Regulation of immune responses by L-arginine metabolism

Bronte, Vincenzo; Zanovello, Paola

doi:10.1038/nri1668

Cited by 1,775Immune cells in cancerAmino Acid Enzymes and MetabolismCancer Research and Treatments

Regulation of immune responses by L-arginine metabolism

Bronte, Vincenzo, Zanovello, Paola·2005·Nature Reviews Immunology

DOI 10.1038/nri1668

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Abstract

L-Arginine is an essential amino acid for birds and young mammals, and it is a conditionally essential amino acid for adult mammals, as it is important in situations in which requirements exceed production, such as pregnancy. Recent findings indicate that increased metabolism of L-arginine by myeloid cells can result in the impairment of lymphocyte responses to antigen during immune responses and tumour growth. Two enzymes that compete for L-arginine as a substrate - arginase and nitric-oxide synthase - are crucial components of this lymphocyte-suppression pathway, and the metabolic products of these enzymes are important moderators of T-cell function. This Review article focuses on the relevance of L-arginine metabolism by myeloid cells for immunity under physiological and pathological conditions.

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Neutrophils, by releasing arginase or ROS, can inhibit NK-cell or T-cell activation by depriving extracellular levels of L-arginine, necessary for T-cell activation.
“Along with activation of innate or adaptive immune cells, neutrophils, by releasing arginase or ROS, can inhibit NK-cell or T-cell activation by depriving extracellular levels of L-arginine, necessary for T-cell activation [225].”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [225]

