Transcriptome Landscape of Intracellular Brucella ovis Surviving in RAW264.7 Macrophage Immune System.


Journal

Inflammation
ISSN: 1573-2576
Titre abrégé: Inflammation
Pays: United States
ID NLM: 7600105

Informations de publication

Date de publication:
Oct 2020
Historique:
pubmed: 21 5 2020
medline: 16 7 2021
entrez: 21 5 2020
Statut: ppublish

Résumé

Brucella ovis infection results in genital damage and epididymitis in rams, placental inflammation and rare abortion in ewes, and neonatal mortality in lambs. However, the mechanism underlying B. ovis infection remains unclear. In the present study, we used prokaryotic transcriptome sequencing to identify the differentially expressed genes (DEGs) between wild-type B. ovis and intracellular B. ovis in RAW264.7 macrophages. Gene ontology (GO) term enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis were performed, and quantitative reverse transcriptase PCR (qRT-PCR) was used to validate the top 10 upregulated and downregulated DEGs. The results showed that 212 genes were differentially expressed, including 68 upregulated and 144 downregulated genes, which were mainly enriched in 30 GO terms linked to biological process, cellular component, and molecular function. KEGG analysis showed that the DEGs were enriched in the hypoxia-inducible factor 1 (HIF-1) signaling pathway, mitogen-activated protein kinase (MAPK) signaling pathway, beta-alanine metabolism, and quorum sensing pathway. BME_RS01160, BME_RS04270, BME_RS08185, BME_RS12880, BME_RS25875, predicted_RNA865, and predicted_RNA953 were confirmed with the transcriptome sequencing data. Hence, our findings not only reveal the intracellular parasitism of B. ovis in the macrophage immune system, but also help to understand the mechanism of chronic B. ovis infection.

Identifiants

pubmed: 32430895
doi: 10.1007/s10753-020-01239-4
pii: 10.1007/s10753-020-01239-4
pmc: PMC7235551
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1649-1666

Subventions

Organisme : the National Science Foundation for Young Scientists of China
ID : 31802215

