Increased expression of interleukin-5 (IL-5), IL-13, and tumor necrosis factor alpha genes in intestinal lymph cells of sheep selected for enhanced resistance to nematodes during infection with Trichostrongylus colubriformis

Infection and Immunity

Volumn 73, Issue 4, 2005, Pages 2175-2183

  Pernthaner, Anton ^a   Cole, Sally Ann ^a   Morrison, Lilian ^a   Hein, Wayne R ^a  

^a AGRESEARCH   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA; INTERLEUKIN 5;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC RESISTANCE; GENETIC SUSCEPTIBILITY; GENOTYPE; INFECTION SENSITIVITY; INTESTINE LYMPH; LYMPHOCYTE; MALE; NEMATODIASIS; NONHUMAN; PRIORITY JOURNAL; SHEEP; TRICHOSTRONGYLUS COLUBRIFORMIS; ANIMAL; CD4+ T LYMPHOCYTE; CYTOLOGY; GENETICS; IMMUNOLOGY; INTESTINE; LYMPH; PARASITOLOGY; TRICHOSTRONGYLOSIS; TRICHOSTRONGYLUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; GENOTYPE; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-4; INTERLEUKIN-5; INTESTINES; LYMPH; MALE; SHEEP; TRICHOSTRONGYLOSIS; TRICHOSTRONGYLUS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 16244377076     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.4.2175-2183.2005     Document Type: Article

References (57)

