Leukocyte transcriptome from chickens infected with avian pathogenic Escherichia coli identifies pathways associated with resistance

Results in Immunology

Volumn 2, Issue , 2012, Pages 44-53

  Sandford, Erin E ^a   Orr, Megan ^b   Shelby, Mandy ^a   Li, Xianyao ^c   Zhou, Huaijun ^c   Johnson, Timothy J ^d   Kariyawasam, Subhashinie ^e   Liu, Peng ^b   Nolan, Lisa K ^a   Lamont, Susan J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Iowa State University   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Avian pathogenic Escherichia coli; Chicken; Immune resp nse; Leukocytes; Microarray; Transcriptome

Indexed keywords

ESCHERICHIA COLI VACCINE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AVIAN COLIBACILLOSIS; AVIAN PATHOGENIC ESCHERICHIA COLI; CHICKEN; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC RESISTANCE; GENETIC SELECTION; IMMUNE RESPONSE; LEUKOCYTE; MALE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; UPREGULATION; VACCINATION;

EID: 84867304729     PISSN: None     EISSN: 22112839     Source Type: Journal    
DOI: 10.1016/j.rinim.2012.02.003     Document Type: Article

References (73)

1. Abasht B., Kaiser M.G., Lamont S.J. Toll-like receptor gene expression in cecum and spleen of advanced intercross line chicks infected with Salmonella enterica serovar Enteritidis. Veterinary Immunology and Immunopathology 2008, 123:314-323.
2. Ask B., van der Waaij E.H., Stegeman J.A., van Arendonk J.A. Genetic variation among broiler genotypes in susceptibility to colibacillosis. Poultry Science 2006, 85:415-421.
3. Barker K.A., Hampe A., Stoeckle M.Y., Hanafusa H. Transformation-associated cytokine 9E3/CEF4 is chemotactic for chicken peripheral blood mononuclear cells. Journal of Virology 1993, 67:3528-3533.
4. Barnes H.J., Nolan L.K., Vaillancourt J.P. Colibacillosis. Diseases of Poultry 2008, 691-732. Blackwell Publishing, Ames, Iowa. twelfth ed. Y.M. Saif (Ed.).
5. Barrett T., Troup D.B., Wilhite S.E., Ledoux R., Rudnev D., Evangelista C., et al. NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Research 2009, 37:D5-D15.
6. Bastiani M., Vidotto M.C., Horn F. An avian pathogenic Escherichia coli isolate induces caspase 3/7 activation in J774 macrophages. FEMS Microbiology Letters 2005, 253:133-140.
7. Bisaillon J.R., Meek A.H., Feltmate T.E. An assessment of condemnations of broiler chicken carcasses. Canadian Journal of Veterinary Research 1988, 52:269-276.
8. Brownlie R., Allan B. Avian toll-like receptors. Cell and Tissue Research 2011, 343:121-130.
9. Brownlie R., Zhu J., Allan B., Mutwiri G.K., Babiuk L.A., Potter A., et al. Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Molecular Immunology 2009, 46:3163-3170.
10. Cavero D., Schmutz M., Philipp H.C., Preisinger R. Breeding to reduce susceptibility to Escherichia coli in layers. Poultry Science 2009, 88:2063-2068.
11. Ciraci C., Lamont S.J. Avian-specific TLRs and downstream effector responses to CpG-induction in chicken macrophages. Developmental and Comparative Immunology 2011, 35:392-398.
12. Ciraci C., Tuggle C.K., Wannemuehler M.J., Nettleton D., Lamont S.J. Unique genome-wide transcriptome profiles of chicken macrophages exposed to Salmonella-derived endotoxin. BMC Genomics 2010, 11:545.
13. Chiang H.I., Swaggerty C.L., Kogut M.H., Dowd S.E., Li X., Pevzner I.Y., et al. Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44K Agilent microarray. BMC Genomics 2008, 9:526.
14. Chuammitri P., Ostojik J., Andreasen C.B., Redmond S.B., Lamont S.J., Palik D. Chicken heterophil extracellular traps (HETs): novel defense mechanism of chicken heterophils. Veterinary Immunology and Immunopathology 2009, 129:126-131.
