Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids
Open accessAbstract
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
PDIM's ability to mask pathogen-associated molecular patterns of the cell wall from the innate immune system enables M. tuberculosis to recruit naive rather than microbicidal macrophages.
“This is partly explained by its ability to mask pathogen- associated molecular patterns of the cell wall from the innate immune system, enabling M. tuberculosis to recruit naive rather than microbicidal macrophages112.”
From The mycobacterial cell envelope — a moving target (2020) · cites this paper as [112]
Phenolic glycolipids promote recruitment of M. tuberculosis permissive macrophages via stimulation of host chemokine receptor 2 expression, whereas invasion of TLR-responsive microbicidal macrophages producing reactive nitrogen and oxygen species is impaired.
“In addition, phenolic glycolipids promote the recruitment of M. tuberculosis permissive macrophages via stimulation of host chemokine receptor 2 expression, whereas the invasion of TLR responsive microbicidal macrophages producing reactive nitrogen and oxygen species is impaired (6).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [6]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Recognition of microorganisms and activation of the immune response
Medzhitov, R. (2007) · Nature · doi:10.1038/nature06246 · Cited by 2,862 · see citing works
The role of nasal carriage in Staphylococcus aureus infections
Wertheim, H. F., Melles, D. C., Vos, M. C., van Leeuwen, W., van Belkum, A., Verbrugh, H. A., & Nouwen, J. L. (2005) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(05)70295-4 · Cited by 2,685 · see citing works
Topographical Continuity of Bacterial Populations in the Healthy Human Respiratory Tract
Charlson, E. S., Bittinger, K., Haas, A. R., Fitzgerald, A. S., Frank, I., Yadav, A., Bushman, F. D., & Collman, R. G. (2011) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201104-0655oc · Cited by 1,144 · see citing works
Monocyte-Mediated Defense Against Microbial Pathogens
Serbina, N. V., Jia, T., Hohl, T. M., & Pamer, E. G. (2008) · Annual Review of Immunology · doi:10.1146/annurev.immunol.26.021607.090326 · Cited by 1,116 · see citing works
Chan, J., Xing, Y., Magliozzo, R. S., & Bloom, B. R. (1992) · The Journal of Experimental Medicine · doi:10.1084/jem.175.4.1111 · Cited by 1,062 · see citing works
Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans
Comas, I., Coscollá, M., Luò, T., Borrell, S., Holt, K. E., Kato‐Maeda, M., Parkhill, J., Malla, B., Berg, S., Thwaites, G. E., et al. (2013) · Nature Genetics · doi:10.1038/ng.2744 · Cited by 1,027 · see citing works
Variable host–pathogen compatibility in Mycobacterium tuberculosis
Gagneux, S., DeRiemer, K., Vân, T. T. T., Kato‐Maeda, M., de Jong, B. C., Narayanan, S., Nicol, M. P., Niemann, S., Kremer, K., Gutierrez, M. C., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511240103 · Cited by 984 · see citing works
The Role of the Granuloma in Expansion and Dissemination of Early Tuberculous Infection
Davis, J. M., & Ramakrishnan, L. (2009) · Cell · doi:10.1016/j.cell.2008.11.014 · Cited by 907 · see citing works
Self-citationRevisiting the role of the granuloma in tuberculosis
Ramakrishnan, L. (2012) · Nature reviews. Immunology · doi:10.1038/nri3211 · Cited by 887 · see citing works
Self-citationA glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response
Reed, M. B., Domenech, P., Manca, C., Su, H., Barczak, A. K., Kreiswirth, B. N., Kaplan, G., & Barry, C. E. (2004) · Nature · doi:10.1038/nature02837 · Cited by 763 · see citing works
Inducible nitric oxide synthase in human diseases
Kröncke, K.-D., Fehsel, K., & Kolb‐Bachofen, V. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00648.x · Cited by 585 · see citing works
The lta4h Locus Modulates Susceptibility to Mycobacterial Infection in Zebrafish and Humans
Tobin, D. M., Vary, J. C., Ray, J. P., Walsh, G. S., Dunstan, S. J., Bang, N. D., Hagge, D. A., Khadge, S., King, M., Hawn, T. R., et al. (2010) · Cell · doi:10.1016/j.cell.2010.02.013 · Cited by 529 · see citing works
