Gene expression in the chicken caecum in response to infections with non-typhoid Salmonella

. 2014 Dec 05 ; 45 (1) : 119. [epub] 20141205

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid25475706

Chickens can be infected with Salmonella enterica at any time during their life. However, infections within the first hours and days of their life are epidemiologically the most important, as newly hatched chickens are highly sensitive to Salmonella infection. Salmonella is initially recognized in the chicken caecum by TLR receptors and this recognition is followed by induction of chemokines, cytokines and many effector genes. This results in infiltration of heterophils, macrophages, B- and T-lymphocytes and changes in total gene expression in the caecal lamina propria. The highest induction in expression is observed for matrix metalloproteinase 7 (MMP7). Expression of this gene is increased in the chicken caecum over 4000 fold during the first 10 days after the infection of newly hatched chickens. Additional highly inducible genes in the caecum following S. Enteritidis infection include immune responsive gene 1 (IRG1), serum amyloid A (SAA), extracellular fatty acid binding protein (ExFABP), serine protease inhibitor (SERPINB10), trappin 6-like (TRAP6), calprotectin (MRP126), mitochondrial ES1 protein homolog (ES1), interferon-induced protein with tetratricopeptide repeats 5 (IFIT5), avidin (AVD) and transglutaminase 4 (TGM4). The induction of expression of these proteins exceeds a factor of 50. Similar induction rates are also observed for chemokines and cytokines such as IL1β, IL6, IL8, IL17, IL18, IL22, IFNγ, AH221 or iNOS. Once the infection is under control, which happens approx. 2 weeks after infection, expression of IgY and IgA increases to facilitate Salmonella elimination from the gut lumen. This review outlines the function of individual proteins expressed in chickens after infection with non-typhoid Salmonella serovars.

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Withanage GS, Kaiser P, Wigley P, Powers C, Mastroeni P, Brooks H, Barrow P, Smith A, Maskell D, McConnell I. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar typhimurium. Infect Immun. 2004;72:2152–2159. doi: 10.1128/IAI.72.4.2152-2159.2004. PubMed DOI PMC

Beal RK, Wigley P, Powers C, Hulme SD, Barrow PA, Smith AL. Age at primary infection with Salmonella enterica serovar Typhimurium in the chicken influences persistence of infection and subsequent immunity to re-challenge. Vet Immunol Immunopathol. 2004;100:151–164. doi: 10.1016/j.vetimm.2004.04.005. PubMed DOI

Beal RK, Powers C, Wigley P, Barrow PA, Kaiser P, Smith AL. A strong antigen-specific T-cell response is associated with age and genetically dependent resistance to avian enteric salmonellosis. Infect Immun. 2005;73:7509–7516. doi: 10.1128/IAI.73.11.7509-7516.2005. PubMed DOI PMC

de Freitas Neto OC, Setta A, Imre A, Bukovinski A, Elazomi A, Kaiser P, Berchieri A, Jr, Barrow P, Jones M. A flagellated motile Salmonella Gallinarum mutant (SG Fla+) elicits a pro-inflammatory response from avian epithelial cells and macrophages and is less virulent to chickens. Vet Microbiol. 2013;165:425–433. doi: 10.1016/j.vetmic.2013.04.015. PubMed DOI

Wigley P, Hulme SD, Powers C, Beal RK, Berchieri A, Jr, Smith A, Barrow P. Infection of the reproductive tract and eggs with Salmonella enterica serovar pullorum in the chicken is associated with suppression of cellular immunity at sexual maturity. Infect Immun. 2005;73:2986–2990. doi: 10.1128/IAI.73.5.2986-2990.2005. PubMed DOI PMC

Clayton DJ, Bowen AJ, Hulme SD, Buckley AM, Deacon VL, Thomson NR, Barrow PA, Morgan E, Jones MA, Watson M, Stevens MP: Analysis of the role of 13 major fimbrial subunits in colonisation of the chicken intestines bySalmonella entericaserovar Enteritidis reveals a role for a novel locus.BMC Microbiol 2008, 8:228. PubMed PMC

