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Analysis of Gene Expression Responses to a Salmonella Infection in Rugao Chicken Intestine Using GeneChips

  • Luan, D.Q. (College of Animal Science and Technology, Yangzhou University) ;
  • Chang, G.B. (College of Animal Science and Technology, Yangzhou University) ;
  • Sheng, Z.W. (College of Animal Science and Technology, Yangzhou University) ;
  • Zhang, Y. (College of Animal Science and Technology, Yangzhou University) ;
  • Zhou, W. (College of Animal Science and Technology, Yangzhou University) ;
  • Li, Z.Z. (Crop Cultivation and Farming System, Huazhong Agricultural University) ;
  • Liu, Y. (Institute of Agricultural Resources and Environment Research/Engineering Research Center for Digital Agriculture, Jiangsu Academy of Agricultural Sciences) ;
  • Chen, G.H. (College of Animal Science and Technology, Yangzhou University)
  • Received : 2011.06.10
  • Accepted : 2011.09.01
  • Published : 2012.02.01

Abstract

Poultry products are an important source of Salmonella enterica. An effective way to reduce food poisoning due to Salmonella would be to breed chickens more resistant to infection. Unfortunately host responses to Salmonella are complex with many factors involved. To learn more about responses to Salmonella in young chickens of 2 wk old, a cDNA Microarray containing 13,319 probes was performed to compare gene expression profiles between two chicken groups under control and Salmonella infected conditions. Newly hatched chickens were orally infected with S. enterica serovar Enteritidis. Since the intestine is one of the important barriers the bacteria encounter after oral inoculation, intestine gene expression was investigated at 2 wk old. There were 588 differentially expressed genes detected, of which 276 were known genes, and of the total number 266 were up-regulated and 322 were down-regulated. Differences in gene expression between the two chicken groups were found in control as well as Salmonella infected conditions indicating a difference in the intestine development between the two chicken groups which might be linked to the difference in Salmonella susceptibility. The differential expressions of 4 genes were confirmed by quantitative real-time PCR and the results indicated that the expression changes of these genes were generally consistent with the results of GeneChips. The findings in this study have lead to the identification of novel genes and possible cellular pathways, which are host dependent.