Self-citationMayer-Barber, K. D., Barber, D. L., Shenderov, K., White, S., Wilson, M. S., Cheever, A. W., Kugler, D. G., Hieny, S. E., Caspar, P., Núñez, G., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0904189 · Cited by 472 · see citing works
Tuberculosis Pathogenesis and Immunity
Philips, J. A., & Ernst, J. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132458 · Cited by 415 · see citing works
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
Self-citationAntonelli, L. R. D. V., Rothfuchs, A. G., Gonçalves, R., Roffê, E., Cheever, A. W., Báfica, A. L. B., Salazar, A. Μ., Feng, C. G., & Sher, A. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40817 · Cited by 292 · see citing works
Ordway, D. J., Henao-Tamayo, M. I., Harton, M. R., Palanisamy, G. S., Troudt, J. M., Shanley, C. A., Basaraba, R. J., & Orme, I. M. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.1.522 · Cited by 259 · see citing works
Evaluation of the pathogenesis and treatment of Mycobacterium marinum infection in zebrafish
Takaki, K. K., Davis, J. M., Winglee, K., & Ramakrishnan, L. (2013) · Nature Protocols · doi:10.1038/nprot.2013.068 · Cited by 245 · see citing works
Self-citationDichotomous Role of the Macrophage in Early Mycobacterium marinum Infection of the Zebrafish
Clay, H., Davis, J. M., Beery, D., Anna Huttenlocher, A., Lyons, S. E., & Ramakrishnan, L. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.06.004 · Cited by 243 · see citing works
Self-citationFlores-Villanueva, P. O., Ruiz-Morales, J. A., Song, C., Flores, L. M., Jo, E., Montaño, M., Barnes, P. F., Selman, M., & Granados, J. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050126 · Cited by 241 · see citing works
Prevalence of Gram-Negative Rods in the Normal Pharyngeal Flora
Rosenthal, S. L., & TAGER, I. B. (1975) · Annals of Internal Medicine · doi:10.7326/0003-4819-83-3-355 · Cited by 205 · see citing works
Experimental and natural infections in M y D 88‐ and IRAK ‐4‐deficient mice and humans
von Bernuth, H., Pïcard, C., Puel, A., & Casanova, J. (2012) · European Journal of Immunology · doi:10.1002/eji.201242683 · Cited by 180 · see citing works
The pneumococcus: why a commensal misbehaves
Weiser, J. N. (2009) · Journal of Molecular Medicine · doi:10.1007/s00109-009-0557-x · Cited by 179 · see citing works
Scott, H. M., & Flynn, J. L. (2002) · Infection and Immunity · doi:10.1128/iai.70.11.5946-5954.2002 · Cited by 171 · see citing works
The dimycocerosate ester polyketide virulence factors of mycobacteria
Onwueme, K. C., Vos, C. J., Zurita, J., Ferreras, J. A., & Quadri, L. E. N. (2005) · Progress in Lipid Research · doi:10.1016/j.plipres.2005.07.001 · Cited by 151 · see citing works
Sinsimer, D., Huet, G., Manca, C., Tsenova, L., Koo, M.-S., Kurepina, N. E., Kana, B. D., Mathema, B., Marras, S. A. E., Kreiswirth, B. N., et al. (2008) · Infection and Immunity · doi:10.1128/iai.01663-07 · Cited by 139 · see citing works
van der Vaart, M., van Soest, J. J., Spaink, H. P., & Meijer, A. H. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.010843 · Cited by 134 · see citing works
Brannon, M. K., Davis, J. M., Mathias, J. R., Hall, C. J., Emerson, J., Crosier, P. S., Anna Huttenlocher, A., Ramakrishnan, L., & Moskowitz, S. M. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01288.x · Cited by 126 · see citing works
Self-citationcRACE: a simple method for identification of the 5′ end of mRNAs
MARUYAMA, I. N., Rakow, T. L., & Maruyama, H. I. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.18.3796 · Cited by 121 · see citing works
Yu, J., Tran, V., Li, M., Huang, X., Niu, C., Wang, D., Zhu, J., Wang, J., Gao, Q., & Liu, J. (2012) · Infection and Immunity · doi:10.1128/iai.06370-11 · Cited by 115 · see citing works
Host defenses against bacterial lower respiratory tract infection
Eddens, T. J., & Kolls, J. K. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2012.07.005 · Cited by 103 · see citing works
An In Vivo Platform for Rapid High-Throughput Antitubercular Drug Discovery
Takaki, K. K., Cosma, C. L., Troll, M. A., & Ramakrishnan, L. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.06.008 · Cited by 101 · see citing works
