Bordetella Avium Causes Induction of Apoptosis and Nitric Oxide Synthase in Turkey Tracheal Explant Cultures

Overview

Journal Microbes Infect

Publisher Elsevier

Specialties Allergy & Immunology
Microbiology

Date 2011 May 26

PMID 21609777

Citations 4

Authors

David M Miyamoto

Kristin Ruff

Nathan M Beach

Stephanie B Stockwell

Angella Dorsey-Oresto

Isaac Masters

Louise M Temple

Affiliations

Soon will be listed here.

Abstract

Bordetellosis is an upper respiratory disease of turkeys caused by Bordetella avium in which the bacteria attach specifically to ciliated respiratory epithelial cells. Little is known about the mechanisms of pathogenesis of this disease, which has a negative impact in the commercial turkey industry. In this study, we produced a novel explant organ culture system that was able to successfully reproduce pathogenesis of B. avium in vitro, using tracheal tissue derived from 26 day-old turkey embryos. Treatment of the explants with whole cells of B. avium virulent strain 197N and culture supernatant, but not lipopolysaccharide (LPS) or tracheal cytotoxin (TCT), specifically induced apoptosis in ciliated cells, as shown by annexin V and TUNEL staining. LPS and TCT are known virulence factors of Bordetella pertussis, the causative agent of whooping cough. Treatment with whole cells of B. avium and LPS specifically induced NO response in ciliated cells, shown by uNOS staining and diaphorase activity. The explant system is being used as a model to elucidate specific molecules responsible for the symptoms of bordetellosis.

Citing Articles

Characterization of Temperate LPS-Binding Bordetella avium Phages That Lack Superinfection Immunity.

Serian D, Churin Y, Hammerl J, Rohde M, Jung A, Muller A Microbiol Spectr. 2023; 11(3):e0370222.

PMID: 37125905 PMC: 10269795. DOI: 10.1128/spectrum.03702-22.

A rare case of pneumonia complicated by .

Lavrenko A, Digtiar N, Gerasymenko N, Kaidashev I Clin Case Rep. 2020; 8(6):1039-1043.

PMID: 32577260 PMC: 7303856. DOI: 10.1002/ccr3.2800.

Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice.

Perniss A, Schmidt N, Gurtner C, Dietert K, Schwengers O, Weigel M Sci Rep. 2018; 8(1):5681.

PMID: 29632402 PMC: 5890243. DOI: 10.1038/s41598-018-23830-4.

Monoclonal antibodies directed against the outer membrane protein of Bordetella avium.

Liu G, Liang M, Zuo X, Zhao X, Guo F, Yang S Monoclon Antib Immunodiagn Immunother. 2013; 32(4):295-300.

PMID: 23909425 PMC: 3733320. DOI: 10.1089/mab.2012.0124.

References

Furukawa K, Harrison D, Saleh D, Shennib H, Chagnon F, Giaid A . Expression of nitric oxide synthase in the human nasal mucosa. Am J Respir Crit Care Med. 1996; 153(2):847-50. DOI: 10.1164/ajrccm.153.2.8564142. View

Banan A, Fields J, Decker H, Zhang Y, Keshavarzian A . Nitric oxide and its metabolites mediate ethanol-induced microtubule disruption and intestinal barrier dysfunction. J Pharmacol Exp Ther. 2000; 294(3):997-1008. View

Sekiya K, Futaesaku Y, Nakase Y . Electron microscopic observations on tracheal epithelia of mice infected with Bordetella bronchiseptica. Microbiol Immunol. 1988; 32(5):461-72. DOI: 10.1111/j.1348-0421.1988.tb01406.x. View

Di Fabio J, Caroff M, Karibian D, Richards J, Perry M . Characterization of the common antigenic lipopolysaccharide O-chains produced by Bordetella bronchiseptica and Bordetella parapertussis. FEMS Microbiol Lett. 1992; 76(3):275-81. DOI: 10.1016/0378-1097(92)90348-r. View

Heiss L, Flak T, Lancaster Jr J, McDaniel M, Goldman W . Nitric oxide mediates Bordetella pertussis tracheal cytotoxin damage to the respiratory epithelium. Infect Agents Dis. 1993; 2(4):173-7. View

