Heme protects Pseudomonas aeruginosa and Staphylococcus aureus from calprotectin-induced iron starvation
Open accessAbstract
Pseudomonas aeruginosa and Staphylococcus aureus are opportunistic bacterial pathogens that cause severe infections in immunocompromised individuals and patients with cystic fibrosis. Both P. aeruginosa and S. aureus require iron to infect the mammalian host. To obtain iron, these pathogens may rely on siderophore-mediated ferric iron uptake, ferrous iron uptake, or heme uptake at different points during infection. The preferred iron source depends on environmental conditions, including the presence of iron-sequestering host-defense proteins. Here, we investigate how the presence of heme, a highly relevant iron source during infection, affects bacterial responses to iron withholding by the innate immune protein calprotectin (CP). Prior work has shown that P. aeruginosa is starved of iron in the presence of CP. We report that P. aeruginosa upregulates expression of heme uptake machinery in response to CP. Furthermore, we show that heme protects P. aeruginosa from CP-mediated inhibition of iron uptake and iron-starvation responses. We extend our study to a second bacterial pathogen, S. aureus, and demonstrate that CP also inhibits iron uptake and induces iron-starvation responses by this pathogen. Similarly to P. aeruginosa, we show that heme protects S. aureus from CP-mediated inhibition of iron uptake and iron-starvation responses. These findings expand our understanding of microbial responses to iron sequestration by CP and highlight the importance of heme utilization for bacterial adaptation to host iron-withholding strategies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the presence of the Fe-sequestering protein calprotectin, haem availability is essential for the survival of Staphylococcus aureus and Pseudomonas aeruginosa, highlighting the importance of haem as an Fe source within the host.
“For instance, in the presence of the Fe- sequestering protein calprotectin, haem availability is essential for the survival of S. aureus and Pseudomonas aeruginosa , highlighting the importance of haem as an Fe source within the host 41 .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [41]
The Results and Discussion report that haem protects both species from calprotectin-induced iron depletion and starvation. They do not establish that haem is essential for their survival in the presence of calprotectin; the Discussion describes its protective role during infection as a possibility, not a demonstrated host finding. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Lung Infections Associated with Cystic Fibrosis
Lyczak, J. B., Cannon, C. L., & Pier, G. B. (2002) · Clinical Microbiology Reviews · doi:10.1128/cmr.15.2.194-222.2002 · Cited by 1,634 · see citing works
Cleavage of the haem-protein link by acid methylethylketone
Teale, F. W. J. (1959) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(59)90407-x · Cited by 1,242 · see citing works
Iron in infection and immunity
Cassat, J. E., & Skaar, E. P. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.04.010 · Cited by 1,214 · see citing works
Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U. E., Cekici, A., Meyer, K. C., Birrer, P., Bellon, G., Berger, J., Weiß, T., et al. (2002) · Journal of Clinical Investigation · doi:10.1172/jci13870 · Cited by 1,100 · see citing works
Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K. C., Birrer, P., Bellon, G., Berger, J., Weiss, T., et al. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0213870 · Cited by 932 · 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
Pseudomonas Aeruginosa Biofilms in Cystic fibrosis
Høiby, N., Ciofu, O., & Bjarnsholt, T. (2010) · Future Microbiology · doi:10.2217/fmb.10.125 · Cited by 687 · see citing works
Iron-Source Preference of <i>Staphylococcus aureus</i> Infections
Skaar, E. P., Humayun, M., Bae, T., DeBord, K. L., & Schneewind, O. (2004) · Science · doi:10.1126/science.1099930 · Cited by 440 · see citing works
Bacterial ferrous iron transport: the Feo system
Lau, C. K. Y., Krewulak, K. D., & Vogel, H. J. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv049 · Cited by 428 · 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
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
Functional and clinical aspects of the myelomonocyte protein calprotectin.
