The signaling networks of the herpesvirus entry mediator (TNFRSF14) in immune regulation

Immunological Reviews

Volumn 244, Issue 1, 2011, Pages 169-187

  Steinberg, Marcos W ^a,b   Cheung, Timothy C ^a,c   Ware, Carl F ^a  

^a BURNHAM INSTITUTE   (United States)

^b Tanabe Research Laboratories   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Asthma; Autoimmunity; Cancer; Cytokines; Inflammation; T cells

Indexed keywords

CD28 ANTIGEN; CONCANAVALIN A; DECOY RECEPTOR 3; DEXTRAN SULFATE; GLYCOPROTEIN; HERPESVIRUS ENTRY MEDIATOR; HYBRID PROTEIN; INTERLEUKIN 13; LYMPHOTOXIN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN BTLA; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; ASTHMA; AUTOIMMUNE DISEASE; BINDING SITE; BLOOD LEVEL; COLITIS; CONTROLLED STUDY; ENTERITIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; HEPATITIS; HERPES SIMPLEX VIRUS 1; HISTOCOMPATIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LISTERIA MONOCYTOGENES; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH17 CELL; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, CD; AUTOIMMUNITY; GENE EXPRESSION; GPI-LINKED PROTEINS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE ACTIVATION; LYMPHOTOXIN BETA RECEPTOR; LYMPHOTOXIN-ALPHA; MICE; MICE, KNOCKOUT; PROTEIN BINDING; RECEPTOR CROSS-TALK; RECEPTORS, IMMUNOLOGIC; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 14; TUMOR NECROSIS FACTOR-ALPHA; VIRAL ENVELOPE PROTEINS;

EID: 80054850189     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2011.01064.x     Document Type: Article

References (125)

1. Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 1996;87:427-436.
2. Spear PG, Manoj S, Yoon M, Jogger CR, Zago A, Myscofski D. Different receptors binding to distinct interfaces on herpes simplex virus gD can trigger events leading to cell fusion and viral entry. Virology 2006;344:17-24.
3. Murphy TL, Murphy KM. Slow down and survive: enigmatic immunoregulation by BTLA and HVEM. Annu Rev Immunol 2010;28:389-411.
4. Ware CF. Network communications: lymphotoxins, LIGHT, and TNF. Annu Rev Immunol 2005;23:787-819.
5. De Trez C, Ware CF. The TNF receptor and Ig superfamily members form an integrated signaling circuit controlling dendritic cell homeostasis. Cytokine Growth Factor Rev 2008;19:277-284.
6. Gavalda N, Gutierrez H, Davies AM. Developmental regulation of sensory neurite growth by the tumor necrosis factor superfamily member LIGHT. J Neurosci 2009;29:1599-1607.
7. Bassols J, Moreno JM, Ortega F, Ricart W, Fernandez-Real JM. Characterization of herpes virus entry mediator as a factor linked to obesity. Obesity 2010;18:239-246.
8. Kim HM, Jeong CS, Choi HS, Kawada T, Yu R. LIGHT/TNFSF14 enhances adipose tissue inflammatory responses through its interaction with HVEM. FEBS Lett 2011;585:579-584.
9. Cheung TC, et al. Unconventional ligand activation of herpesvirus entry mediator signals cell survival. Proc Natl Acad Sci USA 2009;106:6244-6249.
10. Rooney IA, et al. The lymphotoxin-beta receptor is necessary and sufficient for LIGHT-mediated apoptosis of tumor cells. J Biol Chem 2000;275:14307-14315.
11. Cheung TC, et al. Evolutionarily divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway. Proc Natl Acad Sci USA 2005;102:13218-13223.
12. Compaan DM, Gonzalez LC, Tom I, Loyet KM, Eaton D, Hymowitz SG. Attenuating lymphocyte activity: the crystal structure of the BTLA-HVEM complex. J Biol Chem 2005;280:39553-39561.
13. Nelson CA, et al. Structural determinants of herpesvirus entry mediator recognition by murine B and T lymphocyte attenuator. J Immunol 2008;180:940-947.
