Protein tyrosine kinase and mitogen-activated protein kinase signalling pathways contribute to differences in heterophil-mediated innate immune responsiveness between two lines of broilers

Avian Pathology

Volumn 40, Issue 3, 2011, Pages 289-297

  Swaggerty, C L ^a   He, H ^a   Genovese, K J ^a   Pevzner, I Y ^b   Kogut, M H ^a  

^a SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

^b Cobb Vantress Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROPHILE ANTIBODY; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR;

ANIMAL; ANIMAL SALMONELLOSIS; ARTICLE; CHICKEN; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SALMONELLA ENTERITIDIS; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, HETEROPHILE; CHICKENS; IMMUNITY, INNATE; MAP KINASE SIGNALING SYSTEM; PROTEIN-TYROSINE KINASES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); GALLUS GALLUS; SALMONELLA ENTERITIDIS;

EID: 79959495850     PISSN: 03079457     EISSN: 14653338     Source Type: Journal    
DOI: 10.1080/03079457.2011.565310     Document Type: Article

References (64)

1. Akira, S. (2001a). Toll-like receptors and innate immunity. Advances in Immunology, 78, 1-56.
2. Akira, S., Takada, H. & Kaisho, T. (2001b). Toll-like receptors: critical proteins linking innate and acquired immunity. Nature Immunology, 2, 675-680.
3. Alberola-Ila, J. & Hernández-Hoyos, G. (2003). The Ras/MAPK cascade and the control of positive selection. Immunological Reviews, 191, 79-96.
4. Anderson, K.V. (2000). Toll signaling pathways in the innate immune response. Current Opinion in Immunology, 12, 13-19.
5. Ashwell, J.D. (2006). The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nature Reviews Immunology, 6, 532-540.
6. Austic, R.E. & Nesheim, M.C. (1990). Poultry Production 13th edn. Philadelphia, PA: Lea & Febiger Publishing Co.
7. Bendelac, A. & Fearon, D.T. (1997). Innate immunity: innate pathways that control acquired immunity. Current Opinion in Immunology, 9, 1-3.
8. Cao, J., Chen, T., Gong, Y., Ying, B., Li, D., Xu, W., et al. (2010). Molecular mechanisms of the secretion of cytokines and chemokines from human monocytes activated by pneumococcal surface protein A (PspA): roles of mitogen-activated protein kinases and NF-kappaB. Microbial Pathogenesis, 48, 220-229.
9. Cloutier, A., Ear, T., Blais-Charron, E. & Dubois, C.M. (2007). Differential involvement of NF-kB and MAP kinase pathways in the generation of inflammatory cytokines by human neutrophils. Journal of Leukocyte Biology, 81, 567-577.
10. Cloutier, A., Ear, T., Borissevitch, O., Larivee, P. & McDonald, P.P. (2003). Inflammatory cytokine expression is independent of the c-Jun N-terminal kinase/AP-1 signaling cascade in human neutrophils. The Journal of Immunology, 171, 3751-3761.
11. de Greeff, A., Benga, L., Wichgers Schreur, P.J., Valentin-Weigand, P., Rebel, J.M.J. & Smith, H.E. (2009). Involvement of NF-kB and MAP-kinases in the transcriptional response of alveolar macrophages to Streptococcus suis. Veterinary Microbiology, 141, 59-67.
12. Dong, C., Davis, R.J. & Flavell, R.A. (2002). MAP kinases in the immune response. Annual Review of Immunology, 20, 55-72.
13. Fearon, D.T. & Locksley, R.M. (1996). The instructive role of innate immunity in the acquired immune response. Science, 272, 50-54.
14. Ferro, P.J., Swaggerty, C.L., Kaiser, P., Pevzner, I.Y. & Kogut, M.H. (2004). Heterophils isolated from chickens resistant to extraintestinal Salmonella enteritidis infection express higher levels of pro-inflammatory cytokine mRNA following infection than heterophils from susceptible chickens. Epidemiology and Infection, 132, 1029-1037.
