Entry - *147740 - INTERLEUKIN 3; IL3 - OMIM
 
* 147740

INTERLEUKIN 3; IL3


Alternative titles; symbols

MULTI-CSF


HGNC Approved Gene Symbol: IL3

Cytogenetic location: 5q31.1   Genomic coordinates (GRCh38) : 5:132,060,655-132,063,204 (from NCBI)


TEXT

Description

Interleukin-3 is a hematopoietic colony-stimulating factor that is capable of supporting the proliferation of a broad range of hematopoietic cell types. Interleukin-3 also has neurotrophic activity (Chavany et al., 1998).


Cloning and Expression

Clark-Lewis et al. (1986) chemically synthesized interleukin-3, a protein of 140 amino acids. Interleukin-3 is one of the group of lymphokines produced by T cells after activation with mitogens or antigens. The protein has been purified to homogeneity and has been shown to be a glycoprotein with an apparent molecular mass of 28,000. The structure of the protein has been deduced from sequencing of cDNA clones encoding IL3, and biologically active IL3 has been chemically synthesized based on the predicted amino acid sequence. A broad spectrum of biologic activities of IL3 suggests that this lymphokine regulates the proliferation and differentiation of early hematopoietic/lymphoid stem cells, as well as cells committed to many hematopoietic lineages. Because of its potent growth-promoting activity for multiple hematopoietic cell lineages, it has acquired a variety of designations such as mast-cell growth factor, burst-stimulating activity, multi-colony-stimulating factor, among others. There appears to be a single IL3 gene. The cDNA clones (Fung et al., 1984; Yokota et al., 1984) indicate that the precursor has 166 amino acids.

Yang et al. (1986) identified the human IL3 gene and found that it has a high degree of homology with those of gibbon and mouse.


Mapping

By using a cDNA clone, Ihle et al. (1987) mapped the IL3 gene to mouse chromosome 11 in a series of hamster x mouse somatic cell hybrids. To confirm the chromosomal assignment, they sought evidence for linkage between IL3 and other genes on chromosome 11. They found that indeed there was linkage with an oncogene known to map to mouse chromosome 11; linkage was studied in genetic crosses between 2 strains of mice. Webb et al. (1989) confirmed the assignment of both Il-3 and Il-5 to mouse chromosome 11. In man, the IL3 locus maps to the long arm of chromosome 5 in the area that is deleted in the 5q-minus syndrome, namely, 5q23-q31, by study of somatic cell hybrids and by in situ hybridization (Le Beau et al., 1987). Grimaldi and Meeker (1989) concluded that the IL3 gene is situated centromeric to the CSF2 gene.

Using chromosome-5-linked DNA probes to study somatic cell hybrids retaining partial chromosome 5 and cells from patients with acquired deletions of 5q, Huebner et al. (1990) concluded that the order of genes on 5q is as follows: cen--HEXB--DHFR--(IL5, IL4)--IL3--CSF2--FGFA--(CSF1R, PDGFRB)--ADRB2R--CSF1--qter. Furthermore, they concluded that the order and orientation of the closely linked IL3/CSF2 gene pair is cen--5-prime IL3 3-prime,5-prime CSF2 3-prime--qter.

By fluorescence in situ hybridization, Le Beau et al. (1993) mapped the IL3 gene to 5q31.1.


Gene Function

Yang et al. (1986) showed that primate IL3 is functionally related to murine Il3 in terms of multipotent colony-stimulating activity.

From in vivo studies in the cynomolgus macaque, Donahue et al. (1988) concluded that IL3 infusion expands an early cell population that subsequently requires the action of a later-acting factor such as GMCSF (CSF2; 138960) to complete its development. Thus, linkage of the genes coding these 2 hematopoietic factors, which are within 9 kb of each other on chromosome 5 (Yang et al., 1988), may have a functional significance.

Chavany et al. (1998) examined the effect of IL3 on embryonic motor neuron survival in mixed spinal cord cultures. The results suggested the motor neuron degeneration is not directly triggered by the high level of expression of IL3.

Using DNA microarrays to analyze IL3-dependent murine FL5.12 pro-B cells, Devireddy et al. (2001) found that the gene undergoing maximal transcriptional induction after cytokine withdrawal is 24p3, which encodes a secreted lipocalin (LCN2; 600181). Conditioned medium from IL3-deprived cells contained 24p3 and induced apoptosis in naive cells, even when IL3 was present. 24p3 also induced apoptosis in a wide variety of leukocytes but not other cell types. Apoptotic sensitivity correlated with the presence of a putative 24p3 cell surface receptor. Devireddy et al. (2001) concluded that IL3 deprivation activates 24p3 transcription, leading to synthesis and secretion of 24p3, which induces apoptosis through an autocrine pathway. In addition to murine FL5.12 pro-B cells many other cell types were sensitive to 24p3-mediated apoptosis: murine primary thymocytes, murine primary splenocytes, murine primary bone marrow cells, human primary neutrophils, and human peripheral blood lymphocytes. In contrast, human primary macrophages, HeLa cells, and Jurkat cells were not susceptible to 24p3-mediated apoptosis.

