Home LiteratureArticle Details
PMID: 8971006 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Transcriptional activation of the interleukin-8 gene by respiratory syncytial virus infection in alveolar epithelial cells: nuclear translocation of the RelA transcription factor as a mechanism producing airway mucosal inflammation.

Journal of virology ·Vol. 70 ·No. 12 ·1996-12-00 ·Pages 8773-81

Garofalo R, Sabry M, Jamaluddin M, Yu RK, Casola A, Ogra PL, Brasier AR

Abstract

The most common cause of epidemic pediatric respiratory disease, respiratory syncytial virus (RSV), stimulates interleukin-8 (IL-8) synthesis upon infecting airway epithelium, an event necessary for the development of mucosal inflammation. We investigated the mechanism for enhanced IL-8 production in human A549 type II pulmonary epithelial cells. Infection with sucrose-purified RSV (pRSV) produced a time-dependent increase in the transcriptional initiation rate of the IL-8 gene. Transient transfection of the human IL-8 promoter mutated in the binding site for nuclear factor-kappaB (NF-kappaB) demonstrated that this sequence was essential for pRSV-activated transcription. Gel mobility shift assays demonstrated pRSV induction of sequence-specific binding complexes; these complexes were supershifted only by antibodies directed to the potent NF-kappaB transactivating subunit RelA. Both Western immunoblot and indirect immunofluorescence assays showed that cytoplasmic RelA in uninfected cells became localized to the nucleus after pRSV infection. RelA activation requires replicating RSV, because neither conditioned medium nor UV-inactivated pRSV was able to stimulate its translocation. We conclude that RelA undergoes changes in subcellular distribution in airway epithelial cells upon pRSV infection. The ability of replicating RSV to activate RelA translocation may play an important role in activating IL-8 and other inflammatory gene products necessary for airway mucosal inflammation seen in RSV disease.

