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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BackgroundInfluential
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Background
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“In particular, Th2 lymphocytes produce IL-4, a key player in driving Th2 differentiation of naive T cells and in B cell activation (14).”
Background
Association between genes encoding components of the IL-4/IL-4 receptor pathway and dermatitis in children
Hussein, Y. M., Shalaby, S. M., Nassar, A., Alzahrani, S. S., Alharbi, A. S., & Nouh, M. (2014) · Gene · doi:10.1016/j.gene.2014.04.024 · Cited by 43
“024 Interleukin 4 (IL-4) is central to the development of the T helper 2 (Th2) phenotypes that induce immunoglobulin ε isotype switching and secretion of IgE and promote transmigration of effector cells (Nelms et al., 1999).”
BackgroundInfluential
Targeted Toxins in Brain Tumor Therapy
Li, Y. M., & Hall, W. A. (2010) · Toxins · doi:10.3390/toxins2112645 · Cited by 44
“Interleukin-4 (IL-4) is a pleiotropic cytokine which is primarily produced by Th2-type T lymphocytes, mast cells, and basophils [41].”
Background
Recombinant IL-4/13A and IL-4/13B induce arginase activity and down-regulate nitric oxide response of primary goldfish (Carassius auratus L.) macrophages
Hodgkinson, J. W., Fibke, C. D., & Belosevic, M. (2016) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2016.08.014 · Cited by 44
“Functionally, IL-4 is well defined as a central cytokine in mediating the Th2 phenotype in lymphocytes, promoting a differentiation into cells capable of producing other type 2 cytokines (Nelms et al., 1999), in addition to suppression of IFNg-producing CD4þ (Th1) cells (Ouyang et al.”
Background
Interleukin-4 Receptor Alpha: From Innate to Adaptive Immunity in Murine Models of Cutaneous Leishmaniasis
Hurdayal, R., & Brombacher, F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01354 · Cited by 44
STAT6-Dependent Differentiation and Production of IL-5 and IL-13 in Murine NK2 Cells
Katsumoto, T., Kimura, M. Y., Yamashita, M., Hosokawa, H., Hashimoto, K., Hasegawa, A., Omori, M., Miyamoto, T. K., Taniguchi, M., & Nakayama, T. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.8.4967 · Cited by 45
Factors Regulating the Effect of IL-4 on Intestinal Epithelial Barrier Function
Leo, V. D., Yang, P., Berin, M. C., & Perdue, M. H. (2002) · International Archives of Allergy and Immunology · doi:10.1159/000066778 · Cited by 46
Interleukin 4 and STAT6 gene polymorphisms are associated with systemic lupus erythematosus in Chinese patients
Yu, H., Liu, P., Lin, Y., Chen, W. J., Lee, J., Wang, L., Yang, Y., & Chiang, B. (2010) · Lupus · doi:10.1177/0961203310371152 · Cited by 44
Interleukin‐4 increases murine airway response to kinins, via up‐regulation of bradykinin B1‐receptors and altered signalling along mitogen‐activated protein kinase pathways
Bryborn, M., Mikael Adner, A., & Cardell, L. (2004) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2004.02031.x · Cited by 44
Insulin Receptor Substrate-2-dependent Interleukin-4 Signaling in Macrophages Is Impaired in Two Models of Type 2 Diabetes Mellitus
Hartman, M. E., O’Connor, J. C., Godbout, J. P., Minor, K. D., Mazzocco, V. R., & Freund, G. G. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404368200 · Cited by 45
STAT4 and STAT6, their role in cellular and humoral immunity and in diverse human diseases
Tolomeo, M., & Cascio, A. (2024) · International Reviews of Immunology · doi:10.1080/08830185.2024.2395274 · Cited by 45
“IL-2Rγc is prevalently expressed in lymphocytes whereas IL-13Rα1 in non-hematopoietic cells [18].”
The involvement of interleukin-1 and interleukin-4 in the response of human annulus fibrosus cells to cyclic tensile strain: an altered mechanotransduction pathway with degeneration
Gilbert, H. T. J., Hoyland, J. A., Freemont, A. J., & Millward-Sadler, S. J. (2011) · Arthritis Research & Therapy · doi:10.1186/ar3229 · Cited by 43
“During IL-4R activation, IL-4 first binds IL-4Ra, leading to the recruitment of a second receptor subunit, predominantly IL-2Rg in cells of haematopoietic origin [61] (termed ‘type I IL-4R’) and IL-13Ra1 in cells of nonhaematopoietic origin [62-64] (termed ‘type II IL-4R’).”