15. Fujioka, S., Niu, J., Schmidt, C., Sclabas, G.M., Peng, B., Uwagawa, T., et al. (2004). NF-kB and AP-1 connection: mechanism of NF-kBdependent regulation of AP-1 activity. Molecular and Cellular Biology, 24, 7806-7819.
16. Genovese, K.J., He, H., Lowry, V.K. & Kogut, M.H. (2007). Comparison of MAP and tyrosine kinase signaling in heterophils from commercial and wild-type turkeys. Developmental & Comparative Immunology, 31, 927-933.
17. Genovese, K.J., He, H., Lowry, V.K., Swaggerty, C.L. & Kogut, M.H. (2006). Comparison of heterophil functions of modern commercial and wild-type Rio Grande turkeys. Avian Pathology, 35, 217-223.
18. Hachicha, M., Rathanaswami, P., Nacche, P.H. & McColl, S.R. (1998). Regulation of chemokine gene expression in human peripheral blood neutrophils phagocytosing microbial pathogens. The Journal of Immunology, 160, 449-454.
19. Hayden, M.S. & Ghosh, S. (2008). Shared principles in NF-kB signaling. Cell, 132, 344-362.
20. Hayden, M.S., West, A.P. & Ghosh, S. (2006). NF-kB and the immune response. Oncogene, 25, 6758-6780.
21. He, H., Farnell, M.B. & Kogut, M.H. (2003). Inflammatory agonist stimulation and signal pathway of oxidative burst in neonatal chicken heterophils. Comparative Biochemistry and Physiology, 135, 177-184.
22. Huang, Q., Yang, J., Lin, Y., Walker, C., Cheng, J., Liu, Z.-G., et al. (2004). Differential regulation of interleukin 1 receptor and Toll-like receptor signaling by MEKK3. Nature Immunology, 5, 8-103.
23. Janeway, C.A. Jr & Medzhitov, R. (2002). Innate immune recognition. Annual Review of Immunology, 20, 197-216.
24. Johnson, G.L. & Lapadat, R. (2002). Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science, 298, 1911-1912.
25. Kaiser, P., Rothwell, L., Galyov, E.E., Barrow, P.A., Burnside, J. & Wigley, P. (2000). Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis, and Salmonella gallinarum. Microbiology, 146, 3217-3226.
26. Kawai, T. & Akira, S. (2007). Signaling to NF-kB by Toll-like receptors. Trends in Molecular Medicine, 13, 460-469.
27. Kawai, T. & Akira, S. (2010). The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature Immunology, 11, 373-384.
28. Khalaf, H., Jass, J. & Olsson, P.-E. (2010). Differential cytokine regulation by NF-kB and AP-1 in Jurkat T-cells. BMC Immunology, 11, 1-12.
29. Kim, H.Y. & Rikihisa, Y. (2002). Roles of p38 mitogen-activated protein kinase, NF-kB, and protein kinase C in proinflammatory cytokine mRNA expression by human peripheral blood leukocytes, monocytes, and neutrophils in response to Anaplasma phagocytophila. Infection and Immunity, 70, 4132-4141.
30. Kobayashi, S.D., Voyich, J.M., Buhl, C.L., Stahl, R.M. & DeLeo, F.R. (2002). Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proceedings of the National Academy of Sciences of the United States of America, 99, 6901-6906.
31. Kogut, M.H., Genovese, K.J. & He, H. (2007). Flagellin and lipopoly saccharide stimulate the MEK-ERK signaling pathway in chicken heterophils through differential activation of the small GTPases, Ras and Rap1. Molecular Immunology, 44, 1729-1736.
32. Kogut, M.H., Genovese, K.J. & Lowry, V.K. (2001). Differential activation of signal transduction pathways mediating phagocytosis, oxidative burst, and degranulation by chicken heterophils in response to stimulation with opsonized Salmonella enteritidis. Inflammation, 25, 7-15.
