Mycobacterial P1-Type ATPases Mediate Resistance to Zinc Poisoning in Human Macrophages
Open accessAbstract
Mycobacterium tuberculosis thrives within macrophages by residing in phagosomes and preventing them from maturing and fusing with lysosomes. A parallel transcriptional survey of intracellular mycobacteria and their host macrophages revealed signatures of heavy metal poisoning. In particular, mycobacterial genes encoding heavy metal efflux P-type ATPases CtpC, CtpG, and CtpV, and host cell metallothioneins and zinc exporter ZnT1, were induced during infection. Consistent with this pattern of gene modulation, we observed a burst of free zinc inside macrophages, and intraphagosomal zinc accumulation within a few hours postinfection. Zinc exposure led to rapid CtpC induction, and ctpC deficiency caused zinc retention within the mycobacterial cytoplasm, leading to impaired intracellular growth of the bacilli. Thus, the use of P(1)-type ATPases represents a M. tuberculosis strategy to neutralize the toxic effects of zinc in macrophages. We propose that heavy metal toxicity and its counteraction might represent yet another chapter in the host-microbe arms race.
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?
Loss of Zn detoxification machinery in several bacterial pathogens, including Group A and B streptococci, M. tuberculosis and S. pneumoniae, results in decreased intracellular survival or in vivo survival in mouse models of infection.
“Loss of Zn detoxification machinery in several bacterial pathogens, including Group A and B streptococci 166 , M. tuberculosis and S. pneumoniae , results in decreased intracellular survival 167-170 or in vivo survival in mouse models of infection 169 .”
From Nutritional immunity: the battle for nutrient metals at the host–pathogen interface (2022) · cites this paper as [167]
M. tuberculosis expresses p-type ATPase to promote zinc efflux and resist metal intoxication.
“As with copper, M. tuberculosis express p-type ATPase to promote zinc efflux and to resist metal intoxication (239, 242).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [242]
Transcriptional profiling of M. tuberculosis in human macrophages identified signs of metal intoxication in bacteria and in the host, revealing a burst of free zinc in macrophages and intraphagosomal zinc accumulation.
“Transcriptional profiling of M. tuberculosis in human macrophages identified signs of metal intoxication in bacteria and in the host, revealing a burst of free zinc in macrophages and intraphagosomal zinc accumulation (18).”
From Transition Metals and Virulence in Bacteria (2016) · cites this paper as [18]
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
Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence
Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., et al. (1998) · Nature · doi:10.1038/31159 · Cited by 7,847 · see citing works
Exaptation—a missing term in the science of form
Gould, S. J., & Vrba, E. S. (1982) · Paleobiology · doi:10.1017/s0094837300004310 · Cited by 5,136 · see citing works
The Essential Toxin: Impact of Zinc on Human Health
Plum, L. M., Rink, L., & Haase, H. (2010) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph7041342 · Cited by 1,577 · see citing works
Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg
Vidal, S. M., Malo, D., Vogan, K., Skamene, E., & Gros, P. (1993) · Cell · doi:10.1016/0092-8674(93)90135-d · Cited by 1,104 · see citing works
Synthetic fluorescent sensors for studying the cell biology of metals
Domaille, D. W., Que, E. L., & Chang, C. J. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.69 · Cited by 1,080 · see citing works
Armstrong, J. A., & Hart, P. D. (1971) · The Journal of Experimental Medicine · doi:10.1084/jem.134.3.713 · Cited by 991 · see citing works
Regulation of metallothionein gene expression by oxidative stress and metal ions
Andrews, G. K. (2000) · Biochemical Pharmacology · doi:10.1016/s0006-2952(99)00301-9 · Cited by 834 · see citing works
Mammalian Zinc Transporters: Nutritional and Physiologic Regulation
Lichten, L. A., & Cousins, R. J. (2009) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-033009-083312 · Cited by 732 · 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
Zinc is a novel intracellular second messenger
Yamasaki, S., Sakata-Sogawa, K., Hasegawa, A., Suzuki, T., Kabu, K., Sato, E., Kurosaki, T., Yamashita, S., Tokunaga, M., Nishida, K., et al. (2007) · Journal of Cell Biology · doi:10.1083/jcb.200702081 · Cited by 592 · see citing works
De Voss, J. J., Rutter, K., Schroeder, B. G., Su, H., Zhu, Y., & Barry, C. E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1252 · Cited by 532 · see citing works
