Whole blood microarray analysis of pigs showing extreme phenotypes after a porcine reproductive and respiratory syndrome virus infection

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Schroyen, Martine ^a   Steibel, Juan P ^b   Koltes, James E ^a   Choi, Igseo ^c   Raney, Nancy E ^b   Eisley, Christopher ^d   Fritz Waters, Eric ^a   Reecy, James M ^a   Dekkers, Jack C M ^a   Rowland, Robert R R ^e   Lunney, Joan K ^c   Ernst, Catherine W ^b   Tuggle, Christopher K ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d Iowa State University   (United States)

^e KANSAS STATE UNIVERSITY   (United States)

Author keywords

Immune response; Microarray; PCIT; Pig; PRRS; Transcriptomics; WGCNA

Indexed keywords

CCAAT BINDING FACTOR; INTERFERON; THIOREDOXIN INTERACTING PROTEIN; CYTOKINE; RNA;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIUM ISOLATE; BLOOD ANALYSIS; BLOOD SAMPLING; CHROMOSOME 4; ENRICHMENT CULTURE; GENE CLUSTER; GENE EXPRESSION; GENETIC REGULATION; GENOTYPE; GROWTH RATE; IMMUNE RESPONSE; MICROARRAY ANALYSIS; MYCOPLASMA HYOPNEUMONIAE; NONHUMAN; PHENOTYPE; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT LOCUS; RNA ANALYSIS; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SWINE INFLUENZA VIRUS; TRANSCRIPTOMICS; VIREMIA; VIRUS LOAD; WEIGHT GAIN; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; PROCEDURES; TISSUE MICROARRAY; VIROLOGY;

ANIMALIA; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

ANIMALS; CYTOKINES; GENE EXPRESSION; GENE EXPRESSION REGULATION; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RNA; SWINE; TISSUE ARRAY ANALYSIS; VIRAL LOAD; VIREMIA;

EID: 84936772332     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1741-8     Document Type: Article

References (62)

