Inflammatory monocytes and NK cells play a crucial role in DNAM-1-dependent control of cytomegalovirus infection

Journal of Experimental Medicine

Volumn 213, Issue 9, 2016, Pages 1835-1850

  Rovis, Tihana Lenac ^a   Brlic, Paola Kucan ^a   Kaynan, Noa ^b   Lisnic, Vanda Juranic ^a   Brizic, Ilija ^a   Jordan, Stefan ^c   Tomic, Adriana ^a,e   Kvestak, Daria ^a   Babic, Marina ^a   Tsukerman, Pinchas ^b   Colonna, Marco ^d   Koszinowski, Ulrich ^c   Messerle, Martin ^e   Mandelboim, Ofer ^b   Krmpotic, Astrid ^a   Jonjic, Stipan ^a  

^a UNIVERSITY OF RIJEKA   (Croatia)

^b HEBREW UNIVERSITY   (Israel)

^c UNIVERSITY OF MUNICH   (Germany)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD96 RECEPTOR; DNAX ACCESSORY MOLECULE 1 PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INHIBITORY RECEPTOR TIGIT; M20.1 PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; POLIOVIRUS RECEPTOR; RECEPTOR; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS RECEPTOR; CD226 ANTIGEN; INTERLEUKIN 12; NOS2 PROTEIN, MOUSE; T LYMPHOCYTE ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DOWN REGULATION; ENDOPLASMIC RETICULUM; INFECTION CONTROL; INFLAMMATORY CELL; LYMPHOCYTE DEPLETION; MONOCYTE; MONONUCLEAR PHAGOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; VIRUS TITRATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CYTOMEGALOVIRUS INFECTIONS; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CYTOMEGALOVIRUS INFECTIONS; INTERLEUKIN-12; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MONOCYTES; NITRIC OXIDE SYNTHASE TYPE II; RECEPTORS, VIRUS;

EID: 84984849260     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20151899     Document Type: Article

References (70)

1. Alexandre, Y.O., C.D. Cocita, S. Ghilas, and M. Dalod. 2014. Deciphering the role of DC subsets in MCMV infection to better understand immune protection against viral infections. Front. Microbiol. 5:378. http://dx.doi.org/10.3389/fmicb.2014.00378
2. Aranda, P.S., D.M. LaJoie, and C.L. Jorcyk. 2012. Bleach gel: a simple agarose gel for analyzing RNA quality. Electrophoresis. 33:366-369. http://dx.doi.org/10.1002/elps.201100335
3. Bottino, C., R. Castriconi, D. Pende, P. Rivera, M. Nanni, B. Carnemolla, C. Cantoni, J. Grassi, S. Marcenaro, N. Reymond, et al. 2003. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 198:557-567. http://dx.doi.org/10.1084/jem.20030788
4. Bradford, R.D., Y.G. Yoo, M. Golemac, E.P. Pugel, S. Jonjic, and W.J. Britt. 2015. Murine CMV-induced hearing loss is associated with inner ear inflammation and loss of spiral ganglia neurons. PLoS Pathog. 11:e1004774. http://dx.doi.org/10.1371/journal.ppat.1004774
5. Britt, W.J., D. Cekinovic, and S. Jonjic. 2013. Murine Model of Neonatal Cytomegalovirus Infection. In Cytomegaloviruses From Molecular Pathogenesis to Intervention. M.J. Reddehase, editor. Caister Academic Press, Norfolk, UK. pp. 119-141.
6. Brune, W., H. Hengel, and U.H. Koszinowski. 2001. A mouse model for cytomegalovirus infection. Curr. Protoc. Immunol. 19:Unit 19.7. http://dx.doi.org/10.1002/0471142735.im1907s43
7. Brune, W., M. Wagner, and M. Messerle. 2006. Manipulating cytomegalovirus genomes by BAC mutagenesis: strategies and applications. Cytomegaloviruses From Molecular Pathogenesis to Intervention. M.J. Reddehase, editor. Caister Academic Press, Norfolk, UK. pp. 63-89.