Chaudhuri RR, Morgan E, Peters SE, Pleasance SJ, Hudson DL, Davies HM, Wang J, van Diemen PM, Buckley AM, Bowen AJ, Pullinger GD, Turner DJ, Langridge GC, Turner AK, Parkhill J, Charles IG, Maskell DJ, Stevens MP: Comprehensive assignment of roles forSalmonellaTyphimurium genes in intestinal colonization of food-producing animals.PLoS Genet 2013, 9:e1003456. PubMed PMC

Rychlik I, Lovell MA, Barrow PA. The presence of genes homologous to the K88 genes faeH and faeI on the virulence plasmid of Salmonella Gallinarum. FEMS Microbiol Lett. 1998;159:255–260. doi: 10.1111/j.1574-6968.1998.tb12869.x. PubMed DOI

Kuzminska-Bajor M, Kuczkowski M, Grzymajlo K, Wojciech L, Sabat M, Kisiela D, Wieliczko A, Ugorski M. Decreased colonization of chicks by Salmonella enterica serovar Gallinarum expressing mannose-sensitive FimH adhesin from Salmonella enterica serovar Enteritidis. Vet Microbiol. 2012;158:205–210. doi: 10.1016/j.vetmic.2012.01.029. PubMed DOI

Misselwitz B, Kreibich SK, Rout S, Stecher B, Periaswamy B, Hardt WD. Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun. 2011;79:330–341. doi: 10.1128/IAI.00581-10. PubMed DOI PMC

Kaniga K, Trollinger D, Galan JE. Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J Bacteriol. 1995;177:7078–7085. PubMed PMC

Matulova M, Varmuzova K, Sisak F, Havlickova H, Babak V, Stejskal K, Zdrahal Z, Rychlik I: Chicken innate immune response to oral infection withSalmonella entericaserovar Enteritidis.Vet Res 2013, 44:37. PubMed PMC

Shea JE, Hensel M, Gleeson C, Holden DW. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1996;93:2593–2597. doi: 10.1073/pnas.93.6.2593. PubMed DOI PMC

Pavlova B, Volf J, Ondrackova P, Matiasovic J, Stepanova H, Crhanova M, Karasova D, Faldyna M, Rychlik I: SPI-1-encoded type III secretion system ofSalmonella entericais required for the suppression of porcine alveolar macrophage cytokine expression.Vet Res 2011, 42:16. PubMed PMC

Monack DM, Raupach B, Hromockyj AE, Falkow S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci U S A. 1996;93:9833–9838. doi: 10.1073/pnas.93.18.9833. PubMed DOI PMC

Rychlik I, Karasova D, Sebkova A, Volf J, Sisak F, Havlickova H, Kummer V, Imre A, Szmolka A, Nagy B: Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) ofSalmonella entericaserovar Enteritidis for chickens.BMC Microbiol 2009, 9:268. PubMed PMC

Dieye Y, Ameiss K, Mellata M, Curtiss R 3rd: TheSalmonellaPathogenicity Island (SPI) 1 contributes more than SPI2 to the colonization of the chicken bySalmonella entericaserovar Typhimurium.BMC Microbiol 2009, 9:3. PubMed PMC

Karasova D, Sebkova A, Havlickova H, Sisak F, Volf J, Faldyna M, Ondrackova P, Kummer V, Rychlik I: Influence of 5 majorSalmonellapathogenicity islands on NK cell depletion in mice infected withSalmonella entericaserovar Enteritidis.BMC Microbiol 2010, 10:75. PubMed PMC

van der Heijden J, Finlay BB. Type III effector-mediated processes in Salmonella infection. Future Microbiol. 2012;7:685–703. doi: 10.2217/fmb.12.49. PubMed DOI

Gewirtz AT, Siber AM, Madara JL, McCormick BA. Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect Immun. 1999;67:608–617. PubMed PMC