A Role for the ATP7A Copper-transporting ATPase in Macrophage Bactericidal Activity
White, C., Lee, J., Kambe, T., Fritsche, K., & Petris, M. J. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.070201 · Cited by 524 · see citing works
Graham, J. E., & Clark‐Curtiss, J. E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11554 · Cited by 450 · see citing works
Wagner, D., Maser, J. M., Lai, B. C. H., Cai, Z., Barry, C. E., zu Bentrup, K. H., Russell, D. G., & Bermudez, L. E. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.3.1491 · Cited by 430 · see citing works
Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis
Pelicic, V., Jackson, M., Reyrat, J., Jacobs, W. R., Gicquel, B., & Guilhot, C. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10955 · Cited by 423 · see citing works
Self-citationThe Function of Zinc Metallothionein: A Link between Cellular Zinc and Redox State
Maret, W. (2000) · Journal of Nutrition · doi:10.1093/jn/130.5.1455s · Cited by 417 · see citing works
Gee, K. R., Zhou, Z., Qian, W., & Kennedy, R. T. (2002) · Journal of the American Chemical Society · doi:10.1021/ja011774y · Cited by 406 · see citing works
The structure and function of heavy metal transport P1B-ATPases
ARGÜELLO, J. M., Eren, E., & González‐Guerrero, M. (2007) · BioMetals · doi:10.1007/s10534-006-9055-6 · Cited by 391 · see citing works
A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis
Vandal, O. H., Pierini, L. M., Schnappinger, D., Nathan, C. F., & Ehrt, S. (2008) · Nature Medicine · doi:10.1038/nm.1795 · Cited by 368 · see citing works
Mycobacterium tuberculosis and the environment within the phagosome
Rohde, K. H., Yates, R. M., Purdy, G. E., & Russell, D. G. (2007) · Immunological Reviews · doi:10.1111/j.1600-065x.2007.00547.x · Cited by 361 · see citing works
Toll-like receptor–mediated regulation of zinc homeostasis influences dendritic cell function
Kitamura, H., Morikawa, H., Kamon, H., Iguchi, M., Hojyo, S., Fukada, T., Yamashita, S., Kaisho, T., Akira, S., Murakami, M., et al. (2006) · Nature Immunology · doi:10.1038/ni1373 · Cited by 355 · see citing works
CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator
Liu, T., Ramesh, A., Ma, Z., Ward, S. K., Zhang, L., George, G. N., Talaat, A. M., Sacchettini, J. C., & Giedroc, D. P. (2007) · Nature Chemical Biology · doi:10.1038/nchembio844 · Cited by 338 · see citing works
Intracellular zinc homeostasis and zinc signaling
Murakami, M., & Hirano, T. (2008) · Cancer Science · doi:10.1111/j.1349-7006.2008.00854.x · Cited by 333 · see citing works
Copper resistance is essential for virulence of <i>Mycobacterium tuberculosis</i>
Wolschendorf, F., Ackart, D., Shrestha, T. B., Hascall-Dove, L., Nolan, S., Lamichhane, G., Wang, Y., Bossmann, S. H., Basaraba, R. J., & Niederweis, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009261108 · Cited by 332 · see citing works
Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition
Siegrist, M. S., Unnikrishnan, M., McConnell, M. J., Borowsky, M. L., Cheng, T., Siddiqi, N., Fortune, S. M., Moody, D. B., & Rubin, E. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900589106 · Cited by 329 · see citing works
Cellular zinc sensors: MTF-1 regulation of gene expression
Andrews, G. K. (2001) · BioMetals · doi:10.1023/a:1012932712483 · Cited by 325 · see citing works
Rodríguez, G. M., & Smith, I. (2005) · Journal of Bacteriology · doi:10.1128/jb.188.2.424-430.2006 · Cited by 257 · see citing works
Oxidative Stress Activates Metal-responsive Transcription Factor-1 Binding Activity
Dalton, T. P., Li, Q., Bittel, D., Liang, L., & Andrews, G. K. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.42.26233 · Cited by 237 · see citing works
Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-γ expression in activated human T cells
Aydemir, T. B., Liuzzi, J. P., McClellan, S., & Cousins, R. J. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.1208759 · Cited by 229 · see citing works
Glutathione and Transition-Metal Homeostasis in Escherichia coli
Helbig, K., Bleuel, C., Krauss, G.-J., & Nies, D. H. (2008) · Journal of Bacteriology · doi:10.1128/jb.00271-08 · Cited by 218 · see citing works
Karyadi, E., West, C. E., Schultink, W., Nelwan, R. H. H., Gross, R., Amin, Z., Dolmans, W. M. V., Schlebusch, H., & van der Meer, J. W. M. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/75.4.720 · Cited by 209 · 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
CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis
Ward, S. K., Abomoelak, B., Hoye, E. A., Steinberg, H. N., & Talaat, A. M. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07273.x · Cited by 198 · see citing works
Protection against zinc toxicity by metallothionein and zinc transporter 1
Palmiter, R. D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401022101 · Cited by 197 · see citing works
Tailleux, L., Waddell, S. J., Pelizzola, M., Mortellaro, A., Withers, M., Tanne, A. J., Castagnoli, P. R., Gicquel, B., Stoker, N. G., Butcher, P. D., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001403 · Cited by 197 · see citing works
Self-citationIron-cofactored Superoxide Dismutase Inhibits Host Responses to Mycobacterium tuberculosis
Edwards, K. M., Cynamon, M. H., Voladri, R. K. R., Hager, C., DeStefano, M. S., Tham, K. T., LAKEY, D. L., Bochan, M. R., & Kernodle, D. S. (2001) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.164.12.2106093 · Cited by 196 · see citing works
Caminero, J. A., PENA, M. J., Campos-Herrero, M. I., RODRÍGUEZ, J. C., GARCÍA, I., Cabrera, P., Lafoz, C., Samper, S., Takiff, H. E., AFONSO, O., et al. (2001) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.164.7.2101031 · Cited by 179 · see citing works
Regulation of T cell receptor signaling by activation-induced zinc influx
Yu, M., Lee, W., Tomar, D., Pryshchep, S., Cześnikiewicz‐Guzik, M., Lamar, D. L., Li, G., Singh, K., Tian, L., Weyand, C. M., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20100031 · Cited by 168 · see citing works
Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry
Plüddemann, A., Mukhopadhyay, S., & Gordon, S. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00989.x · Cited by 162 · see citing works
Macrophage nutriprive antimicrobial mechanisms
Appelberg, R. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0206079 · Cited by 145 · see citing works
Cadmium Toxicity in Glutathione Mutants ofEscherichia coli
Helbig, K., Große, C., & Nies, D. H. (2008) · Journal of Bacteriology · doi:10.1128/jb.00272-08 · Cited by 113 · see citing works
Chan, H., Babayan, V., Blyumin, E., Gandhi, C., Hak, K., Harake, D. E., Kumar, K., Lee, P., Li, T. T., Liu, H. Y., et al. (2010) · Microbial Physiology · doi:10.1159/000319588 · Cited by 110 · see citing works
The many niches and strategies used by pathogenic mycobacteria for survival within host macrophages
de Chastellier, C. (2009) · Immunobiology · doi:10.1016/j.imbio.2008.12.005 · Cited by 109 · see citing works
A Cadmium-Lead-sensing ArsR-SmtB Repressor with Novel Sensory Sites
Cavet, J. S., Graham, A. I., Meng, W., & Robinson, N. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307877200 · Cited by 79 · see citing works
Beard, S. J., Hughes, M., & Poole, R. K. (1995) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1995.tb07778.x · Cited by 76 · see citing works
Chaperone-mediated Cu+ Delivery to Cu+ Transport ATPases
González‐Guerrero, M., Hong, D., & ARGÜELLO, J. M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.016329 · Cited by 59 · see citing works
Immersion autometallographic tracing of zinc ions in Alzheimer beta-amyloid plaques
Stoltenberg, M., Bruhn, M., Søndergaard, C. S., Doering, P., West, M. J., Larsen, A., Troncoso, J. C., & Danscher, G. (2005) · Histochemistry and Cell Biology · doi:10.1007/s00418-005-0787-0 · Cited by 56 · see citing works
Green, J. A., Lewin, S. R., Wightman, F., Lee, M., Ravindran, T., & Paton, N. I. (2005) · PubMed · Cited by 38 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Nutritional immunity: transition metals at the pathogen–host interface
Hood, M. I., & Skaar, E. P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2836 · Cited by 1,535 · see citing works
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
Metal homeostasis and resistance in bacteria
Chandrangsu, P., Rensing, C., & Helmann, J. D. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.15 · Cited by 812 · see citing works
The Role of Zinc in Antiviral Immunity
Read, S. A., Obeid, S., Ahlenstiel, C., & Ahlenstiel, G. (2019) · Advances in Nutrition · doi:10.1093/advances/nmz013 · Cited by 754 · see citing works
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
Mycobacterium tuberculosis: success through dormancy
Gengenbacher, M., & Kaufmann, S. H. E. (2012) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2012.00331.x · Cited by 698 · see citing works
Virulence factors of the Mycobacterium tuberculosis complex
Forrellad, M. A., Klepp, L. I., Gioffré, A., y García, J. S., Morbidoni, H. R., Santangelo, M. D. L. P., Cataldi, A. A., & Bigi, F. (2013) · Virulence · doi:10.4161/viru.22329 · Cited by 646 · see citing works
Zinc in Wound Healing Modulation
