PBMCs transcriptome profiles identified breed-specific transcriptome signatures for PRRSV vaccination in German Landrace and Pietrain pigs
Autoři:
Md. Aminul Islam aff001; Christiane Neuhoff aff001; Sharmin Aqter Rony aff001; Christine Große-Brinkhaus aff001; Muhammad Jasim Uddin aff002; Michael Hölker aff001; Dawit Tesfaye aff001; Ernst Tholen aff001; Karl Schellander aff001; Maren Julia Pröll-Cornelissen aff001
Působiště autorů:
Department of Animal Breeding and Husbandry, Institute of Animal Science, University of Bonn, Endenicher Allee 15, Bonn, Germany
aff001; Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh
aff002; Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh
aff003; School of Veterinary Science, The University of Queensland, Gatton campus, Brisbane, QLD, Australia
aff004; Teaching and Research Station on Frankenforst, Faculty of Agriculture, University of Bonn, Königswinter, Germany
aff005
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222513
Souhrn
Porcine reproductive and respiratory syndrome (PRRS) is a devastating viral disease affecting the swine industry worldwide. Genetic variation in host immunity has been considered as one of the potential determinants to improve the immunocompetence, thereby resistance to PRRS. Therefore, the present study aimed to investigate the breed difference in innate immune response to PRRSV vaccination between German Landrace (DL) and Pietrain (Pi) pigs. We analyzed microarray-based transcriptome profiles of peripheral blood mononuclear cells (PBMCs) collected before (0 h) and 24 h after PRRSV vaccination from purebred DL and Pi pigs with three biological replicates. In total 4,269 transcripts were identified to be differentially expressed in PBMCs in at least any of four tested contrast pairs (i.e. DL-24h vs. DL-0h, Pi-24h vs. Pi-0h, DL-0h vs. Pi-0h and DL-24h vs. Pi-24h). The number of vaccine-induced differentially expressed genes (DEGs) was much higher (2,459) in DL pigs than that of Pi pigs (291). After 24 h of PRRSV vaccination, 1,046 genes were differentially expressed in PMBCs of DL pigs compared to that of Pi (DL-24h vs. Pi-24h), indicating the breed differences in vaccine responsiveness. The top biological pathways significantly affected by DEGs of both breeds were linked to immune response functions. The network enrichment analysis identified ADAM17, STAT1, MMS19, RPA2, BAD, UCHL5 and APC as potential regulatory genes for the functional network of PRRSV vaccine response specific for DL; while FOXO3, IRF2, ADRBK1, FHL3, PPP2CB and NCOA6 were found to be the most potential hubs of Pi specific transcriptome network. In conclusion, our data provided insights of breed-specific host transcriptome responses to PRRSV vaccination which might contribute in better understanding of PPRS resistance in pigs.
Klíčová slova:
Biology and life sciences – Genetics – Gene expression – Genomics – Genome analysis – Organisms – Eukaryota – Computational biology – Animals – Gene identification and analysis – Genetic networks – Computer and information sciences – Network analysis – Medicine and health sciences – Microbiology – Vertebrates – Amniotes – Mammals – Infectious diseases – Immunology – Immune response – Vaccination and immunization – Public and occupational health – Preventive medicine – Virology – Infectious disease control – Vaccines – Transcriptome analysis – Swine – Virus effects on host gene expression
Zdroje
1. Nelsen CJ, Murtaugh MP, Faaberg KS. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 1999; 73(1): 270–80. 9847330
2. Lunney JK, Steibel JP, Reecy JM, Fritz E, Rothschild MF, Kerrigan M, et al. Probing genetic control of swine responses to PRRSV infection: current progress of the PRRS host genetics consortium. BMC Proc. 2011; 5(Suppl 4): S30.