Références

Pandey, A., F. Lin, A.L. Cabello, L.F. da Costa, X. Feng, H.Q. Feng, M.Z. Zhang, T. Iwawaki, A. Rice-Ficht, T.A. Ficht, P. de Figueiredo, and Q.M. Qin. 2018. Activation of host IRE1α-dependent signaling axis contributes the intracellular parasitism of Brucella melitensis. Frontiers in Cellular and Infection Microbiology 8: 103.
pubmed: 29732320 pmcid: 5919948
Rittig, M.G., A. Kaufmann, A. Robins, B. Shaw, H. Sprenger, D. Gemsa, V. Foulongne, B. Rouot, and J. Dornand. 2003. Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. Journal of Leukocyte Biology 74: 1045–1055.
pubmed: 12960272
Adams, L.G. 2002. The pathology of brucellosis reflects the outcome of the battle between the host genome and the Brucella genome. Veterinary Microbiology 90: 553–561.
pubmed: 12414171
Li, S., Y. Liu, Y. Wang, H. Chen, C. Liu, and Y. Wang. 2019. Lateral flow biosensor combined with loop-mediated isothermal amplification for simple, rapid, sensitive, and reliable detection of Brucella spp. Infect Drug Resist 12: 2343–2353.
pubmed: 31440069 pmcid: 6679679
Das, A., B. Kumar, S. Chakravarti, C. Prakash, R.P. Singh, V. Gupta, K.P. Singh, R.K. Agrawal, V.K. Chaturvedi, Abhishek, and G. Shrinet. 2018. Rapid visual isothermal nucleic acid-based detection assay of Brucella species by polymerase spiral reaction. Journal of Applied Microbiology 125: 646–654.
pubmed: 30152897
Lusk Pfefer, T.S., R. Timme, and J.A. Kase. 2018. Identification of Brucella genus and eight Brucella species by Luminex bead-based suspension array. Food Microbiology 70: 113–119.
pubmed: 29173617
Abd El-Wahab, E.W., Y.M. Hegazy, W.F. El-Tras, A. Mikheal, A.F. Kabapy, M. Abdelfatah, M. Bruce, and M.M. Eltholth. 2019. A multifaceted risk model of brucellosis at the human-animal interface in Egypt. Transboundary and Emerging Diseases 66: 2383–2401.
pubmed: 31309735
Hosein, H.I., H.M. Zaki, N.M. Safwat, A.M.S. Menshawy, S. Rouby, A. Mahrous, and B.E. Madkour. 2018. Evaluation of the General Organization of Veterinary Services control program of animal brucellosis in Egypt: An outbreak investigation of brucellosis in buffalo. Vet World 11: 748–757.
pubmed: 30034165 pmcid: 6048072
Njeru, J., G. Wareth, F. Melzer, K. Henning, M.W. Pletz, R. Heller, and H. Neubauer. 2016. Systematic review of brucellosis in Kenya: Disease frequency in humans and animals and risk factors for human infection. BMC Public Health 16: 853.
pubmed: 27549329 pmcid: 4994226
Perin, G., N.B. Bottari, A.D. Silva, A.M. Jaguezeski, T.M.A. Gomes, T.F. Lopes, M.R.C. Schetinger, V.M. Morsch, and A.S. Da Silva. 2019. Cholinesterase's activities of infected mice by Brucella ovis. Microbial Pathogenesis 132: 137–140.
pubmed: 31028864
Pérez-Etayo, L., M.J. de Miguel, R. Conde-Álvarez, P.M. Muñoz, M. Khames, M. Iriarte, I. Moriyón, and A. Zúñiga-Ripa. 2018. The CO2-dependence of Brucella ovis and Brucella abortus biovars is caused by defective carbonic anhydrases. Veterinary Research 49: 85.
pubmed: 30185220 pmcid: 6126018
Sidhu-Muñoz, R.S., P. Sancho, and N. Vizcaíno. 2016. Brucella ovis PA mutants for outer membrane proteins Omp10, Omp19, SP41, and BepC are not altered in their virulence and outer membrane properties. Veterinary Microbiology 186: 59–66.
pubmed: 27016758
Macedo, A.A., A.P. Silva, J.P. Mol, L.F. Costa, L.N. Garcia, M.S. Araújo, O.A. Martins Filho, T.A. Paixão, and R.L. Santos. 2015. The abcEDCBA-encoded ABC transporter and the virB operon-encoded type IV secretion system of Brucella ovis are critical for intracellular trafficking and survival in ovine monocyte-derived macrophages. PLoS One 10: e0138131.
pubmed: 26366863 pmcid: 4569489