8. Bubić, I., M. Wagner, A. Krmpotić, T. Saulig, S. Kim, W.M. Yokoyama, S. Jonjić, and U.H. Koszinowski. 2004. Gain of virulence caused by loss of a gene in murine cytomegalovirus. J. Virol. 78:7536-7544. http://dx.doi.org/10.1128/JVI.78.14.7536-7544.2004
9. Chadéneau, C., B. LeMoullac, and M.G. Denis. 1994. A novel member of the immunoglobulin gene superfamily expressed in rat carcinoma cell lines. J. Biol. Chem. 269:15601-15605.
10. Chan, C.J., L. Martinet, S. Gilfillan, F. Souza-Fonseca-Guimaraes, M.T. Chow, L. Town, D.S. Ritchie, M. Colonna, D.M. Andrews, and M.J. Smyth. 2014. The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat. Immunol. 15:431-438. http://dx.doi.org/10.1038/ni.2850
11. Chow, A., B.D. Brown, and M. Merad. 2011. Studying the mononuclear phagocyte system in the molecular age. Nat. Rev. Immunol. 11:788-798. http://dx.doi.org/10.1038/nri3087
12. Crane, M.J., K.L. Hokeness-Antonelli, and T.P. Salazar-Mather. 2009. Regulation of inflammatory monocyte/macrophage recruitment from the bone marrow during murine cytomegalovirus infection: role for type I interferons in localized induction of CCR2 ligands. J. Immunol. 183:2810-2817. http://dx.doi.org/10.4049/jimmunol.0900205
13. Crnković-Mertens, I., M. Messerle, I. Milotić, U. Szepan, N. Kucić, A. Krmpotić, S. Jonjić, and U.H. Koszinowski. 1998. Virus attenuation after deletion of the cytomegalovirus Fc receptor gene is not due to antibody control. J. Virol. 72:1377-1382.
14. Daley-Bauer, L.P., G.M. Wynn, and E.S. Mocarski. 2012. Cytomegalovirus impairs antiviral CD8+ T cell immunity by recruiting inflammatory monocytes. Immunity. 37:122-133. http://dx.doi.org/10.1016/j.immuni.2012.04.014
15. Daley-Bauer, L.P., L.J. Roback, G.M. Wynn, and E.S. Mocarski. 2014. Cytomegalovirus hijacks CX3CR1(hi) patrolling monocytes as immune-privileged vehicles for dissemination in mice. Cell Host Microbe. 15:351-362. http://dx.doi.org/10.1016/j.chom.2014.02.002
16. Dalod, M., and C.A. Biron. 2013. Immunoregulatory Cytokine Networks Discovered and Characterized during Murine Cytomegalovirus Infections. In Cytomegaloviruses From Molecular Pathogenesis to Intervention. M.J. Reddehase, editor. Caister Academic Press, Norfolk, UK., 11, 232-258.
