Neutrophils in tuberculosis: friend or foe?

Lowe, David M.; Redford, Paul S.; Wilkinson, Robert J.; O’Garra, Anne; Martineau, Adrian R.

doi:10.1016/j.it.2011.10.003

Cited by 312Tuberculosis Research and EpidemiologyImmune responses and vaccinationsNeutrophil, Myeloperoxidase and Oxidative Mechanisms

Neutrophils in tuberculosis: friend or foe?

Lowe, David M., Redford, Paul S., Wilkinson, Robert J., O’Garra, Anne, Martineau, Adrian R.·2012·Trends in Immunology

DOI 10.1016/j.it.2011.10.003

Open this paper in CoChat — free account

Abstract

Neutrophils are rapidly recruited to sites of mycobacterial infection, where they phagocytose bacilli. Whether neutrophils can kill mycobacteria in vivo probably depends on the tissue microenvironment, stage of infection, individual host, and infecting organism. The interaction of neutrophils with macrophages, as well as the downstream effects on T cell activity, could result in a range of outcomes from early clearance of infection to dissemination of viable bacteria together with an attenuated acquired immune response. In established disease, neutrophils accumulate in situations of high pathogen load or immunological dysfunction, and are likely to contribute to pathology. These activities may have clinical importance in terms of new treatments, targeted interventions and vaccine strategies.

Integrity signals

Registry

Crossref · 10.1016/j.it.2011.10.003

Cites

107 of 107 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

PMNs are important in containment of mycobacteria following their release from apoptotic/necrotic macrophages.
“PMNs are of importance in containment of mycobacteria following their release from apoptotic/necrotic macrophages (118, 119).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [119]