15. Crowley T.M., Haring V.R., Moore R. Chicken anemia virus: an understanding of the in-vitro host response over time. Viral Immunology 2011, 24:3-9.
16. Dalgaard T.S., Norup L.R., Pedersen A.R., Handberg K.J., Jørgensen P.H., Juul-Madsen H.R. Flow cytometric assessment of chicken T cell-mediated immune responses after Newcastle disease virus vaccination and challenge. Vaccine 2010, 28:4506-4514.
17. Dudoit S., Yang Y.H., Callow M.J., Speed T.P. Statistical methods for identifying differentially expressed genes in replicated cDNA microarray experiments. Statistica Sinica 2002, 12:111-139.
18. Dziva F., Stevens M.P. Colibacillosis in poultry: unravelling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts. Avian Pathology 2008, 37:355-366.
19. Edgar R., Domrachey M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research 2002, 30:207-210.
20. Erf G.F. Cell-mediated immunity in poultry. Poultry Science 2004, 83:580-590.
21. Ewers C., Li G., Wilking H., KieΒling S., Alt K., Antáo E.M., et al. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they?. International Journal of Medical Microbiology 2007, 297:163-176.
22. Farnell M.B., Donoghue A.M., de Los Santos F.S., Blore P.J., Hargis B.M., Tellez G., et al. Upregulation of oxidative burst and degranulation in chicken heterophils stimulated with probiotic bacteria. Poultry Science 2006, 85:1900-1906.
23. Gastman B.R., Johnson D.E., Whiteside T.L., Rabinowich H. Caspase-mediated degradation of T-cell receptor ζ-chain. Cancer Research 1999, 59:1422-1427.
24. George T.C., Bilsborough J., Viney J.L., Norment A.M. High antigen dose and activated dendritic cells enable Th cells to escape regulatory T cell-mediated suppression in vitro. European Journal of Immunology 2003, 33:502-511.
25. Göbel T.W., Bolliger L. The chicken TCR ζ-chain restores the function of a mouse T cell hybridoma. Journal of Immunology 1998, 160:1552-1554.
26. Göbel T.W., Fluri M. Identification and analysis of the chicken CD3ε gene. European Journal of Immunology 1997, 27:194-198.
27. Hangalapura B.N., Kaiser M.G., Poel J.J., Parmentier H.K., Lamont S.J. Cold stress equally enhances in vivo pro-inflammatory cytokine gene expression in chicken lines divergently selected for antibody responses. Developmental and Comparative Immunology 2006, 30:503-511.
28. Harmon B.G. Avian heterophils in inflammation and disease resistance. Poultry Science 1998, 77:972-977.
29. Hasenstein J.R., Lamont S.J. Chicken gallinacin gene cluster associated with Salmonella response in advanced intercross line. Avian Diseases 2007, 51:561-567.
30. Hasenstein J.R., Zhang G., Lamont S.J. Analysis of five gallinacin genes and the Salmonella enterica serovar Enteritidis response in poultry. Infection and Immunity 2006, 74:3375-3380.
31. Higgs R., Cormican P., Cahalane S., Allan B., Lloyd A.T., Meade K., et al. Induction of a novel chicken toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infection and Immunity 2006, 74:1692-1698.
32. Huang D.W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths towards the comprehensive functional analysis of large gene lists. Nucleic Acids Research 2009, 37:1-13.
33. Huang D.W., Sherman B.T., Lempicki R.A. Systemic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 2009, 4:44-57.
34. Husebye H., Aune M.H., Stenvik J., Samstad E., Skeldal F., Halaas O., et al. The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory facor-3 on phagosomes. Immunity 2010, 33:583-596.
35. Jakobsen L., Spangholm D.J., Pedersen K., Jensen L.B., Emborg H.D., Agersø Y., et al. Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. International Journal of Food Microbiology 2010, 142:264-272.
36. Johnson T.J., Siek K.E., Johnson S.J., Nolan L.K. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. Journal of Bacteriology 2006, 188:745-758.
