Abstract
Ileal intraepithelial and lamina propria lymphocytes from newborn, 1.5-week-old, and 3-week-old calves were compared to determine to what extent the mucosa becomes populated after birth. Single and dual fluorescence flow cytometry were used with monoclonal antibodies to bovine (Bo) CD molecules to identify lymphocyte subpopulations. Few ileal mucosal lymphocytes were present in calves at birth. However, by 1.5 weeks of age, the villi were populated with large numbers of lymphocytes, and by 3 weeks of age, the numbers had increased further. These included a prominent subpopulation of γδT cells. Several subsets of γδT cells populated ileal mucosa after birth. The predominant subset coexpressed BoCD2, and a smaller subset coexpressed BoCD8. WC1+ γδT cells comprised the smallest subset. All γδT cell subsets coexpressed ACT2, a molecule expressed on activated WC1+ and WC1− γδT cells from cattle.
Keywords: Mucosa, Ileum, TcR1+ lymphocytes, Calves
References
- Baldwin C.L., Teale A.J., Naessens J.G., Goddeeris B.M., MacHugh N.D., Morrison W.I. Characterisation of a subset of bovine T lymphocytes that express BoT4 by monoclonal antibodies and function: similarity to lymphocytes defined by human T4 and murine L3T4. J. Immunol. 1986;136:4385–4391. [PubMed] [Google Scholar]
- Bandeira A., Itohara S., Bonneville M., Burlen-Defranoux O., Mota-Santos T., Coutinho A., Tonegawa S. Vol. 88. 1991. Extrathymic origin of intestinal intraepithelial lymphocytes bearing T-cell antigen receptor γδ; pp. 43–47. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bjorneby J.M., Riggs M.W., Perryman L.E. Cryptosporidium parvum merozoites share neutralization-sensitive epitopes with sporozoites. J. Immunol. 1990;145:298–304. [PubMed] [Google Scholar]
- Bland P.W., Warren L.G. Antigen presentation by epithelial cells of the rat small intestine. II. selective induction of suppressor T cells. Immunology. 1986;58:9–14. [PMC free article] [PubMed] [Google Scholar]
- Chiodini R.J., Davis W.C. The cellular immunology of bovine paratuberculosis: the predominant response is mediated by cytotoxic gamma/delta T lymphocytes which prevent CD4+ activity. Microb. Pathogenesis. 1992;13:447–463. doi: 10.1016/0882-4010(92)90012-d. [DOI] [PubMed] [Google Scholar]
- Crocker G., Sopp P., Parsons K., Davis W.C., Howard C.J. Analysis of the γδ T cell restricted antigen WC1. Vet. Immunol. Immunopathol. 1993;39:137–144. doi: 10.1016/0165-2427(93)90174-3. [DOI] [PubMed] [Google Scholar]
- Davis W.C., Splitter G.S. Bovine CD2. Vet. Immunol. Immunopathol. 1991;27:43–45. doi: 10.1016/0165-2427(91)90077-p. [DOI] [PubMed] [Google Scholar]
- Davis W.C., Marusic S., Lewin H.A., Splitter G.A., Perryman L.E., McGuire T.C., Gorham J.R. The development and analysis of species specific and cross reactive monoclonal antibodies to leukocyte differentiation antigens and antigens of the major histocompatibility complex for use in the study of the immune system in cattle and other species. Vet. Immunol. Immunopathol. 1987;15:337–376. doi: 10.1016/0165-2427(87)90005-5. [DOI] [PubMed] [Google Scholar]
- Davis W.C., Hamilton N.J., Park Y.H., Larsen R.A., Wyatt C.R., Okada K. Ruminant leukocyte differentiation molecules. In: Barta O., editor. MHC, Differentiation Antigens and Cytokines in Animals and Birds. Monographs in Animal Immunology. BAR-LAB; Blacksburg, VA: 1990. pp. 47–70. [Google Scholar]
