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Citations to this article

Neutrophil-mediated innate immune resistance to mycobacteria
Adrian R. Martineau, … , Christopher J. Griffiths, Robert J. Wilkinson
Adrian R. Martineau, … , Christopher J. Griffiths, Robert J. Wilkinson
Published July 2, 2007
Citation Information: J Clin Invest. 2007;117(7):1988-1994. https://doi.org/10.1172/JCI31097.
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Research Article Infectious disease Article has an altmetric score of 4

Neutrophil-mediated innate immune resistance to mycobacteria

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Abstract

Neutrophils contain antimicrobial peptides with antituberculous activity, but their contribution to immune resistance to tuberculosis (TB) infection has not been previously investigated to our knowledge. We determined differential white cell counts in peripheral blood of 189 adults who had come into contact with patients diagnosed with active TB in London, United Kingdom, and evaluated them for evidence of TB infection and capacity to restrict mycobacterial growth in whole-blood assays. Risk of TB infection was inversely and independently associated with peripheral blood neutrophil count in contacts of patients diagnosed with pulmonary TB. The ability of whole blood to restrict growth of Mycobacterium bovis bacille Calmette Guérin and Mycobacterium tuberculosis was impaired 7.3- and 3.1-fold, respectively, by neutrophil depletion. In microbiological media, human neutrophil peptides (HNPs) 1–3 killed M. tuberculosis. The neutrophil peptides cathelicidin LL-37 and lipocalin 2 restricted growth of the organism, the latter in an iron-dependent manner. Black African participants had lower neutrophil counts and lower circulating concentrations of HNP1–3 and lipocalin 2 than south Asian and white participants. Neutrophils contribute substantially to innate resistance to TB infection, an activity associated with their antimicrobial peptides. Elucidation of the regulation of neutrophil antimicrobial peptides could facilitate prevention and treatment of TB.

Authors

Adrian R. Martineau, Sandra M. Newton, Katalin A. Wilkinson, Beate Kampmann, Bridget M. Hall, Niga Nawroly, Geoffrey E. Packe, Robert N. Davidson, Christopher J. Griffiths, Robert J. Wilkinson

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Glibenclamide impairs responses of neutrophils against Burkholderia pseudomallei by reduction of intracellular glutathione
C Kewcharoenwong, D Rinchai, A Nithichanon, GJ Bancroft, M Ato, G Lertmemongkolchai
Scientific Reports 2016
Macrophage defense mechanisms against intracellular bacteria
G Weiss, UE Schaible
Immunological Reviews 2015
New tricks for old dogs: countering antibiotic resistance in tuberculosis with host-directed therapeutics
TR Hawn, JA Shah, D Kalman
Immunological Reviews 2015
Host-Directed Therapies for Tuberculosis: Figure 1
DM Tobin
Cold Spring Harbor Perspectives in Medicine 2015
Pathology and immune reactivity: understanding multidimensionality in pulmonary tuberculosis
A Dorhoi, SH Kaufmann
Seminars in Immunopathology 2015
Immunological mechanisms contributing to the double burden of diabetes and intracellular bacterial infections
K Hodgson, J Morris, T Bridson, B Govan, C Rush, N Ketheesan
Immunology 2015
Heterogeneity in tuberculosis pathology, microenvironments and therapeutic responses
A Lenaerts, CE Barry, V Dartois
Immunological Reviews 2015
Innate Immune Defenses in Human Tuberculosis: An Overview of the Interactions between Mycobacterium tuberculosis and Innate Immune Cells
JK Sia, M Georgieva, J Rengarajan
Journal of Immunology Research 2015
Excessive Cytolytic Responses Predict Tuberculosis Relapse After Apparently Successful Treatment
JM Cliff, JE Cho, JS Lee, K Ronacher, EC King, P Helden, G Walzl, HM Dockrell
