Transcriptional profiling of cecal gene expression in probioticand Salmonella-challenged neonatal chicks

Poultry Science

Volumn 90, Issue 4, 2011, Pages 901-913

  Higgins, S E ^a   Wolfenden, A D ^b   Tellez, G ^b   Hargis, B M ^b   Porter, T E ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Chicken; Gene expression; Microarray; Probiotic; Salmonella

Indexed keywords

AVES; LACTOBACILLUS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

EID: 79952649178     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2010-00907     Document Type: Article

References (59)

1. Akbari, M. R., H. R. Haghighi, J. R. Chambers, J. Brisbin, L. R. Read, and S. Sharif. 2008. Expression of antimicrobial peptides in cecal tonsils of chickens treated with probiotics and infected with Salmonella enterica serovar Typhimurium. Clin. Vaccine Immunol. 15:1689-1693.
2. Bailey, J. S., N. A. Cox, S. E. Craven, and D. E. Cosby. 2002. Serotype tracking of Salmonella through integrated broiler chicken operations. J. Food Prot. 65:742-745.
3. Bailey, J. S., N. J. Stern, and N. A. Cox. 2000. Commercial field trial evaluation of mucosal starter culture to reduce Salmonella incidence in processed broiler carcasses. J. Food Prot. 63:867-870.
4. Benetti, R., G. Del Sal, M. Monte, G. Paroni, C. Brancolini, and C. Schneider. 2001. The death substrate Gas2 binds m-calpain and increases susceptibility to p53-dependent apoptosis. EMBO J. 20:2702-2714.
5. Berndt, A., A. Wilhelm, C. Jugert, J. Pieper, K. Sachse, and U. Methner. 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immun. 75:5993-6007.
6. Brisbin, J. T., J. Gong, and S. Sharif. 2008a. Interactions between commensal bacteria and the gut-associated immune system of chickens. Anim. Health Res. Rev. 9:101-110.
7. Brisbin, J. T., H. Zhou, J. Gong, P. Babour, M. R. Akbari, H. R. Haghighi, H. Yu, A. Clarke, A. J. Sarson, and S. Sharif. 2008b. Gene expression profiling of chicken lymphoid cells after treatment with Lactobacillus acidophilus cellular components. Dev. Comp. Immunol. 32:563-574.
8. Callaway, T. R., T. S. Edringon, R. C. Anderson, J. A. Byrd, and D. J. Nisbet. 2008. Gastrointestinal microbial ecology and the safety of our food supply as related to Salmonella. J. Anim. Sci. 86:E163-E172.
9. Centers for Disease Control and Prevention. 2009. Preliminary Food- Net Data on the incidence of infection with pathogens transmitted commonly through food-10 States, 2008. MMWR Morb. Mortal. Wkly. Rep. 58:333-337.
10. Chen, C. C., and L. F. Lau. 2009. Functions and mechanisms of action of CCN matricellular proteins. Int. J. Biochem. Cell Biol. 41:771-783.
11. Chen, C. C., J. L. Young, R. I. Monzon, N. Chen, V. Todorovic, and L. F. Lau. 2007. Cytotoxicity of TNF-alpha is regulated by integrin-mediated matrix signaling. EMBO J. 26:1257-1267.
12. Chiang, H. I., C. L. Swaggerty, M. H. Kogut, S. E. Dowd, X. Li, I. Y. Pevzner, and H. Zhou. 2008. Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44k Agilent microarray. BMC Genomics 9:526.
13. Corrier, D. E., D. J. Nisbet, J. A. Byrd III, B. M. Hargis, N. K. Keith, M. Peterson, and J. R. Deloach. 1998. Dosage titration of a characterized competitive exclusion culture to inhibit Salmonella colonization in broiler chickens during growout. J. Food Prot. 61:796-801.
