Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages

Naohiko Tanaka; Yoshihiko Hoshino; Jeffrey Gold; Satomi Hoshino; Frank Martiniuk; Takeshi Kurata; Richard Pine; David Levy; William N. Rom; Michael Weiden

doi:10.1165/rcmb.2005-0140OC

Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages

Naohiko Tanaka, Yoshihiko Hoshino, Jeffrey Gold, Satomi Hoshino, Frank Martiniuk, Takeshi Kurata, Richard Pine, David Levy, William N. Rom, Michael Weiden

Pulmonary & Critical Care Medicine

Research output: Contribution to journal › Article › peer-review

36 Scopus citations

Abstract

Pulmonary tuberculosis (TB) has been characterized by inflammation with increased pro- or anti-inflammatory cytokines produced by macrophages. We have reported that IFN produces inhibitory C/EBPβ and represses transcription of the HIV-1 LTR in macrophages. STAT-1 and type 1 IFN receptor knockout mice have macrophages that are defective in IFN signaling, yet LPS stimulation induces inhibitory C/EBPβ, demonstrating that other cytokines can induce this represser. LPS or Mycobacterium tuberculosis-derived lipoarabinomannan induce the anti-inflammatory cytokine interleukin (IL)-10, which represses the HIV-1 LTR in differentiated THP-1 macrophages by inducing inhibitory C/EBPβ. In contrast, in undifferentiated THP-1 monocytes, IL-10 did not inhibit HIV-1 replication or induce C/EBPβ. IL-10 signal transduction uses STAT-3, and macrophages from STAT-3^-/- mice fail to produce inhibitory C/EBPβ after LPS or IL-10 stimulation. Transfection of STAT-3 into THP-1 cells enhances C/EBPβ promoter activity. THP-1 differentiation also increases STAT-3 protein, but not STAT-3 gene transcription, and induces a translational regulator, CUG-binding protein, that was essential for production of C/EBPβ. Differentiation induced post-transcriptional regulation is required to produce inhibitory C/EBPβ in response to IL-10. Only macrophages are able to repress HIV-1 LTR promoter activity and inhibit viral replication in response to IL-10 or type 1 IFN.

Original language	English (US)
Pages (from-to)	406-411
Number of pages	6
Journal	American journal of respiratory cell and molecular biology
Volume	33
Issue number	4
DOIs	https://doi.org/10.1165/rcmb.2005-0140OC
State	Published - Oct 2005

Keywords

Infection
Innate immunity
Repression
Transcription factors

ASJC Scopus subject areas

Molecular Biology
Pulmonary and Respiratory Medicine
Clinical Biochemistry
Cell Biology

Access to Document

10.1165/rcmb.2005-0140OC

Fingerprint Dive into the research topics of 'Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages'. Together they form a unique fingerprint.

Cite this

Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages. / Tanaka, Naohiko; Hoshino, Yoshihiko; Gold, Jeffrey; Hoshino, Satomi; Martiniuk, Frank; Kurata, Takeshi; Pine, Richard; Levy, David; Rom, William N.; Weiden, Michael.

In: American journal of respiratory cell and molecular biology, Vol. 33, No. 4, 10.2005, p. 406-411.

Research output: Contribution to journal › Article › peer-review

Tanaka, Naohiko ; Hoshino, Yoshihiko ; Gold, Jeffrey ; Hoshino, Satomi ; Martiniuk, Frank ; Kurata, Takeshi ; Pine, Richard ; Levy, David ; Rom, William N. ; Weiden, Michael. / Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages. In: American journal of respiratory cell and molecular biology. 2005 ; Vol. 33, No. 4. pp. 406-411.

@article{96cd6f4c61ff4515a7b91fb7db4d3401,

title = "Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages",

abstract = "Pulmonary tuberculosis (TB) has been characterized by inflammation with increased pro- or anti-inflammatory cytokines produced by macrophages. We have reported that IFN produces inhibitory C/EBPβ and represses transcription of the HIV-1 LTR in macrophages. STAT-1 and type 1 IFN receptor knockout mice have macrophages that are defective in IFN signaling, yet LPS stimulation induces inhibitory C/EBPβ, demonstrating that other cytokines can induce this represser. LPS or Mycobacterium tuberculosis-derived lipoarabinomannan induce the anti-inflammatory cytokine interleukin (IL)-10, which represses the HIV-1 LTR in differentiated THP-1 macrophages by inducing inhibitory C/EBPβ. In contrast, in undifferentiated THP-1 monocytes, IL-10 did not inhibit HIV-1 replication or induce C/EBPβ. IL-10 signal transduction uses STAT-3, and macrophages from STAT-3-/- mice fail to produce inhibitory C/EBPβ after LPS or IL-10 stimulation. Transfection of STAT-3 into THP-1 cells enhances C/EBPβ promoter activity. THP-1 differentiation also increases STAT-3 protein, but not STAT-3 gene transcription, and induces a translational regulator, CUG-binding protein, that was essential for production of C/EBPβ. Differentiation induced post-transcriptional regulation is required to produce inhibitory C/EBPβ in response to IL-10. Only macrophages are able to repress HIV-1 LTR promoter activity and inhibit viral replication in response to IL-10 or type 1 IFN.",