The Journal of Infectious Diseases 2015
Effect of Antiretroviral Therapy on HIV-mediated Impairment of the Neutrophil Antimycobacterial Response
DM Lowe, N Bangani, R Goliath, B Kampmann, KA Wilkinson, RJ Wilkinson, AR Martineau
Annals of the American Thoracic Society 2015
Human neutrophil peptide-1 decreases during ageing in selected Mexican population
B Rivas-Santiago, JE Castañeda-Delgado, J de Haro-Acosta, F Torres-Juarez, I Frausto-Lujan, P Marin-Luevano, R González-Amaro, JA Enciso-Moreno
Immunologic Research 2015
CXCL5/LIX-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis
Geraldine Nouailles, Anca Dorhoi, Markus Koch, Jens Zerrahn, January Weiner 3rd, Kellen C. Faé, Frida Arrey, Stefanie Kuhlmann, Silke Bandermann, Delia Löwe, Hans-Joachim Mollenkopf, Alexis Vogelzang, Catherine Meyer-Schwesinger, Hans-Willi Mittrücker, Gayle McEwen, Stefan H.E. Kaufmann
Journal of Clinical Investigation 2014
IL-1α and complement cooperate in triggering local neutrophilic inflammation in response to adenovirus and eliminating virus-containing cells
NC di Paolo, LK Baldwin, EE Irons, T Papayannopoulou, S Tomlinson, DM Shayakhmetov
PLoS pathogens 2014
The balance between protective and pathogenic immune responses in the TB-infected lung
IM Orme, RT Robinson, AM Cooper
Nature Immunology 2014
Outbreaks of Mycobacterium tuberculosis MDR strains differentially induce neutrophil respiratory burst involving lipid rafts, p38 MAPK and Syk
MM Romero, JI Basile, B López, V Ritacco, L Barrera, MD Sasiain, M Alemán
BMC Infectious Diseases 2014
The lack of a big picture in tuberculosis: the clinical point of view, the problems of experimental modeling and immunomodulation. The factors we should consider when designing novel treatment strategies
C Vilaplana, PJ Cardona
Frontiers in microbiology 2014
Apoptotic Neutrophils Augment the Inflammatory Response to Mycobacterium tuberculosis Infection in Human Macrophages
H Andersson, B Andersson, D Eklund, E Ngoh, A Persson, K Svensson, M Lerm, R Blomgran, O Stendahl
PloS one 2014
Anti-Inflammatory and Antimicrobial Actions of Vitamin D in Combating TB/HIV
AK Coussens, AR Martineau, RJ Wilkinson
Scientifica 2014
Functional analysis of the mRNA profile of neutrophil gelatinase‑associated lipocalin overexpression in esophageal squamous cell carcinoma using multiple bioinformatic tools
BL Wu, CQ Li, ZP Du, F Zhou, JJ Xie, LW Luo, JY Wu, PX Zhang, LY Xu, EM Li
Molecular medicine reports 2014
Acute myeloid leukemia presenting with pulmonary tuberculosis
M Thomas, M AlGherbawe
Case Reports in Infectious Diseases 2014
Cell-Autonomous Effector Mechanisms against Mycobacterium tuberculosis
JD MacMicking
Cold Spring Harbor Perspectives in Medicine 2014
Status of vitamin D, antimicrobial peptide cathelicidin and T helper‑associated cytokines in patients with diabetes mellitus and pulmonary tuberculosis
Y Zhan, L Jiang
Experimental and therapeutic medicine 2014
Striking the Right Balance Determines TB or Not TB
S BoseDasgupta, J Pieters
Frontiers in immunology 2014
Beyond macrophages: the diversity of mononuclear cells in tuberculosis
S Srivastava, JD Ernst, L Desvignes
Immunological Reviews 2014
Role for Gr-1+ Cells in the Control of High-Dose Mycobacterium bovis Recombinant BCG
MW Panas, NL Letvin
Clinical and vaccine immunology : CVI 2014
Gr-1dimCD11b+ Immature Myeloid-Derived Suppressor Cells but Not Neutrophils Are Markers of Lethal Tuberculosis Infection in Mice
EN Tsiganov, EM Verbina, TV Radaeva, VV Sosunov, GA Kosmiadi, IY Nikitina, IV Lyadova
Journal of immunology (Baltimore, Md. : 1950) 2014
Tuberculin skin test and interferon-gamma release assay values are associated with antimicrobial peptides expression in  polymorphonuclear cells during latent tuberculous infection
Castañeda-Delgado JE, Cervantes-Villagrana A, Serrano-Escobedo CJ, Frausto-Lujan I, Rivas-Santiago C, Enciso-Moreno JA, Rivas-Santiago B
Memórias do Instituto Oswaldo Cruz 2014
Early clearance of Mycobacterium tuberculosis: a new frontier in prevention
Verrall AJ, Netea MG, Alisjahbana B, Hill PC, van Crevel R
Immunology 2014
Vitamin D induces interleukin-1β expression: paracrine macrophage epithelial signaling controls M. tuberculosis infection
M Verway, M Bouttier, TT Wang, M Carrier, M Calderon, BS An, E Devemy, F McIntosh, M Divangahi, MA Behr, JH White
PLoS pathogens 2013
Prominent role for T cell-derived tumour necrosis factor for sustained control of Mycobacterium tuberculosis infection
N Allie, SI Grivennikov, R Keeton, NJ Hsu, ML Bourigault, N Court, C Fremond, V Yeremeev, Y Shebzukhov, B Ryffel, SA Nedospasov, VF Quesniaux, M Jacobs
Scientific Reports 2013
Immune vulnerability of infants to tuberculosis
KV Driessche, A Persson, BJ Marais, PJ Fink, KB Urdahl
Clinical & developmental immunology 2013
Host-Directed Therapeutics for Tuberculosis: Can We Harness the Host?
TR Hawn, AI Matheson, SN Maley, O Vandal
Microbiology and molecular biology reviews : MMBR 2013
HIV-1 and the immune response to TB
NF Walker, G Meintjes, RJ Wilkinson
Future Virology 2013
A novel assay of antimycobacterial activity and phagocytosis by human neutrophils
DM Lowe, N Bangani, MR Mehta, DM Lang, AG Rossi, KA Wilkinson, RJ Wilkinson, AR Martineau
Tuberculosis 2013
Blood Cells and Interferon-Gamma Levels Correlation in Latent Tuberculosis Infection
I Takenami, C Loureiro, A Machado, K Emodi, LW Riley, S Arruda
ISRN Pulmonology 2013
Changing world of neutrophils
CI Timár, ÁM Lőrincz, E Ligeti
Pflügers Archiv - European Journal of Physiology 2013
Modulation of neutrophil NETosis: interplay between infectious agents and underlying host physiology
S Hahn, S Giaglis, CS Chowdhury, CS Chowdury, I Hösli, P Hasler
Seminars in Immunopathology 2013
Mice genetically inactivated in interleukin-17A receptor are defective in long-term control of Mycobacterium tuberculosis infection
D Freches, H Korf, O Denis, X Havaux, K Huygen, M Romano
Immunology 2013
Blood neutrophil counts in HIV-infected patients with pulmonary tuberculosis: association with sputum mycobacterial load
AD Kerkhoff, R Wood, DM Lowe, M Vogt, SD Lawn
PloS one 2013
B cells regulate neutrophilia during Mycobacterium tuberculosis infection and BCG vaccination by modulating the interleukin-17 response
L Kozakiewicz, Y Chen, J Xu, Y Wang, K Dunussi-Joannopoulos, Q Ou, JL Flynn, SA Porcelli, WR Jacobs, J Chan
PLoS pathogens 2013
Two human host defense ribonucleases against mycobacteria, the eosinophil cationic protein (RNase 3) and RNase 7
D Pulido, M Torrent, D Andreu, MV Nogués, E Boix
Antimicrobial agents and chemotherapy 2013
Vitamin D deficiency in medical patients at a central hospital in Malawi: a comparison with TB patients from a previous study
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PloS one 2013
Diverse novel functions of neutrophils in immunity, inflammation, and beyond
A Mócsai
Journal of Experimental Medicine 2013
Neutrophilia independently predicts death in tuberculosis
DM Lowe, AK Bandara, GE Packe, RD Barker, RJ Wilkinson, CJ Griffiths, AR Martineau
The European respiratory journal : official journal of the European Society for Clinical Respiratory Physiology 2013
Mycobacterium tuberculosis Infection of the Placenta: A Study of the Early (Innate) Inflammatory Response in Two Cases
CR Abramowsky, J Gutman, JA Hilinski
Pediatric and Developmental Pathology 2012
Neutrophils Exert Protection in the Early Tuberculous Granuloma by Oxidative Killing of Mycobacteria Phagocytosed from Infected Macrophages
CT Yang, CJ Cambier, JM Davis, CJ Hall, PS Crosier, L Ramakrishnan
Cell Host & Microbe 2012
