Constitutive Crosspresentation of Tissue Antigens by Dendritic Cells Controls CD8+ T Cell Tolerance In Vivo

Immunity

Volumn 28, Issue 4, 2008, Pages 521-532

  Luckashenak, Nancy ^a   Schroeder, Samira ^a   Endt, Katrin ^a   Schmidt, Darja ^a   Mahnke, Karsten ^b   Bachmann, Martin F ^c   Marconi, Peggy ^d   Deeg, Cornelia A ^a   Brocker, Thomas ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c CYTOS BIOTECHNOLOGY AG   (Switzerland)

^d UNIVERSITY OF FERRARA   (Italy)

Author keywords

CELLIMMUNO

Indexed keywords

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS PRESENTATION; CROSS TOLERANCE; DENDRITIC CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; IMMUNOREGULATION; IN VIVO STUDY; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS; APOPTOSIS; AUTOIMMUNE DISEASES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CROSS-PRIMING; DENDRITIC CELLS; IMMUNE TOLERANCE; LISTERIA MONOCYTOGENES; LYMPHOID TISSUE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; RAC1 GTP-BINDING PROTEIN;

EID: 41549093091     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.02.018     Document Type: Article

References (71)

1. Adler A.J., Marsh D.W., Yochum G.S., Guzzo J.L., Nigam A., Nelson W.G., and Pardoll D.M. CD4+ T cell tolerance to parenchymal self-antigens requires presentation by bone marrow-derived antigen-presenting cells. J. Exp. Med. 187 (1998) 1555-1564
2. Albert M., Sauter B., and Bhardwaj N. DCs acquire Ag from apoptotic cells and induce class I-restricted CTLs. Nature 392 (1998) 86-89
3. Albert M.L., Kim J.I., and Birge R.B. alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat. Cell Biol. 2 (2000) 899-905
4. Albert M.L., Pearce S.F., Francisco L.M., Sauter B., Roy P., Silverstein R.L., and Bhardwaj N. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 188 (1998) 1359-1368
5. Belz G.T., Behrens G.M., Smith C.M., Miller J.F., Jones C., Lejon K., Fathman C.G., Mueller S.N., Shortman K., Carbone F.R., and Heath W.R. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 196 (2002) 1099-1104
6. Bennett S.R., Carbone F.R., Karamalis F., Flavell R.A., Miller J.F., and Heath W.R. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393 (1998) 478-480
7. Bennett S.R., Carbone F.R., Karamalis F., Miller J.F., and Heath W.R. Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help. J. Exp. Med. 186 (1997) 65-70
8. Benvenuti F., Hugues S., Walmsley M., Ruf S., Fetler L., Popoff M., Tybulewicz V.L., and Amigorena S. Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science 305 (2004) 1150-1153
9. Bevan M.J. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143 (1976) 1283-1288
10. Blattman J.N., Antia R., Sourdive D.J., Wang X., Kaech S.M., Murali-Krishna K., Altman J.D., and Ahmed R. Estimating the precursor frequency of naive antigen-specific CD8 T cells. J. Exp. Med. 195 (2002) 657-664
11. Bonifaz L., Bonnyay D., Mahnke K., Rivera M., Nussenzweig M.C., and Steinman R.M. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 196 (2002) 1627-1638
12. Brocker T., Riedinger M., and Karjalainen K. Targeted expression of major histocompatibility complex (MHC) class II molecules demonstrates that dendritic cells can induce negative but not positive selection of thymocytes in vivo. J. Exp. Med. 185 (1997) 541-550
13. Buhlmann J.E., Gonzalez M., Ginther B., Panoskaltsis-Mortari A., Blazar B.R., Greiner D.L., Rossini A.A., Flavell R., Noelle R.J., Burgdorf S., et al. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316 (2007) 612-616
14. Burgdorf S., Lukacs-Kornek V., and Kurts C. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176 (2006) 6770-6776
15. Burgdorf S., Kautz A., Böhnert V., Knolle P.A., and Kurts C. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316 (2007) 612-616
16. Cho B.K., Rao V.P., Ge Q., Eisen H.N., and Chen J. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J. Exp. Med. 192 (2000) 549-556
17. Cho J.H., Boyman O., Kim H.O., Hahm B., Rubinstein M.P., Ramsey C., Kim D.M., Surh C.D., and Sprent J. An intense form of homeostatic proliferation of naive CD8+ cells driven by IL-2. J. Exp. Med. 204 (2007) 1787-1801
18. Coles R.M., Mueller S.N., Heath W.R., Carbone F.R., and Brooks A.G. Progression of armed CTL from draining lymph node to spleen shortly after localized infection with herpes simplex virus 1. J. Immunol. 168 (2002) 834-838