keywords = "Infection, Innate immunity, Repression, Transcription factors",

author = "Naohiko Tanaka and Yoshihiko Hoshino and Jeffrey Gold and Satomi Hoshino and Frank Martiniuk and Takeshi Kurata and Richard Pine and David Levy and Rom, {William N.} and Michael Weiden",

year = "2005",

month = oct,

doi = "10.1165/rcmb.2005-0140OC",

language = "English (US)",

volume = "33",

pages = "406--411",

journal = "American Journal of Respiratory Cell and Molecular Biology",

issn = "1044-1549",

publisher = "American Thoracic Society",

number = "4",

}

TY - JOUR

T1 - Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages

AU - Tanaka, Naohiko

AU - Hoshino, Yoshihiko

AU - Gold, Jeffrey

AU - Hoshino, Satomi

AU - Martiniuk, Frank

AU - Kurata, Takeshi

AU - Pine, Richard

AU - Levy, David

AU - Rom, William N.

AU - Weiden, Michael

PY - 2005/10

Y1 - 2005/10

N2 - Pulmonary tuberculosis (TB) has been characterized by inflammation with increased pro- or anti-inflammatory cytokines produced by macrophages. We have reported that IFN produces inhibitory C/EBPβ and represses transcription of the HIV-1 LTR in macrophages. STAT-1 and type 1 IFN receptor knockout mice have macrophages that are defective in IFN signaling, yet LPS stimulation induces inhibitory C/EBPβ, demonstrating that other cytokines can induce this represser. LPS or Mycobacterium tuberculosis-derived lipoarabinomannan induce the anti-inflammatory cytokine interleukin (IL)-10, which represses the HIV-1 LTR in differentiated THP-1 macrophages by inducing inhibitory C/EBPβ. In contrast, in undifferentiated THP-1 monocytes, IL-10 did not inhibit HIV-1 replication or induce C/EBPβ. IL-10 signal transduction uses STAT-3, and macrophages from STAT-3-/- mice fail to produce inhibitory C/EBPβ after LPS or IL-10 stimulation. Transfection of STAT-3 into THP-1 cells enhances C/EBPβ promoter activity. THP-1 differentiation also increases STAT-3 protein, but not STAT-3 gene transcription, and induces a translational regulator, CUG-binding protein, that was essential for production of C/EBPβ. Differentiation induced post-transcriptional regulation is required to produce inhibitory C/EBPβ in response to IL-10. Only macrophages are able to repress HIV-1 LTR promoter activity and inhibit viral replication in response to IL-10 or type 1 IFN.

AB - Pulmonary tuberculosis (TB) has been characterized by inflammation with increased pro- or anti-inflammatory cytokines produced by macrophages. We have reported that IFN produces inhibitory C/EBPβ and represses transcription of the HIV-1 LTR in macrophages. STAT-1 and type 1 IFN receptor knockout mice have macrophages that are defective in IFN signaling, yet LPS stimulation induces inhibitory C/EBPβ, demonstrating that other cytokines can induce this represser. LPS or Mycobacterium tuberculosis-derived lipoarabinomannan induce the anti-inflammatory cytokine interleukin (IL)-10, which represses the HIV-1 LTR in differentiated THP-1 macrophages by inducing inhibitory C/EBPβ. In contrast, in undifferentiated THP-1 monocytes, IL-10 did not inhibit HIV-1 replication or induce C/EBPβ. IL-10 signal transduction uses STAT-3, and macrophages from STAT-3-/- mice fail to produce inhibitory C/EBPβ after LPS or IL-10 stimulation. Transfection of STAT-3 into THP-1 cells enhances C/EBPβ promoter activity. THP-1 differentiation also increases STAT-3 protein, but not STAT-3 gene transcription, and induces a translational regulator, CUG-binding protein, that was essential for production of C/EBPβ. Differentiation induced post-transcriptional regulation is required to produce inhibitory C/EBPβ in response to IL-10. Only macrophages are able to repress HIV-1 LTR promoter activity and inhibit viral replication in response to IL-10 or type 1 IFN.

KW - Infection

KW - Innate immunity

KW - Repression

KW - Transcription factors

UR - http://www.scopus.com/inward/record.url?scp=26244441377&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=26244441377&partnerID=8YFLogxK

U2 - 10.1165/rcmb.2005-0140OC

DO - 10.1165/rcmb.2005-0140OC

M3 - Article

C2 - 16014896

AN - SCOPUS:26244441377

VL - 33

SP - 406

EP - 411

JO - American Journal of Respiratory Cell and Molecular Biology

JF - American Journal of Respiratory Cell and Molecular Biology

SN - 1044-1549

IS - 4

ER -