Self-citationImaging of nitric oxide in a living vertebrate using a diaminofluorescein probe
Lepiller, S., Laurens, V., Bouchot, A., Herbomel, P., Solary, É., & Chluba, J. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.05.025 · Cited by 92 · see citing works
Cosma, C. L., Klein, K. A., Kim, R., Beery, D., & Ramakrishnan, L. (2006) · Infection and Immunity · doi:10.1128/iai.02061-05 · Cited by 92 · see citing works
Self-citationON THE MECHANICS OF DROPLET NUCLEI INFECTION
Wells, W. F., Ratcliffe, H. L., & Crumb, C. (1948) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a119179 · Cited by 75 · see citing works
Phthiocerol Dimycocerosate Transport Is Required for Resisting Interferon‐γ–Independent Immunity
Murry, J. P., Pandey, A. K., Sassetti, C. M., & Rubin, E. J. (2009) · The Journal of Infectious Diseases · doi:10.1086/605128 · Cited by 60 · see citing works
Epidemiology of Primary Tuberculosis in an Industrial School
Bates, J. H., Potts, W. E., & Lewis, M. (1965) · New England Journal of Medicine · doi:10.1056/nejm196504082721403 · Cited by 59 · see citing works
CCL2−2518 (A/G) polymorphisms and tuberculosis susceptibility: a meta-analysis [Review article]
Feng, W.-X., Flores-Villanueva, P. O., Владиславович, М. И., Wu, X.-R., Xiao, J., Jiao, W.-W., Sun, L., Miao, Q., Shen, C., Shen, D., et al. (2011) · The International Journal of Tuberculosis and Lung Disease · doi:10.5588/ijtld.11.0205 · Cited by 33 · see citing works
ON THE MECHANICS OF DROPLET NUCLEI INFECTION
Wells, W. F. (1948) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a119176 · Cited by 32 · see citing works
The allele encoding the mycobacterial Erp protein affects lung disease in mice
Mendonça-Lima, L., Bordat, Y., Pivert, E., Recchi, C., Neyrolles, O., Maitournam, A., Gicquel, B., & Reyrat, J. (2003) · Cellular Microbiology · doi:10.1046/j.1462-5822.2003.00237.x · Cited by 25 · see citing works
Lepiller, S., Laurens, V., Bouchot, A., Herbomel, P., Solary, É., & Chluba, J. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.04.002 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
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
Immune evasion and provocation by Mycobacterium tuberculosis
Chandra, P., Grigsby, S. J., & Philips, J. A. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00763-4 · Cited by 627 · see citing works
Alveolar Macrophages Provide an Early Mycobacterium tuberculosis Niche and Initiate Dissemination
Cohen, S. B., Gern, B. H., Delahaye, J. L., Adams, K. N., Plumlee, C. R., Winkler, J. K., Sherman, D. R., Gerner, M. Y., & Urdahl, K. B. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.08.001 · Cited by 577 · see citing works
Self-citationConsequences of genomic diversity in Mycobacterium tuberculosis
Coscollá, M., & Gagneux, S. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.09.012 · Cited by 450 · see citing works
Host Evasion and Exploitation Schemes of Mycobacterium tuberculosis
Cambier, C. J., Falkow, S., & Ramakrishnan, L. (2014) · Cell · doi:10.1016/j.cell.2014.11.024 · Cited by 432 · see citing works
Self-citationPathogenesis of HIV-1 and Mycobacterium tuberculosis co-infection
Bell, L. C. K., & Noursadeghi, M. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.128 · Cited by 394 · see citing works
γδ T cells: origin and fate, subsets, diseases and immunotherapy
Hu, Y., Hu, Q., Li, Y., Lu, L., Xiang, Z., Yin, Z., Kabelitz, D., & Wu, Y. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01653-8 · Cited by 394 · see citing works
The mycobacterial cell envelope — a moving target
Dulberger, C. L., Rubin, E. J., & Boutte, C. C. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0273-7 · Cited by 365 · see citing works
Immunology of Mycobacterium tuberculosis Infections
Sia, J. K., & Rengarajan, J. (2019) · Microbiology Spectrum · doi:10.1128/microbiolspec.gpp3-0022-2018 · Cited by 320 · see citing works
Identification of polarized macrophage subsets in zebrafish
Chi, M. N., Laplace-Builhe, B., Trávníčková, J., Luz‐Crawford, P., Téjédor, G., Phan, Q. T., Duroux-Richard, I., Levraud, J., Kissa, K., Lutfalla, G., et al. (2015) · eLife · doi:10.7554/elife.07288 · Cited by 295 · see citing works
