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Antigen-independent priming: a transitional response of bovine γδ T-cells to infection

Published online by Cambridge University Press:  17 March 2008

Mark A. Jutila ,
Jeff Holderness ,
Jill C. Graff  and
Jodi F. Hedges
Mark A. Jutila*
Affiliation:
Veterinary Molecular Biology, Montana State University, Molecular Bioscience Building, 960 Technology Blvd., Bozeman, MT 59718, USA
Jeff Holderness
Affiliation:
Veterinary Molecular Biology, Montana State University, Molecular Bioscience Building, 960 Technology Blvd., Bozeman, MT 59718, USA
Jill C. Graff
Affiliation:
Veterinary Molecular Biology, Montana State University, Molecular Bioscience Building, 960 Technology Blvd., Bozeman, MT 59718, USA
Jodi F. Hedges
Affiliation:
Veterinary Molecular Biology, Montana State University, Molecular Bioscience Building, 960 Technology Blvd., Bozeman, MT 59718, USA
*
*Corresponding author. E-mail: [email protected]
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Abstract

Analysis of global gene expression in immune cells has provided unique insights into immune system function and response to infection. Recently, we applied microarray and serial analysis of gene expression (SAGE) techniques to the study of γδ T-cell function in humans and cattle. The intent of this review is to summarize the knowledge gained since our original comprehensive studies of bovine γδ T-cell subsets. More recently, we have characterized the effects of mucosal infection or treatment with microbial products or mitogens on gene expression patterns in sorted γδ and αβ T-cells. These studies provided new insights into the function of bovine γδ T-cells and led to a model in which response to pathogen-associated molecular patterns (PAMPs) induces ‘priming’ of γδ T-cells, resulting in more robust responses to downstream cytokine and/or antigen signals. PAMP primed γδ T-cells are defined by up-regulation of a select number of cytokines, including MIP1α and MIP1β, and by antigens such as surface IL2 receptor α (IL-2Rα) and CD69, in the absence of a prototypic marker for an activated γδ T-cell, IFN-γ. Furthermore, PAMP primed γδ T-cells are more capable of proliferation in response to IL-2 or IL-15 in the absence of antigen. PAMPs such as endotoxin, peptidoglycan and β-glucan are effective γδ T-cell priming agents, but the most potent antigen-independent priming agonists defined to date are condensed oligomeric tannins produced by some plants.

Keywords

γδ T-cellslymphocytesimmune systeminnate immunitymyeloid cellgene expressioncattle
Type
Review Article
Information
Animal Health Research Reviews , Volume 9 , Issue 1 , June 2008 , pp. 47 - 57
Copyright
Copyright © Cambridge University Press 2008

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References

Abrahamsen, MS (1998). Bovine T cell responses to Cryptosporidium parvum infection. International Journal of Parasitology 28: 1083–1088.CrossRefGoogle Scholar
Aderem, AA, Cohen, DS, Wright, SD and Cohn, ZA (1986). Bacterial lipopolysaccharides prime macrophages for enhanced release of arachidonic acid metabolites. The Journal of Experimental Medicine 164: 165–179.CrossRefGoogle ScholarPubMed
Ahn, JS, Konno, A, Gebe, JA, Aruffo, A, Hamilton, MJ, Park, YH and Davis, WC (2002). Scavenger receptor cysteine-rich domains 9 and 11 of WC1 are receptors for the WC1 counter receptor. Journal of Leukocyte Biology 72: 382–390.CrossRefGoogle ScholarPubMed
Akiyama, H, Sato, Y, Watanabe, T, Nagaoka, MH, Yoshioka, Y, Shoji, T, Kanda, T, Yamada, K, Totsuka, M and Teshima, R (2005). Dietary unripe apple polyphenol inhibits the development of food allergies in murine models. FEBS Letters 579: 4485–4491.CrossRefGoogle ScholarPubMed
Baldwin, CL, Sathiyaseelan, T, Naiman, B, White, AM, Brown, R, Blumerman, S, Rogers, A and Black, SJ (2002). Activation of bovine peripheral blood gammadelta T cells for cell division and IFN-gamma production. Veterinary Immunology and Immunopathology 87: 251–259.CrossRefGoogle ScholarPubMed
Blackwell, JM, Goswami, T, Evans, CAW, Sibthorpe, D, Papo, N, White, JK, Searle, S, Miller, EN, Peacock, CS, Mohammed, H and Ibrahim, M (2001). SLC11A1 (formerly NRAMP1) and disease resistance. Microreview. Cellular Microbiology 3: 773–784.CrossRefGoogle Scholar
Boismenu, R and Havran, WL (1998). Gammadelta T cells in host defense and epithelial cell biology. Clinical Immunology and Immunopathology 86: 121–133.CrossRefGoogle ScholarPubMed
Born, W, Cady, C, Jones-Carson, J, Mukasa, A, Lahn, M and O'Brien, R (1999). Immunoregulatory functions of gamma delta T cells. Advanced Immunology 71: 77–144.CrossRefGoogle ScholarPubMed
Born, W, Jin, N, Aydintug, M, Wands, J, French, J, Roark, C and O'Brien, R (2007). γδ T lymphocytes – selectable cells within the innate system? Journal of Clinical Immunology 27: 133–144.CrossRefGoogle ScholarPubMed
Born, WK, Reardon, CL and O'Brien, RL (2006). The function of [gamma][delta] T cells in innate immunity. Current Opinion in Immunology 18: 31–38.CrossRefGoogle ScholarPubMed
Brandes, M, Willimann, K and Moser, B (2005). Professional antigen-presentation function by human gammadelta T cells. Science 309: 264–268.CrossRefGoogle ScholarPubMed
Caramalho, I, Lopes-Carvalho, T, Ostler, D, Zelenay, S, Haury, M and Demengeot, J (2003). Regulatory T cells selectively express Toll-like receptors and are activated by lipopolysaccharide. The Journal of Experimental Medicine 197: 403–411.CrossRefGoogle ScholarPubMed
Chen, X, Beutler, JA, McCloud, TG, Loehfelm, A, Yang, L, Dong, HF, Chertov, OY, Salcedo, R, Oppenheim, JJ and Howard, OM (2003). Tannic acid is an inhibitor of CXCL12 (SDF-1alpha)/CXCR4 with antiangiogenic activity. Clinical Cancer Research 9: 3115–3123.Google ScholarPubMed
Ciccone, E, Viale, O, Bottino, C, Pende, D, Migone, N, Casorati, G, Tambussi, G, Moretta, A and Moretta, L (1988). Antigen recognition by human T cell receptor gamma-positive lymphocytes. Specific lysis of allogeneic cells after activation in mixed lymphocyte culture. The Journal of Experimental Medicine 167: 1517–1522.CrossRefGoogle Scholar
Collins, RA, Werling, D, Duggan, SE, Bland, AP, Parsons, KR and Howard, CJ (1998). Gammadelta T cells present antigen to CD4+ alphabeta T cells. Journal of Leukocyte Biology 63: 707–714.CrossRefGoogle ScholarPubMed
Daubenberger, CA, Taracha, EL, Gaidulis, L, Davis, WC and McKeever, DJ (1999). Bovine gammadelta T-cell responses to the intracellular protozoan parasite Theileria parva. Infection and Immunity 67: 2241–2249.CrossRefGoogle Scholar
Davis, WC, Brown, WC, Hamilton, MJ, Wyatt, CR, Orden, JA, Khalid, AM and Naessens, J (1996). Analysis of monoclonal antibodies specific for the [gamma][delta] TcR. Veterinary Immunology and Immunopathology 52: 275–283.CrossRefGoogle ScholarPubMed
Deetz, CO, Hebbeler, AM, Propp, NA, Cairo, C, Tikhonov, I and Pauza, CD (2006). Gamma interferon secretion by human V{gamma}2V{delta}2 T cells after stimulation with antibody against the T cell receptor plus the Toll-like receptor 2 agonist Pam3Cys. Infection and Immunity 74: 4505–4511.CrossRefGoogle Scholar
Egan, PJ and Carding, SR (2000). Downmodulation of the inflammatory response to bacterial infection by gammadelta T cells cytotoxic for activated macrophages. The Journal of Experimental Medicine 191: 2145–2158.CrossRefGoogle ScholarPubMed
Fahrer, AM, Konigshofer, Y, Kerr, EM, Ghandour, G, Mack, DH, Davis, MM and Chien, YH (2001). Attributes of gammadelta intraepithelial lymphocytes as suggested by their transcriptional profile. Proceedings of the National Academy of Sciences of the United States of America 98: 10261–10266.CrossRefGoogle ScholarPubMed
Ferrick, DA, Schrenzel, MD, Mulvania, T, Hsieh, B, Ferlin, WG and Lepper, H (1995). Differential production of interferon-gamma and interleukin-4 in response to Th1- and Th2-stimulating pathogens by gamma delta T cells in vivo. Nature 373: 255–257.CrossRefGoogle ScholarPubMed
Ferrick, DA, King, DP, Jackson, KA, Braun, RK, Tam, S, Hyde, DM and Beaman, BL (2000). Intraepithelial gamma delta T lymphocytes: sentinel cells at mucosal barriers. Springer Seminars in Immunopathology 22: 283–296.CrossRefGoogle ScholarPubMed
Fikri, Y, Denis, O, Pastoret, P and Nyabenda, J (2001). Purified bovine WC1+ gamma delta T lymphocytes are activated by staphylococcal enterotoxins and toxic shock syndrome toxin-1 superantigens: proliferation response, TCR V gamma profile and cytokines expression. Immunology Letters 77: 87–95.CrossRefGoogle ScholarPubMed
Fikri, Y, Pastoret, PP and Nyabenda, J (2002). Costimulatory molecule requirement for bovine WC1+ gammadelta T cells' proliferative response to bacterial superantigens. Scandinavian Journal of Immunology 55: 373–381.CrossRefGoogle ScholarPubMed
Frazier, RA, Papadopoulou, A, Mueller-Harvey, I, Kissoon, D and Green, RJ (2003). Probing protein–tannin interactions by isothermal titration microcalorimetry. Journal of Agricultural and Food Chemistry 51: 5189–5195.CrossRefGoogle ScholarPubMed
Graff, JC and Jutila, MA (2007). Differential regulation of CD11b on γδ T cells and monocytes in response to unripe apple tannins. Journal of Leukocyte Biology 82: 603–607.CrossRefGoogle Scholar
Graff, JC, Behnke, M, Radke, J, White, M and Jutila, MA (2006). A comprehensive SAGE database for the analysis of {gamma} {delta} T cells. International Immunology 18: 613–626.CrossRefGoogle Scholar
Hagerman, AE and Butler, LG (1981). The specificity of proanthocyanidin–protein interactions. Journal of Biological Chemistry 256: 4494–4497.CrossRefGoogle ScholarPubMed
Hayday, AC (2000) [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annual Reviews in Immunology 18: 975–1026.CrossRefGoogle Scholar
