Cited by 1,545Cytokine Signaling Pathways and InteractionsT-cell and B-cell ImmunologyReceptor Mechanisms and Signaling

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THE IL-4 RECEPTOR: Signaling Mechanisms and Biologic Functions

Nelms, Keats, Keegan, Achsah D., Zamorano, José, Ryan, John J., Paul, William E.·1999·Annual Review of Immunology

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Abstract

Interleukin-4 is a multifunctional cytokine that plays a critical role in the regulation of immune responses. Its effects depend upon binding to and signaling through a receptor complex consisting of the IL-4R alpha chain and the common gamma chain (gamma c), resulting in a series of phosphorylation events mediated by receptor-associated kinases. In turn, these cause the recruitment of mediators of cell growth, of resistance to apoptosis, and of gene activation and differentiation. Here we describe our current understanding of the organization of the IL-4 receptor, of the signaling pathways that are induced as a result of receptor occupancy, and of the various mechanisms through which receptor function is modulated. We particularly emphasize the modular nature of the receptor and the specialization of different receptor regions for distinct functions, most notably the independent regulation of cell growth and gene activation.

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Crossref · 10.1146/annurev.immunol.17.1.701

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Background
Retracted
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Background
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Background
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Background
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Background
Alternatively spliced variants of interleukin-4 promote inflammation differentially
Luzina, I. G., Lockatell, V., Todd, N. W., Highsmith, K., Keegan, A. D., Hasday, J. D., & Atamas, S. P. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0510271 · Cited by 28
“It shares sequence homology, receptor chains, and some functional effects with IL-13 [1].”
BackgroundInfluential
Trim32 Deficiency Enhances Th2 Immunity and Predisposes to Features of Atopic Dermatitis
Liu, Y., Wang, Z., Torre, R. D. L., Barling, A. N., Tsujikawa, T., Hornick, N. I., Hanifin, J. M., Simpson, E. L., Wang, Y., Swanzey, E., et al. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2016.09.020 · Cited by 29
“The expression of IL-17A and CCL20 is mediated through Stat3 (Hau et al., 2014; Li et al., 2015; Mack et al., 2012), whereas the expression of IL-4 and IL-5 is mediated through Stat6 (Chan et al., 2001; Nelms et al., 1999).”
Influential
Fungal immunomodulatory protein-fve could modulate airway remodel through by affect IL17 cytokine
Lee, Y.-T., Wu, C.-T., Sun, H., Ko, J., & Lue, K.-H. (2017) · Journal of Microbiology Immunology and Infection · doi:10.1016/j.jmii.2017.06.008 · Cited by 28
Interleukin-4 and Interleukin-10 Gene Polymorphisms in Patients with Inflammatory Bowel Disease
Daryani, N. E., Saghazadeh, A., Moossavi, S., Sadr, M., Shahkarami, S., Soltani, S., Farhadi, E., & Rezaei, N. (2017) · Immunological Investigations · doi:10.1080/08820139.2017.1360343 · Cited by 28
“Example range from cytokine production, immunoglobulin isotype switching, inflammation to tissue adhesion (Nelms et al., 1999).”
Background
Tribbles homolog 1 deficiency modulates function and polarization of murine bone marrow–derived macrophages
Arndt, L., Dokas, J., Gericke, M. T., Kutzner, C. E., Müller, S., Jeromin, F., Thiery, J., & Burkhardt, R. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000703 · Cited by 28
“Currently, it is not clear how Trib1 controls the abundance of JAK1 and JAK3 in macrophages.”
BackgroundInfluential
CCL2/MCP-1 signaling drives extracellular matrix turnover by diverse macrophage subsets
Jürgensen, H. J., Silva, L. M., Krigslund, O., van Putten, S., Madsen, D. H., Behrendt, N., Engelholm, L. H., & Bugge, T. H. (2019) · Matrix Biology Plus · doi:10.1016/j.mbplus.2019.03.002 · Cited by 28
“The latter observation is unexpected in light of the, at least partially shared, receptor subsets of IL-4 and IL-13 [57,58], and highlights the functional differences of the two wound healing-associated cytokines.”
