Intestinal cytokine response of commercial source broiler chicks to Salmonella typhimurium infection

Poultry Science

Volumn 87, Issue 7, 2008, Pages 1335-1346

  Fasina, Y O ^a   Holt, P S ^b   Moran, E T ^a   Moore, R W ^b   Conner, D E ^a   McKee, S R ^a  

^a AUBURN UNIVERSITY   (United States)

^b RUSSELL RESEARCH CENTER   (United States)

Author keywords

Commercial type broiler chick; Cytokine; Intestine; Salmonella typhimurium

Indexed keywords

GALLUS GALLUS; SALMONELLA TYPHIMURIUM;

EID: 46249111690     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2007-00526     Document Type: Article

References (86)

1. Akiho, A., W. I. Khan, A. Al-Kaabi, P. Blennerhassett, Y. Deng, and S. M. Collins. 2007. Cytokine modulation of muscarinic receptors in the murine intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G250-G255.
2. Alam, M. S., T. Akaike, S. Okamoto, T. Kubota, J. Yoshitake, T. Sawa, Y. Miyamoto, F. Tamura, and H. Maeda. 2002. Role of nitric oxide in host defense in murine salmonellosis as a function of its antibacterial and antiapoptotic activities. Infect. Immun. 70:3130-3142.
3. Asif, M., K. A. Jenkins, L. S. Hilton, W. G. Kimpton, A. G. D. Bean, and J. W. Lowenthal. 2004. Cytokines as adjuvants for avian vaccines. Immunol. Cell Biol. 82:638-643.
4. Babu, U., R. A. Dalloul, M. Okamura, H. S. Lillehoj, H. Xie, R. B. Raybourne, D. Gaines, and R. A. Heckert. 2004. Salmonella Enteritidis clearance and immune responses in chickens following Salmonella vaccination and challenge. Vet. Immunol. Immunopathol. 101:251-257.
5. Bailey, J. S. 1988. Integrated colonization control of Salmonella in poultry. Poult. Sci. 67:928-932.
6. Bar-Shira, E., and A. Friedman. 2006. Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev. Comp. Immunol. 30:930-941.
7. Bar-Shira, E., D. Sklan, and A. Friedman. 2003. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Dev. Comp. Immunol. 27:147-157.
8. Barouch, D. H., N. L. Letvin, and R. A. Seder. 2004. The role of cytokine DNAs as vaccine adjuvants for optimizing cellular immune responses. Immunol. Rev. 202:266-274.
9. Barrow, P. A. 2007. Salmonella infections: Immune and nonimmune protection with vaccines. Avian Pathol. 36:1-13.
10. Barrow, P. A., M. B. Huggins, M. A. Lovell, and J. M. Simpson. 1987b. Observations of the pathogenesis of experimental Salmonella Typhimurium infection in chickens. Res. Vet. Sci. 42:194-199.
11. Barrow, P. A., M. A. Lovell, and J. M. Simpson. 1988. Intestinal colonization in the chicken of food-poisoning Salmonella serotypes; microbial characteristics associated with fecal excretion. Avian Pathol. 17:571-588.
12. Barrow, P. A., G. C. Mead, C. Wray, and M. Duchet-Suchaux. 2003. Control of food-poisoning Salmonella in poultry - Biological options. World's Poult. Sci. J. 59:373-383.
13. Barrow, P. A., J. F. Tucker, and J. M. Simpson. 1987a. Inhibition of colonization of the chicken alimentary tract with Salmonella Typhimurium gram-negative facultative anaerobic bacteria. Epidemiol. Infect. 98:311-322.
14. Beal, R. K., C. Powers, T. F. Davidson, P. A. Barrow, and A. L. Smith. 2006. Clearance of Salmonella enterica serovar Typhimurium in chickens is independent of B-cell function. Infect. Immun. 74:1442-1444.
15. Beal, R. K., C. Powers, P. Wigley, P. A. Barrow, and A. L. Smith. 2004a. Temporal dynamics of cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium. Avian Pathol. 33:25-33.
