Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-19T00:03:12.978Z Has data issue: false hasContentIssue false

Cellular infiltration at skin lesions and draining lymph nodes of sheep infested with adult Hyalomma anatolicum anatolicum ticks

Published online by Cambridge University Press:  15 July 2005

D. K. V. BOPPANA
Affiliation:
Departments of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai 500007, India
S. K. WIKEL
Affiliation:
Center for Microbial Pathogenesis, School of Medicine, University of Connecticut Health Center, 263 Farmington Avenue, MC3710, Farmington, CT 06030, USA
D. G. RAJ
Affiliation:
Animal Biotechnology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai 500007, India
M. B. MANOHAR
Affiliation:
Veterinary Pathology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai 500007, India
J. LALITHA
Affiliation:
Departments of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai 500007, India

Abstract

Immunohistochemical analysis of skin and draining lymph nodes of sheep repeatedly infested with the ixodid tick Hyalomma anatolicum anatolicum were studied for different antigen-presenting cells and lymphocyte subpopulations. Infiltration of neutrophils, macrophages and lymphocytes adjacent to the tick bite site were observed. Skin biopsies showed significant increases in dermal infiltration of CD8+ and γδ+ T cells at 72 h and 8 days after both primary and secondary infestation. Infiltrations of MHC-II DR/DQ decreased at 72 h after tick infestation, whereas significant increases were recorded for 8-day skin biopsies. CD1+ cellular infiltrations were observed during secondary infestations at the dermis. Decreased ratios of CD4[ratio ]CD8 T cells and MHC-II[ratio ]CD1 antigen-presenting cells were observed in both infestations compared to healthy skin biopsies. Ratios of αβ[ratio ]γδ T cells increased gradually during infestation compared to uninfested skin. The regional lymph nodes from tick-infested sheep showed an increased CD8+, γδ+ T and CD1+ cellular infiltration compared to control lymph nodes. CD4+ T cells were decreased. There were no significant changes in CD45R+ cellular infiltration either at skin lesions or regional lymph nodes.

