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PMID: 8627674 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Inducible translational regulation of the NF-IL6 transcription factor by respiratory syncytial virus infection in pulmonary epithelial cells.

Journal of virology ·Vol. 70 ·No. 3 ·1996-03-00 ·Pages 1554-63

Jamaluddin M, Garofalo R, Ogra PL, Brasier AR

Abstract

Respiratory syncytial virus (RSV), the most common etiologic agent of epidemic pediatric respiratory disease, infects and replicates in the human airway epithelium, resulting in the induction of cellular gene products essential for immune and inflammatory responses. We describe the effect of RSV infection on nuclear factor-IL6 (NF-IL6) expression, a human basic domain-leucine zipper-containing transcription factor that alone in combination with other inducible transcription factors regulates the expression of cytokine and adhesion molecule genes. RSV-infected human type II pulmonary alveolar epithelial cells (A549) synthesize a single 45.7-kDa isoform of NF-IL6 rapidly and in a time-dependent manner. NF-IL6 is first detectable after 3 h of infection and continues to accumulate until 48 h (until the cells lose viability). NF-IL6 production could not be induced by UV-inactivated virus, demonstrating the requirement of viral replication for NF-IL6 synthesis. Immunoprecipitation after [35S]methionine metabolic labeling was done to investigate the mechanism for NF-IL6 production. There was robust NF-IL6 protein synthesis within RSV-infected (24 h) cells. Protein synthesis occurred without detectable changes in the abundance or size of the single 1.8-kb NF-IL6 mRNA. RNase protection assay of transfected chloramphenicol acetyltransferase reporter genes driven by either wild-type or mutated NF-IL6 binding sites show a virus-induced increase in NF-IL6-dependent transcription. These studies have demonstrated a novel inducible mechanism for translational control of NF-IL6 synthesis and identify this transcription factor as a potential effector of the host response to RSV infection.