Johne, B., Fagerhol, M. K., Lyberg, T., Prydz, H., Brandtzaeg, P., Naess‐Andresen, C. F., & Dale, I. (1997) · Molecular Pathology · doi:10.1136/mp.50.3.113 · Cited by 380 · see citing works
Molecular Mechanisms of <i>Staphylococcus aureus</i> Iron Acquisition
Hammer, N. D., & Skaar, E. P. (2011) · Annual Review of Microbiology · doi:10.1146/annurev-micro-090110-102851 · Cited by 379 · see citing works
Ochsner, U. A., Johnson, Z., & Vasil, M. L. (2000) · Microbiology · doi:10.1099/00221287-146-1-185 · Cited by 310 · see citing works
<i>Staphylococcus aureus</i> IsdB Is a Hemoglobin Receptor Required for Heme Iron Utilization
Torres, V. J., Pishchany, G., Humayun, M., Schneewind, O., & Skaar, E. P. (2006) · Journal of Bacteriology · doi:10.1128/jb.01335-06 · Cited by 302 · 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
Self-citationPseudomonas aeruginosa transcriptome during human infection
Cornforth, D. M., Dees, J. L., Ibberson, C. B., Huse, H., Mathiesen, I. H. M., Kirketerp‐Møller, K., Wolcott, R. D., Rumbaugh, K. P., Bjarnsholt, T., & Whiteley, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717525115 · Cited by 270 · 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
A Staphylococcus aureus Regulatory System that Responds to Host Heme and Modulates Virulence
Torres, V. J., Stauff, D. L., Pishchany, G., Bezbradica, J. S., Gordy, L. E., Iturregui, J., Anderson, K. L., Dunman, P. M., Joyce, S., & Skaar, E. P. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.03.001 · Cited by 241 · see citing works
Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition
Wang, Y., Wilks, J. C., Danhorn, T., Ramos, I., Croal, L., & Newman, D. K. (2011) · Journal of Bacteriology · doi:10.1128/jb.00396-11 · Cited by 239 · see citing works
Role of Iron Uptake Systems in Pseudomonas aeruginosa Virulence and Airway Infection
Minandri, F., Imperi, F., Frangipani, E., Bonchi, C., Visaggio, D., Facchini, M., Pasquali, P., Bragonzi, A., & Visca, P. (2016) · Infection and Immunity · doi:10.1128/iai.00098-16 · Cited by 228 · see citing works
The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin
Clarke, S. R., Mohamed, R., Bian, L., Routh, A. F., Kokai-Kun, J. F., Mond, J. J., Tarkowski, A., & Foster, S. J. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.04.005 · Cited by 225 · cited 5× · see citing works
“In a systemic infection model, S. aureus isdB was differentially expressed in various tissues, indicating different degrees of iron starvation in distinct parts of the body, and a lower bacterial burden was observed in the heart for ΔisdB relative to the parent strain Newman (43).”
BackgroundInfluentialMetal limitation and toxicity at the interface between host and pathogen
Becker, K. W., & Skaar, E. P. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12087 · Cited by 223 · see citing works
The Influence of Iron on Pseudomonas aeruginosa Physiology
Oglesby, A. G., Farrow, J. M., Lee, J., Tomaras, A. P., Greenberg, E. P., Pesci, E. C., & Vasil, M. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m707840200 · Cited by 222 · see citing works
Self-citationKehl-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
Transition Metal Sequestration by the Host-Defense Protein Calprotectin
Zygiel, E. M., & Nolan, E. M. (2018) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-062917-012312 · Cited by 187 · see citing works
Self-citationCAS agar diffusion assay for the measurement of siderophores in biological fluids
Shin, S. H., Lim, Y., Lee, S. E., Yang, N. W., & Rhee, J. H. (2001) · Journal of Microbiological Methods · doi:10.1016/s0167-7012(00)00229-3 · Cited by 176 · see citing works
Recinos, D. A., Sekedat, M. D., Hernandez, A., Cohen, T. S., Sakhtah, H., Prince, A. S., Price‐Whelan, A., & Dietrich, L. E. P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213901109 · Cited by 167 · see citing works