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Natural Suppressor (NS) Cells, Neonatal Tolerance, and Total Lymphoid Irradiation: Exploring Obscure Relationships
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A Defect in Tryptophan Catabolism Impairs Tolerance in Nonobese Diabetic Mice
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Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1+)CD11b+ immature myeloid suppressor cells
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Cytokine and nitric oxide regulation of the immunosuppression in Trypanosoma cruzi infection
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Sepsis: An arginine deficiency state?
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Cooperative Role of Interferon Regulatory Factor 1 and p91 (STAT1) Response Elements in Interferon-γ-inducible Expression of Human Indoleamine 2,3-Dioxygenase Gene
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Arginases in parasitic diseases
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Immortalized Myeloid Suppressor Cells Trigger Apoptosis in Antigen-Activated T Lymphocytes
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Nitric oxide and thiol redox regulation of Janus kinase activity
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Vitamin A deficiency in mice causes a systemic expansion of myeloid cells
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Reactive Oxygen Species and 12/15-Lipoxygenase Contribute to the Antiproliferative Capacity of Alternatively Activated Myeloid Cells Elicited during Helminth Infection
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Cytokine Expanded Myeloid Precursors Function as Regulatory Antigen-Presenting Cells and Promote Tolerance through IL-10-Producing Regulatory T Cells
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CD80+Gr-1+ Myeloid Cells Inhibit Development of Antifungal Th1 Immunity in Mice with Candidiasis
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Potential cardioprotective actions of no-releasing aspirin
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Role of Immature Myeloid Gr-1+ Cells in the Development of Antitumor Immunity
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Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents
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Chemoprevention of prostate carcinogenesis by alpha-difluoromethylornithine in TRAMP mice.
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CTLA-4–Ig Activates Forkhead Transcription Factors and Protects Dendritic Cells from Oxidative Stress in Nonobese Diabetic Mice
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Sustained exposure to bacterial antigen induces interferon-γ-dependent T cell receptor ζ down-regulation and impaired T cell function
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Helicobacter pylori Arginase Inhibits T Cell Proliferation and Reduces the Expression of the TCR ζ-Chain (CD3ζ)
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Inducible nitric oxide synthase in T cells regulates T cell death and immune memory
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Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice
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Classical and Slow-Binding Inhibitors of Human Type II Arginase
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Nitric Oxide-Mediated Regulation of Gamma Interferon-Induced Bacteriostasis: Inhibition and Degradation of Human Indoleamine 2,3-Dioxygenase
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Expansion of Myeloid Suppressor Cells in SHIP-Deficient Mice Represses Allogeneic T Cell Responses
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Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice
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Cyclophosphamide Induces the Development of Early Myeloid Cells Suppressing Tumor Cell Growth by a Nitric Oxide-Dependent Mechanism
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Superantigen-Induced CD4 T Cell Tolerance Mediated by Myeloid Cells and IFN-γ
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Activation of cGMP-dependent Protein Kinase Iβ Inhibits Interleukin 2 Release and Proliferation of T Cell Receptor-stimulated Human Peripheral T Cells
Fischer, T. A., Palmetshofer, A., Gambaryan, S. P., Butt, E., Jassoy, C., Walter, U., Sopper, S., & Lohmann, S. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009781200 · Cited by 86 · see citing works
In vivo and in vitro apoptosis of human thymocytes are associated with nitrotyrosine formation
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Activation of the Stem Cell-Derived Tyrosine Kinase/RON Receptor Tyrosine Kinase by Macrophage-Stimulating Protein Results in the Induction of Arginase Activity in Murine Peritoneal Macrophages
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ALTERATIONS IN ARGININE METABOLIC ENZYMES IN TRAUMA
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Myelopoiesis-associated immune suppressor cells in mice bearing metastatic Lewis lung carcinoma tumors: gamma interferon plus tumor necrosis factor alpha synergistically reduces immune suppressor and tumor growth-promoting activities of bone marrow cells and diminishes tumor recurrence and metastasis.
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Murine Graft‐versus‐Host Disease across Minor Barriers: Immunosuppressive Aspects of Natural Suppressor Cells
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Antioxidant Treatment Reduces Expansion and Contraction of Antigen-Specific CD8+T Cells during Primary but Not Secondary Viral Infection
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Immunocompromised tumor-bearing mice show a selective loss of STAT5a/b expression in T and B lymphocytes
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Cutting Edge: HIV-1 Infection Induces a Selective Reduction in STAT5 Protein Expression
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Arginine metabolic pathways involved in the modulation of tumor‐induced angiogenesis by macrophages
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Control of the Autoimmune Response by Type 2 Nitric Oxide Synthase
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Arginase AI Is Upregulated in Acute Immune Complex-Induced Inflammation
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Myeloid-derived-suppressor cells as regulators of the immune system
Gabrilovich, D. I., & Nagaraj, S. (2009) · Nature Reviews Immunology · doi:10.1038/nri2506 · Cited by 6,753 · see citing works
Obesity induces a phenotypic switch in adipose tissue macrophage polarization
Lumeng, C. N., Bodzin, J. L., & Saltiel, A. R. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29881 · Cited by 4,664 · see citing works
Coordinated regulation of myeloid cells by tumours
Gabrilovich, D. I., Ostrand-Rosenberg, S., & Bronte, V. (2012) · Nature Reviews Immunology · doi:10.1038/nri3175 · Cited by 3,544 · see citing works
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Amino acids: Metabolism, functions, and nutrition
Wu, G. (2009) · Amino Acids · doi:10.1007/s00726-009-0269-0 · Cited by 3,004 · see citing works
Human nutrition, the gut microbiome and the immune system
Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., & Gordon, J. I. (2011) · Nature · doi:10.1038/nature10213 · Cited by 2,588 · see citing works
Macrophages as regulators of tumour immunity and immunotherapy
DeNardo, D. G., & Ruffell, B. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0127-6 · Cited by 2,542 · see citing works
Differential Roles of M1 and M2 Microglia in Neurodegenerative Diseases
Tang, Y., & Le, W. (2016) · Molecular Neurobiology · doi:10.1007/s12035-014-9070-5 · Cited by 2,190 · see citing works
The metabolic signature of macrophage responses
Viola, A., Munari, F., Sánchez-Rodríguez, R., Scolaro, T., & Castegna, A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01462 · Cited by 2,021 · see citing works
L-Arginine Modulates T Cell Metabolism and Enhances Survival and Anti-tumor Activity
Geiger, R., Rieckmann, J. C., Wolf, T., Basso, C., Feng, Y., Fuhrer, T., Kogadeeva, M., Picotti, P., Meissner, F., Mann, M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.031 · Cited by 1,775 · see citing works
Myeloid-Derived Suppressor Cells: Linking Inflammation and Cancer
Ostrand‐Rosenberg, S., & Sinha, P. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802740 · Cited by 1,733 · see citing works
Inhibitory B7-family molecules in the tumour microenvironment
Zou, W., & Chen, L. (2008) · Nature Reviews Immunology · doi:10.1038/nri2326 · Cited by 1,608 · see citing works
Amino acids and immune function
Li, P., Yin, Y., Li, D., Kim, S. W., & Wu, G. (2007) · British Journal Of Nutrition · doi:10.1017/s000711450769936x · Cited by 1,588 · see citing works
Macrophages: master regulators of inflammation and fibrosis
Wynn, T., & Barron, L. (2010) · Seminars in Liver Disease · doi:10.1055/s-0030-1255354 · Cited by 1,392 · see citing works
Cancer despite immunosurveillance: immunoselection and immunosubversion
Zitvogel, L., Tesniere, A., & Kroemer, G. (2006) · Nature reviews. Immunology · doi:10.1038/nri1936 · Cited by 1,324 · see citing works
The cancer metabolic reprogramming and immune response
Xia, L., Oyang, L., Lin, J., Tan, S., Han, Y., Wu, N., Yi, P., Tang, L., Pan, Q., Rao, S., et al. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01316-8 · Cited by 1,312 · see citing works
Altered macrophage differentiation and immune dysfunction in tumor development
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Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell–suppressive activity
Movahedi, K., Guilliams, M., den Bossche, J. V., den Bergh, R. V., Gysemans, C. A., Beschin, A., BAETSELIER, P. D., & Ginderachter, J. A. V. (2008) · Blood · doi:10.1182/blood-2007-07-099226 · Cited by 1,234 · see citing works
HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment
Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J., Youn, J.-I., Cheng, P., Cho, H.-I., Celis, E., Quiceno, D. G., Padhya, T., et al. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20100587 · Cited by 1,173 · see citing works
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“…2C) and produced high levels of nitrite upon culture (Figure 2D), suggesting expression of inducible nitric oxide synthase (iNOS); both arginase and iNOS have been previously linked to immunosuppression by Gr-1 + CD11b + cells in tumor-bearing mice (Bronte and Zanovello, 2005; Ma et al., 2011).”
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Arginine Metabolism in Myeloid Cells Shapes Innate and Adaptive Immunity
Rodrı́guez, P. C., Ochoa, A. C., & Al-Khami, A. A. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00093 · Cited by 287 · see citing works
Role of arginine metabolism in immunity and immunopathology
Peranzoni, E., Marigo, I., Dolcetti, L., Ugel, S., Sonda, N., Taschin, E., Mantelli, B., Bronte, V., & Zanovello, P. (2007) · Immunobiology · doi:10.1016/j.imbio.2007.09.008 · Cited by 178 · see citing works
Self-citation

