IL-17 family cytokines and the expanding diversity of effector T cell lineages

Weaver, Casey T.; Hatton, Robin D.; Mangan, Paul R.; Harrington, Laurie E.

doi:10.1146/annurev.immunol.25.022106.141557

Cited by 1,842Psoriasis: Treatment and PathogenesisT-cell and B-cell ImmunologyIL-33, ST2, and ILC Pathways

IL-17 family cytokines and the expanding diversity of effector T cell lineages

Weaver, Casey T., Hatton, Robin D., Mangan, Paul R., Harrington, Laurie E.·2007·Annual Review of Immunology

DOI 10.1146/annurev.immunol.25.022106.141557

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Abstract

Since its conception two decades ago, the Th1-Th2 paradigm has provided a framework for understanding T cell biology and the interplay of innate and adaptive immunity. Naive T cells differentiate into effector T cells with enhanced functional potential for orchestrating pathogen clearance largely under the guidance of cytokines produced by cells of the innate immune system that have been activated by recognition of those pathogens. This secondary education of post-thymic T cells provides a mechanism for appropriately matching adaptive immunity to frontline cues of the innate immune system. Owing in part to the rapid identification of novel cytokines of the IL-17 and IL-12 families using database searches, the factors that specify differentiation of a new effector T cell lineage-Th17-have now been identified, providing a new arm of adaptive immunity and presenting a unifying model that can explain many heretofore confusing aspects of immune regulation, immune pathogenesis, and host defense.

