Cited by 646Immune Response and InflammationTuberculosis Research and EpidemiologyImmune cells in cancer

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Toll-like receptor–induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens

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El Kasmi, Karim C, Qualls, Joseph E, Pesce, John T, Smith, Amber M, Thompson, Robert W, Henao-Tamayo, Marcela, Basaraba, Randall J, König, Till, Schleicher, Ulrike, Koo, Mi-Sun, Kaplan, Gilla, Fitzgerald, Katherine A, Tuomanen, Elaine I, Orme, Ian M, Kanneganti, Thirumala-Devi, Bogdan, Christian, Wynn, Thomas A, Murray, Peter J·2008·Nature Immunology

DOI 10.1038/ni.1671PMC PMC2584974

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Abstract

Toll-like receptor (TLR) signaling in macrophages is required for antipathogen responses, including the biosynthesis of nitric oxide from arginine, and is essential for immunity to Mycobacterium tuberculosis, Toxoplasma gondii and other intracellular pathogens. Here we report a 'loophole' in the TLR pathway that is advantageous to these pathogens. Intracellular pathogens induced expression of the arginine hydrolytic enzyme arginase 1 (Arg1) in mouse macrophages through the TLR pathway. In contrast to diseases dominated by T helper type 2 responses in which Arg1 expression is greatly increased by interleukin 4 and 13 signaling through the transcription factor STAT6, TLR-mediated Arg1 induction was independent of the STAT6 pathway. Specific elimination of Arg1 in macrophages favored host survival during T. gondii infection and decreased lung bacterial load during tuberculosis infection.