Neutrophils in the activation and regulation of innate and adaptive immunity
Mantovani, A., Cassatella, M. A., Costantini, C., & Jaillon, S. (2011) · Nature reviews. Immunology · doi:10.1038/nri3024 · Cited by 3,045 · see citing works
An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis
Berry, M. P. R., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A. A., Oni, T., Wilkinson, K. A., Banchereau, R., Skinner, J., Wilkinson, R. J., et al. (2010) · Nature · doi:10.1038/nature09247 · Cited by 1,898 · see citing works
Self-citation
Vitamin D3 Induces Autophagy in Human Monocytes/Macrophages via Cathelicidin
Yuk, J., Shin, D., Lee, H., Yang, C., Jin, H. S., Kim, K., Lee, Z., Lee, S.-H., Kim, J., & Jo, E. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.08.004 · Cited by 787 · see citing works
High-dose vitamin D3 during intensive-phase antimicrobial treatment of pulmonary tuberculosis: a double-blind randomised controlled trial
Martineau, A. R., Timms, P. M., Bothamley, G. H., Hanifa, Y., Islam, K., Claxton, A. P., Packe, G. E., Moore-Gillon, J. C., Darmalingam, M., Davidson, R. N., et al. (2011) · The Lancet · doi:10.1016/s0140-6736(10)61889-2 · Cited by 581 · see citing works
Self-citation
Mycobacterium tuberculosis Infects Dendritic Cells with High Frequency and Impairs Their Function In Vivo
Wolf, A. J., Linas, B. S., Trevejo-Nuñez, G., Kincaid, E., Tamura, T., Takatsu, K., & Ernst, J. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.4.2509 · Cited by 558 · see citing works
Neutrophils Are the Predominant Infected Phagocytic Cells in the Airways of Patients With Active Pulmonary TB
Eum, S.-Y., Kong, J.-H., Hong, M.-S., Lee, Y.-J., Kim, J.-H., Hwang, S.-H., Cho, S.-N., Via, L. E., & Barry, C. E. (2010) · Chest · doi:10.1378/chest.09-0903 · Cited by 548 · see citing works
IL-17, Produced by Lymphocytes and Neutrophils, Is Necessary for Lipopolysaccharide-Induced Airway Neutrophilia: IL-15 as a Possible Trigger
Ferretti, S., Bonneau, O., Dubois, G. R., Jones, C. E., & Trifilieff, A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.4.2106 · Cited by 542 · see citing works
IL-17-Mediated Regulation of Innate and Acquired Immune Response against Pulmonary Mycobacterium bovis Bacille Calmette-Guerin Infection
Umemura, M., Yahagi, A., Hamada, S., Begum, M. D., Watanabe, H., Kawakami, K., Suda, T., Sudo, K., Nakae, S., Iwakura, Y., et al. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.6.3786 · Cited by 516 · see citing works
Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guérin.
Molloy, A., Laochumroonvorapong, P., & Kaplan, G. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.180.4.1499 · Cited by 501 · see citing works
Neutrophil-mediated innate immune resistance to mycobacteria
Martineau, A. R., Newton, S. M., Wilkinson, K. A., Kampmann, B., Hall, B. M., Nawroly, N., Packe, G. E., Davidson, R. N., Griffiths, C. J., & Wilkinson, R. J. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31097 · Cited by 394 · see citing works
Self-citation
Regulation of neutrophils by interferon-γ limits lung inflammation during tuberculosis infection
Nandi, B., & Behar, S. M. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20110919 · Cited by 373 · see citing works
Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes
Abadie, V., Badell, E., Douillard, P., Ensergueix, D., Leenen, P. J. M., Tanguy, M., Fiette, L., Saeland, S., Gicquel, B., & Winter, N. (2005) · Blood · doi:10.1182/blood-2005-03-1281 · Cited by 356 · see citing works
Programmed death-1 (PD-1)–deficient mice are extraordinarily sensitive to tuberculosis
Lázár‐Molnár, E., Chen, B., Sweeney, K. A., Wang, E. J., Liu, W., Lin, J., Porcelli, S. A., Almo, S. C., Nathenson, S. G., & Jacobs, W. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007394107 · Cited by 339 · see citing works
CD4 T Cells Promote Rather than Control Tuberculosis in the Absence of PD-1–Mediated Inhibition
Barber, D. L., Mayer-Barber, K. D., Feng, C. G., Sharpe, A. H., & Sher, A. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1003304 · Cited by 329 · see citing works
When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system
Silva, M. T. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0809549 · Cited by 321 · see citing works
Clearance of apoptotic and necrotic cells and its immunological consequences
Krysko, D. V., D’Herde, K., & Vandenabeele, P. (2006) · Apoptosis · doi:10.1007/s10495-006-9527-8 · Cited by 316 · see citing works
Mechanisms for induction of acquired host immunity by neutrophil peptide defensins
Lillard, J. W., Boyaka, P. N., Chertov, O., Oppenheim, J. J., & McGhee, J. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.651 · Cited by 305 · see citing works
Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A
Santo, C. D., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R. G., Salio, M., Middleton, M. R., & Cerundolo, V. (2010) · Nature Immunology · doi:10.1038/ni.1942 · Cited by 304 · see citing works
Coactivation of Syk Kinase and MyD88 Adaptor Protein Pathways by Bacteria Promotes Regulatory Properties of Neutrophils