Background
IL-4 and IL-13 Receptor Signaling From 4PS to Insulin Receptor Substrate 2: There and Back Again, a Historical View
Keegan, A. D., Zamorano, J., Keselman, A. M., & Heller, N. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01037 · Cited by 44
SCID/NOD mice model for 5-FU induced intestinal mucositis: Safety and effects of probiotics as therapy
Huang, L., Chiau, J. C., Cheng, M.-L., Chan, W., Jiang, C., Chang, S., Yeung, C., & Lee, H. (2018) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2018.07.007 · Cited by 43
Genome-wide transcriptome analysis of the STAT6-regulated genes in advanced-stage cutaneous T-cell lymphoma
Gaydosik, A. M., Queen, D., Trager, M. H., Akilov, O. E., Geskin, L. J., & Fuschiotti, P. (2020) · Blood · doi:10.1182/blood.2019004725 · Cited by 43
Biologic Functions and Signaling of the Interleukin-4 Receptor Complexes
Gessner, A., & Röllinghoff, M. (2000) · Immunobiology · doi:10.1016/s0171-2985(00)80084-4 · Cited by 44
Cytokine Receptors—Regulators of Antimycobacterial Immune Response
Druszczyńska, M., Godkowicz, M., Kulesza, J., Wawrocki, S., & Fol, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031112 · Cited by 43
“The cytokine exerts its biological activities through interaction with two surface receptor complexes, the type I IL-4R and the type II IL-4R (Figure 4) [54].”
Background
Berberine promotes M2 macrophage polarisation through the IL-4-STAT6 signalling pathway in ulcerative colitis treatment
Xiong, K., Deng, J., Yue, T., Hu, W., Zeng, X., Yang, T., & Xiao, T. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e14176 · Cited by 42
“In addition, IL-4 induces downstream signalling via IL-4Rα, with the Y residue in the intracellular IL-4Rα domain acting as a docking site for the SH domain of the intracellular signalling molecule to activate STAT6 [43].”
Background
Losartan inhibits conventional dendritic cell maturation and Th1 and Th17 polarization responses: Νovel mechanisms of preventive effects on lipopolysaccharide-induced acute lung injury
Qiu, H.-B. (2011) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2011.818 · Cited by 41
“Although the exact reason remains unclear, one possibility is that there are several other cellular sources of IL-4, including NK T cells, γδ T cells, basophils, mast cells, eosinophils and stromal cells (35).”
Influence of a cocoa‐enriched diet on specific immune response in ovalbumin‐sensitized rats
Pérez, T., Ramiro‐Puig, E., Pérez-Cano, F. J., Castellote, C., Permanyer, J., Franch, À., & Castell, M. (2008) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200700396 · Cited by 42
“This reaction ultimately produces plasma cells that secrete copious amounts of Ab. Cytokines, such as IL- 4, IL-10 and IL-6, influence the development of Ab SCs [41]; specifically, IL-4 controls the specificity of immunoglobulin class switching [ 42 ].”
Background
MEK1/2 Inhibition Promotes Macrophage Reparative Properties
Long, M. E., Eddy, W. E., Gong, K.-Q., Lovelace-Macon, L., McMahan, R. S., Charron, J., Liles, W. C., & Manicone, A. M. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1601059 · Cited by 42
“Macrophages require the transcription factor STAT6 for increased expression of many IL-4/IL-13–regulated genes (24).”
Background
IL-4 controls activated neutrophil FcγR2b expression and migration into inflamed joints
Panda, S. K., Wigerblad, G., Jiang, L., Jiménez-Andrade, Y., Iyer, V. S., Shen, Y., Boddul, S. V., Guerreiro‐Cacais, A. O., Raposo, B., Kasza, Z., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1914186117 · Cited by 42
Mast cells regulate procollagen I (α1) production by bronchial fibroblasts derived from subjects with asthma through IL-4/IL-4δ2 ratio
Plante, S., Semlali, A., Joubert, P., Bissonnette, É. Y., Laviolette, M., Hamid, Q. A., & Chakir, J. (2006) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2005.12.1349 · Cited by 43
Dual Effect of Central Injection of Recombinant Rat Interleukin-4 on Lipopolysaccharide-Induced Sickness Behavior in Rats
Bluthé, R.-M. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00305-0 · Cited by 42
“IL-4 is a pleiotropic cytokine produced by activated helper T cells which exerts multiple biological effects through binding to specific receptors on the cell surface (Mire-Sluis 1998; Nelms et al. 1999).”