14. Sedy JR, et al. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol 2005;6:90-98.
15. Bodmer JL, Schneider P, Tschopp J. The molecular architecture of the TNF superfamily. Trends Biochem Sci 2002;27:19-26.
16. Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001;104:487-501.
17. Eck MJ, Beutler B, Kuo G, Sprang SR. Crystallization of trimeric recombinant human tumor necrosis factor (cachectin). J Biol Chem 1988;263:12816-12819.
18. Granger SW, Ware CF. Commentary: turning on LIGHT. J Clin Invest 2001;108:1741-1742.
19. Granger SW, Butrovich KD, Houshmand P, Edwards WR, Ware CF. Genomic characterization of LIGHT reveals linkage to an immune response locus on chromosome 19p13.3 and distinct isoforms generated by alternate splicing or proteolysis. J Immunol 2001;167:5122-5128.
20. Browning JL, et al. Lymphotoxin beta, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell 1993;72:847-856.
21. Crowe PD, et al. A lymphotoxin-beta-specific receptor. Science 1994;264:707-710.
22. Shaikh RB, et al. Constitutive expression of LIGHT on T cells leads to lymphocyte activation, inflammation, and tissue destruction. J Immunol 2001;167:6330-6337.
23. Wang J, et al. The regulation of T cell homeostasis and autoimmunity by T cell derived LIGHT. J Clin Invest 2001;108:1771-1780.
24. Castellano R, et al. Mechanisms regulating expression of the tumor necrosis factor-related light gene. Role of calcium-signaling pathway in the transcriptional control. J Biol Chem 2002;277:42841-42851.
25. Wroblewski VJ, et al. Decoy receptor 3 (DcR3) is proteolytically processed to a metabolic fragment having differential activities against Fas ligand and LIGHT. Biochem Pharmacol 2003;65:657-667.
26. Cheung TC, et al. Polymorphic variants of LIGHT (TNF superfamily-14) alter receptor avidity and bioavailability. J Immunol 2010;185:1949-1958.
27. Cheung TC, et al. T cell intrinsic heterodimeric complexes between HVEM and BTLA determine receptivity to the surrounding microenvironment. J Immunol 2009;183:7286-7296.
28. Pitti RM, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature 1998;396:699-702.
29. Lin WW, Hsieh SL. Decoy receptor 3: a pleiotropic immunomodulator and biomarker for inflammatory diseases, autoimmune diseases and cancer. Biochem Pharmacol 2011;81:838-847.
30. Chen G, Luo D. Over-expression of decoy receptor 3 in gastric precancerous lesions and carcinoma. Ups J Med Sci 2008;113:297-304.
31. Shen HW, Gao SL, Wu YL, Peng SY. Overexpression of decoy receptor 3 in hepatocellular carcinoma and its association with resistance to Fas ligand-mediated apoptosis. World J Gastroenterol 2005;11:5926-5930.
32. Wu Y, et al. Clinical significance of detecting elevated serum DcR3/TR6/M68 in malignant tumor patients. Int J Cancer 2003;105:724-732.
33. Migone TS, et al. TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator. Immunity 2002;16:479-492.
34. Yu KY, Kwon B, Ni J, Zhai Y, Ebner R, Kwon BS. A newly identified member of tumor necrosis factor receptor superfamily (TR6) suppresses LIGHT-mediated apoptosis. J Biol Chem 1999;274:13733-13736.
35. Zhan C, et al. Decoy strategies: the structure of TL1A:DcR3 complex. Structure 2011;19:162-171.
36. Hayashi S, Miura Y, Tateishi K, Takahashi M, Kurosaka M. Decoy receptor 3 is highly expressed in patients with rheumatoid arthritis. Mod Rheumatol 2010;20:63-68.
37. Han B, et al. DcR3 as a diagnostic parameter and risk factor for systemic lupus erythematosus. Int Immunol 2008;20:1067-1075.
38. Fayad R, Brand MI, Stone D, Keshavarzian A, Qiao L. Apoptosis resistance in ulcerative colitis: high expression of decoy receptors by lamina propria T cells. Eur J Immunol 2006;36:2215-2222.
39. Sung HH, et al. Transgenic expression of decoy receptor 3 protects islets from spontaneous and chemical-induced autoimmune destruction in nonobese diabetic mice. J Exp Med 2004;199:1143-1151.
40. Watanabe N, et al. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol 2003;4:670-679.
41. Gonzalez LC, et al. A coreceptor interaction between the CD28 and TNF receptor family members B and T lymphocyte attenuator and herpesvirus entry mediator. Proc Natl Acad Sci USA 2005;102:1116-1121.
42. Carfi A, et al. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell 2001;8:169-179.
43. Gavrieli M, Watanabe N, Loftin SK, Murphy TL, Murphy KM. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of B and T lymphocyte attenuator required for association with protein tyrosine phosphatases SHP-1 and SHP-2. Biochem Biophys Res Commun 2003;312:1236-1243.
44. Chemnitz JM, Lanfranco AR, Braunstein I, Riley JL. B and T lymphocyte attenuator-mediated signal transduction provides a potent inhibitory signal to primary human CD4 T cells that can be initiated by multiple phosphotyrosine motifs. J Immunol 2006;176:6603-6614.
45. Gavrieli M, Murphy KM. Association of Grb-2 and PI3K p85 with phosphotyrosile peptides derived from BTLA. Biochem Biophys Res Commun 2006;345:1440-1445.
46. Vendel AC, Calemine-Fenaux J, Izrael-Tomasevic A, Chauhan V, Arnott D, Eaton DL. B and T lymphocyte attenuator regulates B cell receptor signaling by targeting Syk and BLNK. J Immunol 2009;182:1509-1517.
47. Han P, Goularte OD, Rufner K, Wilkinson B, Kaye J. An inhibitory Ig superfamily protein expressed by lymphocytes and APCs is also an early marker of thymocyte positive selection. J Immunol 2004;172:5931-5939.
48. Oya Y, et al. Development of autoimmune hepatitis-like disease and production of autoantibodies to nuclear antigens in mice lacking B and T lymphocyte attenuator. Arthritis Rheum 2008;58:2498-2510.
49. Krieg C, Han P, Stone R, Goularte OD, Kaye J. Functional analysis of B and T lymphocyte attenuator engagement on CD4+ and CD8+ T cells. J Immunol 2005;175:6420-6427.
50. Wang XF, et al. Distinct expression and inhibitory function of B and T lymphocyte attenuator on human T cells. Tissue Antigens 2007;69:145-153.
51. De Trez C, et al. The inhibitory HVEM-BTLA pathway counter regulates lymphotoxin receptor signaling to achieve homeostasis of dendritic cells. J Immunol 2008;180:238-248.
52. Otsuki N, Kamimura Y, Hashiguchi M, Azuma M. Expression and function of the B and T lymphocyte attenuator (BTLA/CD272) on human T cells. Biochem Biophys Res Commun 2006;344:1121-1127.
53. Truong W, et al. BTLA targeting modulates lymphocyte phenotype, function, and numbers and attenuates disease in nonobese diabetic mice. J Leukoc Biol 2009;86:41-51.
54. Liu X, et al. Cutting edge: a critical role of B and T lymphocyte attenuator in peripheral T cell tolerance induction. J Immunol 2009;182:4516-4520.
55. Albring JC, et al. Targeting of B and T lymphocyte associated (BTLA) prevents graft-versus-host disease without global immunosuppression. J Exp Med 2010;207:2551-2559.
56. Derre L, et al. BTLA mediates inhibition of human tumor-specific CD8+ T cells that can be partially reversed by vaccination. J Clin Invest 2010;120:157-167.
57. Han L, et al. Soluble B and T lymphocyte attenuator possesses antitumor effects and facilitates heat shock protein 70 vaccine-triggered antitumor immunity against a murine TC-1 cervical cancer model in vivo. J Immunol 2009;183:7842-7850.
58. Paulos CM, June CH. Putting the brakes on BTLA in T cell-mediated cancer immunotherapy. J Clin Invest 2010;120:76-80.
59. Maiza H, Leca G, Mansur IG, Schiavon V, Boumsell L, Bensussan A. A novel 80-kD cell surface structure identifies human circulating lymphocytes with natural killer activity. J Exp Med 1993;178:1121-1126.
60. Giustiniani J, Bensussan A, Marie-Cardine A. Identification and characterization of a transmembrane isoform of CD160 (CD160-TM), a unique activating receptor selectively expressed upon human NK cell activation. J Immunol 2009;182:63-71.
61. Agrawal S, et al. Cutting edge: MHC class I triggering by a novel cell surface ligand costimulates proliferation of activated human T cells. J Immunol 1999;162:1223-1226.
62. Barakonyi A, et al. Cutting edge: engagement of CD160 by its HLA-C physiological ligand triggers a unique cytokine profile secretion in the cytotoxic peripheral blood NK cell subset. J Immunol 2004;173:5349-5354.
63. Le Bouteiller P, et al. Engagement of CD160 receptor by HLA-C is a triggering mechanism used by circulating natural killer (NK) cells to mediate cytotoxicity. Proc Natl Acad Sci USA 2002;99:16963-16968.
64. Cai G, Anumanthan A, Brown JA, Greenfield EA, Zhu B, Freeman GJ. CD160 inhibits activation of human CD4+ T cells through interaction with herpesvirus entry mediator. Nat Immunol 2008;9:176-185.
65. Giustiniani J, Marie-Cardine A, Bensussan A. A soluble form of the MHC class I-specific CD160 receptor is released from human activated NK lymphocytes and inhibits cell-mediated cytotoxicity. J Immunol 2007;178:1293-1300.
66. Abecassis S, et al. Identification of a novel CD160+ CD4+ T-lymphocyte subset in the skin: a possible role for CD160 in skin inflammation. J Invest Dermatol 2007;127:1161-1166.
67. Maeda M, et al. Murine CD160, Ig-like receptor on NK cells and NKT cells, recognizes classical and nonclassical MHC class I and regulates NK cell activation. J Immunol 2005;175:4426-4432.
68. Farren TW, et al. Differential and tumor-specific expression of CD160 in B-cell malignancies. Blood 2011;118:2174-2183.
69. Liu FT, et al. CD160 signaling mediates PI3K-dependent survival and growth signals in chronic lymphocytic leukemia. Blood 2010;115:3079-3088.
70. Campadelli-Fiume G, et al. The multipartite system that mediates entry of herpes simplex virus into the cell. Rev Med Virol 2007;17:313-336.
71. Heldwein EE, Krummenacher C. Entry of herpesviruses into mammalian cells. Cell Mol Life Sci 2008;65:1653-1668.
72. Akhtar J, Shukla D. Viral entry mechanisms: cellular and viral mediators of herpes simplex virus entry. FEBS J 2009;276:7228-7236.
73. Krummenacher C, Baribaud I, Eisenberg RJ, Cohen GH. Cellular localization of nectin-1 and glycoprotein D during herpes simplex virus infection. J Virol 2003;77:8985-8999.
74. Sciortino MT, et al. Involvement of HVEM receptor in activation of nuclear factor kappaB by herpes simplex virus 1 glycoprotein D. Cell Microbiol 2008;10:2297-2311.
75. Krummenacher C, et al. Comparative usage of herpesvirus entry mediator A and nectin-1 by laboratory strains and clinical isolates of herpes simplex virus. Virology 2004;322:286-299.
76. Taylor JM, et al. Alternative entry receptors for herpes simplex virus and their roles in disease. Cell Host Microbe 2007;2:19-28.
77. Yoon M, Kopp SJ, Taylor JM, Storti CS, Spear PG, Muller WJ. Functional interaction between herpes simplex virus type 2 gD and HVEM transiently dampens local chemokine production after murine mucosal infection. PLoS ONE 2011;6:e16122.
78. Kopp SJ, et al. Infection of neurons and encephalitis after intracranial inoculation of herpes simplex virus requires the entry receptor nectin-1. Proc Natl Acad Sci USA 2009;106:17916-17920.
79. Xu Y, et al. Selective targeting of the LIGHT-HVEM costimulatory system for the treatment of graft-versus-host disease. Blood 2007;109:4097-4104.
80. Hurchla MA, Sedy JR, Murphy KM. Unexpected role of B and T lymphocyte attenuator in sustaining cell survival during chronic allostimulation. J Immunol 2007;178:6073-6082.