Temple L, Weiss A, Walker K, Barnes H, Christensen V, Miyamoto D . Bordetella avium virulence measured in vivo and in vitro. Infect Immun. 1998; 66(11):5244-51. PMC: 108655. DOI: 10.1128/IAI.66.11.5244-5251.1998. View

Preston A, Petersen B, Duus J, Kubler-Kielb J, Ben-Menachem G, Li J . Complete structures of Bordetella bronchiseptica and Bordetella parapertussis lipopolysaccharides. J Biol Chem. 2006; 281(26):18135-44. DOI: 10.1074/jbc.M513904200. View

Opremcak L, Rheins M . Scanning electron microscopy of mouse ciliated oviduct and tracheal epithelium infected in vitro with Bordetella pertussis. Can J Microbiol. 1983; 29(4):415-20. DOI: 10.1139/m83-067. View

Gavrieli Y, Sherman Y, Ben-Sasson S . Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 1992; 119(3):493-501. PMC: 2289665. DOI: 10.1083/jcb.119.3.493. View

10.

Kobzik L, Bredt D, Lowenstein C, Drazen J, Gaston B, Sugarbaker D . Nitric oxide synthase in human and rat lung: immunocytochemical and histochemical localization. Am J Respir Cell Mol Biol. 1993; 9(4):371-7. DOI: 10.1165/ajrcmb/9.4.371. View

11.

Rosbe K, Mims J, Prazma J, Petrusz P, Rose A, Drake A . Immunohistochemical localization of nitric oxide synthase activity in upper respiratory epithelium. Laryngoscope. 1996; 106(9 Pt 1):1075-9. DOI: 10.1097/00005537-199609000-00006. View

12.

Buttery L, Evans T, Springall D, Carpenter A, Cohen J, Polak J . Immunochemical localization of inducible nitric oxide synthase in endotoxin-treated rats. Lab Invest. 1994; 71(5):755-64. View

13.

Ermert M, Ruppert C, Gunther A, Duncker H, Seeger W, Ermert L . Cell-specific nitric oxide synthase-isoenzyme expression and regulation in response to endotoxin in intact rat lungs. Lab Invest. 2002; 82(4):425-41. PMC: 7102244. DOI: 10.1038/labinvest.3780436. View

14.

Soane M, Jackson A, Maskell D, Allen A, Keig P, Dewar A . Interaction of Bordetella pertussis with human respiratory mucosa in vitro. Respir Med. 2000; 94(8):791-9. DOI: 10.1053/rmed.2000.0823. View

15.

GRAY J, Roberts J, Dillman R, Simmons D . Pathogenesis of change in the upper respiratory tracts of turkeys experimentally infected with an Alcaligenes faecalis isolate. Infect Immun. 1983; 42(1):350-5. PMC: 264564. DOI: 10.1128/iai.42.1.350-355.1983. View

16.

Weinrauch Y, Zychlinsky A . The induction of apoptosis by bacterial pathogens. Annu Rev Microbiol. 1999; 53:155-87. DOI: 10.1146/annurev.micro.53.1.155. View

17.

Koopman G, Reutelingsperger C, Kuijten G, Keehnen R, Pals S, van Oers M . Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 1994; 84(5):1415-20. View

18.

Flak T, Goldman W . Autotoxicity of nitric oxide in airway disease. Am J Respir Crit Care Med. 1996; 154(4 Pt 2):S202-6. DOI: 10.1164/ajrccm/154.4_Pt_2.S202. View

19.

Flak T, Goldman W . Signalling and cellular specificity of airway nitric oxide production in pertussis. Cell Microbiol. 2001; 1(1):51-60. DOI: 10.1046/j.1462-5822.1999.00004.x. View

20.

Lin A, Chang C, McCormick C . Molecular cloning and expression of an avian macrophage nitric-oxide synthase cDNA and the analysis of the genomic 5'-flanking region. J Biol Chem. 1996; 271(20):11911-9. DOI: 10.1074/jbc.271.20.11911. View