1. Akiho, H., P. Blennerhassett, Y. Deng, and S. M. Collins. 2002. Role of IL-4, IL-13, and STAT6 in inflammation-induced hypercontractility of murine smooth muscle cells. Am. J. Physiol. Gastrointest. Liver Physiol. 282:G226-G232.
2. Almeria, S., A. Canals, D. S. Zarlenga, and L. C. Gasbarre. 1997. Quantification of cytokine gene expression in lamina propria lymphocytes of cattle following infection with Ostertagia ostertagi. J. Parasitol. 83:1051-1055.
3. Bancroft, A. J., D. Artis, D. D. Donaldson, J. P. Sypek, and R. K. Grencis. 2000. Gastrointestinal nematode expulsion in IL-4 knockout mice is IL-13 dependent. Eur. J. Immunol. 30:2083-2091.
4. Bancroft, A. J., A. N. McKenzie, and R. K. Grencis. 1998. A critical role for IL-13 in resistance to intestinal nematode infection. J. Immunol. 160:3453-3461.
5. Bao, S., S. J. McClure, D. L. Emery, and A. J. Husband. 1996. Interleukin-5 mRNA expressed by eosinophils and gamma/delta T cells in parasite-immune sheep. Eur. J. Immunol. 26:552-556.
6. Bisset, S. A., C. A. Morris, J. C. McEwan, and A. Vlassoff. 2001. Breeding sheep in New Zealand that are less reliant on anthelmintics to maintain health and productivity. N. Z. Vet. J. 49:236-246.
7. Bisset, S. A., A. Vlassoff, P. G. C. Douch, W. E. Jonas, C. J. West, and R. S. Green. 1996. Nematode burdens and immunological responses following natural challenge in Romney lambs selectively bred for low or high faecal worm egg count. Vet. Parasitol. 61:249-263.
8. Brown, W. C., A. C. Rice-Ficht, and D. M. Estes. 1998. Bovine type 1 and type 2 responses. Vet. Immunol. Immunopathol. 63:45-55.
9. Buxton, D., K. M. Thomson, S. Maley, J. M. Wastling, E. A. Innes, W. R. Panton, and S. Nicoll. 1994. Primary and secondary responses of the ovine lymph node to Toxoplasma gondii: cell output in efferent lymph and parasite detection. J. Comp. Pathol. 111:231-241.
10. Cabaj, W., M. Stankiewicz, S. A. Bisset, A. Pernthaner, C. J. West, and E. Hadas. 1996. Immunisation of nematode resistant or susceptible Romney lambs with Oxfendazole abbreviated infections against pasture challenge. Acta Parasitol. 41:159-165.
11. Cabaj, W., M. Stankiewicz, W. E. Jonas, A. Pernthaner, and S. Lawrence. 1996. The effect of immunization of sheep with drug-abbreviated infections of Trichostrongylus colubriformis on in vitro lymphocyte blastogenic responses. Acta Parasitol. 41:97-102.
12. Canals, A., D. S. Zarlenga, S. Almeria, and L. C. Gasbarre. 1997. Cytokine profile induced by a primary infection with Ostertagia ostertagi in cattle. Vet. Immunol. Immunopathol. 58:63-75.
13. Dandie, G. W., S. J. Ragg, and H. K. Muller. 1992. Migration of Langerhans cells from carcinogen-treated sheep skin. J. Investig. Dermatol. 99:S51-S53.
14. Dehlawi, M. S., and P. K. Goyal. 2003. Responses of inbred mouse strains to infection with intestinal nematodes. J. Helminthol. 77:119-124.
15. Douch, P. G. C., R. S. Green, and P. L. Risdon. 1994. Antibody responses of sheep to challenge with Trichostrongylus colubriformis and the effect of dexamethasone treatment. Int. J. Parasitol. 24:921-928.
16. Else, K. J., G. M. Entwistle, and R. K. Grencis. 1993. Correlations between worm burden and markers of Th1 and Th2 cell subset induction in an inbred strain of mouse infected with Trichuris muris. Parasite Immunol. 15:595-600.
17. Else, K. J., and F. D. Finkelman. 1998. Intestinal nematode parasites, cytokines and effector mechanisms. Int. J. Parasitol. 28:1145-1158.
18. Emery, D. L., S. J. McClure, B. M. Wagland, and W. O. Jones. 1992. Studies of stage-specific immunity against Trichostrongylus colubriformis in sheep: immunization by normal and truncated infections. Int. J. Parasitol. 22:215-220.
19. Garside, P., M. W. Kennedy, D. Wakelin, and C. E. Lawrence. 2000. Immunopathology of intestinal helminth infection. Parasite Immunol. 22:605-612.
20. Gasbarre, L. C. 1997. Effects of gastrointestinal nematode infection on the ruminant immune system. Vet. Parasitol. 72:327-337.
21. Gasbarre, L. C., E. A. Leighton, and T. Sonstegard. 2001. Role of the bovine immune system and genome in resistance to gastrointestinal nematodes. Vet. Parasitol. 98:51-64.
22. Gill, H. S., K. Altmann, M. L. Cross, and A. J. Husband. 2000. Induction of T helper 1- and T helper 2-type immune responses during Haemonchus contortus infection in sheep. Immunology 99:458-463.
23. Grencis, R. K. 2001. Cytokine regulation of resistance and susceptibility to intestinal nematode infection-from host to parasite. Vet. Parasitol. 100:45-50.
24. Grencis, R. K. 1997. Th2-mediated host protective immunity to intestinal nematode infections. Philos. Trans. R. Soc. Lond. B 352:1377-1384.
25. Hein, W. R., T. Barber, S. Cole, L. Morrison, and A. Pernthaner. Long-term collection and characterization of afferent lymph from the ovine small intestine. J. Immunol. Methods 293:153-168.
26. Ishikawa, N., P. K. Goyal, Y. R. Mahida, K. F. Li, and D. Wakelin. 1998. Early cytokine responses during intestinal parasitic infections. Immunology 93:257-263.
27. Khan, W. I., P. Blennerhasset, C. Ma, K. I. Matthaei, and S. M. Collins. 2001. Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunol. 23:39-42.
28. Lalani, I., K. Bhol, and A. R. Ahmed. 1997. Interleukin-10: biology, role in inflammation and autoimmunity, Ann. Allergy Asthma Immunol. 79:469-483.
29. Lawrence, C. E., J. C. Paterson, L. M. Higgins, T. T. MacDonald, M. W. Kennedy, and P. Garside. 1998. IL-4-regulated enteropathy in an intestinal nematode infection. Eur. J. Immunol. 28:2672-2684.
30. MacHugh, N. D., A. Bensaid, W. C. Davis, C. J. Howard, K. R. Parsons, B. Jones, and A. Kaushal. 1988. Characterization of a bovine thymic differentiation antigen analogous to CD1 in the human. Scand. J. Immunol. 27:541-547.
