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CIS, a cytokine inducible SH2 protein, is a target of the JAK-STAT5 pathway
and modulates STAT5 activation
A Matsumoto, M Masuhara, K Mitsui, M Yokouchi, M Ohtsubo, H Misawa, A Miyajima and A Yoshimura
Insititute of Life Science, Kurume University, Japan.
We searched for immediate early cytokine responsive genes and isolated a
novel gene, CIS (Cytokine Inducible SH2 containing protein) that is induced
in hematopoietic cells by a subset of cytokines including interleukin-2
(IL-2), IL-3, and erythropoietin (EPO). The mutant IL-2 receptor that fails
to activate STAT5 could not induce CIS, suggesting that STAT5 is involved
in the cytokine-inducible expression of CIS. We cloned the 5'-flanking
region of the CIS gene and found that about 200 bases upstream of the
transcription-initiation site contain four potential STAT5 binding sites
(MGF boxes). Luciferase reporter assays showed that these MGF boxes were
essential for EPO-dependent promoter activity. Expression of STAT5 and the
EPO receptor in HEK293 cells conferred EPO-dependent activation of the CIS
promoter. These data indicate that CIS is a target of the JAK-STAT5 pathway
of cytokine receptors. CIS contains an SH2 domain and binds to tyrosine-
phosphorylated EPO and IL-3 receptors. In HEK293 cells expressing STAT5 and
the EPO receptor, EPO-dependent tyrosine phosphorylation of STAT5, as well
as EPO-dependent CIS-promoter activation, was suppressed when CIS was
coexpressed. Moreover, the induction of oncostatin M, another STAT5 target,
as well as the tyrosine-phosphorylation of STAT5, were partially suppressed
by CIS expression in Ba/F3 cells. Thus, CIS is a feedback modulator of
STAT5; its expression is induced by STAT5 and it negatively modulates STAT5
activation.
Volume 89,
Issue 9,
pp. 3148-3154,
05/01/1997
Copyright © 1997 by The American Society of Hematology

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May 15, 2001;
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3547 - 3557.
[Abstract]
[Full Text]
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D. L. Barber, B. K. Beattie, J. M. Mason, M. H.-H. Nguyen, M. Yoakim, B. G. Neel, A. D. D'Andrea, and D. A. Frank
A common epitope is shared by activated signal transducer and activator of transcription-5 (STAT5) and the phosphorylated erythropoietin receptor: implications for the docking model of STAT activation
Blood,
April 15, 2001;
97(8):
2230 - 2237.
[Abstract]
[Full Text]
[PDF]
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S. Bhattacharya, B. A. Stout, M. E. Bates, P. J. Bertics, and J. S. Malter
Granulocyte Macrophage Colony-Stimulating Factor and Interleukin-5 Activate STAT5 and Induce CIS1 mRNA in Human Peripheral Blood Eosinophils
Am. J. Respir. Cell Mol. Biol.,
March 1, 2001;
24(3):
312 - 316.
[Abstract]
[Full Text]
[PDF]
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C. Brender, M. Nielsen, K. Kaltoft, G. Mikkelsen, Q. Zhang, M. Wasik, N. Billestrup, and N. Odum
STAT3-mediated constitutive expression of SOCS-3 in cutaneous T-cell lymphoma
Blood,
February 15, 2001;
97(4):
1056 - 1062.
[Abstract]
[Full Text]
[PDF]
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B. Sporri, P. E. Kovanen, A. Sasaki, A. Yoshimura, and W. J. Leonard
JAB/SOCS1/SSI-1 is an interleukin-2-induced inhibitor of IL-2 signaling
Blood,
January 1, 2001;
97(1):
221 - 226.
[Abstract]
[Full Text]
[PDF]
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P. L. Bergad, S. J. Schwarzenberg, J. T. Humbert, M. Morrison, S. Amarasinghe, H. C. Towle, and S. A. Berry
Inhibition of growth hormone action in models of inflammation
Am J Physiol Cell Physiol,
December 1, 2000;
279(6):
C1906 - C1917.
[Abstract]
[Full Text]
[PDF]
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F. Gesbert and J. D. Griffin
Bcr/Abl activates transcription of the Bcl-X gene through STAT5
Blood,
September 15, 2000;
96(6):
2269 - 2276.