3. Murtaugh MP, Xiao Z, Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 2002; 15(4): 533–547. doi: 10.1089/088282402320914485 12513925
4. Labarque G, Van Gucht S, Van Reeth K, Nauwynck H, Pensaert M. Respiratory tract protection upon challenge of pigs vaccinated with attenuated porcine reproductive and respiratory syndrome virus vaccines. Vet Microbiol. 2003; 95(3): 187–197. doi: 10.1016/s0378-1135(03)00157-3 12935746
5. Loving CL, Osorio FA, Murtaugh MP, Zuckermann FA. Innate and adaptive immunity against Porcine Reproductive and Respiratory Syndrome Virus. Vet Immunol Immunopathol. 2015; 167(1–2): 1–14. doi: 10.1016/j.vetimm.2015.07.003 26209116
6. Glass EJ. The molecular pathways underlying host resistance and tolerance to pathogens. Front Genet. 2012; 3: 263. doi: 10.3389/fgene.2012.00263 23403960
7. Rowland RR, Lunney J, Dekkers J. Control of porcine reproductive and respiratory syndrome (PRRS) through genetic improvements in disease resistance and tolerance. Front Genet. 2012; 3: 260. doi: 10.3389/fgene.2012.00260 23403935
8. Vestal DJ, Jeyaratnam JA. The Guanylate-Binding Proteins: Emerging Insights into the Biochemical Properties and Functions of This Family of Large Interferon-Induced Guanosine Triphosphatase: J Interferon Cytokine Res. 2011; 31(1): 89–97. doi: 10.1089/jir.2010.0102 21142871
9. Boddicker N, Waide EH, Rowland RR, Lunney JK, Garrick DJ, Reecy JM, et al. Evidence for a major QTL associated with host response to porcine reproductive and respiratory syndrome virus challenge. J Anim Sci. 2012; 90(6): 1733–1746. doi: 10.2527/jas.2011-4464 22205662
10. Koltes J E, Fritz-Waters E, Eisley CJ, Choi I, Bao H, Kommadath A, Sero NVL, Boddicker NJJ, Abrams SM, Schroyen M, Loyd H, Tuggle CK, Plastow GS, Guan L, Stothard P, Lunney JK, Liu P, Carpenter S, Rowland RRR, Dekkers JCM, and Reecy JM. Identification of a putative quantitative trait nucleotide in guanylate binding protein 5 for host response to PRRS virus infection. BMC Genomics. 2015; 16: 412. doi: 10.1186/s12864-015-1635-9 26016888
11. Abella G, Pena RN, Nogareda C, Armengol R, Vidal A, Moradell L, et al. A WUR SNP is associated with European Porcine Reproductive and Respiratory Virus Syndrome resistance and growth performance in pigs. Res Vet Sci. 2016; 104: 117–122. doi: 10.1016/j.rvsc.2015.12.014 26850549
12. Li Y, Sun Y, Xing F, Kang L, Wang P, Wang L, et al. Identification of a single nucleotide promoter polymorphism regulating the transcription of ubiquitin specific protease 18 gene related to the resi- stance to porcine reproductive and respiratory syndrome virus infection. Vet Immunol Immunopathol. 2014; 162(3–4): 65–71. doi: 10.1016/j.vetimm.2014.09.007 25446846
13. Xing J, Xing F, Zhang C, Zhang Y, Wang N, Li Y, et al. Genome-wide gene expression profiles in lung tissues of pig breeds differing in resistance to porcine reproductive and respiratory syndrome virus. PLoS ONE. 2014; 9(1): e86101. doi: 10.1371/journal.pone.0086101 24465897
14. Halbur PG, Rothschild MF, Thacker BJ, Meng XJ, Paul PS, Bruna JD. Differences in susceptibility of Duroc, Hampshire, and Meishan pigs to infection with a high virulence strain (VR2385) of porcine reproductive and respiratory syndrome virus (PRRSV). J Anim Breed Genet. 1998; 115(3): 181–189.