The balance between protective and pathogenic immune responses in the TB-infected lung
Orme, I. M., Robinson, R., & Cooper, A. M. (2014) · Nature Immunology · doi:10.1038/ni.3048 · Cited by 286 · see citing works
Nitric oxide prevents a pathogen-permissive granulocytic inflammation during tuberculosis
Mishra, B. B., Lovewell, R. R., Olive, A. J., Zhang, G., Wang, W., Eugenín, E. A., Smith, C. M., Phuah, J. Y., Long, J. E., Dubuke, M. L., et al. (2017) · Nature Microbiology · doi:10.1038/nmicrobiol.2017.72 · Cited by 280 · see citing works
Gopal, R., Monin, L., Slight-Webb, S. R., Uche, U. N., Blanchard, E. L., Junecko, B. A. F., Ramos‐Payán, R., Stallings, C. L., Reinhart, T. A., Kolls, J. K., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004099 · Cited by 277 · see citing works
How sisters grow apart: mycobacterial growth and division
Kieser, K., & Rubin, E. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3299 · Cited by 260 · see citing works
Augenstreich, J., Arbues, A., Simeone, R., Haanappel, E., Wegener, A., Sayes, F., Le Chevalier, F., Chalut, C., Malaga, W., Guilhot, C., et al. (2017) · Cellular Microbiology · doi:10.1111/cmi.12726 · Cited by 240 · see citing works
Quigley, J., Hughitt, V. K., Velikovsky, C. A., Mariuzza, R. A., El-Sayed, N. M., & Briken, V. (2017) · mBio · doi:10.1128/mbio.00148-17 · Cited by 234 · see citing works
Pathogenicity and virulence of Mycobacterium tuberculosis
Rahlwes, K. C., Dias, B., Campos, P. C., Álvarez-Arguedas, S., & Shiloh, M. U. (2022) · Virulence · doi:10.1080/21505594.2022.2150449 · Cited by 221 · see citing works
Macrophages: sentinels and regulators of the immune system
Franken, L., Schiwon, M., & Kurts, C. (2016) · Cellular Microbiology · doi:10.1111/cmi.12580 · Cited by 211 · see citing works
Trained immunity as a molecular mechanism for BCG immunotherapy in bladder cancer
van Puffelen, J. H., Keating, S. T., Oosterwijk, E., van der Heijden, A. G., Netea, M. G., Joosten, L. A. B., & Vermeulen, S. H. H. M. (2020) · Nature Reviews Urology · doi:10.1038/s41585-020-0346-4 · Cited by 204 · see citing works
The distinct fate of smooth and rough Mycobacterium abscessus variants inside macrophages
Roux, A., Viljoen, A. J., Bah, A., Siméone, R., Bernut, A., Laencina, L., Deramaudt, T. B., Rottman, M., Herrmann, J., Majlessi, L., et al. (2016) · Open Biology · doi:10.1098/rsob.160185 · Cited by 201 · see citing works
Macrophage: A Cell With Many Faces and Functions in Tuberculosis
Ahmad, F., Rani, A., Alam, A., Zarin, S., Pandey, S., Singh, H., Hasnain, S. E., & Ehtesham, N. Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.747799 · Cited by 200 · see citing works
Cholesterol and fatty acids grease the wheels of Mycobacterium tuberculosis pathogenesis
Wilburn, K. M., Fieweger, R. A., & VanderVen, B. C. (2018) · Pathogens and Disease · doi:10.1093/femspd/fty021 · Cited by 191 · see citing works
The architectures of iterative type I PKS and FAS
Herbst, D. A., Townsend, C. A., & Maier, T. (2018) · Natural Product Reports · doi:10.1039/c8np00039e · Cited by 191 · see citing works
Dormant, quiescent, tolerant and persister cells: Four synonyms for the same target in cancer
Vallette, F. M., Olivier, C., Lézot, F., Oliver, L., Cochonneau, D., Lalier-Bretaudeau, L., Cartron, P., & Heymann, D. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.11.004 · Cited by 184 · see citing works
Mechanisms of Fish Macrophage Antimicrobial Immunity
Grayfer, L., Kerimoğlu, B., Yaparla, A., Hodgkinson, J. W., Xie, J., & Belosevic, M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01105 · Cited by 183 · see citing works
Nano- and micro-based inhaled drug delivery systems for targeting alveolar macrophages
Lee, W., Loo, C., Traini, D., & Young, P. M. (2015) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2015.1039509 · Cited by 181 · see citing works
Immunity and Immunopathology in the Tuberculous GranulomaPreprint
Pagán, A. J., & Ramakrishnan, L. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a018499 · Cited by 180 · see citing works
Self-citationTuberculosis and the art of macrophage manipulation