Marvig, R. L., Damkiær, S., Khademi, S. M. H., Markussen, T. M., Molin, S., & Jelsbak, L. (2014) · mBio · doi:10.1128/mbio.00966-14 · Cited by 164 · see citing works
Diaz-Ochoa, V. E., Lam, D., Lee, C. S., Klaus, S., Behnsen, J., Liu, J. Z., Chim, N., Nuccio, S.-P., Rathi, S. G., Mastroianni, J. R., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.05.005 · Cited by 164 · see citing works
Calcium Ion Gradients Modulate the Zinc Affinity and Antibacterial Activity of Human Calprotectin
Brophy, M. B., Hayden, J. A., & Nolan, E. M. (2012) · Journal of the American Chemical Society · doi:10.1021/ja307974e · Cited by 156 · see citing works
Self-citationDamron, F. H., Oglesby, A. G., Wilks, A., & Barbier, M. (2016) · Scientific Reports · doi:10.1038/srep39172 · Cited by 156 · see citing works
Self-citationSputum and serum calprotectin are useful biomarkers during CF exacerbation
Gray, R. D., Imrie, M., Boyd, A., Porteous, D. J., Innes, J. A., & Greening, A. P. (2010) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2010.01.005 · Cited by 139 · see citing works
Wakeman, C. A., Moore, J. L., Noto, M. J., Zhang, Y., Singleton, M. D., Prentice, B. M., Gilston, B. A., Doster, R. S., Gaddy, J. A., Chazin, W. J., et al. (2016) · Nature Communications · doi:10.1038/ncomms11951 · Cited by 137 · see citing works
Dieppois, G., Ducret, V., Caille, O., & Perron, K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038148 · Cited by 132 · see citing works
Nguyen, A. T., O’Neill, M. J., Watts, A. M., Robson, C. L., Lamont, I. L., Wilks, A., & Oglesby, A. G. (2014) · Journal of Bacteriology · doi:10.1128/jb.01491-14 · Cited by 132 · see citing works
Self-citationManganese acquisition and homeostasis at the host-pathogen interface
Lisher, J. P., & Giedroc, D. P. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00091 · Cited by 127 · 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 · cited 2× · see citing works
“We chose to perform these studies using CDM, which contains 300 nM manganese, 5 μM iron, and 6 μM zinc because it is a defined medium that lacks heme (29).”
MethodSelf-citationGarcia, Y. M., Barwinska‐Sendra, A., Tarrant, E., Skaar, E. P., Waldron, K. J., & Kehl‐Fie, T. E. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006125 · Cited by 124 · see citing works
Konings, A. F., Martin, L. W., SHARPLES, K. J., Roddam, L. F., Latham, R. D., Reid, D. W., & Lamont, I. L. (2013) · Infection and Immunity · doi:10.1128/iai.00418-13 · Cited by 121 · see citing works
Extracellular Heme Uptake and the Challenge of Bacterial Cell Membranes
Huang, W., & Wilks, A. (2017) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060815-014214 · Cited by 105 · see citing works
Iron depletion enhances production of antimicrobials by Pseudomonas aeruginosa
Nguyen, A. T., Jones, J. W., Ruge, M. A., Kane, M. A., & Oglesby-Sherrouse, A. G. (2015) · Journal of Bacteriology · doi:10.1128/jb.00072-15 · Cited by 88 · see citing works
Self-citation<i>Staphylococcus aureus</i> haem oxygenases are differentially regulated by iron and haem
Reniere, M. L., & Skaar, E. P. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06363.x · Cited by 86 · see citing works
Ahlgren, H. G., Benedetti, A., Landry, J., Bernier, J., Matouk, E., Radzioch, D., Lands, L. C., Rousseau, S., & Nguyen, D. M. (2015) · BMC Pulmonary Medicine · doi:10.1186/s12890-015-0062-7 · Cited by 78 · see citing works
Pishchany, G., Dickey, S. E., & Skaar, E. P. (2009) · Infection and Immunity · doi:10.1128/iai.01531-08 · Cited by 77 · see citing works
Radin, J. N., Kelliher, J. L., Solórzano, P. K. P., & Kehl‐Fie, T. E. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1006040 · Cited by 77 · see citing works
Pseudomonas aeruginosa,Staphylococcus aureus, and Fluoroquinolone Use