Resting eosinophils express neither MHC class II proteins or costimulatory B7 molecules and fail to induce proliferation of T cells to antigens. Celestin et al. (2001) reported that IL3 induces expression of HLA-DR and B7.2 (601020) on eosinophils, but, unlike IL5 (147580) and GMCSF, it does not induce expression of B7.1 (112203). IL3-treated eosinophils supported modest T-cell proliferation in response to superantigen toxic shock syndrome-1 antigen, as well as proliferation of HLA-DR-restricted T-cell clones to tetanus toxoid (TT) and influenza virus antigenic peptides. The response was blocked by anti-B7.2 monoclonal antibody. IL3-treated eosinophils were unable to present native TT antigen to either resting or TT-specific cloned T cells. Parallel experiments established that IL5 and GMCSF induce T-cell proliferation to peptides but not to native TT antigen. Celestin et al. (2001) suggested that eosinophils activated by IL3 may contribute to T-cell activation in allergic and parasitic diseases by presenting superantigens and peptides to T cells.

Kiser et al. (2006) used retroviral integration mutagenesis and a chemical frameshift mutagen to transform Il3-dependent mouse bone marrow-derived PB-3c mast cells to Il3 independence. With 21 of 22 clones, Il3 independence resulted from a recessive mechanism, and reversion to Il3 dependence was observed in hybrids with the parental cell line. Recessive clones displayed increased phosphorylated Erk1 (MAPK3; 601795)/Erk2 (MAPK1; 176948) expression and were sensitive to inhibition of Mek (see MAP2K1; 176872), but not Raf1 (164760). The dominant Il3-independent clone showed no signs of MAP kinase pathway activation, but it had constitutive phosphorylation of Stat5 (601511). Kiser et al. (2006) concluded that Il3-dependent PB-3c mast cells have multiple options to acquire Il3 growth autonomy, including transcriptional and posttranscriptional mechanisms affecting the distal regulators Erk or Stat5.

Siracusa et al. (2011) demonstrated that TSLP (607003) promotes systemic basophilia, that disruption of TSLP-TSLPR (300357) interactions results in defective basophil responses, and that TSLPR-sufficient basophils can restore TH2-cell-dependent immunity in vivo. TSLP acted directly on bone marrow-resident progenitors to promote basophil responses selectively. Critically, TSLP could elicit basophil responses in both IL3-IL3R-sufficient and -deficient environments, and genomewide transcriptional profiling and functional analyses identified heterogeneity between TSLP-elicited versus IL3-elicited basophils. Furthermore, activated human basophils expressed TSLPR, and basophils isolated from eosinophilic esophagitis (see 610247) patients were distinct from classical basophils. Siracusa et al. (2011) concluded that collectively, their studies identified previously unrecognized heterogeneity within the basophil cell lineage and indicated that expression of TSLP may influence susceptibility to multiple allergic diseases by regulating basophil hematopoiesis and eliciting a population of functionally distinct basophils that promote TH2 cytokine-mediated inflammation.

By retrospectively analyzing the plasma of septic patients, Weber et al. (2015) found that increased IL3 levels within the first 24 hours after sepsis onset predicted death. Flow cytometric and immunohistochemical analyses of splenectomy patients showed that IL3-producing, CD19 (107265)-positive B cells carrying markers for innate response activator (IRA) B cells amplified inflammation. Weber et al. (2015) proposed that IL3 is a major upstream orchestrator of the septic inflammatory phase.

By overexpression analysis in mouse lung epithelial (MLE) cells, Tong et al. (2020) showed that Rnft2 (620254) negatively regulated Il3ra (308385) stability through ubiquitination and proteasomal degradation in response to Il3 signaling. Rnft2 affected Il3ra abundance and signaling in response to Il3 by associating with Il3ra and targeting it as a substrate. In vitro analysis in MLE cells revealed that Il3 augmented proinflammatory cellular responses to lipopolysaccharide (LPS) through Rnft2 and Il3ra, as LPS sensitized cells to Il3 through stabilization of Il3ra. Mutation analysis identified lys357 of Il3ra as a critical residue for regulation of its stability, as lys357 mutants were resistant to Rnft2-directed degradation. Analysis with a mouse model for pneumonia and severe lung injury found that Il3 drove inflammation in LPS-induced lung injury in vivo, and further analysis revealed that lung inflammation was regulated through the Rnft2/Il3ra/Il3 axis. Moreover, analysis with parenchymal explant lung samples from human cystic fibrosis (CF; 219700) patients showed that the RNFT2/IL3RA/IL3 axis was also involved in human inflammatory lung disease.


Molecular Genetics

Yamada et al. (2001) designed a case-control study to investigate association between rheumatoid arthritis and a single-nucleotide polymorphism (SNP) in the IL3 promoter region. A particularly strong association was observed in females with early onset.