37. Johnson T.J., Kariyawasam S., Wannamuehler Y., Mangiamele P., Johnson S.J., Doetkott C., et al. The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. Journal of Bacteriology 2007, 189:3228-3236.
38. Kaiser P., Rothwell L., Galyov E.E., Barrow P.A., Burnside J., Wigley P. Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiology 2000, 12:3217-3226.
39. Kannan L., Liyanage R., Lay J.O., Rath N.C. Evaluation of beta defensin 2 production by chicken heterophils using direct MALDI mass spectrometry. Molecular Immunology 2009, 46:3151-3156.
40. Koskinen R., Salomonsen J., Tregaskes C.A., Young J.R., Goodchild M., Bumstead N., et al. The chicken CD4 gene has remained conserved in evolution. Immunogenetics 2002, 54:520-525.
41. Kottom T.J., Nolan L.K., Robinson M., Brown J., Gustad T., Horne S.M., et al. Further characterization of a complement-sensitive mutant of a virulent avian Escherichia coli isolate. Avian Diseases 1997, 41:817-823.
42. Li G., Tivendale K.A., Liu P., Feng Y., Wannemuehler Y., Cai W., et al. Transcriptome analysis of avian pathogenic Escherichia coli O1 in chicken serum reveals adaptive responses to systemic infection. Infection and Immunity 2011, 79:1951-1960.
43. Li X., Chiang H.I., Zhu J., Dowd S.E., Zhou H. Characterization of a newly developed chicken 44K Agilent microarray. BMC Genomics 2008, 9:60.
44. Li X., Swaggerty C.L., Kogut M.H., Chiang H.I., Wang Y., Genovese K.J., et al. Gene expression profiling of the local cecal response of genetic chicken lines that differ in their susceptibility to Campylobacter jejuni colonization. PLoS One 2010, 5:e11827.
45. Li Y.D., Liu Y.P., Cao D.M., Yan Y.M., Hou Y.N., Zhao J.Y., et al. Induction of small G protein RhoB by non-genotoxic stress inhibits apoptosis and activates NF-κB. Journal of Cellular Physiology 2011, 226:729-738.
46. Lu Y., Sarson A.J., Gong J., Zhou H., Zhu W., Kang Z., et al. Expression profiles of genes in Toll-like receptor-mediated signaling of broiler infected with Clostridium perfringens. Clinical and Vaccine Immunology 2009, 16:1639-1647.
47. Lutful Kabir S.M. Avian colibacillosis and salmonellosis: a closer look at epideminology, pathogenesis, diagnosis, control and public health concerns. International Journal of Environmental Research and Public Health 2010, 7:89-114.
48. Lynne A.M., Foley S.L., Nolan L.K. Immune response to recombinant Escherichia coli Iss protein in poultry. Avian Diseases 2006, 50:273-276.
49. Maréchal Y., Pesesse X., Jia Y., Pouillon V., Pérez-Morga D., Daniel J., et al. Inositol 1,3,4,5-tetrakisphosphate controls proapoptotic Bim gene expression and survival in B cells. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:13978-13983.
50. Mellata M., Dho-Moulin M., Dozois C.M., Curtiss R., Lehoux B., Fairbrother J.M. Role of avian pathogenic Escherichia coli virulence factors in bacterial interaction with chicken heterophils and macrophages. Infection and Immunity 2003, 71:494-503.
51. Moulin-Schouleur M., Schouler C., Tailliez P., Kao M.R., Bree A., Germon P., et al. Common virulence factors and genetic relationships between O18:K1:H7 Escherichia coli isolates of human and avian origin. Journal of Clinical Microbiology 2006, 44:3484-3492.
52. Mukhopadhyay S., Plüddemann A., Hoe J.C., Williams K.J., Varin A., Makepeace K., et al. Immune inhibitory ligand CD200 induction by TLRs and NLRs limits macrophage activation to protect the host from menigococcal septicemia. Cell Host and Microbe 2010, 8:236-247.
53. Nerren J.R., Swaggerty C.L., MacKinnon K.M., Genovese K.J., He H., Pevzner I., et al. Differential mRNA expression of the avian-specific toll-like receptor 15 between heterophils from Salmonella-susceptible and -resistant chickens. Immunogenetics 2009, 61:71-77.