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BackgroundMethod
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Background
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Background
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“…induction mechanism in Mycobacterium bovis Bacillus Calmette-Guérin (BCG), which produces yet-unidenti ﬁ ed microbial products that stimulate Toll-like receptors (TLRs) 2 and 4 to induce secretion of IL-6, IL-10, and G-CSF, which in turn activate STAT3 via autocrine/paracrine signaling [59,60].”
Background
Progression and Dissemination of Pulmonary Mycobacterium Avium Infection in a Susceptible Immunocompetent Mouse Model
Rosenbloom, R., Gavrish, I., Tseng, A. E., Seidel, K., Yabaji, S. M., Gertje, H. P., Huber, B. R., Kramnik, I., & Crossland, N. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23115999 · Cited by 10
“However, alternatively activated macrophages (M2) that express Arginase-1 (Arg1) typically associated with the Th2 driven immune response have also been described in TB and NTM granulomas [15,16], where they may play immunomodulatory or pro-fibrotic roles [16,17].”
Background
Osteopontin: an essential regulatory protein in idiopathic pulmonary fibrosis
Zhu, X., Ji, J., & Han, X. (2023) · Journal of Molecular Histology · doi:10.1007/s10735-023-10169-y · Cited by 10
“Moreover, it has been found that Th2 cytokines such as IL-4 and IL-13 induce macrophage M2-type polarization in lung fibrosis (El Kasmi et al. 2008), which may lead to IPF.”
Distinct roles of arginases 1 and 2 in diabetic nephropathy
Morris, S. M., You, H., Gao, T., Vacher, J., Cooper, T. K., & Awad, A. S. (2017) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00158.2017 · Cited by 10
“For example, ablation of arginase-1 expression in macrophages renders mice more susceptible to infection by mycobacteria (8), indicating that long-term treatment with a nonselective arginase inhibitor may compromise host responses to certain pathogens.”
Background
Interactions of helminths with macrophages: therapeutic potential for inflammatory intestinal disease
Smith, H., Forman, R. A., Mair, I., & Else, K. J. (2018) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2018.1505498 · Cited by 11
Mycobacterium Lrp/AsnC family transcriptional factor modulates the arginase pathway as both a sensor and a transcriptional repressor
Yan, S., Zhen, J., Li, Y., Huang, Y., Ai, X., Li, Y., Stojkoska, A., Huang, X. S., Ruan, C., Li, J., et al. (2021) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2021.06.018 · Cited by 9
M-MDSC in vitro generation from mouse bone marrow with IL-3 reveals high expression and functional activity of arginase 1
Aintablian, A., Strozniak, S., Heuer, M., & Lutz, M. B. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1130600 · Cited by 9
“gondii in mouse macrophages by outcompeting iNOS activity, whereas Arg1 deletion reinstalls iNOS activity and results in a better survival of the mice due to increased NO-dependent microbial killing (58).”
Background
Histological and biochemical changes in a rat rotator cuff tear model with or without the subacromial bursa
Miura, Y., Endo, K., & Sekiya, I. (2024) · Tissue and Cell · doi:10.1016/j.tice.2024.102370 · Cited by 9
The arginase-polyamine signaling axis in immune cells: Implications for immune modulation and host-pathogen interactions
Aziz, S., Ahmed, A., Singh, P., & Mukhopadhyay, S. (2025) · iScience · doi:10.1016/j.isci.2025.114363 · Cited by 10
“86,112 Consistent with these findings, researchers observed elevated Arg1 mRNA expression in the lungs of Mtb - infected mice, and Arg1 -deficient mice had reduced Mtb burden, highlighting the protective effect of limiting arginase activity.”
VapC12 ribonuclease toxin modulates host immune response during Mycobacterium tuberculosis infection
Tyagi, S., Sadhu, S., Sharma, T., Paul, A., Pandey, M., Nain, V. K., Rathore, D. K., Chatterjee, S., Awasthi, A., & Pandey, A. K. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1302163 · Cited by 9
Pathogen Strategies to Evade Innate Immune Response: A Signaling Point of View
Miguel, B., Celeste, M. G., & Teresa, M. (2012) · InTech eBooks · doi:10.5772/37771 · Cited by 14
“The pathogens M. tuberculosis and Toxoplasma gondii promote their survival in macrophages, through TLR2-MYD88-dependent induction of IL-6, IL-10 and granulocyte colony-stimulating factor (GCSF) (El Kasmi et al., 2008).”
Human hepatocyte transplantation corrects the inherited metabolic liver disorder arginase deficiency in mice
Angarita, S., Truong, B., Khoja, S., Nitzahn, M., Rajbhandari, A. K., Zhuravka, I., Duarte, S. M., Lin, M. G., Lam, A. K., Cederbaum, S. D., et al. (2018) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2018.04.005 · Cited by 8
“The FRG-CKO arginase mouse was generated by mating the FRG mouse [16] and the conditional arginase knockout (CKO) [18] and screening for homozygosity of the 4 genes; subsequent intercrossing was performed until the complete knockout was obtained (Fah−/−/ Rag2−/−/Il2rγ−/−/Argflox/flox).”
Method
Arginase‐dependent suppression by CpG‐ODN plus IFA‐induced splenic myeloid CD11b+Gr1+ cells
Ranocchia, R. P., Gorlino, C. V., Crespo, M. I., Harman, M. F., Liscovsky, M. V., Morón, G., Maletto, B. A., & Pistoresi-Palencia, M. C. (2011) · Immunology and Cell Biology · doi:10.1038/icb.2011.98 · Cited by 9