Type
Research Article
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allen, J. R. ( 1973). Tick resistance: basophils in skin reactions of resistant guineapigs. International Journal for Parasitology 3, 195200.CrossRefGoogle Scholar
Allen, J. R., Doube, B. M. and Kemp, D. H. ( 1977). Histology of bovine skin reactions to Ixodes holocyclus, Neuman. Canadian Journal of Comparative Medicine 41, 2635.Google Scholar
Allen, J. R., Khalil, H. M. and Wikel, S. K. ( 1979). Langerhans cells trap tick salivary gland antigens in tick-resistant guinea-pigs. Journal of Immunology 122, 563565.Google Scholar
Beaudouin, E., Kanny, G., Guerin, B., Guerin, L., Plenat, F. and Moneret-Vautrin, D. A. ( 1997). Unusual manifestations of hypersensitivity after a tick bite: report of two cases. Annals of Allergy, Asthma and Immunology 79, 4346.CrossRefGoogle Scholar
Berenberg, J. L., Ward, P. A. and Sonenshine, D. E. ( 1972). Tick-bite injury: mediation by complement-derived chemotactic factor. Journal of Immunology 109, 451456.Google Scholar
Bergman, D. K., Palmer, M. J., Caimano, M. J., Rodolf, J. D. and Wikel, S. K. ( 2000). Isolation and molecular cloning of a secreted immunosuppressant protein from Dermacentor andersoni salivary gland. Journal of Parasitology 86, 516525.CrossRefGoogle Scholar
Bockenstedt, L. K., Shanafelt, M. C., Belperron, A., Mao, J. and Barthold, S. W. ( 2003). Humoral immunity reflects altered T helper cell bias in Borrelia burgdorferi infected γδ T-cell-deficit mice. Infection and Immunity 71, 29382940.CrossRefGoogle Scholar
Boppana, D. K. V., Dhinakar Raj, G., John Lalitha., Wikel, S. K., Latha, B. R. and Gomathinayagam, S. ( 2004). In vivo immunomodulatory effects of ixodid ticks on ovine circulating T- and B-lymphocytes. Parasite Immunology 26, 8393.CrossRefGoogle Scholar
Bos, J. D., Hagenaars, C., Das, P. K., Krieg, S. R., Vroom, W. J. and Kapsenberg, M. L. ( 1989). Predominance of ‘memory’ T cells (CD4+ CDw29+) over ‘naïve’ T cells (CD4+ CD45R+) in both normal and diseased human skin. Archives of Dermatology Research 281, 2430.CrossRefGoogle Scholar
Bos, J. D. and Kapsenberg, M. L. ( 1993). The skin immune system: progress in cutaneous biology. Immunology Today 14, 7578.CrossRefGoogle Scholar
Brossard, M. and Fivaz, V. ( 1982). Ixodes ricinus L: mast cells, basophils and eosinophils in the sequence of cellular events in the skin of infested or reinfested rabbits. Parasitology 85, 583592.CrossRefGoogle Scholar
Brossard, M. and Wikel, S. K. ( 2004). Tick immunobiology. Parasitology 129, S161S167.CrossRefGoogle Scholar
Brown, W. C., Davis, W. C., Choi, S. H., Dobbelaere, D. A. E. and Splitter, G. A. ( 1994). Functional and phenotypic characterization of WCI+ γδ+ T cells isolated from Babesia bovis – stimulated T cell lines. Cellular Immunology 153, 927.CrossRefGoogle Scholar
Daubenberger, C. A., Taracha, E. L., Gaideelis, L., Davis, W. C. and Mc Keever, D. J. ( 1999). Bovine γδ+ T cell responses to the intracellular protozoan parasite. Infection and Immunity 67, 22412249.Google Scholar
Ferreira, B. R., Szabo, M. J. P., Cavassani, K. A., Bechara, G. H. and Silva, J. S. ( 2003). Antigens from Rhipicephalus sanguineus ticks elicit potent cell-mediated immune responses in resistant but not in susceptible animals. Veterinary Parasitology 115, 3548.CrossRefGoogle Scholar
Gill, H. S. ( 1986). Kinetics of mast cell, basophil and eosinophils populations at Hyalomma anatolicum feeding sites on cattle and the acquisition of resistance. Journal of Parasitology 93, 305315.CrossRefGoogle Scholar
Gill, H. S. and Walker, A. R., ( 1984). Histological analysis of tick feeding sites during acquisition of resistance of Hyalomma anatolicum anatolicum. Proceedings of the British Society for Parasitology, Spring meeting, 1984. Parasitology 89, IXXiV.Google Scholar
Gillespie, R. D., Dolan, M. C., Piesman, J. and Titus, R. G. ( 2001). Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick, Ixodes scapularis. Journal of Immunology 166, 43194326.CrossRefGoogle Scholar
Jorundsson, E., Press, C. MCL. and Landsverk, T. ( 2000). Distribution of MHC-II and CD1 molecules in the skin of lambs and changes during experimentally-induced contact hypersensitivity. Veterinary Immunology and Immunopathology 74, 87101.CrossRefGoogle Scholar
Jutila, M. A. ( 1996), γ/δ T cell/endothelial cell interactions. Veterinary Immunology and Immunopathology 54, 105110.CrossRefGoogle Scholar