1. Holtkamp DJ, Kliebenstein JB, Neumann EJ, Zimmerman JJ, Rotto HF, Yoder TK, et al. Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J Swine Health Prod. 2013;21(2):72-84.
2. Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, Seitzinger AH, et al. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc. 2005;227(3):385-92.
3. Done SH, Paton DJ, White ME. Porcine reproductive and respiratory syndrome (PRRS): a review, with emphasis on pathological, virological and diagnostic aspects. Br Vet J. 1996;152(2):153-74.
4. Meulenberg JJ, Hulst MM, de Meijer EJ, Moonen PL, den Besten A, de Kluyver EP, et al. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology. 1993;192(1):62-72.
5. Lunney JK, Benfield DA, Rowland RR. Porcine reproductive and respiratory syndrome virus: an update on an emerging and re-emerging viral disease of swine. Virus Res. 2010;154(1-2):1-6.
6. Kimman TG, Cornelissen LA, Moormann RJ, Rebel JM, Stockhofe-Zurwieden N. Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine. 2009;27(28):3704-18.
7. Otake S, Dee S, Corzo C, Oliveira S, Deen J. Long-distance airborne transport of infectious PRRSV and Mycoplasma hyopneumoniae from a swine population infected with multiple viral variants. Vet Microbiol. 2010;145(3-4):198-208.
8. 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.
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):1733-46.
10. Boddicker NJ, Garrick DJ, Rowland RR, Lunney JK, Reecy JM, Dekkers JC. Validation and further characterization of a major quantitative trait locus associated with host response to experimental infection with porcine reproductive and respiratory syndrome virus. Anim Genet. 2013;45(1):48-58.
11. Boddicker NJ, Bjorkquist A, Rowland RR, Lunney JK, Reecy JM, Dekkers JC. Genome-wide association and genomic prediction for host response to porcine reproductive and respiratory syndrome virus infection. Genet Sel Evol. 2014;46:18.
12. Badaoui B, Rutigliano T, Anselmo A, Vanhee M, Nauwynck H, Giuffra E, et al. RNA-sequence analysis of primary alveolar macrophages after in vitro infection with porcine reproductive and respiratory syndrome virus strains of differing virulence. PLoS One. 2014;9(3):e91918.
13. Miller LC, Fleming D, Arbogast A, Bayles DO, Guo B, Lager KM, et al. Analysis of the swine tracheobronchial lymph node transcriptomic response to infection with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. BMC Vet Res. 2012;8:208.
14. Xiao S, Jia J, Mo D, Wang Q, Qin L, He Z, et al. Understanding PRRSV infection in porcine lung based on genome-wide transcriptome response identified by deep sequencing. PLoS One. 2010;5(6):e11377.
15. Xiao S, Mo D, Wang Q, Jia J, Qin L, Yu X, et al. Aberrant host immune response induced by highly virulent PRRSV identified by digital gene expression tag profiling. BMC Genomics. 2010;11:544.
16. Zhou P, Zhai S, Zhou X, Lin P, Jiang T, Hu X, et al. Molecular characterization of transcriptome-wide interactions between highly pathogenic porcine reproductive and respiratory syndrome virus and porcine alveolar macrophages in vivo. Int J Biol Sci. 2011;7(7):947-59.
17. Genini S, Delputte PL, Malinverni R, Cecere M, Stella A, Nauwynck HJ, et al. Genome-wide transcriptional response of primary alveolar macrophages following infection with porcine reproductive and respiratory syndrome virus. J Gen Virol. 2008;89(Pt 10):2550-64.
18. 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.
19. 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):437-48.
20. Bates JS, Petry DB, Eudy J, Bough L, Johnson RK. Differential expression in lung and bronchial lymph node of pigs with high and low responses to infection with porcine reproductive and respiratory syndrome virus. J Anim Sci. 2008;86(12):3279-89.
21. Wysocki M, Chen H, Steibel JP, Kuhar D, Petry D, Bates J, et al. Identifying putative candidate genes and pathways involved in immune responses to porcine reproductive and respiratory syndrome virus (PRRSV) infection. Anim Genet. 2012;43(3):328-32.
22. Arceo ME, Ernst CW, Lunney JK, Choi I, Raney NE, Huang T, et al. Characterizing differential individual response to porcine reproductive and respiratory syndrome virus infection through statistical and functional analysis of gene expression. Front Genet. 2012;3:321.
23. Steibel JP, Wysocki M, Lunney JK, Ramos AM, Hu ZL, Rothschild MF, et al. Assessment of the swine protein-annotated oligonucleotide microarray. Anim Genet. 2009;40(6):883-93.
24. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.
25. Reverter A, Chan EK. Combining partial correlation and an information theory approach to the reversed engineering of gene co-expression networks. Bioinformatics. 2008;24(21):2491-7.
26. 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.
27. Steibel JP, Rosa GJ. On reference designs for microarray experiments. Stat Appl Genet Mol Biol. 2005;4:Article36.
28. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics. 2007;23(20):2700-7.
29. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, et al. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 2002;30(4):e15.
30. R Development Core Team. R: A lanuage and environment for statistical comupting. Vienna, Austria: R Foundation for Statistical Computing; 2010.
31. 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. New York, NY: Springer; 2005. p. 397-420.
32. Rosa GJ, Steibel JP, Tempelman RJ. Reassessing design and analysis of two-colour microarray experiments using mixed effects models. Comp Funct Genomics. 2005;6(3):123-31.