MacDougall, C., Harpe, S. E., Powell, J. P., Johnson, C. K., Edmond, M. B., & Polk, R. E. (2005) · Emerging infectious diseases · doi:10.3201/eid1108.050116 · Cited by 76 · see citing works
Zygiel, E. M., Nelson, C. E., Brewer, L. K., Oglesby-Sherrouse, A. G., & Nolan, E. M. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006819 · Cited by 76 · see citing works
Self-citationWang, J., Lonergan, Z. R., Gonzalez-Gutierrez, G., Nairn, B. L., Maxwell, C. N., Zhang, Y., Andreini, C., Karty, J. A., Chazin, W. J., Trinidad, J. C., et al. (2019) · Cell chemical biology · doi:10.1016/j.chembiol.2019.02.011 · Cited by 76 · see citing works
Iron accumulates in the lavage and explanted lungs of cystic fibrosis patients
Ghio, A. J., Roggli, V. L., Soukup, J. M., Richards, J. H., Randell, S. H., & Muhlebach, M. S. (2012) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2012.10.010 · Cited by 75 · see citing works
Regulation of Pseudomonas aeruginosa Virulence by Distinct Iron Sources
Reinhart, A. A., & Oglesby, A. G. (2016) · Genes · doi:10.3390/genes7120126 · Cited by 70 · see citing works
Self-citationCho, H., Jeong, D., Liu, Q., Yeo, W., Vogl, T., Skaar, E. P., Chazin, W., & Bae, T. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005026 · Cited by 69 · see citing works
Djapgne, L., Panja, S., Brewer, L. K., Gans, J. H., Kane, M. A., Woodson, S. A., & Oglesby, A. G. (2018) · Journal of Bacteriology · doi:10.1128/jb.00704-17 · Cited by 63 · see citing works
Self-citationTranscriptome Analysis of Pseudomonas aeruginosa Cultured in Human Burn Wound Exudates
Gonzalez, M. R., Ducret, V., Leoni, S., Fleuchot, B., Jafari, P., Raffoul, W., Applegate, L. A., Que, Y., & Perron, K. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00039 · Cited by 53 · see citing works
A Heme-responsive Regulator Controls Synthesis of Staphyloferrin B in Staphylococcus aureus
Laakso, H. A., Marolda, C. L., Pinter, T. B., Stillman, M. J., & Heinrichs, D. E. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.696625 · Cited by 52 · see citing works
Siderophores of the Human Pathogenic Fluorescent Pseudomonads.
Budzikiewicz, H. (2001) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026013395560 · Cited by 41 · see citing works
Radin, J. N., Zhu, J., Brazel, E. B., McDevitt, C. A., & Kehl‐Fie, T. E. (2018) · Infection and Immunity · doi:10.1128/iai.00642-18 · Cited by 41 · see citing works
Iron and CF‐related anemia: Expanding clinical and biochemical relationships
Gifford, A. H., Miller, S., Jackson, B. P., Hampton, T. H., O’Toole, G. A., Stanton, B. A., & Parker, H. W. (2010) · Pediatric Pulmonology · doi:10.1002/ppul.21335 · Cited by 39 · see citing works
Park, R., Sun, H., Choi, M., Bai, Y.-H., & Shin, S. (2005) · PubMed · Cited by 37 · see citing works
Evaluation of some Staphylococcus aureus iron-regulated proteins as vaccine targets
Ster, C., Beaudoin, F., Diarra, M. S., Jacques, M., Malouin, F., & Lacasse, P. (2010) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2010.03.010 · Cited by 34 · see citing works
Exploring Iron Withholding by the Innate Immune Protein Human Calprotectin
Zygiel, E. M., & Nolan, E. M. (2019) · Accounts of Chemical Research · doi:10.1021/acs.accounts.9b00250 · Cited by 33 · see citing works
Self-citationGlasser, N. R., Hunter, R. C., Liou, T. G., & Newman, D. K. (2019) · PLoS ONE · doi:10.1371/journal.pone.0226578 · Cited by 20 · see citing works
Preparation and Iron Redox Speciation Study of the Fe(II)-Binding Antimicrobial Protein Calprotectin
Hadley, R. C., & Nolan, E. M. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9030-6_25 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Nutritional immunity: the battle for nutrient metals at the host–pathogen interface
Murdoch, C. C., & Skaar, E. P. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00745-6 · Cited by 701 · see citing works