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IL-17, Produced by Lymphocytes and Neutrophils, Is Necessary for Lipopolysaccharide-Induced Airway Neutrophilia: IL-15 as a Possible Trigger
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Prevention of experimental autoimmune encephalomyelitis by antibodies against interleukin 12.
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An Interleukin (IL)-10/IL-12 Immunoregulatory Circuit Controls Susceptibility to Autoimmune Disease
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THE EVOLUTION OF ADAPTIVE IMMUNITY
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Thymic Origin of Intestinal αß T Cells Revealed by Fate Mapping of RORγt + Cells
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The IL-27R (WSX-1) Is Required to Suppress T Cell Hyperactivity during Infection
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Basophils Produce IL-4 and Accumulate in Tissues after Infection with a Th2-inducing Parasite
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IL-17E, a Novel Proinflammatory Ligand for the IL-17 Receptor Homolog IL-17Rh1
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IL-1-Independent Role of IL-17 in Synovial Inflammation and Joint Destruction During Collagen-Induced Arthritis
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Lymphokine-mediated regulation of the proliferative response of clones of T helper 1 and T helper 2 cells.
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Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract
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Cloning and characterization of IL-17B and IL-17C, two new members of the IL-17 cytokine family
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Requirement of tumor necrosis factor receptor-associated factor (TRAF)6 in interleukin 17 signal transduction
Schwandner, R., Yamaguchi, K., & Cao, Z. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.7.1233 · Cited by 349 · see citing works
GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells
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Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system
Voehringer, D., Reese, T. A., Huang, X., Shinkai, K., & Locksley, R. M. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20052448 · Cited by 349 · see citing works
Cutting edge: IL-17D, a novel member of the IL-17 family, stimulates cytokine production and inhibits hemopoiesis
Starnes, T., Broxmeyer, H. E., Robertson, M. J., & Hromas, R. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.2.642 · Cited by 331 · see citing works
IL-27 and IFN- α Signal via Stat1 and Stat3 and Induce T-Bet and IL-12R β 2 in Naive T Cells
Hibbert, L., Pflanz, S., Malefyt, R. D. W., & Kastelein, R. A. (2003) · Journal of Interferon & Cytokine Research · doi:10.1089/10799900360708632 · Cited by 318 · see citing works
Blocking of Interleukin-17 during Reactivation of Experimental Arthritis Prevents Joint Inflammation and Bone Erosion by Decreasing RANKL and Interleukin-1
Koenders, M. I., Lubberts, E., Oppers‐Walgreen, B., van den Bersselaar, L., Helsen, M. M. A., Padova, F. E. D., Boots, A. M. H., Gram, H., Joosten, L. A. B., & van den Berg, W. B. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62961-6 · Cited by 310 · see citing works
Induction of Experimental Autoimmune Encephalomyelitis in IL-12 Receptor-β2-Deficient Mice: IL-12 Responsiveness Is Not Required in the Pathogenesis of Inflammatory Demyelination in the Central Nervous System
Zhang, G., Gran, B., Yu, S., Li, J., Siglienti, I., Chen, X., Kamoun, M., & Rostami, A. M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.4.2153 · Cited by 305 · see citing works
Studies with IL-10-/- mice: an overview
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MOLECULAR CHARACTERIZATION OF THE HUMAN INTERLEUKIN (Il)-17 RECEPTOR
Yao, Z., Spriggs, M. K., Derry, J. M. J., Strockbine, L. D., Park, L. S., VandenBos, T., Zappone, J., Painter, S. L., & Armitage, R. J. (1997) · Cytokine · doi:10.1006/cyto.1997.0240 · Cited by 280 · see citing works
Molecular Phylogeny within Type I Cytokines and Their Cognate Receptors
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Nuclear Hormone Receptors in T Lymphocytes