33. Storey JD. The positive false discovery rate: A Bayesian interpretation and the q-value. Ann Stat. 2003;31(6):2013-35.
34. Eisley C, Fritz-Waters E, Choi I, Koltes J, Boddicker N, Reecy J, Lunney J, Carpenter S, Tuggle C, Liu P, Dekkers J: Analysis of gene expression in a region associated with host response to porcine reproductive and respiratory syndrome virus challenge. In: Plant & Animal Genome XXII, San Diego, CA; 2014 https://pagconfexcom/pag/xxii/webprogram/Paper10997html.
35. Koltes JE, Fritz-Water E, Eisley CJ, Choi I, Bao H, Kommadath A, et al. Identification of a putative quantitative trait nucleotide in Guanylate Binding Protein 5 for host response to PRRS virus infection. BMC Genomics. 2015;16:412.
36. Langfelder P, Horvath S. Fast R Functions for Robust Correlations and Hierarchical Clustering. J Stat Softw. 2012;46(11):i11.
37. Langfelder P, Horvath S. Eigengene networks for studying the relationships between co-expression modules. BMC Syst Biol. 2007;1:54.
38. Shoemaker JE, Lopes TJ, Ghosh S, Matsuoka Y, Kawaoka Y, Kitano H. CTen: a web-based platform for identifying enriched cell types from heterogeneous microarray data. BMC Genomics. 2012;13:460.
39. Koesterke L, Milfeld K, Vaughn M, Stanzione D, Koltes J, Weeks N, et al. Optimizing the PCIT algorithm on stampede's Xeon and Xeon Phi processors for faster discovery of biological networks. In: Proceedings of the Conference on Extreme Science and Engineering Discovery Environment: Gateway to Discovery. 2013. p. 2013.
40. Koesterke L, Koltes J, Weeks N, Milfeld K, Vaughn M, Reecy J, et al. Discovery of biological networks using an optimized partial correlation coefficient with information theory algorthim on Stampede's Xeon and Xeons Phi processors. Concurrency Computation Prac Experience. 2014;26:2178-90.
41. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.
42. Freeman TC, Goldovsky L, Brosch M, van Dongen S, Maziere P, Grocock RJ, et al. Construction, visualisation, and clustering of transcription networks from microarray expression data. PLoS Comput Biol. 2007;3(10):2032-42.
43. Liu S, Lin L, Jiang P, Wang D, Xing Y. A comparison of RNA-Seq and high-density exon array for detecting differential gene expression between closely related species. Nucleic Acids Res. 2011;39(2):578-88.
44. Sirbu A, Kerr G, Crane M, Ruskin HJ. RNA-Seq vs dual- and single-channel microarray data: sensitivity analysis for differential expression and clustering. PLoS One. 2012;7(12):e50986.
45. Zhao S, Fung-Leung WP, Bittner A, Ngo K, Liu X. Comparison of RNA-Seq and microarray in transcriptome profiling of activated T cells. PLoS One. 2014;9(1):e78644.
46. Fuller TF, Ghazalpour A, Aten JE, Drake TA, Lusis AJ, Horvath S. Weighted gene coexpression network analysis strategies applied to mouse weight. Mamm Genome. 2007;18(6-7):463-72.
47. Van Gucht S, Van Reeth K, Nauwynck H, Pensaert M. Porcine reproductive and respiratory syndrome virus infection increases CD14 expression and lipopolysaccharide-binding protein in the lungs of pigs. Viral Immunol. 2005;18(1):116-26.
48. Costers S, Lefebvre DJ, Delputte PL, Nauwynck HJ. Porcine reproductive and respiratory syndrome virus modulates apoptosis during replication in alveolar macrophages. Arch Virol. 2008;153(8):1453-65.
49. Teodoro JG, Branton PE. Regulation of apoptosis by viral gene products. J Virol. 1997;71(3):1739-46.
50. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805-20.
51. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol. 2011;1(6):519-25.
52. Dawson HD, Loveland JE, Pascal G, Gilbert JG, Uenishi H, Mann KM, et al. Structural and functional annotation of the porcine immunome. BMC Genomics. 2013;14:332.
53. Miller LC, Laegreid WW, Bono JL, Chitko-McKown CG, Fox JM. Interferon type I response in porcine reproductive and respiratory syndrome virus-infected MARC-145 cells. Arch Virol. 2004;149(12):2453-63.
54. Van Reeth K, Labarque G, Nauwynck H, Pensaert M. Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity. Res Vet Sci. 1999;67(1):47-52.
55. Souza C, Choi I, Araujo K, Abrams S, Kerrigan M, Rowland RR, Lunney J: Comparative serum immune responses of pigs after a challenge with porcine reproductive and respiratory syndrome virus (PRRSV). In: Proceedings of the 10th IVIS International Veterinary Immunology Symposium, P0514: 2013; Milan, Italy; 2013, www.ivis2013.org/allegati/Abstract_book.pdf .
56. Hulst M, Loeffen W, Weesendorp E. Pathway analysis in blood cells of pigs infected with classical swine fever virus: comparison of pigs that develop a chronic form of infection or recover. Arch Virol. 2013;158(2):325-39.
57. Rauw WM. Immune response from a resource allocation perspective. Front Genet. 2012;3:267.
58. Tschopp J, Schroder K. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat Rev Immunol. 2010;10(3):210-5.
59. Bi J, Song S, Fang L, Wang D, Jing H, Gao L, et al. Porcine reproductive and respiratory syndrome virus induces IL-1beta production depending on TLR4/MyD88 pathway and NLRP3 inflammasome in primary porcine alveolar macrophages. Mediators Inflamm. 2014;2014:403515.
60. Lee CC, Freinkman E, Sabatini DM, Ploegh HL. The protein synthesis inhibitor blasticidin s enters mammalian cells via leucine-rich repeat-containing protein 8D. J Biol Chem. 2014;289(24):17124-31.
61. Pilla DM, Hagar JA, Haldar AK, Mason AK, Degrandi D, Pfeffer K, et al. Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc Natl Acad Sci U S A. 2014;111(16):6046-51.
62. Wagner E, Frank MM. Therapeutic potential of complement modulation. Nat Rev Drug Discov. 2010;9(1):43-56.