Hedges, JF, Cockrell, D, Jackiw, L, Meissner, N and Jutila, MA (2003a). Differential mRNA expression in circulating γδ T lymphocyte subsets defines unique tissue-specific functions. Journal of Leukocyte Biology 73: 306–314.CrossRefGoogle ScholarPubMed
Hedges, JF, Graff, JC and Jutila, MA (2003b). Transcriptional profiling of gamma delta T cells. Journal of Immunology 171: 4959–4964.CrossRefGoogle ScholarPubMed
Hedges, JF, Lubick, KJ and Jutila, MA (2005). γδ T cells respond directly to pathogen associated molecular patterns. Journal of Immunology 174: 6045–6053.CrossRefGoogle ScholarPubMed
Hedges, JF, Buckner, DL, Rask, KM, Kerns, HMM, Jackiw, LO, Trunkle, TC, Pascual, DW and Jutila, MA (2007). Mucosal lymphatic-derived γδ T cells respond early to experimental Salmonella enterocolits by increasing expression of IL-2Rα. Cellular Immunology 246: 8–16.CrossRefGoogle Scholar
Holderness, J, Jackiw, L, Kimmel, E, Kerns, HMM, Radke, M, Hedges, JF, Petrie, C, McCurley, P, Glee, PM, Palecanda, A and Jutila, MA (2007). Select plant tannins induce IL-2Rα up-regulation and augment cell division in γδ T cells. Journal of Immunology 179: 6468–6478.CrossRefGoogle ScholarPubMed
Hou, DX, Masuzaki, S, Hashimoto, F, Uto, T, Tanigawa, S, Fujii, M and Sakata, Y (2007). Green tea proanthocyanidins inhibit cyclooxygenase-2 expression in LPS-activated mouse macrophages: molecular mechanisms and structure–activity relationship. Archives of Biochemistry and Biophysics 460: 67–74.CrossRefGoogle ScholarPubMed
Jameson, J and Havran, WL (2007). Skin gammadelta T-cell functions in homeostasis and wound healing. Immunological Reviews 215: 114–122.CrossRefGoogle ScholarPubMed
Jones, WM, Watts, GM, Robinson, MK, Vestweber, D and Jutila, MA (1997). Comparison of E-selectin-binding glycoprotein ligands on human lymphocytes, neutrophils, and bovine gamma delta T cells. Journal of Immunology 159: 3574–3583.CrossRefGoogle ScholarPubMed
Jutila, MA and Kurk, S (1996). Analysis of bovine gamma delta T cell interactions with E-, P-, and L-selectin. Characterization of lymphocyte on lymphocyte rolling and the effects of O-glycoprotease. Journal of Immunology 156: 289–296.CrossRefGoogle Scholar
Jutila, MA, Wilson, E and Kurk, S (1997). Characterization of an adhesion molecule that mediates leukocyte rolling on 24 h cytokine- or lipopolysaccharide-stimulated bovine endothelial cells under flow conditions. The Journal of Experimental Medicine 186: 1701–1711.CrossRefGoogle ScholarPubMed
Kawai, K, Tsuno, NH, Kitayama, J, Okaji, Y, Yazawa, K, Asakage, M, Hori, N, Watanabe, T, Takahashi, K and Nagawa, H (2004). Epigallocatechin gallate attenuates adhesion and migration of CD8+ T cells by binding to CD11b. Journal of Allergy and Clinical Immunology 113: 1211–1217.CrossRefGoogle ScholarPubMed
Kern, M, Tjaden, Z, Ngiewih, Y, Puppel, N, Will, F, Dietrich, H, Pahlke, G and Marko, D (2005). Inhibitors of the epidermal growth factor receptor in apple juice extract. Molecular Nutrition and Food Research 49: 317–328.CrossRefGoogle ScholarPubMed
Komano, H, Fujiura, Y, Kawaguchi, M, Matsumoto, S, Hashimoto, Y, Obana, S, Mombaerts, P, Tonegawa, S, Yammamoto, H, Itohara, S, Nanno, M and Ishikawa, H (1995). Homeostatic regulation of intestinal epithelia by intraepithelial {gamma} {delta} T cells. Proceedings of the National Academy of Sciences of the United States of America 92: 6147–6151.CrossRefGoogle ScholarPubMed