Upadhyay, S., Mittal, E., & Philips, J. A. (2018) · Pathogens and Disease · doi:10.1093/femspd/fty037 · Cited by 178 · see citing works
Kanabalan, R. D., Lee, L. J., Lee, T. Y., Chong, P. P., Hassan, L., Ismail, R., & Chin, V. K. (2021) · Microbiological Research · doi:10.1016/j.micres.2020.126674 · Cited by 175 · see citing works
Zebrafish Infection: From Pathogenesis to Cell Biology
Torraca, V., & Mostowy, S. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.10.002 · Cited by 171 · see citing works
Biphasic Dynamics of Macrophage Immunometabolism during Mycobacterium tuberculosis Infection
Shi, L., Jiang, Q., Bushkin, Y., Subbian, S., & Tyagi, S. (2019) · mBio · doi:10.1128/mbio.02550-18 · Cited by 169 · see citing works
Innate Control of Adaptive Immunity: Beyond the Three-Signal Paradigm
Jain, A., & Pasare, C. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1602000 · Cited by 169 · see citing works
Kramnik, I., & Beamer, G. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0538-9 · Cited by 164 · see citing works
Polarization of immune responses in fish: The ‘macrophages first’ point of view
Wiegertjes, G. F., Wentzel, A. S., Spaink, H. P., Elks, P. M., & Fink, I. R. (2015) · Molecular Immunology · doi:10.1016/j.molimm.2015.09.026 · Cited by 163 · see citing works
Batt, S. M., Minnikin, D. E., & Besra, G. S. (2020) · Biochemical Journal · doi:10.1042/bcj20200194 · Cited by 160 · see citing works
Phenolic Glycolipid Facilitates Mycobacterial Escape from Microbicidal Tissue-Resident Macrophages
Cambier, C. J., O’Leary, S. M., O’Sullivan, M. P., Keane, J., & Ramakrishnan, L. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.003 · Cited by 158 · see citing works
Self-citationImmune cell interactions in tuberculosis
Flynn, J. L., & Chan, J. (2022) · Cell · doi:10.1016/j.cell.2022.10.025 · Cited by 157 · see citing works
Molecular basis of mycobacterial survival in macrophages
Awuh, J. A., & Flo, T. H. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2422-8 · Cited by 155 · see citing works
Torraca, V., Masud, S., Spaink, H. P., & Meijer, A. H. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.015594 · Cited by 152 · see citing works
Cadena, A. M., Flynn, J. L., & Fortune, S. M. (2016) · mBio · doi:10.1128/mbio.00342-16 · Cited by 151 · see citing works
Pathology and immune reactivity: understanding multidimensionality in pulmonary tuberculosis
Dorhoi, A., & Kaufmann, S. H. E. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0531-3 · Cited by 150 · see citing works
Mycobacterial Dormancy Systems and Host Responses in Tuberculosis
Peddireddy, V., Doddam, S. N., & Ahmed, N. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00084 · Cited by 148 · see citing works
Moving tuberculosis vaccines from theory to practice
Andersen, P. L., & Scriba, T. J. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0174-z · Cited by 145 · see citing works
Lastrucci, C., Bénard, A., Balboa, L., Pingris, K., Souriant, S., Poincloux, R., Saati, T. A., Rasolofo, V., González-Montaner, P., Inwentarz, S., et al. (2015) · Cell Research · doi:10.1038/cr.2015.123 · Cited by 139 · see citing works
The Mycobacterium tuberculosis capsule: a cell structure with key implications in pathogenesis
Kalscheuer, R., Palacios, A., Anso, I., Cifuente, J. O., Anguíta, J., Jacobs, W. R., Guerin, M. E., & Prados‐Rosales, R. (2019) · Biochemical Journal · doi:10.1042/bcj20190324 · Cited by 137 · see citing works
Hopke, A., Nicke, N., Hidu, E. E., Degani, G., Popolo, L., & Wheeler, R. T. (2016) · PLOS Pathogens · doi:10.1371/journal.ppat.1005644 · Cited by 131 · see citing works
More than Skin Deep: Functional Genomic Basis for Resistance to Amphibian Chytridiomycosis
Ellison, A., Tunstall, T. S., DiRenzo, G. V., Hughey, M. C., Rebollar, E. A., Belden, L. K., Harris, R. N., Ibáñez, R., Lips, K. R., & Zamudio, K. R. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu285 · Cited by 131 · see citing works
Biology of Bony Fish Macrophages
Hodgkinson, J. W., Grayfer, L., & Belosevic, M. (2015) · Biology · doi:10.3390/biology4040881 · Cited by 130 · see citing works
Torraca, V., Cui, C., Boland, R., Bebelman, J., van der Sar, A. M., Smit, M. J., Siderius, M. H., Spaink, H. P., & Meijer, A. H. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.017756 · Cited by 129 · see citing works