Keestra MA, Winter MG, Klein-Douwel D, Xavier MN, Winter SE, Kim A, Tsolis RM, Bäumler AJ. A Salmonella virulence factor activates the NOD1/NOD2 signaling pathway. MBio. 2011;2:e00266–11. PubMed PMC

Haraga A, Miller SI. A Salmonella enterica serovar Typhimurium translocated leucine-rich repeat effector protein inhibits NF-κB-dependent gene expression. Infect Immun. 2003;71:4052–4058. doi: 10.1128/IAI.71.7.4052-4058.2003. PubMed DOI PMC

St Paul M, Brisbin JT, Abdul-Careem MF, Sharif S. Immunostimulatory properties of Toll-like receptor ligands in chickens. Vet Immunol Immunopathol. 2013;152:191–199. doi: 10.1016/j.vetimm.2012.10.013. PubMed DOI

MacKinnon KM, He H, Nerren JR, Swaggerty CL, Genovese KJ, Kogut MH. Expression profile of toll-like receptors within the gastrointestinal tract of 2-day-old Salmonella enteriditis-infected broiler chickens. Vet Microbiol. 2009;137:313–319. doi: 10.1016/j.vetmic.2009.01.024. PubMed DOI

Genovese KJ, He H, Swaggerty CL, Kogut MH. The avian heterophil. Dev Comp Immunol. 2013;41:334–340. doi: 10.1016/j.dci.2013.03.021. PubMed DOI

Swaggerty CL, Kogut MH, Ferro PJ, Rothwell L, Pevzner IY, Kaiser P. Differential cytokine mRNA expression in heterophils isolated from Salmonella-resistant and -susceptible chickens. Immunology. 2004;113:139–148. doi: 10.1111/j.1365-2567.2004.01939.x. PubMed DOI PMC

Iqbal M, Philbin VJ, Withanage GS, Wigley P, Beal RK, Goodchild MJ, Barrow P, McConnell I, Maskell DJ, Young J, Bumstead N, Boyd Y, Smith AL. Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar typhimurium. Infect Immun. 2005;73:2344–2350. doi: 10.1128/IAI.73.4.2344-2350.2005. PubMed DOI PMC

Pan Z, Cong Q, Geng S, Fang Q, Kang X, You M, Jiao X. Flagellin from recombinant attenuated Salmonella enterica serovar Typhimurium reveals a fundamental role in chicken innate immunity. Clin Vaccine Immunol. 2012;19:304–312. doi: 10.1128/CVI.05569-11. PubMed DOI PMC

McNeilly TN, Mitchell MC, Nisbet AJ, McAteer S, Erridge C, Inglis NF, Smith DG, Low JC, Gally DL, Huntley JF, Mahajan A. IgA and IgG antibody responses following systemic immunization of cattle with native H7 flagellin differ in epitope recognition and capacity to neutralise TLR5 signalling. Vaccine. 2010;28:1412–1421. doi: 10.1016/j.vaccine.2009.10.148. PubMed DOI

Matulova M, Havlickova H, Sisak F, Rychlik I: Vaccination of chickens with SPI1-lon and SPI1-lon-fliC mutant ofSalmonella entericaSerovar Enteritidis.PLoS One 2013, 8:e66172. PubMed PMC

Berndt A, Wilhelm A, Jugert C, Pieper J, Sachse K, Methner U. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect Immun. 2007;75:5993–6007. doi: 10.1128/IAI.00695-07. PubMed DOI PMC

Crhanova M, Hradecka H, Faldynova M, Matulova M, Havlickova H, Sisak F, Rychlik I. Immune response of chicken gut to natural colonization by gut microflora and to Salmonella enterica serovar Enteritidis infection. Infect Immun. 2011;79:2755–2763. doi: 10.1128/IAI.01375-10. PubMed DOI PMC

Van Immerseel F, De Buck J, De SI, Mast J, Haesebrouck F, Ducatelle R. Dynamics of immune cell infiltration in the caecal lamina propria of chickens after neonatal infection with a Salmonella Enteritidis strain. Dev Comp Immunol. 2002;26:355–364. doi: 10.1016/S0145-305X(01)00084-2. PubMed DOI