Kress, E, Hedges, JF and Jutila, MA (2006). Distinct gene expression in human V[delta]1 and V[delta]2 [gamma][delta] T cells following non-TCR agonist stimulation. Molecular Immunology 43: 2002–2011.CrossRefGoogle Scholar
Lahmers, KK, Hedges, JF, Jutila, MA, Deng, M, Abrahamsen, MS and Brown, WC (2006). Comparative gene expression by WC1+ {gamma} {delta} and CD4+ {alpha} {beta} T lymphocytes, which respond to Anaplasma marginale, demonstrates higher expression of chemokines and other myeloid cell-associated genes by WC1+ {gamma} {delta} T cells. Journal of Leukocyte Biology 80: 939–952.CrossRefGoogle Scholar
Lin, Y, Wong, K and Calame, K (1997). Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 276: 596–599.CrossRefGoogle ScholarPubMed
Liu, H, Komai-Koma, M, Xu, D and Liew, FY (2006). Toll-like receptor 2 signaling modulates the functions of CD4+ CD25+ regulatory T cells. Proceedings of the National Academy of Sciences of the United States of America 103: 7048–7053.CrossRefGoogle ScholarPubMed
Lubick, K and Jutila, MA (2006). LTA recognition by bovine {gamma} {delta} T cells involves CD36. Journal of Leukocyte Biology 79: 1268–1270.CrossRefGoogle Scholar
MacHugh, ND, Mburu, JK, Carol, MJ, Wyatt, CR, Orden, JA and Davis, WC (1997). Identification of two distinct subsets of bovine gamma delta T cells with unique cell surface phenotype and tissue distribution. Immunology 92: 340–345.CrossRefGoogle ScholarPubMed
Mak, TW and Ferrick, DA (1998). The gammadelta T cell bridge: linking innate and acquired immunity. Nature Medicine 4: 764–765.CrossRefGoogle ScholarPubMed
Mao, TK, Powel, J, van de, WJ, Keen, CL, Schmitz, HH, Hammerstone, JF and Gershwin, ME (2000). The effect of cocoa procyanidins on the transcription and secretion of interleukin 1 beta in peripheral blood mononuclear cells. Life Sciences 66: 1377–1386.CrossRefGoogle ScholarPubMed
Mao, TK, van de, WJ, Keen, CL, Schmitz, HH and Gershwin, ME (2002a). Effect of cocoa flavanols and their related oligomers on the secretion of interleukin-5 in peripheral blood mononuclear cells. Journal of Medicinal Food 5: 17–22.CrossRefGoogle ScholarPubMed
Mao, TK, van de, WJ, Keen, CL, Schmitz, HH and Gershwin, ME (2002b). Modulation of TNF-alpha secretion in peripheral blood mononuclear cells by cocoa flavanols and procyanidins. Developmental Immunology 9: 135–141.CrossRefGoogle ScholarPubMed
Mao, TK, van de, WJ, Keen, CL, Schmitz, HH and Gershwin, ME (2003). Cocoa flavonols and procyanidins promote transforming growth factor-beta1 homeostasis in peripheral blood mononuclear cells. Experimental Biology and Medicine (Maywood) 228: 93–99.CrossRefGoogle ScholarPubMed
Meissner, N, Radke, J, Hedges, JF, White, M, Behnke, M, Bertolino, S, Abrahamsen, MS and Jutila, MA (2003). Comparative gene expression analysis in circulating γδ T-cell subsets defines distinct immunoregulatory phenotypes and reveals their relationship to myeloid cells. Journal of Immunology 170: 356–364.CrossRefGoogle Scholar
Miyamoto, K, Murayama, T, Nomura, M, Hatano, T, Yoshida, T, Furukawa, T, Koshiura, R and Okuda, T (1993). Antitumor activity and interleukin-1 induction by tannins. Anticancer Research 13: 37–42.Google ScholarPubMed
