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PMID: 7935454 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A critical cytoplasmic domain of the interleukin-5 (IL-5) receptor alpha chain and its function in IL-5-mediated growth signal transduction.

Molecular and cellular biology ·Vol. 14 ·No. 11 ·1994-11-00 ·Pages 7404-13

Takaki S, Kanazawa H, Shiiba M, Takatsu K

Abstract

Interleukin-5 (IL-5) regulates the production and function of B cells, eosinophils, and basophils. The IL-5 receptor (IL-5R) consists of two distinct membrane proteins, alpha and beta. The alpha chain (IL-5R alpha) is specific to IL-5. The beta chain is the common beta chain (beta c) of receptors for IL-3 and granulocyte-macrophage colony-stimulating factor (GM-CSF). The cytoplasmic domains of both alpha and beta chains are essential for signal transduction. In this study, we generated cDNAs of IL-5R alpha having various mutations in their cytoplasmic domains and examined the function of these mutants by expressing them in IL-3-dependent FDC-P1 cells. The membrane-proximal proline-rich sequence of the cytoplasmic domain of IL-5R alpha, which is conserved among the alpha chains of IL-5R, IL-3R, and GM-CSF receptor (GM-CSFR), was found to be essential for the IL-5-induced proliferative response, expression of nuclear proto-oncogenes such as c-jun, c-fos, and c-myc, and tyrosine phosphorylation of cellular proteins including JAK2 protein-tyrosine kinase. In addition, analysis using chimeric receptors which consist of the extracellular domain of IL-5R alpha and the cytoplasmic domain of beta c suggested that dimerization of the cytoplasmic domain of beta c may be an important step in activating the IL-5R complex and transducing intracellular growth signals.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Cell Division/physiology Cell Line Cytoplasm/physiology DNA Primers/genetics Gene Expression Interleukin-5/physiology Mice Molecular Sequence Data Phosphorylation Protein Conformation Proto-Oncogenes Receptors, Interleukin/chemistry,genetics,physiology Receptors, Interleukin-5 Sequence Deletion Signal Transduction/physiology
Chemicals
DNA Primers Interleukin-5 Receptors, Interleukin Receptors, Interleukin-5
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Takaki S
Department of Immunology, University of Tokyo, Japan.
Kanazawa H
Shiiba M
Takatsu K
References (45)
45 references, click to expand
  1. Identification of the second subunit of the murine interleukin-5 receptor: interleukin-3 receptor-like protein, AIC2B is a component of the high affinity interleukin-5 receptor.
    EMBO J. 1991 Oct;10(10):2833-8 PMID: 1915265
  2. Critical cytoplasmic region of the interleukin 6 signal transducer gp130 is conserved in the cytokine receptor family.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11349-53 PMID: 1662392
  3. Molecular cloning and expression of the human interleukin 5 receptor.
    J Exp Med. 1992 Feb 1;175(2):341-51 PMID: 1732409
  4. Human growth hormone and extracellular domain of its receptor: crystal structure of the complex.
    Science. 1992 Jan 17;255(5042):306-12 PMID: 1549776
  5. Interleukin-3-dependent expression of the c-myc and c-fos proto-oncogenes in hemopoietic cell lines.
    EMBO J. 1986 Feb;5(2):317-23 PMID: 3086085
  6. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  7. Hematopoietic growth factors activate the tyrosine phosphorylation of distinct sets of proteins in interleukin-3-dependent murine cell lines.
    Mol Cell Biol. 1988 May;8(5):2214-8 PMID: 3260330
  8. Receptors for T cell-replacing factor/interleukin 5. Specificity, quantitation, and its implication.
    J Exp Med. 1988 Sep 1;168(3):863-78 PMID: 3262707
  9. Characterization of high-affinity receptors for interleukin 5 on interleukin 5-dependent cell lines.
    Proc Natl Acad Sci U S A. 1989 Apr;86(7):2311-5 PMID: 2784567
  10. Multiple hematopoietic growth factors signal through tyrosine phosphorylation.
    Growth Factors. 1990;2(2-3):213-20 PMID: 1692720
  11. Distribution of IL-5 receptor-positive B cells. Expression of IL-5 receptor on Ly-1(CD5)+ B cells.
    J Immunol. 1990 Jun 1;144(11):4218-25 PMID: 1692859
  12. Cloning and expression of a gene encoding an interleukin 3 receptor-like protein: identification of another member of the cytokine receptor gene family.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5459-63 PMID: 1695379
  13. Molecular cloning of a second subunit of the receptor for human granulocyte-macrophage colony-stimulating factor (GM-CSF): reconstitution of a high-affinity GM-CSF receptor.
    Proc Natl Acad Sci U S A. 1990 Dec;87(24):9655-9 PMID: 1702217
  14. Molecular cloning and expression of the murine interleukin-5 receptor.
    EMBO J. 1990 Dec;9(13):4367-74 PMID: 2265612