14. Derache, C., E. Esnault, C. Bonsergent, Y. Le Vern, P. Quere, and A. Lalmanach. 2009. Differential modulation of β-defensin gene expression by Salmonella Enteritidis in intestinal epithelial cells from resistant and susceptible chicken inbred lines. Dev. Comp. Immunol. 33:959-966.
15. Eaves-Pyles, T., C. Szabo, and A. L. Salzman. 1999. Bacterial invasion is not required for activation of NF-κB in enterocytes. Infect. Immun. 67:800-804.
16. Ellestad, L. E., W. Carre, M. Muchow, S. A. Jenkins, X. Wang, L. A. Cogburn, and T. E. Porter. 2006. Gene expression profiling during cellular differentiation in the embryonic pituitary gland using cDNA microarrays. Physiol. Genomics 25:414-425.
17. Gast, R. K., and S. T. Benson. 1995. The comparative virulence for chicks of Salmonella enteritidis phage type 4 isolates and isolates of phage types commonly found in poultry in the United States. Avian Dis. 39:567-574.
18. Haghighi, H. R., M. F. Abdul-Careem, R. A. Dara, J. R. Chambers, and S. Sharif. 2008. Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet. Microbiol. 126:225-233.
19. Haraga, A., and S. I. Miller. 2003. A Salmonella enterica serovar Typhimurium translocated leucine-rich repeat effector protein inhibits NF-κB dependent gene expression. Infect. Immun. 71:4052-4058.
20. Hargis, B. M., D. J. Caldwell, and J. A. Byrd. 2001. Microbial Pathogens of Poultry: Live Bird Considerations. CRC Press LLC, Boca Raton, FL.
21. Head, J. A., and S. W. Kennedy. 2007. Differential expression, induction, and stability of CYP1A4 and CYP1A5 mRNA in chicken and herring gull embryo hepatocytes. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 145:617-624.
22. Higgins, J. P., S. E. Higgins, J. L. Vicente, A. D. Wolfenden, G. Tellez, and B. M. Hargis. 2007. Temporal effects of lactic acid bacteria probiotic culture on Salmonella in neonatal broilers. Poult. Sci. 86:1662-1666.
23. Higgins, J. P., S. E. Higgins, A. D. Wolfenden, S. N. Henderson, A. Torres-Rodriguez, J. L. Vicente, B. M. Hargis, and G. Tellez. 2010. Effect of lactic acid bacteria probiotic culture treatment timing on Salmonella Enteritidis in neonatal broilers. Poult. Sci. 89:243-247.
24. Higgins, S. E., J. P. Higgins, A. D. Wolfenden, S. N. Henderson, A. Torres-Rodriguez, G. Tellez, and B. M. Hargis. 2008. Evaluation of a Lactobacillus-based probiotic culture for the reduction of Salmonella Enteritidis in neonatal chicks. Poult. Sci. 87:27-31.
25. Higgins, S. E., A. Torres-Rodriguez, J. L. Vicente, C. D. Sartor, C. M. Pixley, G. M. Nava, G. Tellez, J. T. Barton, and B. M. Hargis. 2005. Evaluation of intervention strategies for idiopathic diarrhea in commercial turkey brooding houses. J. Appl. Poult. Res. 14:345-348.
26. Iyer, C., A. Kosters, G. Sethi, A. B. Kunnumakkara, B. B. Aggarwal, and J. Versalovic. 2008. Probiotic Lactobacillus reuteri promotes TNF-induced apoptosis in human myeloid leukemia-derived cells by modulation of NF-κB and MAPK signalling. Cell. Microbiol. 10:1442-1452.
27. Juric, V., C. Chen, and L. F. Lau. 2009. Fas-mediated apoptosis is regulated by the extracellular protein CCN1 (CYR61) in vitro and in vivo. Mol. Cell. Biol. 29:3266-3279.
28. Kimura, A. C., V. Reddy, R. Marcus, P. R. Cieslak, J. C. Mohle-Boetani, H. D. Kassenborg, S. D. Seler, F. P. Hardnett, T. Barrett, and D. L. Swerdlow. 2004. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotyope Enteritidis infections in the United States: A case-control study in FoodNet site. Clin. Infect. Dis. 38(Suppl. 3):S244-S252.