Ivanov II, Frutos RL, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008;4:337–349. doi: 10.1016/j.chom.2008.09.009. PubMed DOI PMC

Eyerich S, Eyerich K, Cavani A, Schmidt-Weber C. IL-17 and IL-22: siblings, not twins. Trends Immunol. 2010;31:354–361. doi: 10.1016/j.it.2010.06.004. PubMed DOI

He H, Genovese KJ, Kogut MH. Modulation of chicken macrophage effector function by T(H)1/T(H)2 cytokines. Cytokine. 2011;53:363–369. doi: 10.1016/j.cyto.2010.12.009. PubMed DOI

Matulova M, Rajova J, Vlasatikova L, Volf J, Stepanova H, Havlickova H, Sisak F, Rychlik I: Characterization of chicken spleen transcriptome after infection withSalmonella entericaserovar Enteritidis.PLoS One 2012, 7:e48101. PubMed PMC

Matulova M, Stepanova H, Sisak F, Havlickova H, Faldynova M, Kyrova K, Volf J, Rychlik I: Cytokine signaling in splenic leukocytes from vaccinated and non-vaccinated chickens after intravenous infection withSalmonellaEnteritidis.PLoS One 2012, 7:e32346. PubMed PMC

Kogut MH, He H, Genovese KJ. Bacterial toll-like receptor agonists induce sequential NF-kappaB-mediated leukotriene B4 and prostaglandin E2 production in chicken heterophils. Vet Immunol Immunopathol. 2012;145:159–170. doi: 10.1016/j.vetimm.2011.11.003. PubMed DOI

Schokker D, Smits MA, Hoekman AJ, Parmentier HK, Rebel JM. Effects of Salmonella on spatial-temporal processes of jejunal development in chickens. Dev Comp Immunol. 2010;34:1090–1100. doi: 10.1016/j.dci.2010.05.013. PubMed DOI

Coble DJ, Sandford EE, Ji T, Abernathy J, Fleming D, Zhou H, Lamont SJ: Impacts ofSalmonellaEnteritidis infection on liver transcriptome in broilers.Genesis. in press. PubMed

Varmuzova K, Matulova ME, Sebkova A, Sekelova Z, Havlickova H, Sisak F, Babak V, Rychlik I: The early innate response of chickens toSalmonella entericais dependent on the presence of O-antigen but not on serovar classification.PLoS One 2014, 9:e96116. PubMed PMC

Matulova M, Havlickova H, Sisak F, Babak V, Rychlik I. SPI1 defective mutants of Salmonella enterica induce cross-protective immunity in chickens against challenge with serovars Typhimurium and Enteritidis. Vaccine. 2013;31:3156–3162. doi: 10.1016/j.vaccine.2013.05.002. PubMed DOI

Puthenedam M, Wu F, Shetye A, Michaels A, Rhee KJ, Kwon JH. Matrilysin-1 (MMP7) cleaves galectin-3 and inhibits wound healing in intestinal epithelial cells. Inflamm Bowel Dis. 2011;17:260–267. doi: 10.1002/ibd.21443. PubMed DOI PMC

Kita H, Hikichi Y, Hikami K, Tsuneyama K, Cui ZG, Osawa H, Ohnishi H, Mutoh H, Hoshino H, Bowlus CL, Yamamoto H, Sugano K. Differential gene expression between flat adenoma and normal mucosa in the colon in a microarray analysis. J Gastroenterol. 2006;41:1053–1063. doi: 10.1007/s00535-006-1894-y. PubMed DOI

Lopez-Boado YS, Wilson CL, Hooper LV, Gordon JI, Hultgren SJ, Parks WC. Bacterial exposure induces and activates matrilysin in mucosal epithelial cells. J Cell Biol. 2000;148:1305–1315. doi: 10.1083/jcb.148.6.1305. PubMed DOI PMC

van Hemert S, Hoekman AJ, Smits MA, Rebel JM. Immunological and gene expression responses to a Salmonella infection in the chicken intestine. Vet Res. 2007;38:51–63. doi: 10.1051/vetres:2006048. PubMed DOI