Authors: Bronte, V., & Zanovello, P.
Affiliations: University of Padua (IT)
Corresponding author: Bronte, Vincenzo
ORCID: Bronte, Vincenzo
Zanovello, Paola
Venue: Nature Reviews Immunology
Publisher: Springer Science and Business Media LLC
Published: 2005-08
Volume: 5
Issue: 8
Pages: 641-654
ISSN: 1474-1733 (ISSN-L)
1474-1741
DOI: 10.1038/nri1668
OpenAlex: W1977179270
Cited by: 1,775
References: 146
Citations by year: 2026: 69 · 2025: 78 · 2024: 75 · 2023: 96 · 2022: 81 · 2021: 114 · 2020: 100 · 2019: 92 · 2018: 97 · 2017: 89 · 2016: 119 · 2015: 92 · 2014: 95 · 2013: 96 · 2012: 97
FWCI: 3.93
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Immunology (publishedVersion)
PubMed (publishedVersion)
Padua Research Archive (University of Padova) (submittedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
Keywords: arginine metabolism, immune regulation, arginase, nitric oxide synthase, myeloid cells, T cell function, lymphocyte suppression, tumor growth, immunosuppression, essential amino acids
MeSH terms: Animals, Arginase, Arginine, Humans, Immunity, Cellular, Suppressor Factors, Immunologic, T-Lymphocytes, Reactive Oxygen Species, Nitric Oxide Synthase, Myeloid Cells, Reactive Nitrogen Species

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Regulation of immune responses by L-arginine metabolism

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