Upregulation of chicken TLR4, TLR15 and MyD88 in heterophils and monocyte-derived macrophages stimulated with Eimeria tenella in vitro

Experimental Parasitology

Volumn 133, Issue 4, 2013, Pages 427-433

  Zhou, Zuoyong ^a   Wang, Zhiying ^a   Cao, Liting ^a   Hu, Shijun ^a   Zhang, Ze ^b   Qin, Bo ^a   Guo, Zhili ^a   Nie, Kui ^a  

^a SOUTHWEST UNIVERSITY   (China)

^b CHONGQING UNIVERSITY   (China)

Author keywords

Chicken; Eimeria tenella; Heterophils; Monocyte derived macrophages; Signal adaptors; Toll like receptors

Indexed keywords

MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 15; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STIMULATION; COCCIDIOSIS; CONTROLLED STUDY; EIMERIA TENELLA; GENE EXPRESSION REGULATION; GENE SEQUENCE; HOST RESISTANCE; IN VITRO STUDY; INFECTION RESISTANCE; MACROPHAGE; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CELLS, CULTURED; CHICKENS; EIMERIA TENELLA; GENE EXPRESSION; MACROPHAGES; MYELOID DIFFERENTIATION FACTOR 88; NEUTROPHILS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; UP-REGULATION;

EID: 84874411698     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2013.01.002     Document Type: Article

References (44)