Zhang, X., Majlessi, L., Dériaud, E., Leclerc, C., & Lo‐Man, R. (2009) · Immunity · doi:10.1016/j.immuni.2009.09.016 · Cited by 302 · see citing works
Neutrophil Responses toMycobacterium tuberculosisInfection in Genetically Susceptible and Resistant Mice
Eruslanov, E. B., Lyadova, I. V., Kondratieva, T. K., Majorov, K. B., Scheglov, I. V., Orlova, M. O., & Apt, A. S. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1744-1753.2005 · Cited by 289 · see citing works
Neutrophils Play a Protective Nonphagocytic Role in SystemicMycobacterium tuberculosisInfection of Mice
Pedrosa, J., Saunders, B. M., Appelberg, R., Orme, I. M., Silva, M. T., & Cooper, A. M. (2000) · Infection and Immunity · doi:10.1128/iai.68.2.577-583.2000 · Cited by 283 · see citing works
Toll-like receptor pathways in the immune responses to mycobacteria
Quesniaux, V. F. J., Fremond, C., Jacobs, M., Parida, S. K., Nicolle, D. M., Yeremeev, V., Bihl, F., Erard, F., Botha, T., Drennan, M., et al. (2004) · Microbes and Infection · doi:10.1016/j.micinf.2004.04.016 · Cited by 280 · see citing works
Neutrophil extracellular traps are induced by Mycobacterium tuberculosis
Ramos-Kichik, V., Mondragón‐Flores, R., Mondragón-Castelán, M. E., González‐Pozos, S., Muñiz‐Hernández, S., Rojas-Espinosa, O., Chacón‐Salinas, R., Estrada-Parra, S. A., & Estrada‐García, I. (2008) · Tuberculosis · doi:10.1016/j.tube.2008.09.009 · Cited by 280 · see citing works
Macrophages Acquire Neutrophil Granules for Antimicrobial Activity against Intracellular Pathogens
Tan, B. H., Meinken, C., Bastian, M., Bruns, H., Legaspi, A., Ochoa, M. T., Krutzik, S. R., Bloom, B. R., Ganz, T., Modlin, R. L., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.3.1864 · Cited by 267 · see citing works
Identification of diagnostic markers for tuberculosis by proteomic fingerprinting of serum
Agranoff, D., Fernández-Reyes, D., Papadopoulos, M. C., Rojas, S. A., Herbster, M., Loosemore, A., Tarelli, E., Sheldon, J., Schwenk, A., Pollok, R., et al. (2006) · The Lancet · doi:10.1016/s0140-6736(06)69342-2 · Cited by 263 · see citing works
Programmed Death (PD)-1:PD-Ligand 1/PD-Ligand 2 Pathway Inhibits T Cell Effector Functions during Human Tuberculosis
Jurado, J. O., Alvarez, I. B., Pasquinelli, V., Martínez, G., Quiroga, M. F., Abbate, E. H., Musella, R. M., Chuluyán, E., & García, V. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.1.116 · Cited by 257 · see citing works
Pathological role of interleukin 17 in mice subjected to repeated BCG vaccination after infection with Mycobacterium tuberculosis
Cruz, A., Fraga, A. G., Fountain, J. J., Rangel‐Moreno, J., Torrado, E., Saraiva, M., Pereira, D. R., Randall, T. D., Pedrosa, J., Cooper, A. M., et al. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20100265 · Cited by 256 · see citing works
Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3‐signaling chemokines
Seiler, P. J., Aichele, P., Bandermann, S., Hauser, A. E., Lu, B., Gerard, N. P., Gerard, C. J., Ehlers, S., Mollenkopf, H., & Kaufmann, S. H. E. (2003) · European Journal of Immunology · doi:10.1002/eji.200323956 · Cited by 237 · see citing works
Enhanced protection to Mycobacterium tuberculosis infection in IL‐10‐deficient mice is accompanied by early and enhanced Th1 responses in the lung
Redford, P. S., Boonstra, A., Read, S., Pitt, J. M., Graham, C. M., Stavropoulos, E., Bancroft, G. J., & O’Garra, A. (2010) · European Journal of Immunology · doi:10.1002/eji.201040433 · Cited by 233 · see citing works
Self-citation
Lung Neutrophils Facilitate Activation of Naive Antigen-Specific CD4+ T Cells during Mycobacterium tuberculosis Infection
Blomgran, R., & Ernst, J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100001 · Cited by 230 · see citing works
NK Cell-Derived IFN-γ Differentially Regulates Innate Resistance and Neutrophil Response in T Cell-Deficient Hosts Infected with Mycobacterium tuberculosis
Feng, C. G., Kaviratne, M., Rothfuchs, A. G., Cheever, A. W., Hieny, S. E., Young, H. A., Wynn, T. A., & Sher, A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.7086 · Cited by 229 · see citing works
The adaptor molecule CARD9 is essential for tuberculosis control
Dorhoi, A., Desel, C., Yeremeev, V., Pradl, L., Brinkmann, V., Mollenkopf, H., Hanke, K., Groß, O., Ruland, J., & Kaufmann, S. H. E. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20090067 · Cited by 202 · see citing works
Mice Lacking Myeloid Differentiation Factor 88 Display Profound Defects in Host Resistance and Immune Responses to Mycobacterium avium Infection Not Exhibited by Toll-Like Receptor 2 (TLR2)- and TLR4-Deficient Animals
Feng, C. G., Scanga, C. A., Collazo, C. M., Cheever, A. W., Hieny, S. E., Caspar, P., & Sher, A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.9.4758 · Cited by 198 · see citing works
Mycobacterium tuberculosis Promotes Apoptosis in Human Neutrophils by Activating Caspase-3 and Altering Expression of Bax/Bcl-xL Via an Oxygen-Dependent Pathway
