Random migration precedes stable target cell interactions of tumor-infiltrating T cells

Journal of Experimental Medicine

Volumn 203, Issue 12, 2006, Pages 2749-2761

  Mrass, Paulus ^a   Takano, Hajime ^b   Lai, Guan Ng ^a   Daxini, Sachin ^a   Lasaro, Marcio O ^a   Iparraguirre, Amaya ^a   Cavanagh, Lois L ^a   Von Andrian, Ulrich H ^c   Ertl, Hildegund C J ^a   Haydon, Philip G ^b   Weninger, Wolfgang ^a,b  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR ANTIGEN;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOTHERAPY; MICROENVIRONMENT; PRIORITY JOURNAL; T LYMPHOCYTE; TARGET CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR REGRESSION;

ANIMALS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL MOVEMENT; CYTOTOXICITY, IMMUNOLOGIC; LYMPHOCYTES, TUMOR-INFILTRATING; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; T-LYMPHOCYTES; THYMOMA;

EID: 33751501463     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20060710     Document Type: Article

References (51)

1. Dunn, G.P., L.J. Old, and R.D. Schreiber. 2004. The three Es of cancer immunoediting. Annu. Rev. Immunol. 22:329-360.
2. Jager, E., D. Jager, and A. Knuth. 2003. Antigen-specific immunotherapy and cancer vaccines. Int. J. Cancer. 106:817-820.
3. Ho, W.Y., J.N. Blattman, M.L. Dossett, C. Yee, and P.D. Greenberg. 2003. Adoptive immunotherapy: engineering T cell responses as biologic weapons for tumor mass destruction. Cancer Cell. 3:431-437.
4. Sadelain, M., I. Riviere, and R. Brentjens. 2003. Targeting tumours with genetically enhanced T lymphocytes. Nat. Rev. Cancer. 3:35-45.
5. Schuler, G., B. Schuler-Thurner, and R.M. Steinman. 2003. The use of dendritic cells in cancer immunotherapy. Curr. Opin. Immunol. 15:138-147.
6. Gilboa, E. 2004. The promise of cancer vaccines. Nat. Rev. Cancer. 4:401-411.
7. Blattman, J.N., and P.D. Greenberg. 2004. Cancer immunotherapy: a treatment for the masses. Science. 305:200-205.
8. Dudley, M.E., and S.A. Rosenberg. 2003. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat. Rev. Cancer. 3:666-675.
9. Pardoll, D. 2003. Does the immune system see tumors as foreign or self? Annu. Rev. Immunol. 21:807-839.
10. Kircher, M.F., J.R. Allport, E.E. Graves, V. Love, L. Josephson, A.H. Lichtman, and R. Weissleder. 2003. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res. 63:6838-6846.
11. Mandl, S., C. Schimmelpfennig, M. Edinger, R.S. Negrin, and C.H. Contag. 2002. Understanding immune cell trafficking patterns via in vivo bioluminescence imaging. J. Cell. Biochem. Suppl. 39:239-248.
12. Luster, A.D., R. Alon, and U.H. von Andrian. 2005. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6:1182-1190.
13. Sallusto, F., and C.R. Mackay. 2004. Chemoattractants and their receptors in homeostasis and inflammation. Curr. Opin. Immunol. 16:724-731.
14. Zhang, T., R. Somasundaram, K. Berencsi, L. Caputo, P. Rani, D. Guerry, E. Furth, B.J. Rollins, M. Putt, P. Gimotty, et al. 2005. CXC chemokine ligand 12 (stromal cell-derived factor 1 alpha) and CXCR4-dependent migration of CTLs toward melanoma cells in organotypic culture. J. Immunol. 174:5856-5863.
15. Musha, H., H. Ohtani, T. Mizoi, M. Kinouchi, T. Nakayama, K. Shiiba, K. Miyagawa, H. Nagura, O. Yoshie, and I. Sasaki. 2005. Selective in-filtration of CCR5(+)CXCR3(+) T lymphocytes in human colorectal carcinoma. Int. J. Cancer. 116:949-956.
16. Blankenstein, T. 2005. The role of tumor stroma in the interaction between tumor and immune system. Curr. Opin. Immunol. 17:180-186.
17. Spiotto, M.T., D.A. Rowley, and H. Schreiber. 2004. Bystander elimination of antigen loss variants in established tumors. Nat. Med. 10:294-298.
18. Rothstein, T.L., M. Mage, G. Jones, and L.L. McHugh. 1978. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J. Immunol. 121:1652-1656.
19. Sanderson, C.J. 1976. The mechanism of T cell mediated cytotoxicity. II. Morphological studies of cell death by time-lapse microcinematography. Proc. R. Soc. Lond. B. Biol. Sci. 192:241-255.
20. Matter, A. 1979. Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes. Immunology. 36:179-190.
21. 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.
22. Miller, M.J., S.H. Wei, M.D. Cahalan, and I. Parker. 2003. Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc. Natl. Acad. Sci. USA. 100:2604-2609.
23. Germain, R.N., F. Castellino, M. Chieppa, J.G. Egen, A.Y. Huang, L.Y. Koo, and H. Qi. 2005. An extended vision for dynamic high-resolution intravital immune imaging. Semin. Immunol. 17:431-441.
24. Cahalan, M.D., I. Parker, S.H. Wei, and M.J. Miller. 2002. Two-photon tissue imaging: seeing the immune system in a fresh light. Nat. Rev. Immunol. 2:872-880.