15. Ait-Ali T, Wilson AD, Carre W, Westcott DG, Frossard JP, Mellencamp MA, et al. Host inhibits replication of European porcine reproductive and respiratory syndrome virus in macrophages by altering differential regulation of type-I interferon transcriptional response. Immunogenetics. 2011; 63(7): 437–448. doi: 10.1007/s00251-011-0518-8 21380581
16. Christopher-Hennings J, Holler LD, Benfield DA, Nelson EA. Detection and duration of porcine reproductive and respiratory syndrome virus in semen, serum, peripheral blood mononuclear cells, and tissues from Yorkshire, Hampshire, and Landrace boars. J Vet Diagn Invest. 2001; 13(2): 133–142. doi: 10.1177/104063870101300207 11289209
17. Petry DB, Holl JW, Weber JS, Doster AR, Osorio FA, Johnson RK. Biological responses to porcine respiratory and reproductive syndrome virus in pigs of two genetic populations. J Anim Sci. 2005; 83(7): 1494–1502. doi: 10.2527/2005.8371494x 15956456
18. Reiner G, Willems H, Pesch S, Ohlinger VF. Variation in resistance to the porcine reproductive and respiratory syndrome virus (PRRSV) in Pietrain and Miniature pigs. J Anim Breed Genet. 2010; 127(2): 100–106. doi: 10.1111/j.1439-0388.2009.00818.x 20433517
19. Pröll MJ, Neuhoff C, Schellander K, Uddin MJ, Cinar MU, Sahadevan S, Qu X, Islam MA, Mller MA, Drosten C, Tesfaye D, Tholen E, Groe-Brinkhaus C. Transcriptome Profile of Lung Dendritic Cells after In Vitro Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) Infection. PLoS ONE. 2017; 12(11): e0187735. doi: 10.1371/journal.pone.0187735 29140992
20. Xiao S, Mo D, Wang Q, Jia J, Qin L, Yu X, Niu Y, Zhao X, Xiaohong Liu and Yaosheng Chen Aberrant host immune response induced by highly virulent PRRSV identified by digital gene expression tag profiling. BMC Genomics. 2010; 11: 544. doi: 10.1186/1471-2164-11-544 20929578
21. Siegrist C-A. General aspects of vaccinations. In: Stanley A. Plotkin WO, Offit Paul A., editor. Vaccines. 6th ed. Saunders, USA: Elsevier Health Sciences 2012. p. 14–32.
22. Schroyen M, Eisley C, Koltes JE, Fritz-Waters E, Choi I, Plastow GS, Guan L, Stothard P, Bao H, Kommadath A, Reecy JM, Lunney JK, Rowland RRR, Dekkers JCM, Tuggle CK. Bioinformatic analyses in early host response to Porcine Reproductive and Respiratory Syndrome virus (PRRSV) reveals pathway differences between pigs with alternate genotypes for a major host response QTL. BMC Genomics. 2016; 17: 196. doi: 10.1186/s12864-016-2547-z 26951612
23. Kommadath A, Bao H, Choi I, Reecy JM, Koltes JE, Fritz-Waters E, Eisley CJ, Grant JR, Rowland RRR, Tuggle CK, Dekkers JCM, Lunney JK, Guan LL, Stothard P, Plastow GS. Genetic architecture of gene expression underlying variation in host response to porcine reproductive and respiratory syndrome virus infection. Sci. Rep. 2017; 7: 46203. doi: 10.1038/srep46203 28393889
24. Islam MA, Grosse-Brinkhaus C, Pröll MJ, Uddin MJ, Rony SA, Tesfaye D, et al. Deciphering transcriptome profiles of peripheral blood mononuclear cells in response to PRRSV vaccination in pigs. BMC Genomics. 2016; 17: 641. doi: 10.1186/s12864-016-2849-1 27528396
25. Islam MA, Grosse-Brinkhaus C, Pröll MJ, Uddin MJ, Rony SA, Tesfaye D, et al. PBMC transcriptome profiles identifies the potential candidate genes and functional networks controlling the innate and the adaptive immune response to PRRSV vaccine in Pietrain pig. PLoS ONE. 2017; 12(3): e0171828. doi: 10.1371/journal.pone.0171828 28278192
26. Carvalho BS, Irizarry RA. A framework for oligonucleotide microarray preprocessing. Bioinformatics. 2010; 26(19): 2363–2367. doi: 10.1093/bioinformatics/btq431 20688976
27. Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and computational biology solutions using r and bioconductor: Springer 2005 pp.397–442.
28. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A typical and powerful approach to multiple testing. J R STAT SOC B. 1995; 57: 289–300.
29. Breuer K, Foroushani AK, Laird MR, Chen C, Sribnaia A, Lo R, et al. InnateDB: systems bio- logy of innate immunity and beyond–recent updates and continuing curation. Nucleic Acids Res. 2013; 41(Database issue): 24.
30. Mudunuri U, Che A, Yi M, Stephens RM. bioDBnet: the biological database network. Bioinformatics. 2009; 25(4): 555–556. doi: 10.1093/bioinformatics/btn654 19129209
31. Xia J, Benner MJ, Hancock RE. NetworkAnalyst–integrative approaches for protein-protein interaction network analysis and visual exploration. Nucleic Acids Res. 2014; 42(Web Server issue): 26.