Perskvist, N., Long, M., Stendahl, O. I., & Zheng, L. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.12.6358 · Cited by 196 · see citing works
Local Immune Responses Correlate with Presentation and Outcome in Tuberculosis
Condos, R., Rom, W. N., LIU, Y. M., & Schluger, N. W. (1998) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.157.3.9705044 · Cited by 195 · see citing works
Mycobacterial Infection in TLR2 and TLR6 Knockout Mice
Sugawara, I., Yamada, H., Li, C., Mizuno, S., Takeuchi, O., & Akira, S. (2003) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2003.tb03404.x · Cited by 194 · see citing works
Neutrophils Influence the Level of Antigen Presentation during the Immune Response to Protein Antigens in Adjuvants
Yang, C.-W., Strong, B., Miller, M. J., & Unanue, E. R. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001289 · Cited by 179 · see citing works
Enhancement of Innate and Cell-Mediated Immunity by Antimycobacterial Antibodies
Vallière, S. D., Abate, G., Blazevic, A., Heuertz, R. M., & Hoft, D. F. (2005) · Infection and Immunity · doi:10.1128/iai.73.10.6711-6720.2005 · Cited by 173 · see citing works
Genetically Determined Susceptibility to Tuberculosis in Mice Causally Involves Accelerated and Enhanced Recruitment of Granulocytes
Keller, C., Hoffmann, R. F. G., Lang, R., Brandau, S., Hermann, C., & Ehlers, S. (2006) · Infection and Immunity · doi:10.1128/iai.00057-06 · Cited by 165 · see citing works
Tumor Necrosis Factor Alpha Stimulates Killing ofMycobacterium tuberculosisby Human Neutrophils
Kisich, K. O., Higgins, M. P., Diamond, G., & Heifets, L. B. (2002) · Infection and Immunity · doi:10.1128/iai.70.8.4591-4599.2002 · Cited by 157 · see citing works
Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: Apoptosis as infection-promoting factor
Laskay, T., van Zandbergen, G., & Solbach, W. (2008) · Immunobiology · doi:10.1016/j.imbio.2007.11.010 · Cited by 153 · see citing works
Chemokine secretion by human polymorphonuclear granulocytes after stimulation with Mycobacterium tuberculosis and lipoarabinomannan
Riedel, D., & Kaufmann, S. H. E. (1997) · Infection and Immunity · doi:10.1128/iai.65.11.4620-4623.1997 · Cited by 137 · see citing works
Killing of Mycobacterium tuberculosis by Neutrophils: A Nonoxidative Process
Jones, G. S., Amirault, H. J., & Andersen, B. R. (1990) · The Journal of Infectious Diseases · doi:10.1093/infdis/162.3.700 · Cited by 133 · see citing works
In vitro activity of the antimicrobial peptides human and rabbit defensins and porcine leukocyte protegrin against Mycobacterium tuberculosis
Miyakawa, Y., Ratnakar, P., Rao, A. G., et al. (1996) · Infection and Immunity · doi:10.1128/iai.64.3.926-932.1996 · Cited by 131 · see citing works
Rapid Neutrophil Response Controls Fast‐Replicating Intracellular Bacteria but Not Slow‐ReplicatingMycobacterium tuberculosis
Seiler, P. J., Aichele, P., Raupach, B., Odermatt, B., Steinhoff, U., & Kaufmann, S. H. E. (2000) · The Journal of Infectious Diseases · doi:10.1086/315278 · Cited by 129 · see citing works
Capacity of Human Neutrophils to Kill Mycobacterium tuberculosis
Brown, A. E., Holzer, T. J., & Andersen, B. R. (1987) · The Journal of Infectious Diseases · doi:10.1093/infdis/156.6.985 · Cited by 115 · see citing works
The Two-Domain LysX Protein of Mycobacterium tuberculosis Is Required for Production of Lysinylated Phosphatidylglycerol and Resistance to Cationic Antimicrobial Peptides
Maloney, E., Stankowska, D. L., Zhang, J., Fol, M., Cheng, Q.-J., Lun, S., Bishai, W. R., Rajagopalan, M. R., Chatterjee, D., & Madiraju, M. V. V. S. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000534 · Cited by 113 · see citing works
Macrophages exposed to Mycobacterium tuberculosis release chemokines able to recruit selected leucocyte subpopulations: focus on γδ cells
Ferrero, E., Biswas, P., Vettoretto, K., et al. (2003) · Immunology · doi:10.1046/j.1365-2567.2003.01600.x · Cited by 112 · see citing works
Programmed death ligand 1 is over‐expressed by neutrophils in the blood of patients with active tuberculosis
McNab, F. W., Berry, M. P. R., Graham, C. M., Bloch, S. A. A., Oni, T., Wilkinson, K. A., Wilkinson, R. J., Kon, O. M., Banchereau, J., Chaussabel, D., et al. (2011) · European Journal of Immunology · doi:10.1002/eji.201141421 · Cited by 110 · see citing works
Self-citation
Bronchoalveolar lavage, sputum and exhaled clinically relevant inflammatory markers: values in healthy adults
Balbi, B., Pignatti, P., Corradi, M., Baiardi, P., Bianchi, L. N. C., Brunetti, G., Radaeli, A., Moscato, G., Mutti, A., Spanevello, A., et al. (2007) · European Respiratory Journal · doi:10.1183/09031936.00112306 · Cited by 101 · see citing works
Expression of Chemokines and Induction of Rapid Cell Death in Human Blood Neutrophils by Mycobacterium tuberculosis
Kasahara, K., Sato, I., Ogura, K., Takeuchi, H. T., Kobayashi, K., & Adachi, M. (1998) · The Journal of Infectious Diseases · doi:10.1086/515585 · Cited by 97 · see citing works
Neutrophil-Mediated Mycobacteriocidal Immunity in the Lung duringMycobacterium bovisBCG Infection in C57BL/6 Mice