Lin, P.-H., Sermersheim, M., Li, H., Lee, P. H. U., Steinberg, S. M., & Ma, J. (2017) · Nutrients · doi:10.3390/nu10010016 · Cited by 643 · see citing works
Immunometabolism at the interface between macrophages and pathogens
Russell, D. G., Huang, L., & VanderVen, B. C. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0124-9 · Cited by 461 · see citing works
Transition Metals and Virulence in Bacteria
Palmer, L. D., & Skaar, E. P. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-120215-035146 · Cited by 449 · see citing works
The Role of Copper and Zinc Toxicity in Innate Immune Defense against Bacterial Pathogens
Djoko, K. Y., Ong, C.-L. Y., Walker, M. J., & McEwan, A. G. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.647099 · Cited by 417 · see citing works
Chen, B., Yu, P., Chan, W. N., Xie, F., Zhang, Y., Liang, L., Leung, K. T., Lo, K. W., Yu, J., Tse, G. M. K., et al. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01679-y · Cited by 420 · see citing works
Immune Response to Mycobacterium tuberculosis: A Narrative Review
de Martino, M., Lodi, L., Galli, L., & Chiappini, E. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00350 · Cited by 356 · see citing works
Zinc signals and immune function
Haase, H., & Rink, L. (2013) · BioFactors · doi:10.1002/biof.1114 · Cited by 305 · see citing works
Multiple Toxin-Antitoxin Systems in Mycobacterium tuberculosis
Sala, A. J., Bordes, P., & Genevaux, P. (2014) · Toxins · doi:10.3390/toxins6031002 · Cited by 264 · see citing works
Gerwien, F., Skrahina, V., Kasper, L., Hube, B., & Brunke, S. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux050 · Cited by 246 · see citing works
Multiple impacts of zinc on immune function
Haase, H., & Rink, L. (2014) · Metallomics · doi:10.1039/c3mt00353a · Cited by 237 · see citing works
Metallothioneins: Emerging Modulators in Immunity and Infection
Vignesh, K. S., & Deepe, G. S. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18102197 · Cited by 231 · see citing works
Subramanian Vignesh, K., Landero Figueroa, J. A., Porollo, A., Caruso, J. A., & Deepe, G. S. (2013) · Immunity · doi:10.1016/j.immuni.2013.09.006 · Cited by 230 · see citing works
Transposon-mediated site-specific recombination: A defined in vitro system
Reed, R. R. (1981) · Cell · doi:10.1016/0092-8674(81)90178-1 · Cited by 224 · see citing works
Mycobacteria, metals, and the macrophage
Neyrolles, O., Wolschendorf, F., Mitra, A., & Niederweis, M. (2015) · Immunological Reviews · doi:10.1111/imr.12265 · Cited by 217 · see citing works
Self-citationMetal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper
Stafford, S. L., Bokil, N. J., Achard, M. E. S., Kapétanovic, R., Schembri, M. A., McEwan, A. G., & Sweet, M. J. (2013) · Bioscience Reports · doi:10.1042/bsr20130014 · Cited by 205 · see citing works
Eat Prey, Live: Dictyostelium discoideum As a Model for Cell-Autonomous Defenses
Dunn, J. D., Bosmani, C., Barisch, C., Raykov, L., Lefrançois, L. H., Cardenal‐Muñoz, E., López-Jiménez, A. T., & Soldati, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01906 · Cited by 186 · see citing works
Antimicrobial Mechanisms of Macrophages and the Immune Evasion Strategies of Staphylococcus aureus
Flannagan, R. S., Heit, B., & Heinrichs, D. E. (2015) · Pathogens · doi:10.3390/pathogens4040826 · Cited by 195 · see citing works
Bacterial Strategies to Maintain Zinc Metallostasis at the Host-Pathogen Interface
Capdevila, D. A., Wang, J., & Giedroc, D. P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.742023 · Cited by 181 · see citing works
Tuberculosis and the art of macrophage manipulation
Upadhyay, S., Mittal, E., & Philips, J. A. (2018) · Pathogens and Disease · doi:10.1093/femspd/fty037 · Cited by 178 · see citing works
The Role of Zinc and Zinc Homeostasis in Macrophage Function
Gao, H., Dai, W., Zhao, L., Min, J.-X., & Wang, F.-D. (2018) · Journal of Immunological Research · doi:10.1155/2018/6872621 · Cited by 159 · see citing works
Neutrophil extracellular traps enhance macrophage killing of bacterial pathogens
Monteith, A. J., Miller, J. M., Maxwell, C. N., Chazin, W., & Skaar, E. P. (2021) · Science Advances · doi:10.1126/sciadv.abj2101 · Cited by 167 · see citing works
Strategies for the development of metalloimmunotherapies
Sun, X., Zhou, X., Shi, X., Abed, O. A., An, X., Lei, Y. L., & Moon, J. J. (2024) · Nature Biomedical Engineering · doi:10.1038/s41551-024-01221-7 · Cited by 181 · see citing works
Inducible antibacterial responses in macrophages
Sweet, M. J., Ramnath, D., Singhal, A., & Kapétanovic, R. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-01080-y · Cited by 163 · see citing works