33. Kogut, M.H., Genovese, K.J., He, H. & Kaiser, P. (2008). Flagellin and lipopolysaccharide up-regulation of IL-6 and CXCLi2 gene expression in chicken heterophils is mediated by ERK1/2-dependent activation of AP-1 and NF-kB signaling pathways. Innate Immunity, 14, 213-222.
34. Kogut, M.H., Rothwell, L. & Kaiser, P. (2003). Differential regulation of cytokine gene expression by avian heterophils during receptormediated phagocytosis of opsonized and non-opsonized Salmonella enteritidis. Journal of Interferon and Cytokine Research, 23, 319-327.
35. Kogut, M.H., Swaggerty, C.L., He, H., Pevzner, I.Y. & Kaiser, P. (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 and Infection, 8, 1866-1874.
36. Kogut, M.H., Tellez, G.I., McGruder, E.D., Hargis, B.M., Williams, J.D., Corrier, D.E., et al. (1994). Heterophils are decisive components in the early responses of chickens to Salmonella enteritidis infections. Microbial Pathogenesis, 16, 141-151.
37. Kyriakis, J.M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E.A., Ahmad, M.F., et al. (1994). The stress-activated protein kinase subfamily of c-Jun kinases. Nature, 369, 156-160.
38. Li, X., Swaggerty, C.L., Kogut, M.H., Chiang, H., Wang, Y., Genovese, K.J., et al. (2008). The paternal effect of Campylobacter jejuni colonization in ceca in broilers. Poultry Science, 87, 1742-1747.
39. Liu, Y., Shepherd, E.G. & Nelin, L.D. (2007). MAPK phosphatases* regulating the immune response. Nature Reviews Immunology, 7, 202-212.
40. Mannering, S.I. & Cheers, C. (2002). Interleukin-2 and loss of immunity in experimental Mycobacterium avium infection. Infection and Immunity, 70, 27-35.
41. Maruyama, K., Sano, G., Ray, N., Takada, Y. & Matsuo, K. (2007). c-Fos-deficient mice are susceptible to Salmonella enterica serovar Typhimurium infection. Infection and Immunity, 75, 1520-1523.
42. Medzhitov, R. & Janeway, C.A. Jr (1997a). Innate immunity: impact on the adaptive immune response. Current Opinion in Immunology, 9, 4-9.
43. Medzhitov, R. & Janeway, C.A., Jr. (1997b). Innate immunity: the virtues of a nonclonal system of recognition. Cell, 91, 295-298.
44. Muzio, M., Polentarutti, N., Bosisio, D., Manoj Kumar, P.P. & Mantovani, A. (2000). Toll-like receptor family and signalling pathway. Biochemical Society Transactions, 28, 563-566.
45. National Research Council. (1994). Nutrient Requirements of Poultry 9th edn (pp. 19-34). Washington, DC: National Academy Press.
46. Nerren, J.R., Swaggerty, C.L., MacKinnon, K.M., Genovese, K.J., He, H., Pevzner, I.Y., et al. (2009). Differential mRNA expression of the avian-specific toll-like receptor 15 between heterophils from Salmonella-susceptible and-resistant chickens. Immunogenetics, 61, 71-77.
47. Parish, C.R. & O'Neill, E.R. (1997). Dependence of the adaptive immune response on innate immunity: some questions answered but new paradoxes emerge. Immunology and Cell Biology, 75, 523-527.
48. Requena, P., Daddaoua, A., Guadix, E., Zarzuelo, A., Suarez, M.D., de Sanchez, M.F., et al. (2009). Bovine glycomacropeptide induces cytokine production in human monocytes through the stimulation of the MAPK and the NF-kB signal transduction pathways. British Journal of Pharmacology, 157, 1232-1240.
49. Romagnani, S. (1992). Induction of Th1 and Th2 responses: a key role for the 'natural' immune response? Immunology Today, 13, 379-381.
50. Roux, P.P. & Blenis, J. (2004). ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiology and Molecular Biology Reviews, 68, 320-344.