Fulton, S. A., Reba, S. M., Martin, T. D., & Boom, W. H. (2002) · Infection and Immunity · doi:10.1128/iai.70.9.5322-5327.2002 · Cited by 96 · see citing works
Mycobacterium bovis BCG‐infected neutrophils and dendritic cells cooperate to induce specific T cell responses in humans and mice
Morel, C., Badell, E., Abadie, V., Robledo-Sarmiento, M., Setterblad, N., Gluckman, J. C., Gicquel, B., Boudaly, S., & Winter, N. (2008) · European Journal of Immunology · doi:10.1002/eji.200737905 · Cited by 95 · see citing works
Role of Human Neutrophil Peptide–1 as a Possible Adjunct to Antituberculosis Chemotherapy
Kalita, A., Verma, I., & Khuller, G. K. (2004) · The Journal of Infectious Diseases · doi:10.1086/424463 · Cited by 93 · see citing works
Mycobacterium tuberculosis 19-kDa Lipoprotein Promotes Neutrophil Activation
Neufert, C. F., Pai, R. K., Noss, E. H., Berger, M., Boom, W. H., & Harding, C. V. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.3.1542 · Cited by 92 · see citing works
Fusion of Azurophil Granules with Phagosomes and Activation of the Tyrosine Kinase Hck Are Specifically Inhibited During Phagocytosis of Mycobacteria by Human Neutrophils
N’Diaye, E.-N., Darzacq, X., Astarie‐Dequeker, C., et al. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.9.4983 · Cited by 90 · see citing works
Antibacterial activity of human neutrophil peptide-1 against Mycobacterium tuberculosis H37Rv: in vitro and ex vivo study
Sharma, S., Verma, I., & Khuller, G. K. (2000) · European Respiratory Journal · doi:10.1034/j.1399-3003.2000.16a20.x · Cited by 89 · see citing works
Neutrophils recruited to the site ofMycobacterium bovisBCG infection undergo apoptosis and modulate lipid body biogenesis and prostaglandin E2production by macrophages
D’Ávila, H., Roque, N. R., Cardoso, R. M., Castro-Faria-Neto, H. C., Melo, R. C. N., & Bozza, P. T. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01233.x · Cited by 87 · see citing works
Neutrophils fromMycobacterium avium-Infected Mice Produce TNF-α, IL-12, and IL-1β and Have a Putative Role in Early Host Response
Petrofsky, M., & Bermudez, L. E. (1999) · Clinical Immunology · doi:10.1006/clim.1999.4709 · Cited by 86 · see citing works
Mycobacterium bovis Bacillus Calmette-Guérin Vaccination Mobilizes Innate Myeloid-Derived Suppressor Cells Restraining In Vivo T Cell Priming via IL-1R–Dependent Nitric Oxide Production
Martino, A., Badell, E., Abadie, V., Balloy, V., Chignard, M., Mistou, M., Combadière, B., Combadière, C., & Winter, N. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903348 · Cited by 86 · see citing works
Mycobacterium tuberculosisTriggers Apoptosis in Peripheral Neutrophils Involving Toll-Like Receptor 2 and p38 Mitogen Protein Kinase in Tuberculosis Patients
Alemán, M., Schierloh, P., de la Barrera, S., Musella, R. M., Saab, M. A., Baldini, M., Abbate, E. H., & Sasiain, M. D. C. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.5150-5158.2004 · Cited by 84 · see citing works
Predictors of Short-Term Prognosis in Patients with Pulmonary Tuberculosis
Barnes, P. F., Leedom, J. M., Chan, L. S., Wong, S. F., Shah, J. J., Vachon, L. A., Overturf, G. D., & Modlin, R. L. (1988) · The Journal of Infectious Diseases · doi:10.1093/infdis/158.2.366 · Cited by 83 · see citing works
Rab5a GTPase regulates fusion between pathogen-containing phagosomes and cytoplasmic organelles in human neutrophils
Perskvist, N., Roberg, K. B., Kulyté, A., & Stendahl, O. I. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.6.1321 · Cited by 81 · see citing works
Mycobacterium tuberculosis-induced apoptotic neutrophils trigger a pro-inflammatory response in macrophages through release of heat shock protein 72, acting in synergy with the bacteria
Persson, A., Blomgran, R., Rahman, S., Zheng, L., & Stendahl, O. I. (2007) · Microbes and Infection · doi:10.1016/j.micinf.2007.11.007 · Cited by 81 · see citing works
Therapeutic Potential of Human Neutrophil Peptide 1 against Experimental Tuberculosis
Sharma, S., Verma, I., & Khuller, G. K. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.2.639-640.2001 · Cited by 81 · see citing works
Rat Neutrophils Prevent the Development of Tuberculosis
Sugawara, I., Udagawa, T., & Yamada, H. (2004) · Infection and Immunity · doi:10.1128/iai.72.3.1804-1806.2004 · Cited by 80 · see citing works
Elevated Levels of α-Defensins in Plasma and BAL Fluid of Patients With Active Pulmonary Tuberculosis
Ashitani, J.-I., Mukae, H., Hiratsuka, T., et al. (2002) · CHEST Journal · doi:10.1378/chest.121.2.519 · Cited by 78 · see citing works
Airway epithelial cell signaling in response to bacterial pathogens
Gómez, M. I., & Prince, A. S. (2007) · Pediatric Pulmonology · doi:10.1002/ppul.20735 · Cited by 77 · see citing works
Evidence for activation of a respiratory burst in the interaction of human neutrophils with Mycobacterium tuberculosis
May, M. E., & Spagnuolo, P. J. (1987) · Infection and Immunity · doi:10.1128/iai.55.9.2304-2307.1987 · Cited by 76 · see citing works