Inorganic fraction of oil sands process-affected water induces mammalian macrophage stress gene expression and acutely modulates immune cell functional markers at both the gene and protein levels
Phillips, N., Lillico, D. M. E., Qin, R., McAllister, M., El‐Din, M. G., Belosevic, M., & Stafford, J. L. (2020) · Toxicology in Vitro · doi:10.1016/j.tiv.2020.104875 · Cited by 9
Arginine and NASH – Do macrophages deliver the first hit?
Scheja, L., & Kluwe, J. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.11.001 · Cited by 9
“Induction of iNOS is a hallmark of classically activated (M1) macrophages and type 1 T helper (Th1) cell responses with iNOS producing oxidative stress, thus promoting antipathogen responses [1,2] but also metabolic disorders, such as insulin resistance [3].”
Background
Metabolomic Analysis of Diverse Mice Reveals Hepatic Arginase-1 as Source of Plasma Arginase in Plasmodium chabaudi Infection
Davis, N. M., Lissner, M. M., Massis, L. M., Richards, C. L., Chevée, V., Gupta, A. S., Gherardini, F. C., Monack, D. M., & Schneider, D. S. (2021) · mBio · doi:10.1128/mbio.02424-21 · Cited by 8
“Arg1 floxed mice were purchased from JAX (C.B6-Arg1tm1Pmu/J, stock #008817, El Kasmi et al. 2008) and Cre mice (Tie2: B6.”
BackgroundMethod
From Inflammation to Wound Healing: Using a Simple Model to Understand the Functional Versatility of Murine Macrophages
Childs, L. M., Paskow, M. J., Morris, S. M., Hesse, M., & Strogatz, S. H. (2011) · Bulletin of Mathematical Biology · doi:10.1007/s11538-011-9637-5 · Cited by 8
“This can compromise their ability to control some intracellular microbial pathogens by interfering with the production of NO (El Kasmi et al. 2008).”
Inhibitory effect of citrinin on lipopolisaccharide-induced nitric oxide production by mouse macrophage cells
Sugiyama, K., Yamazaki, R., Kinoshita, M., Kamata, Y., Tani, F., Minai, Y., & Sugita‐Konishi, Y. (2013) · Mycotoxin Research · doi:10.1007/s12550-013-0175-x · Cited by 8
Partial Restoration of Macrophage Alteration from Diet-Induced Obesity in Response to Porphyromonas gingivalis Infection
Richard, G., Trivedi, N. S., Belta, C. A., & Amar, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070320 · Cited by 8
“Induction of Arg1 in macrophages thwarts effective immunity against intracellular pathogens due to the inhibition of macrophage M1 polarization [10,36], consistent with our finding that a specific Arg1 inhibitor (ABH) increased the M1 polarization of BMMW after P.”
Result
Macrophage polarization in lymph node granulomas from cattle and pigs naturally infected with Mycobacterium tuberculosis complex
Larenas‐Muñoz, F., Hamed, M. G., Ruedas‐Torres, I., Sánchez‐Carvajal, J. M., Domı́nguez, J., Pallarés, F. J., Carrasco, L., Rodríguez-Gómez, I. M., & Gómez-Laguna, J. (2024) · Veterinary Pathology · doi:10.1177/03009858241231606 · Cited by 7
Engineered local delivery of extracellular vesicles loaded with si-TNF-α, via a core-sheath 3D-bio-printed scaffold as an effective wound dressing
Vakilian, S., Jamshidi‐Adegani, F., Al‐Fahdi, F., Mirsanei, Z., Al‐Kindi, J., Al-Riyami, K. O., Alwahaibi, N., Shalaby, A., Al‐Harrasi, A., Al‐Sharabi, N., et al. (2024) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2024.106189 · Cited by 8
ATP–NLRP3 inflammasome axis enhances the immunosuppressive effect of myeloid-derived suppressor cells
Ando, T., Sakurai, K., Hoshi, M., Tezuka, H., Sakai, Y., Kato, T., & Ito, H. (2025) · Immunobiology · doi:10.1016/j.imbio.2025.153119 · Cited by 7
Loss of TRIM24 promotes IL-10 expression via CBP/p300-dependent IFNβ1 transcription during macrophage activation
Hui, Z., Fu, Y., Chen, Y., Yin, J., Fang, H., Tu, Y., Gu, Y., & Zhang, J. (2023) · Inflammation Research · doi:10.1007/s00011-023-01751-x · Cited by 7
“gondii infection, however, ARG1 is dispensable for LPS induced sepsis [43].”
Background
4,4’-Methylene diphenyl diisocyanate exposure induces expression of alternatively activated macrophage-associated markers and chemokines partially through Krüppel-like factor 4 mediated signaling in macrophages
Lin, C., Law, B. F., & Hettick, J. M. (2023) · Xenobiotica · doi:10.1080/00498254.2023.2284867 · Cited by 7
“CEBPB binds to the promoter region of M2 macrophage-associated markers such as Arg1 , therefore promoting macrophages towards M2 phenotypes (El Kasmi et al. 2008).”
Background
Flow Cytometric Characterization of Macrophages Infected in vitro with Salmonella enterica Serovar Typhimurium Expressing Red Fluorescent Protein
Brigo, N., Pfeifhofer‐Obermair, C., Demetz, E., Tymoszuk, P., & Weiß, G. (2022) · BIO-PROTOCOL · doi:10.21769/bioprotoc.4440 · Cited by 7
T Cell Hypo-Responsiveness against Leishmania major in MAP Kinase Phosphatase (MKP) 2 Deficient C57BL/6 Mice Does Not Alter the Healer Disease Phenotype
Schroeder, J., McGachy, H. A., Woods, S., Plevin, R. J., & Alexander, J. K. (2013) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002064 · Cited by 7
Alternative activation of macrophages by filarial nematodes is MyD88-independent
Mylonas, K. J., Hoeve, M. A., MacDonald, A. S., & Allen, J. E. (2012) · Immunobiology · doi:10.1016/j.imbio.2012.07.006 · Cited by 7
“The complete absence of arginase activity in LPSreated MyD88−/− BMM are consistent with findings highlighting he importance of TLR-mediated arginase production by microial pathogens (Kasmi et al. 2008).”
Background
Modulation of STAT-1, STAT-3, and STAT-6 activities in THP-1 derived macrophages infected with two Trypanosoma cruzi strains
