In vitro gene expression profile of bovine peripheral blood mononuclear cells in early Mycobacterium bovis infection

Cheng,Yafen; Chou,Chung‑Hsi; Tsai,Hsiang‑Jung

doi:10.3892/etm.2015.2814

In vitro gene expression profile of bovine peripheral blood mononuclear cells in early Mycobacterium bovis infection

Authors:
- Yafen Cheng
- Chung‑Hsi Chou
- Hsiang‑Jung Tsai
View Affiliations

Affiliations: School of Veterinary Medicine, National Taiwan University, Taipei 10617, Taiwan, R.O.C.
Published online on: October 19, 2015 https://doi.org/10.3892/etm.2015.2814
Pages: 2102-2118
Copyright: © Cheng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The intracellular parasite Mycobacterium bovis (M. bovis) causes tuberculosis in cattle and humans. Understanding the interactions between M. bovis and host cells is essential in developing tools for the prevention, detection, and treatment of M. bovis infection. Gene expression profiles provide a large amount of information regarding the molecular mechanisms underlying these interactions. The present study analyzed changes in gene expression in bovine peripheral blood mononuclear cells (PBMCs) at 0, 4 and 24 h following exposure to M. bovis. Using bovine whole‑genome microarrays, a total of 420 genes were identified that exhibited significant alterations in expression (≥2‑fold). Significantly enriched genes were identified using the Kyoto Encyclopedia of Genes and Genomes database, of which the highest differentially expressed genes were associated with the immune system, signal transduction, endocytosis, cellular transport, inflammation, and apoptosis. Of the genes associated with the immune system, 84.85% displayed downregulation. These findings support the view that M. bovis inhibits signaling pathways of antimycobacterial host defense in bovine PBMCs. These in vitro data demonstrated that molecular alterations underlying the pathogenesis of tuberculosis begin early, during the initial 24 h following M. bovis infection.