Lysosomal Disorders Drive Susceptibility to Tuberculosis by Compromising Macrophage Migration
Berg, R. D., Levitte, S., O’Sullivan, M. P., O’Leary, S. M., Cambier, C. J., Cameron, J. R., Takaki, K. K., Moens, C. B., Tobin, D. M., Keane, J., et al. (2016) · Cell · doi:10.1016/j.cell.2016.02.034 · Cited by 129 · see citing works
Self-citationMcClean, C. M., & Tobin, D. M. (2016) · Pathogens and Disease · doi:10.1093/femspd/ftw068 · Cited by 128 · see citing works
Self-citationA Macrophage Response to Mycobacterium leprae Phenolic Glycolipid Initiates Nerve Damage in Leprosy
Madigan, C. A., Cambier, C. J., Kelly‐Scumpia, K. M., Scumpia, P. O., Cheng, T., Zailaa, J., Bloom, B. R., Moody, D. B., Smale, S. T., Sagasti, A., et al. (2017) · Cell · doi:10.1016/j.cell.2017.07.030 · Cited by 126 · see citing works
Self-citationCronan, M. R., Hughes, E. J., Brewer, W. J., Viswanathan, G., Hunt, E. G., Singh, B., Mehra, S., Oehlers, S. H., Gregory, S. G., Kaushal, D., et al. (2021) · Cell · doi:10.1016/j.cell.2021.02.046 · Cited by 123 · see citing works
Self-citationSensing of M ycobacterium tuberculosis and consequences to both host and bacillus
Stamm, C. E., Collins, A. C., & Shiloh, M. U. (2015) · Immunological Reviews · doi:10.1111/imr.12263 · Cited by 122 · see citing works
Garg, A. D., Vandenberk, L., Fang, S., Fasche, T., Van Eygen, S., Maes, J., Van Woensel, M., Koks, C., Vanthillo, N., Graf, N., et al. (2017) · Cell Death & Differentiation · doi:10.1038/cdd.2017.15 · Cited by 120 · see citing works
Barczak, A. K., Avraham, R., Singh, S., Luo, S. S., Zhang, W. R., Bray, M.-A., Hinman, A. E., Thompson, M., Nietupski, R. M., Golas, A., et al. (2017) · PLOS Pathogens · doi:10.1371/journal.ppat.1006363 · Cited by 120 · see citing works
Macrophage-Dependent Cytoplasmic Transfer during Melanoma Invasion In Vivo
Roh‐Johnson, M., Shah, A. N., Stonick, J. A., Poudel, K. R., Kargl, J., Yang, G. H. Y., Martino, J. S. D., Hernandez, R. E., Gast, C. E., Zarour, L. R., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.11.003 · Cited by 119 · see citing works
Self-citationIncreased Complement C1q Level Marks Active Disease in Human Tuberculosis
Cai, Y., Yang, Q., Tang, Y., Zhang, M., Liu, H., Zhang, G., Deng, Q., Huang, J., Gao, Z., Zhou, B., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092340 · Cited by 119 · see citing works
Lerner, T. R., Queval, C. J., Fearns, A., Repnik, U., Griffiths, G. W., & Gutierrez, M. G. (2018) · BMC Biology · doi:10.1186/s12915-017-0471-6 · Cited by 116 · see citing works
Fit for consumption: zebrafish as a model for tuberculosis
Cronan, M. R., & Tobin, D. M. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.016089 · Cited by 114 · see citing works
Self-citationXie, Y., Tolmeijer, S. H., Oskam, J. M., Tonkens, T., Meijer, A. H., & Schaaf, M. J. M. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.037887 · Cited by 112 · see citing works
MmpL Proteins in Physiology and Pathogenesis of M. tuberculosis
Melly, G. C., & Purdy, G. E. (2019) · Microorganisms · doi:10.3390/microorganisms7030070 · Cited by 110 · see citing works
Mycobacterium tuberculosis Complex Members Adapted to Wild and Domestic Animals
Malone, K. M., & Gordon, S. V. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-64371-7_7 · Cited by 109 · see citing works
pks5-recombination-mediated surface remodelling in Mycobacterium tuberculosis emergence
Boritsch, E. C., Frigui, W., Cascioferro, A., Malaga, W., Etienne, G., Laval, F., Pawlik, A., Le Chevalier, F., Orgeur, M., Ma, L., et al. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2015.19 · Cited by 104 · see citing works
Blanc, L., Gilleron, M., Prandi, J., Song, O., Jang, M.-S., Gicquel, B., Drocourt, D., Neyrolles, O., Brodin, P. M., Tiraby, G., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707840114 · Cited by 102 · see citing works
Hif-1α–Induced Expression of Il-1β Protects against Mycobacterial Infection in Zebrafish
Ogryzko, N. V., Lewis, A., Wilson, H. L., Meijer, A. H., Renshaw, S. A., & Elks, P. M. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1801139 · Cited by 101 · see citing works
