DNGR-1 is dispensable for CD8+ T-cell priming during respiratory syncytial virus infection

European Journal of Immunology

Volumn 44, Issue 8, 2014, Pages 2340-2348

  Durant, Lydia R ^a   Pereira, Catherine ^a   Boakye, Aime ^a   Makris, Spyridon ^a   Kausar, Fahima ^a   Goritzka, Michelle ^a   Johansson, Cecilia ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Cross presentation; DNGR 1; Lung infection; Virus

Indexed keywords

DNGR 1 PROTEIN; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; EPITHELIUM CELL; FEMALE; INOCULATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS INDUCTION; WILD TYPE;

CD8+ T CELL; CROSS-PRESENTATION; DNGR-1; LUNG INFECTION; VIRUS;

ACTINS; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; DENDRITIC CELLS; EPITHELIAL CELLS; LECTINS, C-TYPE; LUNG; MICE; MICE, INBRED BALB C; RECEPTORS, IMMUNOLOGIC; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; VIRAL LOAD;

EID: 84906092604     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444454     Document Type: Article

References (37)

1. Borchers, A. T., Chang, C., Gershwin, M. E. and Gershwin, L. J., Respiratory syncytial virus-a comprehensive review. Clinic. Rev. Allerg. Immunol. 2013. 45: 331-379.
2. Blanken, M. O., Rovers, M. M., Molenaar, J. M., Winkler-Seinstra, P. L., Meijer, A., Kimpen, J. L. L. and Bont, L., Respiratory Syncytial Virus and Recurrent Wheeze in Healthy Preterm Infants. N. Engl. J. Med. 2013. 368: 1791-1799.
3. Openshaw, P. J. and Chiu, C., Protective and dysregulated T cell immunity in RSV infection. Curr. Opin. Virol. 2013. 3: 468-474.
4. Tregoning, J. S., Yamaguchi, Y., Harker, J., Wang, B. and Openshaw, P. J. M., The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J. Virol. 2008. 82: 4115-4124.
5. Rutigliano, J. A., Rock, M. T., Johnson, A. K., Crowe, J. E. and Graham, B. S., Identification of an H-2D(b)-restricted CD8 +cytotoxic T lymphocyte epitope in the matrix protein of respiratory syncytial virus. Virology 2005. 337: 335-343.
6. Blum, J. S., Wearsch, P. A. and Cresswell, P., Pathways of antigen processing. Annu. Rev. Immunol. 2013. 31: 443-473.
7. Lukens, M. V., Kruijsen, D., Coenjaerts, F. E. J., Kimpen, J. L. L. and van Bleek, G. M., Respiratory syncytial virus-induced activation and migration of respiratory dendritic cells and subsequent antigen presentation in the lung-draining lymph node. J. Virol. 2009. 83: 7235-7243.
8. Ruckwardt, T. J., Malloy, A. M. W., Morabito, K. M. and Graham, B. S., Quantitative and qualitative deficits in neonatal lung-migratory dendritic cells impact the generation of the CD8+ T cell response. PLoS Pathog. 2014. 10: e1003934.
9. Demoor, T., Petersen, B. C., Morris, S., Mukherjee, S., Ptaschinski, C., De Almeida Nagata, D. E., Kawai, T. et al., IPS-1 Signaling has a nonredundant role in mediating antiviral responses and the clearance of respiratory syncytial virus. J. Immunol. 2012. 189: 5942-5945.
10. Neyt, K. and Lambrecht, B. N., The role of lung dendritic cell subsets in immunity to respiratory viruses. Immunol. Rev. 2013. 255: 57-67.
11. Braciale, T. J., Sun, J. and Kim, T. S., Regulating the adaptive immune response to respiratory virus infection. Nat. Rev. Immunol. 2012. 2: 295-305.
12. Shortman, K. and Heath, W. R., The CD8+ dendritic cell subset. Immunol. Rev. 2010. 234: 18-31.
13. Joffre, O. P., Segura, E., Savina, A. and Amigorena, S., Cross-presentation by dendritic cells. Nat. Rev. Immunol. 2012. 12: 557-569.
14. Desch, A. N., Randolph, G. J., Murphy, K., Gautier, E. L., Kedl, R. M., Lahoud, M. H., Caminschi, I. et al., CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J. Exp. Med. 2011. 208: 1789-1797.
15. Sancho, D., Mourão-Sá, D., Joffre, O. P., Schulz, O., Rogers, N. C., Pennington, D. J., Carlyle, J. R. et al., Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Invest. 2008. 118: 2098-2110.
16. Huysamen, C., Willment, J. A., Dennehy, K. M. and Brown, G. D., CLEC9A is a novel activation C-type lectin-like receptor expressed on BDCA3+ dendritic cells and a subset of monocytes. J. Biol. Chem. 2008. 283: 16693-16701.
17. Caminschi, I., Proietto, A. I., Ahmet, F., Kitsoulis, S., Shin Teh, J., Lo, J. C. Y., Rizzitelli, A. et al., The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood 2008. 112: 3264-3273.
