Breathing life into pathogens: the influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract: Oxygen and intestinal pathogens
Abstract
The gastrointestinal tract provides a variety of environmental challenges to any bacterium seeking to successfully colonize or cause disease in a host. A major obstacle is the varied oxygen concentrations encountered at different sites in the intestine. Here we review the mechanisms bacterial pathogens utilize to sense oxygen within the gastrointestinal tract, and recent insights into how this acts as a signal to trigger virulence and to modulate host responses.
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The O2 level at the luminal surface of the intestinal tract has been reported to range from 2% to 7%.
“typically, the O2 level at the luminal surface has been reported to range from 2% to 7% [19–21].”
From Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions (2015) · cites this paper as [20]
Cites
The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis
Maxwell, P. H., Wiesener, M. S., Chang, G.-W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., & Ratcliffe, P. J. (1999) · Nature · doi:10.1038/20459 · Cited by 5,180 · see citing works
Lupp, C., Robertson, M. L., Wickham, M. E., Sekirov, I., Champion, O. L., Gaynor, E. C., & Finlay, B. B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.06.010 · Cited by 1,310 · see citing works
Gut inflammation provides a respiratory electron acceptor for Salmonella
Winter, S., Thiennimitr, P., Winter, M. G., Butler, B. P., Huseby, D. L., Crawford, R. W., Russell, J. M., Bevins, C. L., Adams, L. G., Tsolis, R. M., et al. (2010) · Nature · doi:10.1038/nature09415 · Cited by 1,271 · 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 1,133 · see citing works
Stecher, B., Robbiani, R., Walker, A. W., Westendorf, A. M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A. J., Buer, J., Parkhill, J., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050244 · Cited by 1,048 · see citing works
Hypoxia-Inducible Factor 1 (HIF-1) Pathway
Semenza, G. L. (2007) · Science s STKE · doi:10.1126/stke.4072007cm8 · Cited by 942 · 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
Continuous Recording of Blood Oxygen Tensions by Polarography
Clark, L. C., Wolf, R., Granger, D., & Taylor, Z. (1953) · Journal of Applied Physiology · doi:10.1152/jappl.1953.6.3.189 · Cited by 885 · see citing works
HIF-1α expression regulates the bactericidal capacity of phagocytes
Peyssonnaux, C., Datta, V., Cramer, T., Doedens, A. L., Theodorakis, E. A., Gallo, R. L., Hurtado‐Ziola, N., Nizet, V., & Johnson, R. S. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23865 · Cited by 702 · see citing works
Tuberculous Granulomas Are Hypoxic in Guinea Pigs, Rabbits, and Nonhuman Primates
Via, L. E., Lin, P. L., Ray, S. M., Carrillo, J., Allen, S. S., Eum, S. Y., Taylor, K. L., Klein, E. C., Manjunatha, U. H., Gonzales, J., et al. (2008) · Infection and Immunity · doi:10.1128/iai.01515-07 · Cited by 665 · see citing works
Greenberg, J. T., Monach, P. A., Chou, J. H., Josephy, P. D., & Demple, B. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6181 · Cited by 556 · see citing works
Lupp, C., Robertson, M. L., Wickham, M. E., Sekirov, I., Champion, O. L., Gaynor, E. C., & Finlay, B. B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.08.002 · Cited by 501 · see citing works
The ability of Salmonella to enter mammalian cells is affected by bacterial growth state.
Lee, C. A., & Falkow, S. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.11.4304 · Cited by 463 · see citing works
Macrophage responses to hypoxia: relevance to disease mechanisms
Lewis, J. S., Lee, J. A., Underwood, J. C. E., Harris, A. L., & Lewis, C. E. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.66.6.889 · Cited by 383 · see citing works
He, G., Shankar, R. A., Chzhan, M., Samouilov, A., Kuppusamy, P., & Zweier, J. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4586 · Cited by 383 · see citing works
Modulation of Shigella virulence in response to available oxygen in vivo
Marteyn, B., West, N. P., Browning, D. F., Cole, J. A., Shaw, J. G., Palm, F., Mounier, J., Prévost, M., Sansonetti, P. J., & Tang, C. M. (2010) · Nature · doi:10.1038/nature08970 · Cited by 323 · see citing works
Self-citationRegulation and Temporal Expression Patterns of Vibrio cholerae Virulence Genes during Infection
Lee, S. H., Hava, D. L., Waldor, M. K., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)81551-2 · Cited by 294 · see citing works
Respiration of <i>Escherichia coli</i> in the Mouse Intestine
Jones, S. A., Chowdhury, F. Z., Fabich, A. J., Anderson, A., Schreiner, D. M., House, A. L., Autieri, S. M., Leatham, M. P., Lins, J. J., Jorgensen, M., et al. (2007) · Infection and Immunity · doi:10.1128/iai.00484-07 · Cited by 223 · see citing works
Dual oxidase in mucosal immunity and host–microbe homeostasis
Bae, Y. S., Choi, M. K., & Lee, W. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.05.003 · Cited by 213 · see citing works
Motility allows S. Typhimurium to benefit from the mucosal defence
Stecher, B., Barthel, M., Schlumberger, M. C., Haeberli, L., Rabsch, W., Kremer, M., & Hardt, W. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01118.x · Cited by 198 · see citing works
Hypoxia causes an increase in phagocytosis by macrophages in a HIF-1α-dependent manner
