Visualizing the innate and adaptive immune responses underlying allograft rejection by two-photon microscopy

Nature Medicine

Volumn 17, Issue 6, 2011, Pages 744-749

  Celli, Susanna ^a,b   Albert, Matthew L ^a,b   Bousso, Philippe ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD8 ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL INFILTRATION; CELL MIGRATION; CLINICAL EVALUATION; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; DENDRITIC CELL; DONOR; EAR; GRAFT REJECTION; HOST; HOST CELL; HUMAN; IMAGING; IMMUNOTHERAPY; INNATE IMMUNITY; LYMPH NODE; MONONUCLEAR CELL; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; SKIN CELL; SKIN GRAFT;

ADAPTIVE IMMUNITY; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; GRAFT REJECTION; IMMUNITY, INNATE; LANGERHANS CELLS; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; SKIN; SKIN TRANSPLANTATION;

EID: 79958121166     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2376     Document Type: Article

References (40)

1. Auchincloss, H. Jr. & Sultan, H. Antigen processing and presentation in transplantation. Curr. Opin. Immunol. 8, 681-687 (1996). (Pubitemid 26385398)
2. Rosenberg, A.S. & Singer, A. Cellular basis of skin allograft rejection: an in vivo model of immune-mediated tissue destruction. Annu. Rev. Immunol. 10, 333-358 (1992).
3. Ingulli, E. Mechanism of cellular rejection in transplantation. Pediatr. Nephrol. 25, 61-74 (2010).
4. Talmage, D.W., Dart, G., Radovich, J. & Lafferty, K.J. Activation of transplant immunity: effect of donor leukocytes on thyroid allograft rejection. Science 191, 385-388 (1976).
5. Richards, D.M. et al. Indirect minor histocompatibility antigen presentation by allograft recipient cells in the draining lymph node leads to the activation and clonal expansion of CD4+ T cells that cause obliterative airways disease. J. Immunol. 172, 3469-3479 (2004). (Pubitemid 38337927)
6. Ochando, J.C., Krieger, N.R. & Bromberg, J.S. Direct versus indirect allorecognition: Visualization of dendritic cell distribution and interactions during rejection and tolerization. Am. J. Transplant. 6, 2488-2496 (2006). (Pubitemid 44359439)
7. Larsen, C.P., Austyn, J.M. & Morris, P.J. The role of graft-derived dendritic leukocytes in the rejection of vascularized organ allograft. Recent findings on the migration and function of dendritic leukocytes after transplantation. Ann. Surg. 212, 308-315 (1990).
8. Valujskikh, A., Hartig, C. & Heeger, P.S. Indirectly primed CD8+ T cells are a prominent component of the allogeneic T-cell repertoire after skin graft rejection in mice. Transplantation 71, 418-421 (2001). (Pubitemid 32175979)
9. Garrod, K.R. et al. NK cell patrolling and elimination of donor-derived dendritic cells favor indirect alloreactivity. J. Immunol. 184, 2329-2336 (2010).
10. Lakkis, F.G., Arakelov, A., Konieczny, B.T. & Inoue, Y. Immunologic 'ignorance' of vascularized organ transplants in the absence of secondary lymphoid tissue. Nat. Med. 6, 686-688 (2000). (Pubitemid 30398793)
11. Zhou, P. et al. Secondary lymphoid organs are important but not absolutely required for allograft responses. Am. J. Transplant. 3, 259-266 (2003). (Pubitemid 36407042)
12. Barker, C.F. & Billingham, R.E. The role of afferent lymphatics in the rejection of skin homografts. J. Exp. Med. 128, 197-221 (1968).
13. Wang, J. et al. Donor lymphoid organs are a major site of alloreactive T-cell priming following intestinal transplantation. Am. J. Transplant. 6, 2563-2571 (2006). (Pubitemid 44571676)
14. Schenk, A.D., Nozaki, T., Rabant, M., Valujskikh, A. & Fairchild, R.L. Donor-reactive CD8 memory T cells infiltrate cardiac allografts within 24-h post-transplant in naive recipients. Am. J. Transplant. 8, 1652-1661 (2008).
15. Kreisel, D. et al. Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: an alternative mechanism of allorecognition. Nat. Med. 8, 233-239 (2002). (Pubitemid 34250100)
16. Gelman, A.E. et al. Cutting edge: Acute lung allograft rejection is independent of secondary lymphoid organs. J. Immunol. 182, 3969-3973 (2009).
17. Rocha, P.N., Plumb, T.J., Crowley, S.D. & Coffman, T.M. Effector mechanisms in transplant rejection. Immunol. Rev. 196, 51-64 (2003).
18. Strid, J. et al. Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat. Immunol. 9, 146-154 (2008).
19. Nishibu, A. et al. Behavioral responses of epidermal Langerhans cells in situ to local pathological stimuli. J. Invest. Dermatol. 126, 787-796 (2006).
20. Peters, N.C. et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970-974 (2008).
21. Chtanova, T. et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29, 487-496 (2008).
22. Matsuo, S., Kurisaki, A., Sugino, H., Hashimoto, I. & Nakanishi, H. Analysis of skin graft survival using green fluorescent protein transgenic mice. J. Med. Invest. 54, 267-275 (2007). (Pubitemid 350143741)
23. Ehst, B.D., Ingulli, E. & Jenkins, M.K. Development of a novel transgenic mouse for the study of interactions between CD4 and CD8 T cells during graft rejection. Am. J. Transplant. 3, 1355-1362 (2003). (Pubitemid 37288079)
24. Konjufca, V. & Miller, M.J. Two-photon microscopy of host-pathogen interactions: acquiring a dynamic picture of infection in vivo. Cell. Microbiol. 11, 551-559 (2009).
25. Ng, L.G., Mrass, P., Kinjyo, I., Reiner, S.L. & Weninger, W. Two-photon imaging of effector T-cell behavior: lessons from a tumor model. Immunol. Rev. 221, 147-162 (2008). (Pubitemid 351230121)
26. Kissenpfennig, A. et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22, 643-654 (2005). (Pubitemid 40719199)
27. Sen, D., Forrest, L., Kepler, T.B., Parker, I. & Cahalan, M.D. Selective and site-specific mobilization of dermal dendritic cells and Langerhans cells by TH1-and TH2-polarizing adjuvants. Proc. Natl. Acad. Sci. USA 107, 8334-8339 (2010).
28. Wang, L. et al. Langerin expressing cells promote skin immune responses under defined conditions. J. Immunol. 180, 4722-4727 (2008).
29. Obhrai, J.S. et al. Langerhans cells are not required for efficient skin graft rejection. J. Invest. Dermatol. 128, 1950-1955 (2008). (Pubitemid 352001229)
30. Beil, W.J., Meinardus-Hager, G., Neugebauer, D.C. & Sorg, C. Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J. Leukoc. Biol. 52, 135-142 (1992).
31. Léon, B., Lopez-Bravo, M. & Ardavin, C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26, 519-531 (2007). (Pubitemid 46602998)
32. Robben, P.M., LaRegina, M., Kuziel, W.A. & Sibley, L.D. Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J. Exp. Med. 201, 1761-1769 (2005). (Pubitemid 41002895)
33. Benichou, G., Valujskikh, A. & Heeger, P.S. Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J. Immunol. 162, 352-358 (1999). (Pubitemid 29018940)
34. Le Borgne, M. et al. Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo. Immunity 24, 191-201 (2006). (Pubitemid 43214588)
35. Valujskikh, A., Lantz, O., Celli, S., Matzinger, P. & Heeger, P.S. Cross-primed CD8+ T cells mediate graft rejection via a distinct effector pathway. Nat. Immunol. 3, 844-851 (2002).
36. Rosenberg, A.S. & Singer, A. Evidence that the effector mechanism of skin allograft rejection is antigen-specific. Proc. Natl. Acad. Sci. USA 85, 7739-7742 (1988).
37. Breart, B., Lemaitre, F., Celli, S. & Bousso, P. Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J. Clin. Invest. 118, 1390-1397 (2008). (Pubitemid 351500432)
38. Boissonnas, A., Fetler, L., Zeelenberg, I.S., Hugues, S. & Amigorena, S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 204, 345-356 (2007). (Pubitemid 46294550)
39. Van den Broeck, W., Derore, A. & Simoens, P. Anatomy and nomenclature of murine lymph nodes: Descriptive study and nomenclatory standardization in BALB/cAnNCrl mice. J. Immunol. Methods 312, 12-19 (2006). (Pubitemid 43795993)
40. Celli, S., Garcia, Z. & Bousso, P. CD4 T cells integrate signals delivered during successive DC encounters in vivo. J. Exp. Med. 202, 1271-1278 (2005). (Pubitemid 41586957)