Roles of calcium and annexins in phagocytosis and elimination of an attenuated strain ofMycobacterium tuberculosisin human neutrophils
Majeed, M., Perskvist, N., Ernst, J. D., et al. (1998) · Microbial Pathogenesis · doi:10.1006/mpat.1997.0200 · Cited by 75 · see citing works
Early Inhibition of Mycobacterial Growth by Human Alveolar Macrophages is not Due to Nitric Oxide
ASTON, C., Rom, W. N., Talbot, A. T., & Reibman, J. (1998) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.157.6.9705028 · Cited by 72 · see citing works
Human Neutrophils, Activated with Cytokines or Not, Do Not Kill Virulent Mycobacterium tuberculosis
Denis, M. (1991) · The Journal of Infectious Diseases · doi:10.1093/infdis/163.4.919 · Cited by 67 · see citing works
Pulmonary Immune Responses during Primary Mycobacterium bovis – Calmette-Guerin Bacillus Infection in C57Bl/6 Mice
Fulton, S. A., Martin, T. D., Redline, R. W., & Boom, W. H. (2000) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.22.3.3776 · Cited by 61 · see citing works
B Cells Delay Neutrophil Migration toward the Site of Stimulus: Tardiness Critical for Effective Bacillus Calmette-Guérin Vaccination against Tuberculosis Infection in Mice
Kondratieva, T. K., Rubakova, E. I., Linge, I. A., Evstifeev, V., Majorov, K. B., & Apt, A. S. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0902011 · Cited by 55 · see citing works
Guinea Pig Neutrophils Infected withMycobacterium tuberculosisProduce Cytokines Which Activate Alveolar Macrophages in Noncontact Cultures
Sawant, K. V., & McMurray, D. N. (2007) · Infection and Immunity · doi:10.1128/iai.00858-06 · Cited by 52 · see citing works
Mycobacterial Infection Primes T Cells and Macrophages for Enhanced Recruitment of Neutrophils
Appelberg, R. (1992) · Journal of Leukocyte Biology · doi:10.1002/jlb.51.5.472 · Cited by 51 · see citing works
Role of leukotrienes in killing of Mycobacterium bovis by neutrophils
Coffey, M., Phare, S. M., & Peters-Golden, M. L. (2004) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2004.03.012 · Cited by 50 · see citing works
Mechanisms of Polymorphonuclear Neutrophil–Mediated Induction of HIV‐1 Replication in Macrophages during Pulmonary Tuberculosis
Hoshino, Y., Hoshino, S., Gold, J. A., et al. (2007) · The Journal of Infectious Diseases · doi:10.1086/513438 · Cited by 50 · see citing works
Mycobacterium bovis bacille Calmette Guerin infection of human neutrophils induces CXCL8 secretion by MyD88-dependent TLR2 and TLR4 activation
Godaly, G., & Young, D. B. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00489.x · Cited by 48 · see citing works
Interleukin-8 enhances nonoxidative intracellular killing of Mycobacterium fortuitum by human granulocytes
Nibbering, P. H., Pos, O., Stevenhagen, A., et al. (1993) · Infection and Immunity · doi:10.1128/iai.61.8.3111-3116.1993 · Cited by 47 · see citing works
Interleukin (IL)-8 (CXCL8) induces cytokine expression and superoxide formation by guinea pig neutrophils infected with Mycobacterium tuberculosis
Lyons, M. J., Yoshimura, T., & McMurray, D. N. (2004) · Tuberculosis · doi:10.1016/j.tube.2003.09.003 · Cited by 45 · see citing works
Lactoferrin enhanced efficacy of the BCG vaccine to generate host protective responses against challenge with virulent Mycobacterium tuberculosis
Hwang, S., Wilk, K., Budnicka, M., Olsen, M. R., Bangale, Y. A., Hunter, R. L., Kruzel, M. L., & Actor, J. K. (2007) · Vaccine · doi:10.1016/j.vaccine.2007.07.005 · Cited by 44 · see citing works
Difference in neutrophil cytokine production induced by pathogenic and non‐pathogenic mycobacteria
Fäldt, J., Dahlgren, C., & Ridell, M. (2002) · Apmis · doi:10.1034/j.1600-0463.2002.1100901.x · Cited by 42 · see citing works
Mycobacterium bovisBCG Vaccination Augments Interleukin-8 mRNA Expression and Protein Production in Guinea Pig Alveolar Macrophages Infected withMycobacterium tuberculosis
Lyons, M. J., Yoshimura, T., & McMurray, D. N. (2002) · Infection and Immunity · doi:10.1128/iai.70.10.5471-5478.2002 · Cited by 42 · see citing works
In Tuberculous Pleural Effusions, Activated Neutrophils Undergo Apoptosis and Acquire a Dendritic Cell–Like Phenotype
Alemán, M., de la Barrera, S., Schierloh, P., et al. (2005) · The Journal of Infectious Diseases · doi:10.1086/431680 · Cited by 42 · see citing works
Spontaneous or Mycobacterium tuberculosis‐induced apoptotic neutrophils exert opposite effects on the dendritic cell‐mediated immune response
Alemán, M., de la Barrera, S., Schierloh, P., Yokobori, N. K., Baldini, M., Musella, R. M., Abbate, E. H., & Sasiain, M. D. C. (2007) · European Journal of Immunology · doi:10.1002/eji.200636771 · Cited by 40 · see citing works
The potential of human neutrophil peptides in tuberculosis therapy.
Fu, L. (2003) · PubMed · Cited by 39 · see citing works
Gr-1+ cells, but not neutrophils, limit virus replication and lesion development following flank infection of mice with herpes simplex virus type-1
Wojtasiak, M., Pickett, D. L., Tate, M. D., Bedoui, S., Job, E. R., Whitney, P. G., Brööks, A. G., & Reading, P. C. (2010) · Virology · doi:10.1016/j.virol.2010.08.001 · Cited by 39 · see citing works