17. Dalod, M., T. Hamilton, R. Salomon, T.P. Salazar-Mather, S.C. Henry, J.D. Hamilton, and C.A. Biron. 2003. Dendritic cell responses to early murine cytomegalovirus infection: subset functional specialization and differential regulation by interferon alpha/beta. J. Exp. Med. 197:885-898. http://dx.doi.org/10.1084/jem.20021522
18. de Andrade, L.F., M.J. Smyth, and L. Martinet. 2014. DNAM-1 control of natural killer cells functions through nectin and nectin-like proteins. Immunol. Cell Biol. 92:237-244. http://dx.doi.org/10.1038/icb.2013.95
19. Drutman, S.B., J.C. Kendall, and E.S. Trombetta. 2012. Inflammatory spleen monocytes can upregulate CD11c expression without converting into dendritic cells. J. Immunol. 188:3603-3610. http://dx.doi.org/10.4049/jimmunol.1102741
20. Farrell, H.E., N. Davis-Poynter, K. Bruce, C. Lawler, L. Dolken, M. Mach, and P.G. Stevenson. 2015. Lymph Node Macrophages Restrict Murine Cytomegalovirus Dissemination. J. Virol. 89:7147-7158. http://dx.doi.org/10.1128/JVI.00480-15
21. Fuchs, A., M. Cella, E. Giurisato, A.S. Shaw, and M. Colonna. 2004. Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J. Immunol. 172:3994-3998. http://dx.doi.org/10.4049/jimmunol.172.7.3994
22. Gautier, E.L., T. Shay, J. Miller, M. Greter, C. Jakubzick, S. Ivanov, J. Helft, A. Chow, K.G. Elpek, S. Gordonov, et al. Immunological Genome Consortium. 2012. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13:1118-1128. http://dx.doi.org/10.1038/ni.2419
23. Gaya, M., A. Castello, B. Montaner, N. Rogers, C. Reis e Sousa, A. Bruckbauer, and F.D. Batista. 2015. Host response. Inflammation-induced disruption of SCS macrophages impairs B cell responses to secondary infection. Science. 347:667-672. http://dx.doi.org/10.1126/science.aaa1300
24. Gilfillan, S., C.J. Chan, M. Cella, N.M. Haynes, A.S. Rapaport, K.S. Boles, D.M. Andrews, M.J. Smyth, and M. Colonna. 2008. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigenpresenting cells and tumors. J. Exp. Med. 205:2965-2973. http://dx.doi.org/10.1084/jem.20081752
25. Gromeier, M., S. Lachmann, M.R. Rosenfeld, P.H. Gutin, and E. Wimmer. 2000. Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc. Natl. Acad. Sci. USA. 97:6803-6808. http://dx.doi.org/10.1073/pnas.97.12.6803
26. Guilliams, M., F. Ginhoux, C. Jakubzick, S.H. Naik, N. Onai, B.U. Schraml, E. Segura, R. Tussiwand, and S. Yona. 2014. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14:571-578. http://dx.doi.org/10.1038/nri3712
27. Hargett, D., and T.E. Shenk. 2010. Experimental human cytomegalovirus latency in CD14+ monocytes. Proc. Natl. Acad. Sci. USA. 107:20039-20044. http://dx.doi.org/10.1073/pnas.1014509107
28. Heise, M.T., and H.W. Virgin IV. 1995. The T-cell-independent role of gamma interferon and tumor necrosis factor alpha in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J. Virol. 69:904-909.
29. Hirota, T., K. Irie, R. Okamoto, W. Ikeda, and Y. Takai. 2005. Transcriptional activation of the mouse Necl-5/Tage4/PVR/CD155 gene by fibroblast growth factor or oncogenic Ras through the Raf-MEK-ERK-AP-1 pathway. Oncogene. 24:2229-2235. http://dx.doi.org/10.1038/sj.onc.1208409
30. Hokeness, K.L., W.A. Kuziel, C.A. Biron, and T.P. Salazar-Mather. 2005. Monocyte chemoattractant protein-1 and CCR2 interactions are required for IFN-alpha/beta-induced inflammatory responses and antiviral defense in liver. J. Immunol. 174:1549-1556. http://dx.doi.org/10.4049/jimmunol.174.3.1549
