The Murine DUB-1 Gene is Specifically Induced by the Betac Subunit of Interleukin-3 Receptor

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 1996 Sep 1

PMID 8756639

Citations 20

Authors

Y Zhu

M Pless

R Inhorn

B Mathey-Prevot

A D DAndrea

Affiliations

Soon will be listed here.

Abstract

Cytokines regulate cell growth and differentiation by inducing the expression of specific target genes. We have recently isolated a cytokine-inducible, immediate-early cDNA, DUB-1, that encodes a deubiquitinating enzyme. The DUB-1 mRNA was specifically induced by the receptors for interleukin-3, granulocyte-macrophage colony-stimulating factor, and interleukin-5, suggesting a role for the beta common (betac subunit known to be shared by these receptors. In order to identify the mechanism of cytokine induction, we isolated a murine genomic clone for DUB-1 containing a functional promoter region. The DUB-1 gene contains two exons, and the nucleotide sequence of its coding region is identical to the sequence of DUB-1 cDNA. Various regions of the 5' flanking region of the DUB-1 gene were assayed for cytokine-inducible activity. An enhancer region that retains the beta c-specific inducible activity of the DUB-1 gene was identified. Enhancer activity was localized to a 112-bp fragment located 1.4 kb upstream from the ATG start codon. Gel mobility shift assays revealed two specific protein complexes that bound to this minimal enhancer region. One complex was induced by betac signaling, while the other was noninducible. Finally, the membrane-proximal region of human betac was required for DUB-1 induction. In conclusion, DUB-1 is the first example of an immediate-early gene that is induced by a specific subunit of a cytokine receptor. Further analysis of the DUB-1 enhancer element may reveal specific determinants of a betac-specific signaling pathway.

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References

Park L, Martin U, Sorensen R, Luhr S, Morrissey P, Cosman D . 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; 89(10):4295-9. PMC: 49068. DOI: 10.1073/pnas.89.10.4295. View

Palacios R, Steinmetz M . Il-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell. 1985; 41(3):727-34. DOI: 10.1016/s0092-8674(85)80053-2. View

Liang P, Pardee A . Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992; 257(5072):967-71. DOI: 10.1126/science.1354393. View

Wegenka U, Buschmann J, Lutticken C, Heinrich P, Horn F . Acute-phase response factor, a nuclear factor binding to acute-phase response elements, is rapidly activated by interleukin-6 at the posttranslational level. Mol Cell Biol. 1993; 13(1):276-88. PMC: 358907. DOI: 10.1128/mcb.13.1.276-288.1993. View

Sims S, Cha Y, Romine M, Gao P, Gottlieb K, Deisseroth A . A novel interferon-inducible domain: structural and functional analysis of the human interferon regulatory factor 1 gene promoter. Mol Cell Biol. 1993; 13(1):690-702. PMC: 358947. DOI: 10.1128/mcb.13.1.690-702.1993. View

Beadling C, Johnson K, Smith K . Isolation of interleukin 2-induced immediate-early genes. Proc Natl Acad Sci U S A. 1993; 90(7):2719-23. PMC: 46167. DOI: 10.1073/pnas.90.7.2719. View

Cochran B . Regulation of immediate early gene expression. NIDA Res Monogr. 1993; 125:3-24. View

Liang P, Averboukh L, Pardee A . Distribution and cloning of eukaryotic mRNAs by means of differential display: refinements and optimization. Nucleic Acids Res. 1993; 21(14):3269-75. PMC: 309766. DOI: 10.1093/nar/21.14.3269. View

Witthuhn B, Quelle F, Silvennoinen O, Yi T, Tang B, Miura O . JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin. Cell. 1993; 74(2):227-36. DOI: 10.1016/0092-8674(93)90414-l. View

10.

Sato N, Sakamaki K, Terada N, Arai K, Miyajima A . 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; 12(11):4181-9. PMC: 413712. DOI: 10.1002/j.1460-2075.1993.tb06102.x. View

11.

Liboi E, Carroll M, DAndrea A, Mathey-Prevot B . Erythropoietin receptor signals both proliferation and erythroid-specific differentiation. Proc Natl Acad Sci U S A. 1993; 90(23):11351-5. PMC: 47980. DOI: 10.1073/pnas.90.23.11351. View

12.

Watanabe S, Muto A, Yokota T, Miyajima A, Arai K . Differential regulation of early response genes and cell proliferation through the human granulocyte macrophage colony-stimulating factor receptor: selective activation of the c-fos promoter by genistein. Mol Biol Cell. 1993; 4(10):983-92. PMC: 275732. DOI: 10.1091/mbc.4.10.983. View

13.

Seldin D, Leder P . Mutational analysis of a critical signaling domain of the human interleukin 4 receptor. Proc Natl Acad Sci U S A. 1994; 91(6):2140-4. PMC: 43325. DOI: 10.1073/pnas.91.6.2140. View

14.

Darnell Jr J, Kerr I, Stark G . Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 1994; 264(5164):1415-21. DOI: 10.1126/science.8197455. View

15.

Quelle F, Sato N, Witthuhn B, Inhorn R, Eder M, Miyajima A . JAK2 associates with the beta c chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol Cell Biol. 1994; 14(7):4335-41. PMC: 358804. DOI: 10.1128/mcb.14.7.4335-4341.1994. View

16.

Witthuhn B, Silvennoinen O, Miura O, Lai K, Cwik C, Liu E . Involvement of the Jak-3 Janus kinase in signalling by interleukins 2 and 4 in lymphoid and myeloid cells. Nature. 1994; 370(6485):153-7. DOI: 10.1038/370153a0. View

17.

Kawamura M, McVicar D, Johnston J, Blake T, Chen Y, Lal B . Molecular cloning of L-JAK, a Janus family protein-tyrosine kinase expressed in natural killer cells and activated leukocytes. Proc Natl Acad Sci U S A. 1994; 91(14):6374-8. PMC: 44204. DOI: 10.1073/pnas.91.14.6374. View

18.

Sato N, Miyajima A . Multimeric cytokine receptors: common versus specific functions. Curr Opin Cell Biol. 1994; 6(2):174-9. DOI: 10.1016/0955-0674(94)90133-3. View

19.

Ihle J, Witthuhn B, Quelle F, Yamamoto K, Thierfelder W, Kreider B . Signaling by the cytokine receptor superfamily: JAKs and STATs. Trends Biochem Sci. 1994; 19(5):222-7. DOI: 10.1016/0968-0004(94)90026-4. View

20.

Hou J, Schindler U, Henzel W, Ho T, Brasseur M, McKnight S . An interleukin-4-induced transcription factor: IL-4 Stat. Science. 1994; 265(5179):1701-6. DOI: 10.1126/science.8085155. View