16. Beal, R. K., P. Wigley, C. Powers, S. D. Hulme, P. A. Barrow, and A. L. Smith. 2004b. Age at primary infection with Salmonella enterica serovar Typhimurium in the chicken influences persistence of infection and subsequent immunity to rechallenge. Vet. Immunol. Immunopathol. 100:151-164.
17. Bird, S., J. Zou, T. Wang, B. Munday, C. Cunningham, and C. J. Secombes. 2002. Evolution of interleukin-1β. Cytokine Growth Factor Rev. 13:483-502.
18. Bjerrum, L., R. M. Engberg, and K. Pederson. 2003. Infection models for Salmonella Typhimurium DT110 in day-old and 14-day-old broiler chickens kept in isolators. Avian Dis. 47:1474-1480.
19. Borish, L., R. Rosenbaum, L. Albury, and S. Clark. 1989. Activation of neutrophils by recombinant interleukin 6. Cell. Immunol. 121:280-289.
20. Centers for Disease Control and Prevention (CDC). 2006. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-10 States, United States, 2005. MMRW 55:392-395.
21. Cheeseman, J. H., M. G. Kaiser, C. Ceraci, P. Kaiser, and S. J. Lamont. 2007. Breed effect on early cytokine mRNA expression in spleen and cecum of chickens with and without Salmonella Enteritidis infection. Dev. Comp. Immunol. 31:52-60.
22. Coburn, B., G. A. Grassl, and B. B. Finlay. 2007. Salmonella, the host and disease: A brief review. Immunol. Cell Biol. 85:112-118.
23. Collins, S. M. 1996. Gut motor function: immunological control in enteric infection and inflammation. Gastroenterology 111:1683-1699.
24. Corthay, A. 2006. A three-cell model for activation of naïve T helper cells. Scand. J. Immunol. 64:93-96.
25. Crippen, T. L., C. L. Shefield, H. He, V. K. Lowry, and M. H. Kogut. 2003. Differential nitric oxide production by chicken immune cells. Dev. Comp. Immunol. 27:603-610.
26. De Waal Malefyt, R., J. Abrams, B. Bennet, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174:1209-1220.
27. Doyle, M. P., and M. C. Erickson. 2006. Reducing the carriage of foodborne pathogens in livestock and poultry. Poult. Sci. 85:960-973.
28. Eckmann, L., and M. F. Kagnoff. 2001. Cytokines in host defense against Salmonella. Microbes Infect. 3:1191-1200.
29. Ferris, K. E., A. M. Aalsburg, and G. R. Iseminger. 2002. Salmonella serotypes from animals and related sources during July 2001-June 2002. Proc. US Anim. Health Assoc. 106:467-497.
30. Ferro, P. J., C. L. Swaggerty, H. Haiqi, L. Rothwell, P. Kaiser, and M. H. Kogut. 2005. Recombinant chicken IL-6 does not activate heterophils isolated from day-old chicken in-vitro. Dev. Comp. Immunol. 29:375-383.
31. Ferro, P. J., C. L. Swaggerty, P. Kaiser, I. Y. Pevzner, and M. H. Kogut. 2004. Heterophils isolated from chickens resistant to extra-intestinal Salmonella Enteritidis infection express higher levels of pro-inflammatory cytokine mRNA following infection than heterophils from susceptible chickens. Epidemiol. Infect. 132:1029-1037.
32. Fife, M. S., A. Gutierrez, E. M. Ogilvie, C. J. W. Stock, J. M. Samuel, W. Thomson, L. F. Mack, C. M. Lewis, and P. Woo. 2006. Novel IL-10 gene family associations with systemic juvenile idiopathic arthritis. Arthritis Res. Ther. 8:R148.
33. Grimble, R. F. 1998. Nutritional modulation of cytokine biology. Nutrition 14:634-640.
34. Gulig, P. A. 1996. Pathogenesis of systemic disease. Pages 2774-2787 in Escherichia coli and Salmonella. F. C. Neidhardt, R. Curtis III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger, ed. Am. Soc. Microbiol., Washington, DC.