Keywords

References

  1. Al-Shahrour, F., R. Diaz-Uriarte and J. Dopazo. 2004. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20:578-580. https://doi.org/10.1093/bioinformatics/btg455
  2. Amundson, S. A., M. Bittner, P. Meltzer, J. Trent and A. J. Fornace Jr. 2001. Physiological function as regulation of large transcriptional programs: the cellular response to genotoxic stress. Comp. Biochem. Physiol. B. 129:703-710. https://doi.org/10.1016/S1096-4959(01)00389-X
  3. Barrow, P. A., M. B. Huggins, M. A. Lovell and J. M. Simpson. 1987. Observations on the pathogenesis of experimental Salmonella typhimurium infection in chickens. Res. Vet. Sci. 42:194-199.
  4. Bourneuf, E., F. Hérault, C. Chicault, W. Carré, S. Assaf, A. Monnier, S. Mottier, S. Lagarrigue, M. Douaire, J. Mosser and C. Diot. 2006. GeneChip analysis of differential gene expression in the liver of lean and fat chickens. Gene. 372: 162-170. https://doi.org/10.1016/j.gene.2005.12.028
  5. Bryan, E. D. and M. P. Doyle. 1995. Health risks and consequences of Salmonella and campylobacter jejuni in raw meat. J. Food Prot. 58:326-344.
  6. Eckmann, L., J. R. Smith, M. P. Housley, M. B. Dwinell and M. F. Kagnoff. 2000. Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria Salmonella. J. Biol. Chem. 275:14084-14094. https://doi.org/10.1074/jbc.275.19.14084
  7. Hillier, L. W., W. Miller, E. Birney, W. Warren, R. C. Hardison, C. P. Ponting, P. Bork, D. W. Burt, M. A. Groenen, M. E. Delany, J. B. Dodgson, A. T. Chinwalla, P. F. Cliften, S. W. Clifton, K. D. Delehaunty, C. Fronick, R. S. Fulton, T. A. Graves, C. Kremitzki, D. Layman, V. Magrini, J. D. McPherson, T. L. Miner, P. Minx, W. E. Nash, M. N. Nhan, J. O. Nelson, L. G. Oddy, C. S. Pohl, J. Randall-Maher, S. M. Smith, J. W. Wallis, S. P. Yang, M. N. Romanov, C. M. Rondelli, B. Paton, J. Smith, D. Morrice, L. Daniels, H. G. Tempest, L. Robertson, J. S. Masabanda, D. K. Griffin, A. Vignal, V. Fillon, L. Jacobbson, S. Kerje, L. Andersson, R. P. Crooijmans, J. Aerts, J. J. vander Poel, H. Ellegren, R. B. Caldwell, S. J. Hubbard, D. V. Grafham, A. M. Kierzek, S. R. McLaren, I. M. Overton, H. Arakawa, K. J. Beattie, Y. Bezzubov, P. E. Boardman, J. K. Bonfield, M. D. Croning, R. M. Davies, M. D. Francis, S. J. Humphray, C. E. Scott, R. G. Taylor, C. Tickle, W. R. Brown, J. Rogers, J. M. Buerstedde, S. A. Wilson, L. Stubbs, I. Ovcharenko, L. Gordon, S. Lucas, M. M. Miller, H. Inoko, T. Shiina, J. Kaufman, J. Salomonsen, K. Skjoedt, G. K. Wong, J. Wang, B. Liu, J. Wang, J. Yu, H. Yang, M. Nefedov, M. Koriabine, P. J. Dejong, L. Goodstadt, C. Webber, N. J. Dickens, I. Letunic, M. Suyama, D. Torrents, C. von Mering, E. M. Zdobnov, K. Makova, A. Nekrutenko, L. Elnitski, P. Eswara, D. C. King, S. Yang, S. Tyekucheva, A. Radakrishnan, R. S. Harris, F. Chiaromonte, J. Taylor, J. He, M. Rijnkels, S. Griffiths-Jones, A. Ureta-Vidal, M. M. Hoffman, J. Severin, S. M. Searle, A. S. Law, D. Speed, D. Waddington, Z. Cheng, E. Tuzun, E. Eichler, Z. Bao, P. Flicek, D. D. Shteynberg, M. R. Brent, J. M. Bye, E. J. Huckle, S. Chatterji, C. Dewey, L. Pachter, A. Kouranov, Z. Mourelatos, A. G. Hatzigeorgiou, A. H. Paterson, R. Ivarie, M. Brandstrom, E. Axelsson, N. Backstrom, S. Berlin, M. T. Webster, O. Pourquie, A. Reymond, C. Ucla, S. E. Antonarakis, M. Long, J. J. Emerson, E. Betran, I. Dupanloup, H. Kaessmann, A. S. Hinrichs, G. Bejerano, T. S. Furey, R. A. Harte, B. Raney, A. Siepel, W. J. Kent, D. Haussler, E. Eyras, R. Castelo, J. F. Abril, S. Castellano, F. Camara, G. Parra, R. Guigo, G. Bourque, G. Tesler, P. A. Pevzner, A. Smit, L. A. Fulton, E. R. Mardis and R. K. Wilson. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695-716. https://doi.org/10.1038/nature03154
  8. International Chicken Genome Sequencing Consortium. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695-716. https://doi.org/10.1038/nature03154
  9. Guillot, J. F., C. Beaumont, F. Bellatif, C. Mouline, F. Lantier, P. Colin and J. Protais. 1995. Comparison of resistance of various poultry lines to infection by Salmonella enteritidis. Vet. Res. 26:81-86.
  10. Keestra, A. M., M. R. de Zoete, R. A. van Aubel and J. P. van Putten. 2008. Functional characterization of chicken TLR5 reveals species-specific recognition of flagellin. Mol. Immunol. 45(5):1298-307. https://doi.org/10.1016/j.molimm.2007.09.013