31. Mackay, C. R., J. F. Maddox, K. J. Gogolin-Ewens, and M. R. Brandon. 1985. Characterization of two sheep lymphocyte differentiation antigens, SBU-T1 and SBU-T6. Immunology 55:729-737.
32. Madden, K. B., L. Whitman, C. Sullivan, W. C. Gause, J. F. Urban, Jr., I. M. Katona, F. D. Finkelman, and T. Shea-Donohue. 2002. Role of STAT6 and mast cells in IL-4- and IL-13-induced alterations in murine intestinal epithelial cell function. J. Immunol. 169:4417-4422.
33. Matsuda, S., R. Uchikawa, M. Yamada, and N. Arizono. 1995. Cytokine mRNA expression profiles in rats infected with the intestinal nematode Nippostrongylus brasiliensis. Infect. Immun. 63:4653-4660.
34. McClure, S. J., B. M. Wagland, and D. L. Emery. 1991. Effects of Freund's adjuvants on local, draining and circulating lymphocyte populations in sheep. Immunol. Cell Biol. 69:361-367.
35. McKenzie, G. J., A. Bancroft, R. K. Grencis, and A. N. McKenzie. 1998. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr. Biol. 8:339-342.
36. Morris, C. A., A. Vlassoff, S. A. Bisset, R. L. Baker, T. G. Watson, C. J. West, and M. Wheeler. 2000. Continued selection of Romney sheep for resistance or susceptibility to nematode infection: estimates of direct and correlated responses. Animal Sci. 70:17-27.
37. Patterson, H. D., and R. Thompson. 1971. Recovery of inter-block information when block sizes are unequal. Biometrika 58:545-554.
38. Pepin, M., D. Cannella, J. J. Fontaine, J. C. Pittet, and A. Le Pape. 1992. Ovine mononuclear phagocytes in situ: identification by monoclonal antibodies and involvement in experimental pyogranulomas. J. Leukoc. Biol. 51:188-198.
39. Pernthaner, A., W. Cabaj, M. Stankiewicz, J. Davies, and D. Maass. 1997. Cytokine mRNA expression and IFN-gamma production of immunised nematode resistant and susceptible lambs against natural poly-generic challenge. Acta Parasitol. 42:180-186.
40. Pernthaner, A., S. A. Cole, T. Gatehouse, and W. R. Hein. 2002. Phenotypic diversity of antigen-presenting cells in ovine-afferent intestinal lymph. Arch. Med. Res. 33:405-412.
41. Pernthaner, A., R. J. Shaw, M. M. McNeill, L. Morrison, and W. R. Hein. 2005. Total and nematode-specific IgE responses in intestinal lymph of genetically resistant and susceptible sheep during infection with Trichostrongylus colubriformis. Vet. Immunol. Immunopathol. 104:69-80.
42. Pernthaner, A., M. Stankiewicz, W. Cabaj, and W. Jonas. 1995. Immune responsiveness of Romney sheep selected for resistance or susceptibility to gastrointestinal nematodes: field studies. Vet. Immunol. Immunopathol. 48: 97-103.
43. Pernthaner, A., A. Vlassoff, P. G. C. Douch, and D. R. Maass. 1997. Cytokine mRNA expression and IFN-γ production in nematode resistant and susceptible line lambs artificially infected with gastro-intestinal nematodes. Acta Parasitol. 42:55-61.
44. Ragg, S. J., G. W. Dandie, G. M. Woods, and H. K. Muller. 1995. Abrogation of afferent lymph dendritic cell function after cutaneously applied chemical carcinogens. Cell Immunol. 162:80-88.
45. Rothel, J. S., L. A. Corner, M. W. Lightowlers, H. F. Seow, P. McWaters, G. Entrican, and P. R. Wood. 1998. Antibody and cytokine responses in efferent lymph following vaccination with different adjuvants. Vet. Immunol. Immunopathol. 63:167-183.
46. Ryan, S., L. Tiley, I. McConnell, and B. Blacklaws. 2000. Infection of dendritic cells by the Maedi-visna lentivirus. J. Virol. 74:10096-10103.
47. Schallig, H., M. A. van Leeuwen, and W. M. L. Hendrikx. 1994. Immune responses of Texel sheep to excretory/secretory products of adult Haemonchus contenus. Parasitology 108:351-357.
48. Schallig, H. D. 2000. Immunological responses of sheep to Haemonchus contortus. Parasitology 120(Suppl.):S63-S72.
49. Schopf, L. R., K. F. Hoffmann, A. W. Cheever, J. F. Urban, Jr., and T. A. Wynn. 2002. IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 168:2383-2392.
50. Stankiewicz, M., W. Cabaj, A. Pernthaner, W. Jonas, and B. Rabel. 1996. Drug-abbreviated infections and development of immunity against Trichostrongylus colubriformis in sheep. Int. J. Parasitol. 26:97-103.
51. Torgerson, P. R., and S. Lloyd. 1993. The B cell dependence of Haemonchus contenus antigen-induced lymphocyte proliferation. Int. J. Parasitol. 23:925-930.
52. Urban, J., H. Fang, Q. Liu, M. J. Ekkens, S. J. Chen, D. Nguyen, V. Mitro, D. D. Donaldson, C. Byrd, R. Peach, S. C. Morris, F. D. Finkelman, L. Schöpf, and W. C. Cause. 2000. IL-13-mediated worm expulsion is B7 independent and IFN-gamma sensitive. J. Immunol. 164:4250-4256.
53. Urban, J. F., Jr., R. Payer, C. Sullivan, J. Goldhill, T. Shea-Donohue, K. Madden, S. C. Morris, I. Katona, W. Cause, M. Ruff, L. S. Mansfield, and F. D. Finkelman. 1996. Local TH1 and TH2 responses to parasitic infection in the intestine: regulation by IFN-gamma and IL-4. Vet. Immunol. Immunopathol. 54:337-344.
54. Watkins, C., S. Lau, R. Thistlethwaite, J. Hopkins, and G. D. Harkiss. 1999. Analysis of reporter gene expression in ovine dermis and afferent lymph dendritic cells in vitro and in vivo. Vet. Immunol. Immunopathol. 72:125-133.
55. Whitlock, H. V. 1948. Some modifications of the McMaster helminth egg-counting techniques and apparatus. J. Counc. Sci. Ind. Res. 21:177-180.
56. Wynn, T. A. 2003. IL-13 effector functions. Annu. Rev. Immunol. 21:425-456.
57. Zhou, Y., S. Bao, T. L. Rothwell, and A. J. Husband. 1996. Differential expression of interleukin-5 mRNA+ cells and eosinophils in Nippostrongylus brasiliensis infection in resistant and susceptible strains of mice. Eur. J. Immunol. 26:2133-2139.