18. Poulin, L. F., Salio, M., Griessinger, E., Anjos-Afonso, F., Craciun, L., Chen, J.-L., Keller, A. M. et al., Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J. Exp. Med. 2010. 207: 1261-1271.
19. Poulin, L. F., Reyal, Y., Uronen-Hansson, H., Schraml, B., Sancho, D., Murphy, K. M., Håkansson, U. K. et al., DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and non-lymphoid tissues. Blood 2012. 119: 6052-6062.
20. Ahrens, S., Zelenay, S., Sancho, D., Hanč, P., Kjær, S., Feest, C., Fletcher, G. et al., F-Actin is an evolutionarily conserved damage-associated molecular pattern recognized by dngr-1, a receptor for dead cells. Immunity 2012. 36: 635-645.
21. Zhang, J.-G., Czabotar, P. E., Policheni, A. N., Caminschi, I., Wan, S. S., Kitsoulis, S., Tullett, K. M. et al., The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 2012. 36: 646-657.
22. Sancho, D., Joffre, O. P., Keller, A. M., Rogers, N. C., Martínez, D., Hernanz-Falcón, P., Rosewell, I. et al., Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009. 458: 899-903.
23. Zelenay, S., Keller, A. M., Whitney, P. G., Schraml, B. U., Deddouche, S., Rogers, N. C., Schulz, O. et al., The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J. Clin. Invest. 2012. 122: 1615-1627.
24. Iborra, S., Izquierdo, H. M., Martínez-López, M., Blanco-Menéndez, N., Reis e Sousa, C. and Sancho, D., The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J. Clin. Invest. 2012. 122: 1628-1643.
25. Johnson, J. E., Gonzales, R. A., Olson, S. J., Wright, P. F. and Graham, B. S., The histopathology of fatal untreated human respiratory syncytial virus infection. Mod. Pathol. 2007. 20: 108-119.
26. Openshaw, P. J. M. and Tregoning, J. S., Immune responses and disease enhancement during respiratory syncytial virus infection. Clin. Microbiol. Rev. 2005. 18: 541-555.
27. Loebbermann, J., Thornton, H., Durant, L., Sparwasser, T., Webster, K. E., Sprent, J., Culley, F. J. et al., Regulatory T cells expressing granzyme B play a critical role in controlling lung inflammation during acute viral infection. Mucosal. immunology 2012. 5: 161-172.
28. Loebbermann, J., Schnoeller, C., Thornton, H., Durant, L., Sweeney, N. P., Schuijs, M., O'Garra, A. et al., IL-10 regulates viral lung immunopathology during acute respiratory syncytial virus infection in mice. PLoS ONE. 2012. 7: e32371.
29. Chang, J. and Braciale, T. J., Respiratory syncytial virus infection suppresses lung CD8+ T-cell effector activity and peripheral CD8+ T-cell memory in the respiratory tract. Nat. Med. 2002. 8: 54-60.
30. Kulkarni, A. B., Collins, P. L., Bacik, I., Yewdell, J. W., Bennink, J. R., Crowe, J. E. and Murphy, B. R., Cytotoxic T cells specific for a single peptide on the M2 protein of respiratory syncytial virus are the sole mediators of resistance induced by immunization with M2 encoded by a recombinant vaccinia virus. J. Virol. 1995. 69: 1261-1264.
31. Chang, J., Srikiatkhachorn, A. and Braciale, T. J., Visualization and characterization of respiratory syncytial virus F-specific CD8(+) T cells during experimental virus infection. J Immunol. 2001. 167: 4254-4260.
32. Jiang, S., Borthwick, N. J., Morrison, P., Gao, G. F. and Steward, M. W., Virus-specific CTL responses induced by an H-2K(d)-restricted, motif-negative 15-mer peptide from the fusion protein of respiratory syncytial virus. J. Gen. Virol. 2002. 83: 429-438.
33. Zelenay, S. and Sousa, C. R. E. Adaptive immunity after cell death. Trends Immunol. 2013. 34: 329-335.
34. Helft, J., Manicassamy, B., Guermonprez, P., Hashimoto, D., Silvin, A., Agudo, J., Brown, B. D. et al., Cross-presenting CD103+ dendritic cells are protected from influenza virus infection. J. Clin. Invest. 2012. 122: 4037-4047.
35. Desch, A. N., Henson, P. M. and Jakubzick, C. V., Pulmonary dendritic cell development and antigen acquisition. Immunol. Res. 2013. 55: 178-186.
36. Culley, F. J., Pollott, J. and Openshaw, P. J. M. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 2002. 196: 1381-1386.
37. Asselin-Paturel, C., Boonstra, A., Dalod, M., Durand, I., Yessaad, N., Dezutter-Dambuyant, C., Vicari, A. et al., Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2001. 2: 1144-1150.