Azurophil Granule Proteins Constitute the Major Mycobactericidal Proteins in Human Neutrophils and Enhance the Killing of Mycobacteria in Macrophages
P Jena, S Mohanty, T Mohanty, S Kallert, M Morgelin, T Lindstrøm, N Borregaard, S Stenger, A Sonawane, OE Sørensen
PloS one 2012
Comparison of interferon-γ-, interleukin (IL)-17- and IL-22-expressing CD4 T cells, IL-22-expressing granulocytes and proinflammatory cytokines during latent and active tuberculosis infection
J Cowan, S Pandey, LG Filion, JB Angel, A Kumar, DW Cameron
Clinical & Experimental Immunology 2012
Lipocalin 2 regulates inflammation during pulmonary mycobacterial infections
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PloS one 2012
Mycobacterium tuberculosis inhibits neutrophil apoptosis, leading to delayed activation of naive CD4 T cells
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Cell Host & Microbe 2012
The Role of Iron Metabolism in Lung Inflammation and Injury
J Kim
Journal of Allergy & Therapy 2012
Antimicrobial Peptides in Innate Immunity against Mycobacteria
DM Shin, EK Jo
Immune Network 2011
Iron metabolism and the innate immune response to infection
EE Johnson, M Wessling-Resnick
Microbes and Infection 2011
Optimization of a whole blood intracellular cytokine assay for measuring innate cell responses to mycobacteria
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Journal of Immunological Methods 2011
Clinical characteristics and outcomes of Mycobacterium tuberculosis disease in adult patients with hematological malignancies
CY Chen, WH Sheng, A Cheng, W Tsay, SY Huang, JL Tang, YC Chen, JY Wang, HF Tien, SC Chang
BMC Infectious Diseases 2011
Human Polymorphisms as Clinical Predictors in Leprosy
EP de Oca
Journal of Tropical Medicine 2011
Development of Vaccines Against Burkholderia Pseudomallei
N Patel, L Conejero, MD Reynal, A Easton, GJ Bancroft, RW Titball
Frontiers in microbiology 2011
Induction of β-defensins by l-isoleucine as novel immunotherapy in experimental murine tuberculosis
CE Rivas-Santiago, B Rivas-Santiago, DA León, J Castañeda-Delgado, RH Pando
Clinical & Experimental Immunology 2011
Reciprocal seasonal variation in vitamin D status and tuberculosis notifications in Cape Town, South Africa
AR Martineau, S Nhamoyebonde, T Oni, MX Rangaka, S Marais, N Bangani, R Tsekela, L Bashe, V Azevedo, J Caldwell, TR Venton, PM Timms, KA Wilkinson, RJ Wilkinson
Proceedings of the National Academy of Sciences 2011
Mycobacterium bovis bacilli Calmette-Guerin regulates leukocyte recruitment by modulating alveolar inflammatory responses
M Andersson, N Lutay, O Hallgren, G Westergren-Thorsson, M Svensson, G Godaly
Innate immunity 2011
Immune interference in Mycobacterium tuberculosis intracellular iron acquisition through siderocalin recognition of carboxymycobactins
TM Hoette, MC Clifton, AM Zawadzka, MA Holmes, RK Strong, KN Raymond
ACS chemical biology 2011
Effects of myeloid differentiation primary response gene 88 (MyD88) activation on Helicobacter infection in vivo and induction of a Th17 response
M Obonyo, B Rickman, DG Guiney
Helicobacter 2011
Lung Neutrophils Facilitate Activation of Naive Antigen-Specific CD4 + T Cells during Mycobacterium tuberculosis Infection
R Blomgran, JD Ernst
Journal of immunology (Baltimore, Md. : 1950) 2011
Anti-Tuberculosis Activity of α-Helical Antimicrobial Peptides: De Novo Designed L- and D-Enantiomers Versus L- and D-LL37
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Protein and peptide letters 2011
Siderocalin inhibits the intracellular replication of Mycobacterium tuberculosis in macrophages
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FEMS Immunology and Medical Microbiology 2010
The role of iron in the immune response to bacterial infection
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Immunologic Research 2010