Cytogenetics

In a case of B-lineage acute lymphocytic leukemia associated with peripheral blood eosinophilia, Grimaldi and Meeker (1989) found that a chromosomal translocation t(5;14)(q31;q32) joined the immunoglobulin heavy chain joining region (IGHJ; 147010) to the promoter region of the IL3 gene in opposite transcriptional orientations. They suggested that activation of the IL3 gene by the enhancer of the immunoglobulin heavy chain gene played a central role in the pathogenesis of the leukemia and the associated eosinophilia. Meeker et al. (1990) found excess IL3 mRNA produced by leukemic cells in one patient; in a second patient, serum IL3 levels correlated with disease activity.


Animal Model

In addition to their role in stimulating the proliferation and differentiation of various hematopoietic progenitor cells, IL3 and other cytokines have been found to have neurotrophic activity and to be associated with neurologic disorders, suggesting their complex role in the central nervous system (CNS). IL3 is expressed by neurons and astrocytes in mouse brain. Some interleukins, including IL3, are associated with both neurodegeneration and repair in the CNS. IL1-beta (IL1B; 147720) and other cytokines, including IL3, are neurotrophic at low concentration, or neurotoxic at high concentration. To understand the pleiotropic role of IL3 and how it exerts its role in the pathogenesis of CNS injury, several groups generated transgenic mice and analyzed their phenotype. Cockayne et al. (1994) found that transgenic mice expressing an antisense RNA for IL3 exhibited either a lymphoproliferative syndrome or a progressive neurologic dysfunction characterized by abnormal rotatory movement and ataxia. Chiang et al. (1996) generated transgenic mice for IL3 under the control of the glial fibrillary acidic protein gene (GFAP; 137780) promoter to target expression of Il3 to astrocytes. These mice developed a progressive motor dysfunction characterized, at onset, by impaired rotarod performance. They attributed the dysfunction to demyelination induced by activation and recruitment of microglial cells in the brain. Chavany et al. (1998) developed a transgenic IL3 mouse that overexpressed mouse IL3 under the control of a cytomegalovirus (CMV) promoter to achieve widespread expression of the transgene in various organs. They showed that general overexpression of IL3 in mice leads to a motor neuron disease with several features of human amyotrophic lateral sclerosis and progressive muscular atrophy. Furthermore, these symptoms were associated with a severe autoimmune reaction against spinal cord motor neurons. The animals exhibited hind limb paralysis at 7 months of age, associated with dendritic and axonal degeneration, loss of motor neurons in the spinal cord, and autoimmune reaction against these cells.

Robin et al. (2006) noted that Runx1 (151385) -/- mice die at embryonic day 12 to 13 with no aorta-gonad-mesonephros (AGM) region and fetal liver hematopoiesis, and that Runx1 +/- mice have reduced adult-repopulating ability of hematopoietic stem cells (HSCs). Since IL3 is a RUNX1 target, they examined whether Il3 affects HSCs in the mouse embryo. Using limiting dilution and Poisson statistical analysis, Robin et al. (2006) found that Runx1 +/- mice had fewer HSCs in AGM, but not in yolk sac or placenta, than wildtype mice. AGM-derived HSCs cultured from Runx1 +/- mice in the presence of Il3, but not other cytokines, followed by transplantation, rescued the HSCs in a dose-dependent manner. In situ hybridization and flow cytometric analysis showed that expression of Il3 was strong in wildtype embryos, but it was reduced in Runx1 +/- embryos and absent in Runx1 -/- embryos. RT-PCR and FACS analyses demonstrated expression of all mouse Il3 receptor chains (see IL3RA; 308385) in HSCs of both wildtype and Runx1 +/- mice. Transplantation experiments showed that Il3 neutralizing antibody or deletion of Il3 prevented growth of normal HSC numbers. Robin et al. (2006) proposed that IL3 acts as a survival and proliferation factor for preexisting HSCs and is critical for HSC fate determination and expansion in the embryo.

To induce polymicrobial sepsis, Weber et al. (2015) subjected wildtype mice and Il3-null mice, which had normal monocyte and neutrophil blood profiles, to cecal ligation and puncture (CLP). Unlike wildtype CLP mice, Il3-null CLP mice were protected from sepsis and mortality, with or without antibiotic treatment. Wildtype mice showed neutrophilia and monocytosis, accompanied by high serum levels of Il1b, Tnf (191160), and Il6 (147620) early after CLP, whereas Il3-null mice had unchanged phagocyte numbers. Wildtype CLP mice accumulated phagocytes in lung and liver and had abnormal liver morphology, indicating that Il3 contributed to septic shock. Wildtype CLP mice also generated large numbers of progenitor cells in bone marrow in an Il3- and lipopolysaccharide-dependent manner. Il3-null CLP mice treated with recombinant IL3 succumbed to infection. Cd19-positive B cells in spleen, carrying markers for IRA B cells, were the major source of Il3, and Il3 and IRA cell numbers increased following CLP. Weber et al. (2015) concluded that Il3-producing IRA B cells induce emergency myelopoiesis and potentiate septic shock in mice.