Myeloperoxidase Exerts Microbicidal Activity againstMycobacterium tuberculosis
Borelli, V., Banfi, E., Perrotta, M. G., et al. (1999) · Infection and Immunity · doi:10.1128/iai.67.8.4149-4152.1999 · Cited by 38 · see citing works
Elevated levels of circulating adhesion molecules in patients with active pulmonary tuberculosis
Mukae, H., Ashitani, J.-I., Tokojima, M., et al. (2003) · Respirology · doi:10.1046/j.1440-1843.2003.00471.x · Cited by 36 · see citing works
Phagocytosis and killing ofMycobacterium aviumcomplex by human neutrophils
Hartmann, P., Becker, R., Franzen, C., et al. (2001) · Journal of Leukocyte Biology · doi:10.1189/jlb.69.3.397 · Cited by 35 · see citing works
Towards a ‘Human‐like’ Model of Tuberculosis: Intranasal Inoculation of LPS Induces Intragranulomatous Lung Necrosis in Mice Infected Aerogenically with Mycobacterium tuberculosis
Cardona, P.-J., Llatjós, R., Gordillo, S., et al. (2001) · Scandinavian Journal of Immunology · doi:10.1046/j.1365-3083.2001.00842.x · Cited by 33 · see citing works
[Neutrophil participation in early control and immune activation during experimental pulmonary tuberculosis].
Barrios‐Payán, J., Aguilar‐León, D., Lascurain-Ledezma, R., et al. (2007) · PubMed · Cited by 32 · see citing works
BCG Priming of Dendritic Cells Enhances T Regulatory and Th1 Function and Suppresses Allergen-Induced Th2 Function in vitro and in vivo
Ahrens, B., Grüber, C., Rha, R.-D., et al. (2009) · International Archives of Allergy and Immunology · doi:10.1159/000222673 · Cited by 31 · see citing works
Immune responses in tuberculosis: antibodies and CD4‐CD8 lymphocytes with vascular adhesion molecules and cytokines (chemokines) cause a rapid antigen‐specific cell infiltration at sites of bacillus Calmette–Guérin reinfection
Shigenaga, T., Dannenberg, A. M., Lowrie, D. B., Said, W. B. M., Urist, M. J., Abbey, H., Schofield, B., Mounts, P., & Sugisaki, K. (2001) · Immunology · doi:10.1046/j.1365-2567.2001.01195.x · Cited by 28 · see citing works
Treatment with recombinant granulocyte colony‐stimulating factor (Filgrastin TM ) stimulates neutrophils and tissue macrophages and induces an effective non‐specific response against Mycobacterium avium in mice
Bermudez, L. E., Petrofsky, M., & Stevens, P. R. (1998) · Immunology · doi:10.1046/j.1365-2567.1998.00529.x · Cited by 28 · see citing works
Cytokines Enhance Neutrophils from Human Immunodeficiency Virus‐Negative Donors and AIDS Patients to Inhibit the Growth ofMycobacterium aviumIn Vitro
Newman, G. W., Guarnaccia, J. R., Remold, H. G., et al. (1997) · The Journal of Infectious Diseases · doi:10.1086/513987 · Cited by 28 · see citing works
Lung Repair and Granuloma Formation
Antony, V. B., Sahn, S. A., Harada, R. N., et al. (1983) · CHEST Journal · doi:10.1378/chest.83.5_supplement.95s · Cited by 25 · see citing works
Altered cellular infiltration and cytokine levels during early Mycobacterium tuberculosis sigC mutant infection are associated with late-stage disease attenuation and milder immunopathology in mice
Abdul-Majid, K.-B., Ly, L. H., Converse, P. J., et al. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-151 · Cited by 24 · see citing works
Mannose-binding lectin enhances the attachment and phagocytosis of mycobacteria in vitro.
Bonar, A., Chmiela, M., Rudnicka, W., et al. (2005) · PubMed · Cited by 21 · see citing works
Human phagocytes lack the ability to kill Mycobacterium gordonae, a non-pathogenic mycobacteria
Reyes-Ruvalcaba, D., González‐Cortés, C., & Rivero-Lezcano, O. M. (2008) · Immunology Letters · doi:10.1016/j.imlet.2007.11.010 · Cited by 21 · see citing works
Lung repair and granuloma formation. Tubercle bacilli stimulated neutrophils release chemotactic factors for monocytes
Vb, A., Sahn, S. A., Harada, R. N., et al. (1983) · CHEST Journal · doi:10.1378/chest.83.5.95s · Cited by 19 · see citing works
Apoptosis and oxidative burst in neutrophils infected with Mycobacterium spp.
González‐Cortés, C., Reyes-Ruvalcaba, D., Diez‐Tascón, C., & Rivero-Lezcano, O. M. (2009) · Immunology Letters · doi:10.1016/j.imlet.2009.07.006 · Cited by 18 · see citing works
Studies on the Interaction of Mycobacterium microti and Mycobacterium lepraemurium with Mouse Polymorphonuclear Leucocytes
Smith, C. C., Barr, R., & Alexander, J. K. (1979) · Journal of General Microbiology · doi:10.1099/00221287-112-1-185 · Cited by 17 · see citing works
Mycobacterial lipoarabinomannan affects human polymorphonuclear and mononuclear phagocyte functions differently.
Fietta, A. M., Francioli, C., & Grassi, G. G. (2000) · PubMed · Cited by 12 · see citing works
Activation of peripheral phagocytes in BCG-vaccinated subjects
Vuotto, M. L., Ielpo, M. T. L., Liguori, G., et al. (2000) · Luminescence · doi:10.1002/1522-7243(200005/06)15:3 · Cited by 4 · see citing works
Experimental Tuberculous Pleural Effusion
Lemon, W. S., & Feldman, W. H. (2019) · American Review of Tuberculosis · Cited by 3 · see citing works