Mokuno, Y, Matsuguchi, T, Takano, M, Nishimura, H, Washizu, J, Ogawa, T, Takeuchi, O, Akira, S, Nimura, Y and Yoshikai, Y (2000). Expression of Toll-like receptor 2 on gamma delta T cells bearing invariant V gamma 6/V delta 1 induced by Escherichia coli infection in mice. Journal of Immunology 165: 931–940.CrossRefGoogle ScholarPubMed
Moser, B and Brandes, M (2006). Gammadelta T cells: an alternative type of professional APC. Trends in Immunology 27: 112–118.CrossRefGoogle ScholarPubMed
Mwangi, DM, McKeever, DJ, Nyanjui, JK, Barbet, AF and Mahan, SM (2002). Immunisation of cattle against heartwater by infection with Cowdria ruminantium elicits T lymphocytes that recognise major antigenic proteins 1 and 2 of the agent. Veterinary Immunology and Immunopathology 85: 23–32.CrossRefGoogle ScholarPubMed
Naiman, BM, Alt, D, Bolin, CA, Zuerner, R and Baldwin, CL (2001). Protective killed Leptospira borgpetersenii vaccine induces potent Th1 immunity comprising responses by CD4 and gammadelta T lymphocytes. Infection and Immunity 69: 7550–7558.CrossRefGoogle ScholarPubMed
Nevo, Y and Nelson, N (2006). The NRAMP family of metal-ion transporters. Biochimica et Biophysica Acta 1763: 609–620.CrossRefGoogle ScholarPubMed
O'Brien, RL, Yin, X, Huber, SA, Ikuta, K and Born, WK (2000). Depletion of a gamma delta T cell subset can increase host resistance to a bacterial infection. Journal of Immunology 165: 6472–6479.CrossRefGoogle ScholarPubMed
Osakabe, N, Yasuda, A, Natsume, M, Takizawa, T, Terao, J and Kondo, K (2002). Catechins and their oligomers linked by C4→C8 bonds are major cacao polyphenols and protect low-density lipoprotein from oxidation in vitro. Experimental Biology and Medicine (Maywood) 227: 51–56.CrossRefGoogle Scholar
Piskurich, JF, Lin, KI, Lin, Y, Wang, Y, Ting, JP and Calame, K (2000). BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nature Immunology 1: 526–532.CrossRefGoogle ScholarPubMed
Rhodes, SG, Hewinson, RG and Vordermeier, HM (2001). Antigen recognition and immunomodulation by gamma delta T cells in bovine tuberculosis. Journal of Immunology 166: 5604–5610.CrossRefGoogle ScholarPubMed
Rivas, A, Koide, J, Cleary, ML and Engleman, EG (1989). Evidence for involvement of the gamma, delta T cell antigen receptor in cytotoxicity mediated by human alloantigen-specific T cell clones. The Journal of Immunology 142: 1840–1846.CrossRefGoogle ScholarPubMed
Sathiyaseelan, T, Naiman, B, Welte, S, Machugh, N, Black, SJ and Baldwin, CL (2002). Immunological characterization of a gammadelta T-cell stimulatory ligand on autologous monocytes. Immunology 105: 181–189.CrossRefGoogle ScholarPubMed
Shires, J, Theodoridis, E and Hayday, AC (2001). Biological insights into TCRgammadelta+ and TCRalphabeta+ intraepithelial lymphocytes provided by serial analysis of gene expression (SAGE). Immunity 15: 419–434.CrossRefGoogle ScholarPubMed
Shoji, T, Akazome, Y, Kanda, T and Ikeda, M (2004). The toxicology and safety of apple polyphenol extract. Food Chemistry and Toxicology 42: 959–967.CrossRefGoogle ScholarPubMed
Shoji, T, Masumoto, S, Moriichi, N, Akiyama, H, Kanda, T, Ohtake, Y and Goda, Y (2006). Apple procyanidin oligomers absorption in rats after oral administration: analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. Journal of Agricultural Food Chemistry 54: 884–892.CrossRefGoogle ScholarPubMed
