Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T11:45:17.632Z Has data issue: false hasContentIssue false

Contribution of in vivo and ex vivo studies to understanding the role of antigen-presenting cells and T cell subsets in immunity to cattle diseases

Published online by Cambridge University Press:  28 February 2007

C. J. Howard*
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire RG20 7NN, UK
J. C. Hope
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire RG20 7NN, UK
B. Villarreal-Ramos
Affiliation:
Institute for Animal Health, Compton, Newbury, Berkshire RG20 7NN, UK
*
*Institute for Animal Health, Compton, Newbury RG20 7NN, UK. E-mail: chris.howard@bbsrc.ac.uk

Abstract

In vivo and ex vivo studies of the immune system in relation to infectious disease that are carried out in the natural target species provide data that are relevant to understanding the biology of the immune cells and immunity to infection. This is particularly the case for diseases that show host specificity. Ex vivo studies that exploit the surgical cannulation of lymphatic ducts have allowed access to natural dendritic cells. Investigations of these cells have revealed the presence of subpopulations that differ in their ability to stimulate T cells and differ in the range of cytokines synthesized. These differences would be forecast to have major effects on the bias and type of immune response that are induced. Studies in vivo of the effect of depleting T-cell populations with monoclonal antibodies (mAbs) have shown how different T-cell populations have differing critical roles for different infectious diseases, and how they may contribute to the immune response and pathology after infection. Here the case is made for how studies in cattle have aided our understanding of immunity to several infections that can be exploited for the rational design of effective vaccination and control strategies.

Type
Research Article
Copyright
Copyright © CAB International 2004

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

Adams, S, van der Laan, LJ, Vernon Wilson, E, Renardel de Lavalette, C, Dopp, EA, Dijkstra, CD, Simmons, D L and van den Berg, T K (1998). Signal-regulatory protein is selectively expressed by myeloid and neuronal cells. Journal of Immunology 161: 18531859.CrossRefGoogle ScholarPubMed
Baldwin, CL, Sathiyaseelan, B, Naiman, B, White, AM, Brown, R, Blumerman,, S and Black, SJ (2002). Activation of bovine peripheral blood γδ T cells for cell division and IFN-γ production. Veterinary Immunology and Immunopathology 87: 251259.Google Scholar
Bruce, CJ, Howard, CJ, Thomas, LH, Tempest,, PR and Taylor, G (1999). Depletion of bovine CD8+ T cells with chCC63, a chimaeric mouse-bovine antibody. Veterinary Immunology and Immunopathology 71: 215231.CrossRefGoogle ScholarPubMed
Bembridge, GP, MacHugh, ND, McKeever, D, Awino, E, Sopp, P, Collins, RA, Gelder, KI and Howard, CJ (1995). CD45RO expression on bovine T cells: relation to biological function. Immunology 86: 537544.Google Scholar
Brooke, GP, Parsons, KR and Howard, CJ (1998). Cloning of two members of the SIRP alpha family of protein tyrosine phosphatase binding proteins in cattle that are expressed on monocytes and a subpopulation of dendritic cells and which mediate binding to CD4 T cells. European Journal of Immunology 28: 111.3.0.CO;2-V>CrossRefGoogle Scholar
Clevers, H, MacHugh, ND, Bensaid, A, Dunlap, S, Baldwin, CL, Kaushal, A, Iams, K, Howard, CJ and Morrison, WI (1990). Identification of a bovine surface antigen uniquely expressed on CD4-CD8– T cell receptor gamma/delta+ T lymphocytes. European Journal of Immunology 20: 809817.CrossRefGoogle ScholarPubMed