Soler-Lloréns, P., Y. Gil-Ramírez, A. Zabalza-Baranguá, M. Iriarte, R. Conde-Álvarez, A. Zúñiga-Ripa, B. San Román, M.S. Zygmunt, N. Vizcaíno, A. Cloeckaert, M.J. Grilló, I. Moriyón, and I. López-Goñi. 2014. Mutants in the lipopolysaccharide of Brucella ovis are attenuated and protect against B. ovis infection in mice. Veterinary Research 45: 72.
pubmed: 25029920 pmcid: 4107470
Buccheri, M.A., E. Salvo, M. Coci, G.M. Quero, L. Zoccarato, V. Privitera, and G. Rappazzo. Investigating microbial indicators of anthropogenic marine pollution by 16S and 18S high-throughput sequencing (HTS) library analysis. 2019. FEMS Microbiology Letters. https://doi.org/10.1093/femsle/fnz179 .
Wu, Z., F.J. Gatesoupe, Q. Zhang, X. Wang, Y. Feng, S. Wang, D. Feng, and A. Li. 2019. High-throughput sequencing reveals the gut and lung prokaryotic community profiles of the Chinese giant salamander (Andrias davidianus). Molecular Biology Reports 46: 5143–5154.
pubmed: 31364018
Jain, C., L.M. Rodriguez-R, A.M. Phillippy, K.T. Konstantinidis, and S. Aluru. 2018. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications 9: 5114.
pubmed: 30504855 pmcid: 6269478
Numanagić, I., J.K. Bonfield, F. Hach, J. Voges, J. Ostermann, C. Alberti, M. Mattavelli, and S.C. Sahinalp. 2016. Comparison of high-throughput sequencing data compression tools. Nature Methods 13: 1005–1008.
pubmed: 27776113
Singh, A., and P. Bhatia. 2016. Automated Sanger Analysis Pipeline (ASAP): A tool for rapidly analyzing sanger sequencing data with minimum user interference. Journal of Biomolecular Techniques 27: 129–131.
pubmed: 27790076
Albayrak, L., K. Khanipov, G. Golovko, and Y. Fofanov. 2019. Broom: Application for non-redundant storage of high throughput sequencing data. Bioinformatics 35: 143–145.
pubmed: 30010786
Dodds, K.G., J.C. McEwan, R. Brauning, T.C. van Stijn, S.J. Rowe, K.M. McEwan, and S.M. Clarke. 2019. G3 (Bethesda). Exclusion and genomic relatedness methods for assignment of parentage using genotyping-by-sequencing data. 9: 3239–3247.
Sadedin, S.P., and A. Oshlack. 2019. Bazam: A rapid method for read extraction and realignment of high-throughput sequencing data. Genome Biology 20: 78.
pubmed: 30999943 pmcid: 6472072
Nietsch, R., J. Haas, A. Lai, D. Oehler, S. Mester, K.S. Frese, F. Sedaghat-Hamedani, E. Kayvanpour, A. Keller, and B. Meder. 2016. The role of quality control in targeted next-generation sequencing library preparation. Genom Ptoteom Bioinf 14: 200–206.
Escobar, A., P.I. Rodas, and C. Acuña-Castillo. 2018. Macrophage-Neisseria gonorrhoeae interactions: A better understanding of pathogen mechanisms of immunomodulation. Frontiers in Immunology 9: 3044.
pubmed: 30627130 pmcid: 6309159
BoseDasgupta, S., and J. Pieters. 2018. Macrophage-microbe interaction: Lessons learned from the pathogen mycobacterium tuberculosis. Seminars in Immunopathology 40: 577–591.
pubmed: 30306257
Xu, S.J., H.T. Hu, H.L. Li, and S. Chang. 2019. The role of miRNAs in immune cell development, immune cell activation, and tumor immunity: With a focus on macrophages and natural killer cells. Cells. https://doi.org/10.3390/cells8101140 .
Hartenstein, V., and P. Martinez. 2019. Phagocytosis in cellular defense and nutrition: A food-centered approach to the evolution of macrophages. Cell and Tissue Research 377: 527–547.
pubmed: 31485720 pmcid: 6750737
Wang, Y., H. Liu, and J. Zhao. 2019, 2019. Macrophage polarization induced by probiotic bacteria: A concise review. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-019-09612-y .
Ma, Y., Y. Liang, N. Wang, L. Cui, Z. Chen, H. Wu, C. Zhu, Z. Wang, S. Liu, and H. Li. Avian flavivirus infection of monocytes/macrophages by extensive subversion of host antiviral innate immune responses. 2019. Journal of Virology. https://doi.org/10.1128/JVI.00978-19 .