29. Le Negrate, G., B. Faustin, K. Welsh, M. Loeffler, M. Krajewska, P. Hasegawa, S. Mukherjee, K. Orth, S. Krajewske, A. Godzik, D. G. Guiney, and J. C. Reed. 2008. Salmonella secreted factor L deubiquitinase of Salmonella typhimurium inhibits NF-κB, suppresses IκBa ubiquitination and modulates innate immune responses. J. Immunol. 180:5045-5056.
30. Lin, P. W., T. R. Nasr, A. J. Berardinelli, A. Kumar, and A. S. Neish. 2008. The probiotic Lactobacillus GG may augment intestinal host defense by regulating apoptosis and promoting cytoprotective responses in the developing murine gut. Pediatr. Res. 64:511-516.
31. Ma, Z., D. J. Webb, M. Jo, and S. L. Gonias. 2001. Endogenously produced urokinase-type plasminogen activator is a major determinant of the basal level of activated ERK/MAP kinase and prevents apoptosis in MDA-MB-231 breast cancer cells. J. Cell Sci. 114:3387-3396.
32. Marcus, R., J. K. Varma, C. Medus, E. J. Boothe, B. J. Anderson, T. Crume, K. E. Fullerton, M. R. Moore, P. L. White, E. Lyszkowicz, A. C. Voetsch, and F. J. Angulo. 2007. Re-assessment of risk factors for sporadic Salmonella serotype Enteritidis infections: A case-control study in five FoodNet sites, 2002-2003. Epidemiol. Infect. 135:84-92.
33. McCrea, B. A., K. S. Macklin, R. A. Norton, J. B. Hess, and S. F. Bilgili. 2006. A longitudinal study of Salmonella and Campylobacter jejuni isolates from day of hatch through processing by automated ribotyping. J. Food Prot. 69:2908-2914.
34. Mennigen, R., K. Nolte, E. Rijcken, M. Utech, B. Loeffler, N. Senninger, and M. Bruewer. 2009. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 296:G1140-G1149.
35. Miettinen, M., A. Lehtonen, I. Julkunen, and S. Matikainen. 2000. Lactobacilli and streptococci activate NF-κB and STAT signaling pathways in human macrophages. J. Immunol. 164:3733-3740.
36. Neish, A. S., A. T. Gewirtz, H. Zeng, A. N. Young, M. E. Hobert, V. Karmali, A. S. Rao, and J. L. Madara. 2000. Prokaryotic regulation of epithelial responses by inhibition of IκB-α ubiquitination. Science 289:1560-1563.
37. O'Mahony, C., P. Scully, D. O'Mahoney, S. Murphy, F. O'Brien, A. Lyons, G. Sherlock, J. MacSharry, B. Keily, F. Shanahan, and L. O'Mahoney. 2008. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-κB activation. PLoS Pathog. 4:e1000112.
38. Panigrahi, P., G. T. Braileanu, H. Chen, and O. C. Stine. 2007. Probiotic bacteria change Escherichia coli-induced gene expression in cultured colonocytes: Implication in intestinal pathophysiology. World J. Gastroenterol. 13:6370-6378.
39. Pasparakis, M. 2008. IKK/NF-κ B signaling in intestinal epithelial cells controls immune homeostasis in the gut. Mucosal Immunol. 1:S54-S57.
40. Patterson, J. A., and K. M. Burkholder. 2003. Application of prebiotics and probiotics in poultry. Poult. Sci. 82:627-631.
41. Phillips, J., and J. H. Eberwine. 1996. Antisense RNA amplification: A linear amplification method for analyzing the mRNA population from single living cells. Methods 10:283-288.
42. Ramana, K. V., and S. K. Srivastava. 2006. Mediation of aldose reductase in lipopolysaccharide-induced inflammatory signals in mouse peritoneal macrophages. Cytokine 36:115-122.
43. Rantala, M., and E. Nurmi. 1973. Prevention of the growth of Salmonella infantis in chicks by the flora of the alimentary tract of chickens. Br. Poult. Sci. 14:627-630.
44. Revolledo, L., A. J. P. Ferreira, and G. C. Mead. 2006. Prospects in Salmonella control: Competitive exclusion, probiotics, and enhancement of avian intestinal immunity. J. Appl. Poult. Res. 15:341-351.
