Abstract
Cytokine-inducible protein SSI-1 [signal transducers and activators of transcription (STAT)-induced STAT inhibitor 1, also referred to as SOCS-1 (suppressor of cytokine signaling 1) or JAB (Janus kinase-binding protein)] negatively regulates cytokine receptor signaling by inhibition of JAK kinases. The SSI family of proteins includes eight members that are structurally characterized by an SH2 domain and a C-terminal conserved region that we have called the SC-motif. In this study, we investigated the roles of these domains in the function of SSI-1. Results of reporter assays demonstrated that the pre-SH2 domain (24 aa in front of the SH2 domain) and the SH2 domain of SSI-1 were required for the suppression by SSI-1 of interleukin 6 signaling. Coexpression studies of COS7 cells revealed that these domains also were required for inhibition of three JAKs (JAK1, JAK2, and TYK2). Furthermore, deletion of the SH2 domain, but not the pre-SH2 domain, resulted in loss of association of SSI-1 with TYK2. Thus, SSI-1 associates with JAK family kinase via its SH2 domain, and the pre-SH2 domain is required for the function of SSI-1. Deletion of the SC-motif markedly reduced expression of SSI-1 protein in M1 cells, and this reduction was reversed by treatment with proteasome inhibitors, suggesting that this motif is required to protect the SSI-1 molecule from proteolytic degradation. Based on these findings, we concluded that three distinct domains of SSI-1 (the pre-SH2 domain, the SH2 domain, and the SC-motif) cooperate in the suppression of interleukin 6 signaling.
MeSH Terms
Amino Acid Sequence
Animals
COS Cells
Carrier Proteins/chemistry,metabolism
Conserved Sequence
Humans
Interleukin-6/antagonists & inhibitors,physiology
Intracellular Signaling Peptides and Proteins
Luciferases/genetics
Mice
Mice, Inbred BALB C
Molecular Sequence Data
Mutagenesis, Site-Directed
Peptide Fragments/chemistry,immunology
Point Mutation
Protein-Tyrosine Kinases/antagonists & inhibitors
Recombinant Fusion Proteins/biosynthesis
Recombinant Proteins/chemistry,metabolism
Repressor Proteins
Sequence Alignment
Sequence Deletion
Sequence Homology, Amino Acid
Signal Transduction
Suppressor of Cytokine Signaling 1 Protein
Suppressor of Cytokine Signaling Proteins
Transfection
src Homology Domains
Chemicals
Carrier Proteins
Interleukin-6
Intracellular Signaling Peptides and Proteins
Peptide Fragments
Recombinant Fusion Proteins
Recombinant Proteins
Repressor Proteins
SOCS1 protein, human
Socs1 protein, mouse
Suppressor of Cytokine Signaling 1 Protein
Suppressor of Cytokine Signaling Proteins
Luciferases
Protein-Tyrosine Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Narazaki M
Department of Medicine III, Osaka University Medical School, 2-2, Yamada-oka, Suita, Osaka 565-0871, Japan.
Fujimoto M
Matsumoto T
Morita Y
Saito H
Kajita T
Yoshizaki K
Naka T
Kishimoto T
References (20)
20 references, click to expand
-
Identification of residues in GTPase-activating protein Src homology 2 domains that control binding to tyrosine phosphorylated growth factor receptors and p62.
J Biol Chem. 1992 Nov 15;267(32):22779-86
PMID: 1385407
-
Binding of a high affinity phosphotyrosyl peptide to the Src SH2 domain: crystal structures of the complexed and peptide-free forms.
Cell. 1993 Mar 12;72(5):779-90
PMID: 7680960
-
Induction by interleukin-6 of interferon regulatory factor 1 (IRF-1) gene expression through the palindromic interferon response element pIRE and cell type-dependent control of IRF-1 binding to DNA.
EMBO J. 1994 Apr 15;13(8):1942-9
PMID: 8168491
-
Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins.
Science. 1994 Jun 3;264(5164):1415-21
PMID: 8197455
-
Stat4, a novel gamma interferon activation site-binding protein expressed in early myeloid differentiation.
Mol Cell Biol. 1994 Jul;14(7):4342-9
PMID: 8007943
-
Jaks and Stats in signaling by the cytokine receptor superfamily.
Trends Genet. 1995 Feb;11(2):69-74
PMID: 7716810
-
A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors.
EMBO J. 1995 Jun 15;14(12):2816-26
PMID: 7796808
-
Interleukin-6 family of cytokines and gp130.
Blood. 1995 Aug 15;86(4):1243-54
PMID: 7632928
-
CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway and modulates STAT5 activation.
Blood. 1997 May 1;89(9):3148-54
PMID: 9129017
-
A family of cytokine-inducible inhibitors of signalling.
Nature. 1997 Jun 26;387(6636):917-21
PMID: 9202125
-
A new protein containing an SH2 domain that inhibits JAK kinases.
Nature. 1997 Jun 26;387(6636):921-4
PMID: 9202126
-
Structure and function of a new STAT-induced STAT inhibitor.
Nature. 1997 Jun 26;387(6636):924-9
PMID: 9202127
-
Cloning and functional analysis of new members of STAT induced STAT inhibitor (SSI) family: SSI-2 and SSI-3.
Biochem Biophys Res Commun. 1997 Aug 8;237(1):79-83
PMID: 9266833
-
Cloning and characterization of novel CIS family genes.
Biochem Biophys Res Commun. 1997 Oct 20;239(2):439-46
PMID: 9344848
-
Cytokine signaling: cytokine-inducible signaling inhibitors.
Curr Biol. 1997 Dec 1;7(12):R784-8
PMID: 9382832
-
Twenty proteins containing a C-terminal SOCS box form five structural classes.
Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):114-9
PMID: 9419338
-
Growth hormone preferentially induces the rapid, transient expression of SOCS-3, a novel inhibitor of cytokine receptor signaling.
J Biol Chem. 1998 Jan 16;273(3):1285-7
PMID: 9430658
-
Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses.
Cell. 1998 May 1;93(3):373-83
PMID: 9590172
-
Jak2 is essential for signaling through a variety of cytokine receptors.
Cell. 1998 May 1;93(3):385-95
PMID: 9590173
-
Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis.
Cell. 1998 May 1;93(3):397-409
PMID: 9590174