19. Cose S., Brammer C., Khanna K.M., Masopust D., and Lefrancois L. Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur. J. Immunol. 36 (2006) 1423-1433
20. Derbinski J., Schulte A., Kyewski B., and Klein L. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat. Immunol. 2 (2001) 1032-1039
21. DeVoss J., Hou Y., Johannes K., Lu W., Liou G.I., Rinn J., Chang H., Caspi R.R., Fong L., and Anderson M.S. Spontaneous autoimmunity prevented by thymic expression of a single self-antigen. J. Exp. Med. 203 (2006) 2727-2735
22. Faideau B., Lotton C., Lucas B., Tardivel I., Elliott J.F., Boitard C., and Carel J.C. Tolerance to proinsulin-2 is due to radioresistant thymic cells. J. Immunol. 177 (2006) 53-60
23. Gaebler J., Arnold J., and Kyewski B. Promiscuous gene expression and the developmental dynamics of medullary thymic epithelial cells. Eur. J. Immunol. 37 (2007) 3363-3372
24. Gallegos A.M., and Bevan M.J. Central tolerance to tissue-specific antigens mediated by direct and indirect antigen presentation. J. Exp. Med. 200 (2004) 1039-1049
25. Gallegos A.M., and Bevan M.J. Central tolerance: Good but imperfect. Immunol. Rev. 209 (2006) 290-296
26. Garcia C.A., Prabakar K.R., Diez J., Cao Z.A., Allende G., Zeller M., Dogra R., Mendez A., Rosenkranz E., Dahl U., et al. Dendritic cells in human thymus and periphery display a proinsulin epitope in a transcription-dependent, capture-independent fashion. J. Immunol. 175 (2005) 2111-2122
27. Goldrath A.W., Luckey C.J., Park R., Benoist C., and Mathis D. The molecular program induced in T cells undergoing homeostatic proliferation. Proc. Natl. Acad. Sci. USA 101 (2004) 16885-16890
28. Graham D.B., Stephenson L.M., Lam S.K., Brim K., Lee H.M., Bautista J., Gilfillan S., Akilesh S., Fujikawa K., and Swat W. An ITAM-signaling pathway controls cross-presentation of particulate but not soluble antigens in dendritic cells. J. Exp. Med. 204 (2007) 2889-2897
29. Hamilton S.E., Wolkers M.C., Schoenberger S.P., and Jameson S.C. The generation of protective memory-like CD8+ T cells during homeostatic proliferation requires CD4+ T cells. Nat. Immunol. 7 (2006) 475-481
30. Harshyne L.A., Zimmer M.I., Watkins S.C., and Barratt-Boyes S.M. A role for class A scavenger receptor in dendritic cell nibbling from live cells. J. Immunol. 170 (2003) 2302-2309
31. Heath W.R., and Carbone F.R. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 19 (2001) 47-64
32. Hernandez J., Aung S., Redmond W.L., and Sherman L.A. Phenotypic and functional analysis of CD8(+) T cells undergoing peripheral deletion in response to cross-presentation of self-antigen. J. Exp. Med. 194 (2001) 707-717
33. Hordijk P.L. Regulation of NADPH oxidases: The role of Rac proteins. Circ. Res. 98 (2006) 453-462
34. Huang A.Y., Golumbek P., Ahmadzadeh M., Jaffee E., Pardoll D.M., and Levitsky H.I. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 264 (1994) 961-965
35. Huang F.P., Platt N., Wykes M., Major J.R., Powell T.J., Jenkins C.D., and MacPherson G.G. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191 (2000) 435-444
36. Kaksonen M., Toret C.P., and Drubin D.G. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7 (2006) 404-414
37. Kerksiek K.M., Niedergang F., Chavrier P., Busch D.H., and Brocker T. Selective Rac1 inhibition in dendritic cells diminishes apoptotic cell uptake and cross-presentation in vivo. Blood 105 (2005) 742-749
38. Kurts C., Heath W.R., Carbone F.R., Allison J., Miller J.F., and Kosaka H. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184 (1996) 923-930
39. Kurts C., Kosaka H., Carbone F.R., Miller J.F., and Heath W.R. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J. Exp. Med. 186 (1997) 239-245
40. Kurts C., Miller J.F., Subramaniam R.M., Carbone F.R., and Heath W.R. Major histocompatibility complex class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction. J. Exp. Med. 188 (1998) 409-414
41. Kyewski B., and Klein L. A central role for central tolerance. Annu. Rev. Immunol. 24 (2006) 571-606
42. Lauber K., Blumenthal S.G., Waibel M., and Wesselborg S. Clearance of apoptotic cells: Getting rid of the corpses. Mol. Cell 14 (2004) 277-287
43. Lauterbach H., Kerksiek K.M., Busch D.H., Berto E., Bozac A., Mavromara P., Manservigi R., Epstein A.L., Marconi P., and Brocker T. Protection from bacterial infection by a single vaccination with replication-deficient mutant herpes simplex virus type 1. J. Virol. 78 (2004) 4020-4028
