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PMID: 10225979 Published · ppublish English Clinical Trial Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Constitutive activation of an epithelial signal transducer and activator of transcription (STAT) pathway in asthma.

The Journal of clinical investigation ·Vol. 103 ·No. 9 ·1999-05-00 ·Pages 1353-61

Sampath D, Castro M, Look DC, Holtzman MJ

Abstract

Cytokine effects on immunity and inflammation often depend on the transcription factors termed signal transducers and activators of transcription (STATs), so STAT signaling pathways are candidates for influencing inflammatory disease. We reasoned that selective IFN responsiveness of the first STAT family member (Stat1) and Stat1-dependent immune-response genes such as intercellular adhesion molecule-1 (ICAM-1), IFN regulatory factor-1 (IRF-1), and Stat1 itself in airway epithelial cells provides a basis for detecting cytokine signaling abnormalities in inflammatory airway disease. On the basis of nuclear localization and phosphorylation, we found that epithelial Stat1 (but not other control transcription factors) was invariably activated in asthmatic compared with normal control or chronic bronchitis subjects. Furthermore, epithelial levels of activated Stat1 correlated with levels of expression for epithelial ICAM-1, IRF-1, and Stat1, and in turn, ICAM-1 levels correlated with T-cell accumulation in tissue. However, only low levels of IFN-gamma or IFN-gamma-producing cells were detected in airway tissue in all subjects. The results therefore provide initial evidence linking abnormal behavior of STAT pathways for cytokine signaling to the development of an inflammatory disease. In that context, the results also change the current scheme for asthma pathogenesis to one that must include a localized gain in transcriptional signal ordinarily used for a T helper 1-type cytokine (IFN-gamma) in combination with allergy-driven overproduction of T helper 2-type cytokines.