Smyth, AJ, Welsh, MD, Girvin, RM and Pollock, JM (2001). In vitro responsiveness of gammadelta T cells from Mycobacterium bovis-infected cattle to mycobacterial antigens: predominant involvement of WC1(+) cells. Infection and Immunity 69: 89–96.CrossRefGoogle ScholarPubMed
Sopp, P and Howard, CJ (2001). IFN gamma and IL-4 production by CD4, CD8 and WC1 gamma delta TCR(+)T cells from cattle lymph nodes and blood. Veterinary Immunology and Immunopathology 81: 85–96.CrossRefGoogle ScholarPubMed
Tokura, T, Nakano, N, Ito, T, Matsuda, H, Nagasako-Akazome, Y, Kanda, T, Ikeda, M, Okumura, K, Ogawa, H and Nishiyama, C (2005). Inhibitory effect of polyphenol-enriched apple extracts on mast cell degranulation in vitro targeting the binding between IgE and FcepsilonRI. Bioscience, Biotechnology and Biochemistry 69: 1974–1977.CrossRefGoogle ScholarPubMed
Tuo, W, Bazer, FW, Davis, WC, Zhu, D and Brown, WC (1999). Differential effects of type I IFNs on the growth of WC1− CD8+ gamma delta T cells and WC1+ CD8− gamma delta T cells in vitro. Journal of Immunology 162: 245–253.CrossRefGoogle ScholarPubMed
Walcheck, B and Jutila, MA (1994). Bovine gamma delta T cells express high levels of functional peripheral lymph node homing receptor (L-selectin). International Immunology 6: 81–91.CrossRefGoogle ScholarPubMed
Wang, L, Das, H, Kamath, A and Bukowski, JF (2001). Human V gamma 2V delta 2 T cells produce IFN-gamma and TNF-‘alpha with an on/off/on cycling pattern in response to live bacterial products. Journal of Immunology 167: 6195–6201.CrossRefGoogle Scholar
Wesch, D, Beetz, S, Oberg, HH, Marget, M, Krengel, K and Kabelitz, D (2006). Direct costimulatory effect of TLR3 ligand poly(I:C) on human {gamma} {delta} T lymphocytes. The Journal of Immunology 176: 1348–1354.CrossRefGoogle ScholarPubMed
Wijngaard, P, MacHugh, ND, Metzelaar, M, Romberg, S, Bensaid, A, Pepin, L, Davis, WC and Cleavers, H (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: 3476–3482.CrossRefGoogle ScholarPubMed
Wilson, E, Aydintug, MK and Jutila, MA (1999). A circulating bovine gamma delta T cell subset, which is found in large numbers in the spleen, accumulates inefficiently in an artificial site of inflammation: correlation with lack of expression of E-selectin ligands and L-selectin. Journal of Immunology 162: 4914–4919.CrossRefGoogle Scholar
Wilson, E, Hedges, JF, Butcher, EC and Jutila, MA (2002). Bovine gammadelta T cell subsets express different patterns of chemokine responsiveness and adhesion molecules: a mechanism for tissue specific gammadelta T cell subset accumulation. Journal of Immunology 169: 4970–4975.CrossRefGoogle Scholar
Zhang, WY, Liu, HQ, Xie, KQ, Yin, LL, Li, Y, Kwik-Uribe, L and Zhu, XZ (2006). Procyanidin dimer B2 [epicatechin-(4beta-8)-epicatechin] suppresses the expression of cyclooxygenase-2 in endotoxin-treated monocytic cells. Biochemistry and Biophysics Research Communications 345: 508–515.CrossRefGoogle Scholar
Zuany-Amorim, C, Ruffie, C, Haile, S, Vargaftig, BB, Pereira, P and Pretolani, M (1998). Requirement for gammadelta T cells in allergic airway inflammation. Science 280: 1265–1267.CrossRefGoogle ScholarPubMed