Collins, RA, Sopp, P, Gelder, KI, Morrison, WI and Howard, CJ (1996). Bovine gamma/delta TcR+ T lymphocytes are stimulated to proliferate by autologous Theileria annulatainfected cells in the presence of interleukin-2. Scandinavian Journal of Immunology 44: 444452.Google Scholar
Cooper, MA, Fehniger, TA, Fuchs, A, Colonna, M and Caligiuri, MA (2004). NK cell and DC interactions. Trends in Immunology 25: 4752.CrossRefGoogle ScholarPubMed
Fehniger, TA and Caligiuri, MA (2001). Ontogeny and expansion of human natural killer cells: clinical implications. International Reviews of Immunology 20: 503534.CrossRefGoogle ScholarPubMed
Gliddon, DR and Howard, CJ (2002). CD26 is expressed on a restricted subpopulation of dendritic cells in vivo. European Journal of Immunology 32: 14721481.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Gliddon, DR, Hope, JC, Brooke, GP and Howard, CJ (2004). DEC-205 expression on migrating dendritic cells in afferent lymph. Immunology 111: 262272.Google Scholar
Goddeeris, BM, Morrison, WI and Teale, AJ (1986). Generation of bovine cytotoxic cell lines, specific for cells infected with the protozoan parasite Theileria parva and restricted by products of the major histocompatibility complex. European Journal of Immunology 16: 12431249.CrossRefGoogle ScholarPubMed
Haig, DM, Hopkins, J and Miller, HRP (1999). Local immune responses in afferent and efferent lymph. Immunology 96: 155163.CrossRefGoogle ScholarPubMed
Hanby Flarida, MD, Trask, OJ, Yang, TL and Baldwin, CL (1996). Modulation of WC1, a lineage-specific cell surface molecule of gamma/delta T cells augments cellular proliferation. Immunology 88: 116123.CrossRefGoogle ScholarPubMed
Heino, WR and Griebel, PJ (2003). A road less travelled: large animal models in immunological research. Nature Reviews. Immunology 3: 7984.Google Scholar
Hope, JC, Sopp, P, Collins, RA and Howard, CJ (2001). Differences in the induction of CD8+ T-cell responses by subpopulations of dendritic cells from afferent lymph are related to IL-1 alpha secretion. Journal of Leukocyte Biology 69: 271279.CrossRefGoogle ScholarPubMed
Hope, JC, Sopp, P and Howard, C J (2002). NK-like CD8 (+) cells in immunologically naive neonatal calves that respond to dendritic cells infected with Mycobacterium bovis BCG. Journal of Leukocyte Biology 71: 184194.CrossRefGoogle ScholarPubMed
Hotary, KB, Yana, I, Sabeh, F, Li, XY, Holmbeck, K, Birkedal-Hansen, H, Allen, ED, Hiraoka, N and Weiss, SJ (2002). Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. Journal of Experimental Medicine 195: 295308.CrossRefGoogle ScholarPubMed
Howard, CJ and Hope, JC (2000). Dendritic cells, implications on function from studies of the afferent lymph veiled cell. Veterinary Immunology and Immunopathology 77: 113.CrossRefGoogle ScholarPubMed
Howard, CJ and Morrison, WI (1994). The leukocytes: markers, tissue distribution and functional characterisation. In Goddeeris, BM and Morrison, WI (editors). Cell mediated Immunity in Ruminants. Boca Raton: CRC Press, pp 118.Google Scholar
Howard, CJ, Sopp, P, Parsons, KR and Finch, J (1989). In vivo depletion of BoT4 (CD4) and of non-T4/T8 lymphocyte subsets in cattle with monoclonal antibodies. European Journal of Immunology 19: 757764.CrossRefGoogle ScholarPubMed