Molecular basis of mycobacterial survival in macrophages
Awuh, J. A., & Flo, T. H. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2422-8 · Cited by 155 · see citing works
The innate immune response in human tuberculosis
Lerner, T. R., Borel, S., & Gutierrez, M. G. (2015) · Cellular Microbiology · doi:10.1111/cmi.12480 · Cited by 145 · see citing works
The Role of Nutrition in COVID-19 Susceptibility and Severity of Disease: A Systematic Review
James, P. T., Ali, Z., Armitage, A. E., Bonell, A., Cerami, C., Drakesmith, H., Jobe, M., Jones, K. S., Liew, Z., Moore, S. E., et al. (2021) · The Journal of Nutrition · doi:10.1093/jn/nxab059 · Cited by 147 · see citing works
Metals as phagocyte antimicrobial effectors
Sheldon, J. R., & Skaar, E. P. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.04.002 · Cited by 143 · see citing works
Nutrient Zinc at the Host–Pathogen Interface
Lonergan, Z. R., & Skaar, E. P. (2019) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2019.06.010 · Cited by 129 · see citing works
Metallothionein 1: A New Spotlight on Inflammatory Diseases
Dai, H., Wang, L., Li, L., Huang, Z. W., & Ye, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.739918 · Cited by 143 · see citing works
Bacterial Metabolism Shapes the Host–Pathogen Interface
Passalacqua, K. D., Charbonneau, M., & O’Riordan, M. X. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0027-2015 · Cited by 143 · see citing works
Role of Calprotectin in Withholding Zinc and Copper from Candida albicans
Besold, A. N., Gilston, B. A., Radin, J. N., Ramsoomair, C. K., Culbertson, E. M., Li, C. X., Cormack, B. P., Chazin, W., Kehl‐Fie, T. E., & Culotta, V. (2017) · Infection and Immunity · doi:10.1128/iai.00779-17 · Cited by 134 · see citing works
An Antimicrobial Role for Zinc in Innate Immune Defense Against Group A Streptococcus
Ong, C.-L. Y., Gillen, C. M., Barnett, T. C., Walker, M. J., & McEwan, A. G. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu053 · Cited by 124 · see citing works
Antimicrobial Susceptibility Testing of Antimicrobial Peptides to Better Predict Efficacy
Mercer, D. K., Torres, M. D. T., Duay, S. S., Lovie, E., Simpson, L. W., von Köckritz‐Blickwede, M., de la Fuente‐Núñez, C., O′Neil, D. A., & Angeles-Boza, A. M. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00326 · Cited by 136 · see citing works
Resistance mechanisms of Mycobacterium tuberculosis against phagosomal copper overload
Rowland, J. L., & Niederweis, M. (2012) · Tuberculosis · doi:10.1016/j.tube.2011.12.006 · Cited by 131 · see citing works
The ESX-3 Secretion System Is Necessary for Iron and Zinc Homeostasis in Mycobacterium tuberculosis
Serafini, A., Pisu, D., Palù, G., Rodriguez, G. M., & Manganelli, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078351 · Cited by 131 · see citing works
Gleason, J. E., Galaleldeen, A., Peterson, R. L., Taylor, A. B., Holloway, S. P., Waninger‐Saroni, J., Cormack, B. P., Cabelli, D. E., Hart, P. J., & Culotta, V. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400137111 · Cited by 127 · see citing works
Fungal zinc metabolism and its connections to virulence
Staats, C. C., Kmetzsch, L., Schrank, A., & Vainstein, M. H. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00065 · Cited by 119 · see citing works
The role of metal ions in the virulence and viability of bacterial pathogens
Neville, S. L. (2019) · Biochemical Society Transactions · doi:10.1042/bst20180275 · Cited by 114 · see citing works
Metallobiology of host–pathogen interactions: an intoxicating new insight
Botella, H., Stadthagen, G., Lugo-Villarino, G., de Chastellier, C., & Neyrolles, O. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.01.005 · Cited by 111 · see citing works
Self-citationCompetition for zinc binding in the host-pathogen interaction
Cerasi, M., Ammendola, S., & Battistoni, A. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00108 · Cited by 111 · see citing works
Antimicrobial Resistance inListeriaSpecies
Luque-Sastre, L., Arroyo, C., Fox, E. M., McMahon, B. J., Bai, L., Li, F., & Fanning, S. (2018) · Microbiology Spectrum · doi:10.1128/microbiolspec.arba-0031-2017 · Cited by 108 · see citing works
Zinc disrupts central carbon metabolism and capsule biosynthesis in Streptococcus pyogenes
Ong, C.-L. Y., Walker, M. J., & McEwan, A. G. (2015) · Scientific Reports · doi:10.1038/srep10799 · Cited by 107 · see citing works
Mycobacterium tuberculosis MetabolismPreprint
Warner, D. F. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a021121 · Cited by 102 · see citing works
Mycobacteria and the Intraphagosomal Environment: Take It With a Pinch of Salt(s)!