Niikura T, Hirata R, Weil SC. A novel interferon-inducible gene expressed during myeloid differentiation. Blood Cells Mol Dis. 1997;23:337–349. doi: 10.1006/bcmd.1997.0151. PubMed DOI

Kumar P, Sweeney TR, Skabkin MA, Skabkina OV, Hellen CU, Pestova TV. Inhibition of translation by IFIT family members is determined by their ability to interact selectively with the 5′-terminal regions of cap0-, cap1- and 5′ppp- mRNAs. Nucleic Acids Res. 2014;42:3228–3245. doi: 10.1093/nar/gkt1321. PubMed DOI PMC

Barber MR, Aldridge JR, Jr, Fleming-Canepa X, Wang YD, Webster RG, Magor KE. Identification of avian RIG-I responsive genes during influenza infection. Mol Immunol. 2013;54:89–97. doi: 10.1016/j.molimm.2012.10.038. PubMed DOI PMC

Fensterl V, Sen GC. The ISG56/IFIT1 gene family. J Interferon Cytokine Res. 2011;31:71–78. doi: 10.1089/jir.2010.0101. PubMed DOI PMC

Fasina YO, Hoerr FJ, McKee SR, Conner DE. Influence of Salmonella enterica serovar Typhimurium infection on intestinal goblet cells and villous morphology in broiler chicks. Avian Dis. 2010;54:841–847. doi: 10.1637/9055-090809-Reg.1. PubMed DOI

Lee CG, Jenkins NA, Gilbert DJ, Copeland NG, O’Brien WE. Cloning and analysis of gene regulation of a novel LPS-inducible cDNA. Immunogenetics. 1995;41:263–270. doi: 10.1007/BF00172150. PubMed DOI

Li Y, Zhang P, Wang C, Han C, Meng J, Liu X, Xu S, Li N, Wang Q, Shi X, Cao X. Immune responsive gene 1 (IRG1) promotes endotoxin tolerance by increasing A20 expression in macrophages through reactive oxygen species. J Biol Chem. 2013;288:16225–16234. doi: 10.1074/jbc.M113.454538. PubMed DOI PMC

Hall CJ, Boyle RH, Astin JW, Flores MV, Oehlers SH, Sanderson LE, Ellett F, Lieschke GJ, Crosier KE, Crosier PS. Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating beta-oxidation-dependent mitochondrial ROS production. Cell Metab. 2013;18:265–278. doi: 10.1016/j.cmet.2013.06.018. PubMed DOI

Descalzi CF, Dozin B, Zerega B, Cermelli S, Gentili C, Cancedda R. Ex-FABP, extracellular fatty acid binding protein, is a stress lipocalin expressed during chicken embryo development. Mol Cell Biochem. 2002;239:221–225. doi: 10.1023/A:1020548118241. PubMed DOI

Di Marco E, Sessarego N, Zerega B, Cancedda R, Cancedda FD. Inhibition of cell proliferation and induction of apoptosis by ExFABP gene targeting. J Cell Physiol. 2003;196:464–473. doi: 10.1002/jcp.10310. PubMed DOI

Correnti C, Clifton MC, Abergel RJ, Allred B, Hoette TM, Ruiz M, Cancedda R, Raymond KN, Descalzi F, Strong RK. Galline Ex-FABP is an antibacterial siderocalin and a lysophosphatidic acid sensor functioning through dual ligand specificities. Structure. 2011;19:1796–1806. doi: 10.1016/j.str.2011.09.019. PubMed DOI PMC

Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, Paixao TA, Butler BP, Chu H, Santos RL, Berger T, Mak TW, Tsolis RM, Bevins CL, Solnick JV, Dandekar S, Bäumler AJ. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe. 2009;5:476–486. doi: 10.1016/j.chom.2009.03.011. PubMed DOI PMC