Howard, CJ, Sopp, P, Parsons, KR, McKeever, DJ, Taracha, EL, Jones, BV, MacHugh, ND and Morrison, WI (1991). Distinction of naive and memory BoCD4 lymphocytes in calves with a monoclonal antibody, CC76, to a restricted determinant of the bovine leukocyte-common antigen, CD45. European Journal of Immunology 21: 22192226.CrossRefGoogle ScholarPubMed
Howard, CJ, Clarke, MC, Sopp, P and Brownlie, J (1992). Immunity to bovine virus diarrhoea virus in calves: the role of different T-cell subpopulations analysed by specific depletion in vivo with monoclonal antibodies. Veterinary Immunology and Immunopathology 32: 303314.Google Scholar
Howard, CJ, Sopp, P, Brownlie, J, Kwong, LS, Parsons, KR and Taylor, G (1997). Identification of two distinct populations of dendritic cells in afferent lymph that vary in their ability to stimulate T cells. Journal of Immunology 159: 53725382.CrossRefGoogle ScholarPubMed
Howard, CJ, Collins, RA, Sopp, P, Brooke, GP, Kwong, LS, Parsons, KR, Weynants, V, Letesson, JJ and Bembridge, GP (1999). T-cell responses and the influence of dendritic cells in cattle. Advances in Veterinary Medicine 41: 275288.CrossRefGoogle ScholarPubMed
Howard, CJ, Hope, JC, Stephens, SA, Gliddon, DR and Brooke, GP (2002). Co-stimulation and modulation of the ensuing immune response. Veterinary Immunology and Immunopathology 87: 123130.CrossRefGoogle ScholarPubMed
Huang, FP, Platt, N, Wykes, M, Major, JR, Powell, TJ, Jenkins, CD and MacPherson, GG (2000). A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. Journal of Experimental Medicine 191: 435443.Google Scholar
Kennedy, HE, Welsh, MD, Bryson, DG, Cassidy, JP, Forster, FI, Howard, CJ, Collins, RA and Pollock, TM (2002) Modulation of immune responses to Mycobacterium bovis in cattle depleted of WC1 + γδ T cells. Infection and Immunity 70: 14881500.CrossRefGoogle Scholar
Liu, L, Zhang, M, Jenkins, C and MacPherson, GG (1998). Dendritic cell heterogeneity in vivo: two functionally different dendritic cell populations in rat intestinal lymph can be distinguished by CD4 expression. Journal of Immunology 161: 11461155.CrossRefGoogle ScholarPubMed
MacHugh, ND, Wijngaard, PL, Clevers, HC and Davis, WC (1993). Clustering of monoclonal antibodies recognizing different members of the WC1 gene family. Veterinary Immunology and Immunopathology 39: 155160.CrossRefGoogle ScholarPubMed
Mackay, CR, Marston, WL and Dudler, L (1990). Naive and memory T cells show distinct pathways of lymphocyte recirculation. Journal of Experimental Medicine 171: 801817.CrossRefGoogle ScholarPubMed
McKeever, DJ, MacHugh, ND, Goddeeris, BM, Awino, E and Morrison, WI (1991). Bovine afferent lymph veiled cells differ from blood monocytes in phenotype and accessory function. Journal of Immunology 147: 37033709.CrossRefGoogle ScholarPubMed
Mempel, TR, Henrickson, SE and Von Andrian, UH (2004). T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154159.CrossRefGoogle ScholarPubMed
Moretta, A (2002). Natural killer cells and dendritic cells: rendezvous in abused tissues Nature Reviews. Immunology 2: 957964.Google Scholar
Naessens, J, Scheerlinck, JP, De Buysscher, EV, Kennedy, D and Sileghem, M (1998). Effective in vivo depletion of T cell subpopulations and loss of memory cells in cattle using mouse monoclonal antibodies. Veterinary Immunology and Immunopathology 64: 219234.CrossRefGoogle ScholarPubMed
Naessens, J, Mwangi, DM, Buza, J and Moloo, SK (2003). Local skin reaction (chancre) induced following inoculation of metacyclic trypanosomes in cattle by tsetse flies is dependent on CD4 T lymphocytes. Parasite Immunology 25: 413419.CrossRefGoogle ScholarPubMed