Flagged first, then by citations

Sorted by citations

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
Neutrophil-derived cytokines: facts beyond expression
Tecchio, C., Micheletti, A., & Cassatella, M. A. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00508 · Cited by 699 · see citing works
Neutrophils Exert Protection in the Early Tuberculous Granuloma by Oxidative Killing of Mycobacteria Phagocytosed from Infected Macrophages
Yang, C.-T., Cambier, C. J., Davis, J. M., Hall, C. J., Crosier, P. S., & Ramakrishnan, L. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.07.009 · Cited by 293 · see citing works

Authors: Lowe, D. M., Redford, P. S., Wilkinson, R. J., O’Garra, A., & Martineau, A. R.
Affiliations: University of Cape Town (ZA)
National Institute for Medical Research (GB)
Queen Mary University of London (GB)
Corresponding author: Lowe, David M.
ORCID: Lowe, David M.
Wilkinson, Robert J.
O’Garra, Anne
Martineau, Adrian R.
Venue: Trends in Immunology
Publisher: Elsevier BV
Published: 2012-01
Volume: 33
Issue: 1
Pages: 14-25
ISSN: 1471-4906 (ISSN-L)
DOI: 10.1016/j.it.2011.10.003
OpenAlex: W2040544951
Cited by: 312
References: 107
Citations by year: 2026: 13 · 2025: 13 · 2024: 17 · 2023: 12 · 2022: 16 · 2021: 10 · 2020: 26 · 2019: 23 · 2018: 25 · 2017: 32 · 2016: 25 · 2015: 22 · 2014: 35 · 2013: 31 · 2012: 12
FWCI: 3.10
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (088316, 84323)
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords: neutrophils, tuberculosis, mycobacterial infection, neutrophil phagocytosis, neutrophil-macrophage interaction, T cell response, bacterial dissemination, immune dysfunction, pathogen load, tuberculosis pathology
MeSH terms: Animals, Humans, Macrophages, Mycobacterium, Neutrophils, Tuberculosis

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

Neutrophils in tuberculosis: friend or foe?

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks