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Published in: Medical Microbiology and Immunology 5-6/2018

01-11-2018 | Original Investigation

Cellular distribution of CD200 receptor in rats and its interaction with cytomegalovirus e127 protein

Authors: Mohamed A. El-Mokhtar, Agnieszka Bauer, Julia Madela, Sebastian Voigt

Published in: Medical Microbiology and Immunology | Issue 5-6/2018

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Abstract

CD200 is a membrane protein that interacts with CD200R on the surface of immune cells and delivers an inhibitory signal. In this study, we characterized the distribution of inhibitory CD200R in rats. In addition, we investigated if e127, a homologue of rat CD200 expressed by rat cytomegalovirus (RCMV), can suppress immune functions in vitro. RT-PCR analysis was carried out to test the expression of CD200R in different rat tissues and flow cytometry was performed to characterize CD200R at the cellular level. To test the inhibitory functions of e127, a co-culture system was utilized in which immune cells were incubated with e127-expressing cells. The strongest CD200R expression was detected in lymphoid organs such as bone marrow and spleen. Flow cytometry analyses showed that CD200R+ cells were mainly CD4 dendritic cells (DC) and CD4+ T cells in the spleen. In blood, nearly all monocytes and granulocytes expressed CD200R and in bone marrow the NKRP1low subset of natural killer cells highly expressed CD200R. In addition, both peritoneal macrophages and the NR8383 macrophage cell line carried CD200R. At the functional level, viral e127 conferred an inhibitory signal on TNFα and IL6 cytokine release from IFNγ-stimulated macrophages. However, e127 did not affect the cytotoxic activity of DC. CD200R in the rat is mainly expressed on myeloid cells but also on non-myeloid cell subsets, and RCMV e127 can deliver inhibitory signals to immune cells by engaging CD200R. The RCMV model provides a useful tool to study potential immune evasion mechanisms of the herpesviridae and opens new avenues for understanding and controlling herpesvirus infections.
Literature
1.
go back to reference Wright GJ, Puklavec MJ, Willis AC, Hoek RM, Sedgwick JD, Brown MH, Barclay AN (2000) Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity 13(2):233–242CrossRef Wright GJ, Puklavec MJ, Willis AC, Hoek RM, Sedgwick JD, Brown MH, Barclay AN (2000) Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity 13(2):233–242CrossRef
2.
go back to reference Chen Z, Kapus A, Khatri I, Kos O, Zhu F, Gorczynski RM (2018) Cell membrane-bound CD200 signals both via an extracellular domain and following nuclear translocation of a cytoplasmic fragment. Leuk Res 69:72–80CrossRef Chen Z, Kapus A, Khatri I, Kos O, Zhu F, Gorczynski RM (2018) Cell membrane-bound CD200 signals both via an extracellular domain and following nuclear translocation of a cytoplasmic fragment. Leuk Res 69:72–80CrossRef
3.
go back to reference Mihrshahi R, Barclay AN, Brown MH (2009) Essential roles for Dok2 and RasGAP in CD200 receptor-mediated regulation of human myeloid cells. J Immunol 183(8):4879–4886CrossRef Mihrshahi R, Barclay AN, Brown MH (2009) Essential roles for Dok2 and RasGAP in CD200 receptor-mediated regulation of human myeloid cells. J Immunol 183(8):4879–4886CrossRef
4.
go back to reference Lyons A, McQuillan K, Deighan BF, O’Reilly JA, Downer EJ, Murphy AC, Watson M, Piazza A, O’Connell F, Griffin R, Mills KH, Lynch MA (2009) Decreased neuronal CD200 expression in IL-4-deficient mice results in increased neuroinflammation in response to lipopolysaccharide. Brain Behav Immun 23(7):1020–1027CrossRef Lyons A, McQuillan K, Deighan BF, O’Reilly JA, Downer EJ, Murphy AC, Watson M, Piazza A, O’Connell F, Griffin R, Mills KH, Lynch MA (2009) Decreased neuronal CD200 expression in IL-4-deficient mice results in increased neuroinflammation in response to lipopolysaccharide. Brain Behav Immun 23(7):1020–1027CrossRef
5.