REFERENCES

  1. Celestin, J., Rotschke, O., Falk, K., Ramesh, N., Jabara, H., Strominger, J., Geha, R. S. IL-3 induces B7.2 (CD86) expression and costimulatory activity in human eosinophils. J. Immun. 167: 6097-6104, 2001. [PubMed: 11714768, related citations] [Full Text]

  2. Chavany, C., Vicario-Abejon, C., Miller, G., Jendoubi, M. Transgenic mice for interleukin 3 develop motor neuron degeneration associated with autoimmune reaction against spinal cord motor neurons. Proc. Nat. Acad. Sci. 95: 11354-11359, 1998. [PubMed: 9736740, images, related citations] [Full Text]

  3. Chiang, C. S., Powell, H. C., Gold, L. H., Samimi, A., Campbell, I. L. Macrophage/microglial-mediated primary demyelination and motor disease induced by the central nervous system production of interleukin-3 in transgenic mice. J. Clin. Invest. 97: 1512-1524, 1996. [PubMed: 8617885, related citations] [Full Text]

  4. Clark-Lewis, I., Aebersold, R., Ziltener, H., Schrader, J. W., Hood, L. E., Kent, S. B. H. Automated chemical synthesis of a protein growth factor for hemopoietic cells, interleukin-3. Science 231: 134-139, 1986. [PubMed: 3079915, related citations] [Full Text]

  5. Cockayne, D. A., Bodine, D. M., Cline, A., Nienhuis, A. W., Dunbar, C. E. Transgenic mice expressing antisense interleukin-3 RNA develop a B-cell lymphoproliferative syndrome or neurologic dysfunction. Blood 84: 2699-2710, 1994. [PubMed: 7919383, related citations]

  6. Devireddy, L. R., Teodoro, J. G., Richard, F. A., Green, M. R. Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science 293: 829-834, 2001. [PubMed: 11486081, related citations] [Full Text]

  7. Donahue, R. E., Seehra, J., Metzger, M., Lefebvre, D., Rock, B., Carbone, S., Nathan, D. G., Garnick, M., Sehgal, P. K., Laston, D., LaVallie, E., McCoy, J., Schendel, P. F., Norton, C., Turner, K., Yang, Y.-C., Clark, S. C. Human IL-3 and GM-CSF act synergistically in stimulating hematopoiesis in primates. Science 241: 1820-1823, 1988. [PubMed: 3051378, related citations] [Full Text]

  8. Fung, M. C., Hapel, A. J., Ymer, S., Cohen, D. R., Johnson, R. M., Campbell, H. D., Young, I. G. Molecular cloning of cDNA for murine interleukin-3. Nature 307: 233-237, 1984. [PubMed: 6420702, related citations] [Full Text]

  9. Grimaldi, J. C., Meeker, T. C. The t(5;14) chromosomal translocation in a case of acute lymphocytic leukemia joins the interleukin-3 gene to the immunoglobulin heavy chain gene. Blood 73: 2081-2085, 1989. [PubMed: 2499362, related citations]

  10. Huebner, K., Nagarajan, L., Besa, E., Angert, E., Lange, B. J., Cannizzaro, L. A., van den Berghe, H., Santoli, D., Finan, J., Croce, C. M., Nowell, P. C. Order of genes on human chromosome 5q with respect to 5q interstitial deletions. Am. J. Hum. Genet. 46: 26-36, 1990. [PubMed: 2294753, related citations]

  11. Ihle, J. N., Silver, J., Kozak, C. A. Genetic mapping of the mouse interleukin 3 gene to chromosome 11. J. Immun. 138: 3051-3054, 1987. [PubMed: 3494779, related citations]

  12. Kiser, K. F., Colombi, M., Moroni, C. Isolation and characterization of dominant and recessive IL-3-independent hematopoietic transformants. Oncogene 25: 6595-6603, 2006. [PubMed: 16702946, related citations] [Full Text]

  13. Le Beau, M. M., Epstein, N. D., O'Brien, S. J., Nienhuis, A. W., Yang, Y.-C., Clark, S. C., Rowley, J. D. The interleukin 3 gene is located on human chromosome 5 and is deleted in myeloid leukemias with a deletion of 5q. Proc. Nat. Acad. Sci. 84: 5913-5917, 1987. [PubMed: 3497400, related citations] [Full Text]

  14. Le Beau, M. M., Espinosa, R., III, Neuman, W. L., Stock, W., Roulston, D., Larson, R. A., Keinanen, M., Westbrook, C. A. Cytogenetic and molecular delineation of the smallest commonly deleted region of chromosome 5 in malignant myeloid diseases. Proc. Nat. Acad. Sci. 90: 5484-5488, 1993. [PubMed: 8516290, related citations] [Full Text]