Winoto, A., & Littman, D. R. (2002) · Cell · doi:10.1016/s0092-8674(02)00710-9 · Cited by 260 · see citing works
IL-18–stimulated GADD45β required in cytokine-induced, but not TCR-induced, IFN-γ production
Yang, J., Zhu, H., Murphy, T. L., Ouyang, W., & MURPHY, K. M. M. (2001) · Nature Immunology · doi:10.1038/84264 · Cited by 238 · see citing works
A Novel Cytokine Receptor-Ligand Pair
Shi, Y., Ullrich, S. J., Zhang, J., Connolly, K., Grzegorzewski, K. J., Barber, M. C., Wang, W., Wathen, K., Hodge, V., Fisher, C. L., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910228199 · Cited by 232 · cited 2× · see citing works
“IL-17B and IL-17C do not appear to be products of lymphocytes, but they may be recruited indirectly by IL-17A and IL-17F and have a number of overlapping activities with these family members (47, 51, 61, 62).”
Background
Effect of targeted disruption of STAT4 and STAT6 on the induction of experimental autoimmune encephalomyelitis
Chitnis, T., Najafian, N., Benou, C., Salama, A. D., Grusby, M. J., Sayegh, M. H., & Khoury, S. J. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12563 · Cited by 230 · see citing works
IL-27 Limits IL-2 Production during Th1 Differentiation
Villarino, A. V., Stumhofer, J. S., Saris, C. J. M., Kastelein, R. A., de Sauvage, F. J., & Hunter, C. A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.1.237 · Cited by 216 · see citing works
Further Checkpoints in Th1 Development
Robinson, D. S., & O’Garra, A. (2002) · Immunity · doi:10.1016/s1074-7613(02)00331-x · Cited by 204 · see citing works
Helper T cells regulate type-2 innate immunity in vivo
Shinkai, K., Mohrs, M., & Locksley, R. M. (2002) · Nature · doi:10.1038/nature01202 · Cited by 201 · see citing works
Regulatory T Cell Suppression and Anergy Are Differentially Regulated by Proinflammatory Cytokines Produced by TLR-Activated Dendritic Cells
Kubo, T., Hatton, R. D., Oliver, J. R., Liu, X., Elson, C. O., & Weaver, C. T. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.12.7249 · Cited by 201 · see citing works
Self-citation
Induction of interferon-γ production in Th1 CD4+ T cells: evidence for two distinct pathways for promoter activation
Yang, J., Murphy, T. L., Ouyang, W., & MURPHY, K. M. M. (1999) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199902)29:02 · Cited by 195 · see citing works
Origins of the TH1-TH2 model: a personal perspective
Coffman, R. L. (2006) · Nature Immunology · doi:10.1038/ni0606-539 · Cited by 192 · see citing works
Silencing T-bet Defines a Critical Role in the Differentiation of Autoreactive T Lymphocytes
Lovett‐Racke, A. E., Rocchini, A., Choy, J., Northrop, S. C., Hussain, R. Z., Ratts, R. B., Sikder, D. S., & Racke, M. K. (2004) · Immunity · doi:10.1016/j.immuni.2004.09.010 · Cited by 183 · see citing works
IL-18 Directs Autoreactive T Cells and Promotes Autodestruction in the Central Nervous System Via Induction of IFN-γ by NK Cells
Shi, F., Takeda, K., Akira, S., Sarvetnick, N., & Ljunggren, H. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.6.3099 · Cited by 178 · see citing works
Essential Role of GATA3 for the Maintenance of Type 2 Helper T (Th2) Cytokine Production and Chromatin Remodeling at the Th2 Cytokine Gene Loci
Yamashita, M., Ukai‐Tadenuma, M., Miyamoto, T. K., Sugaya, K., Hosokawa, H., Hasegawa, A., Kimura, M. Y., Taniguchi, M., DeGregori, J. V., & Nakayama, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m403688200 · Cited by 160 · see citing works
Interleukin 18–independent engagement of interleukin 18 receptor-α is required for autoimmune inflammation
Gutcher, I., Urich, E., Wolter, K., Prinz, M., & Becher, B. (2006) · Nature Immunology · doi:10.1038/ni1377 · Cited by 158 · see citing works
IL-12– and IL-23–induced T helper cell subsets
Bettelli, E., & Kuchroo, V. K. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20042279 · Cited by 144 · see citing works
TGFβ1, a ‘Jack of all trades’: the link with pro-inflammatory IL-17-producing T cells
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Antibodies Against IL-12 Prevent Superantigen-Induced and Spontaneous Relapses of Experimental Autoimmune Encephalomyelitis