Babu US, Gaines DW, Lillehoj H, Raybourne RB. Differential reactive oxygen and nitrogen production and clearance of Salmonella serovars by chicken and mouse macrophages. Dev Comp Immunol. 2006;30:942–953. doi: 10.1016/j.dci.2005.12.001. PubMed DOI

Matiasovic J, Stepanova H, Volf J, Kubala L, Ovesna P, Rychlik I, Faldyna M. Influence of the lipopolysaccharide structure of Salmonella enterica serovar Enteritidis on interactions with pig neutrophils. Vet Microbiol. 2011;150:167–172. doi: 10.1016/j.vetmic.2011.01.007. PubMed DOI

Burlak C, Whitney AR, Mead DJ, Hackstadt T, Deleo FR. Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Mol Cell Proteomics. 2006;5:620–634. doi: 10.1074/mcp.M500336-MCP200. PubMed DOI

Furutani Y, Kato A, Yasue H, Alexander LJ, Beattie CW, Hirose S. Evolution of the trappin multigene family in the Suidae. J Biochem. 1998;124:491–502. doi: 10.1093/oxfordjournals.jbchem.a022140. PubMed DOI

Tremblay GM, Vachon E, Larouche C, Bourbonnais Y. Inhibition of human neutrophil elastase-induced acute lung injury in hamsters by recombinant human pre-elafin (trappin-2) Chest. 2002;121:582–588. doi: 10.1378/chest.121.2.582. PubMed DOI

Vachon E, Bourbonnais Y, Bingle CD, Rowe SJ, Janelle MF, Tremblay GM. Anti-inflammatory effect of pre-elafin in lipopolysaccharide-induced acute lung inflammation. Biol Chem. 2002;383:1249–1256. doi: 10.1515/BC.2002.138. PubMed DOI

Zeeuwen PL, Hendriks W, de Jong WW, Schalkwijk J. Identification and sequence analysis of two new members of the SKALP/elafin and SPAI-2 gene family. Biochemical properties of the transglutaminase substrate motif and suggestions for a new nomenclature. J Biol Chem. 1997;272:20471–20478. doi: 10.1074/jbc.272.33.20471. PubMed DOI

Steinert PM, Marekov LN. The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J Biol Chem. 1995;270:17702–17711. doi: 10.1074/jbc.270.30.17702. PubMed DOI

Teigelkamp S, Bhardwaj RS, Roth J, Meinardus-Hager G, Karas M, Sorg C. Calcium-dependent complex assembly of the myeloic differentiation proteins MRP-8 and MRP-14. J Biol Chem. 1991;266:13462–13467. PubMed

Lusitani D, Malawista SE, Montgomery RR. Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect Immun. 2003;71:4711–4716. doi: 10.1128/IAI.71.8.4711-4716.2003. PubMed DOI PMC

Champaiboon C, Sappington KJ, Guenther BD, Ross KF, Herzberg MC. Calprotectin S100A9 calcium-binding loops I and II are essential for keratinocyte resistance to bacterial invasion. J Biol Chem. 2009;284:7078–7090. doi: 10.1074/jbc.M806605200. PubMed DOI PMC

Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe. 2012;11:227–239. doi: 10.1016/j.chom.2012.01.017. PubMed DOI PMC

Nisapakultorn K, Ross KF, Herzberg MC. Calprotectin expression inhibits bacterial binding to mucosal epithelial cells. Infect Immun. 2001;69:3692–3696. doi: 10.1128/IAI.69.6.3692-3696.2001. PubMed DOI PMC

Hyland KA, Kohrt L, Vulchanova L, Murtaugh MP. Mucosal innate immune response to intragastric infection by Salmonella enterica serovar Choleraesuis. Mol Immunol. 2006;43:1890–1899. doi: 10.1016/j.molimm.2005.10.011. PubMed DOI

Gruys E, Toussaint MJ, Niewold TA, Koopmans SJ. Acute phase reaction and acute phase proteins. J Zhejiang Univ Sci B. 2005;6:1045–1056. doi: 10.1631/jzus.2005.B1045. PubMed DOI PMC

Burggraaf S, Karpala AJ, Bingham J, Lowther S, Selleck P, Kimpton W, Bean AG. H5N1 infection causes rapid mortality and high cytokine levels in chickens compared to ducks. Virus Res. 2014;185:23–31. doi: 10.1016/j.virusres.2014.03.012. PubMed DOI PMC

Murakami T, Inoshima Y, Sakamoto E, Fukushi H, Sakai H, Yanai T, Ishiguro N. AA amyloidosis in vaccinated growing chickens. J Comp Pathol. 2013;149:291–297. doi: 10.1016/j.jcpa.2013.02.002. PubMed DOI

Zerega B, Camardella L, Cermelli S, Sala R, Cancedda R, Descalzi CF. Avidin expression during chick chondrocyte and myoblast development in vitro and in vivo: regulation of cell proliferation. J Cell Sci. 2001;114:1473–1482. PubMed

Green NM. Avidin. Adv Protein Chem. 1975;29:85–133. doi: 10.1016/S0065-3233(08)60411-8. PubMed DOI

Videnska P, Sisak F, Havlickova H, Faldynova M, Rychlik I: Influence ofSalmonella entericaserovar Enteritidis infection on the composition of chicken cecal microbiota.BMC Vet Res 2013, 9:140. PubMed PMC

Nordentoft S, Molbak L, Bjerrum L, De Vylder J, Van Immerseel F, Pedersen K: The influence of the cage system and colonisation ofSalmonellaEnteritidis on the microbial gut flora of laying hens studied by T-RFLP and 454 pyrosequencing.BMC Microbiol 2011, 11:187. PubMed PMC

Cuperus T, Coorens M, van Dijk A, Haagsman HP. Avian host defense peptides. Dev Comp Immunol. 2013;41:352–369. doi: 10.1016/j.dci.2013.04.019. PubMed DOI

Nitto T, Dyer KD, Czapiga M, Rosenberg HF. Evolution and function of leukocyte RNase A ribonucleases of the avian species, Gallus gallus. J Biol Chem. 2006;281:25622–25634. doi: 10.1074/jbc.M604313200. PubMed DOI

Rosenberg HF. RNase A ribonucleases and host defense: an evolving story. J Leukoc Biol. 2008;83:1079–1087. doi: 10.1189/jlb.1107725. PubMed DOI PMC

Yang D, Chen Q, Rosenberg HF, Rybak SM, Newton DL, Wang ZY, Fu Q, Tchernev VT, Wang M, Schweitzer B, Kingsmore SF, Patel DD, Oppenheim JJ, Howard OM. Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. J Immunol. 2004;173:6134–6142. doi: 10.4049/jimmunol.173.10.6134. PubMed DOI PMC

Zhao SH, Kuhar D, Lunney JK, Dawson H, Guidry C, Uthe JJ, Bearson SM, Recknor J, Nettleton D, Tuggle CK. Gene expression profiling in Salmonella Choleraesuis-infected porcine lung using a long oligonucleotide microarray. Mamm Genome. 2006;17:777–789. doi: 10.1007/s00335-005-0155-3. PubMed DOI

Elli L, Ciulla MM, Busca G, Roncoroni L, Maioli C, Ferrero S, Bardella MT, Bonura A, Paliotti R, Terrani C, Braidotti P. Beneficial effects of treatment with transglutaminase inhibitor cystamine on the severity of inflammation in a rat model of inflammatory bowel disease. Lab Invest. 2011;91:452–461. doi: 10.1038/labinvest.2010.186. PubMed DOI