MeSH Terms
Cell Nucleus/metabolism DNA-Binding Proteins/genetics,metabolism Epithelial Cells Epithelium/metabolism Humans Inflammation Interleukin-8/genetics,metabolism Lung/cytology,metabolism NF-kappa B/genetics,metabolism Respiratory Syncytial Viruses/metabolism Transcription Factor RelA Transcription Factors/genetics,metabolism Transcriptional Activation Tumor Cells, Cultured
Chemicals
DNA-Binding Proteins Interleukin-8 NF-kappa B Transcription Factor RelA Transcription Factors
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Garofalo R
Department of Medicine, University of Texas Medical Branch, Galveston 77555-1060, USA.
Sabry M
Jamaluddin M
Yu R K
Casola A
Ogra P L
Brasier A R
References (54)
54 references, click to expand
  1. Respiratory syncytial virus infection in children with bronchopulmonary dysplasia.
    Pediatrics. 1988 Aug;82(2):199-203 PMID: 3399292
  2. Calcium requirement for syncytium formation in HEp-2 cells by respiratory syncytial virus.
    J Clin Microbiol. 1988 Jan;26(1):139-41 PMID: 3343306
  3. Double-stranded RNA activates binding of NF-kappa B to an inducible element in the human beta-interferon promoter.
    EMBO J. 1989 Apr;8(4):1129-38 PMID: 2663471
  4. Childhood asthma following hospitalization with acute viral bronchiolitis in infancy.
    Pediatr Pulmonol. 1989;7(3):153-8 PMID: 2797929
  5. An inducible 50-kilodalton NF kappa B-like protein and a constitutive protein both bind the acute-phase response element of the angiotensinogen gene.
    Mol Cell Biol. 1990 Mar;10(3):1023-32 PMID: 2106065
  6. Optimized use of the firefly luciferase assay as a reporter gene in mammalian cell lines.
    Biotechniques. 1989 Nov-Dec;7(10):1116-22 PMID: 2698191
  7. Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B.
    Mol Cell Biol. 1990 Apr;10(4):1498-506 PMID: 2181276
  8. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction.
    Biotechniques. 1990 May;8(5):528-35 PMID: 2357375
  9. A family of constitutive C/EBP-like DNA binding proteins attenuate the IL-1 alpha induced, NF kappa B mediated trans-activation of the angiotensinogen gene acute-phase response element.
    EMBO J. 1990 Dec;9(12):3933-44 PMID: 2174352
  10. Interleukin-8 gene expression by a pulmonary epithelial cell line. A model for cytokine networks in the lung.
    J Clin Invest. 1990 Dec;86(6):1945-53 PMID: 2254454
  11. Processing of the precursor of NF-kappa B by the HIV-1 protease during acute infection.
    Nature. 1991 Apr 18;350(6319):625-6 PMID: 2017258
  12. The inducible transcription activator NF-kappa B: regulation by distinct protein subunits.
    Biochim Biophys Acta. 1991 Apr 16;1072(1):63-80 PMID: 2018779
  13. Shape changes, exocytosis, and cytosolic free calcium changes in stimulated human eosinophils.
    J Clin Invest. 1991 Jun;87(6):2012-7 PMID: 2040692
  14. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1.
    EMBO J. 1991 Aug;10(8):2247-58 PMID: 2065663
  15. Interleukin-8 gene expression in human bronchial epithelial cells.
    J Biol Chem. 1991 Oct 15;266(29):19611-7 PMID: 1918068
  16. Eosinophil degranulation in the respiratory tract during naturally acquired respiratory syncytial virus infection.
    J Pediatr. 1992 Jan;120(1):28-32 PMID: 1731020
  17. Influenza virus A infection induces interleukin-8 gene expression in human airway epithelial cells.
    FEBS Lett. 1992 Sep 14;309(3):327-9 PMID: 1516705
  18. I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention.
    Genes Dev. 1992 Oct;6(10):1899-913 PMID: 1340770
  19. Selection of optimal kappa B/Rel DNA-binding motifs: interaction of both subunits of NF-kappa B with DNA is required for transcriptional activation.
    Mol Cell Biol. 1992 Oct;12(10):4412-21 PMID: 1406630
  20. Tumor necrosis factor alpha and interferon gamma synergistically induce interleukin 8 production in a human gastric cancer cell line through acting concurrently on AP-1 and NF-kB-like binding sites of the interleukin 8 gene.
    J Biol Chem. 1992 Nov 5;267(31):22506-11 PMID: 1331059
  21. Chronic human immunodeficiency virus type 1 infection stimulates distinct NF-kappa B/rel DNA binding activities in myelomonoblastic cells.
    J Virol. 1993 Sep;67(9):5235-46 PMID: 8394446
  22. Distinct mechanisms for regulation of the interleukin-8 gene involve synergism and cooperativity between C/EBP and NF-kappa B.
    Mol Cell Biol. 1993 Nov;13(11):7191-8 PMID: 8413306
  23. Corticosteroids differentially regulate secretion of IL-6, IL-8, and G-CSF by a human bronchial epithelial cell line.
    Am J Physiol. 1993 Oct;265(4 Pt 1):L360-8 PMID: 7694480
  24. Respiratory syncytial virus-induced cytokine production by a human bronchial epithelial cell line.
    Am J Physiol. 1993 Nov;265(5 Pt 1):L472-8 PMID: 8238534
  25. Novel Pseudomonas product stimulates interleukin-8 production in airway epithelial cells in vitro.
    J Clin Invest. 1994 Jan;93(1):26-32 PMID: 8282796
