Subtle CXCR3-dependent chemotaxis of CTLs within infected tissue allows efficient target localization

Journal of Immunology

Volumn 195, Issue 11, 2015, Pages 5285-5295

  Ariotti, Silvia ^a   Beltman, Joost B ^a,b,c   Borsje, Rianne ^a   Hoekstra, Mirjam E ^a   Halford, William P ^d   Haanen, John B A G ^a   De Boer, Rob J ^b   Schumacher, Ton N M ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c LEIDEN UNIVERSITY   (Netherlands)

^d SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; LIGAND; CXCR3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL FUNCTION; CELL MOTILITY; CELLULAR DISTRIBUTION; CHEMOTAXIS; COMPUTER SIMULATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EPIDERMIS; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; IN VIVO STUDY; INFECTION CONTROL; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TARGET CELL; VIRAL SKIN DISEASE; VIRUS CELL INTERACTION; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; NEUTROPHIL CHEMOTAXIS; TRANSGENIC MOUSE; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; CHEMOTAXIS, LEUKOCYTE; COMPUTER SIMULATION; EPIDERMIS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, CXCR3; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84948809050     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500853     Document Type: Article

References (33)

1. Alvarez, D., E. H. Vollmann, and U. H. von Andrian. 2008. Mechanisms and consequences of dendritic cell migration. Immunity 29: 325-342.
2. Heath, W. R., and F. R. Carbone. 2009. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 10: 1237-1244.
3. Rose, D. M., R. Alon, and M. H. Ginsberg. 2007. Integrin modulation and signaling in leukocyte adhesion and migration. Immunol. Rev. 218: 126-134.
4. Filipe-Santos, O., P. Pescher, B. Breart, C. Lippuner, T. Aebischer, N. Glaichenhaus, G. F. Späth, and P. Bousso. 2009. A dynamic map of antigen recognition by CD4 T cells at the site of Leishmania major infection. Cell Host Microbe 6: 23-33.
5. Schaeffer, M., S. J. Han, T. Chtanova, G. G. van Dooren, P. Herzmark, Y. Chen, B. Roysam, B. Striepen, and E. A. Robey. 2009. Dynamic imaging of T cellparasite interactions in the brains of mice chronically infected with Toxoplasma gondii. J. Immunol. 182: 6379-6393.
6. Wilson, E. H., T. H. Harris, P. Mrass, B. John, E. D. Tait, G. F. Wu, M. Pepper, E. J. Wherry, F. Dzierzinski, D. Roos, et al. 2009. Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 30: 300-311.
7. Hickman, H. D., G. V. Reynoso, B. F. Ngudiankama, S. S. Cush, J. Gibbs, J. R. Bennink, and J. W. Yewdell. 2015. CXCR3 chemokine receptor enables local CD8(+) T cell migration for the destruction of virus-infected cells. Immunity 42: 524-537.
8. Worbs, T., T. R. Mempel, J. Bölter, U. H. von Andrian, and R. Förster. 2007. CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J. Exp. Med. 204: 489-495.
9. Germain, R. N., E. A. Robey, and M. D. Cahalan. 2012. A decade of imaging cellular motility and interaction dynamics in the immune system. Science 336: 1676-1681.
10. Beltman, J. B., C. D. C. Allen, J. G. Cyster, and R. J. de Boer. 2011. B cells within germinal centers migrate preferentially from dark to light zone. Proc. Natl. Acad. Sci. USA 108: 8755-8760.
11. Castellino, F., A. Y. Huang, G. Altan-Bonnet, S. Stoll, C. Scheinecker, and R. N. Germain. 2006. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 440: 890-895.
12. Hugues, S., A. Scholer, A. Boissonnas, A. Nussbaum, C. Combadière, S. Amigorena, and L. Fetler. 2007. Dynamic imaging of chemokine-dependent CD8+ T cell help for CD8+ T cell responses. Nat. Immunol. 8: 921-930.
13. Okada, T., M. J. Miller, I. Parker, M. F. Krummel, M. Neighbors, S. B. Hartley, A. O'Garra, M. D. Cahalan, and J. G. Cyster. 2005. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 3: e150.