  15. Meeker, T. C., Hardy, D., Willman, C., Hogan, T., Abrams, J. Activation of the interleukin-3 gene by chromosome translocation in acute lymphocytic leukemia with eosinophilia. Blood 76: 285-289, 1990. [PubMed: 2114933, related citations]

  16. Robin, C., Ottersbach, K., Durand, C., Peeters, M., Vanes, L., Tybulewicz, V., Dzierzak, E. An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev. Cell 11: 171-180, 2006. [PubMed: 16890157, related citations] [Full Text]

  17. Siracusa, M. C., Saenz, S. A., Hill, D. A., Kim, B. S., Headley, M. B., Doering, T. A., Wherry, E. J., Jessup, H. K., Siegel, L. A., Kambayashi, T., Dudek, E. C., Kubo, M., Cianferoni, A., Spergel, J. M., Ziegler, S. F., Comeau, M. R., Artis, D. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature 477: 229-233, 2011. [PubMed: 21841801, images, related citations] [Full Text]

  18. Tong, Y., Lear, T. B., Evankovich, J., Chen, Y., Londino, J. D., Myerburg, M. M., Zhang, Y., Popescu, I. D., McDyer, J. F., McVerry, B. J., Lockwood, K. C., Jurczak, M. J., Liu, Y., Chen, B. B. The RNFT2/IL-3R-alpha axis regulates IL-3 signaling and innate immunity. JCI Insight 5: e133652, 2020. [PubMed: 31990690, images, related citations] [Full Text]

  19. Webb, G. C., Lee, J. S., Campbell, H. D., Young, I. G. The genes for interleukins 3 and 5 map to the same locus on mouse chromosome 11. Cytogenet. Cell Genet. 50: 107-110, 1989. [PubMed: 2789124, related citations] [Full Text]

  20. Weber, G. F., Chousterman, B. G., He, S., Fenn, A. M., Nairz, M., Anzai, A., Brenner, T., Uhle, F., Iwamoto, Y., Robbins, C. S., Noiret, L., Maier, S. L., and 11 others. Interleukin-3 amplifies acute inflammation and is a potential therapeutic target in sepsis. Science 347: 1260-1265, 2015. [PubMed: 25766237, images, related citations] [Full Text]

  21. Yamada, R., Tanaka, T., Unoki, M., Nagai, T., Sawada, T., Ohnishi, Y., Tsunoda, T., Yukioka, M., Maeda, A., Suzuki, K., Tateishi, H., Ochi, T., Nakamura, Y., Yamamoto, K. Association between a single-nucleotide polymorphism in the promoter of the human interleukin-3 gene and rheumatoid arthritis in Japanese patients, and maximum-likelihood estimation of combinatorial effect that two genetic loci have on susceptibility to the disease. Am. J. Hum. Genet. 68: 674-685, 2001. [PubMed: 11179015, related citations] [Full Text]

  22. Yang, Y.-C., Ciarletta, A. B., Temple, P. A., Chung, M. P., Kovacic, S., Witek-Giannotti, J. S., Leary, A. C., Kriz, R., Donahue, R. E., Wong, G. G., Clark, S. C. Human IL-3 (multi-CSF): identification by expression cloning of a novel hematopoietic growth factor related to murine IL-3. Cell 47: 3-10, 1986. [PubMed: 3489530, related citations] [Full Text]

  23. Yang, Y.-C., Kovacic, S., Kriz, R., Wolf, S., Clark, S. C., Wellems, T. E., Nienhuis, A., Epstein, N. The human genes for GM-CSF and IL3 are closely linked in tandem on chromosome 5. Blood 71: 958-961, 1988. [PubMed: 2833332, related citations]

  24. Yokota, T., Lee, F., Rennick, D., Hall, C., Arai, N., Mosmann, T., Nabel, G., Cantor, H., Arai, K. Isolation and characterization of a mouse cDNA clone that expresses mast-cell growth-factor activity in monkey cells. Proc. Nat. Acad. Sci. 81: 1070-1074, 1984. [PubMed: 6322187, related citations] [Full Text]


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* 147740

INTERLEUKIN 3; IL3


Alternative titles; symbols

MULTI-CSF


HGNC Approved Gene Symbol: IL3

Cytogenetic location: 5q31.1   Genomic coordinates (GRCh38) : 5:132,060,655-132,063,204 (from NCBI)


TEXT

Description

Interleukin-3 is a hematopoietic colony-stimulating factor that is capable of supporting the proliferation of a broad range of hematopoietic cell types. Interleukin-3 also has neurotrophic activity (Chavany et al., 1998).