  26. Requirement for nuclear factor (NF)-kappa B p65 and NF-interleukin-6 binding elements in the tumor necrosis factor response region of the granulocyte colony-stimulating factor promoter.
    Blood. 1994 May 1;83(9):2469-79 PMID: 7513199
  27. Tumor necrosis factor and lymphotoxin. Qualitative and quantitative differences in the mediation of early and late cellular response.
    J Biol Chem. 1994 May 20;269(20):14575-83 PMID: 8182064
  28. Viral induction of the human beta interferon promoter: modulation of transcription by NF-kappa B/rel proteins and interferon regulatory factors.
    J Virol. 1994 Aug;68(8):4707-15 PMID: 8035474
  29. Interleukin-8, interleukin-6, and soluble tumour necrosis factor receptor type I release from a human pulmonary epithelial cell line (A549) exposed to respiratory syncytial virus.
    Immunology. 1994 May;82(1):126-33 PMID: 7519169
  30. Analysis of cells obtained by bronchial lavage of infants with respiratory syncytial virus infection.
    Arch Dis Child. 1994 Nov;71(5):428-32 PMID: 7826113
  31. Domain organization of I kappa B alpha and sites of interaction with NF-kappa B p65.
    Mol Cell Biol. 1995 Apr;15(4):2166-72 PMID: 7891711
  32. Interleukin-1 alpha mediates the enhanced expression of intercellular adhesion molecule-1 in pulmonary epithelial cells infected with respiratory syncytial virus.
    Am J Respir Cell Mol Biol. 1995 Nov;13(5):602-9 PMID: 7576697
  33. Respiratory syncytial virus increases IL-8 gene expression and protein release in A549 cells.
    Am J Physiol. 1995 Dec;269(6 Pt 1):L865-72 PMID: 8572249
  34. Rhinovirus stimulation of interleukin-6 in vivo and in vitro. Evidence for nuclear factor kappa B-dependent transcriptional activation.
    J Clin Invest. 1996 Jan 15;97(2):421-30 PMID: 8567963
  35. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity.
    Cell. 1996 Mar 22;84(6):853-62 PMID: 8601309
  36. Tumor necrosis factor activates angiotensinogen gene expression by the Rel A transactivator.
    Hypertension. 1996 Apr;27(4):1009-17 PMID: 8613256
  37. Inducible translational regulation of the NF-IL6 transcription factor by respiratory syncytial virus infection in pulmonary epithelial cells.
    J Virol. 1996 Mar;70(3):1554-63 PMID: 8627674
  38. Induction of interleukin (IL)-8 gene expression by respiratory syncytial virus involves activation of nuclear factor (NF)-kappa B and NF-IL-6.
    J Infect Dis. 1996 Aug;174(2):262-7 PMID: 8699053
  39. Angiotensinogen gene activation by angiotensin II is mediated by the rel A (nuclear factor-kappaB p65) transcription factor: one mechanism for the renin angiotensin system positive feedback loop in hepatocytes.
    Mol Endocrinol. 1996 Mar;10(3):252-64 PMID: 8833654
  40. Growth and serological characteristics of respiratory syncytial virus.
    J Infect Dis. 1962 Jan-Feb;110:8-16 PMID: 13867292
  41. A plaque assay for respiratory syncytial virus.
    Proc Soc Exp Biol Med. 1963 Mar;112:583-9 PMID: 14033060
  42. NF-kappa B: a lesson in family values.
    Cell. 1995 Feb 24;80(4):529-32 PMID: 7867060
  43. Nasal cytokine production in viral acute upper respiratory infection of childhood.
    J Infect Dis. 1995 Mar;171(3):584-92 PMID: 7876605
  44. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation.
    Science. 1995 Mar 10;267(5203):1485-8 PMID: 7878466
  45. Structure, regulation and function of NF-kappa B.
    Annu Rev Cell Biol. 1994;10:405-55 PMID: 7888182
  46. Pathological changes in virus infections of the lower respiratory tract in children.
    J Clin Pathol. 1970 Feb;23(1):7-18 PMID: 4909103
  47. Respiratory syncytial virus. I. Concentration and purification of the infectious virus.
    Acta Med Okayama. 1978 Aug;32(4):265-72 PMID: 153087
  48. The development of respiratory syncytial virus-specific IgE and the release of histamine in nasopharyngeal secretions after infection.
    N Engl J Med. 1981 Oct 8;305(15):841-6 PMID: 6168908
  49. Infectivity of respiratory syncytial virus by various routes of inoculation.
    Infect Immun. 1981 Sep;33(3):779-83 PMID: 7287181
  50. Respiratory syncytial viral infection in infants with congenital heart disease.
    N Engl J Med. 1982 Aug 12;307(7):397-400 PMID: 7088112
  51. Long-term prospective study in children after respiratory syncytial virus infection.
    J Pediatr. 1984 Sep;105(3):358-64 PMID: 6470859
  52. Risk of primary infection and reinfection with respiratory syncytial virus.
    Am J Dis Child. 1986 Jun;140(6):543-6 PMID: 3706232
  53. Cyclosporin A inhibits rDNA transcription in lymphosarcoma P1798 cells.
    J Biol Chem. 1987 Nov 25;262(33):16150-6 PMID: 3680246
  54. Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B.
    Proc Natl Acad Sci U S A. 1989 Apr;86(7):2336-40 PMID: 2494664
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-12-00
Pages
8773-81
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190974
Subset
IM
Grants
NIAID NIH HHS · AI/HL 15939-14A1 · United States
NICHD NIH HHS · R30HD 27841 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com