Searching for novel intercellular signal-transducing molecules in the kidney and their clinical application
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Clinical and Experimental Nephrology 2010
The immunology of tuberculosis: From bench to bedside
K DHEDA, SK SCHWANDER, B ZHU, RN van ZYL-SMIT, Y ZHANG
Respirology 2010
Is Mycobacterium tuberculosis stressed out? A critical assessment of the genetic evidence
CL Stallings, MS Glickman
Microbes and infection / Institut Pasteur 2010
Differential activity of innate defense antimicrobial peptides against Nocardia species
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BMC Microbiology 2010
Intracellular Mycobacterium avium intersect transferrin in the Rab11(+) recycling endocytic pathway and avoid lipocalin 2 trafficking to the lysosomal pathway
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The Journal of Infectious Diseases 2010
Mendelian randomization: potential use of genetics to enable causal inferences regarding HIV-associated biomarkers and outcomes
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Current Opinion in HIV and AIDS 2010
Human Lung Immunity against Mycobacterium tuberculosis
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American journal of respiratory and critical care medicine 2010
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Microbes and infection / Institut Pasteur 2010
Cell-Mediated Immune Responses in Tuberculosis
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Annual Review of Immunology 2009
Ironing out the wrinkles in host defense: interactions between iron homeostasis and innate immunity
L Wang, BJ Cherayil
Journal of Innate Immunity 2009
1α,25-dihydroxyvitamin D3inhibits matrix metalloproteinases induced byMycobacterium tuberculosisinfection
A Coussens, PM Timms, BJ Boucher, TR Venton, AT Ashcroft, KH Skolimowska, SM Newton, KA Wilkinson, RN Davidson, CJ Griffiths, RJ Wilkinson, AR Martineau
Immunology 2009
Immunomodulation with recombinant interferon-gamma1b in pulmonary tuberculosis
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PloS one 2009
Association between Gc genotype and susceptibility to TB is dependent on vitamin D status
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The European respiratory journal : official journal of the European Society for Clinical Respiratory Physiology 2009
Dexamethasone, cerebrospinal fluid matrix metalloproteinase concentrations and clinical outcomes in tuberculous meningitis
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PloS one 2009
Lipocalin 2 Is Required for Pulmonary Host Defense against Klebsiella Infection
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Journal of immunology (Baltimore, Md. : 1950) 2009
Kinetics of Lethal Factor and Poly- d -Glutamic Acid Antigenemia during Inhalation Anthrax in Rhesus Macaques
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Infection and immunity 2009
Expression of Cathelicidin LL-37 during Mycobacterium tuberculosis Infection in Human Alveolar Macrophages, Monocytes, Neutrophils, and Epithelial Cells
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Infection and immunity 2008
Determinants of natural immunity against tuberculosis in an endemic setting: factors operating at the level of macrophage-Mycobacterium tuberculosis interaction
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Clinical & Experimental Immunology 2008
Expression and Secretion of Cathelicidin LL-37 in Human Epithelial Cells after Infection by Mycobacterium bovis Bacillus Calmette-Guérin
P Méndez-Samperio, E Miranda, A Trejo
Clinical and vaccine immunology : CVI 2008
Homeostatic regulation of blood neutrophil counts.
von Vietinghoff S, Ley K
Journal of immunology (Baltimore, Md. : 1950) 2008

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