Mackay, C. R., Maddox, J. F., Gogolin-Ewens, K. J. and Brandon, M. R. ( 1985), Characterization of two sheep lymphocyte differentiation antigens, SBU-T1 and SBU-T6. Immunology 55, 729737.Google Scholar
Mackay, C. R., Maddox, J. F. and Brandon, M. R. ( 1987). A monoclonal antibody to the P220 component of sheep LCA identifies B cells and a unique lymphocyte subset. Cellular Immunology 110, 4655.CrossRefGoogle Scholar
Mackay, C. R., Maddox, J. F., Wijffels, G. L., Mackay, I. R. and Waker, I. D. ( 1988). Characterization of a 95,000 molecule on sheep leucocyte homologous to murine pgp-1 and human CD44. Immunology 65, 9399.Google Scholar
Mackay, C. R. ( 2001). Chemokines: immunology's high impact factors. Nature, Immunology 2, 9599.CrossRefGoogle Scholar
Maddox, J. F., Mackay, C. R. and Brandon, M. R. ( 1985). Surface antigens, SBU-T4 and SBU-T8 of sheep T lymphocyte subsets defined by monoclonal antibodies. Immunology 55, 739748.Google Scholar
Mbow, M. L., Rutti, B. and Brossard, M. ( 1994). Infiltration of CD4+, CD8+ T cells, and expression of ICAM-1, Ia antigens, IL-1α and TNF-α in the skin lesion of BALB/c mice undergoing repeated infestations with nymphal Ixodes ricinus ticks. Immunology 82, 596602.Google Scholar
Meeusen Els, N. T. ( 1998). Differential migration of Th1 and Th2 cells-implications for vaccine and infection studies. Veterinary Immunology and Immunopathology 63, 157166.CrossRefGoogle Scholar
Nash, A. D., Egan, P. J., Kimpton, W., Elhay, M. J. and Bowels, V. M. ( 1996). Local cell traffic and cytokine production associated with ectoparasite infection. Veterinary Immunology and Immunopathology 54, 269279.CrossRefGoogle Scholar
Nuttall, P. A. and Labuda, M. ( 2003). Dynamics of infection in tick vectors and at the tick-host interface, Advances in Virus Research 60, 233272.Google Scholar
Palmer, A., Grewal, A. S. and Dhillon, P. ( 1996). Immunological cross-reactivity between salivary gland proteins of Hyalomma anatolicum anatolicum and Boophilus microplus ticks. Veterinary Immunology and Immunopathology 51, 345352.Google Scholar
Puri, N. K., Gogolin-Ewens, K. J. and Brandon, M. R. ( 1987). Monoclonal antibodies to sheep MHC class I and class II molecules: biochemical characterization of three class I gene products and four distinct subpopulations of class II molecules. Veterinary Immunology and Immunopathology 15, 5986.CrossRefGoogle Scholar
Ribeiro, J. M. C. ( 1989). Role of saliva in tick/host interactions. Experimental and Applied Acarology 7, 1520.CrossRefGoogle Scholar
Riek, R. F. ( 1962). Studies on the reactions of animals to infestation with ticks. VI. Resistance of cattle to infestation with the tick Boophilus microplus. Australian Journal of Agricultural Research 13, 532550.Google Scholar
Scheger, A. V. and Lincoln, D. T. ( 1976). Boophilus microplus: characterization of enzymes introduced into the host. Australian Journal of Biological Sciences 29, 482497.Google Scholar
Schoeler, G. B., Manweiler, S. A. and Wikel, S. K. ( 1999). Ixodes scapularis: effects of repeated infestations with pathogen-free nymphs on macrophage and T lymphocyte cytokine responses of Balb/c and C3H/HeN mice. Experimental Parasitology 92, 239248.CrossRefGoogle Scholar
Schoeler, G. B. and Wikel, S. K. ( 2001). Modulation of host immunity by haematophagous arthropods. Annals of Tropical Medical and Parasitology 95, 755771.CrossRefGoogle Scholar
Silberberg-Sinakin, I., Thorbecke, G. J., Baer, R. L., Rosenthal, S. A. and Berezowksy, V. ( 1976). Antigen-bearing Langerhans cells skin, dermal lymphatics and in lymph nodes. Cellular Immunology 25, 137.CrossRefGoogle Scholar
Snedecor, G. W. and Cochran, W. G. ( 1980). Stastical Methods. Iowa State University Press, Ames, Iowa, USA.
Spada, F. M., Grant, E. P., Peters, P. J., Sugita, M., Melian, A., Leslie, D. S., Lee, H. K., Van Donselaar, E., Hanson, D. A., Krensky, A. M., Majdic, O., Porcelli, S. A., Morita, C. T. and Brenner, M. B. ( 2000). Self-recognition of CD1 by gamma/delta T cells: implications for innate immunity. Journal of Experimental Medicine 191, 937948.CrossRefGoogle Scholar
Wikel, S. K. ( 1982). Immune responses to arthropods and their products. Annual Review of Entomology 27, 2148.CrossRefGoogle Scholar
Wikel, S. K. ( 1996). Host immunity to ticks. Annual Review of Entomology 41, 122.CrossRefGoogle Scholar
Wikel, S. K. and Bergman, D. ( 1997). Tick-host immunology: significant advances and challenges opportunities. Parasitology Today 13, 383389.CrossRefGoogle Scholar
Willadsen, P. ( 1980). Immunity to ticks. Advances in Parasitology 18, 293313.CrossRefGoogle Scholar