Constantinescu, C. S., Wysocka, M., Hilliard, B. A., Ventura, E. S., Lavi, E., Trinchieri, G., & Rostami, A. M. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.9.5097 · Cited by 144 · see citing works
Pathogen-induced Th1 phenotype development in CD4+ αβ-TCR transgenic T cells is macrophage dependent
Hsleh, C.-S., Macatonia, S. E., O’Garra, A., & MURPHY, K. M. M. (1993) · International Immunology · doi:10.1093/intimm/5.4.371 · Cited by 134 · see citing works
Soluble and Transmembrane Isoforms of Novel Interleukin-17 Receptor-like Protein by RNA Splicing and Expression in Prostate Cancer
Haudenschild, D. R., Moseley, T. A., Rose, L., & Reddi, A. H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109372200 · Cited by 133 · see citing works
Identification, cloning and characterization of interleukin-17 and its family from zebrafish
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Cutting Edge: Evidence for Ligand-Independent Multimerization of the IL-17 Receptor
Kramer, J. M., Yi, L., Shen, F., Maitra, A., Jiao, X., Jin, T., & Gaffen, S. L. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.2.711 · Cited by 115 · see citing works
Direct cloning and extended culture of antigen-specific MHC-restricted, proliferating T lymphocytes
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Cellular and humoral immunity to Leishmania major in genetically susceptible mice after in vivo depletion of L3T4+ T cells.
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Enhanced autoimmune arthritis in IFN-gamma receptor-deficient mice is conditioned by mycobacteria in Freund's adjuvant and by increased expansion of Mac-1+ myeloid cells.
Matthys, P., Vermeire, K., Mitera, T., Heremans, H., Huang, S., Schols, D., Wolf-Peeters, C. D., & Billiau, A. (1999) · PubMed · Cited by 95 · see citing works
Induction of cartilage damage by overexpression of T cell interleukin‐17A in experimental arthritis in mice deficient in interleukin‐1
Koenders, M. I., Lubberts, E., Oppers‐Walgreen, B., van den Bersselaar, L., Helsen, M. M. A., Kolls, J. K., Joosten, L. A. B., & van den Berg, W. B. (2005) · Arthritis & Rheumatism · doi:10.1002/art.20885 · Cited by 92 · see citing works
Reduced susceptibility to collagen-induced arthritis in mice deficient in IFN-gamma receptor.
Kageyama, Y., Koide, Y., Yoshida, A., Uchijima, M., Arai, T., Miyamoto, S., Ozeki, T., Hiyoshi, M., KUSHIDA, K., & Inoue, T. M. N. (1998) · PubMed · Cited by 86 · see citing works
Enhanced Autoimmune Arthritis in IFN-γ Receptor-Deficient Mice Is Conditioned by Mycobacteria in Freund’s Adjuvant and by Increased Expansion of Mac-1+ Myeloid Cells
Matthys, P., Vermeire, K., Mitera, T., Heremans, H., Huang, S., Schols, D., Wolf‐Peeters, C. D., & Billiau, A. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.6.3503 · Cited by 84 · see citing works
An Absolute Requirement for STAT4 and a Role for IFN-γ as an Amplifying Factor in IL-12 Induction of the Functional IL-18 Receptor Complex
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Reduced Susceptibility to Collagen-Induced Arthritis in Mice Deficient in IFN-γ Receptor
Kageyama, Y., Koide, Y., Yoshida, A., Uchijima, M., Arai, T., Miyamoto, S., Ozeki, T., Hiyoshi, M., KUSHIDA, K., & Inoue, T. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.3.1542 · Cited by 74 · see citing works
Evi27 encodes a novel membrane protein with homology to the IL17 receptor
Tian, E., Sawyer, J. R., Largaespada, D. A., Jenkins, N. A., Copeland, N. G., & Shaughnessy, J. D. (2000) · Oncogene · doi:10.1038/sj.onc.1203577 · Cited by 67 · see citing works
Expression of IL-17B in neurons and evaluation of its possible role in the chromosome 5q-linked form of Charcot–Marie–Tooth disease
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Recognition strategies in the innate immune system of ancestral chordates
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Purified Fc epsilon R+ bone marrow and splenic non-B, non-T cells are highly enriched in the capacity to produce IL-4 in response to immobilized IgE, IgG2a, or ionomycin
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The TNF receptor family member CD27 signals to Jun N-terminal kinase via Traf-2
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Flagged first, then by citations