Morrison, WI and Goddeeris, BM (1990). Cytotoxic T cells in immunity to Theileria parva in cattle. Current Topics in Microbiology and Immunology 155: 7993.Google ScholarPubMed
Okragly, AJ, Hanby-Flarida, M, Mann, D and Baldwin, CL (1996). Bovine g/d T-cell proliferation is associated with self-derived molecules constitutively expressed in vivo on mononuclear phagocytes. Immunology 87: 7179.Google Scholar
Oldham, G, Bridger, JC, Howard, CJ and Parsons, KR (1993). In vivo role of lymphocyte subpopulations in the control of virus excretion and mucosal antibody responses of cattle infected with rotavirus. Journal of Virology 67: 50125019.CrossRefGoogle ScholarPubMed
Olsson, T, Bakhiet, M, Hojeberg, B, Ljungdahl, A, Edlund, C, Andersson, G, Ekre, HP, Fung-Leung, WP, Mak, T, Wigzell, H, Wigzell, H, Fiszer, U and Kristensson, K (1993). CD8 is critically involved in lymphocyte activation by a T. brucei brucei-released molecule. Cell 72: 715727.CrossRefGoogle Scholar
Ostman, A and Bohmer, FD (2001). Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatases. Trends in Cell Biology 11: 258266.Google Scholar
Proost, P, Struyf, S, Schols, D, Opdenakker, G, Sozzani, S, Allavena, P, Mantovani, A, Augustyns, K, Bal, G, Haemers, A, Lambeir, AM, Scharpe, S, Van Damme, J and DeMeester, I (1999). Truncation of macrophage-derived chemokine by CD26/ dipeptidyl-peptidase IV beyond its predicted cleavage site affects chemotactic activity and CC chemokine receptor 4 interaction. Journal of Biological Chemistry 274: 39883993.CrossRefGoogle ScholarPubMed
Pulendran, B, Smith, JL, Caspary, G, Brasel, K, Pettit, D, Maraskovsky, E and Maliszewski, CR (1999). Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proceedings of the National Academy of Sciences of the United States of America 96: 10361041.Google Scholar
Rissoan, MC, Soumelis, V, Kadowaki, N, Grouard, G, Briere, F, Malefyt, RW and Liu, YJ (1999). Reciprocal control of T helper cell and dendritic cell differentiation. Science 283: 11831186.CrossRefGoogle ScholarPubMed
Rottenberg, ME, Bakhiet, M, Olsson, T, Kristensson, K, Mak, T, Wigzell, H and Orn, A (1993). Differential susceptibilities of mice genomically deleted of CD4 and CD8 to infections with Trypanosoma cruzi or Trypanosoma brucei. Infection and Immunity 61: 51295133.CrossRefGoogle ScholarPubMed
Seiffert, M, Brossart, P, Cant, C, Cella, M, Colonna, M, Brugger, W, Kanz, L, Ullrich, A and Buhring, HJ (2001). Signal-regulatory protein alpha (SIRPalpha) but not SIRPbeta is involved in T-cell activation, binds to CD47 with high affinity and is expressed on immature CD34(+)CD38(–) hematopoietic cells. Blood 97: 27412749.CrossRefGoogle Scholar
Sileghem, M and Naessens, J (1995). Are CD8 T cells involved in control of African trypanosomiasis in a natural host environment? European Journal of Immunology 25: 19651971.CrossRefGoogle Scholar
Smith, RE, Patel, V, Seatter, SD, Deehan, MR, Brown, MH, Brooke, GP, Goodridge, HS, Howard, CJ, Rigley, KP, Harnett, W and Harnett, MM (2003). A novel MyD-1 (SIRPα1alpha) signaling pathway that inhibits LPS-induced TNFalpha production by monocytes. Blood 102: 25322540.Google Scholar
Sopp, P and Howard, CJ (2001). IFN-γ and IL-4 production by CD4, CD8 and WC1 γδ T cells from cattle lymph nodes and blood. Veterinary Immunology and Immunopathology 81: 8596.CrossRefGoogle Scholar
Stephens, SA, Brownlie, J, Charleston, B and Howard, CJ (2003). Differences in cytokine synthesis by the sub-populations of dendritic cells from afferent lymph. Immunology 110: 4857.Google Scholar