32. Lunney JK, Chen H. Genetic control of host resistance to porcine reproductive and respiratory syndrome virus (PRRSV) infection. Virus Res. 2010; 154(1–2):161–169. doi: 10.1016/j.virusres.2010.08.004 20709118
33. Flori L, Gao Y, Laloe D, Lemonnier G, Leplat JJ, Teillaud A, et al. Immunity traits in pigs: substantial genetic variation and limited covariation. PLoS ONE. 2011; 6(7): e22717. doi: 10.1371/journal.pone.0022717 21829490
34. Ponsuksili S, Murani E, Walz C, Schwerin M, Wimmers K. Pre- and postnatal hepatic gene expression profiles of two pig breeds differing in body composition: insight into pathways of metabolic regulation. Physiol Genomics. 2007; 29 (3): 267–279. doi: 10.1152/physiolgenomics.00178.2006 17264241
35. Clapperton M, Bishop SC, Glass EJ. Innate immune traits differ between Meishan and Large White pigs. Vet Immunol Immunopathol. 2005; 104(3–4): 131–144. doi: 10.1016/j.vetimm.2004.10.009 15734534
36. Opriessnig T, Patterson AR, Madson DM, Pal N, Rothschild M, Kuhar D, et al. Difference in severity of porcine circovirus type two-induced pathological lesions between Landrace and Pietrain pigs. J Anim Sci. 2009; 87(5): 1582–1590. doi: 10.2527/jas.2008-1390 19181769
37. Gao Y, Flori L, Lecardonnel J, Esquerre D, Hu ZL, Teillaud A, et al. Transcriptome analysis of porcine PBMCs after in vitro stimulation by LPS or PMA/ionomycin using an expression array targeting the pig immune response. BMC Genomics. 2010;11(292):1471–2164.
38. Gardy JL, Lynn DJ, Brinkman FS, Hancock RE. Enabling a systems biology approach to immunology: focus on innate immunity. Trends Immunol. 2009; 30(6): 249–262. doi: 10.1016/j.it.2009.03.009 19428301
39. Macneil LT, Walhout AJ. Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression. Genome Res. 2011; 21(5): 645–657. doi: 10.1101/gr.097378.109 21324878
40. Hu ZL1, Park CA, Wu XL, Reecy JM. Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic Acids Res. 2013; 41(Database issue): D871–879. doi: 10.1093/nar/gks1150 23180796
41. Drew JE, Farquharson AJ, Mayer CD, Vase HF, Coates PJ, Steele RJ, et al. Predictive gene signatures: molecular markers distinguishing colon adenomatous polyp and carcinoma. PLoS ONE. 2014; 9(11): e113071. doi: 10.1371/journal.pone.0113071 25423035
42. Franaszczyk M, Bilinska ZT, Sobieszczanska-Malek M, Michalak E, Sleszycka J, Sioma A, et al. The BAG3 gene variants in Polish patients with dilated cardiomyopathy: four novel mutations and a genotype-phenotype correlation. J Transl Med. 2014; 12: 192. doi: 10.1186/1479-5876-12-192 25008357
43. Kumagai K, Nimura Y, Mizota A, Miyahara N, Aoki M, Furusawa Y, et al. Arpc1b gene is a candidate prediction marker for choroidal malignant melanomas sensitive to radiotherapy. Invest Ophthalmol Vis Sci. 2006; 47(6): 2300–2304. doi: 10.1167/iovs.05-0810 16723437
44. Gooz Monika. ADAM-17: The Enzyme That Does It All. Crit Rev Biochem Mol Biol. 2010; 45(2): 146–169. doi: 10.3109/10409231003628015 20184396
45. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, Castner BJ, Stocking KL, Reddy P, Srinivasan S, Nelson N, Boiani N, Schooley KA, Gerhart M, Davis R, Fitzner JN, Johnson RS, Paxton RJ, March CJ, Cerretti DP. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature. 1997; 385: 729–733. doi: 10.1038/385729a0 9034190
46. Gooz M, Gooz P, Luttrell LM, Raymond JR. 5-HT2A receptor induces ERK phosphorylation and proliferation through ADAM-17 tumor necrosis factor-alpha-converting enzyme (TACE) activation and heparin-bound epidermal growth factor-like growth factor (HB-EGF) shedding in mesangial cells. J Biol Chem. 2006; 281: 21004–21012. doi: 10.1074/jbc.M512096200 16737974