Interleukins and STAT Signaling
Haque, S. J., & Sharma, P. (2006) · Vitamins and hormones · doi:10.1016/s0083-6729(06)74007-9 · Cited by 28
Expression and Targeting of Interleukin-4 Receptor for Primary and Advanced Ovarian Cancer Therapy
Kioi, M., Takahashi, S., Kawakami, M., Kawakami, K., Kreitman, R. J., & Puri, R. K. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1043 · Cited by 28
“Interleukin-4 (IL-4) is an important Th2-derived cytokine, which is involved in mediating numerous antitumor immune-modulating activities (5).”
Background
A single administration of interleukin-4 antagonistic mutant DNA inhibits allergic airway inflammation in a mouse model of asthma
Nishikubo, K., Murata, Y., Tamaki, S., Sugama, K., Imanaka‐Yoshida, K., Yuda, N., Kai, M., Takamura, S., Sebald, W., Adachi, Y., et al. (2003) · Gene Therapy · doi:10.1038/sj.gt.3302131 · Cited by 28
Donor IL-4-treatment induces alternatively activated liver macrophages and IDO-expressing NK cells and promotes rat liver allograft acceptance
Wang, C., Tay, S. S., Tran, G. T., Hodgkinson, S. J., Allen, R. D. M., Hall, B. M., McCaughan, G. W., Sharland, A. F., & Bishop, G. A. (2009) · Transplant Immunology · doi:10.1016/j.trim.2009.11.005 · Cited by 28
“IL-4 plays a central role in humoral and cell-mediated immunity where it promotes B cell activation and immunoglobulin classswitching, as well as T cell survival and differentiation (reviewed in [1]).”
Background
Polymorphisms in IL-4Rα Correlate with Airways Hyperreactivity, Eosinophilia, and Ym Protein Expression in Allergic IL-13−/− Mice
Webb, D. C., Matthaei, K. I., Cai, Y., McKenzie, A. N. J., & Foster, P. S. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.2.1092 · Cited by 28
“(11, 12) and in isotype switching of B cell Ab production to IgE”
Background
STAT6 Controls the Number of Regulatory T Cells In Vivo, Thereby Regulating Allergic Lung Inflammation
Dorsey, N., Chapoval, S. P., Smith, E., Skupsky, J., Scott, D. W., & Keegan, A. D. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300486 · Cited by 27
IL-4-dependent CD86 expression requires JAK/STAT6 activation and is negatively regulated by PKCδ
Deszo, E. L., Brake, D. K., Kelley, K. W., & Freund, G. G. (2003) · Cellular Signalling · doi:10.1016/s0898-6568(03)00137-2 · Cited by 27
Role of Chinese herbal medicinal ingredients in secretion of cytokines by PCV2-induced endothelial cells
Hu, Y., He, K., & Wang, X. (2015) · Journal of Immunotoxicology · doi:10.3109/1547691x.2015.1017624 · Cited by 27
“IL-4 aids in antigen-stimulated polarization of naive TH cells into TH2 effector cells and also helps to propagate TH2 responses by binding its receptor (IL-4R ) and activating signal transducer and activator of transcription (STAT)-6 signaling pathways (Nelms et al., 1999; Shimoda et al., 1996).”
Background
Relationship between the IL ‐4 gene promoter ‐590C/T (rs2243250) polymorphism and susceptibility to autoimmune diseases: a meta‐analysis
Qiu, L., Ni, J., Cen, H., Wen, P., Zhang, M., Liang, Y., Pan, H., Mao, C., & Ye, D. (2014) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/jdv.12435 · Cited by 36
On the Role IL-4/IL-13 Heteroreceptor Plays in Regulation of Type 1 Diabetes
Ukah, T., Cattin-Roy, A. N., Chen, W., Miller, M. M., Barik, S., & Zaghouani, H. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700410 · Cited by 27
“the HR on other cell types (10) to drive anti-inflammatory function against Th1 cells.”
Background
Dietary supplementation with blueberry partially restores T-cell-mediated function in high-fat-diet-induced obese mice
Lewis, E. D., Ren, Z., DeFuria, J., Obin, M. S., Meydani, S. N., & Wu, D. (2018) · British Journal Of Nutrition · doi:10.1017/s0007114518001034 · Cited by 28
Interleukin 4 induces the expression of inducible nitric oxide synthase in eosinophils
Paoliello-Paschoalato, A. B., Oliveira, S. H. P., & Cunha, F. Q. (2005) · Cytokine · doi:10.1016/j.cyto.2005.01.001 · Cited by 27
Interleukin-13 augments transforming growth factor-β1-induced tissue inhibitor of metalloproteinase-1 expression in primary human airway fibroblasts
Zhou, X., Trudeau, J. B., Schoonover, K. J., Lundin, J. I., Barnes, S. M., Cundall, M. J., & Wenzel, S. E. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00035.2004 · Cited by 27