Anand, R., Gribar, S. C., Li, J., Kohler, J. W., Branca, M. F., Dubowski, T. D., Sodhi, C. P., & Hackam, D. J. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0307195 · Cited by 192 · see citing works
Bekker, M., Alexeeva, S., Laan, W., Sawers, R. G., de Mattos, J. T., & Hellingwerf, K. J. (2009) · Journal of Bacteriology · doi:10.1128/jb.01156-09 · Cited by 153 · see citing works
Fink, R. C., Evans, M. R., Porwollik, S., Vázquez‐Torres, A., Jones‐Carson, J., Troxell, B., Libby, S. J., McClelland, M., & Hassan, H. M. (2007) · Journal of Bacteriology · doi:10.1128/jb.00726-06 · Cited by 149 · see citing works
Hypoxia-independent activation of HIF-1 by enterobacteriaceae and their siderophores
Hartmann, H., Eltzschig, H. K., Wurz, H., Hantke, K., Rakin, A., Yazdi, A. S., Matteoli, G., Bohn, E., Autenrieth, I. B., Karhausen, J., et al. (2008) · Gastroenterology · doi:10.1053/j.gastro.2007.12.008 · Cited by 143 · see citing works
Green, J. D., Crack, J. C., Thomson, A. J., et al. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.01.008 · Cited by 127 · see citing works
Kovacikova, G., Lin, W., & Skorupski, K. (2010) · Journal of Bacteriology · doi:10.1128/jb.00193-10 · Cited by 120 · see citing works
Macrophage activation by culture in an anoxic environment
Albina, J. E., Henry, W. L., Mastrofrancesco, B., Martin, B. A., & Reichner, J. S. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.9.4391 · Cited by 119 · see citing works
Melican, K., Boekel, J., Månsson, L., Sandoval, R. M., Tanner, G. A., Källskog, Ö., Palm, F., Molitoris, B. A., & Richter‐Dahlfors, A. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01182.x · Cited by 110 · see citing works
The aerobic/anaerobic interface
Sawers, R. G. (1999) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(99)80032-0 · Cited by 100 · see citing works
Chlamydia pneumoniaedirectly interferes with HIF-1α stabilization in human host cells
Rupp, J., Gieffers, J., Klinger, M. H. F., van Zandbergen, G., Wrase, R., Maass, M., Solbach, W., Deiwick, J., & Hellwig‐Bürgel, T. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00948.x · Cited by 95 · see citing works
The Global Regulator ArcA Modulates Expression of Virulence Factors in Vibrio cholerae
Sengupta, N., Paul, K., & Chowdhury, R. (2003) · Infection and Immunity · doi:10.1128/iai.71.10.5583-5589.2003 · Cited by 79 · see citing works
Edwards, J. C., Johnson, M. S., & Taylor, B. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05411.x · Cited by 69 · see citing works
Anaerobic Regulation of Shigella flexneri Virulence: ArcA Regulates fur and Iron Acquisition Genes
Boulette, M. L., & Payne, S. M. (2007) · Journal of Bacteriology · doi:10.1128/jb.00621-07 · Cited by 61 · see citing works
Schüller, S., & Phillips, A. D. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02216.x · Cited by 55 · see citing works
Müsken, A., Bielaszewska, M., Greune, L., et al. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02496-07 · Cited by 54 · see citing works
An Unexpected Role for Hypoxic Response: Oxygenation and Inflammation
Peyssonnaux, C., & Johnnson, R. S. (2004) · Cell Cycle · doi:10.4161/cc.3.2.687 · Cited by 40 · see citing works
Månsson, L., Melican, K., Molitoris, B. A., et al. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.01019.x · Cited by 36 · see citing works
Marrero, K., Sánchez, A., Rodríguez‐Ulloa, A., et al. (2008) · Research in Microbiology · doi:10.1016/j.resmic.2008.10.005 · Cited by 35 · see citing works
Ando, H., Abé, H., Sugimoto, N., et al. (2007) · Microbiology · doi:10.1099/mic.0.2006/000893-0 · Cited by 30 · see citing works
Role of anaerobiosis in virulence of Salmonella typhimuirium
Singh, R. D., Khullar, M., & Ganguly, N. K. (2000) · Molecular and Cellular Biochemistry · doi:10.1023/a:1026545630773 · Cited by 29 · see citing works
Unden, G. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00071-1 · Cited by 27 · see citing works
Handa, K., Ohmura, M., Nishime, C., et al. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-1241-1_61 · Cited by 10 · see citing works
Torres, L. N., & Filho, I. P. T. (2001) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2001000100017 · Cited by 5 · see citing works
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Tiso, M., & Schechter, A. N. (2015) · PLOS ONE · doi:10.1371/journal.pone.0119712 · Cited by 311 · see citing works
Anoxic Conditions Promote Species-Specific Mutualism between Gut Microbes <i>In Silico</i>
Heinken, A., & Thiele, I. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.00101-15 · Cited by 123 · see citing works
- Authors
- Marteyn, B., Scorza, F. B., Sansonetti, P. J., & Tang, C.
- Affiliations
- Imperial College London (GB)
- Institut Pasteur (FR)
- Venue
- Cellular Microbiology
- Publisher
- Wiley
- Published
- 2010-12-19
- Volume
- 13
- Issue
- 2
- Pages
- 171-176
- ISSN
- 1462-5814 (ISSN-L)
- OpenAlex
- W1836564745
- Cited by
- 102
- References
- 43
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 10 · 2023: 8 · 2022: 8 · 2021: 7 · 2020: 6 · 2019: 9 · 2018: 8 · 2017: 6 · 2016: 9 · 2015: 7 · 2014: 6 · 2013: 3 · 2012: 6
- FWCI
- 0.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cellular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- oxygen sensing, bacterial virulence, gastrointestinal tract, intestinal colonization, host-pathogen interaction, pathogenic bacteria, host immune response
- MeSH terms
- Animals, Bacteria, Humans, Oxygen, Virulence, Virulence Factors, Gastrointestinal Tract, Host-Pathogen Interactions, Immune Evasion
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