51. Singh, R.A.K. & Zhang, J.Z. (2004). Differential activation of ERK, p38, and JNK required for Th1 and Th2 deviation in myelin-reactive T cells induced by altered peptide ligand. The Journal of Immunology, 173, 7299-7307.
52. Strassheim, D., Asehnoune, K., Park, J.S., Kim, J.Y., He, Q., Richter, D., et al. (2004). Phosphoinositide 3-kinase and Akt occupy central roles in inflammatory responses of Toll-like receptor 2-stimulated neutrophils. The Journal of Immunology, 172, 5727-5733.
53. Swaggerty, C.L., Ferro, P.J., Pevzner, I.Y. & Kogut, M.H. (2005a). Heterophils are associated with resistance to systemic Salmonella enteritidis infection in genetically distinct lines of chickens. FEMS Immunology and Medical Microbiology, 43, 149-154.
54. Swaggerty, C.L., Genovese, K.J., He, H., Duke, S.E., Pevzner, I.Y. & Kogut, M.H. (2011). Broiler breeders with an efficient innate immune response are more resistant to Eimeria tenella. Poultry Science, in press.
55. Swaggerty, C.L., Kaiser, P., Rothwell, L., Pevzner, I.Y. & Kogut, M.H. (2006). Heterophil cytokine mRNA profiles from genetically distinct lines of chickens with differential heterophil-mediated innate immune responses. Avian Pathology, 35, 102-108.
56. Swaggerty, C.L., Kogut, M.H., Ferro, P.J., Rothwell, L., Pevzner, I.Y. & Kaiser, P. (2004). Differential cytokine mRNA expression in heterophils isolated from Salmonella-resistant and-susceptible chickens. Immunology, 113, 139-148.
57. Swaggerty, C.L., Lowry, V.K., Ferro, P.J., Pevzner, I.Y. & Kogut, M.H. (2005b). Disparity in susceptibility to vancomycin-resistant Enterococcus organ invasion in commercial broiler chickens that differ in innate immune responsiveness. Food and Agricultural Immunology, 16, 1-15.
58. Swaggerty, C.L., Pevzner, I.Y., Ferro, P.J., Crippen, T.L. & Kogut, M.H. (2003a). Association between in vitro heterophil function and the feathering gene in commercial broiler chickens. Avian Pathology, 32, 483-488.
59. Swaggerty, C.L., Pevzner, I.Y., Lowry, V.K., Farnell, M.B. & Kogut, M.H. (2003b). Functional comparison of heterophils isolated from commercial broiler chickens. Avian Pathology, 32, 95-102.
60. Vitiello, M., D'Isanto, M., Galdiero, M., Raieta, K., Tortora, A., Rotondo, P., et al. (2004). Interleukin-8 production by THP-1 cells stimulated by Salmonella enterica serovar Typhimurium porins is mediated by AP-1, NF-kB and MAPK pathways. Cytokine, 27, 15-24.
61. Wozniok, I., Hornbach, A., Schmitt, C., Frosch, M., Einsele, H., Hube, B., et al. (2007). Induction of ERK-kinase signalling triggers morphotype-specific killing of Candida albicans filaments by human neutrophils. Cellular Microbiology, 10, 807-820.
62. Yamashiro, S., Kamohara, H., Wang, J.-M., Yang, D., Gong, W.-H. & Yoshimura, T. (2001). Phenotypic and functional change of cytokineactivated neutrophils: inflammatory neutrophils are heterogeneous and enhance adaptive immune responses. Journal of Leukocyte Biology, 69, 698-704.
63. Yeh, M.-C., Mukaro, V., Hii, C.S. & Ferrante, A. (2010). Regulation of neutrophil-mediated killing of Staphylococcus aureus and chemotaxis by c-jun NH2 terminal kinases. Journal of Leukocyte Biology, 87, 925-932.
64. Yum, H.K., Arcaroli, J., Kupfner, J., Shenkar, R., Penninger, J.M., Sasaki, T., et al. (2001). Involvement of phosphoinositide 3-kinases in neutrophil activation and the development of acute lung injury. The Journal of Immunology, 167, 6601-6608.