31. Holzki, J.K., F. Dağ, I. Dekhtiarenko, U. Rand, R. Casalegno-Garduño, S. Trittel, T. May, P. Riese, and L. Čičin-Šain. 2015. Type I Interferon Released by Myeloid Dendritic Cells Reversibly Impairs Cytomegalovirus Replication by Inhibiting Immediate Early Gene Expression. J. Virol. 89:9886-9895. http://dx.doi.org/10.1128/JVI.01459-15
32. Iijima, N., L.M. Mattei, and A. Iwasaki. 2011. Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc. Natl. Acad. Sci. USA. 108:284-289. http://dx.doi.org/10.1073/pnas.1005201108
33. Italiani, P., and D. Boraschi. 2014. From Monocytes to M1/M2 Macrophages:Phenotypical vs. Functional Differentiation. Front. Immunol. 5:514. http://dx.doi.org/10.3389/fimmu.2014.00514
34. Joller, N., J.P. Hafler, B. Brynedal, N. Kassam, S. Spoerl, S.D. Levin, A.H. Sharpe, and V.K. Kuchroo. 2011. Cutting edge: TIG IT has T cell-intrinsic inhibitory functions. J. Immunol. 186:1338-1342. http://dx.doi.org/10.4049/jimmunol.1003081
35. Juranic Lisnic, V., M. Babic Cac, B. Lisnic, T. Trsan, A. Mefferd, C. Das Mukhopadhyay, C.H. Cook, S. Jonjic, and J. Trgovcich. 2013. Dual analysis of the murine cytomegalovirus and host cell transcriptomes reveal new aspects of the virus-host cell interface. PLoS Pathog. 9:e1003611. http://dx.doi.org/10.1371/journal.ppat.1003611
36. Kamran, N., Y. Takai, J. Miyoshi, S.K. Biswas, J.S. Wong, and S. Gasser. 2013. Toll-like receptor ligands induce expression of the costimulatory molecule CD155 on antigen-presenting cells. PLoS One. 8:e54406. http://dx.doi.org/10.1371/journal.pone.0054406
37. Kosmac, K., G.R. Bantug, E.P. Pugel, D. Cekinovic, S. Jonjic, and W.J. Britt. 2013. Glucocorticoid treatment of MCMV infected newborn mice attenuates CNS inflammation and limits deficits in cerebellar development. PLoS Pathog. 9:e1003200. http://dx.doi.org/10.1371/journal.ppat.1003200
38. Levin, S.D., D.W. Taft, C.S. Brandt, C. Bucher, E.D. Howard, E.M. Chadwick, J. Johnston, A. Hammond, K. Bontadelli, D. Ardourel, et al. 2011. Vstm3 is a member of the CD28 family and an important modulator of T-cell function. Eur. J. Immunol. 41:902-915. http://dx.doi.org/10.1002/eji.201041136
39. Lim, J.K., C.J. Obara, A. Rivollier, A.G. Pletnev, B.L. Kelsall, and P.M. Murphy. 2011. Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in West Nile virus encephalitis. J. Immunol. 186:471-478. http://dx.doi.org/10.4049/jimmunol.1003003
40. Magri, G., A. Muntasell, N. Romo, A. Sáez-Borderías, D. Pende, D.E. Geraghty, H. Hengel, A. Angulo, A. Moretta, and M. López-Botet. 2011. NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood. 117:848-856. http://dx.doi.org/10.1182/blood -2010-08-301374
41. Martinet, L., and M.J. Smyth. 2015. Balancing natural killer cell activation through paired receptors. Nat. Rev. Immunol. 15:243-254. http://dx.doi.org/10.1038/nri3799
42. Martinet, L., L. Ferrari De Andrade, C. Guillerey, J.S. Lee, J. Liu, F. Souza-Fonseca-Guimaraes, D.S. Hutchinson, T.B. Kolesnik, S.E. Nicholson, N.D. Huntington, and M.J. Smyth. 2015. DNAM-1 expression marks an alternative program of NK cell maturation. Cell Reports. 11:85-97. http://dx.doi.org/10.1016/j.celrep.2015.03.006
43. Martinez, F.O., and S. Gordon. 2014. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6:13. http://dx.doi.org/10.12703/P6-13