Berthelot L, Papista C, Maciel TT, Biarnes-Pelicot M, Tissandie E, Wang PH, Tamouza H, Jamin A, Bex-Coudrat J, Gestin A, Boumediene A, Arcos-Fajardo M, England P, Pillebout E, Walker F, Daugas E, Vrtosvnik F, Flamant M, Benhamou M, Cogné M, Moura IC, Monteiro RC. Transglutaminase is essential for IgA nephropathy development acting through IgA receptors. J Exp Med. 2012;209:793–806. doi: 10.1084/jem.20112005. PubMed DOI PMC

Berndt A, Methner U. B cell and macrophage response in chicks after oral administration of Salmonella Typhimurium strains. Comp Immunol Microbiol Infect Dis. 2004;27:235–246. doi: 10.1016/j.cimid.2003.11.002. PubMed DOI

Bar-Shira E, Sklan D, Friedman A. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Dev Comp Immunol. 2003;27:147–157. doi: 10.1016/S0145-305X(02)00076-9. PubMed DOI

Desmidt M, Ducatelle R, Mast J, Goddeeris BM, Kaspers B, Haesebrouck F. Role of the humoral immune system in Salmonella enteritidis phage type four infection in chickens. Vet Immunol Immunopathol. 1998;63:355–367. doi: 10.1016/S0165-2427(98)00112-3. PubMed DOI

Boes M, Prodeus AP, Schmidt T, Carroll MC, Chen J. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med. 1998;188:2381–2386. doi: 10.1084/jem.188.12.2381. PubMed DOI PMC

Berndt A, Methner U. Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella Typhimurium strains. Vet Immunol Immunopathol. 2001;78:143–161. doi: 10.1016/S0165-2427(00)00264-6. PubMed DOI

Pieper J, Methner U, Berndt A. Characterization of avian gammadelta T-cell subsets after Salmonella enterica serovar Typhimurium infection of chicks. Infect Immun. 2011;79:822–829. doi: 10.1128/IAI.00788-10. PubMed DOI PMC

Hong YH, Lillehoj HS, Dalloul RA, Min W, Miska KB, Tuo W, Lee SH, Han JY, Lillehoj EP. Molecular cloning and characterization of chicken NK-lysin. Vet Immunol Immunopathol. 2006;110:339–347. doi: 10.1016/j.vetimm.2005.11.002. PubMed DOI

Berndt A, Pieper J, Methner U. Circulating gamma delta T cells in response to Salmonella enterica serovar Enteritidis exposure in chickens. Infect Immun. 2006;74:3967–3978. doi: 10.1128/IAI.01128-05. PubMed DOI PMC

Matulova M, Havlickova H, Sisak F, Rychlik I. Vaccination of chickens with Salmonella Pathogenicity Island (SPI) 1 and SPI2 defective mutants of Salmonella enterica serovar Enteritidis. Vaccine. 2012;30:2090–2097. doi: 10.1016/j.vaccine.2012.01.050. PubMed DOI

Sasai K, Aita M, Lillehoj HS, Miyamoto T, Fukata T, Baba E. Dynamics of lymphocyte subpopulation changes in the cecal tonsils of chickens infected with Salmonella Enteritidis. Vet Microbiol. 2000;74:345–351. doi: 10.1016/S0378-1135(00)00193-0. PubMed DOI

Kogut MH, Genovese KJ, He H, Swaggerty CL, Jiang Y. Modulation of chicken intestinal immune gene expression by small cationic peptides as feed additives during the first week posthatch. Clin Vaccine Immunol. 2013;20:1440–1448. doi: 10.1128/CVI.00322-13. PubMed DOI PMC

Hoszowski A, Truszczynski M. Prevention of Salmonella typhimurium caecal colonisation by different preparations for competitive exclusion. Comp Immunol Microbiol Infect Dis. 1997;20:111–117. doi: 10.1016/S0147-9571(96)00042-2. PubMed DOI

Paulin SM, Jagannathan A, Campbell J, Wallis TS, Stevens MP. Net replication of Salmonella enterica serovars Typhimurium and Choleraesuis in porcine intestinal mucosa and nodes is associated with their differential virulence. Infect Immun. 2007;75:3950–3960. doi: 10.1128/IAI.00366-07. PubMed DOI PMC

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