25. Sumen, C., T.R. Mempel, I.B. Mazo, and U.H. von Andrian. 2004. Intravital microscopy: visualizing immunity in context. Immunity. 21:315-329.
26. Bousso, P., and E.A. Robey. 2004. Dynamic behavior of T cells and thymocytes in lymphoid organs as revealed by two-photon microscopy. Immunity. 21:349-355.
27. Kawakami, N., U.V. Nagerl, F. Odoardi, T. Bonhoeffer, H. Wekerle, and A. Flugel. 2005. Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion. J. Exp. Med. 201:1805-1814.
28. Miller, M.J., S.H. Wei, I. Parker, and M.D. Cahalan. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science. 296:1869-1873.
29. Bousso, P., and E. Robey. 2003. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat. Immunol. 4:579-585.
30. Mempel, T.R., S.E. Henrickson, and U.H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 427:154-159.
31. Shakhar, G., R.L. Lindquist, D. Skokos, D. Dudziak, J.H. Huang, M.C. Nussenzweig, and M.L. Dustin. 2005. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat. Immunol. 6:707-714.
32. Hugues, S., L. Fetler, L. Bonifaz, J. Helft, F. Amblard, and S. Amigorena. 2004. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat. Immunol. 5:1235-1242.
33. Tang, Q., J.Y. Adams, A.J. Tooley, M. Bi, B.T. Fife, P. Serra, P. Santamaria, R.M. Locksley, M.F. Krummel, and J.A. Bluestone. 2006. Visualizing regulatory T cell control of autoimmune responses in non-obese diabetic mice. Nat. Immunol. 7:83-92.
34. + T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J. Exp. Med. 201:1815-1823.
35. Sawada, S., J.D. Scarborough, N. Killeen, and D.R. Littman. 1994. A lineage-specific transcriptional silencer regulates CD4 gene expression during T lymphocyte development. Cell. 77:917-929.
36. Wurster, A.L., G. Siu, J.M. Leiden, and S.M. Hedrick. 1994. Elf-1 binds to a critical element in a second CD4 enhancer. Mol. Cell. Biol. 14:6452-6463.
37. Kowalczyk, D.W., A.P. Wlazlo, M. Blaszczyk-Thurin, Z.Q. Xiang, W. Giles-Davis, and H.C. Ertl. 2001. A method that allows easy characterization of tumor-infiltrating lymphocytes. J. Immunol. Methods. 253:163-175.
38. Haas, A.R., J. Sun, A. Vachani, A.F. Wallace, M. Silverberg, V. Kapoor, and S.M. Albelda. 2006. Cycloxygenase-2 inhibition augments the efficacy of a cancer vaccine. Clin. Cancer Res. 12:214-222.
39. Condeelis, J., and J.E. Segall. 2003. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer. 3:921-930.
40. Underhill, D.M., M. Bassetti, A. Rudensky, and A. Aderem. 1999. Dynamic interactions of macrophages with T cells during antigen presentation. J. Exp. Med. 190:1909-1914.
41. Witt, C.M., S. Raychaudhuri, B. Schaefer, A.K. Chakraborty, and E.A. Robey. 2005. Directed migration of positively selected thymocytes visualized in real time. PLoS Biol. 3:e160.
42. Friedl, P., S. Borgmann, and E.B. Brocker. 2001. Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J. Leukoc. Biol. 70:491-509.
43. Bromley, S.K., W.R. Burack, K.G. Johnson, K. Somersalo, T.N. Sims, C. Sumen, M.M. Davis, A.S. Shaw, P.M. Allen, and M.L. Dustin. 2001. The immunological synapse. Annu. Rev. Immunol. 19:375-396.
44. McGavern, D.B., U. Christen, and M.B. Oldstone. 2002. Molecular anatomy of antigen-specific CD8(+) T cell engagement and synapse formation in vivo. Nat. Immunol. 3:918-925.
45. Gunzer, M., A. Schafer, S. Borgmann, S. Grabbe, K.S. Zanker, E.B. Brocker, E. Kampgen, and P. Friedl. 2000. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity. 13:323-332.
46. Bingle, L., N.J. Brown, and C.E. Lewis. 2002. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196:254-265.
47. Huse, M., B.F. Lillemeier, M.S. Kuhns, D.S. Chen, and M.M. Davis. 2006. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7:247-255.
48. Mora, J.R., M.R. Bono, N. Manjunath, W. Weninger, L.L. Cavanagh, M. Rosemblatt, and U.H. Von Andrian. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature. 424:88-93.
49. Pearce, E.L., A.C. Mullen, G.A. Martins, C.M. Krawczyk, A.S. Hutchins, V.P. Zediak, M. Banica, C.B. DiCioccio, D.A. Gross, C.A. Mao, et al. 2003. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science. 302:1041-1043.
50. Mrass, P., M. Rendl, M. Mildner, F. Gruber, B. Lengauer, C. Ballaun, L. Eckhart, and E. Tschachler. 2004. Retinoic acid increases the expression of p53 and proapoptotic caspases and sensitizes keratinocytes to apoptosis: a possible explanation for tumor preventive action of retinoids. Cancer Res. 64:6542-6548.
51. von Andrian, U.H. 1996. Intravital microscopy of the peripheral lymph node microcirculation in mice. Microcirculation. 3:287-300.