Storset, AK, Kulberg, S, Berg, I, Boysen, P, Hope, JC and Dissen, E (2004). NKp46 defined a subset of bovine leukocytes with natural killer cell characteristics. European Journal of Immunology 34: 669676.CrossRefGoogle ScholarPubMed
Struyf, S, De Meester, I, Scharpe, S, Lenaerts, JP, Menten, P, Wang, JM, Proost, P and Van Damme, J (1998). Natural truncation of RANTES abolishes signaling through the CC chemokine receptors CCR1 and CCR3, impairs its chemotactic potency and generates a CC chemokine inhibitor. European Journal of Immunology 28: 12621271.Google Scholar
Takamatsu, HH, Kirkham, PA and Parkhouse, RME (1997). A gamma/delta cell specific surface receptor (WC1) signalling G0/G1 cell cycle arrest. European Journal of Immunology 27: 105110.Google Scholar
Tani, K, Ogushi, F, Huang, L, Kawano, T, Tada, H, Hariguchi, N and Sone, S (2000). CD13 aminopeptidase N, a novel chemoattractant for T lymphocytes in pulmonary sarcoidosis. American Journal of Respiratory and Critical Care Medicine 161: 16361642.Google Scholar
Taylor, G, Thomas, LH, Wyld, SG, Furze, J, Sopp, P and Howard, CJ (1995). Role of T-lymphocyte subsets in recovery from respiratory syncytial virus infection in calves. Journal of Virology 69: 66586664.CrossRefGoogle ScholarPubMed
Thomas, LH, Cook, RS, Howard, CJ, Gaddum, RM and Taylor, G (1996). Influence of selective T-lymphocyte depletion on the lung pathology of gnotobiotic calves and the distribution of different T-lymphocyte subsets following challenge with bovine respiratory syncytial virus. Research in Veterinary Science 61: 3844.CrossRefGoogle ScholarPubMed
Trinchieri, G (2003). Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nature reviews. Immunology 3: 133146.CrossRefGoogle ScholarPubMed
Valdez, RA, McGuire, TC, Brown, WC, Davis, WC and Knowles, DP (2001). Long-term in vivo depletion of functional CD4+ T lymphocytes from calves requires both thymectomy and anti-CD4 monoclonal antibody treatment. Immunology 102: 426433.CrossRefGoogle ScholarPubMed
Valdez, RA, McGuire, TC, Brown, WC, Davis, WC and Knowles, DP (2000). An in vivo model to investigate lymphocyte-mediated immunity during acute hemoparasitic infections. Use of a monoclonal antibody to selectively deplete CD4+ T lymphocytes from thymectomized calves. Annals of the New York Academy of Sciences 916: 233236.CrossRefGoogle Scholar
Valdez, RA, McGuire, TC, Brown, WC, Davis, WC, Jordan, JM and Knowles, DP (2002). Selective in vivo depletion of CD4 (+) T lymphocytes with anti-CD4 monoclonal antibody during acute infection of calves with Anaplasma marginale. Clinical and Diagnostic Laboratory Immunology 9: 417424.Google ScholarPubMed
Villarreal-Ramos, B, McAulay, M, Chance, V, Martin, M, Morgan, J and Howard, CJ (2003). Investigation of the role of CD8+ T cells in bovine tuberculosis in vivo. Infection and Immunity 71: 42974303.CrossRefGoogle ScholarPubMed
Vremec, D, Pooley, J, Hochrein, H, Wu, L and Shortman, K (2000). CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. Journal of Immunology 164: 29782986.CrossRefGoogle ScholarPubMed
Werling, D, Hope, JC, Chaplin, P, Collins, RA, Taylor, G and Howard, C J (1999). Involvement of caveolae in the uptake of respiratory syncytial virus antigen by dendritic cells. Journal of Leukocyte Biology 66: 5058.CrossRefGoogle ScholarPubMed
Wijngaard, PL, MacHugh, ND, Metzelaar, MJ, Romberg, S, Bensaid, A, Pepin, L, Davis, W C and Clevers, HC (1994). Members of the novel WC1 gene family are differentially expressed on subsets of bovine CD4-CD8- gamma delta T lymphocytes Journal of Immunology 152 34763482.Google Scholar