[Abstract]
[Full Text]
[PDF]
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S. Li, S. Chen, X. Xu, A. Sundstedt, K. M. Paulsson, P. Anderson, S. Karlsson, H.-O. Sjogren, and P. Wang
Cytokine-Induced Src Homology 2 Protein (Cis) Promotes T Cell Receptor-Mediated Proliferation and Prolongs Survival of Activated T Cells
J. Exp. Med.,
March 20, 2000;
191(6):
985 - 994.
[Abstract]
[Full Text]
[PDF]
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V. Lacronique, A. Boureux, R. Monni, S. Dumon, M. Mauchauffe, P. Mayeux, F. Gouilleux, R. Berger, S. Gisselbrecht, J. Ghysdael, et al.
Transforming properties of chimeric TEL-JAK proteins in Ba/F3 cells
Blood,
March 15, 2000;
95(6):
2076 - 2083.
[Abstract]
[Full Text]
[PDF]
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C. Sillaber, F. Gesbert, D. A. Frank, M. Sattler, and J. D. Griffin
STAT5 activation contributes to growth and viability in Bcr/Abl-transformed cells
Blood,
March 15, 2000;
95(6):
2118 - 2125.
[Abstract]
[Full Text]
[PDF]
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Y. R. Boisclair, J. Wang, J. Shi, K. R. Hurst, and G. T. Ooi
Role of the Suppressor of Cytokine Signaling-3 in Mediating the Inhibitory Effects of Interleukin-1beta on the Growth Hormone-dependent Transcription of the Acid-labile Subunit Gene in Liver Cells
J. Biol. Chem.,
February 11, 2000;
275(6):
3841 - 3847.
[Abstract]
[Full Text]
[PDF]
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D. Krebs and D. Hilton
SOCS: physiological suppressors of cytokine signaling
J. Cell Sci.,
January 8, 2000;
113(16):
2813 - 2819.
[Abstract]
[PDF]
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C.-L. Yu, Y.-J. Jin, and S. J. Burakoff
Cytosolic Tyrosine Dephosphorylation of STAT5. POTENTIAL ROLE OF SHP-2 IN STAT5 REGULATION
J. Biol. Chem.,
January 7, 2000;
275(1):
599 - 604.
[Abstract]
[Full Text]
[PDF]
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A. C. Ward, I. Touw, and A. Yoshimura
The Jak-Stat pathway in normal and perturbed hematopoiesis
Blood,
January 1, 2000;
95(1):
19 - 29.
[Full Text]
[PDF]
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P. A. Ram and D. J. Waxman
SOCS/CIS Protein Inhibition of Growth Hormone-stimulated STAT5 Signaling by Multiple Mechanisms
J. Biol. Chem.,
December 10, 1999;
274(50):
35553 - 35561.
[Abstract]
[Full Text]
[PDF]
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D. E. Isaksen, H. Baumann, P. A. Trobridge, A. G. Farr, S. D. Levin, and S. F. Ziegler
Requirement for Stat5 in Thymic Stromal Lymphopoietin-Mediated Signal Transduction
J. Immunol.,
December 1, 1999;
163(11):
5971 - 5977.
[Abstract]
[Full Text]
[PDF]
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S.-F. Lee, H.-M. Huang, J.-R. Chao, S. Lin, H.-F. Yang-Yen, and J. J.-Y. Yen
Cytokine Receptor Common beta Chain as a Potential Activator of Cytokine Withdrawal-Induced Apoptosis
Mol. Cell. Biol.,
November 1, 1999;
19(11):
7399 - 7409.
[Abstract]
[Full Text]
[PDF]
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J. A. Hansen, K. Lindberg, D. J. Hilton, J. H. Nielsen, and N. Billestrup
Mechanism of Inhibition of Growth Hormone Receptor Signaling by Suppressor of Cytokine Signaling Proteins
Mol. Endocrinol.,
November 1, 1999;
13(11):
1832 - 1843.
[Abstract]
[Full Text]
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I.-H. Lee, W. P. Li, K. B. Hisert, and L. B. Ivashkiv
Inhibition of Interleukin 2 Signaling and Signal Transducer and Activator of Transcription (Stat)5 Activation during T Cell Receptor-Mediated Feedback Inhibition of T Cell Expansion
J. Exp. Med.,
November 1, 1999;
190(9):
1263 - 1274.