35. Hammer, M., J. Mages, H. Dietrich, F. Schmitz, F. Striebel, P. J. Murray, H. Wagner, and R. Lang. 2005. Control of dual-specificity phosphatase-1 expression in activated macrophages by IL-10. Eur. J. Immunol. 35:2991-3001.
36. Henderson, S. C., D. I. Bounous, and M. D. Lee. 1999. Early events in the pathogenesis of avian salmonellosis. Infect. Immun. 67:3580-3586.
37. Hideshima, T., K. Podar, D. Chauhan, and K. C. Anderson. 2005. Cytokines and signal transduction. Best Pract. Res. Clin. Haematol. 18:509-524.
38. Holt, P. S., R. K. Gast, R. E. Porter, and H. D. Stone. 1999. Hyporesponsiveness of the systemic and mucosal humoral immune systems in chickens infected with Salmonella enterica serovar Enteritidis at one day of age. Poult. Sci. 78:1510-1517.
39. Holt, P. S., and R. E. Porter. 1993. Effect of induced molting on the recurrence of a previous Salmonella Enteritidis infection. Poult. Sci. 72:2069-2078.
40. Humphrey, T. J. 1999. Contamination of meat and eggs with Salmonella serotype Enteritidis. Pages 183-192 in Salmonella enterica serotype Enteritidis in humans and animals: Epidemiology, pathogenesis and control. A. M. Saeed, ed. Iowa State University Press, Ames.
41. Jones, S. A. 2005. Direct transition from innate to acquired immunity: Defining a role for IL-6. J. Immunol. 175:3463-3468.
42. Kaiser, P., L. Rothwell, E. E. Galyov, P. A. Barrow, J. Burnside, and P. Wigley. 2000. Differential cytokine expression in avian cells in response to invasion by Salmonella Typhimurium, Salmonella Enteritidis, and Salmonella Gallinarum. Microbiology 146:3217-3226.
43. Kiessling, C. R., J. H. Cutting, M. Loftis, W. M. Kiessling, A. R. Data, and J. N. Sofos. 2002. Antimicrobial resistance of food-related Salmonella isolates 1999-2000. J. Food Prot. 65:603-608.
44. Kitagawa, H., T. Imagawa, and M. Uehara. 1996. The apical caecal diverticulum of chicken identified as a lymphoid organ. J. Anat. 189:667-672.
45. Koenen, M. E., A. G. Boonstra-Blom, and S. H. M. Jeurissen. 2002. Immunological differences between layer- and broiler-type chickens. Vet. Immunol. Immunopathol. 89:47-56.
46. Kogut, M. H., L. Rothwell, and P. Kaiser. 2002. Differential effects of age on chicken heterophil functional activation by recombinant chicken interleukin-2. Dev. Comp. Immunol. 26:817-830.
47. Kogut, M., L. Rothwell, and P. Kaiser. 2003. Differential regulation of cytokine gene expression by avian heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella Enteritidis. J. Interferon Cytokine Res. 23:319-327.
48. Kogut, M. H., L. Rothwell, and P. Kaiser. 2005. IFN-γ priming of chicken heterophils upregulates the expression of proinflammatory and Th1 cytokine mRNA following receptor-mediated phagocytosis of Salmonella enterica serovar enteritidis. J. Interferon Cytokine Res. 25:73-81.
49. Kogut, M. H., C. Swaggerty, H. He, I. Pevzner, and P. Kaiser. 2006. Toll-like receptor agonists stimulate differential functional activation and cytokine and chemokine gene expression in heterophils isolated from chickens with differential innate responses. Microbes Infect. 8:1866-1874.
50. Leshchinsky, T. V., and K. C. Klasing. 2001. Divergence of the inflammatory response in two types of chickens. Dev. Comp. Immunol. 25:629-638.