Matrix metalloproteinases: Expression, regulation and role in the immunopathology of tuberculosis
Sabir, N., Hussain, T. A., Mangi, M. H., Zhao, D., & Zhou, X. (2019) · Cell Proliferation · doi:10.1111/cpr.12649 · Cited by 100 · see citing works
Levitte, S., Adams, K. N., Berg, R. D., Cosma, C. L., Urdahl, K. B., & Ramakrishnan, L. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.07.007 · Cited by 99 · see citing works
Self-citationMorales, R. A., & Allende, M. L. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00253 · Cited by 99 · see citing works
Protection and pathology in TB: learning from the zebrafish model
Meijer, A. H. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0522-4 · Cited by 99 · see citing works
Lipid metabolism and its implication in mycobacteria–host interaction
Gago, G., Diacovich, L., & Gramajo, H. C. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.11.020 · Cited by 96 · see citing works
Determining macrophage versus neutrophil contributions to innate immunity using larval zebrafish
Rosowski, E. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.041889 · Cited by 82 · see citing works
Biosynthesis of mycobacterial lipids by polyketide synthases and beyond
Quadri, L. E. N. (2014) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2014.896859 · Cited by 94 · see citing works
Paolo, N. C. D., Shafiani, S., Day, T., Papayannopoulou, T., Russell, D. W., Iwakura, Y., Sherman, D. R., Urdahl, K. B., & Shayakhmetov, D. M. (2015) · Immunity · doi:10.1016/j.immuni.2015.11.016 · Cited by 94 · see citing works
Self-citationComparative studies of Toll-like receptor signalling using zebrafish
Kanwal, Z., Wiegertjes, G. F., Veneman, W. J., Meijer, A. H., & Spaink, H. P. (2014) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2014.02.003 · Cited by 93 · see citing works
Iizasa, E., Chuma, Y., Uematsu, T., Kubota, M., Kawaguchi, H., Umemura, M., Toyonaga, K., Kiyohara, H., Yano, I., Colonna, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22620-3 · Cited by 92 · see citing works
Silver Nanoparticles for the Therapy of Tuberculosis
Tăbăran, F., MATEA, C. T., Mocan, T., Tăbăran, F., Mihaiu, M., Iancu, C., & MOCAN, L. C. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s241183 · Cited by 92 · see citing works
Mycocerosic acid synthase exemplifies the architecture of reducing polyketide synthases
Herbst, D. A., Jakob, R. P., Zähringer, F., & Maier, T. (2016) · Nature · doi:10.1038/nature16993 · Cited by 88 · see citing works
Hattori, Y., Morita, D., Fujiwara, N., Mori, D., Nakamura, T., Harashima, H., Yamasaki, S., & Sugita, M. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.566489 · Cited by 87 · see citing works
Xing, Z., Afkhami, S., Bavananthasivam, J., Fritz, D. K., D’Agostino, M. R., Vaseghi‐Shanjani, M., Yao, Y., & Jeyanathan, M. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4mr0220-446r · Cited by 85 · see citing works
mTOR-regulated mitochondrial metabolism limits mycobacterium-induced cytotoxicity
Pagán, A. J., Lee, L. J., Edwards-Hicks, J., Moens, C. B., Tobin, D. M., Busch‐Nentwich, E. M., Pearce, E. L., & Ramakrishnan, L. (2022) · Cell · doi:10.1016/j.cell.2022.08.018 · Cited by 82 · see citing works
Self-citationPhenotypic Heterogeneity in Mycobacterium tuberculosis
Dhar, N., McKinney, J. D., & Manina, G. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.tbtb2-0021-2016 · Cited by 81 · see citing works
Sex differences in the C57BL/6 model of Mycobacterium tuberculosis infection
Dibbern, J., Eggers, L. F., & Schneider, B. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-11438-z · Cited by 80 · see citing works
The cause–effect relation of tuberculosis on incidence of diabetes mellitus
Bisht, M. K., Dahiya, P., Ghosh, S., & Mukhopadhyay, S. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1134036 · Cited by 80 · see citing works
Skin and Soft Tissue Infections Due to Nontuberculous Mycobacteria
Misch, E. A., Saddler, C. M., & Davis, J. M. (2018) · Current Infectious Disease Reports · doi:10.1007/s11908-018-0611-3 · Cited by 79 · see citing works
Why don’t we have an effective tuberculosis vaccine yet?