Soldati, T., & Neyrolles, O. (2012) · Traffic · doi:10.1111/j.1600-0854.2012.01358.x · Cited by 106 · see citing works
Self-citationZinc: Multidimensional Effects on Living Organisms
Cuajungco, M. P., Ramirez, M. S., & Tolmasky, M. E. (2021) · Biomedicines · doi:10.3390/biomedicines9020208 · Cited by 105 · see citing works
Anticytolytic Screen Identifies Inhibitors of Mycobacterial Virulence Protein Secretion
Rybniker, J., Chen, J. M., Sala, C., Hartkoorn, R. C., Vocat, A., Benjak, A., Boy‐Röttger, S., Zhang, M., Székely, R., Greff, Z., et al. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.09.008 · Cited by 98 · see citing works
Focarelli, F., Giachino, A., & Waldron, K. J. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010617 · Cited by 97 · see citing works
Mastropasqua, M. C., D’Orazio, M., Cerasi, M., Pacello, F., Gismondi, A., Canini, A., Canuti, L., Consalvo, A., Ciavardelli, D., Chirullo, B., et al. (2017) · Molecular Microbiology · doi:10.1111/mmi.13834 · Cited by 93 · see citing works
Zinc depletion induces ribosome hibernation in mycobacteria
Li, Y., Sharma, M. R., Koripella, R. K., Yang, Y., Kaushal, P. S., Lin, Q., Wade, J. T., Gray, T. A., Derbyshire, K. M., Agrawal, R. K., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1804555115 · Cited by 94 · see citing works
Padilla-Benavides, T., Long, J. E., Raimunda, D., Sassetti, C. M., & Argüello, J. M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.448175 · Cited by 91 · see citing works
Zinc excess increases cellular demand for iron and decreases tolerance to copper in Escherichia coli
Xu, Z., Wang, P., Wang, H., Yu, Z. H., Au-Yeung, H. Y., Hirayama, T., Sun, H., & Yan, A. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.010023 · Cited by 91 · see citing works
Targeting the Proteostasis Network for Mycobacterial Drug Discovery
Lupoli, T. J., Vaubourgeix, J., Burns-Huang, K. E., & Gold, B. S. (2018) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.7b00231 · Cited by 89 · see citing works
Healy, C. M., Muñoz‐Wolf, N., Strydom, J., Faherty, L., Williams, N. C., Kenny, S., Donnelly, S. C., & Cloonan, S. M. (2021) · Respiratory Research · doi:10.1186/s12931-021-01722-y · Cited by 89 · 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
Harris, N. C., Sato, M., Herman, N. A., Twigg, F. F., Cai, W., Liu, J., Zhu, X., Downey, J., Khalaf, R., Martin, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705016114 · Cited by 87 · 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
Leblanc, C., Prudhomme, T., Tabouret, G., Ray, A. A., Burbaud, S., Cabantous, S., Mourey, L., Guilhot, C., & Chalut, C. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003097 · Cited by 86 · see citing works
Salina, E. G., Waddell, S. J., Hoffmann, N. A., Rosenkrands, I., Butcher, P. D., & Kaprelyants, A. S. (2014) · Open Biology · doi:10.1098/rsob.140106 · Cited by 82 · see citing works
Self-citationBettencourt, P., Marion, S., Pires, D., Santos, L. F., Lastrucci, C., Carmo, N., Blake, J., Benes, V., Griffiths, G., Neyrolles, O., et al. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00019 · Cited by 84 · see citing works
Self-citationThe impact of metal availability on immune function during infection
Monteith, A. J., & Skaar, E. P. (2021) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2021.08.004 · Cited by 83 · see citing works
Iron and zinc exploitation during bacterial pathogenesis
Ma, L. M., Terwilliger, A. L., & Maresso, A. W. (2015) · Metallomics · doi:10.1039/c5mt00170f · Cited by 83 · see citing works
Bacterial Killing in Macrophages and Amoeba: Do they all use a Brass Dagger?
German, N., Doyscher, D., & Rensing, C. (2013) · Future Microbiology · doi:10.2217/fmb.13.100 · Cited by 79 · see citing works
Zinc is an important inter-kingdom signal between the host and microbe
Xia, P., Lian, S., Wu, Y., Yan, L., Quan, G., & Zhu, G. (2021) · Veterinary Research · doi:10.1186/s13567-021-00913-1 · Cited by 78 · see citing works
Metallothionein: a Potential Link in the Regulation of Zinc in Nutritional Immunity
Rahman, M. T., & Karim, M. M. (2018) · Biological Trace Element Research · doi:10.1007/s12011-017-1061-8 · Cited by 77 · see citing works
Toward a Molecular Understanding of Metal Transport by P1B-Type ATPases
Rosenzweig, A. C., & ARGÜELLO, J. M. (2012) · Current topics in membranes · doi:10.1016/b978-0-12-394390-3.00005-7 · Cited by 71 · see citing works
Vignesh, K. S., & Deepe, G. S. (2016) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2016.02.020 · Cited by 72 · see citing works
The roles of transition metals in the physiology and pathogenesis of Streptococcus pneumoniae
Honsa, E. S., Johnson, M. D. L., & Rosch, J. W. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00092 · Cited by 69 · see citing works
Haeili, M., Moore, C. V., Davis, C. J. C., Cochran, J. B., Shah, S., Shrestha, T. B., Zhang, Y., Bossmann, S. H., Benjamin, W. H., Kutsch, O., et al. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02316-13 · Cited by 70 · see citing works
Biphasic zinc compartmentalisation in a human fungal pathogen
Crawford, A., Lehtovirta‐Morley, L. E., Alamir, O., Niemiec, M. J., Alawfi, B. S., Alsarraf, M., Skrahina, V., Costa, A. C. B. P., Anderson, A., Yellagunda, S., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007013 · Cited by 68 · see citing works
Ellis, T., Chiappi, M., García‐Trenco, A., Al‐Ejji, M., Sarkar, S., Georgiou, T. K., Shaffer, M. S. P., Tetley, T. D., Schwander, S., Ryan, M. P., et al. (2018) · ACS Nano · doi:10.1021/acsnano.7b08264 · Cited by 68 · see citing works
Stocks, C. J., Phan, M., Achard, M. E. S., Nhu, N. T. K., Condon, N. D., Gawthorne, J. A., Lo, A. W. H., Peters, K. M., McEwan, A. G., Kapétanovic, R., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820870116 · Cited by 66 · see citing works
Tolerance and Persistence to Drugs: A Main Challenge in the Fight Against Mycobacterium tuberculosis
Boldrin, F., Provvedi, R., Mazzabò, L. C., Segafreddo, G., & Manganelli, R. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01924 · Cited by 68 · see citing works
Dietary zinc and the control of Streptococcus pneumoniae infection
Eijkelkamp, B. A., Morey, J. R., Neville, S. L., Tan, A., Pederick, V. G., Cole, N., Singh, P., Ong, C. Y., de Vega, R. G., Clases, D., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007957 · Cited by 63 · see citing works
Zinc Exploitation by Pathogenic Fungi
Wilson, D., Citiulo, F., & Hube, B. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003034 · Cited by 62 · see citing works
The Role of Intermetal Competition and Mis-Metalation in Metal Toxicity
Barwinska‐Sendra, A., & Waldron, K. J. (2017) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2017.01.003 · Cited by 62 · see citing works
Sanson, M. A., Makthal, N., Flores, A. R., Olsen, R. J., Musser, J. M., & Kumaraswami, M. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1304 · Cited by 60 · see citing works
Chandrangsu, P., & Helmann, J. D. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006515 · Cited by 60 · see citing works
Raimunda, D., Long, J. E., Padilla‐Benavides, T., Sassetti, C. M., & ARGÜELLO, J. M. (2013) · Molecular Microbiology · doi:10.1111/mmi.12454 · Cited by 59 · see citing works
Single‐cell deconstruction of post‐sepsis skeletal muscle and adipose tissue microenvironments
Cho, D. S., Schmitt, R. E., Dasgupta, A., Ducharme, A. M., & Doles, J. D. (2020) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12596 · Cited by 57 · see citing works
Role in metal homeostasis of CtpD, a Co2+transporting P1B4‐ATPase ofMycobacterium smegmatis
Raimunda, D., Long, J. E., Sassetti, C. M., & ARGÜELLO, J. M. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08082.x · Cited by 57 · see citing works
Stocks, C. J., Schembri, M. A., Sweet, M. J., & Kapétanovic, R. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.4ri0917-358r · Cited by 56 · see citing works