Sidhu-Muñoz, R.S., P. Sancho, and N. Vizcaíno. 2018. Evaluation of human trophoblasts and ovine testis cell lines for the study of the intracellular pathogen Brucella ovis. FEMS Microbiology Letters 365: 24.
Silva, T.M., J.P. Mol, M.G. Winter, V. Atluri, M.N. Xavier, S.F. Pires, T.A. Paixão, H.M. Andrade, R.L. Santos, and R.M. Tsolis. 2014. The predicted ABC transporter AbcEDCBA is required for type IV secretion system expression and lysosomal evasion by Brucella ovis. PLoS One 9: e114532.
pubmed: 25474545 pmcid: 4256435
Silva, T.M., Paixão, T.A., Costa, E.A., Xavier, M.N., Sá, J.C., Moustacas, V.S., den Hartigh, A.B., Carvalho Neta, A.V , Oliveira, S.C., Tsolis, R., and Santos, R.L. Putative ATP-binding cassette transporter is essential for Brucella ovis pathogenesis in mice. 2011. Infection and Immunity 79: 1706–1717.
pubmed: 21300772 pmcid: 3067543
Covert, J., A.J. Mathison, L. Eskra, M. Banai, and G. Splitter. 2009. Brucella melitensis, B. neotomae and B. ovis elicit common and distinctive macrophage defense transcriptional responses. Experimental Biology and Medicine (Maywood, N.J.) 234: 1450–1467.
Galindo, R.C., P.M. Muñoz, M.J. de Miguel, C.M. Marin, J.M. Blasco, C. Gortazar, K.M. Kocan, and J. de la Fuente. 2009. Differential expression of inflammatory and immune response genes in rams experimentally infected with a rough virulent strain of Brucella ovis. Veterinary Immunology and Immunopathology 127: 295–303.
pubmed: 19056128
David, V., A. Martin, T. Isakova, C. Spaulding, L. Qi, V. Ramirez, K.B. Zumbrennen-Bullough, C.C. Sun, H.Y. Lin, J.L. Babitt, and M. Wolf. 2016. Inflammation and functional iron deficiency regulate fibroblast growth factor 23 production. Kidney International 89: 135–146.
pubmed: 26535997 pmcid: 4854810
Reyes, A.W., L.T. Arayan, H.L. Simborio, H.T. Hop, W. Min, H.J. Lee, D.H. Kim, H.H. Chang, and S. Kim. 2016. Dextran sulfate sodium upregulates MAPK signaling for the uptake and subsequent intracellular survival of Brucella abortus in murine macrophages. Microbial Pathogenesis 91: 68–73.
pubmed: 26626959
Dimitrakopoulos, O., K. Liopeta, G. Dimitracopoulos, and F. Paliogianni. 2013. Replication of Brucella melitensis inside primary human monocytes depends on mitogen activated protein kinase signaling. Microbes and Infection 15: 450–460.
pubmed: 23628412
Mika, L.A., W. Braun, E. Ciaccio, and R.J. Goodlow. 1954. The nature of the effect of alpha-alanine on population changes of Brucella. Journal of Bacteriology 68: 562–569.
pubmed: 13211558 pmcid: 357440
Altenbern, R.A., H.S. Ginoza, and D.R. Willoams. 1957. Metabolism and population changes in Brucella abortus. I. Roles of alanine and pantothenate in population changes. Journal of Bacteriology 73: 691–696.
pubmed: 13449033 pmcid: 289852
Tomita, H., Y. Yokooji, T. Ishibashi, T. Imanaka, and H. Atomi. 2014. An archaeal glutamate decarboxylase homolog functions as an aspartate decarboxylase and is involved in β-alanine and coenzyme a biosynthesis. Journal of Bacteriology 196: 1222–1230.
pubmed: 24415726 pmcid: 3957723
Yokota, M., S. Yahagi, and H. Masaki. 2018. Ethyl 2,4-dicarboethoxy pantothenate, a derivative of pantothenic acid, prevents cellular damage initiated by environmental pollutants through Nrf2 activation. Journal of Dermatological Science 92: 162–171.
pubmed: 30219519
Taminiau, B., M. Daykin, S. Swift, M.L. Boschiroli, A. Tibor, P. Lestrate, X. De Bolle, D. O'Callaghan, P. Williams, and J.J. Letesson. 2002. Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis. Infection and Immunity 70: 3004–3011.
pubmed: 12010991 pmcid: 128001
Delrue, R.M., C. Deschamps, S. Léonard, C. Nijskens, I. Danese, J.M. Schaus, S. Bonnot, J. Ferooz, A. Tibor, X. De Bolle, and J.J. Letesson. 2005. A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cellular Microbiology 7: 1151–1161.
pubmed: 16008582