Key players in the regulation of iron homeostasis at the host-pathogen interface
Ullah, I., & Lang, M. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1279826 · Cited by 76 · see citing works
van Dijk, M. C., de Kruijff, R. M., & Hagedoorn, P.-L. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.857237 · Cited by 41 · see citing works
Motz, R. N., Guo, C., Sargun, A., Walker, G. T., Sassone‐Corsi, M., Raffatellu, M., & Nolan, E. M. (2024) · Journal of the American Chemical Society · doi:10.1021/jacs.3c14490 · Cited by 35 · see citing works
Self-citationNelson, C. E., Huang, W., Zygiel, E. M., Nolan, E. M., Kane, M. A., & Oglesby, A. G. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.00519-21 · Cited by 24 · see citing works
Self-citationHuang, Y., Li, L., Li, Y., Lu, N., Qin, H., Wang, R., Li, W., Cheng, Z., Li, Z., Kang, P., et al. (2024) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2024.05.007 · Cited by 21 · see citing works
Metal sequestration by S100 proteins in chemically diverse environments
Rosen, T., Wang, K.-K. A., & Nolan, E. M. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2021.12.006 · Cited by 19 · see citing works
Self-citationIron Metabolism of the Skin: Recycling versus Release
Surbek, M., Sukseree, S., & Eckhart, L. (2023) · Metabolites · doi:10.3390/metabo13091005 · Cited by 19 · see citing works
de Lima, V. M., Batista, B. B., & da Silva Neto, J. F. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.873536 · Cited by 17 · see citing works
Bacterial Responses to Iron Withholding by Calprotectin
Obisesan, A. O., Zygiel, E. M., & Nolan, E. M. (2021) · Biochemistry · doi:10.1021/acs.biochem.1c00572 · Cited by 13 · see citing works
Self-citationSouche, A., Vandenesch, F., Doléans-Jordheim, A., & Moreau, K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076609 · Cited by 12 · see citing works
Intersection of the microbiome and immune metabolism in lupus
Garcia, A. C., Six, N., Ma, L., & Morel, L. M. (2024) · Immunological Reviews · doi:10.1111/imr.13360 · Cited by 11 · see citing works
Enriquez, K. T., Plummer, W. D., Neufer, P. D., Chazin, W., Dupont, W. D., & Skaar, E. P. (2023) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2023.106808 · Cited by 7 · see citing works
Yan, Z., Xia, L., Xu, X., MA, B., Yuan, X., Yang, K., Li, K., Ye, X., Zhang, L., & Chen, T. (2023) · Chemical Biology & Drug Design · doi:10.1111/cbdd.14322 · Cited by 7 · see citing works
Zhang, W., Ma, Y., Xie, Y., Liu, X., Tan, L., Zhao, J., Ni, Y., Wang, Z., Li, C., & Xu, B. (2024) · Food Microbiology · doi:10.1016/j.fm.2024.104685 · Cited by 7 · see citing works
Weiner, J. M., Lee, W. H., Nolan, E. M., & Oglesby, A. G. (2025) · Journal of Bacteriology · doi:10.1128/jb.00029-25 · Cited by 7 · see citing works
Self-citationLee, W. H., Oglesby, A. G., & Nolan, E. M. (2025) · mSystems · doi:10.1128/msystems.00576-25 · Cited by 6 · see citing works
Self-citationIron Sequestration by Murine Calprotectin Induces Starvation Responses in Pseudomonas aeruginosa
Peet, J. J. Y., Phan, A. D., Oglesby, A. G., & Nolan, E. M. (2024) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.3c00539 · Cited by 5 · see citing works
Self-citationHeme and immunity: The heme oxygenase dichotomy
Perry, M., & Hamza, I. (2025) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2025.112844 · Cited by 5 · see citing works
Dual species biofilms are enhanced by metabolite cross-feeding
Brunson, D. N., Lam, L. N., & Lemos, J. A. C. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.07.003 · Cited by 4 · see citing works
Perera, Y. R., Enriquez, K. T., Rodriguez, A., Garcia, V., Akizuki, T., Naretto, A., Togashi, M., Guillen, R., Skaar, E. P., & Chazin, W. (2025) · Protein Science · doi:10.1002/pro.70294 · Cited by 4 · see citing works
Lee, W. H., Zygiel, E. M., Lee, C. H., Oglesby, A. G., & Nolan, E. M. (2025) · mBio · doi:10.1128/mbio.03846-24 · Cited by 4 · see citing works