[Abstract]
[Full Text]
[PDF]
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C. Bjorbak, K. El-Haschimi, J. D. Frantz, and J. S. Flier
The Role of SOCS-3 in Leptin Signaling and Leptin Resistance
J. Biol. Chem.,
October 15, 1999;
274(42):
30059 - 30065.
[Abstract]
[Full Text]
[PDF]
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M. J. Aman, T.-S. Migone, A. Sasaki, D. P. Ascherman, M.-h. Zhu, E. Soldaini, K. Imada, A. Miyajima, A. Yoshimura, and W. J. Leonard
CIS Associates with the Interleukin-2 Receptor beta Chain and Inhibits Interleukin-2-dependent Signaling
J. Biol. Chem.,
October 15, 1999;
274(42):
30266 - 30272.
[Abstract]
[Full Text]
[PDF]
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M. L. Janas, P. Hodgkin, M. Hibbs, and D. Tarlinton
Genetic Evidence for Lyn as a Negative Regulator of IL-4 Signaling
J. Immunol.,
October 15, 1999;
163(8):
4192 - 4198.
[Abstract]
[Full Text]
[PDF]
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M. A. Cassatella, S. Gasperini, C. Bovolenta, F. Calzetti, M. Vollebregt, P. Scapini, M. Marchi, R. Suzuki, A. Suzuki, and A. Yoshimura
Interleukin-10 (IL-10) Selectively Enhances CIS3/SOCS3 mRNA Expression in Human Neutrophils: Evidence for an IL-10-Induced Pathway That Is Independent of STAT Protein Activation
Blood,
October 15, 1999;
94(8):
2880 - 2889.
[Abstract]
[Full Text]
[PDF]
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S. A. Qureshi, R. M. Kim, Z. Konteatis, D. E. Biazzo, H. Motamedi, R. Rodrigues, J. A. Boice, J. R. Calaycay, M. A. Bednarek, P. Griffin, et al.
Mimicry of erythropoietin by a nonpeptide molecule
PNAS,
October 12, 1999;
96(21):
12156 - 12161.
[Abstract]
[Full Text]
[PDF]
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S. S. Watowich, X. Xie, U. Klingmuller, J. Kere, M. Lindlof, S. Berglund, and A. de la Chapelle
Erythropoietin Receptor Mutations Associated With Familial Erythrocytosis Cause Hypersensitivity to Erythropoietin in the Heterozygous State
Blood,
October 1, 1999;
94(7):
2530 - 2532.
[Abstract]
[Full Text]
[PDF]
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A. Matsumoto, Y. Seki, M. Kubo, S. Ohtsuka, A. Suzuki, I. Hayashi, K. Tsuji, T. Nakahata, M. Okabe, S. Yamada, et al.
Suppression of STAT5 Functions in Liver, Mammary Glands, and T Cells in Cytokine-Inducible SH2-Containing Protein 1 Transgenic Mice
Mol. Cell. Biol.,
September 1, 1999;
19(9):
6396 - 6407.
[Abstract]
[Full Text]
[PDF]
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A. Pezet, H. Favre, P. A. Kelly, and M. Edery
Inhibition and Restoration of Prolactin Signal Transduction by Suppressors of Cytokine Signaling
J. Biol. Chem.,
August 27, 1999;
274(35):
24497 - 24502.
[Abstract]
[Full Text]
[PDF]
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P. Tollet-Egnell, A. Flores-Morales, A. Stavréus-Evers, L. Sahlin, and G. Norstedt
Growth Hormone Regulation of SOCS-2, SOCS-3, and CIS Messenger Ribonucleic Acid Expression in the Rat
Endocrinology,
August 1, 1999;
140(8):
3693 - 3704.
[Abstract]
[Full Text]
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N. Tanaka, K. Kaneko, H. Asao, H. Kasai, Y. Endo, T. Fujita, T. Takeshita, and K. Sugamura
Possible Involvement of a Novel STAM-associated Molecule "AMSH" in Intracellular Signal Transduction Mediated by Cytokines
J. Biol. Chem.,
July 2, 1999;
274(27):
19129 - 19135.