Oliveira, M. M., Bonturi, C. R., Salu, B. R., Oliva, M. L. V., Mortara, R. A., & Orikaza, C. M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1038332 · Cited by 6
Brief Report: Detection of Urine Lipoarabinomannan Is Associated With Proinflammatory Innate Immune Activation, Impaired Host Defense, and Organ Dysfunction in Adults With Severe HIV-Associated Tuberculosis in Uganda
Cummings, M. J., Bakamutumaho, B., Jain, K., Price, A., Owor, N., Kayiwa, J. T., Namulondo, J., Byaruhanga, T., Muwanga, M., Nsereko, C., et al. (2023) · JAIDS Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/qai.0000000000003159 · Cited by 6
mTOR-Mediated Cell Death and Infection
Li, S., Wang, Q., & Su, B. (2021) · Infectious Microbes & Diseases · doi:10.1097/im9.0000000000000063 · Cited by 6
Metabolomic Characteristics of Nontuberculous Mycobacterial Pulmonary Disease
Kim, J.-E., Chae, W., Kim, J., Yim, J., Cho, J., & Kwak, N. (2024) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiae100 · Cited by 6
Identification of compounds that decrease numbers of Mycobacteria in human macrophages in the presence of serum amyloid P
Xiang, W., Cox, N., & Gomer, R. H. (2017) · Journal of Leukocyte Biology · doi:10.1189/jlb.1a0317-118rr · Cited by 6
Regulation of cells of the arterial wall by hypoxia and its role in the development of atherosclerosis
Norda, S., & Papadantonaki, R. (2022) · VASA · doi:10.1024/0301-1526/a001044 · Cited by 7
Enhancement of Inducible Nitric Oxide Synthase Activity by Low Molecular Weight Peptides Derived from Protamine: A Potential Therapy for Chronic Rhinosinusitis
Balijepalli, A. S., Comstock, A. T., Wang, X., Jensen, G. C., Hershenson, M. B., Zacharek, M. A., Sajjan, U. S., & Meyerhoff, M. E. (2015) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.5b00110 · Cited by 6
Correction: MAP Kinase Phosphatase-2 Plays a Key Role in the Control of Infection with Toxoplasma gondii by Modulating iNOS and Arginase-1 Activities in Mice
Woods, S., Schroeder, J., McGachy, H. A., Plevin, R. J., Roberts, C. W., & Alexander, J. K. (2013) · PLoS Pathogens · doi:10.1371/annotation/408bc3ff-0000-4e72-b4fb-839c6c848178 · Cited by 6
Arginine as host directed therapy in tuberculosis: insights from modulating arginine metabolism by supplementation and arginase inhibition
Jiang, Q., Kumar, R., Zhao, Y. P., Subbian, S., & Shi, L. (2025) · One Health Advances · doi:10.1186/s44280-025-00070-6 · Cited by 5
“Studies show that Mtb exploits this competition by upregulating Arg1 expression, thereby limiting NO production and impairing bacterial clearance [11].”
Divergent roles of red cell arginase in humans and mice: RBC Arg1 KO mice show preserved systemic l-arginine bioavailability and infarct size in vivo
Heuser, S. K., Li, J., Li, Z., LoBue, A., Heard, K., Hocks, J., Suvorava, T., Cadeddu, R., Strupp, C., Dunaway, L. S., et al. (2025) · Redox Biology · doi:10.1016/j.redox.2025.103768 · Cited by 5
“Arg1 flox/flox mice were purchased from the Jackson Laboratory (Jax stock: 008817) [48].”
HIF-2α Blows Out the Flames of Adipose Tissue Macrophages to Keep Obesity in a Safe Zone
Aouadi, M. (2014) · Diabetes · doi:10.2337/db14-0878 · Cited by 5
“Therefore, ARG1 activity can decrease NO production via the limitation of arginine availability (18).”
Background
Lysosomal acidity and cathepsin L activate eosinophils via ARG1-mediated arginine metabolism in allergic airway inflammation
Han, Y., Li, N., Zhao, Y. F., Jin, Z., Lv, B., Shen, D., Chen, X., Weng, Q., Zhang, M., Chen, K., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65400-z · Cited by 5
Fasciola hepatica GST mu-class suppresses the cytokine storm induced by E. coli -lipopolysaccharide, whereas it modulates the dynamic of peritoneal macrophages in a mouse model and suppresses the classical activation of macrophages
Valdés‐Fernández, B. N., Ruiz‐Jiménez, C., Armina-Rodríguez, A., Méndez, L. B., & Espino, A. M. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.03475-23 · Cited by 5
Unbalanced Arginine pathway and altered maturation of pleural macrophages in Th2-deficient mice during Litomosoides sigmodontis filarial infection
Remion, E., Gal, J., Chaouch, S., Rodrigues, J., Vallarino-Lhermitte, N., Alonso, J., Kohl, L., Hübner, M. P., Fercoq, F., & Martin, C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.866373 · Cited by 4
“This highlights previous reports indicating that Arg1 can be induced independently of IL4R signaling and supports the use of multiple markers when assessing macrophage activation status (70, 71).”
Background
M. tuberculosis curli pili (MTP) facilitates a reduction of microbicidal activity of infected THP-1 macrophages during early stages of infection
Ashokcoomar, S., Reedoy, K., Loots, D. T., Beukes, D., van Reenen, M., Pillay, B., & Pillay, M. (2022) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2022.101907 · Cited by 4
A review of tuberculosis and parasitic disease co-infection in ungulates, with regard to the potential threat to European bison ( Bison bonasus)
Gałązka, M., Didkowska, A., Anusz, K., & Pyziel, A. M. (2023) · Polish Journal of Veterinary Sciences · doi:10.24425/pjvs.2023.145018 · Cited by 4
Interactions Between Toxoplasma Effectors and Host Immune Responses
Butcher, B. A., Reese, M. L., Boothroyd, J. C., & Denkers, E. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-396481-6.00014-3 · Cited by 5