1. Abasht B., Kaiser M.G., Lamont S.J. Toll-like receptor gene expression in cecum and spleen of advanced intercross line chicks infected with Salmonella enterica serovar Enteritidis. Veterinary Immunology and Immunopathology 2008, 123:314-323.
2. Augustine P.C. Cell: sporozoite interactions and invasion by apicomplexan parasites of the genus Eimeria. International Journal for Parasitology 2001, 31:1-8.
3. Baba E., Tsukamoto Y., Fukata T., Sasai K., Arakawa A. Increase of mannose residues, as Salmonella typhimurium-adhering factor, on the cecal mucosa of germ-free chickens infected with Eimeria tenella. American Journal of Veterinary Research 1993, 54:1471-1475.
4. Baba E., Wakeshima H., Fukui K., Fukata T., Arakawa A. Adhesion of bacteria to the cecal mucosal surface of conventional and germ-free chickens infected with Eimeria tenella. American Journal of Veterinary Research 1992, 53:194-197.
5. Brisbin J.T., Zhou H., Gong J., Sabour P., Akbari M.R., Haghighi H.R., Yu H., Clarke A., Sarson A.J., Sharif S. Gene expression profiling of chicken lymphoid cells after treatment with Lactobacillus acidophilus cellular components. Developmental & Comparative Immunology 2008, 32:563-574.
6. Brownlie R., Allan B. Avian toll-like receptors. Cell and Tissue Research 2011, 343:121-130.
7. Cormican P., Lloyd A.T., Downing T., Connell S.J., Bradley D., O'Farrelly C. The avian Toll-Like receptor pathway-subtle differences amidst general conformity. Developmental & Comparative Immunology 2009, 33:967-973.
8. Dalloul R.A., Lillehoj H.S. Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Review of Vaccines 2006, 5:143-163.
9. Del C.E., Gallego M., Lee S.H., Lillehoj H.S., Quilez J., Lillehoj E.P., Sanchez-Acedo C. Induction of protective immunity against Eimeria tenella infection using antigen-loaded dendritic cells (DC) and DC-derived exosomes. Vaccine 2011, 29:3818-3825.
10. Dulski P., Turner M. The purification of sporocysts and sporozoites from Eimeria tenella oocysts using Percoll density gradients. Avian Diseases 1988, 32:235-239.
11. Dykstra D.D., Reid W.M. Monensin, Eimeria tenella infection, and effects on the bacterial populations in the ceca of gnotobiotic chickens. Poultry Science 1978, 57:398-402.
12. Farnell M.B., He H., Kogut M.H. Differential activation of signal transduction pathways mediating oxidative burst by chicken heterophils in response to stimulation with lipopolysaccharide and lipoteichoic acid. Inflammation 2003, 27:225-231.
13. Gazzinelli R.T., Denkers E.Y. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nature Reviews Immunology 2006, 6:895-906.
14. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nature Reviews Immunology 2005, 5:953-964.
15. He H., Farnell M.B., Kogut M.H. Inflammatory agonist stimulation and signal pathway of oxidative burst in neonatal chicken heterophils. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2003, 135:177-184.
16. Higgs R., Cormican P., Cahalane S., Allan B., Lloyd A.T., Meade K., James T., Lynn D.J., Babiuk L.A., O'Farrelly C. Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infection and Immunity 2006, 74:1692-1698.
17. Hong Y.H., Lillehoj H.S., Lillehoj E.P., Lee S.H. Changes in immune-related gene expression and intestinal lymphocyte subpopulations following Eimeria maxima infection of chickens. Veterinary Immunology and Immunopathology 2006, 114:259-272.
18. Iqbal M., Philbin V.J., Smith A.L. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Veterinary Immunology and Immunopathology 2005, 104:117-127.
19. Karpala A.J., Lowenthal J.W., Bean A.G. Activation of the TLR3 pathway regulates IFN beta production in chickens. Developmental & Comparative Immunology 2008, 32:435-444.
20. Kawai T., Akira S. TLR signaling. Seminars in Immunology 2007, 19:24-32.
21. Keestra A.M., van Putten J.P. Unique properties of the chicken TLR4/MD-2 complex: selective lipopolysaccharide activation of the MyD88-dependent pathway. The Journal of Immunology 2008, 181:4354-4362.
22. Kogut M.H., Genovese K.J., Lowry V.K. Differential activation of signal transduction pathways mediating phagocytosis, oxidative burst, and degranulation by chicken heterophils in response to stimulation with opsonized Salmonella enteritidis. Inflammation 2001, 25:7-15.
23. Kogut M.H., Iqbal M., He H., Philbin V., Kaiser P., Smith A. Expression and function of Toll-like receptors in chicken heterophils. Developmental & Comparative Immunology 2005, 29:791-807.
24. Kropf P., Freudenberg M.A., Modolell M., Price H.P., Herath S., Antoniazi S., Galanos C., Smith D.F., Muller I. Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infection and Immunity 2004, 72:1920-1928.
25. Loharungsikul S., Troye-Blomberg M., Amoudruz P., Pichyangkul S., Yongvanitchit K., Looareesuwan S., Mahakunkijcharoen Y., Sarntivijai S., Khusmith S. Expression of toll-like receptors on antigen-presenting cells in patients with falciparum malaria. Acta Tropica 2008, 105:10-15.
26. MacKinnon K.M., He H., Nerren J.R., Swaggerty C.L., Genovese K.J., Kogut M.H. Expression profile of toll-like receptors within the gastrointestinal tract of 2-day-old Salmonella enteriditis-infected broiler chickens. Veterinary Microbiology 2009, 137:313-319.
27. McDonald V., Shirley M.W. Past and future: vaccination against Eimeria. Parasitology 2009, 136:1477-1489.
28. Medzhitov R. Toll-like receptors and innate immunity. Nature Reviews Immunology 2001, 1:135-145.
29. Mun H.S., Aosai F., Norose K., Chen M., Piao L.X., Takeuchi O., Akira S., Ishikura H., Yano A. TLR2 as an essential molecule for protective immunity against Toxoplasma gondii infection. International Immunology 2003, 15:1081-1087.
30. Nerren J.R., He H., Genovese K., Kogut M.H. Expression of the avian-specific toll-like receptor 15 in chicken heterophils is mediated by gram-negative and gram-positive bacteria, but not TLR agonists. Veterinary Immunology and Immunopathology 2010, 136:151-156.
31. O'Mahony D.S., Pham U., Iyer R., Hawn T.R., Liles W.C. Differential constitutive and cytokine-modulated expression of human Toll-like receptors in primary neutrophils, monocytes, and macrophages. International journal of Medical Sciences 2008, 5:1-8.
32. O'Neill L.A., Fitzgerald K.A., Bowie A.G. The Toll-IL-1 receptor adaptor family grows to five members. Trends in Immunology 2003, 24:286-290.
33. Qin Z.R., Arakawa A., Baba E., Fukata T., Miyamoto T., Sasai K., Withanage G.S. Eimeria tenella infection induces recrudescence of previous Salmonella enteritidis infection in chickens. Poultry Science 1995, 74:1786-1792.
34. Scanga C.A., Aliberti J., Jankovic D., Tilloy F., Bennouna S., Denkers E.Y., Medzhitov R., Sher A. Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. The Journal of Immunology 2002, 168:5997-6001.
35. Shirley M.W., Smith A.L., Blake D.P. Challenges in the successful control of the avian coccidia. Vaccine 2007, 25:5540-5547.
36. Sukhumavasi W., Egan C.E., Warren A.L., Taylor G.A., Fox B.A., Bzik D.J., Denkers E.Y. TLR adaptor MyD88 is essential for pathogen control during oral toxoplasma gondii infection but not adaptive immunity induced by a vaccine strain of the parasite. The Journal of Immunology 2008, 181:3464-3473.
37. Sumners L.H., Miska K.B., Jenkins M.C., Fetterer R.H., Cox C.M., Kim S., Dalloul R.A. Expression of Toll-like receptors and antimicrobial peptides during Eimeria praecox infection in chickens. Experimental Parasitology 2011, 127:714-718.
38. Swaggerty C.L., Genovese K.J., He H., Duke S.E., Pevzner I.Y., Kogut M.H. Broiler breeders with an efficient innate immune response are more resistant to Eimeria tenella. Poultry Science 2011, 90:1014-1019.
39. Swaggerty C.L., Pevzner I.Y., Lowry V.K., Farnell M.B., Kogut M.H. Functional comparison of heterophils isolated from commercial broiler chickens. Avian Pathology 2003, 32:95-102.
40. Temperley N.D., Berlin S., Paton I.R., Griffin D.K., Burt D.W. Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 2008, 9:62.
41. van Aubel R.A., Keestra A.M., Krooshoop D.J., van Eden W., van Putten J.P. Ligand-induced differential cross-regulation of Toll-like receptors 2, 4 and 5 in intestinal epithelial cells. Molecular Immunology 2007, 44:3702-3714.
42. Wigley P., Hulme S.D., Bumstead N., Barrow P.A. In vivo and in vitro studies of genetic resistance to systemic salmonellosis in the chicken encoded by the SAL1 locus. Microbes and Infection 2002, 4:1111-1120.
43. Williams R.B. A compartmentalised model for the estimation of the cost of coccidiosis to the world's chicken production industry. International Journal for Parasitology 1999, 29:1209-1229.
44. Zhang L., Liu R., Ma L., Wang Y., Pan B., Cai J., Wang M. Eimeria tenella: expression profiling of toll-like receptors and associated cytokines in the cecum of infected day-old and three-week old SPF chickens. Experimental Parasitology 2012, 130:442-448.