IL-4 enhances IFN-λ1 (IL-29) production by plasmacytoid DCs via monocyte secretion of IL-1Ra
Megjugorac, N. J., Gallagher, G. E., & Gallagher, G. E. (2010) · Blood · doi:10.1182/blood-2009-09-246157 · Cited by 43
IL-4 mediates dicloxacillin-induced liver injury in mice
Higuchi, S., Kobayashi, M., Yoshikawa, Y., Tsuneyama, K., Fukami, T., Nakajima, M., & Yokoi, T. (2010) · Toxicology Letters · doi:10.1016/j.toxlet.2010.11.006 · Cited by 41
Interleukin-4 Promoter Polymorphisms: A Genetic Prognostic Factor for Survival in Metastatic Renal Cell Carcinoma
Kleinrath, T., Gassner, C., Lackner, P., Thurnher, M., & Ramoner, R. E. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.07.8154 · Cited by 40
Effect of interleukin-4 on orthodontic tooth movement and associated root resorption
Hakami, Z. W., Kitaura, H., Kimura, K., Ishida, M., Sugisawa, H., Ida, H., Saeed, J., & Takano‐Yamamoto, T. (2014) · European Journal of Orthodontics · doi:10.1093/ejo/cju016 · Cited by 41
“It is a key regulator in humoural and adaptive immunity that regulates the function of lymphocytes and macrophages (17).”
Background
Interleukin 4 Deficiency Reverses Development of Secondary Pseudomonas aeruginosa Pneumonia During Sepsis-Associated Immunosuppression
Song, Z., Zhang, J., Zhang, X., Li, D., Wang, H., Xu, X., Xu, W., Yin, Y. B., & Cao, J. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu668 · Cited by 43
“Thus, macrophage dysfunction [7], neutrophil paralysis [8], dendritic cell deficiency [9], lymphopenia [10], decreased levels of proinflammatory cytokines (tumor necrosis factor α [TNF-α] and interleukin 6 {IL-6}) or monocyte HLA-DR expression, and increased levels of antiinflammatory cytokines (interleukin 10 [IL-10]…”
BackgroundInfluential
Interleukin‐4 can induce interleukin‐4 production in dendritic cells
Maroof, A., Penny, M. A., Kingston, R., Murray, C. M., Islam, S., Bedford, P. A., & Knight, S. C. (2005) · Immunology · doi:10.1111/j.1365-2567.2005.02305.x · Cited by 41
Effect of the fungal immunomodulatory protein FIP-fve on airway inflammation and cytokine production in mouse asthma model
Lee, Y.-T., Lee, S., Sun, H., Lu, K., Ku, M., Sheu, J., Ko, J., & Lue, K.-H. (2012) · Cytokine · doi:10.1016/j.cyto.2012.09.024 · Cited by 41
Leflunomide Induces Apoptosis in Fludarabine-Resistant and Clinically Refractory CLL Cells
Dietrich, S., Krämer, O. H., Hahn, E., Schäfer, C., Giese, T., Hess, M., Tretter, T., Rieger, M. A., Hüllein, J., Zenz, T., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-1049 · Cited by 41
“Accordingly, STAT3 and STAT6 phosphorylation was already inhibited by 10 mg/mL A771726, and higher concentrations of this agent (80mg/mL) completely blocked phosphorylation of these transcription factors (Fig.”
BackgroundInfluential
Interleukin-4 Cytotoxin Therapy Synergizes with Gemcitabine in a Mouse Model of Pancreatic Ductal Adenocarcinoma
Shimamura, T., Royal, R. E., Kioi, M., Nakajima, A., Husain, S. R., & Puri, R. K. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4558 · Cited by 41
“Interleukin-4 (IL-4) is an important Th2-derived cytokine, which is involved in mediating antitumor immune-modulating activities ( 14 ).”