81. Ye Q, et al. Modulation of LIGHT-HVEM costimulation prolongs cardiac allograft survival. J Exp Med 2002;195:795-800.
82. Scheu S, Alferink J, Potzel T, Barchet W, Kalinke U, Pfeffer K. Targeted disruption of LIGHT causes defects in costimulatory T cell activation and reveals cooperation with lymphotoxin beta in mesenteric lymph node genesis. J Exp Med 2002;195:1613-1624.
83. Fan K, et al. Blockade of LIGHT/HVEM and B7/CD28 signaling facilitates long-term islet graft survival with development of allospecific tolerance. Transplantation 2007;84:746-754.
84. Yu P, et al. Priming of naive T cells inside tumors leads to eradication of established tumors. Nat Immunol 2004;5:141-149.
85. Fan Z, et al. NK-cell activation by LIGHT triggers tumor-specific CD8+ T-cell immunity to reject established tumors. Blood 2006;107:1342-1351.
86. Doherty TA, et al. The tumor necrosis factor family member LIGHT is a target for asthmatic airway remodeling. Nat Med 2011;17:596-603.
87. Wei CY, Chou YH, Ho FM, Hsieh SL, Lin WW. Signaling pathways of LIGHT induced macrophage migration and vascular smooth muscle cell proliferation. J Cell Physiol 2006;209:735-743.
88. Soroosh P, et al. Herpesvirus entry mediator (TNFRSF14) regulates the persistence of T helper memory cell populations. J Exp Med 2011;208:797-809.
89. Cohavy O, Zhou J, Granger SW, Ware CF, Targan SR. LIGHT expression by mucosal T cells may regulate IFN-gamma expression in the intestine. J Immunol 2004;173:251-258.
90. Cohavy O, Zhou J, Ware CF, Targan SR. LIGHT is constitutively expressed on T and NK cells in the human gut and can be induced by CD2-mediated signaling. J Immunol 2005;174:646-653.
91. Wang J, et al. The critical role of LIGHT in promoting intestinal inflammation and Crohn's disease. J Immunol 2005;174:8173-8182.
92. Wang J, Fu YX. Tumor necrosis factor family members and inflammatory bowel disease. Immunol Rev 2005;204:144-155.
93. Johansson-Lindbom B, Svensson M, Wurbel MA, Malissen B, Marquez G, Agace W. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med 2003;198:963-969.
94. Berlin C, et al. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 1993;74:185-195.
95. Schaer C, et al. HVEM signalling promotes colitis. PLoS ONE 2011;6:e18495.
96. Steinberg MW, et al. A crucial role for HVEM and BTLA in preventing intestinal inflammation. J Exp Med 2008;205:1463-1476.
97. Dubois PC, et al. Multiple common variants for celiac disease influencing immune gene expression. Nat Genet 2010;42:295-302.
98. Coenen MJ, et al. Common and different genetic background for rheumatoid arthritis and coeliac disease. Hum Mol Genet 2009;18:4195-4203.
99. Hsu H, Solovyev I, Colombero A, Elliott R, Kelley M, Boyle WJ. ATAR, a novel tumor necrosis factor receptor family member, signals through TRAF2 and TRAF5. J Biol Chem 1997;272:13471-13474.
100. Marsters SA, Ayres TM, Skubatch M, Gray CL, Rothe M, Ashkenazi A. Herpesvirus entry mediator, a member of the tumor necrosis factor receptor (TNFR) family, interacts with members of the TNFR-associated factor family and activates the transcription factors NF-kappaB and AP-1. J Biol Chem 1997;272:14029-14032.
101. Sakoda Y, et al. Dichotomous regulation of GVHD through bidirectional functions of the BTLA-HVEM pathway. Blood 2011;117:2506-2514.
102. Deppong C, Degnan JM, Murphy TL, Murphy KM, Green JM. B and T lymphocyte attenuator regulates T cell survival in the lung. J Immunol 2008;181:2973-2979.
103. Deppong C, et al. Cutting edge: B and T lymphocyte attenuator and programmed death receptor-1 inhibitory receptors are required for termination of acute allergic airway inflammation. J Immunol 2006;176:3909-3913.