Cloning and Expression

Clark-Lewis et al. (1986) chemically synthesized interleukin-3, a protein of 140 amino acids. Interleukin-3 is one of the group of lymphokines produced by T cells after activation with mitogens or antigens. The protein has been purified to homogeneity and has been shown to be a glycoprotein with an apparent molecular mass of 28,000. The structure of the protein has been deduced from sequencing of cDNA clones encoding IL3, and biologically active IL3 has been chemically synthesized based on the predicted amino acid sequence. A broad spectrum of biologic activities of IL3 suggests that this lymphokine regulates the proliferation and differentiation of early hematopoietic/lymphoid stem cells, as well as cells committed to many hematopoietic lineages. Because of its potent growth-promoting activity for multiple hematopoietic cell lineages, it has acquired a variety of designations such as mast-cell growth factor, burst-stimulating activity, multi-colony-stimulating factor, among others. There appears to be a single IL3 gene. The cDNA clones (Fung et al., 1984; Yokota et al., 1984) indicate that the precursor has 166 amino acids.

Yang et al. (1986) identified the human IL3 gene and found that it has a high degree of homology with those of gibbon and mouse.


Mapping

By using a cDNA clone, Ihle et al. (1987) mapped the IL3 gene to mouse chromosome 11 in a series of hamster x mouse somatic cell hybrids. To confirm the chromosomal assignment, they sought evidence for linkage between IL3 and other genes on chromosome 11. They found that indeed there was linkage with an oncogene known to map to mouse chromosome 11; linkage was studied in genetic crosses between 2 strains of mice. Webb et al. (1989) confirmed the assignment of both Il-3 and Il-5 to mouse chromosome 11. In man, the IL3 locus maps to the long arm of chromosome 5 in the area that is deleted in the 5q-minus syndrome, namely, 5q23-q31, by study of somatic cell hybrids and by in situ hybridization (Le Beau et al., 1987). Grimaldi and Meeker (1989) concluded that the IL3 gene is situated centromeric to the CSF2 gene.

Using chromosome-5-linked DNA probes to study somatic cell hybrids retaining partial chromosome 5 and cells from patients with acquired deletions of 5q, Huebner et al. (1990) concluded that the order of genes on 5q is as follows: cen--HEXB--DHFR--(IL5, IL4)--IL3--CSF2--FGFA--(CSF1R, PDGFRB)--ADRB2R--CSF1--qter. Furthermore, they concluded that the order and orientation of the closely linked IL3/CSF2 gene pair is cen--5-prime IL3 3-prime,5-prime CSF2 3-prime--qter.

By fluorescence in situ hybridization, Le Beau et al. (1993) mapped the IL3 gene to 5q31.1.


Gene Function

Yang et al. (1986) showed that primate IL3 is functionally related to murine Il3 in terms of multipotent colony-stimulating activity.

From in vivo studies in the cynomolgus macaque, Donahue et al. (1988) concluded that IL3 infusion expands an early cell population that subsequently requires the action of a later-acting factor such as GMCSF (CSF2; 138960) to complete its development. Thus, linkage of the genes coding these 2 hematopoietic factors, which are within 9 kb of each other on chromosome 5 (Yang et al., 1988), may have a functional significance.

Chavany et al. (1998) examined the effect of IL3 on embryonic motor neuron survival in mixed spinal cord cultures. The results suggested the motor neuron degeneration is not directly triggered by the high level of expression of IL3.

Using DNA microarrays to analyze IL3-dependent murine FL5.12 pro-B cells, Devireddy et al. (2001) found that the gene undergoing maximal transcriptional induction after cytokine withdrawal is 24p3, which encodes a secreted lipocalin (LCN2; 600181). Conditioned medium from IL3-deprived cells contained 24p3 and induced apoptosis in naive cells, even when IL3 was present. 24p3 also induced apoptosis in a wide variety of leukocytes but not other cell types. Apoptotic sensitivity correlated with the presence of a putative 24p3 cell surface receptor. Devireddy et al. (2001) concluded that IL3 deprivation activates 24p3 transcription, leading to synthesis and secretion of 24p3, which induces apoptosis through an autocrine pathway. In addition to murine FL5.12 pro-B cells many other cell types were sensitive to 24p3-mediated apoptosis: murine primary thymocytes, murine primary splenocytes, murine primary bone marrow cells, human primary neutrophils, and human peripheral blood lymphocytes. In contrast, human primary macrophages, HeLa cells, and Jurkat cells were not susceptible to 24p3-mediated apoptosis.

Resting eosinophils express neither MHC class II proteins or costimulatory B7 molecules and fail to induce proliferation of T cells to antigens. Celestin et al. (2001) reported that IL3 induces expression of HLA-DR and B7.2 (601020) on eosinophils, but, unlike IL5 (147580) and GMCSF, it does not induce expression of B7.1 (112203). IL3-treated eosinophils supported modest T-cell proliferation in response to superantigen toxic shock syndrome-1 antigen, as well as proliferation of HLA-DR-restricted T-cell clones to tetanus toxoid (TT) and influenza virus antigenic peptides. The response was blocked by anti-B7.2 monoclonal antibody. IL3-treated eosinophils were unable to present native TT antigen to either resting or TT-specific cloned T cells. Parallel experiments established that IL5 and GMCSF induce T-cell proliferation to peptides but not to native TT antigen. Celestin et al. (2001) suggested that eosinophils activated by IL3 may contribute to T-cell activation in allergic and parasitic diseases by presenting superantigens and peptides to T cells.