45. Rozen, S., and H. J. Skaletsky. 2000. Primer3 on the WWW for General Users and for Biologist Programmers. Humana Press, Totowa, NJ.
46. Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, A. Sturn, M. Snuffin, A. Rezantsev, D. Popov, A. Ryltsov, E. Kostukovich, I. Borisovsky, Z. Liu, A. Vinsavich, V. Trush, and J. Quackenbush. 2003. TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34:374-378.
47. Shah, R. D., F. Gonzales, E. Golez, D. Augustin, S. Caudillo, A. Abbott, J. Morello, P. M. McDonough, P. J. Paolini, and H. E. Shubeita. 2005. The antidiabetic agent rosiglitazone upregulates SERCA2 and enhances TNF-a and LPS-induced NF-κ-Bdependent transcription and TNF-a-induced IL-6 secretion in ventricular myocytes. Cell. Physiol. Biochem. 15:41-50.
48. Shima, T., K. Fukushima, H. Setoyama, A. Imaoka, S. Matsumoto, T. Hara, K. Suda, and Y. Umesake. 2008. Differential effects of two probiotic strains with different bacteriological properties on intestinal gene expression, with special reference to indigenous bacteria. FEMS Immunol. Med. Microbiol. 52:69-77.
49. Simon, R., M. D. Radmacher, and K. Dobbin. 2002. Design of studies using DNA microarrays. Genet. Epidemiol. 23:21-36.
50. Spehlmann, M. E., and L. Eckmann. 2009. Nuclear factor-κ B in intestinal protection and destruction. Curr. Opin. Gastroenterol. 25:92-99.
51. Tallant, T., A. Deb, N. Kar, J. Lupica, M. J. deVeer, and J. A. Di-Donato. 2004. Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-κB and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol. 4:33.
52. Unterholzner, L., and A. G. Bowie. 2008. The interplay between viruses and innate immune signaling: Recent insights and therapeutic opportunities. Biochem. Pharmacol. 75:589-602.
53. van Baarlen, P., F. J. Troost, S. vanHemert, C. van der Meer, W. M. de Vos, P. J. de Groot, G. J. E. J. Hooiveld, R. M. Brummer, and M. Kleerebezem. 2009. Differential NF-κB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc. Natl. Acad. Sci. USA 106:2371-2376.
54. Vicente, J. L., A. Torres-Rodriguez, S. E. Higgins, X. Hernandez-Velasco, C. Pixley, G. Tellez, A. M. Donoghue, and B. M. Hargis. 2008. Effect of a selected Lactobacillus species-based probiotic on Salmonella enterica serovar Enteritidis-infected broiler chicks. Avian Dis. 52:143-146.
55. Vicente, J. L., A. D. Wolfenden, A. Torres-Rodriguez, X. Hernandez, S. E. Higgins, G. Tellez, and B. M. Hargis. 2007. Effect of a Lactobacillus spp.-based probiotic and dietary lactose prebiotic on turkey poult performance with or without Salmonella Enteritidis challenge. J. Appl. Poult. Res. 16:361-364.
56. World Health Organization. 2006. Drug resistant Salmonella. Accessed Apr. 21, 2010. http://www.who.int/mediacentre/factsheets/fs139/en/.
57. Yan, F., R. Angel, and C. M. Ashwell. 2007. Characterization of the chicken small intestine type IIB sodium phosphate cotransporter. Poult. Sci. 86:67-76.
58. Zhang, S., H. S. Lillehoj, C. H. Kim, C. L. Keeler, U. Babu, and M. Z. Zhang. 2008. Transcriptional response of chicken macrophages to Salmonella enterica serovar Enteritidis infection. Dev. Biol. (Basel) 132:141-151.
59. Zhou, H., and S. J. Lamont. 2007. Global gene expression profile after Salmonella enterica Serovar enteritidis challenge in two F8 advanced intercross chicken lines. Cytogenet. Genome Res. 117:131-138.