, T., & Weiss, G. (2015) · Metallomics · doi:10.1039/c4mt00328d · Cited by 29 · see citing works
- Authors
- Diaz-Ochoa, V. E., Jellbauer, S., Klaus, S., & Raffatellu, M.
- Affiliations
- University of California, Irvine (US)
- Corresponding author
- Raffatellu, Manuela
- Venue
- Frontiers in Cellular and Infection Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2014
- Volume
- 4
- Pages
- 2-2
- ISSN
- 2235-2988 (ISSN-L)
- PMC
- PMC3900919
- OpenAlex
- W1983281945
- Cited by
- 129
- References
- 143
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 4 · 2023: 8 · 2022: 10 · 2021: 10 · 2020: 8 · 2019: 8 · 2018: 8 · 2017: 16 · 2016: 17 · 2015: 20 · 2014: 8
- FWCI
- 2.31
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cellular and Infection Microbiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institute of General Medical Sciences (T32GM008620)
- National Institute of Allergy and Infectious Diseases (AI083663, R01AI083663, U54AI065359)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- transition metal ions, nutritional immunity, mucosal immunity, intestinal inflammation, metal-binding proteins, antimicrobial peptides, neutrophils, epithelial cells, pathogenic microorganisms, micronutrients
- MeSH terms
- Animals, Bacteria, Fungi, Humans, Ions, Metals, Mucous Membrane, Virulence, Immunity, Mucosal, Host-Pathogen Interactions
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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