MeSH Terms
Asthma/immunology,metabolism Base Sequence Bronchi/cytology,metabolism Case-Control Studies DNA Primers DNA-Binding Proteins/metabolism Epithelial Cells/metabolism Humans Interferon-gamma/metabolism STAT1 Transcription Factor Th1 Cells/immunology Trans-Activators/metabolism
Chemicals
DNA Primers DNA-Binding Proteins STAT1 Transcription Factor STAT1 protein, human Trans-Activators Interferon-gamma
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sampath D
Department of Medicine, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Castro M
Look D C
Holtzman M J
References (34)
34 references, click to expand
  1. The inverse association between tuberculin responses and atopic disorder.
    Science. 1997 Jan 3;275(5296):77-9 PMID: 8974396
  2. Enhancement of antiproliferative activity of gamma interferon by the specific inhibition of tyrosine dephosphorylation of Stat1.
    Mol Cell Biol. 1996 Sep;16(9):4932-41 PMID: 8756652
  3. Reduced production of IL-12 and IL-12-dependent IFN-gamma release in patients with allergic asthma.
    J Immunol. 1997 Jun 1;158(11):5560-5 PMID: 9164981
  4. Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet?
    Immunity. 1997 Jul;7(1):1-11 PMID: 9252115
  5. Interferon gamma and interleukin 4 stimulate prolonged expression of inducible nitric oxide synthase in human airway epithelium through synthesis of soluble mediators.
    J Clin Invest. 1997 Aug 15;100(4):829-38 PMID: 9259582
  6. STATs and gene regulation.
    Science. 1997 Sep 12;277(5332):1630-5 PMID: 9287210
  7. Targeted inhibition of interferon-gamma-dependent intercellular adhesion molecule-1 (ICAM-1) expression using dominant-negative Stat1.
    J Biol Chem. 1997 Nov 7;272(45):28582-9 PMID: 9353323
  8. The association of atopy with a gain-of-function mutation in the alpha subunit of the interleukin-4 receptor.
    N Engl J Med. 1997 Dec 11;337(24):1720-5 PMID: 9392697
  9. Control of epithelial immune-response genes and implications for airway immunity and inflammation.
    Proc Assoc Am Physicians. 1998 Jan-Feb;110(1):1-11 PMID: 9460078
  10. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway.
    J Exp Med. 1998 Mar 2;187(5):675-83 PMID: 9480977
  11. Patterns for RANTES secretion and intercellular adhesion molecule 1 expression mediate transepithelial T cell traffic based on analyses in vitro and in vivo.
    J Exp Med. 1998 Jun 15;187(12):1927-40 PMID: 9625753
  12. A viral mechanism for inhibition of the cellular phosphatase calcineurin.
    Science. 1998 Jul 24;281(5376):562-5 PMID: 9677199
  13. Direct suppression of Stat1 function during adenoviral infection.
    Immunity. 1998 Dec;9(6):871-80 PMID: 9881977
  14. Virus-inducible expression of a host chemokine gene relies on replication-linked mRNA stabilization.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5680-5 PMID: 10318944
  15. Enhanced 5-lipoxygenase activity in lung macrophages compared to monocytes from normal subjects.
    J Immunol. 1987 Mar 1;138(5):1546-50 PMID: 3027181
  16. Association of asthma with serum IgE levels and skin-test reactivity to allergens.
    N Engl J Med. 1989 Feb 2;320(5):271-7 PMID: 2911321
  17. Eosinophilic inflammation in asthma.
    N Engl J Med. 1990 Oct 11;323(15):1033-9 PMID: 2215562
  18. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma.
    N Engl J Med. 1992 Jan 30;326(5):298-304 PMID: 1530827
  19. Cytokines in symptomatic asthma airways.
    J Allergy Clin Immunol. 1992 May;89(5):958-67 PMID: 1374772
  20. Selective induction of intercellular adhesion molecule-1 by interferon-gamma in human airway epithelial cells.
    Am J Physiol. 1992 Jul;263(1 Pt 1):L79-87 PMID: 1353306
  21. c-fos proto-oncogene expression in bronchial biopsies of asthmatics.
    Am J Respir Cell Mol Biol. 1992 Aug;7(2):128-33 PMID: 1353973
  22. Induction of nitric oxide synthase in asthma.
    Lancet. 1993 Dec 18-25;342(8886-8887):1510-3 PMID: 7504773
  23. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages.
    Science. 1994 Mar 18;263(5153):1612-5 PMID: 7510419
  24. Selective interaction of a subset of interferon-gamma response element-binding proteins with the intercellular adhesion molecule-1 (ICAM-1) gene promoter controls the pattern of expression on epithelial cells.
    J Biol Chem. 1994 Mar 25;269(12):8952-8 PMID: 7907595
  25. Linkage analysis of IL4 and other chromosome 5q31.1 markers and total serum immunoglobulin E concentrations.
    Science. 1994 May 20;264(5162):1152-6 PMID: 8178175
  26. Association between atopy and variants of the beta subunit of the high-affinity immunoglobulin E receptor.
    Nat Genet. 1994 Jun;7(2):125-9 PMID: 7920628
  27. Selective differences in vascular endothelial- vs. airway epithelial-T cell adhesion mechanisms.
    Am J Physiol. 1994 Oct;267(4 Pt 1):L422-32 PMID: 7524353
  28. Phenotype of cells expressing mRNA for TH2-type (interleukin 4 and interleukin 5) and TH1-type (interleukin 2 and interferon gamma) cytokines in bronchoalveolar lavage and bronchial biopsies from atopic asthmatic and normal control subjects.
    Am J Respir Cell Mol Biol. 1995 May;12(5):477-87 PMID: 7742012
  29. A hierarchy for integrin expression and adhesiveness among T cell subsets that is linked to TCR gene usage and emphasizes V delta 1+ gamma delta T cell adherence and tissue retention.
    J Immunol. 1995 Aug 1;155(3):1117-31 PMID: 7636183
  30. Abnormal glucocorticoid receptor-activator protein 1 interaction in steroid-resistant asthma.
    J Exp Med. 1995 Dec 1;182(6):1951-8 PMID: 7500041
  31. Stat1 depends on transcriptional synergy with Sp1.
    J Biol Chem. 1995 Dec 22;270(51):30264-7 PMID: 8530443
  32. The one-two of T helper cells: does interferon-gamma knock out the Th2 hypothesis for asthma?
    Am J Respir Cell Mol Biol. 1996 Apr;14(4):316-8 PMID: 8600934
  33. Dominant negative stat3 mutant inhibits interleukin-6-induced Jak-STAT signal transduction.
    J Biol Chem. 1996 Mar 15;271(11):5961-4 PMID: 8626374
  34. Activation of Stat1 by mutant fibroblast growth-factor receptor in thanatophoric dysplasia type II dwarfism.
    Nature. 1997 Mar 20;386(6622):288-92 PMID: 9069288
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1999-05-00
Pages
1353-61
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC408358
Subset
IM
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