Background
Aggressive non-Hodgkin's lymphoma: Concomitant evaluation of interleukin-2, soluble interleukin-2 receptor, interleukin-4, interleukin-6, interleukin-10 and correlation with outcome
Fabre, E., Tabrizi, R., Coulon, V., Monnereau, A., Eghbali, H., Soubeyran, I., & Soubeyran, P. (2005) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190500361029 · Cited by 41
“Moreover, IL-4 plays an important role in tissue adhesion [16] and stimulates B-cell growth.”
Background
Lymphocytes in allergic bronchopulmonary aspergillosis
Knutsen, A. P. (2003) · Frontiers in bioscience · doi:10.2741/994 · Cited by 41
IN VIVO EXPRESSION OF THE INTERLEUKIN 4 RECEPTOR ALPHA BY ASTROCYTES IN EPILEPSY CEREBRAL CORTEX
Liu, H., Prayson, R. A., Estes, M. L., Drazba, J. A., Barnett, G. H., Bingaman, W. E., Liu, J., Jacobs, B., & Barna, B. P. (2000) · Cytokine · doi:10.1006/cyto.2000.0773 · Cited by 41
Identification of Estrogen-Regulated Genes of Potential Importance for the Regulation of Trabecular Bone Mineral Density
Lindberg, M. K., Movérare, S., Eriksson, A.-L., Skrtic, S., Gao, H., Dahlman‐Wright, K., Gustafsson, J.-Α., & Ohlsson, C. (2002) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2002.17.12.2183 · Cited by 41
“IL-4 is a pleiotropic immunomodulatory cytokine produced by Th2 lymphocytes, mast cells, and eosinophils.((57,58)) Some studies indicate that IL-4 might also be involved in the regulation of bone metabolism.”
Background
Dock10, a novel CZH protein selectively induced by interleukin-4 in human B lymphocytes
Yelo, E., Bernardo, M. V., Gimeno, L., Alcaraz-García, M. J., Majado, M. J., & Parrado, A. (2008) · Molecular Immunology · doi:10.1016/j.molimm.2008.04.003 · Cited by 46
“Interleukin-4 (IL4), upon binding to receptors (IL4R) expressed by a wide range of hematopoietic and non-hematopoietic cells, activates signalling cascades, including the IRS2, PI3K, and STAT6 pathways, which induce or modulate cell growth and differentiation processes (Nelms et al., 1999).”
Background
The immunology and genetics of resistance of sheep to Teladorsagia circumcincta
Venturina, V., Gossner, A. G., & Hopkins, J. (2013) · Veterinary Research Communications · doi:10.1007/s11259-013-9559-9 · Cited by 37
“1) as well as stimulating mast cell maturation and proliferation (Finkelman et al., 1990; Nelms et al., 1999; Ansel et al., 2006).”
Albizia lebbeck suppresses histamine signaling by the inhibition of histamine H1 receptor and histidine decarboxylase gene transcriptions
Nurul, I. M., Mizuguchi, H., Shahriar, M., Venkatesh, P., Maeyama, K., Mukherjee, P. K., Hattori, M., Choudhuri, M. S. K., Takeda, N., & Fukui, H. (2011) · International Immunopharmacology · doi:10.1016/j.intimp.2011.07.003 · Cited by 40
“Th1/Th2 imbalance in the immune system towards the Th2 responses results in the clinical expression of nasal allergy and asthma [20].”
Background
Macrophages as Effectors of Acute and Chronic Allograft Injury
Liu, Y., Kloc, M., & Li, X. C. (2016) · Current Transplantation Reports · doi:10.1007/s40472-016-0130-9 · Cited by 40
Virtual memory CD8 T cells expanded by helminth infection confer broad protection against bacterial infection
Lin, J., Mohrs, K., Szaba, F. M., Kummer, L. W., Leadbetter, E. A., & Mohrs, M. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0100-x · Cited by 40
Expression of IL‐10‐triggered STAT3‐dependent IL‐4Rα is required for induction of arginase 1 in visceral leishmaniasis
Biswas, A., Bhattacharya, A., Kar, S., & Das, P. K. (2011) · European Journal of Immunology · doi:10.1002/eji.201040940 · Cited by 44
STAT6−/− mice exhibit decreased cells with alternatively activated macrophage phenotypes and enhanced disease severity in murine neurocysticercosis
Mishra, B. B., Gundra, U. M., & Teale, J. M. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.09.029 · Cited by 40

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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