go back to reference Lyons A, Griffin RJ, Costelloe CE, Clarke RM, Lynch MA (2007) IL-4 attenuates the neuroinflammation induced by amyloid-beta in vivo and in vitro. J Neurochem 101(3):771–781CrossRef Lyons A, Griffin RJ, Costelloe CE, Clarke RM, Lynch MA (2007) IL-4 attenuates the neuroinflammation induced by amyloid-beta in vivo and in vitro. J Neurochem 101(3):771–781CrossRef
6.
go back to reference Avdic S, McSharry BP, Steain M, Poole E, Sinclair J, Abendroth A, Slobedman B (2016) Human cytomegalovirus-encoded human interleukin-10 (IL-10) homolog amplifies its immunomodulatory potential by upregulating human IL-10 in monocytes. J Virol 90(8):3819–3827CrossRef Avdic S, McSharry BP, Steain M, Poole E, Sinclair J, Abendroth A, Slobedman B (2016) Human cytomegalovirus-encoded human interleukin-10 (IL-10) homolog amplifies its immunomodulatory potential by upregulating human IL-10 in monocytes. J Virol 90(8):3819–3827CrossRef
7.
go back to reference Gonzalez-Motos V, Kropp KA, Viejo-Borbolla A (2016) Chemokine binding proteins: an immunomodulatory strategy going viral. Cytokine Growth Factor Rev 30:71–80CrossRef Gonzalez-Motos V, Kropp KA, Viejo-Borbolla A (2016) Chemokine binding proteins: an immunomodulatory strategy going viral. Cytokine Growth Factor Rev 30:71–80CrossRef
8.
go back to reference Guven-Maiorov E, Tsai CJ, Nussinov R (2016) Pathogen mimicry of host protein–protein interfaces modulates immunity. Semin Cell Dev Biol 58:136–145CrossRef Guven-Maiorov E, Tsai CJ, Nussinov R (2016) Pathogen mimicry of host protein–protein interfaces modulates immunity. Semin Cell Dev Biol 58:136–145CrossRef
9.
go back to reference Estep RD, Rawlings SD, Li H, Manoharan M, Blaine ET, O’Connor MA, Messaoudi I, Axthelm MK, Wong SW (2014) The rhesus rhadinovirus CD200 homologue affects immune responses and viral loads during in vivo infection. J Virol 88(18):10635–10654CrossRef Estep RD, Rawlings SD, Li H, Manoharan M, Blaine ET, O’Connor MA, Messaoudi I, Axthelm MK, Wong SW (2014) The rhesus rhadinovirus CD200 homologue affects immune responses and viral loads during in vivo infection. J Virol 88(18):10635–10654CrossRef
10.
go back to reference Griffin BD, Verweij MC, Wiertz EJ (2010) Herpesviruses and immunity: the art of evasion. Vet Microbiol 143(1):89–100CrossRef Griffin BD, Verweij MC, Wiertz EJ (2010) Herpesviruses and immunity: the art of evasion. Vet Microbiol 143(1):89–100CrossRef
11.
go back to reference Favier B (2016) Regulation of neutrophil functions through inhibitory receptors: an emerging paradigm in health and disease. Immunol Rev 273(1):140–155CrossRef Favier B (2016) Regulation of neutrophil functions through inhibitory receptors: an emerging paradigm in health and disease. Immunol Rev 273(1):140–155CrossRef
12.
go back to reference Gompels UA, Nicholas J, Lawrence G, Jones M, Thomson BJ, Martin ME, Efstathiou S, Craxton M, Macaulay HA (1995) The DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution. Virology 209(1):29–51CrossRef Gompels UA, Nicholas J, Lawrence G, Jones M, Thomson BJ, Martin ME, Efstathiou S, Craxton M, Macaulay HA (1995) The DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution. Virology 209(1):29–51CrossRef
13.
go back to reference Nicholas J (1996) Determination and analysis of the complete nucleotide sequence of human herpesvirus 7. J Virol 70(9):5975–5989PubMedPubMedCentral Nicholas J (1996) Determination and analysis of the complete nucleotide sequence of human herpesvirus 7. J Virol 70(9):5975–5989PubMedPubMedCentral
14.
go back to reference Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, Moore PS (1996) Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA 93(25):14862–14867CrossRef Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, Moore PS (1996) Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA 93(25):14862–14867CrossRef
15.
go back to reference Foster-Cuevas M, Wright GJ, Puklavec MJ, Brown MH, Barclay AN (2004) Human herpesvirus 8 K14 protein mimics CD200 in down-regulating macrophage activation through CD200 receptor. J Virol 78(14):7667–7676CrossRef Foster-Cuevas M, Wright GJ, Puklavec MJ, Brown MH, Barclay AN (2004) Human herpesvirus 8 K14 protein mimics CD200 in down-regulating macrophage activation through CD200 receptor. J Virol 78(14):7667–7676CrossRef
16.
go back to reference Shiratori I, Yamaguchi M, Suzukawa M, Yamamoto K, Lanier LL, Saito T, Arase H (2005) Down-regulation of basophil function by human CD200 and human herpesvirus-8 CD200. J Immunol 175(7):4441–4449CrossRef Shiratori I, Yamaguchi M, Suzukawa M, Yamamoto K, Lanier LL, Saito T, Arase H (2005) Down-regulation of basophil function by human CD200 and human herpesvirus-8 CD200. J Immunol 175(7):4441–4449CrossRef
17.
go back to reference Misstear K, Chanas SA, Rezaee SA, Colman R, Quinn LL, Long HM, Goodyear O, Lord JM, Hislop AD, Blackbourn DJ (2012) Suppression of antigen-specific T cell responses by the Kaposi’s sarcoma-associated herpesvirus viral OX2 protein and its cellular orthologue, CD200. J Virol 86(11):6246–6257CrossRef Misstear K, Chanas SA, Rezaee SA, Colman R, Quinn LL, Long HM, Goodyear O, Lord JM, Hislop AD, Blackbourn DJ (2012) Suppression of antigen-specific T cell responses by the Kaposi’s sarcoma-associated herpesvirus viral OX2 protein and its cellular orthologue, CD200. J Virol 86(11):6246–6257CrossRef
18.
go back to reference Mousavinezhad-Moghaddam M, Amin AA, Rafatpanah H, Rezaee SAR (2016) A new insight into viral proteins as immunomodulatory therapeutic agents: KSHV vOX2 a homolog of human CD200 as a potent anti-inflammatory protein. Iran J Basic Med Sci 19(1):2–13PubMedPubMedCentral Mousavinezhad-Moghaddam M, Amin AA, Rafatpanah H, Rezaee SAR (2016) A new insight into viral proteins as immunomodulatory therapeutic agents: KSHV vOX2 a homolog of human CD200 as a potent anti-inflammatory protein. Iran J Basic Med Sci 19(1):2–13PubMedPubMedCentral
19.
go back to reference Langlais CL, Jones JM, Estep RD, Wong SW (2006) Rhesus rhadinovirus R15 encodes a functional homologue of human CD200. J Virol 80(6):3098–3103CrossRef Langlais CL, Jones JM, Estep RD, Wong SW (2006) Rhesus rhadinovirus R15 encodes a functional homologue of human CD200. J Virol 80(6):3098–3103CrossRef
20.
go back to reference Salata C, Curtarello M, Calistri A, Sartori E, Sette P, de Bernard M, Parolin C, Palu G (2009) vOX2 glycoprotein of human herpesvirus 8 modulates human primary macrophages activity. J Cell Physiol 219(3):698–706CrossRef Salata C, Curtarello M, Calistri A, Sartori E, Sette P, de Bernard M, Parolin C, Palu G (2009) vOX2 glycoprotein of human herpesvirus 8 modulates human primary macrophages activity. J Cell Physiol 219(3):698–706CrossRef
21.
go back to reference Zhang L, Stanford M, Liu J, Barrett C, Jiang L, Barclay AN, McFadden G (2009) Inhibition of macrophage activation by the myxoma virus M141 protein (vCD200). J Virol 83(18):9602–9607CrossRef Zhang L, Stanford M, Liu J, Barrett C, Jiang L, Barclay AN, McFadden G (2009) Inhibition of macrophage activation by the myxoma virus M141 protein (vCD200). J Virol 83(18):9602–9607CrossRef
22.
go back to reference Cameron CM, Barrett JW, Liu L, Lucas AR, McFadden G (2005) Myxoma virus M141R expresses a viral CD200 (vOX-2) that is responsible for down-regulation of macrophage and T-cell activation in vivo. J Virol 79(10):6052–6067CrossRef Cameron CM, Barrett JW, Liu L, Lucas AR, McFadden G (2005) Myxoma virus M141R expresses a viral CD200 (vOX-2) that is responsible for down-regulation of macrophage and T-cell activation in vivo. J Virol 79(10):6052–6067CrossRef
23.
go back to reference Jackson SE, Mason GM, Wills MR (2011) Human cytomegalovirus immunity and immune evasion. Virus Res 157(2):151–160CrossRef Jackson SE, Mason GM, Wills MR (2011) Human cytomegalovirus immunity and immune evasion. Virus Res 157(2):151–160CrossRef
24.
go back to reference Baca Jones CC, Kreklywich CN, Messaoudi I, Vomaske J, McCartney E, Orloff SL, Nelson JA, Streblow DN (2009) Rat cytomegalovirus infection depletes MHC II in bone marrow derived dendritic cells. Virology 388(1):78–90CrossRef Baca Jones CC, Kreklywich CN, Messaoudi I, Vomaske J, McCartney E, Orloff SL, Nelson JA, Streblow DN (2009) Rat cytomegalovirus infection depletes MHC II in bone marrow derived dendritic cells. Virology 388(1):78–90CrossRef
25.
go back to reference Voigt S, Mesci A, Ettinger J, Fine JH, Chen P, Chou W, Carlyle JR (2007) Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 26(5):617–627CrossRef Voigt S, Mesci A, Ettinger J, Fine JH, Chen P, Chou W, Carlyle JR (2007) Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 26(5):617–627CrossRef
26.
go back to reference Gruijthuijsen YK, Casarosa P, Kaptein SJ, Broers JL, Leurs R, Bruggeman CA, Smit MJ, Vink C (2002) The rat cytomegalovirus R33-encoded G protein-coupled receptor signals in a constitutive fashion. J Virol 76(3):1328–1338CrossRef Gruijthuijsen YK, Casarosa P, Kaptein SJ, Broers JL, Leurs R, Bruggeman CA, Smit MJ, Vink C (2002) The rat cytomegalovirus R33-encoded G protein-coupled receptor signals in a constitutive fashion. J Virol 76(3):1328–1338CrossRef
27.
go back to reference Stals FS, Zeytinoglu A, Havenith M, de Clercq E, Bruggeman CA (1993) Rat cytomegalovirus-induced pneumonitis after allogeneic bone marrow transplantation: effective treatment with (S)-1-(3-hydroxy-2-phosphonyl-methoxypropyl) cytosine. Antimicrob Agents Chemother 37(2):218–223CrossRef Stals FS, Zeytinoglu A, Havenith M, de Clercq E, Bruggeman CA (1993) Rat cytomegalovirus-induced pneumonitis after allogeneic bone marrow transplantation: effective treatment with (S)-1-(3-hydroxy-2-phosphonyl-methoxypropyl) cytosine. Antimicrob Agents Chemother 37(2):218–223CrossRef
28.
go back to reference Trinite B, Chauvin C, Peche H, Voisine C, Heslan M, Josien R (2005) Immature CD4− CD103+ rat dendritic cells induce rapid caspase-independent apoptosis-like cell death in various tumor and nontumor cells and phagocytose their victims. J Immunol 175(4):2408–2417CrossRef Trinite B, Chauvin C, Peche H, Voisine C, Heslan M, Josien R (2005) Immature CD4 CD103+ rat dendritic cells induce rapid caspase-independent apoptosis-like cell death in various tumor and nontumor cells and phagocytose their victims. J Immunol 175(4):2408–2417CrossRef
29.
go back to reference Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA (2008) Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325:397–415PubMedPubMedCentral Streblow DN, Dumortier J, Moses AV, Orloff SL, Nelson JA (2008) Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr Top Microbiol Immunol 325:397–415PubMedPubMedCentral
30.
go back to reference Voigt S, Sandford GR, Hayward GS, Burns WH (2005) The English strain of rat cytomegalovirus (CMV) contains a novel captured CD200 (vOX2) gene and a spliced CC chemokine upstream from the major immediate-early region: further evidence for a separate evolutionary lineage from that of rat CMV Maastricht. J Gen Virol 86(Pt 2):263–274CrossRef Voigt S, Sandford GR, Hayward GS, Burns WH (2005) The English strain of rat cytomegalovirus (CMV) contains a novel captured CD200 (vOX2) gene and a spliced CC chemokine upstream from the major immediate-early region: further evidence for a separate evolutionary lineage from that of rat CMV Maastricht. J Gen Virol 86(Pt 2):263–274CrossRef
31.
go back to reference Kwong LS, Akkaya M, Barclay AN, Hatherley D (2016) Herpesvirus orthologues of CD200 bind host CD200R but not related activating receptors. J Gen Virol 97(1):179–184CrossRef Kwong LS, Akkaya M, Barclay AN, Hatherley D (2016) Herpesvirus orthologues of CD200 bind host CD200R but not related activating receptors. J Gen Virol 97(1):179–184CrossRef
32.
go back to reference Foster-Cuevas M, Westerholt T, Ahmed M, Brown MH, Barclay AN, Voigt S (2011) Cytomegalovirus e127 protein interacts with the inhibitory CD200 receptor. J Virol 85(12):6055–6059CrossRef Foster-Cuevas M, Westerholt T, Ahmed M, Brown MH, Barclay AN, Voigt S (2011) Cytomegalovirus e127 protein interacts with the inhibitory CD200 receptor. J Virol 85(12):6055–6059CrossRef
33.
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRef Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRef
34.
go back to reference Trinite B, Voisine C, Yagita H, Josien R (2000) A subset of cytolytic dendritic cells in rat. J Immunol 165(8):4202–4208CrossRef Trinite B, Voisine C, Yagita H, Josien R (2000) A subset of cytolytic dendritic cells in rat. J Immunol 165(8):4202–4208CrossRef
35.
go back to reference Sedgwick JD, Ford AL, Foulcher E, Airriess R (1998) Central nervous system microglial cell activation and proliferation follows direct interaction with tissue-infiltrating T cell blasts. J Immunol 160(11):5320–5330PubMed Sedgwick JD, Ford AL, Foulcher E, Airriess R (1998) Central nervous system microglial cell activation and proliferation follows direct interaction with tissue-infiltrating T cell blasts. J Immunol 160(11):5320–5330PubMed
36.
go back to reference Kheradmand T, Trivedi PP, Wolf NA, Roberts PC, Swanborg RH (2008) Characterization of a subset of bone marrow-derived natural killer cells that regulates T cell activation in rats. J Leukoc Biol 83(5):1128–1135CrossRef Kheradmand T, Trivedi PP, Wolf NA, Roberts PC, Swanborg RH (2008) Characterization of a subset of bone marrow-derived natural killer cells that regulates T cell activation in rats. J Leukoc Biol 83(5):1128–1135CrossRef
37.
go back to reference Tanaka T, Masuko T, Yagita H, Tamura T, Hashimoto Y (1989) Characterization of a CD3-like rat T cell surface antigen recognized by a monoclonal antibody. J Immunol 142(8):2791–2795PubMed Tanaka T, Masuko T, Yagita H, Tamura T, Hashimoto Y (1989) Characterization of a CD3-like rat T cell surface antigen recognized by a monoclonal antibody. J Immunol 142(8):2791–2795PubMed
38.
go back to reference Smith T, Groom A, Zhu B, Turski L (2000) Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6(1):62–66CrossRef Smith T, Groom A, Zhu B, Turski L (2000) Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6(1):62–66CrossRef
39.
go back to reference Brenan M, Puklavec M (1992) The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 175(6):1457–1465CrossRef Brenan M, Puklavec M (1992) The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 175(6):1457–1465CrossRef
40.
go back to reference Nady S, Shata MT, Mohey MA, El-Shorbagy A (2017) Protective role of IL-22 against Schistosoma mansoni soluble egg antigen-induced granuloma in vitro. Parasite Immunol 39 (1)CrossRef Nady S, Shata MT, Mohey MA, El-Shorbagy A (2017) Protective role of IL-22 against Schistosoma mansoni soluble egg antigen-induced granuloma in vitro. Parasite Immunol 39 (1)CrossRef
41.