44. Masson, D., A. Jarry, B. Baury, P. Blanchardie, C. Laboisse, P. Lustenberger, and M.G. Denis. 2001. Overexpression of the CD155 gene in human colorectal carcinoma. Gut. 49:236-240. http://dx.doi.org/10.1136/gut.49.2.236
45. Mitchell, B.M., A. Leung, and J.G. Stevens. 1996. Murine cytomegalovirus DNA in peripheral blood of latently infected mice is detectable only in monocytes and polymorphonuclear leukocytes. Virology. 223:198-207. http://dx.doi.org/10.1006/viro.1996.0468
46. Murray, P.J., J.E. Allen, S.K. Biswas, E.A. Fisher, D.W. Gilroy, S. Goerdt, S. Gordon, J.A. Hamilton, L.B. Ivashkiv, T. Lawrence, et al. 2014. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 41:14-20. http://dx.doi.org/10.1016/j.immuni.2014.06.008
47. Nabekura, T., M. Kanaya, A. Shibuya, G. Fu, N.R. Gascoigne, and L.L. Lanier. 2014. Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection. Immunity. 40:225-234. http://dx.doi.org/10.1016/j.immuni.2013.12.011
48. Noda, S., K. Tanaka, S. Sawamura, M. Sasaki, T. Matsumoto, K. Mikami, Y. Aiba, H. Hasegawa, N. Kawabe, and Y. Koga. 2001. Role of nitric oxide synthase type 2 in acute infection with murine cytomegalovirus. J. Immunol. 166:3533-3541. http://dx.doi.org/10.4049/jimmunol.166.5.3533
49. Prod'homme, V., D.M. Sugrue, R.J. Stanton, A. Nomoto, J. Davies, C.R. Rickards, D. Cochrane, M. Moore, G.W. Wilkinson, and P. Tomasec. 2010. Human cytomegalovirus UL141 promotes efficient downregulation of the natural killer cell activating ligand CD112. J. Gen. Virol. 91:2034-2039. http://dx.doi.org/10.1099/vir.0.021931-0
50. Rawlinson, W.D., H.E. Farrell, and B.G. Barrell. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70:8833-8849.
51. Reddehase, M.J. 2002. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat. Rev. Immunol. 2:831-844. http://dx.doi.org/10.1038/nri932
52. Rölle, A., J. Pollmann, E.M. Ewen, V.T. Le, A. Halenius, H. Hengel, and A. Cerwenka. 2014. IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+ NK cell expansion. J. Clin. Invest. 124:5305-5316. http://dx.doi.org/10.1172/JCI77440
53. Serbina, N.V., T. Jia, T.M. Hohl, and E.G. Pamer. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26:421-452. http://dx.doi.org/10.1146/annurev.immunol.26.021607.090326
54. Shibuya, A., D. Campbell, C. Hannum, H. Yssel, K. Franz-Bacon, T. McClanahan, T. Kitamura, J. Nicholl, G.R. Sutherland, L.L. Lanier, and J.H. Phillips. 1996. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity. 4:573-581. http://dx.doi.org/10.1016/S1074-7613(00)70060-4
55. Shifrin, N., D.H. Raulet, and M. Ardolino. 2014. NK cell self tolerance, responsiveness and missing self recognition. Semin. Immunol. 26:138-144. http://dx.doi.org/10.1016/j.smim.2014.02.007
56. Singh-Jasuja, H., A. Thiolat, M. Ribon, M.C. Boissier, N. Bessis, H.G. Rammensee, and P. Decker. 2013. The mouse dendritic cell marker CD11c is down-regulated upon cell activation through Toll-like receptor triggering. Immunobiology. 218:28-39. http://dx.doi.org/10.1016/j.imbio.2012.01.021
57. Smith, L.M., A.R. McWhorter, L.L. Masters, G.R. Shellam, and A.J. Redwood. 2008. Laboratory strains of murine cytomegalovirus are genetically similar to but phenotypically distinct from wild strains of virus. J. Virol. 82:6689-6696. http://dx.doi.org/10.1128/JVI.00160-08