47. Etzerodt A, Rasmussen MR, Svendsen P, Chalaris A, Schwarz J, Galea I, Mller HJ, Moestrup SK. Structural basis for inflammationdriven shedding of CD163 ectodomain and tumor necrosis factor in macrophages. J. Biol. Chem. 2014; 289: 778–788. doi: 10.1074/jbc.M113.520213 24275664
48. Guo Longjun, Niu Junwei, Yu Haidong, Gu Weihong, Li Ren, Luo Xiaolei, Huang Mingming, Tian Zhijun, Feng Li, Wang Yue. Modulation of CD163 Expression by Metalloprotease ADAM17 Regulates Porcine Reproductive and Respiratory Syndrome Virus Entry. J. Virol. 2014; 88(18): 10448–10458. doi: 10.1128/JVI.01117-14 24965453
49. Koyama S, Ishii KJ, Coban C, Akira S. Innate immune response to viral infection. Cytokine. 2008; 43(3): 336–341. doi: 10.1016/j.cyto.2008.07.009 18694646
50. Jamie M Wilkinson, Hua Bao, Andrea Ladinig, Linjun H, Paul S, Joan KL, Graham SP, John C, Harding S. Genome-wide analysis of the transcriptional response to porcine reproductive and respiratory syndrome virus infection at the maternal/fetal interface and in the fetus. BMC Genomics. 2016; 17: 383. doi: 10.1186/s12864-016-2720-4 27207143
51. Kou H, Zhou Y, Gorospe RM, Wang Z. Mms19 protein functions in nucleotide excision repair by sustaining an adequate cellular concentration of the TFIIH component Rad3. Proc Natl Acad Sci U S A. 2008; 105(41): 15714–15719. doi: 10.1073/pnas.0710736105 18836076
52. Machida T, Kubota M, Kobayashi E, Iwadate Y, Saeki N, Yamaura A, Nomura F, Takiguchi M, Hiwasa T. Identification of stroke-associated-antigens via screening of recombinant proteins from the human expression cDNA library (SEREX). J Transl Med. 2015; 13: 71. doi: 10.1186/s12967-015-0393-4 25890248
53. Nathalie MD, Douglas RG. Role of Bcl-2 family members in immunity and disease. BBA-MOL CELL RES. 2004; 1644(23): 179–188.
54. Ana RG, Fung Z, Eric WFL. Role and regulation of the forkhead transcription factors FOXO3a and FOXM1 in carcinogenesis and drug resistance. Chin J Cancer. 2013; 32(7): 365–370. doi: 10.5732/cjc.012.10277 23706767
55. Badaoui B, Tuggle CK, Hu Z, Reecy JM, Ait-Ali T, Anselmo A, et al. Pig immune response to general stimulus and to porcine reproductive and respiratory syndrome virus infection: a meta-analysis approach. BMC Genomics. 2013; 14: 220. doi: 10.1186/1471-2164-14-220 23552196
56. Honda K, Takaoka A, Taniguchi T. Type I Inteferon Gene Induction by the Interferon Regulatory Factor Family of Transcription Factors. Immunity. 2006; 25 (3): 349–360. doi: 10.1016/j.immuni.2006.08.009 16979567
57. Vroon A, Kavelaars A, Limmroth V, Lombardi MS, Goebel MU, Van Dam AM, Caron MG, Sch- edlowski M, Heijnen CJ. G protein-coupled receptor kinase 2 in multiple sclerosis and experimental autoimmune encephalomyelitis. J. Immunol. 2005; 174(7): 4400–4406. doi: 10.4049/jimmunol.174.7.4400 15778405
58. Coghill ID, Brown S, Cottle DL, McGrath MJ, Robinson PA, Nandurkar HH, Dyson JM, Mitchell CA. FHL3 is an Actin-binding protein that regulates -actinin-mediated actin bundling FHL3 localizes to actin stress fibres and enhences cell spreading and stress fibre disassembly. J Biol Chem. 2003; 278(26): 24139–24152. doi: 10.1074/jbc.M213259200 12704194
59. Eydmann ME1, Knowles MA. Mutation analysis of 8p genes POLB and PPP2CB in bladder cancer. Cancer Genet Cytogenet. 1997; 93(2): 167–171. doi: 10.1016/s0165-4608(96)00200-2 9078303
60. Levy DE, Marie I, Prakash A. Ringing the interferon alarm: differential regulation of gene expression at the interface between innate and adaptive immunity. Curr Opin Immunol. 2003; 15(1): 52–58. 12495733
61. Zhang X, Shin J, Molitor TW, Schook LB, Rutherford MS. Molecular responses of macrophages to porcine reproductive and respiratory syndrome virus infection. Virology. 1999; 262(1): 152–162. doi: 10.1006/viro.1999.9914 10489349
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania