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The Human Innate Immune Protein Calprotectin Elicits a Multimetal Starvation Response in Pseudomonas aeruginosa
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Abstract
Transition metal nutrients are critical for growth and infection by all pathogens, and the innate immune system withholds these metals from pathogens to limit their growth in a strategy termed “nutritional immunity.” While multimetal depletion by the host is appreciated, the majority of studies have focused on individual metals. Here, we use the innate immune protein calprotectin (CP), which complexes with several metals, including iron (Fe), zinc (Zn), and manganese (Mn), and the opportunistic pathogen Pseudomonas aeruginosa to investigate multimetal starvation.
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“Subsequent proteomic analysis of the response of P. aeruginosa to CP demonstrated increased expression of proteins involved in pyoverdine-mediated Fe uptake in the presence of CP.35”
From Bacterial Responses to Iron Withholding by Calprotectin (2021) · cites this paper as [35]
In the citing paper
“While these findings support a CP-mediated Fe starvation and sparing responses in P. aeruginosa, the aforementioned proteomic analysis of P. aeruginosa indicated that CP did not affect many PrrF-dependent changes and thus appears to elicit an incomplete Fe-starvation response.35”
From Bacterial Responses to Iron Withholding by Calprotectin (2021) · cites this paper as [35]
In the citing paper
“The proteomic analysis of the effect of CP on the P. aeruginosa proteome also supported these findings; growth of P. aeruginosa under CP-treated and Fe-depleted conditions resulted in a downregulation of proteins involved in phenazine biosynthesis.35”
From Bacterial Responses to Iron Withholding by Calprotectin (2021) · cites this paper as [35]
In the citing paper
“In particular, CP treatment did not affect expression of many Fe-containing metabolic proteins, such as TCA cycle enzymes SdhABCD and AcnB, which are normally downregulated by PrrF sRNAs upon Fe limitation.35”
From Bacterial Responses to Iron Withholding by Calprotectin (2021) · cites this paper as [35]
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Citations
Cites
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
Lack 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 · cited 1×
“Moreover, bacterial pathogens exhibit varying nutritional requirements for transition metals 68 – for instance, some species have a high Fe requirement whereas others require substantially 69 more Mn (12, 13) – and are therefore likely to show species- and strain-specific responses to 70 host multi-metal withholding.”
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
Hassan, M.-E.-T., van der Lelie, D., Springael, D., Römling, U., Ahmed, N., & Mergeay, M. (1999) · Gene · doi:10.1016/s0378-1119(99)00349-2 · Cited by 165
ZnuA and zinc homeostasis in Pseudomonas aeruginosa
Pederick, V. G., Eijkelkamp, B. A., Begg, S. L., Ween, M. P., McAllister, L. J., Paton, J. C., & McDevitt, C. A. (2015) · Scientific Reports · doi:10.1038/srep13139 · Cited by 138 · cited 2×
“been shown under Zn(II)-limiting conditions, indicating a Zn(II)-sparing response (23, 26).”
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
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×
“145 aeruginosa and other pathogens (10, 40).”
Self-citationReinhart, A. A., Powell, D. A., Nguyen, A. T., O'Neill, M., Djapgne, L., Wilks, A., Ernst, R. K., & Oglesby-Sherrouse, A. G. (2015) · Infection and Immunity · doi:10.1128/iai.02707-14 · Cited by 97
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
Self-citationMolecular Evolution of Transition Metal Bioavailability at the Host–Pathogen Interface
Antelo, G. T., Vila, A. J., Giedroc, D. P., & Capdevila, D. A. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2020.08.001 · Cited by 63
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Cited by
Flannagan, R. S., Brozyna, J. R., Kumar, B., Adolf, L. A., Power, J. J., Heilbronner, S., & Heinrichs, D. E. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.101823 · Cited by 23
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
Self-citation(2024) · doi:10.1128/mbio.02395-24 · Cited by 12
Metadata
- Authors
- Nelson, C. E., Huang, W., Zygiel, E. M., Nolan, E. M., Kane, M. A., & Oglesby, A. G.
- Venue
- Microbiology Spectrum
- Publisher
- American Society for Microbiology
- Published
- 2021-10-31
- Volume
- 9
- Issue
- 2
- ISSN
- 2165-0497
- Cited by
- 28
- References
- 11
- Language
- en
- Licence
- creativecommons.org/licenses/by/4.0/ (vor)
- journals.asm.org/non-commercial-tdm-license (tdm)
- Funders
- National Institutes of Health (R01 GM126376)
- University of Maryland Mass Spectrometry Center (SOP1841-IQB2014)
- HHS | National Institutes of Health (T32 AI095190)
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