- Davis W.C., MacHugh N.D., Park Y.H., Hamilton M.J., Wyatt C.R. Identification of a monoclonal antibody reactive with the bovine orthologue of CD3 (BoCD3) Vet. Immunol. Immunopathol. 1993;39:85–91. doi: 10.1016/0165-2427(93)90167-3. [DOI] [PubMed] [Google Scholar]
- Ellis J.A., Baldwin C.L., MacHugh N.D., Bensaid A., Teale A.J., Goddeeris B.M., Norrison W.I. Characterization by a monoclonal antibody and functional analysis of a subset of bovine T lymphocytes that express BoT8, a molecule analogous to human CD8. Immunology. 1986;58:351–358. [PMC free article] [PubMed] [Google Scholar]
- Griebel P.J., Kennedy L., Graham T., Davis W.C., Reynolds J.D. Characterization of B-cell phenotypic changes during ileal and jejunal Peyer's patch development in sheep. Immunology. 1992;77:564–570. [PMC free article] [PubMed] [Google Scholar]
- Hein W.R. Ontogeny of T cells. In: Goddeeris B.M.L., Morrison W.A., editors. Cell-mediated Immunity in Ruminants. CRC Press; Boca Raton, FL: 1994. pp. 19–35. [Google Scholar]
- Hein W.R., Mackay C.R. Prominence of γδT cells in the ruminant immune system. Immunol. Today. 1991;12:30–33. doi: 10.1016/0167-5699(91)90109-7. [DOI] [PubMed] [Google Scholar]
- Howard C.J., Morrison W.A. The leukocytes: markers, tissue distribution and functional characterization. In: Goddeeris B.M.L., Morrison W.A., editors. Cell-Mediated Immunity in Ruminants. CRC Press; Boca Raton, FL: 1994. pp. 1–17. [Google Scholar]
- Howard C.J., Sopp P., Parsons K.R. L-selectin expression differentiates T cells isolated from different lymphoid tissues in cattle but does not correlate with memory. Immunol. 1992;77:228–234. [PMC free article] [PubMed] [Google Scholar]
- Kraehenbuhl J-P., Neutra M.R. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol. Rev. 1992;72:853–879. doi: 10.1152/physrev.1992.72.4.853. [DOI] [PubMed] [Google Scholar]
- Lefrançois L. Vol. 3. 1991. Intraepithelial lymphocytes of the intestinal mucosa: curiouser and curiouser; pp. 99–108. (Semin. Immunol.). [PubMed] [Google Scholar]
- MacHugh N.D., Taracha E.L., Toye P.G. Reactivity of workshop antibodies on L cell and COS cell transfectants expressing bovine CD antigens. Vet. Immunol. Immunopathol. 1993;39:61–67. doi: 10.1016/0165-2427(93)90164-y. [DOI] [PubMed] [Google Scholar]
- MacHugh N.D., Wijngaard P.L.J., Clevers H.C., Davis W.C. Clustering of monoclonal antibodies recognizing different members of the WC1 gene family. Vet. Immunol. Immunopathol. 1993;39:155–160. doi: 10.1016/0165-2427(93)90176-5. [DOI] [PubMed] [Google Scholar]
- MacHugh N.D., Kamau J., Orden J.A., Davis W.C. 1996. Identification of two ditinct subsets of gamma/delta T cells with unique tissue distribution, cell surface phenotype, and T cell receptor rearrangement. in preparation. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mackay C.R., Hein W.R. A large proportion of bovine T cells express the γδ T cell receptor and show a distinct tissue distribution and surface phenotype. Int. Immunol. 1989;1:540–545. doi: 10.1093/intimm/1.5.540. [DOI] [PubMed] [Google Scholar]
- McClure S.J., Hein W.R., Yamaguchi K., Dudler L., Beya M.F., Miyasaka M. Ontogeny, morphology and tissue distribution of a unique subset of CD4− CD8− sheep T lymphocytes. Immunol. Cell Biol. 1989;67:215–221. doi: 10.1038/icb.1989.33. [DOI] [PubMed] [Google Scholar]
- Morrison W.I., Davis W.C. Differentiation antigens expressed predominantly on CD4− CD8− T lymphocytes (WC1, WC2) Vet. Immunol. Immunopathol. 1991;27:71–76. doi: 10.1016/0165-2427(91)90082-n. [DOI] [PubMed] [Google Scholar]