“In addition to STAT-6, the IL-4R molecule has been reported to signal through an IRS-PI3K-Akt pathway (3, 24).”
HIV-1 induced AIDS is an Allergy and the Allergen is the Shed gp120 – a Review, Hypothesis, and Implications
Becker, Y. (2004) · Virus genes · doi:10.1023/b:viru.0000025778.56507.61 · Cited by 27
Distinct signal transduction processes by IL-4 and IL-13 and influences from the Q551R variant of the human IL-4 receptor alpha chain
Kruse, S., Braun, S. L., & Deichmann, K. A. (2002) · Respiratory Research · doi:10.1186/rr174 · Cited by 27
“A variety of inhibitors of the IL-4/IL-13 pathway have been reported, such as SOCS-1 (also known as SSI-1) [21]; however, this inhibitor was suggested to prevent activation of STAT and, for example, act on Jak proteins [37].”
Biological Functions of Interleukin-21 and Its Role in Inflammation
Pelletier, M., & Girard, D. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.275 · Cited by 28
“immune responses[15].”
Fes Mediates the IL-4 Activation of Insulin Receptor Substrate-2 and Cellular Proliferation
Jiang, H., Foltenyi, K., Kashiwada, M., Donahue, L., Vuong, B. Q., Hehn, B. T., & Rothman, P. B. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.4.2627 · Cited by 27
“PtdIns(3,4,5)P3, an enzymatic product of PI3-kinase, is thought to activate two different protein kinases, Akt/PKB and p70S6K (36, 37), lthough the mechanisms by which PtdIns(3,4,5)P3 regulates these two kinases appear to differ (38).”
Background
Janus kinase-3 dependent inflammatory responses in allergic asthma
Malaviya, R., Laskin, D. L., & Malaviya, R. (2010) · International Immunopharmacology · doi:10.1016/j.intimp.2010.04.014 · Cited by 27
“Binding of IL-4 to its cognate receptor on B cells triggers tyrosine phosphorylation of JAK-1 and JAK-3 [85, 86].”
Background
Biomarkers of disease can be detected in mice as early as 4 weeks after initiation of exposure to third-hand smoke levels equivalent to those found in homes of smokers
Adhami, N., Chen, Y., & Martins‐Green, M. M. (2017) · Clinical Science · doi:10.1042/cs20171053 · Cited by 26
Neuronal IL ‐4Rα modulates neuronal apoptosis and cell viability during the acute phases of cerebral ischemia
Lee, H. K., Koh, S., Lo, D. C., & Marchuk, D. A. (2018) · FEBS Journal · doi:10.1111/febs.14498 · Cited by 26
Cytokines and cytokine receptors
O’Shea, J. J., Gadina, M., & Siegel, R. M. (2013) · Elsevier eBooks · doi:10.1016/b978-0-7234-3691-1.00033-7 · Cited by 27
The association of the cytoplasmic domains of interleukin 4 receptor alpha and interleukin 13 receptor alpha 2 regulates interleukin 4 signaling
Andrews, A.-L., Nordgren, I. K., Campbell-Harding, G., Holloway, J. W., Holgate, S. T., Davies, D. E., & Tavassoli, A. (2013) · Molecular BioSystems · doi:10.1039/c3mb70298g · Cited by 26
Hepatitis C virus infection: A “liaison a trois” amongst the virus, the host, and chronic low-level inflammation for human survival
Barnaba, V. (2010) · Journal of Hepatology · doi:10.1016/j.jhep.2010.06.003 · Cited by 26
“) with protective responses against extracelllular pathogens or harmful responses in the case of allergic reactions [93].”
Background
IL-4 influences the differentiation and the susceptibility to activation-induced cell death of human naive CD8+ T cells
Riou, C., Dumont, A. R., Yassine‐Diab, B., Haddad, E. K., & Sékaly, R. (2006) · International Immunology · doi:10.1093/intimm/dxl019 · Cited by 22
“which IL-4 promotes the expression of Bcl-2 is unclear but most probably involves the activation, through the IL-4R signaling pathway, of Akt/PKB, which is known to regulate the expression of Bcl-2 family proteins including Bcl-2 ( 7 ).”
BackgroundInfluential
Spatial regulation of IL-4 signalling in vivo
Redpath, S. A., Heieis, G. A., & Perona‐Wright, G. (2015) · Cytokine · doi:10.1016/j.cyto.2015.02.026 · Cited by 26
IL-4R alpha deficiency influences hippocampal-BDNF signaling pathway to impair reference memory
Brombacher, T. M., Berkiks, I., Pillay, S., Scibiorek, M., Moses, B., & Brombacher, F. (2020) · Scientific Reports · doi:10.1038/s41598-020-73574-3 · Cited by 26
ORIGINAL ARTICLE: Interleukin 6 –174 G/C Promoter Polymorphism and Pregnancy Complications: Results of a Prospective Cohort Study in 1626 Pregnant Women