  15. Interleukin 5 and interleukin 3 induce serine and tyrosine phosphorylations of several cellular proteins in an interleukin 5-dependent cell line.
    Biochem Biophys Res Commun. 1990 Dec 31;173(3):1102-8 PMID: 2125214
  16. Characterization of the murine interleukin 5 receptor by using a monoclonal antibody.
    Int Immunol. 1990;2(2):181-7 PMID: 2088484
  17. Structure-function analysis of interleukin-5 utilizing mouse/human chimeric molecules.
    EMBO J. 1991 May;10(5):1193-9 PMID: 2022187
  18. Molecular basis of a high affinity murine interleukin-5 receptor.
    EMBO J. 1991 Aug;10(8):2133-7 PMID: 2065657
  19. Expression cloning of the human IL-3 receptor cDNA reveals a shared beta subunit for the human IL-3 and GM-CSF receptors.
    Cell. 1991 Sep 20;66(6):1165-74 PMID: 1833064
  20. A human high affinity interleukin-5 receptor (IL5R) is composed of an IL5-specific alpha chain and a beta chain shared with the receptor for GM-CSF.
    Cell. 1991 Sep 20;66(6):1175-84 PMID: 1833065
  21. Two distinct functional high affinity receptors for mouse interleukin-3 (IL-3).
    EMBO J. 1992 May;11(5):1875-84 PMID: 1582416
  22. Cloning of the low-affinity murine granulocyte-macrophage colony-stimulating factor receptor and reconstitution of a high-affinity receptor complex.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4295-9 PMID: 1533931
  23. Cytokine receptors and signal transduction.
    Annu Rev Immunol. 1992;10:295-331 PMID: 1590989
  24. Interleukin-5, eosinophils, and disease.
    Blood. 1992 Jun 15;79(12):3101-9 PMID: 1596561
  25. The erythropoietin receptor transmembrane region is necessary for activation by the Friend spleen focus-forming virus gp55 glycoprotein.
    Mol Cell Biol. 1992 Jul;12(7):2949-57 PMID: 1320192
  26. A protein tyrosine kinase in the interferon alpha/beta signaling pathway.
    Cell. 1992 Jul 24;70(2):313-22 PMID: 1386289
  27. Critical cytoplasmic domains of the common beta subunit of the human GM-CSF, IL-3 and IL-5 receptors for growth signal transduction and tyrosine phosphorylation.
    EMBO J. 1992 Oct;11(10):3541-9 PMID: 1396555
  28. Interleukin-5.
    Curr Opin Immunol. 1992 Jun;4(3):299-306 PMID: 1418709
  29. Signal transduction mediated by growth hormone receptor and its chimeric molecules with the granulocyte colony-stimulating factor receptor.
    Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):123-7 PMID: 7678333
  30. Identification of a ten-amino acid proline-rich SH3 binding site.
    Science. 1993 Feb 19;259(5098):1157-61 PMID: 8438166
  31. Recombinant soluble human interleukin-5 (hIL-5) receptor molecules. Cross-linking and stoichiometry of binding to IL-5.
    J Biol Chem. 1993 Mar 25;268(9):6581-7 PMID: 8454628
  32. A novel dimer configuration revealed by the crystal structure at 2.4 A resolution of human interleukin-5.
    Nature. 1993 May 13;363(6425):172-6 PMID: 8483502
  33. Reconstitution of the functional receptors for murine and human interleukin 5.
    J Exp Med. 1993 Jun 1;177(6):1523-9 PMID: 8496674
  34. IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase.
    Science. 1993 Jun 18;260(5115):1808-10 PMID: 8511589
  35. Ligand-dependent activation of chimeric receptors with the cytoplasmic domain of the interleukin-3 receptor beta subunit (beta IL3).
    J Biol Chem. 1993 Jul 25;268(21):15833-9 PMID: 8340408
  36. JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin.
    Cell. 1993 Jul 30;74(2):227-36 PMID: 8343951
  37. Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase.
    Cell. 1993 Jul 30;74(2):237-44 PMID: 8343952
  38. Structure of the murine Jak2 protein-tyrosine kinase and its role in interleukin 3 signal transduction.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8429-33 PMID: 8378315
  39. Tyrosine phosphorylation of DNA binding proteins by multiple cytokines.
    Science. 1993 Sep 24;261(5129):1730-3 PMID: 8378773
  40. The GTPase dynamin binds to and is activated by a subset of SH3 domains.
    Cell. 1993 Oct 8;75(1):25-36 PMID: 8402898
  41. Signal transduction by the high-affinity GM-CSF receptor: two distinct cytoplasmic regions of the common beta subunit responsible for different signaling.
    EMBO J. 1993 Nov;12(11):4181-9 PMID: 8223433
  42. Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130.
    Science. 1994 Jan 7;263(5143):89-92 PMID: 8272872
  43. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components.
    Science. 1994 Jan 7;263(5143):92-5 PMID: 8272873
  44. Cytokine signal transduction.
    Cell. 1994 Jan 28;76(2):253-62 PMID: 8293462
  45. Structural basis for the binding of proline-rich peptides to SH3 domains.
    Cell. 1994 Mar 11;76(5):933-45 PMID: 7510218
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1994-11-00
Pages
7404-13
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC359275
Subset
IM
Corrections
CommentIn
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