Authors: El Kasmi, K. C., Qualls, J. E., Pesce, J. T., Smith, A. M., Thompson, R. W., Henao-Tamayo, M., Basaraba, R. J., König, T., Schleicher, U., Koo, M.-S., Kaplan, G., Fitzgerald, K. A., Tuomanen, E. I., Orme, I. M., Kanneganti, T.-D., Bogdan, C., Wynn, T. A., & Murray, P. J.
Affiliations: St. Jude Children's Research Hospital (US)
National Institutes of Health (US)
Colorado State University (US)
University Medical Center Freiburg (DE)
Universitätsklinikum Erlangen (DE)
University of Medicine and Dentistry of New Jersey (US)
University of Massachusetts Chan Medical School (US)
Corresponding author: Wynn, Thomas A
Murray, Peter J
ORCID: Qualls, Joseph E
Smith, Amber M
Henao-Tamayo, Marcela
Basaraba, Randall J
Schleicher, Ulrike
Fitzgerald, Katherine A
Tuomanen, Elaine I
Kanneganti, Thirumala-Devi
Bogdan, Christian
Wynn, Thomas A
Murray, Peter J
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2008-11-02
Volume: 9
Issue: 12
Pages: 1399-1406
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni.1671
PMC: PMC2584974
OpenAlex: W2038461328
Cited by: 646
References: 50
Citations by year: 2026: 18 · 2025: 20 · 2024: 19 · 2023: 33 · 2022: 25 · 2021: 48 · 2020: 34 · 2019: 35 · 2018: 32 · 2017: 29 · 2016: 52 · 2015: 51 · 2014: 52 · 2013: 49 · 2012: 39
FWCI: 13.66
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship@UMassChan (submittedVersion)
Funders: National Institutes of Health
National Cancer Institute (P30CA021765)
National Institute of Allergy and Infectious Diseases (AI27913, R01AI027913, AI062921, R01AI066046, AI66046, R01AI062921)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords: arginase-1, Toll-like receptor signaling, macrophages, intracellular pathogens, Mycobacterium tuberculosis, Toxoplasma gondii, nitric oxide, STAT6, host-pathogen interaction, tuberculosis, toxoplasmosis, lung bacterial load
MeSH terms: Animals, Arginase, Bacterial Infections, Immunohistochemistry, Macrophages, Immunoblotting, Mice, Knockout, CCAAT-Enhancer-Binding Protein-beta, STAT6 Transcription Factor, Toll-Like Receptors, Mice, Myeloid Differentiation Factor 88

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Toll-like receptor–induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens

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