MeSH Terms
Base Sequence Binding Sites CCAAT-Enhancer-Binding Proteins Cell Line DNA/metabolism DNA-Binding Proteins/biosynthesis,genetics Epithelial Cells Humans Molecular Sequence Data Nuclear Proteins/biosynthesis,genetics Oligodeoxyribonucleotides Protein Biosynthesis RNA, Messenger/metabolism Respiratory Syncytial Viruses/physiology Time Factors Transcription Factors/biosynthesis,genetics Virus Replication
Chemicals
CCAAT-Enhancer-Binding Proteins DNA-Binding Proteins Nuclear Proteins Oligodeoxyribonucleotides RNA, Messenger Transcription Factors DNA
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Jamaluddin M
Department of Internal Medicine, Sealy Center for Molecular Science, University of Texas Medical Branch, Galveston, USA.
Garofalo R
Ogra P L
Brasier A R
References (49)
49 references, click to expand
  1. Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation.
    Prog Nucleic Acid Res Mol Biol. 1988;35:173-207 PMID: 3065823
  2. 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
  3. Cap recognition and the entry of mRNA into the protein synthesis initiation cycle.
    Trends Biochem Sci. 1988 Feb;13(2):52-6 PMID: 3238751
  4. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family.
    EMBO J. 1990 Jun;9(6):1897-906 PMID: 2112087
  5. 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
  6. LAP, a novel member of the C/EBP gene family, encodes a liver-enriched transcriptional activator protein.
    Genes Dev. 1990 Sep;4(9):1541-51 PMID: 2253878
  7. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA.
    Cell. 1991 Nov 1;67(3):569-79 PMID: 1934061
  8. Cytokine production by epithelial cells.
    FASEB J. 1994 Oct;8(13):1041-7 PMID: 7926369
  9. Regulatory elements and transcription factors controlling basal and cytokine-induced expression of the gene encoding intercellular adhesion molecule 1.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11641-5 PMID: 7972116
  10. Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages.
    Cell. 1995 Jan 27;80(2):353-61 PMID: 7530603
  11. Functional NF-IL6/CCAAT enhancer-binding protein is required for tumor necrosis factor alpha-inducible expression of the granulocyte colony-stimulating factor (CSF), but not the granulocyte/macrophage CSF or interleukin 6 gene in human fibroblasts.
    J Exp Med. 1995 Feb 1;181(2):793-8 PMID: 7530764
  12. Translational regulation in development.
    Cell. 1995 Apr 21;81(2):171-8 PMID: 7736569
  13. Lymphoproliferative disorder and imbalanced T-helper response in C/EBP beta-deficient mice.
    EMBO J. 1995 May 1;14(9):1932-41 PMID: 7744000
  14. CRP2 (C/EBP beta) contains a bipartite regulatory domain that controls transcriptional activation, DNA binding and cell specificity.
    EMBO J. 1995 Jul 3;14(13):3170-83 PMID: 7621830
  15. Transcription stimulation of the Fas-encoding gene by nuclear factor for interleukin-6 expression upon influenza virus infection.
    J Biol Chem. 1995 Jul 28;270(30):18007-12 PMID: 7543095
  16. 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
  17. Growth and serological characteristics of respiratory syncytial virus.
    J Infect Dis. 1962 Jan-Feb;110:8-16 PMID: 13867292
  18. Tumor necrosis factor-induced reversal of adipocytic phenotype of 3T3-L1 cells is preceded by a loss of nuclear CCAAT/enhancer binding protein (C/EBP).
    J Clin Invest. 1992 Jan;89(1):223-33 PMID: 1729273
  19. Mechanism and regulation of eukaryotic protein synthesis.
    Microbiol Rev. 1992 Jun;56(2):291-315 PMID: 1620067
  20. Intercellular adhesion molecule-1 (ICAM-1)-dependent and ICAM-1-independent adhesive interactions between polymorphonuclear leukocytes and human airway epithelial cells infected with parainfluenza virus type 2.
    J Immunol. 1992 Nov 15;149(10):3345-9 PMID: 1358969
  21. Binding of Xenopus oocyte masking proteins to mRNA sequences.
    Nucleic Acids Res. 1992 Nov 11;20(21):5593-600 PMID: 1454524
  22. Regulation of translation in eukaryotic systems.
    Annu Rev Cell Biol. 1992;8:197-225 PMID: 1335743
  23. Regulating the fate of mRNA: the control of cellular iron metabolism.
    Cell. 1993 Jan 15;72(1):19-28 PMID: 8380757
  24. Phosphorylation at threonine-235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2207-11 PMID: 8384717
  25. Respiratory syncytial virus.
    Curr Probl Pediatr. 1993 Feb;23(2):50-79 PMID: 7681743
  26. CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8219-23 PMID: 8367486
  27. Kinetics of the respiratory syncytial virus growth cycle in HeLa cells.
    Arch Gesamte Virusforsch. 1969;28(2):122-32 PMID: 5369728
  28. Morphogenesis of respiratory syncytial virus in a green monkey kidney cell line (Vero).
    J Virol. 1970 Aug;6(2):237-42 PMID: 4100527
  29. Effect of respiratory syncytial virus infection of HeLa-cell macromolecular synthesis.
    J Gen Virol. 1977 Oct;37(1):53-63 PMID: 915484
  30. State of the art: bronchiolitis.
    Am Rev Respir Dis. 1978 Oct;118(4):759-81 PMID: 212970
  31. Respiratory syncytial virus. I. Concentration and purification of the infectious virus.
    Acta Med Okayama. 1978 Aug;32(4):265-72 PMID: 153087
  32. Infectivity of respiratory syncytial virus by various routes of inoculation.
    Infect Immun. 1981 Sep;33(3):779-83 PMID: 7287181
  33. Respiratory syncytial viral infection in infants with congenital heart disease.
    N Engl J Med. 1982 Aug 12;307(7):397-400 PMID: 7088112
  34. Identification of a tenth mRNA of respiratory syncytial virus and assignment of polypeptides to the 10 viral genes.
    J Virol. 1984 Feb;49(2):572-8 PMID: 6546401
  35. Defective regulation of immune responses in respiratory syncytial virus infection.
    J Immunol. 1984 Oct;133(4):1925-30 PMID: 6236259
  36. Influences of mRNA secondary structure on initiation by eukaryotic ribosomes.
    Proc Natl Acad Sci U S A. 1986 May;83(9):2850-4 PMID: 3458245
  37. Expression of the F glycoprotein of respiratory syncytial virus by a recombinant vaccinia virus: comparison of the individual contributions of the F and G glycoproteins to host immunity.
    Proc Natl Acad Sci U S A. 1986 Oct;83(19):7462-6 PMID: 3532115
  38. Monoclonal antibodies to the large glycoproteins of respiratory syncytial virus: possible evidence for several functional antigenic sites.
    J Gen Virol. 1987 Aug;68 ( Pt 8):2161-7 PMID: 2440982
  39. Respiratory syncytial virus infection in children with bronchopulmonary dysplasia.
    Pediatrics. 1988 Aug;82(2):199-203 PMID: 3399292
  40. 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
  41. Transcription factors NF-IL6 and NF-kappa B synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10193-7 PMID: 8234276
  42. 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
  43. The role of NF-kappa B and NF-IL6 transactivating factors in the synergistic activation of human serum amyloid A gene expression by interleukin-1 and interleukin-6.
    J Biol Chem. 1993 Dec 5;268(34):25624-31 PMID: 8244997
  44. Identification of a novel determinant for basic domain-leucine zipper DNA binding activity in the acute-phase inducible nuclear factor-interleukin-6 transcription factor.
    J Biol Chem. 1994 Apr 8;269(14):10341-51 PMID: 8144615
  45. 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
  46. Protein kinase A and C site-specific phosphorylations of LAP (NF-IL6) modulate its binding affinity to DNA recognition elements.
    J Clin Invest. 1994 Jun;93(6):2554-61 PMID: 8200992
  47. Poly(A) binds to initiation factors and increases cap-dependent translation in vitro.
    J Biol Chem. 1994 Jun 24;269(25):17166-73 PMID: 8006024
  48. Cytokines and airway inflammation.
    Ann N Y Acad Sci. 1994 May 28;725:69-82 PMID: 8031010
  49. The scanning model for translation: an update.
    J Cell Biol. 1989 Feb;108(2):229-41 PMID: 2645293
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-03-00
Pages
1554-63
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC189977
Subset
IM
Grants
NIAID NIH HHS · AI/HL 15939-14A1 · United States
NICHD NIH HHS · R30HD 27841 · United States
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