Stonek, F., Metzenbauer, M., Hafner, E., Philipp, K., & Tempfer, C. M. (2008) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2007.00577.x · Cited by 26
IL-4 Down-Regulates Lipopolysaccharide-Induced Formyl Peptide Receptor 2 in Murine Microglial Cells by Inhibiting the Activation of Mitogen-Activated Protein Kinases
Iribarren, P., Cui, Y.-H., Le, Y., Ying, G., Zhang, X., Gong, W., & Wang, J. M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.10.5482 · Cited by 26
“Stimulation of the IL-4R complex by IL-4 results in activation of multiple signaling pathways, one of which involves Stat6.”
BackgroundMethodInfluential
A targeted mutation in the IL-4Rα gene protects mice against autoimmune diabetes
Radu, D. L., Noben-Trauth, N., Hu‐Li, J., Paul, W. E., & Bona, C. A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.230431397 · Cited by 25
Serine Phosphorylation of Stat6 Negatively Controls Its DNA-Binding Function
Maiti, N. R., Sharma, P., Harbor, P. C., & Haque, S. J. (2005) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2005.25.553 · Cited by 27
“(3,21) However, the molecular and cellular events that negatively govern the Stat6-mediated signal transduction and consequent gene activation remain poorly defined.”
Polymorphisms in the interleukin-4 receptor α chain gene influence susceptibility to HIV-1 infection and its progression to AIDS
Soriano, À., Lozano, F., Oliva, H., García, F., Nomdedéu, M., de Lazzari, E., Rodríguez, C., Barrasa, A., Lorenzo, J. I. L., del Romero, J., et al. (2005) · Immunogenetics · doi:10.1007/s00251-005-0041-x · Cited by 26
“Type II IL-4R is also the receptor of IL-13, another key Th2 cytokine that shares most of the IL-4 functions (Hershey 2003; Nelms et al. 1999 ).”
The immunogenic peptide for Th1 development
Takatsu, K., & Kariyone, A. (2002) · International Immunopharmacology · doi:10.1016/s1567-5769(02)00209-6 · Cited by 26
Microenvironments‐Modulated Biomaterials Enhance Spinal Cord Injury Therapy
Li, Y., Zhang, Q., Liu, Z., Fu, C., & Ding, J. (2024) · Advanced Functional Materials · doi:10.1002/adfm.202403900 · Cited by 26
Host-Directed Targeting of LincRNA-MIR99AHG Suppresses Intracellular Growth of Mycobacterium tuberculosis
Gcanga, L., Tamgue, O., Ozturk, M., Pillay, S., Jacobs, R., Chia, J. E., Mbandi, S. K., Davids, M., Dheda, K. U. J., Schmeier, S., et al. (2022) · Nucleic Acid Therapeutics · doi:10.1089/nat.2022.0009 · Cited by 25
“IL-4 signals through two different receptor complexes, type I receptor (IL-4R a /c g chain) and type II receptor (IL-13R a 1) [52,53].”
IL1α and IL4 signalling in human ovarian surface epithelial cells
Papacleovoulou, G., Critchley, H., Hillier, S. G., & Mason, J. I. (2011) · Journal of Endocrinology · doi:10.1530/joe-11-0081 · Cited by 25
Polymorphisms in the IL-13 and IL-4R genes are associated with the development of renal cell carcinoma
Chu, H., Wang, M., Fu, Y., Zhong, D., Shi, D., Ma, L., Pan, X., Qin, C., Yin, C., & Zhang, Z. (2012) · Annals of Oncology · doi:10.1093/annonc/mdr607 · Cited by 25
IL-4 and IL-13 upregulate ornithine decarboxylase expression by PI3K and MAP kinase pathways in vascular smooth muscle cells
Liu, W., Yang, Y., Wu, G., & Ignarro, L. J. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00325.2007 · Cited by 25
“The IL-4R- chain cytoplasmic region appears to have three functionally distinct domains, one that acts as an interaction site for the Janus kinase (Jak), one required for activation of proliferation pathways, and a third involved in the activation of pathways leading to induction of gene expression (30).”
Background
Interleukin 4 –590C/T (rs2243250) Polymorphism Is Associated With Increased Risk of Atopic Dermatitis: Meta-Analysis of Case-Control Studies
Liang, J., Liu, Y., Xue, R., Chen, L., Chen, H., Shao, L., Wang, J., & Zhang, X. (2017) · Dermatitis · doi:10.1097/der.0000000000000265 · Cited by 25
CD4+ T Cell-Specific Deletion of IL-4 Receptor α Prevents Ovalbumin-Induced Anaphylaxis by an IFN-γ-Dependent Mechanism
Nieuwenhuizen, N. E., Herbert, D. R., Lopata, A. L., & Brombacher, F. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.5.2758 · Cited by 25
“subunit is expressed on a wide range of cells (17).”
Background