Wu, S., J. Liu, C. Liu, A. Yang, and J. Qiao. 2020. Quorum sensing for population-level control of bacteria and potential therapeutic applications. 2019. Cellular and Molecular Life Sciences. https://doi.org/10.1007/s00018-019-03326-8 .
Mahdizade-Ari, M., M. Pourhajibagher, and A. Bahador. 2019. Changes of microbial cell survival, metabolic activity, efflux capacity, and quorum sensing ability of Aggregatibacter actinomycetemcomitans due to antimicrobial photodynamic therapy-induced bystander effects. Photodiagnosis and Photodynamic Therapy 26: 287–294.
pubmed: 31026616
Gül, B.Y., D.Y. Imer, P.K. Park, and I. Koyuncu. 2018. Selection of quorum quenching (QQ) bacteria for membrane biofouling control: Effect of different Gram-staining QQ bacteria, Bacillus sp. T5 and Delftia sp. T6, on microbial population in membrane bioreactors. Water Science and Technology 78: 358–366.
pubmed: 30101771
Camele, I., H.S. Elshafie, L. Caputo, and V. De Feo. 2019. Anti-quorum sensing and antimicrobial effect of mediterranean plant essential oils against phytopathogenic bacteria. Frontiers in Microbiology 10: 2619.
pubmed: 31803159 pmcid: 6877472
Theodora, N.A., V. Dominika, and D.E. Waturangi. 2019. Screening and quantification of anti-quorum sensing and antibiofilm activities of phyllosphere bacteria against biofilm forming bacteria. BMC Research Notes 12: 732.
pubmed: 31699135 pmcid: 6839195
Al-Shabib, N.A., F.M. Husain, R.A. Khan, M.S. Khan, M.Z. Alam, F.A. Ansari, S. Laeeq, M. Zubair, S.A. Shahzad, J.M. Khan, A. Alsalme, and I. Ahmad. 2019. Interference of phosphane copper (I) complexes of β-carboline with quorum sensing regulated virulence functions and biofilm in foodborne pathogenic bacteria: A first report. Saudi Journal of Biological Sciences 26: 308–316.
pubmed: 31485170
Uzureau, S., J. Lemaire, E. Delaive, M. Dieu, A. Gaigneaux, M. Raes, X. De Bolle, and J.J. Letesson. 2010. Global analysis of quorum sensing targets in the intracellular pathogen Brucella melitensis 16 M. Journal of Proteome Research 9: 3200–3217.
pubmed: 20387905 pmcid: 2880877

Auteurs

Hanwei Jiao (H)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China. jiaohanwei@swu.edu.cn.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China. jiaohanwei@swu.edu.cn.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China. jiaohanwei@swu.edu.cn.

Bowen Li (B)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Zonglin Zheng (Z)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.

Zhixiong Zhou (Z)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Wenjie Li (W)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Guojing Gu (G)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Juan Liu (J)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Yichen Luo (Y)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Xuehong Shuai (X)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Yu Zhao (Y)

Immunology Research Center, Medical Research Institute, Southwest University, Chongqing, 402460, People's Republic of China.
College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Yuxuan Liu (Y)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.

Yidan Wang (Y)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.

Xinglong Wang (X)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.

Xiaoyan Hu (X)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.

Li Wu (L)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Jixuan Chen (J)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Qingzhou Huang (Q)

College of Animal Science, Southwest University, Chongqing, 402460, People's Republic of China.
Chongqing Veterinary Scientific Engineering Research Center, Southwest University, Chongqing, 402460, People's Republic of China.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH