The Transcriptional Responses of Respiratory Epithelial Cells to Bordetella Pertussis Reveal Host Defensive and Pathogen Counter-defensive Strategies

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2000 Nov 23

PMID 11087813

Citations 42

Authors

C E Belcher

J Drenkow

B Kehoe

T R Gingeras

N McNamara

H Lemjabbar

C Basbaum

D A Relman

Affiliations

Soon will be listed here.

Abstract

Bordetella pertussis, the causative agent of whooping cough, has many well-studied virulence factors and a characteristic clinical presentation. Despite this information, it is not clear how B. pertussis interaction with host cells leads to disease. In this study, we examined the interaction of B. pertussis with a human bronchial epithelial cell line (BEAS-2B) and measured host transcriptional profiles by using high-density DNA microarrays. The early transcriptional response to this pathogen is dominated by altered expression of cytokines, DNA-binding proteins, and NFkappaB-regulated genes. This previously unrecognized response to B. pertussis was modified in similar but nonidentical fashions by the antiinflammatory agents dexamethasone and sodium salicylate. Cytokine protein expression was confirmed, as was neutrophil chemoattraction. We show that B. pertussis induces mucin gene transcription by BEAS-2B cells then counters this defense by using mucin as a binding substrate. A set of genes is described for which the catalytic activity of pertussis toxin is both necessary and sufficient to regulate transcription. Host genomic transcriptional profiling, in combination with functional assays to evaluate subsequent biological events, provides insight into the complex interaction of host and pathogen.

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References

Relman D, Domenighini M, Tuomanen E, Rappuoli R, Falkow S . Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A. 1989; 86(8):2637-41. PMC: 286972. DOI: 10.1073/pnas.86.8.2637. View

Grey S, Arvelo M, Hasenkamp W, Bach F, Ferran C . A20 inhibits cytokine-induced apoptosis and nuclear factor kappaB-dependent gene activation in islets. J Exp Med. 1999; 190(8):1135-46. PMC: 2195658. DOI: 10.1084/jem.190.8.1135. View

Anisowicz A, Messineo M, Lee S, Sager R . An NF-kappa B-like transcription factor mediates IL-1/TNF-alpha induction of gro in human fibroblasts. J Immunol. 1991; 147(2):520-7. View

Rollins B, Walz A, Baggiolini M . Recombinant human MCP-1/JE induces chemotaxis, calcium flux, and the respiratory burst in human monocytes. Blood. 1991; 78(4):1112-6. View

Pizza M, Covacci A, Bartoloni A, Perugini M, Nencioni L, De Magistris M . Mutants of pertussis toxin suitable for vaccine development. Science. 1989; 246(4929):497-500. DOI: 10.1126/science.2683073. View

Flak T, Heiss L, Engle J, Goldman W . Synergistic epithelial responses to endotoxin and a naturally occurring muramyl peptide. Infect Immun. 2000; 68(3):1235-42. PMC: 97273. DOI: 10.1128/IAI.68.3.1235-1242.2000. View

Eckmann L, Smith J, Housley M, Dwinell M, Kagnoff M . Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria Salmonella. J Biol Chem. 2000; 275(19):14084-94. DOI: 10.1074/jbc.275.19.14084. View

Rosenberger C, Scott M, Gold M, Hancock R, Finlay B . Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol. 2000; 164(11):5894-904. DOI: 10.4049/jimmunol.164.11.5894. View

Dohrman A, Miyata S, Gallup M, Li J, Chapelin C, Coste A . Mucin gene (MUC 2 and MUC 5AC) upregulation by Gram-positive and Gram-negative bacteria. Biochim Biophys Acta. 1998; 1406(3):251-9. DOI: 10.1016/s0925-4439(98)00010-6. View

10.

Katada T, Ui M . Direct modification of the membrane adenylate cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein. Proc Natl Acad Sci U S A. 1982; 79(10):3129-33. PMC: 346367. DOI: 10.1073/pnas.79.10.3129. View

11.

Spangrude G, Sacchi F, Hill H, Van Epps D, Daynes R . Inhibition of lymphocyte and neutrophil chemotaxis by pertussis toxin. J Immunol. 1985; 135(6):4135-43. View

12.

Hewlett E, Weiss A, Crane J, Pearson R, ANDERSON H, Myers G . Bordetella extracytoplasmic adenylate cyclase: actions as a bacterial toxin. Dev Biol Stand. 1985; 61:21-6. View

13.

Ishikawa H, ISAYAMA Y . Evidence for sialyl glycoconjugates as receptors for Bordetella bronchiseptica on swine nasal mucosa. Infect Immun. 1987; 55(7):1607-9. PMC: 260565. DOI: 10.1128/iai.55.7.1607-1609.1987. View

14.

Wolpe S, Sherry B, Juers D, Davatelis G, Yurt R, Cerami A . Identification and characterization of macrophage inflammatory protein 2. Proc Natl Acad Sci U S A. 1989; 86(2):612-6. PMC: 286522. DOI: 10.1073/pnas.86.2.612. View

15.

Detmers P, Powell D, Walz A, Clark-Lewis I, Baggiolini M, COHN Z . Differential effects of neutrophil-activating peptide 1/IL-8 and its homologues on leukocyte adhesion and phagocytosis. J Immunol. 1991; 147(12):4211-7. View

16.

Roberts I, Gavin R, Lennon D . Randomized controlled trial of steroids in pertussis. Pediatr Infect Dis J. 1992; 11(11):982-3. View

17.

Matsusaka T, Fujikawa K, Nishio Y, Mukaida N, Matsushima K, Kishimoto T . 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; 90(21):10193-7. PMC: 47740. DOI: 10.1073/pnas.90.21.10193. View

18.

Heiss L, Lancaster Jr J, Corbett J, Goldman W . Epithelial autotoxicity of nitric oxide: role in the respiratory cytopathology of pertussis. Proc Natl Acad Sci U S A. 1994; 91(1):267-70. PMC: 42928. DOI: 10.1073/pnas.91.1.267. View

19.

Cundell D, Kanthakumar K, Taylor G, Goldman W, Flak T, COLE P . Effect of tracheal cytotoxin from Bordetella pertussis on human neutrophil function in vitro. Infect Immun. 1994; 62(2):639-43. PMC: 186151. DOI: 10.1128/iai.62.2.639-643.1994. View

20.

Khelef N, Bachelet C, Vargaftig B, Guiso N . Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infect Immun. 1994; 62(7):2893-900. PMC: 302896. DOI: 10.1128/iai.62.7.2893-2900.1994. View