Abstract
The primary human urethral epithelial cells developed by our laboratory have been immortalized by transduction with a retroviral vector expressing the human papillomavirus E6E7 oncogenes. Analysis of telomerase expression and comparison to that in primary cells revealed detectable levels in the transduced human urethral epithelial cells. Immortalized urethral cells could be passaged over 20 times. Immunofluorescence microscopy studies showed that the immortalized cells were phenotypically similar and responded to gonococcal infection similarly to primary cells. Specifically, positive cytokeratin staining showed that the immortalized cells are keratinocytes; cell surface levels of human asialoglycoprotein receptor increase following gonococcal infection, and, like the primary cells, the immortalized urethral epithelial cells are CD14 negative. Using enzyme-linked immunosorbent assay, we found that interleukin-6 (IL-6) and IL-8 levels in primary urethral epithelial cell supernatants increase after challenge with N. gonorrhoeae. Likewise, the immortalized urethral epithelial cells produced higher levels of IL-6 and IL-8 cytokines in response to gonococcal infection. Cells challenged with a gonococcal lipid A msbB mutant produced reduced IL-6 and IL-8 levels when compared to the parent strain. Additionally, these data suggest that the 1291 msbB lipooligosaccharide may suppress cytokine induction.
MeSH Terms
Asialoglycoprotein Receptor
Cell Transformation, Viral
Cells, Cultured
Cytokines/biosynthesis
Epithelial Cells/cytology,immunology,metabolism
Genes, Viral
Genetic Vectors
Gonorrhea/etiology,immunology,pathology
Humans
Inflammation Mediators/metabolism
Interleukin-6/biosynthesis
Interleukin-8/biosynthesis
Karyotyping
Keratins/metabolism
Lipopolysaccharide Receptors/metabolism
Models, Biological
Neisseria gonorrhoeae/pathogenicity
Oncogene Proteins, Viral/genetics
Papillomavirus E7 Proteins
Phenotype
Receptors, Cell Surface/metabolism
Retroviridae/genetics
Urethra/cytology,immunology,metabolism
Chemicals
Asialoglycoprotein Receptor
Cytokines
E6 protein, Human papillomavirus type 8
Inflammation Mediators
Interleukin-6
Interleukin-8
Lipopolysaccharide Receptors
Oncogene Proteins, Viral
Papillomavirus E7 Proteins
Receptors, Cell Surface
oncogene protein E7, Human papillomavirus type 16
Keratins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Harvey Hillery A
Department of Microbiology, The University of Iowa, Iowa City, Iowa 52242, USA.
Post Deborah M B
Apicella Michael A
References (28)
28 references, click to expand
-
Expression of paragloboside-like lipooligosaccharides may be a necessary component of gonococcal pathogenesis in men.
J Exp Med. 1991 Dec 1;174(6):1601-5
PMID: 1744587
-
Gonococcal infection of human fallopian tube mucosa in organ culture: relationship of mucosal tissue TNF-alpha concentration to sloughing of ciliated cells.
Sex Transm Dis. 1999 Mar;26(3):160-5
PMID: 10100774
-
Specific association of human telomerase activity with immortal cells and cancer.
Science. 1994 Dec 23;266(5193):2011-5
PMID: 7605428
-
Inflammatory cytokines produced in response to experimental human gonorrhea.
J Infect Dis. 1995 Jul;172(1):186-91
PMID: 7797909
-
Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin.
Annu Rev Immunol. 1995;13:437-57
PMID: 7542010
-
A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide.
J Clin Invest. 1996 Jan 15;97(2):359-65
PMID: 8567955
-
The pathogenesis of gonococcal urethritis in men: confocal and immunoelectron microscopic analysis of urethral exudates from men infected with Neisseria gonorrhoeae.
J Infect Dis. 1996 Mar;173(3):636-46
PMID: 8627027
-
Membrane-bound CD154, but not CD40-specific antibody, mediates NF-kappaB-independent IL-6 production in B cells.
Eur J Immunol. 1999 Dec;29(12):3855-66
PMID: 10601993
-
Macropinocytosis as a mechanism of entry into primary human urethral epithelial cells by Neisseria gonorrhoeae.
Infect Immun. 2000 Mar;68(3):1696-9
PMID: 10678991
-
Gonococcal lipooligosaccharide is a ligand for the asialoglycoprotein receptor on human sperm.
Mol Microbiol. 2000 Jun;36(5):1059-70
PMID: 10844691
-
Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor.
Mol Microbiol. 2001 Nov;42(3):659-72
PMID: 11722733
-
Intracellular survival of Neisseria gonorrhoeae in male urethral epithelial cells: importance of a hexaacyl lipid A.
Infect Immun. 2002 Feb;70(2):909-20
PMID: 11796626
-
The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells.
J Virol. 1991 Jan;65(1):473-8
PMID: 1845902
-
The lipooligosaccharides of pathogenic gram-negative bacteria.
Crit Rev Microbiol. 1996;22(3):139-80
PMID: 8894399
-
Bacterial adherence and mucosal cytokine responses. Receptors and transmembrane signaling.
Ann N Y Acad Sci. 1996 Oct 25;797:177-90
PMID: 8993361
-
Telomerase activation and cancer.
J Mol Med (Berl). 1997 Jan;75(1):45-9
PMID: 9020383
-
Ultrastructural analysis of primary human urethral epithelial cell cultures infected with Neisseria gonorrhoeae.
Infect Immun. 1997 Jun;65(6):2420-7
PMID: 9169783
-
Adhesion and invasion by the pathogenic neisseria.
Trends Microbiol. 1997 Jun;5(6):217-21
PMID: 9211640
-
Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor kappaB and activator protein 1 and the induction of inflammatory cytokines.
J Exp Med. 1997 Jul 21;186(2):247-58
PMID: 9221754
-
Attachment of piliated, Opa- and Opc- gonococci and meningococci to epithelial cells elicits cortical actin rearrangements and clustering of tyrosine-phosphorylated proteins.
Infect Immun. 1997 Oct;65(10):4341-9
PMID: 9317047
-
A primer on cytokines: sources, receptors, effects, and inducers.
Clin Microbiol Rev. 1997 Oct;10(4):742-80
PMID: 9336671
-
Neisseria gonorrhoeae induces focal polymerization of actin in primary human urethral epithelium.
Infect Immun. 1998 Jul;66(7):3416-9
PMID: 9632614
-
Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections.
J Infect Dis. 1998 Sep;178(3):742-51
PMID: 9728543
-
Coordinate activation of activator protein 1 and inflammatory cytokines in response to Neisseria gonorrhoeae epithelial cell contact involves stress response kinases.
J Exp Med. 1998 Oct 5;188(7):1277-86
PMID: 9763607
-
Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells.
Nature. 1998 Nov 5;396(6706):84-8
PMID: 9817205
-
Invasion of human mucosal epithelial cells by Neisseria gonorrhoeae upregulates expression of intercellular adhesion molecule 1 (ICAM-1).
Infect Immun. 1999 Mar;67(3):1149-56
PMID: 10024555
-
Host cell interactions and signalling with Neisseria gonorrhoeae.
Curr Opin Microbiol. 1999 Feb;2(1):62-70
PMID: 10047561
-
Local induction of tumor necrosis factor as a molecular mechanism of mucosal damage by gonococci.
Microb Pathog. 1992 May;12(5):333-41
PMID: 1501572