Kiser et al. (2006) used retroviral integration mutagenesis and a chemical frameshift mutagen to transform Il3-dependent mouse bone marrow-derived PB-3c mast cells to Il3 independence. With 21 of 22 clones, Il3 independence resulted from a recessive mechanism, and reversion to Il3 dependence was observed in hybrids with the parental cell line. Recessive clones displayed increased phosphorylated Erk1 (MAPK3; 601795)/Erk2 (MAPK1; 176948) expression and were sensitive to inhibition of Mek (see MAP2K1; 176872), but not Raf1 (164760). The dominant Il3-independent clone showed no signs of MAP kinase pathway activation, but it had constitutive phosphorylation of Stat5 (601511). Kiser et al. (2006) concluded that Il3-dependent PB-3c mast cells have multiple options to acquire Il3 growth autonomy, including transcriptional and posttranscriptional mechanisms affecting the distal regulators Erk or Stat5.

Siracusa et al. (2011) demonstrated that TSLP (607003) promotes systemic basophilia, that disruption of TSLP-TSLPR (300357) interactions results in defective basophil responses, and that TSLPR-sufficient basophils can restore TH2-cell-dependent immunity in vivo. TSLP acted directly on bone marrow-resident progenitors to promote basophil responses selectively. Critically, TSLP could elicit basophil responses in both IL3-IL3R-sufficient and -deficient environments, and genomewide transcriptional profiling and functional analyses identified heterogeneity between TSLP-elicited versus IL3-elicited basophils. Furthermore, activated human basophils expressed TSLPR, and basophils isolated from eosinophilic esophagitis (see 610247) patients were distinct from classical basophils. Siracusa et al. (2011) concluded that collectively, their studies identified previously unrecognized heterogeneity within the basophil cell lineage and indicated that expression of TSLP may influence susceptibility to multiple allergic diseases by regulating basophil hematopoiesis and eliciting a population of functionally distinct basophils that promote TH2 cytokine-mediated inflammation.

By retrospectively analyzing the plasma of septic patients, Weber et al. (2015) found that increased IL3 levels within the first 24 hours after sepsis onset predicted death. Flow cytometric and immunohistochemical analyses of splenectomy patients showed that IL3-producing, CD19 (107265)-positive B cells carrying markers for innate response activator (IRA) B cells amplified inflammation. Weber et al. (2015) proposed that IL3 is a major upstream orchestrator of the septic inflammatory phase.

By overexpression analysis in mouse lung epithelial (MLE) cells, Tong et al. (2020) showed that Rnft2 (620254) negatively regulated Il3ra (308385) stability through ubiquitination and proteasomal degradation in response to Il3 signaling. Rnft2 affected Il3ra abundance and signaling in response to Il3 by associating with Il3ra and targeting it as a substrate. In vitro analysis in MLE cells revealed that Il3 augmented proinflammatory cellular responses to lipopolysaccharide (LPS) through Rnft2 and Il3ra, as LPS sensitized cells to Il3 through stabilization of Il3ra. Mutation analysis identified lys357 of Il3ra as a critical residue for regulation of its stability, as lys357 mutants were resistant to Rnft2-directed degradation. Analysis with a mouse model for pneumonia and severe lung injury found that Il3 drove inflammation in LPS-induced lung injury in vivo, and further analysis revealed that lung inflammation was regulated through the Rnft2/Il3ra/Il3 axis. Moreover, analysis with parenchymal explant lung samples from human cystic fibrosis (CF; 219700) patients showed that the RNFT2/IL3RA/IL3 axis was also involved in human inflammatory lung disease.


Molecular Genetics

Yamada et al. (2001) designed a case-control study to investigate association between rheumatoid arthritis and a single-nucleotide polymorphism (SNP) in the IL3 promoter region. A particularly strong association was observed in females with early onset.


Cytogenetics

In a case of B-lineage acute lymphocytic leukemia associated with peripheral blood eosinophilia, Grimaldi and Meeker (1989) found that a chromosomal translocation t(5;14)(q31;q32) joined the immunoglobulin heavy chain joining region (IGHJ; 147010) to the promoter region of the IL3 gene in opposite transcriptional orientations. They suggested that activation of the IL3 gene by the enhancer of the immunoglobulin heavy chain gene played a central role in the pathogenesis of the leukemia and the associated eosinophilia. Meeker et al. (1990) found excess IL3 mRNA produced by leukemic cells in one patient; in a second patient, serum IL3 levels correlated with disease activity.