  11. Kramer, J., M. Malek and S. J. Lamont. 2003a. Association of twelve candidate gene polymorphisms and response to challenge with Salmonella enteritidis in poultry. Anim. Genet. 34:339-348. https://doi.org/10.1046/j.1365-2052.2003.01027.x
  12. Lamont, S. J. 1998. Impact of genetics on disease resistance. Poult. Sci. 77:1111-1118. https://doi.org/10.1093/ps/77.8.1111
  13. Lamont, S. J., M. G. Kaiser and W. Liu. 2002. Candidate genes for resistance to Salmonella enteritidis colonization in chickens as detected in a novel genetic cross. Vet. Immunol. Immunopathol. 87:423-428. https://doi.org/10.1016/S0165-2427(02)00064-8
  14. Liu, W., M. G. Kaiser and S. J. Lamont, 2003. Natural resistance-asso-ciated macrophage protein 1 gene polymorphisms and response to vaccine against or challenge with Salmonella enteritidis in young chicks. Poult. Sci. 82:259-266. https://doi.org/10.1093/ps/82.2.259
  15. Malek, M. and S. J. Lamont. 2003. Association of INOS, TRAIL, TGF-beta2, TGF-beta3, and IgL genes with response to Salmonella enteritidis in poultry. Genet. Sel. Evol. 35 (Suppl. 1):S99-S111. https://doi.org/10.1186/1297-9686-35-S1-S99
  16. Malek, M., J. R. Hasenstein and S. J. Lamont. 2004. Analysis of chicken TLR4, CD28, MIF, MD-2, and LITAF genes in a Salmonella enteritidis resource population. Poult. Sci. 83:544-549. https://doi.org/10.1093/ps/83.4.544
  17. Petrenko, O., I. Ischenko and P. J. Enrietto. 1997. Characterization of changes in gene expression associated with malignant transformation by the NF-kappaB family member, v-Rel. Oncogene 15(14):1671-1680. https://doi.org/10.1038/sj.onc.1201334
  18. Rabsch, W., H. Tschape and A. J. Baumler. 2001. Non-typhoidal salmonellosis: emerging problems. Microbes Infect. 3:237-247. https://doi.org/10.1016/S1286-4579(01)01375-2
  19. Rosenberger, C. M., A. J. Pollard and B. B. Finlay. 2001. Gene array technology to determine host responses to Salmonella. Microbes Infect. 3:1353-1360. https://doi.org/10.1016/S1286-4579(01)01497-6
  20. Sadeyen, J. R., J. Trotereau, P. Velge, J. Marly, C. Beaumont, P. A. Barrow, N. Bumstead and A. C. Lalmanach. 2004. Salmonella carrier state in chicken: comparison of expression of immune response genes between susceptible and resistant animals. Microbes Infect. 6:1278-1286. https://doi.org/10.1016/j.micinf.2004.07.005
  21. Sasaki, E., H. Okamura, T. Chikamune, Y. Kanai, M. Watanabe, M. Naito and M. Sakurai. 1993. Cloning and expression of the chicken c-kit proto-oncogene. Gene. 128(2):257-261. https://doi.org/10.1016/0378-1119(93)90571-J
  22. Suzuki, S. 1994. Pathogenicity of Salmonella enteritidis in poultry. Int. J. Food Microbiol. 21:89-105. https://doi.org/10.1016/0168-1605(94)90203-8
  23. Wicker, T., J. S. Robertson, S. R. Schulze, F. A. Feltus, V. Magrini, J. A. Morrison, E. R. Mardis, R. K. Wilson, D. G. Peterson, A. H. Paterson and R. Ivarie. 2005. The repetitive landscape of the chicken genome. Genome Res. 15:126-136. https://doi.org/10.1101/gr.2438005
  24. Shin, M., S. Noji, A. Neubüser and S. Yasugi. 2006. FGF10 is required for cell proliferation and gland formation in the stomach epithelium of the chicken embryo. Dev. Biol. 294(1): 11-23. https://doi.org/10.1016/j.ydbio.2005.12.019
  25. Swaggerty, C. L., M. H. Kogut, P. J. Ferro, L. Rothwell, I. Y. Pevzner and P. Kaiser. 2004. Differential cytokine mRNA expression in het-erophils isolated from Salmonella-resistant and -susceptible chickens. Immunology 113:139-148.
  26. Tucker, R. P., C. Hagios, R. Chiquet-Ehrismann and J. Lawler. 1997. In situ localization of thrombospondin-1 and thrombospondin-3 transcripts in the avian embryo. Dev. Dyn. 208(3):326-337. https://doi.org/10.1002/(SICI)1097-0177(199703)208:3<326::AID-AJA4>3.0.CO;2-K
  27. Withanage, G. S., P. Kaiser, P. Wigley, C. Powers, P. Mastroeni, H. Brooks, P. Barrow, A. Smith, D. Maskell and I. McConnell. 2004. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar typhimurium. Infect. Immun. 72:2152-2159. https://doi.org/10.1128/IAI.72.4.2152-2159.2004
  28. Zeng, H., A. Q. Carlson, Y. Guo, Y. Yu, L. S. Collier Hyams, J. L. Madara, A. T. Gewirtz and A. S. Neish. 2003. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171:3668-3674. https://doi.org/10.4049/jimmunol.171.7.3668

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