58. Smith, M.S., G.L. Bentz, J.S. Alexander, and A.D. Yurochko. 2004. Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence. J. Virol. 78:4444-4453. http://dx.doi.org/10.1128/JVI.78.9.4444-4453.2004
59. Soriani, A., A. Zingoni, C. Cerboni, M.L. Iannitto, M.R. Ricciardi, V. Di Gialleonardo, M. Cippitelli, C. Fionda, M.T. Petrucci, A. Guarini, et al. 2009. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood. 113:3503-3511. http://dx.doi.org/10.1182/blood -2008-08-173914
60. Stanietsky, N., H. Simic, J. Arapovic, A. Toporik, O. Levy, A. Novik, Z. Levine, M. Beiman, L. Dassa, H. Achdout, et al. 2009. The interaction of TIG IT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc. Natl. Acad. Sci. USA. 106:17858-17863. http://dx.doi.org/10.1073/pnas.0903474106
61. Stanietsky, N., T.L. Rovis, A. Glasner, E. Seidel, P. Tsukerman, R. Yamin, J. Enk, S. Jonjic, and O. Mandelboim. 2013. Mouse TIG IT inhibits NK-cell cytotoxicity upon interaction with PVR. Eur. J. Immunol. 43:2138-2150. http://dx.doi.org/10.1002/eji.201243072
62. Tomasec, P., E.C. Wang, A.J. Davison, B. Vojtesek, M. Armstrong, C. Griffin, B.P. McSharry, R.J. Morris, S. Llewellyn-Lacey, C. Rickards, et al. 2005. Downregulation of natural killer cell-activating ligand CD155 by human cytomegalovirus UL141. Nat. Immunol. 6:181-188. http://dx.doi.org/10.1038/ni1156
63. Vassena, L., E. Giuliani, G. Matusali, E.A. Cohen, and M. Doria. 2013. The human immunodeficiency virus type 1 Vpr protein upregulates PVR via activation of the ATR-mediated DNA damage response pathway. J. Gen. Virol. 94:2664-2669. http://dx.doi.org/10.1099/vir.0.055541-0
64. Vidal, S., A. Krmpotic, M. Pyzik, and S. Jonjic. 2013. Innate Immunity to Cytomegalovirus in the Murine Model. In Cytomegaloviruses From Molecular Pathogenesis to Intervention. M.J. Reddehase, editor. Caister Academic Press, Norfolk, UK. pp. 192-214.
65. Vo, A.V., E. Takenaka, A. Shibuya, and K. Shibuya. 2016. Expression of DNAM-1 (CD226) on inflammatory monocytes. Mol. Immunol. 69:70-76. http://dx.doi.org/10.1016/j.molimm.2015.11.009
66. Wagner, M., S. Jonjic, U.H. Koszinowski, and M. Messerle. 1999. Systematic excision of vector sequences from the BAC-cloned herpesvirus genome during virus reconstitution. J. Virol. 73:7056-7060.
67. Wikstrom, M.E., A. Khong, P. Fleming, R. Kuns, P.J. Hertzog, I.H. Frazer, C.E. Andoniou, G.R. Hill, and M.A. Degli-Esposti. 2014. The early monocytic response to cytomegalovirus infection is MyD88 dependent but occurs independently of common inflammatory cytokine signals. Eur. J. Immunol. 44:409-419. http://dx.doi.org/10.1002/eji.201243109
68. Yokoyama, W.M., and S. Kim. 2008. Analysis of individual natural killer cell responses. Methods Mol. Biol. 415:179-196.
69. Yu, X., K. Harden, L.C. Gonzalez, M. Francesco, E. Chiang, B. Irving, I. Tom, S. Ivelja, C.J. Refino, H. Clark, et al. 2009. The surface protein TIG IT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat. Immunol. 10:48-57. http://dx.doi.org/10.1038/ni.1674
70. Zucchini, N., G. Bessou, S.H. Robbins, L. Chasson, A. Raper, P.R. Crocker, and M. Dalod. 2008. Individual plasmacytoid dendritic cells are major contributors to the production of multiple innate cytokines in an organspecific manner during viral infection. Int. Immunol. 20:45-56. http://dx.doi.org/10.1093/intimm/dxm119