Animal Model

In addition to their role in stimulating the proliferation and differentiation of various hematopoietic progenitor cells, IL3 and other cytokines have been found to have neurotrophic activity and to be associated with neurologic disorders, suggesting their complex role in the central nervous system (CNS). IL3 is expressed by neurons and astrocytes in mouse brain. Some interleukins, including IL3, are associated with both neurodegeneration and repair in the CNS. IL1-beta (IL1B; 147720) and other cytokines, including IL3, are neurotrophic at low concentration, or neurotoxic at high concentration. To understand the pleiotropic role of IL3 and how it exerts its role in the pathogenesis of CNS injury, several groups generated transgenic mice and analyzed their phenotype. Cockayne et al. (1994) found that transgenic mice expressing an antisense RNA for IL3 exhibited either a lymphoproliferative syndrome or a progressive neurologic dysfunction characterized by abnormal rotatory movement and ataxia. Chiang et al. (1996) generated transgenic mice for IL3 under the control of the glial fibrillary acidic protein gene (GFAP; 137780) promoter to target expression of Il3 to astrocytes. These mice developed a progressive motor dysfunction characterized, at onset, by impaired rotarod performance. They attributed the dysfunction to demyelination induced by activation and recruitment of microglial cells in the brain. Chavany et al. (1998) developed a transgenic IL3 mouse that overexpressed mouse IL3 under the control of a cytomegalovirus (CMV) promoter to achieve widespread expression of the transgene in various organs. They showed that general overexpression of IL3 in mice leads to a motor neuron disease with several features of human amyotrophic lateral sclerosis and progressive muscular atrophy. Furthermore, these symptoms were associated with a severe autoimmune reaction against spinal cord motor neurons. The animals exhibited hind limb paralysis at 7 months of age, associated with dendritic and axonal degeneration, loss of motor neurons in the spinal cord, and autoimmune reaction against these cells.

Robin et al. (2006) noted that Runx1 (151385) -/- mice die at embryonic day 12 to 13 with no aorta-gonad-mesonephros (AGM) region and fetal liver hematopoiesis, and that Runx1 +/- mice have reduced adult-repopulating ability of hematopoietic stem cells (HSCs). Since IL3 is a RUNX1 target, they examined whether Il3 affects HSCs in the mouse embryo. Using limiting dilution and Poisson statistical analysis, Robin et al. (2006) found that Runx1 +/- mice had fewer HSCs in AGM, but not in yolk sac or placenta, than wildtype mice. AGM-derived HSCs cultured from Runx1 +/- mice in the presence of Il3, but not other cytokines, followed by transplantation, rescued the HSCs in a dose-dependent manner. In situ hybridization and flow cytometric analysis showed that expression of Il3 was strong in wildtype embryos, but it was reduced in Runx1 +/- embryos and absent in Runx1 -/- embryos. RT-PCR and FACS analyses demonstrated expression of all mouse Il3 receptor chains (see IL3RA; 308385) in HSCs of both wildtype and Runx1 +/- mice. Transplantation experiments showed that Il3 neutralizing antibody or deletion of Il3 prevented growth of normal HSC numbers. Robin et al. (2006) proposed that IL3 acts as a survival and proliferation factor for preexisting HSCs and is critical for HSC fate determination and expansion in the embryo.

To induce polymicrobial sepsis, Weber et al. (2015) subjected wildtype mice and Il3-null mice, which had normal monocyte and neutrophil blood profiles, to cecal ligation and puncture (CLP). Unlike wildtype CLP mice, Il3-null CLP mice were protected from sepsis and mortality, with or without antibiotic treatment. Wildtype mice showed neutrophilia and monocytosis, accompanied by high serum levels of Il1b, Tnf (191160), and Il6 (147620) early after CLP, whereas Il3-null mice had unchanged phagocyte numbers. Wildtype CLP mice accumulated phagocytes in lung and liver and had abnormal liver morphology, indicating that Il3 contributed to septic shock. Wildtype CLP mice also generated large numbers of progenitor cells in bone marrow in an Il3- and lipopolysaccharide-dependent manner. Il3-null CLP mice treated with recombinant IL3 succumbed to infection. Cd19-positive B cells in spleen, carrying markers for IRA B cells, were the major source of Il3, and Il3 and IRA cell numbers increased following CLP. Weber et al. (2015) concluded that Il3-producing IRA B cells induce emergency myelopoiesis and potentiate septic shock in mice.


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Contributors:
Bao Lige - updated : 02/17/2023
Paul J. Converse - updated : 4/13/2015
Ada Hamosh - updated : 9/21/2011
Paul J. Converse - updated : 3/9/2007
Paul J. Converse - updated : 10/17/2006
Paul J. Converse - updated : 1/28/2002
Ada Hamosh - updated : 8/27/2001
Victor A. McKusick - updated : 3/19/2001
Victor A. McKusick - updated : 10/5/1998

Creation Date:
Victor A. McKusick : 6/2/1986

Edit History:
mgross : 02/17/2023
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mcolton : 4/13/2015
alopez : 9/22/2011
terry : 9/21/2011
mgross : 3/13/2007
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cwells : 3/29/2001
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dkim : 10/13/1998
carol : 10/9/1998
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mark : 11/11/1997
carol : 7/1/1993
supermim : 3/16/1992
carol : 10/9/1990
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supermim : 1/24/1990