Authors: Nelms, K., Keegan, A. D., Zamorano, J., Ryan, J. J., & Paul, W. E.
Affiliations: National Institutes of Health (US)
Corresponding author: Nelms, Keats
Paul, William E.
ORCID: Keegan, Achsah D.
Ryan, John J.
Venue: Annual Review of Immunology
Publisher: Annual Reviews
Published: 1999-04
Volume: 17
Issue: 1
Pages: 701-738
ISSN: 0732-0582 (ISSN-L)
1545-3278
DOI: 10.1146/annurev.immunol.17.1.701
OpenAlex: W2144120552
Cited by: 1,545
References: 190
Citations by year: 2026: 17 · 2025: 27 · 2024: 52 · 2023: 36 · 2022: 54 · 2021: 43 · 2020: 50 · 2019: 44 · 2018: 54 · 2017: 49 · 2016: 52 · 2015: 56 · 2014: 72 · 2013: 52 · 2012: 55
FWCI: 6.85
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords: IL-4, IL-4 receptor, common gamma chain, receptor signaling, receptor phosphorylation, cell growth regulation, apoptosis resistance, gene activation, T cell differentiation, cytokine signaling
MeSH terms: Amino Acid Sequence, Animals, Humans, Molecular Sequence Data, Phosphoproteins, Signal Transduction, Trans-Activators, Interleukin-4, Protein Tyrosine Phosphatases, Calcium-Calmodulin-Dependent Protein Kinases, Mice, Knockout, Receptors, Interleukin-4, Mitogen-Activated Protein Kinases, Intracellular Signaling Peptides and Proteins, JNK Mitogen-Activated Protein Kinases, STAT6 Transcription Factor, Mice, Insulin Receptor Substrate Proteins

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THE IL-4 RECEPTOR: Signaling Mechanisms and Biologic Functions

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