View Figures

View References

1	Etter E, Donado P, Jori F, Caron A, Goutard F and Roger F: Risk analysis and bovine tuberculosis, a re-emerging zoonosis. Ann NY Acad Sci. 1081:61–73. 2006. View Article : Google Scholar : PubMed/NCBI
2	Neill SD, Pollock JM, Bryson DB and Hanna J: Pathogenesis of Mycobacterium bovis infection in cattle. Vet Microbiol. 40:41–52. 1994. View Article : Google Scholar : PubMed/NCBI
3	Kabara E, Kloss CC, Wilson M, Tempelman RJ, Sreevatsan S, Janagama H and Coussens PM: A large-scale study of differential gene expression in monocyte-derived macrophages infected with several strains of Mycobacterium avium subspecies paratuberculosis. Brief Funct Genomics. 9:220–237. 2010. View Article : Google Scholar : PubMed/NCBI
4	Kerrigan AM and Brown GD: Syk-coupled C-type lectins in immunity. Trends Immunol. 32:151–156. 2011. View Article : Google Scholar : PubMed/NCBI
5	Saunders BM and Britton WJ: Life and death in the granuloma: Immunopathology of tuberculosis. Immunol Cell Biol. 85:103–111. 2007. View Article : Google Scholar : PubMed/NCBI
6	Magee DA, Taraktsoglou M, Killick KE, Nalpas NC, Browne JA, Park SD, Conlon KM, Lynn DJ, Hokamp K, Gordon SV, et al: Global gene expression and systems biology analysis of bovine monocyte-derived macrophages in response to in vitro challenge with Mycobacterium bovis. PLoS One. 7:e320342012. View Article : Google Scholar : PubMed/NCBI
7	Netea MG, Van der Meer JW and Kullberg BJ: Toll-like receptors as an escape mechanism from the host defense. Trends Microbiol. 12:484–488. 2004. View Article : Google Scholar : PubMed/NCBI
8	Behar SM, Divangahi M and Remold HG: Evasion of innate immunity by Mycobacterium tuberculosis: Is death an exit strategy? Nat Rev Microbiol. 8:668–674. 2010.PubMed/NCBI
9	Bovine Genome Sequencing and Analysis Consortium. Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, Elnitski L, et al: The genome sequence of taurine cattle: A window to ruminant biology and evolution. Science. 324:522–528. 2009. View Article : Google Scholar : PubMed/NCBI
10	Blanco FC, Soria M, Bianco MV and Bigi F: Transcriptional response of peripheral blood mononuclear cells from cattle infected with Mycobacterium bovis. PLoS One. 7:e410662012. View Article : Google Scholar : PubMed/NCBI
11	Meade KG, Gormley E, O'Farrelly C, Park SD, Costello E, Keane J, Zhao Y and MacHugh DE: Antigen stimulation of peripheral blood mononuclear cells from Mycobacterium bovis infected cattle yields evidence for a novel gene expression program. BMC Genomics. 9:4472008. View Article : Google Scholar : PubMed/NCBI
12	Killick KE, Browne JA, Park SD, Magee DA, Martin I, Meade KG, Gordon SV, Gormley E, O'Farrelly C, Hokamp K and MacHugh DE: Genome-wide transcriptional profiling of peripheral blood leukocytes from cattle infected with Mycobacterium bovis reveals suppression of host immune genes. BMC Genomics. 12:6112011. View Article : Google Scholar : PubMed/NCBI
13	Pollock JM and Neill SD: Mycobacterium bovis infection and tuberculosis in cattle. Vet J. 163:115–127. 2002. View Article : Google Scholar : PubMed/NCBI
14	Aranaz A, Liébana E, Mateos A, Dominguez L, Vidal D, Domingo M, Gonzolez O, Rodriguez-Ferri EF, Bunschoten AE, Van Embden JD and Cousins D: Spacer oligonucleotide typing of Mycobacterium bovis strains from cattle and other animals: A tool for studying epidemiology of tuberculosis. J Clin Microbiol. 34:2734–2740. 1996.PubMed/NCBI
15	Meade KG, Gormley E, Park SD, Fitzsimons T, Rosa GJ, Costello E, Keane J, Coussens PM and MacHugh DE: Gene expression profiling of peripheral blood mononuclear cells (PBMC) from Mycobacterium bovis infected cattle after in vitro antigenic stimulation with purified protein derivative of tuberculin (PPD). Vet Immunol Immunopathol. 113:73–89. 2006. View Article : Google Scholar : PubMed/NCBI
16	Meade KG, Gormley E, Doyle MB, Fitzsimons T, O'Farrelly C, Costello E, Keane J, Zhao Y and MacHugh DE: Innate gene repression associated with Mycobacterium bovis infection in cattle: Toward a gene signature of disease. BMC Genomics. 8:4002007. View Article : Google Scholar : PubMed/NCBI
17	Marchant A, Goetghebuer T, Ota MO, Wolfe I, Ceesay SJ, De Groote D, Corrah T, Bennett S, Wheeler J, Huygen K, et al: Newborns develop a Th1-type immune response to Mycobacterium bovis bacillus Calmette-Guérin vaccination. J Immunol. 163:2249–2255. 1999.PubMed/NCBI
18	Divangahi M, Chen M, Gan H, Desjardins D, Hickman TT, Lee DM, Fortune S, Behar SM and Remold HG: Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol. 10:899–906. 2009. View Article : Google Scholar : PubMed/NCBI
19	Lee J, Remold HG, Ieong MH and Kornfeld H: Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway. J Immunol. 176:4267–4274. 2006. View Article : Google Scholar : PubMed/NCBI
20	Widdison S, Watson M and Coffey TJ: Early response of bovine alveolar macrophages to infection with live and heat-killed Mycobacterium bovis. Dev Comp Immunol. 35:580–591. 2011. View Article : Google Scholar : PubMed/NCBI