go back to reference Dijkstra CD, Van Vliet E, Dopp EA, van der Lelij AA, Kraal G (1985) Marginal zone macrophages identified by a monoclonal antibody: characterization of immuno- and enzyme-histochemical properties and functional capacities. Immunology 55(1):23–30PubMedPubMedCentral Dijkstra CD, Van Vliet E, Dopp EA, van der Lelij AA, Kraal G (1985) Marginal zone macrophages identified by a monoclonal antibody: characterization of immuno- and enzyme-histochemical properties and functional capacities. Immunology 55(1):23–30PubMedPubMedCentral
42.
go back to reference Gotoh S, Itoh M, Fujii Y, Arai S, Sendo F (1986) Enhancement of the expression of a rat neutrophil-specific cell surface antigen by activation with phorbol myristate acetate and concanavalin A. J Immunol 137(2):643–650PubMed Gotoh S, Itoh M, Fujii Y, Arai S, Sendo F (1986) Enhancement of the expression of a rat neutrophil-specific cell surface antigen by activation with phorbol myristate acetate and concanavalin A. J Immunol 137(2):643–650PubMed
43.
go back to reference Robinson AP, White TM, Mason DW (1986) Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57(2):239–247PubMedPubMedCentral Robinson AP, White TM, Mason DW (1986) Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57(2):239–247PubMedPubMedCentral
44.
go back to reference Minas K, Liversidge J (2006) Is the CD200/CD200 receptor interaction more than just a myeloid cell inhibitory signal? Crit Rev Immunol 26(3):213–230CrossRef Minas K, Liversidge J (2006) Is the CD200/CD200 receptor interaction more than just a myeloid cell inhibitory signal? Crit Rev Immunol 26(3):213–230CrossRef
45.
go back to reference Barclay AN (1981) The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology 42(4):593–600PubMedPubMedCentral Barclay AN (1981) The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology 42(4):593–600PubMedPubMedCentral
46.
go back to reference Barclay AN (1981) Different reticular elements in rat lymphoid tissue identified by localization of Ia, Thy-1 and MRC OX 2 antigens. Immunology 44(4):727–736PubMedPubMedCentral Barclay AN (1981) Different reticular elements in rat lymphoid tissue identified by localization of Ia, Thy-1 and MRC OX 2 antigens. Immunology 44(4):727–736PubMedPubMedCentral
47.
go back to reference Wright GJ, Cherwinski H, Foster-Cuevas M, Brooke G, Puklavec MJ, Bigler M, Song Y, Jenmalm M, Gorman D, McClanahan T, Liu MR, Brown MH, Sedgwick JD, Phillips JH, Barclay AN (2003) Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J Immunol 171(6):3034–3046CrossRef Wright GJ, Cherwinski H, Foster-Cuevas M, Brooke G, Puklavec MJ, Bigler M, Song Y, Jenmalm M, Gorman D, McClanahan T, Liu MR, Brown MH, Sedgwick JD, Phillips JH, Barclay AN (2003) Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J Immunol 171(6):3034–3046CrossRef
48.
go back to reference Barclay AN, Wright GJ, Brooke G, Brown MH (2002) CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol 23(6):285–290CrossRef Barclay AN, Wright GJ, Brooke G, Brown MH (2002) CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol 23(6):285–290CrossRef
49.
go back to reference Mehta M, Hetta HF, Abdel-Hameed EA, Rouster SD, Hossain M, Mekky MA, Khalil NK, Mohamed WA, El-Feky MA, Ahmed SH, Daef EA, El-Mokhtar MA, Abdelwahab SF, Medhat A, Sherman KE, Shata MT (2016) Association between IL28B rs12979860 single nucleotide polymorphism and the frequency of colonic Treg in chronically HCV-infected patients. Arch Virol 161(11):3161–3169CrossRef Mehta M, Hetta HF, Abdel-Hameed EA, Rouster SD, Hossain M, Mekky MA, Khalil NK, Mohamed WA, El-Feky MA, Ahmed SH, Daef EA, El-Mokhtar MA, Abdelwahab SF, Medhat A, Sherman KE, Shata MT (2016) Association between IL28B rs12979860 single nucleotide polymorphism and the frequency of colonic Treg in chronically HCV-infected patients. Arch Virol 161(11):3161–3169CrossRef
50.
