Cited by 480Tuberculosis Research and EpidemiologyMycobacterium research and diagnosisImmune Response and Inflammation

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Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids

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Cambier, C. J., Takaki, Kevin K., Larson, Ryan P., Hernandez, Rafael E., Tobin, David M., Urdahl, Kevin B., Cosma, Christine L., Ramakrishnan, Lalita·2014·Nature

DOI 10.1038/nature12799PMC PMC3961847

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Abstract

The evolutionary survival of Mycobacterium tuberculosis, the cause of human tuberculosis, depends on its ability to invade the host, replicate, and transmit infection. At its initial peripheral infection site in the distal lung airways, M. tuberculosis infects macrophages, which transport it to deeper tissues. How mycobacteria survive in these broadly microbicidal cells is an important question. Here we show in mice and zebrafish that M. tuberculosis, and its close pathogenic relative Mycobacterium marinum, preferentially recruit and infect permissive macrophages while evading microbicidal ones. This immune evasion is accomplished by using cell-surface-associated phthiocerol dimycoceroserate (PDIM) lipids to mask underlying pathogen-associated molecular patterns (PAMPs). In the absence of PDIM, these PAMPs signal a Toll-like receptor (TLR)-dependent recruitment of macrophages that produce microbicidal reactive nitrogen species. Concordantly, the related phenolic glycolipids (PGLs) promote the recruitment of permissive macrophages through a host chemokine receptor 2 (CCR2)-mediated pathway. Thus, we have identified coordinated roles for PDIM, known to be essential for mycobacterial virulence, and PGL, which (along with CCR2) is known to be associated with human tuberculosis. Our findings also suggest an explanation for the longstanding observation that M. tuberculosis initiates infection in the relatively sterile environment of the lower respiratory tract, rather than in the upper respiratory tract, where resident microflora and inhaled environmental microbes may continually recruit microbicidal macrophages through TLR-dependent signalling.

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Authors: Cambier, C. J., Takaki, K. K., Larson, R. P., Hernandez, R. E., Tobin, D. M., Urdahl, K. B., Cosma, C. L., & Ramakrishnan, L.
Affiliations: University of Washington (US)
Center for Infectious Disease Research (US)
Corresponding author: Ramakrishnan, Lalita
ORCID: Cambier, C. J.
Takaki, Kevin K.
Larson, Ryan P.
Hernandez, Rafael E.
Tobin, David M.
Urdahl, Kevin B.
Ramakrishnan, Lalita
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2013-12-15
Volume: 505
Issue: 7482
Pages: 218-222
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature12799
PMC: PMC3961847
OpenAlex: W1977138279
Cited by: 480
References: 41
Citations by year: 2026: 19 · 2025: 30 · 2024: 27 · 2023: 31 · 2022: 35 · 2021: 42 · 2020: 46 · 2019: 42 · 2018: 44 · 2017: 48 · 2016: 44 · 2015: 32 · 2014: 38 · 2013: 2
FWCI: 28.09
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Wellcome Trust (103950/Z/14/Z)
National Institutes of Health (DP1OD006782)
National Institute of Mental Health (DP1MH099901)
National Institute of Allergy and Infectious Diseases (R01AI076327, R01AI036396, R37AI054503, R01AI054503)
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: Mycobacterium tuberculosis, Mycobacterium marinum, tuberculosis, macrophage recruitment, immune evasion, phthiocerol dimycocerosate, phenolic glycolipids, pathogen-associated molecular patterns, Toll-like receptor signaling, reactive nitrogen species, bacterial membrane lipids, host-pathogen interaction, zebrafish
MeSH terms: Animals, Female, Glycolipids, Lipids, Macrophages, Membrane Lipids, Mice, Inbred C57BL, Mycobacterium, Mycobacterium tuberculosis, Virulence, Zebrafish, Toll-Like Receptors, Mice, Receptors, CCR2, Immune Evasion

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Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids

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