- Morrison W.I., Baldwin C.L., MacHugh N.D., Teale A.J., Goddeeris B.M., Ellis J. Phenotypic and functional characterisation of bovine lymphocytes. Prog. Vet. Microbiol. Immunol. 1988;4:134–140. [PubMed] [Google Scholar]
- Mukwedeya D.T., Takamatsu H., Parkhouse R.M.E. Identification of bovine B cell reactive and B cell specific monoclonal antibodies. Vet. Immunol. Immunopathol. 1993;39:177–186. doi: 10.1016/0165-2427(93)90179-8. [DOI] [PubMed] [Google Scholar]
- Myers T.J., Schat K.A. Natural killer cell activity of chicken intraepithelial leukocytes against rotavirus-infected target cells. Vet. Immunol. Immunopathol. 1990;26:157–170. doi: 10.1016/0165-2427(90)90064-Y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Park Y.H., Fox L.K., Hamilton M.J., Davis W.C. Suppression of proliferative response of BoCD4+ T lymphocytes by activated BoCD8+ T lymphocytes in the mammary gland of cows with Staphylococcus aureus mastitis. Vet. Immunol. Immunopathol. 1993;36:137–151. doi: 10.1016/0165-2427(93)90103-b. [DOI] [PubMed] [Google Scholar]
- Park Y.H., Jung S.C., Moon J.S., Ku B.G., Wyatt C.R., Hamilton M.J., Fox L.K., Davis W.C. A subset of mammary gland γδ T lymphocytes downregulates BoCD4 T lymphocyte response to Staphylococcus aureus in cattle with intramammary infection. Korean J. Immunol. 1994;16:19–27. [Google Scholar]
- Parsons K.R., Howard C.J., Jones B.V., Sopp P. Investigation of bovine gut associated lymphoid tissue (GALT) using monoclonal antibodies against bovine lymphocytes. Vet. Pathol. 1989;26:396–408. doi: 10.1177/030098588902600505. [DOI] [PubMed] [Google Scholar]
- Parsons K.R., Crocker G., Sopp P., Howard C.J. Identification of monoclonal antibodies specific for the γδ TCR. Vet. Immunol. Immunopathol. 1993;39:161–167. doi: 10.1016/0165-2427(93)90177-6. [DOI] [PubMed] [Google Scholar]
- Sopp P., Howard C.J., Parsons K.R. Investigating monoclonal antibodies to bovine ‘null’ cell antigens using two-colour immunofluorescence. Vet. Immunol. Immunopathol. 1991;27:163–168. doi: 10.1016/0165-2427(91)90095-t. [DOI] [PubMed] [Google Scholar]
- Taguchi T., Aicher W.K., Fujihashi K., Yamamoto M., McGhee J.R., Bluestone J.A., Kiyono H. Novel function for intestinal intraepithelial lymphocytes. Murine CD3+, γδ TycR+ T cells produce IFN-γ and IL-5. J. Immunol. 1991;147:3736–3744. [PubMed] [Google Scholar]
- Waters W.R., Harp J.A., Nonnecke B.J. Phenotypic analysis of peripheral blood lymphocytes and intestinal intraepithelial lymphocytes in calves. Vet. Immunol. Immunopathol. 1995 doi: 10.1016/0165-2427(95)05430-e. in press. [DOI] [PubMed] [Google Scholar]
- Wijngaard P.L.J., Metzelaar M.J., MacHugh N.D., Morrison W.I., Clevers H.C. Molecular characterization of the WC1 antigen expressed specifically on bovine CD4− CD8− T lymphocytes. J. Immunol. 1992;149:3273–3277. [PubMed] [Google Scholar]
- Wilson A.D., Stokes C.R., Bourne F.J. Responses of intraepithelial lymphocytes to T-cell mitogens: a comparison between murine and porcine responses. Immunology. 1986;58:621–625. [PMC free article] [PubMed] [Google Scholar]
- Wyatt C.R., Madruga C., Cluff C., Parish S., Hamilton M.J., Goff W., Davis W.C. Differential distribution of γδT-cell receptor lymphocyte subpopulations in blood and spleen of young and adult cattle. Vet. Immunol. Immunopathol. 1994;40:187–199. doi: 10.1016/0165-2427(94)90019-1. [DOI] [PubMed] [Google Scholar]