go back to reference Geyer H, Hartung E, Mages HW, Weise C, Beluzic R, Vugrek O, Jonjic S, Kroczek RA, Voigt S (2014) Cytomegalovirus expresses the chemokine homologue vXCL1 capable of attracting XCR1+ CD4− dendritic cells. J Virol 88(1):292–302CrossRef Geyer H, Hartung E, Mages HW, Weise C, Beluzic R, Vugrek O, Jonjic S, Kroczek RA, Voigt S (2014) Cytomegalovirus expresses the chemokine homologue vXCL1 capable of attracting XCR1+ CD4 dendritic cells. J Virol 88(1):292–302CrossRef
51.
go back to reference Trivedi PP, Roberts PC, Wolf NA, Swanborg RH (2005) NK cells inhibit T cell proliferation via p21-mediated cell cycle arrest. J Immunol 174(8):4590–4597CrossRef Trivedi PP, Roberts PC, Wolf NA, Swanborg RH (2005) NK cells inhibit T cell proliferation via p21-mediated cell cycle arrest. J Immunol 174(8):4590–4597CrossRef
52.
go back to reference Smeltz RB, Wolf NA, Swanborg RH (1999) Inhibition of autoimmune T cell responses in the DA rat by bone marrow-derived NK cells in vitro: implications for autoimmunity. J Immunol 163(3):1390–1397PubMed Smeltz RB, Wolf NA, Swanborg RH (1999) Inhibition of autoimmune T cell responses in the DA rat by bone marrow-derived NK cells in vitro: implications for autoimmunity. J Immunol 163(3):1390–1397PubMed
53.
go back to reference Lyons A, Downer EJ, Crotty S, Nolan YM, Mills KH, Lynch MA (2007) CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4. J Neurosci 27(31):8309–8313CrossRef Lyons A, Downer EJ, Crotty S, Nolan YM, Mills KH, Lynch MA (2007) CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4. J Neurosci 27(31):8309–8313CrossRef
54.
go back to reference Pietila M, Lehtonen S, Tuovinen E, Lahteenmaki K, Laitinen S, Leskela HV, Natynki A, Pesala J, Nordstrom K, Lehenkari P (2012) CD200 positive human mesenchymal stem cells suppress TNF-alpha secretion from CD200 receptor positive macrophage-like cells. PLoS One 7(2):e31671CrossRef Pietila M, Lehtonen S, Tuovinen E, Lahteenmaki K, Laitinen S, Leskela HV, Natynki A, Pesala J, Nordstrom K, Lehenkari P (2012) CD200 positive human mesenchymal stem cells suppress TNF-alpha secretion from CD200 receptor positive macrophage-like cells. PLoS One 7(2):e31671CrossRef
55.
go back to reference Gorczynski RM (2001) Transplant tolerance modifying antibody to CD200 receptor, but not CD200, alters cytokine production profile from stimulated macrophages. Eur J Immunol 31(8):2331–2337CrossRef Gorczynski RM (2001) Transplant tolerance modifying antibody to CD200 receptor, but not CD200, alters cytokine production profile from stimulated macrophages. Eur J Immunol 31(8):2331–2337CrossRef
56.
go back to reference Rolle A, Olweus J (2009) Dendritic cells in cytomegalovirus infection: viral evasion and host countermeasures. APMIS 117(5–6):413–426CrossRef Rolle A, Olweus J (2009) Dendritic cells in cytomegalovirus infection: viral evasion and host countermeasures. APMIS 117(5–6):413–426CrossRef
57.
go back to reference Coles SJ, Wang EC, Man S, Hills RK, Burnett AK, Tonks A, Darley RL (2011) CD200 expression suppresses natural killer cell function and directly inhibits patient anti-tumor response in acute myeloid leukemia. Leukemia 25(5):792–799CrossRef Coles SJ, Wang EC, Man S, Hills RK, Burnett AK, Tonks A, Darley RL (2011) CD200 expression suppresses natural killer cell function and directly inhibits patient anti-tumor response in acute myeloid leukemia. Leukemia 25(5):792–799CrossRef
58.