54. Nolan L.K., Horne S.M., Giddings C.W., Foley S.L., Johnson T.J., Lynne A.M., et al. Resistance to serum complement, iss, and virulence of avian Escherichia coli. Veterinary Research Communications 2003, 27:101-110.
55. Peighambari S.M., Julian R.J., Gyles C.L. Experimental Escherichia coli respiratory infection in broilers. Avian Diseases 2000, 44:759-769.
56. Pfaff-McDonough S.J., Horne S.M., Giddings C.W., Doetkott J.O., Smith M.H., Nolan L.K. Complement resistance-related traits among Escherichia coli isolates from apparently healthy birds and birds with colibacillosis. Avian Diseases 2000, 44:23-33.
57. Quéré P., Rivas C., Ester K., Novak R., Ragland W.L. Abundance of IFN-α and IFN-γ mRNA in blood of resistant and susceptible chickens infected with Marek's disease virus (MDV) or vaccinated with turkey herpesvirus; and MDV inhibition of subsequent induction of IFN gene transcription. Archives of Virology 2005, 150:507-519.
58. Qureshi M.A. Avian macrophage and immune response: an overview. Poultry Science 2003, 82:691-698.
59. Redmond S.B., Chuammitri P., Andreasen C.B., Palik D., Lamont S.J. Chicken heterophils from commercially selected and non-selected genetic lines express cytokines differently after in vitro exposure to Salmonella enteritidis. Veterinary Immunology and Immunopathology 2009, 1132:129-134.
60. Rodrigues-Siek K.E., Gidding C.W., Doetkott C., Johnson T.J., Fakhr M.K., Nolan L.K. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 2005, 151:2097-2110.
61. Rodrigues-Siek K.E., Gidding C.W., Doetkott C., Johnson T.J., Nolan L.K. Characterizing the APEC pathotype. Veterinary Research 2005, 36:241-256.
62. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biology programmers. Methods in Molecular Biology 2000, 132:365-386.
63. Russell S.M. The effect of airsacculitis on bird weights, uniformity, fecal contamination, processing errors, and populations of Campylobacter spp. and Escherichia coli. Poultry Science 2003, 82:1326-1331.
64. Sandford E.E., Orr M., Balfanz E., Bowerman N., Li X., Zhou H., et al. Spleen transcriptome response to infection with avian pathogenic Escherichia coli in broiler chickens. BMC Genomics 2011, 12:469.
65. Schokker D., Smits M.A., Hoekman A.J., Parmentier H.K., Rebel J.M. Effects of Salmonella on spatial-temporal processes of jejunal development in chickens. Developmental and Comparative Immunology 2010, 34:1090-1100.
66. Sharma J.M. Host factors for disease resistance. Diseases of Poultry 2008, 47-58. Blackwell Publishing, Ames, Iowa. twelfth ed. Y.M. Saif (Ed.).
67. Storey J.D., Tibshirani R. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:9440-9445.
68. Swaggerty C.L., Pevzner I.Y., Kaiser P., Kogut M.H. Profiling pro-inflammatory cytokine and chemokine mRNA expression levels as a novel method for selection of increased innate immune responsiveness. Veterinary Immunology and Immunopathology 2008, 126:35-42.
69. Tivendale K.A., Logue C.M., Kariyawasam S., Jordan D., Hussein A., Li G., et al. Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infection and Immunity 2010, 78:3412-3419.
70. van Dijk A., Veldhuizen E.J., Haagsman H.P. Avian defensins. Veterinary Immunology and Immunopathology 2008, 124:1-18.
71. Viertlboeck B.C., Hanczaruk M.A., Schmitt F.C., Schmitt R., Göbel T.W. Characterization of the chicken CD200 receptor family. Molecular Immunology 2008, 45:2097-2105.
72. Wennerberg K., Rossman K.L., Der C.J. The Ras superfamily at a glance. Journal of Cell Science 2005, 118:843-846.
73. Zhou H., Lamont S.J. Global gene expression profile after Salmonella enterica Serovar enteritidis challenge in two F8 advanced intercross chicken lines. Cytogenetic and Genome Research 2007, 117:131-138.