Neyrolles, O., Mintz, E., & Catty, P. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00089 · Cited by 56 · see citing works
Self-citationBacterial Metallostasis: Metal Sensing, Metalloproteome Remodeling, and Metal Trafficking
Capdevila, D. A., Rondón, J. J., Edmonds, K. A., Rocchio, J. S., Dujovne, M. V., & Giedroc, D. P. (2024) · Chemical Reviews · doi:10.1021/acs.chemrev.4c00264 · Cited by 59 · see citing works
Huo, T., Liu, W., Guo, Y., Yang, C., Lin, J., & Rao, Z. (2015) · BMC Bioinformatics · doi:10.1186/s12859-015-0535-y · Cited by 56 · see citing works
Martin, C. J., Carey, A. F., & Fortune, S. M. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0533-1 · Cited by 57 · see citing works
Zinc limitation triggers anticipatory adaptations in Mycobacterium tuberculosis
Dow, A., Sule, P., O’Donnell, T. J., Burger, A., Mattila, J. T., Antonio, B., Vergara, K., Marcantonio, E., Adams, L. G., James, N., et al. (2021) · PLOS Pathogens · doi:10.1371/journal.ppat.1009570 · Cited by 55 · see citing works
New Insights into the Role of Zinc Acquisition and Zinc Tolerance in Group A Streptococcal Infection
Ong, C.-L. Y., Berking, O., Walker, M. J., & McEwan, A. G. (2018) · Infection and Immunity · doi:10.1128/iai.00048-18 · Cited by 54 · see citing works
Prišić, S., Hwang, H., Dow, A., Barnaby, O. S., Pan, T. S., Lonzanida, J. A., Chazin, W., Steen, H., & Husson, R. N. (2015) · Molecular Microbiology · doi:10.1111/mmi.13022 · Cited by 53 · see citing works
Bobrov, A. G., Kirillina, O. A., Fosso, M. Y., Fetherston, J. D., Miller, M. C., VanCleave, T. T., Burlison, J. A., Arnold, W. K., Lawrenz, M. B., Garneau‐Tsodikova, S., et al. (2017) · Metallomics · doi:10.1039/c7mt00126f · Cited by 53 · see citing works
Buglino, J. A., Sankhe, G. D., Lazar, N., Bean, J. M., & Glickman, M. S. (2021) · eLife · doi:10.7554/elife.65351 · Cited by 53 · see citing works
Iron in intracellular infection: to provide or to deprive?
Silva-Gomes, S., Vale-Costa, S., Appelberg, R., & Gomes, M. S. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00096 · Cited by 51 · see citing works
Zinc Acquisition: A Key Aspect in Aspergillus fumigatus Virulence
Amich, J., & Calera, J. A. (2014) · Mycopathologia · doi:10.1007/s11046-014-9764-2 · Cited by 53 · see citing works
Larsen, S. E., Williams, B. D., Rais, M., Coler, R. N., & Baldwin, S. L. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.840225 · Cited by 50 · see citing works
- Authors
- Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., Wang, C., Tailleux, L., Tilleul, S., Charrière, G. M., Waddell, S. J., Foti, M., Lugo-Villarino, G., Gao, Q., Maridonneau-Parini, I., Butcher, P. D., Castagnoli, P. R., Gicquel, B., de Chastellier, C., & Neyrolles, O.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Institut Pasteur (FR)
- Brighton and Sussex Medical School (GB)
- University of Milano-Bicocca (IT)
- Shanghai Medical College of Fudan University (CN)
- St George's, University of London (GB)
- Singapore Immunology Network (SG)
- Corresponding author
- Neyrolles, Olivier
- ORCID
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 10
- Issue
- 3
- Pages
- 248-259
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3221041
- OpenAlex
- W2128702173
- Cited by
- 381
- References
- 48
- Citations by year
- 2026: 23 · 2025: 20 · 2024: 32 · 2023: 21 · 2022: 27 · 2021: 41 · 2020: 30 · 2019: 32 · 2018: 23 · 2017: 27 · 2016: 19 · 2015: 23 · 2014: 23 · 2013: 21 · 2012: 17
- FWCI
- 13.38
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Sussex Research Online (University of Sussex) (submittedVersion, cc-by)
- HAL (submittedVersion)
- HAL AMU (submittedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Wellcome Trust (086547)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Keywords
- Mycobacterium tuberculosis, zinc efflux, zinc toxicity, metallothionein, ZnT1, phagosome maturation, intracellular bacterial growth, macrophages
- MeSH terms
- Animals, Cells, Cultured, Female, Humans, Macrophages, Mice, Inbred BALB C, Mycobacterium tuberculosis, Tuberculosis, Zinc, Bacterial Proton-Translocating ATPases, Mice
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