[Abstract]
[Full Text]
[PDF]
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S. J. Cohney, D. Sanden, N. A. Cacalano, A. Yoshimura, A. Mui, T. S. Migone, and J. A. Johnston
SOCS-3 Is Tyrosine Phosphorylated in Response to Interleukin-2 and Suppresses STAT5 Phosphorylation and Lymphocyte Proliferation
Mol. Cell. Biol.,
July 1, 1999;
19(7):
4980 - 4988.
[Abstract]
[Full Text]
[PDF]
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S. L. Gaffen, S. Y. Lai, G. D. Longmore, K. D. Liu, and M. A. Goldsmith
Genetic Evidence for an Additional Factor Required for Erythropoietin-Induced Signal Transduction
Blood,
July 1, 1999;
94(1):
74 - 86.
[Abstract]
[Full Text]
[PDF]
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C. J. Auernhammer, C. Bousquet, and S. Melmed
Autoregulation of pituitary corticotroph SOCS-3 expression: Characterization of the murine SOCS-3 promoter
PNAS,
June 8, 1999;
96(12):
6964 - 6969.
[Abstract]
[Full Text]
[PDF]
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C. Bjørbæk, J. K. Elmquist, K. El-Haschimi, J. Kelly, R. S. Ahima, S. Hileman, and J. S. Flier
Activation of SOCS-3 Messenger Ribonucleic Acid in the Hypothalamus by Ciliary Neurotrophic Factor
Endocrinology,
May 1, 1999;
140(5):
2035 - 2043.
[Abstract]
[Full Text]
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M. Nieborowska-Skorska, M. A. Wasik, A. Slupianek, P. Salomoni, T. Kitamura, B. Calabretta, and T. Skorski
Signal Transducer and Activator of Transcription (STAT)5 Activation by BCR/ABL Is Dependent on Intact Src Homology (SH)3 and SH2 Domains of BCR/ABL and Is Required for Leukemogenesis
J. Exp. Med.,
April 19, 1999;
189(8):
1229 - 1242.
[Abstract]
[Full Text]
[PDF]
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R. Y. Liu, C. Fan, R. Garcia, R. Jove, and K. S. Zuckerman
Constitutive Activation of the JAK2/STAT5 Signal Transduction Pathway Correlates With Growth Factor Independence of Megakaryocytic Leukemic Cell Lines
Blood,
April 1, 1999;
93(7):
2369 - 2379.
[Abstract]
[Full Text]
[PDF]
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C.G. Begley and N.A. Nicola
Resolving Conflicting Signals: Cross Inhibition of Cytokine Signaling Pathways
Blood,
March 1, 1999;
93(5):
1443 - 1447.
[Full Text]
[PDF]
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S. Ito, P. Ansari, M. Sakatsume, H. Dickensheets, N. Vazquez, R. P. Donnelly, A. C. Larner, and D. S. Finbloom
Interleukin-10 Inhibits Expression of Both Interferon alpha - and Interferon gamma - Induced Genes by Suppressing Tyrosine Phosphorylation of STAT1
Blood,
March 1, 1999;
93(5):
1456 - 1463.
[Abstract]
[Full Text]
[PDF]
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S. S. Watowich, K. D. Liu, X. Xie, S. Y. Lai, A. Mikami, G. D. Longmore, and M. A. Goldsmith
Oligomerization and Scaffolding Functions of the Erythropoietin Receptor Cytoplasmic Tail
J. Biol. Chem.,
February 26, 1999;
274(9):
5415 - 5421.
[Abstract]
[Full Text]
[PDF]
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C. A. Gebert, S.-H. Park, and D. J. Waxman
Down-Regulation of Liver JAK2-STAT5b Signaling by the Female Plasma Pattern of Continuous Growth Hormone Stimulation
Mol. Endocrinol.,
February 1, 1999;
13(2):
213 - 227.
[Abstract]
[Full Text]
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A. Castro, T. K. Sengupta, D. C. Ruiz, E. Yang, and L. B. Ivashkiv
IL-4 Selectively Inhibits IL-2-Triggered Stat5 Activation, But Not Proliferation, in Human T Cells
J. Immunol.,
February 1, 1999;
162(3):
1261 - 1269.
[Abstract]
[Full Text]
[PDF]
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C. A. Gebert, S.-H. Park, and D. J. Waxman
Termination of Growth Hormone Pulse-Induced STAT5b Signaling
Mol. Endocrinol.,
January 1, 1999;
13(1):
38 - 56.
[Abstract]
[Full Text]
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