14. Semmling, V., V. Lukacs-Kornek, C. A. Thaiss, T. Quast, K. Hochheiser, U. Panzer, J. Rossjohn, P. Perlmutter, J. Cao, D. I. Godfrey, et al. 2010. Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat. Immunol. 11: 313-320.
15. Cockburn, I. A., R. Amino, R. K. Kelemen, S. C. Kuo, S. W. Tse, A. Radtke, L. Mac-Daniel, V. V. Ganusov, F. Zavala, and R. Ménard. 2013. In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. USA 110: 9090-9095.
16. Coppieters, K., N. Amirian, and M. von Herrath. 2012. Intravital imaging of CTLs killing islet cells in diabetic mice. J. Clin. Invest. 122: 119-131.
17. Harris, T. H., E. J. Banigan, D. A. Christian, C. Konradt, E. D. Tait Wojno, K. Norose, E. H. Wilson, B. John, W. Weninger, A. D. Luster, et al. 2012. Generalized Lévy walks and the role of chemokines in migration of effector CD8 + T cells. Nature 486: 545-548.
18. Mueller, S. N., W. Heath, J. D. McLain, F. R. Carbone, and C. M. Jones. 2002. Characterization of two TCR transgenic mouse lines specific for herpes simplex virus. Immunol. Cell Biol. 80: 156-163.
19. Toebes, M., M. Coccoris, A. Bins, B. Rodenko, R. Gomez, N. J. Nieuwkoop, W. van de Kasteele, G. F. Rimmelzwaan, J. B. Haanen, H. Ovaa, and T. N. Schumacher. 2006. Design and use of conditional MHC class I ligands. Nat. Med. 12: 246-251.
20. Halford, W. P., J. W. Balliet, and B. M. Gebhardt. 2004. Re-evaluating natural resistance to herpes simplex virus type 1. J. Virol. 78: 10086-10095.
21. Bins, A. D., A. Jorritsma, M. C. Wolkers, C. F. Hung, T. C. Wu, T. N. Schumacher, and J. B. Haanen. 2005. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat. Med. 11: 899-904.
22. Weeks, B. S., R. S. Ramchandran, J. J. Hopkins, and H. M. Friedman. 2000. Herpes simplex virus type-1 and-2 pathogenesis is restricted by the epidermal basement membrane. Arch. Virol. 145: 385-396.
23. Beltman, J. B., A. F. M. Marée, and R. J. de Boer. 2009. Analysing immune cell migration. Nat. Rev. Immunol. 9: 789-798.
24. Boissonnas, A., L. Fetler, I. S. Zeelenberg, S. Hugues, and S. Amigorena. 2007. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 204: 345-356.
25. Beauchemin, C., N. M. Dixit, and A. S. Perelson. 2007. Characterizing T cell movement within lymph nodes in the absence of antigen. J. Immunol. 178: 5505-5512.
26. Figge, M. T., A. Garin, M. Gunzer, M. Kosco-Vilbois, K. M. Toellner, and M. Meyer-Hermann. 2008. Deriving a germinal center lymphocyte migration model from two-photon data. J. Exp. Med. 205: 3019-3029.
27. Bialek, W., and S. Setayeshgar. 2005. Physical limits to biochemical signaling. Proc. Natl. Acad. Sci. USA 102: 10040-10045.
28. McDonald, B., K. Pittman, G. B. Menezes, S. A. Hirota, I. Slaba, C. C. Waterhouse, P. L. Beck, D. A. Muruve, and P. Kubes. 2010. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330: 362-366.
29. Peters, N. C., J. G. Egen, N. Secundino, A. Debrabant, N. Kimblin, S. Kamhawi, P. Lawyer, M. P. Fay, R. N. Germain, and D. Sacks. 2008. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970-974.
30. Lämmermann, T., P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmuller, C. A. Parent, and R. N. Germain. 2013. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498: 371-375.
31. Koya, R. C., S. Mok, B. Comin-Anduix, T. Chodon, C. G. Radu, M. I. Nishimura, O. N. Witte, and A. Ribas. 2010. Kinetic phases of distribution and tumor targeting by T cell receptor engineered lymphocytes inducing robust antitumor responses. Proc. Natl. Acad. Sci. USA 107: 14286-14291.
32. Mrass, P., H. Takano, L. G. Ng, S. Daxini, M. O. Lasaro, A. Iparraguirre, L. L. Cavanagh, U. H. von Andrian, H. C. Ertl, P. G. Haydon, and W. Weninger. 2006. Random migration precedes stable target cell interactions of tumorinfiltrating T cells. J. Exp. Med. 203: 2749-2761.
33. Vroomans, R. M. A., A. F. M. Marée, R. J. de Boer, and J. B. Beltman. 2012. Chemotactic migration of T cells towards dendritic cells promotes the detection of rare antigens. PLOS Comput. Biol. 8: e1002763.