go back to reference Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369(6475):31–37CrossRef Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369(6475):31–37CrossRef
59.
go back to reference Yang Q, Goding SR, Hokland ME, Basse PH (2006) Antitumor activity of NK cells. Immunol Res 36(1–3):13–25CrossRef Yang Q, Goding SR, Hokland ME, Basse PH (2006) Antitumor activity of NK cells. Immunol Res 36(1–3):13–25CrossRef
60.
go back to reference Coles SJ, Hills RK, Wang EC, Burnett AK, Man S, Darley RL, Tonks A (2012) Increased CD200 expression in acute myeloid leukemia is linked with an increased frequency of FoxP3+ regulatory T cells. Leukemia 26(9):2146–2148CrossRef Coles SJ, Hills RK, Wang EC, Burnett AK, Man S, Darley RL, Tonks A (2012) Increased CD200 expression in acute myeloid leukemia is linked with an increased frequency of FoxP3+ regulatory T cells. Leukemia 26(9):2146–2148CrossRef
61.
go back to reference Tonks A, Hills R, White P, Rosie B, Mills KI, Burnett AK, Darley RL (2007) CD200 as a prognostic factor in acute myeloid leukaemia. Leukemia 21(3):566–568CrossRef Tonks A, Hills R, White P, Rosie B, Mills KI, Burnett AK, Darley RL (2007) CD200 as a prognostic factor in acute myeloid leukaemia. Leukemia 21(3):566–568CrossRef
62.
go back to reference McWhirter JR, Kretz-Rommel A, Saven A, Maruyama T, Potter KN, Mockridge CI, Ravey EP, Qin F, Bowdish KS (2006) Antibodies selected from combinatorial libraries block a tumor antigen that plays a key role in immunomodulation. Proc Natl Acad Sci USA 103(4):1041–1046CrossRef McWhirter JR, Kretz-Rommel A, Saven A, Maruyama T, Potter KN, Mockridge CI, Ravey EP, Qin F, Bowdish KS (2006) Antibodies selected from combinatorial libraries block a tumor antigen that plays a key role in immunomodulation. Proc Natl Acad Sci USA 103(4):1041–1046CrossRef
63.
go back to reference Moreaux J, Hose D, Reme T, Jourdan E, Hundemer M, Legouffe E, Moine P, Bourin P, Moos M, Corre J, Mohler T, De Vos J, Rossi JF, Goldschmidt H, Klein B (2006) CD200 is a new prognostic factor in multiple myeloma. Blood 108(13):4194–4197CrossRef Moreaux J, Hose D, Reme T, Jourdan E, Hundemer M, Legouffe E, Moine P, Bourin P, Moos M, Corre J, Mohler T, De Vos J, Rossi JF, Goldschmidt H, Klein B (2006) CD200 is a new prognostic factor in multiple myeloma. Blood 108(13):4194–4197CrossRef
64.
go back to reference Kretz-Rommel A, Qin F, Dakappagari N, Ravey EP, McWhirter J, Oltean D, Frederickson S, Maruyama T, Wild MA, Nolan MJ, Wu D, Springhorn J, Bowdish KS (2007) CD200 expression on tumor cells suppresses antitumor immunity: new approaches to cancer immunotherapy. J Immunol 178(9):5595–5605CrossRef Kretz-Rommel A, Qin F, Dakappagari N, Ravey EP, McWhirter J, Oltean D, Frederickson S, Maruyama T, Wild MA, Nolan MJ, Wu D, Springhorn J, Bowdish KS (2007) CD200 expression on tumor cells suppresses antitumor immunity: new approaches to cancer immunotherapy. J Immunol 178(9):5595–5605CrossRef
Metadata
Title
Cellular distribution of CD200 receptor in rats and its interaction with cytomegalovirus e127 protein
Authors
Mohamed A. El-Mokhtar
Agnieszka Bauer
Julia Madela
Sebastian Voigt
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
Medical Microbiology and Immunology / Issue 5-6/2018
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-018-0552-3

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