Self-citationEdache, E. I. (2022) · Journal of Virology and Viral Diseases · doi:10.54289/jvvd2200106 · Cited by 4 · see citing works
Almeida, M. R., Videira, M. A. M., Lima, J. C., & Saraiva, L. M. (2025) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2025.112878 · Cited by 4 · see citing works
The Pseudomonas aeruginosa PrrF sRNAs promote biofilm formation at body temperaturePreprint
Chourashi, R., Weiner, J. M., Hoang, T.-M., Ouattara, K. O., & Oglesby, A. G. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.11.628005 · Cited by 2 · see citing works
Self-citationThe Pseudomonas aeruginosa PrrF sRNAs and PqsA promote biofilm formation at body temperature
Chourashi, R., Weiner, J. M., Hoang, T.-M., Ouattara, K. O., & Oglesby, A. G. (2026) · Journal of Bacteriology · doi:10.1128/jb.00507-25 · Cited by 4 · see citing works
Self-citationXiao, J., Wang, Y., Chen, H., Bu, F., Xu, W., Qiu, S., Kang, Y., Wang, D., Wu, H., Hu, Z., et al. (2026) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2026.141645 · Cited by 1 · see citing works
Angeli, S., Rossi, C. S., Colasanto, G., Spizzichino, S., Rosignoli, S., Giorgi, A., Cutruzzolà, F., Paone, A., Tramonti, A., Contestabile, R., et al. (2026) · Journal of Bacteriology · doi:10.1128/jb.00370-25 · Cited by 1 · see citing works
Wang, L., Wang, T., & Zhao, Y. (2026) · Animals and zoonoses. · doi:10.1016/j.azn.2026.07.003 · Cited by 1 · see citing works
Steck, V., McIlvin, M. R., Stefanides, A., Webb, E. A., & Saito, M. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.27.701802
Biological and clinical significance of iron in Pseudomonas aeruginosa biofilms
Weiner, J. M., Chourashi, R., Ouattara, K. O., & Oglesby, A. G. (2026) · Journal of Bacteriology · doi:10.1128/jb.00598-25
Self-citationZhu, J., Wu, B., Luo, M., Peng, Y., Yang, F., Liu, L., Wang, Z., & Huang, D. (2026) · Chemical Engineering Journal · doi:10.1016/j.cej.2026.178732
Cao, J., Zhang, G., Xue, D., Gao, D., Li, X., Guo, J., & Dai, P. (2026) · Microbial Genomics · doi:10.1099/mgen.0.001854
The role of the respiratory microbiome in acute and chronic respiratory diseases
Heinzinger, L. R., Segal, L. N., & Dickson, R. P. (2026) · Nature Reviews Microbiology · doi:10.1038/s41579-026-01377-w
Debley, E., Rao, G., Bhadra, M., Nguyen, T., Shearer, J., Britt, R. D., & Nolan, E. M. (2026) · Journal of the American Chemical Society · doi:10.1021/jacs.6c12304
Self-citation
- Authors
- Zygiel, E. M., Obisesan, A. O., Nelson, C. E., Oglesby, A. G., & Nolan, E. M.
- Affiliations
- Massachusetts Institute of Technology (US)
- University of Maryland, Baltimore (US)
- Corresponding author
- Oglesby, Amanda G.
- Nolan, Elizabeth M.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2021-01
- Volume
- 296
- Pages
- 100160
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC7948498
- OpenAlex
- W3109184006
- Cited by
- 36
- References
- 63
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 6 · 2023: 5 · 2022: 6 · 2021: 3
- FWCI
- 2.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Institutes of Health
- 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 › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- heme uptake, calprotectin, iron starvation, Pseudomonas aeruginosa, Staphylococcus aureus, iron sequestration, innate immunity, bacterial iron acquisition, host-pathogen interaction, iron starvation response, siderophores, ferrous iron uptake
- MeSH terms
- Adaptation, Physiological, Bacterial Proteins, Binding, Competitive, Carrier Proteins, Heme, Humans, Iron, Protein Binding, Pseudomonas aeruginosa, Staphylococcus aureus, Stress, Physiological, Gene Expression Regulation, Bacterial, Siderophores, Leukocyte L1 Antigen Complex, Host-Pathogen Interactions, Bacterial Load
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review