104. Wu TH, Zhen Y, Zeng C, Yi HF, Zhao Y. B and T lymphocyte attenuator interacts with CD3zeta and inhibits tyrosine phosphorylation of TCRzeta complex during T-cell activation. Immunol Cell Biol 2007;85:590-595.
105. Wang Y, et al. The role of herpesvirus entry mediator as a negative regulator of T cell-mediated responses. J Clin Invest 2005;115:711-717.
106. Krieg C, Boyman O, Fu YX, Kaye J. B and T lymphocyte attenuator regulates CD8(+) T cell-intrinsic homeostasis and memory cell generation. Nat Immunol 2007;8:162-171.
107. Iwata A, et al. Protective roles of B and T lymphocyte attenuator in NKT cell-mediated experimental hepatitis. J Immunol 2010;184:127-133.
108. Miller ML, Sun Y, Fu YX. Cutting edge: B and T lymphocyte attenuator signaling on NKT cells inhibits cytokine release and tissue injury in early immune responses. J Immunol 2009;183:32-36.
109. Tao R, Wang L, Murphy KM, Fraser CC, Hancock WW. Regulatory T cell expression of herpesvirus entry mediator suppresses the function of B and T lymphocyte attenuator-positive effector T cells. J Immunol 2008;180:6649-6655.
110. Steinberg MW, Shui JW, Ware CF, Kronenberg M. Regulating the mucosal immune system: the contrasting roles of LIGHT, HVEM, and their various partners. Semin Immunopathol 2009;31:207-221.
111. Shao L, Serrano D, Mayer L. The role of epithelial cells in immune regulation in the gut. Semin Immunol 2001;13:163-176.
112. Hurchla MA, Sedy JR, Gavrieli M, Drake CG, Murphy TL, Murphy KM. B and T lymphocyte attenuator exhibits structural and expression polymorphisms and is highly induced in anergic CD4+ T cells. J Immunol 2005;174:3377-3385.
113. Pierer M, et al. Herpesvirus entry mediator-Ig treatment during immunization aggravates rheumatoid arthritis in the collagen-induced arthritis model. J Immunol 2009;182:3139-3145.
114. Spear PG. Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol 2004;6:401-410.
115. Sedy JR, Spear PG, Ware CF. Cross-regulation between herpesviruses and the TNF superfamily members. Nat Rev Immunol 2008;8:861-873.
116. Reske A, Pollara G, Krummenacher C, Chain BM, Katz DR. Understanding HSV-1 entry glycoproteins. Rev Med Virol 2007;17:205-215.
117. Lasaro MO, et al. Targeting of antigen to the herpesvirus entry mediator augments primary adaptive immune responses. Nat Med 2008;14:205-212.
118. DiMenna L, et al. Augmentation of primary influenza A virus-specific CD8+ T cell responses in aged mice through blockade of an immunoinhibitory pathway. J Immunol 2010;184:5475-5484.
119. Kinkade A, Ware CF. The DARC conspiracy - virus invasion tactics. Trends Immunol 2006;27:362-367.
120. Sun Y, et al. B and T lymphocyte attenuator tempers early infection immunity. J Immunol 2009;183:1946-1951.
121. Heo SK, et al. LIGHT enhances the bactericidal activity of human monocytes and neutrophils via HVEM. J Leukoc Biol 2006;79:330-338.
122. Heo SK, et al. HVEM signaling in monocytes is mediated by intracellular calcium mobilization. J Immunol 2007;179:6305-6310.
123. Lepenies B, et al. Ligation of B and T lymphocyte attenuator prevents the genesis of experimental cerebral malaria. J Immunol 2007;179:4093-4100.
124. Shi G, Luo H, Wan X, Salcedo TW, Zhang J, Wu J. Mouse T cells receive costimulatory signals from LIGHT, a TNF family member. Blood 2002;100:3279-3286.
125. Shui JW, Steinberg MW, Kronenberg M. Regulation of inflammation, autoimmunity, and infection immunity by HVEM-BTLA signaling. J Leukoc Biol 2011;89:517-523.