Davenne, T., & McShane, H. (2016) · Expert Review of Vaccines · doi:10.1586/14760584.2016.1170599 · Cited by 79 · see citing works
The conical shape of DIM lipids promotes Mycobacterium tuberculosis infection of macrophages
Augenstreich, J., Haanappel, E., Ferré, G., Czaplicki, G., Jolibois, F., Destainville, N., Guilhot, C., Milon, A., Astarie‐Dequeker, C., & Chavent, M. G. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1910368116 · Cited by 77 · see citing works
Troll, J. V., Hamilton, M. K., Abel, M. L., Ganz, J., Bates, J. M., Stephens, W. Z., Melançon, E., van der Vaart, M., Meijer, A. H., Distel, M., et al. (2018) · Development · doi:10.1242/dev.155317 · Cited by 77 · see citing works
Host Cell Targets of Released Lipid and Secreted Protein Effectors of Mycobacterium tuberculosis
Augenstreich, J., & Briken, V. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.595029 · Cited by 76 · see citing works
Mycobacteria–host interactions in human bronchiolar airway organoids
Iakobachvili, N., Leon‐Icaza, S. A., Knoops, K., Sachs, N., Mazères, S., Siméone, R., Peixoto, A., Bernard, C., Murris‐Espin, M., Mazières, J., et al. (2021) · Molecular Microbiology · doi:10.1111/mmi.14824 · Cited by 76 · see citing works
A polymorphism in human MR1 is associated with mRNA expression and susceptibility to tuberculosis
Seshadri, C., Thuong, N. T. T., Mai, N. T. H., Bang, N. D., Chau, T. T. H., Lewinsohn, D. M., Thwaites, G. E., Dunstan, S. J., & Hawn, T. R. (2016) · Genes and Immunity · doi:10.1038/gene.2016.41 · Cited by 75 · see citing works
The Mycobacterial Cell Envelope: A Relict From the Past or the Result of Recent Evolution?
Vincent, A. T., Nyongesa, S., Morneau, I., Reed, M. B., Tocheva, E. I., & Veyrier, F. J. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02341 · Cited by 75 · see citing works
Evolutionary Aspects of Macrophages Polarization
Edholm, E., Rhoo, K. H., & Robert, J. (2017) · Results and problems in cell differentiation · doi:10.1007/978-3-319-54090-0_1 · Cited by 70 · see citing works
Chemical Synthesis of Cell Wall Constituents of Mycobacterium tuberculosis
Holzheimer, M., Buter, J., & Minnaard, A. J. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00043 · Cited by 69 · see citing works
Xu, S., Webb, S., Lau, T. C., & Cheng, S. H. (2018) · Scientific Reports · doi:10.1038/s41598-018-25490-w · Cited by 69 · see citing works
The Zebrafish Guide to Tuberculosis Immunity and TreatmentPreprint
Ramakrishnan, L. (2013) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2013.78.023283 · Cited by 69 · see citing works
Self-citationUnderstanding and overcoming the barriers to T cell-mediated immunity against tuberculosis
Urdahl, K. B. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.10.003 · Cited by 68 · see citing works
Self-citationWright, C. C., Hsu, F.-F., Arnett, E., Dunaj, J. L., Davidson, P. M., Pacheco, S. A., Harriff, M., Lewinsohn, D., Schlesinger, L., & Purdy, G. E. (2017) · Infection and Immunity · doi:10.1128/iai.00131-17 · Cited by 60 · see citing works
Spreading of a mycobacterial cell-surface lipid into host epithelial membranes promotes infectivity
Cambier, C. J., Banik, S. M., Buonomo, J. A., & Bertozzi, C. R. (2020) · eLife · doi:10.7554/elife.60648 · Cited by 66 · see citing works
Self-citationLahiri, N., Shah-Rohlfs, R., Layre, E., Young, D. C., Ford, C., Murray, M. B., Fortune, S. M., & Moody, D. B. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.716704 · Cited by 66 · see citing works
- 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
- Venue
- Nature
- Published
- 2013-12-15
- Volume
- 505
- Issue
- 7482
- Pages
- 218-222
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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
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