51. Liljebjelke, K. A., C. L. Hofarce, T. Liu, D. G. White, S. Ayers, S. Young, and J. J. Maurer. 2005. Vertical and horizontal transmission of Salmonella within integrated broiler production sysytem. Foodborne Pathog. Dis. 2:90-102.
52. Low, J. C., M. Angus, G. Hopkins, D. Munro, and S. C. Rankin. 1997. Antimicrobial resistance of Salmonella serovar Typhimurium DT104 isolates and investigation of strains with transferable apramycin resistance. Epidemiol. Infect. 118:97-103.
53. Lowenthal, J. W., M. R. Digby, and J. J. York. 1995. Production of interferon-gamma by chicken T cells. J. Interferon Cytokine Res. 15:933-938.
54. Lowenthal, J. W., B. Lambrecht, T. P. van den Berg, M. E. Andrew, A. D. G. Strom, and A. G. D. Bean. 2000. Avian cytokines - The natural approach to therapeutics. Dev. Comp. Immunol. 24:355-365.
55. Lowry, V. K., M. B. Farnell, P. J. Ferro, C. L. Swaggerty, A. Bahl, and M. H. Kogut. 2005. Purified β-glucan as an abiotic feed additive up-regulates the innate immune response in immature chickens against Salmonella enterica serovar Enteritidis. Int. J. Food Microbiol. 98:309-318.
56. McCormick, B. A., P. M. Hofman, J. Kim, D. K. Carnes, S. I. Miller, and J. L. Madara. 1995. Surface attachment of Salmonella Typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J. Cell Biol. 131:1599-1608.
57. Monteleone, G., I. Peluso, D. Fina, R. Caruso, F. Andrei, C. Tosti, and F. Pallone. 2006. Bacteria and mucosa immunity. Dig. Liver Dis. 38(Suppl. 2):S256-S260.
58. National Research Council. 1994. Nutrient Requirements of Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
59. Ogle, C. K., J. X. Mao, J. Z. Wu, J. D. Ogle, and J. W. Alexander. 1994. The production of tumor necrosis factor, interleukin-1, interleukin-6, and prostaglandin E2 by isolated enterocytes and gut macrophages: Effect of lipopolysaccharide and thermal injury. J. Burn Care Rehabil. 15:470-477.
60. Okamura, M., H. S. Lillehoj, R. B. Raybourne, U. S. Babu, and R. A. Heckert. 2004. Cell-mediated immune responses to a killed Salmonella Enteritidis vaccine: Lymphocyte proliferation, T-cell changes and interleukin-6 (IL-6), IL-1, IL-2, and IFN-y production. Comp. Immunol. Microbiol. Infect. Dis. 27:255-272.
61. Okamura, M., H. S. Lillehoj, R. B. Raybourne, U. S. Babu, R. A. Heckert, H. Tani, K. Sasai, E. Baba, and E. P. Lillehoj. 2005. Differential responses of macrophages to Salmonella enterica serovars Enteritidis and Typhimurium. Vet. Immunol. Immunopathol. 107:325-335.
62. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:2002-2007.
63. Rabsch, W., H. Tschape, and A. J. Baumler. 2001. Non-typhoidal salmonellosis: Emerging problems. Microbes Infect. 3:237-247.
64. Radema, S. A., S. J. van Deventer, and A. Cerami. 1991. Interleukin 1 beta is expressed predominantly by enterocytes in experimental colitis. Gastroenterology 100:1180-1186.
65. Rodríguez-Sáinz, Mdel. C., S. Sanchez-Ramon, C. de Andres, M. Rodriguez-Mahou, and M. A. Munoz-Fernandez. 2002. Th1/Th2 cytokine balance and nitric oxide in cerebrospinal fluid and serum from patients with multiple sclerosis. Eur. Cytokine Netw. 13:110-114.
66. Romagnani, S. 2000. T-cell subsets (Th1 versus Th2). Ann. Allergy Asthma Immunol. 85:9-21.
67. 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.
68. Salyers, A. A. 2002. An overview of the genetic basis of antibiotic resistance in bacteria and its implications for agriculture. Anim. Biotechnol. 13:1-5.