Sorted by citations

Heat Shock Protein A12B Protects Vascular Endothelial Cells Against Sepsis-Induced Acute Lung Injury in Mice
Chen, Y., Wang, L., Kang, Q., Zhang, X., Yu, G., Wan, X., Wang, J., & Zhu, K. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000477308 · Cited by 10,730 · see citing works
Unravelling the pathogenesis of inflammatory bowel disease
Xavier, R. J., & Podolsky, D. K. (2007) · Nature · doi:10.1038/nature06005 · Cited by 4,364 · see citing works
Recognition of microorganisms and activation of the immune response
Medzhitov, R. (2007) · Nature · doi:10.1038/nature06246 · Cited by 2,862 · see citing works
Follicular Helper CD4 T Cells (T FH )
Crotty, S. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101400 · Cited by 2,738 · see citing works
Cytokines in the pathogenesis of rheumatoid arthritis
McInnes, I. B., & Schett, G. A. (2007) · Nature reviews. Immunology · doi:10.1038/nri2094 · Cited by 2,523 · see citing works
Phenotypic and functional features of human Th17 cells
Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E., Filì, L., Ferri, S., Frosali, F., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070663 · Cited by 1,861 · see citing works
TGF-β-induced Foxp3 inhibits TH17 cell differentiation by antagonizing RORγt function
Zhou, L., Lopes, J. E., Chong, M. M. W., Ivanov, I. I., Min, R., Victora, G. D., Shen, Y., Du, J., Rubtsov, Y. P., Rudensky, A. Y., et al. (2008) · Nature · doi:10.1038/nature06878 · Cited by 1,859 · see citing works
Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17–producing human T helper cells
Acosta-Rodriguez, E. V., Napolitani, G., Lanzavecchia, A., & Sallusto, F. (2007) · Nature Immunology · doi:10.1038/ni1496 · Cited by 1,857 · see citing works
IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells
Korn, T., Bettelli, E., Gao, W., Awasthi, A., Jäger, A., Strom, T. B., Oukka, M., & Kuchroo, V. K. (2007) · Nature · doi:10.1038/nature05970 · Cited by 1,841 · see citing works
Surface phenotype and antigenic specificity of human interleukin 17–producing T helper memory cells
Acosta-Rodriguez, E. V., Rivino, L., Geginat, J., Jarrossay, D., Gattorno, M., Lanzavecchia, A., Sallusto, F., & Napolitani, G. (2007) · Nature Immunology · doi:10.1038/ni1467 · Cited by 1,828 · see citing works
A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses
Wu, S., Rhee, K.-J., Albesiano, E., Rabizadeh, S., Wu, X., Yen, H.-R., Huso, D. L., Brancati, F. L., Wick, E., McAllister, F., et al. (2009) · Nature Medicine · doi:10.1038/nm.2015 · Cited by 1,812 · see citing works
Inflammatory bowel disease
Kaser, A., Zeissig, S., & Blumberg, R. S. (2010) · Annual Review of Immunology · doi:10.1146/annurev-immunol-030409-101225 · Cited by 1,806 · see citing works
Specific Microbiota Direct the Differentiation of IL-17-Producing T-Helper Cells in the Mucosa of the Small Intestine
Ivanov, I. I., Frutos, R. D. L., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., Finlay, B. B., & Littman, D. R. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.09.009 · Cited by 1,770 · see citing works
The Biological Functions of T Helper 17 Cell Effector Cytokines in Inflammation
Ouyang, W., Kolls, J. K., & Zheng, Y. (2008) · Immunity · doi:10.1016/j.immuni.2008.03.004 · Cited by 1,698 · see citing works
Control of TH17/Treg Balance by Hypoxia-Inducible Factor 1
Dang, E. V., Barbi, J., Yang, H.-Y., Jinasena, D., Yu, H., Zheng, Y., Bordman, Z., Fu, J., Kim, Y., Yen, H.-R., et al. (2011) · Cell · doi:10.1016/j.cell.2011.07.033 · Cited by 1,595 · see citing works
The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing
Gaffen, S. L., Jain, R., Garg, A. V., & Cua, D. J. (2014) · Nature reviews. Immunology · doi:10.1038/nri3707 · Cited by 1,585 · see citing works
Innate IL-17-producing cells: the sentinels of the immune system
Cua, D. J., & Tato, C. M. (2010) · Nature reviews. Immunology · doi:10.1038/nri2800 · Cited by 1,578 · see citing works
Plasticity of CD4+ T Cell Lineage Differentiation
Zhou, L., Chong, M. M. W., & Littman, D. R. (2009) · Immunity · doi:10.1016/j.immuni.2009.05.001 · Cited by 1,551 · see citing works
Skin immune sentinels in health and disease
Nestle, F. O., Meglio, P. D., Qin, J., & Nickoloff, B. J. (2009) · Nature reviews. Immunology · doi:10.1038/nri2622 · Cited by 1,431 · see citing works
Generation of pathogenic TH17 cells in the absence of TGF-β signalling
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Authors: Weaver, C. T., Hatton, R. D., Mangan, P. R., & Harrington, L. E.
Affiliations: University of Alabama at Birmingham (US)
ORCID: Weaver, Casey T.
Hatton, Robin D.
Harrington, Laurie E.
Venue: Annual Review of Immunology
Publisher: Annual Reviews
Published: 2007-04-01
Volume: 25
Issue: 1
Pages: 821-852
ISSN: 0732-0582 (ISSN-L)
1545-3278
DOI: 10.1146/annurev.immunol.25.022106.141557
OpenAlex: W2156451877
Cited by: 1,842
References: 135
Citations by year: 2026: 18 · 2025: 16 · 2024: 35 · 2023: 33 · 2022: 35 · 2021: 60 · 2020: 47 · 2019: 54 · 2018: 60 · 2017: 79 · 2016: 71 · 2015: 99 · 2014: 124 · 2013: 137 · 2012: 120
FWCI: 18.11
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Keywords: IL-17 family cytokines, IL-12 family cytokines, Th17 cells, effector T cell differentiation, Th1/Th2 paradigm, naive T cell activation, innate-adaptive immune interaction, T cell lineage specification, immune regulation, immune pathogenesis, host defense
MeSH terms: Animals, Cell Differentiation, Humans, Immunity, Innate, Structure-Activity Relationship, Protein Structure, Tertiary, Th1 Cells, Th2 Cells, Interleukin-12, Interleukin-17

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IL-17 family cytokines and the expanding diversity of effector T cell lineages

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