69. SAS Institute Inc. 2004. SAS/STAT User's Guide. Version 9.1 for Windows. SAS Inst. Inc., Cary, NC.
70. Smith, C. K., P. Kaiser, L. Rothwell, T. Humphrey, P. A. Barrow, and M. A. Jones. 2005. Campylobacter jejuni-induced cytokine responses in avian cells. Infect. Immun. 73:2094-2100.
71. Staeheli, P. 2002. Avian interferons/cytokines. J. Interferon Cytokine Res. 22:163-164.
72. Staeheli, P., F. Puehler, K. Schneider, T. W. Gobel, and B. Kaspers. 2001. Cytokines of birds: Conserved functions - A largely different look. J. Interferon Cytokine Res. 21:993-1010.
73. Swaggerty, C. L., P. Kaiser, L. Roththwell, I. Y. Pevzner, and M. H. Kogut. 2006. Heterophil cytokinem RNA profiles from genetically distinct lines of chickens with differential heterophil-mediated innate immune responses. Avian Pathol. 35:102-108.
74. Takehara, K., K. Kobayashi, R. Ruttanapumma, M. Kamikawa, T. Nagata, Y. Yokomizo, and M. Nakamura. 2003. Adjuvant effect of chicken interferon-gamma for inactivated Salmonella Enteritidis antigen. J. Vet. Med. Sci. 65:1337-1341.
75. Taylor, A., J. Verhagen, K. Blaser, M. Akdis, and C. A. Akdis. 2006. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-β: The role of T regulatory cells. Immunology 117:433-442.
76. Tjwa, E. T., J. M. Bradley, C. M. Keenan, A. B. Kroese, and K. A. Sharkey. 2003. Interleukin-1beta activates specific populations of enteric neurons and enteric glia in the guinea pig ileum and colon. Am. J. Physiol. Gastrointest. Liver Physiol. 285:G1268-G1276.
77. Turnbull, P. C. B., and G. H. Snoeyenbos. 1973. Experimental salmonellosis in the chicken. Fate and host response in the alimentary canal, liver, and spleen. Avian Dis. 18:153-177.
78. USDA Laboratory Guide. 2004. Isolation and identification of Salmonella from meat, poultry, and egg products. USDA Food Safety and Inspection Service, Office of Public Health, Laborataory Quality Assurance Division, Athens, GA.
79. Van Ginkel, F. W., H. H. Nguyen, and J. R. McGhee. 2000. Vaccines for mucosal immunity to combat emerging infectious diseases. Emerg. Infect. Dis. 6:123-132.
80. van Hemert, S., A. J. Hoekman, M. A. Smits, and J. M. Rebel. 2006. Gene expression responses to a Salmonella infection in the chicken intestine differ between lines. Vet. Immunol. Immunopathol. 114:247-258.
81. Waller, R. A., and D. B. Duncan. 1969. A Bayes Rule for the symmetric multiple comparison problem. J. Am. Stat. Assoc. 64:1484-1499.
82. Wigley, P., and P. Kaiser. 2003. Avian cytokines in health and disease. Brazilian J. Poult. Sci. 5:1-14.
83. Withanage, G. S. K., 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.
84. Withanage, G. S. K., P. Wigley, P. Kaiser, P. Mastroeni, H. Brooks, C. Powers, R. Beal, P. Barrow, D. Maskell, and I. McConnell. 2005. Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken and in protective immunity to rechallenge. Infect. Immun. 73:5173-5182.
85. Young, R., and A. Craig. 2001. The use and misuse of antibiotics in UK Agriculture - Part 3. Residues of dangerous drugs in intensively produced chicken meat and eggs. The Soil Association, Bristol, UK.
86. Zhang, S., R. A. Kingsley, R. L. Santos, H. Andrew-Polymenis, M. Raffatellu, J. Figueiredo, J. Nunes, R. M. Tsolis, L. G. Adams, and A. J. Baumler. 2003. Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhoea. Infect. Immun. 71:1-12.