44. Lee J.-W., Epardaud M., Sun J., Becker J.E., Cheng A.C., Yonekura A.R., Heath J.K., and Turley S.J. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat. Immunol. 8 (2007) 181-190
45. Li M., Davey G.M., Sutherland R.M., Kurts C., Lew A.M., Hirst C., Carbone F.R., and Heath W.R. Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J. Immunol. 166 (2001) 6099-6103
46. Liu G.Y., Fairchild P.J., Smith R.M., Prowle J.R., Kioussis D., and Wraith D.C. Low avidity recognition of self-antigen by T cells permits escape from central tolerance. Immunity 3 (1995) 407-415
47. Mackay C.R. Homing of naive, memory and effector lymphocytes. Curr. Opin. Immunol. 5 (1993) 423-427
48. Mathis D., and Benoist C. Back to central tolerance. Immunity 20 (2004) 509-516
49. Morgan D.J., Kurts C., Kreuwel H.T., Holst K.L., Heath W.R., and Sherman L.A. Ontogeny of T cell tolerance to peripherally expressed antigens. Proc. Natl. Acad. Sci. USA 96 (1999) 3854-3858
50. Moser M. Dendritic cells in immunity and tolerance-do they display opposite functions?. Immunity 19 (2003) 5-8
51. Neuenhahn M., Kerksiek K.M., Nauerth M., Suhre M.H., Schiemann M., Gebhardt F.E., Stemberger C., Panthel K., Schroder S., Chakraborty T., et al. CD8alpha(+) dendritic cells are required for efficient entry of Listeria monocytogenes into the spleen. Immunity 25 (2006) 619-630
52. Park D., Tosello-Trampont A.C., Elliott M.R., Lu M., Haney L.B., Ma Z., Klibanov A.L., Mandell J.W., and Ravichandran K.S. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450 (2007) 430-434
53. Pooley J.L., Heath W.R., and Shortman K. Cutting edge: Intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166 (2001) 5327-5330
54. Powrie F. T cells in inflammatory bowel disease: Protective and pathogenic roles. Immunity 5 (1995) 171-174
55. Redmond W.L., and Sherman L.A. Peripheral tolerance of CD8 T lymphocytes. Immunity 22 (2005) 275-284
56. Roth E., Schwartzkopff J., and Pircher H. CD40 ligation in the presence of self-reactive CD8 T cells leads to severe immunopathology. J. Immunol. 168 (2002) 5124-5129
57. Ruedl C., Storni T., Lechner F., Bachi T., and Bachmann M.F. Cross-presentation of virus-like particles by skin-derived CD8(-) dendritic cells: A dispensable role for TAP. Eur. J. Immunol. 32 (2002) 818-825
58. Savina A., Jancic C., Hugues S., Guermonprez P., Vargas P., Moura I.C., Lennon-Duménil A.M., Seabra M.C., Raposo G., and Amigorena S. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126 (2006) 205-218
59. Scheinecker C., McHugh R., Shevach E.M., and Germain R.N. Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J. Exp. Med. 196 (2002) 1079-1090
60. Segal A.W. How neutrophils kill microbes. Annu. Rev. Immunol. 23 (2005) 197-223
61. Sigal L.J., Crotty S., Andino R., and Rock K.L. Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398 (1999) 77-80
62. Speiser D.E., Miranda R., Zakarian A., Bachmann M.F., McKall-Faienza K., Odermatt B., Hanahan D., Zinkernagel R.M., and Ohashi P.S. Self antigens expressed by solid tumors do not efficiently stimulate naive or activated T cells: Implications for immunotherapy. J. Exp. Med. 186 (1997) 645-653
63. Steinman R., Turley S., Mellman I., and Inaba K. The induction of tolerance by DCs that have captured apoptotic cells. J. Exp. Med. 191 (2000) 411-416
64. Storni T., and Bachmann M.F. Loading of MHC class I and II presentation pathways by exogenous antigens: A quantitative in vivo comparison. J. Immunol. 172 (2004) 6129-6135
65. Storni T., Ruedl C., Schwarz K., Schwendener R.A., Renner W.A., and Bachmann M.F. Nonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects. J. Immunol. 172 (2004) 1777-1785
66. Turley S., Poirot L., Hattori M., Benoist C., and Mathis D. Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198 (2003) 1527-1537
67. Vermaelen K.Y., Carro-Muino I., Lambrecht B.N., and Pauwels R.A. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193 (2001) 51-60
68. Vezys V., and Lefrancois L. Cutting edge: Inflammatory signals drive organ-specific autoimmunity to normally cross-tolerizing endogenous antigen. J. Immunol. 169 (2002) 6677-6680
69. West M.A., Prescott A.R., Eskelinen E.L., Ridley A.J., and Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr. Biol. 10 (2000) 839-848
70. Wolkers M.C., Brouwenstijn N., Bakker A.H., Toebes M., and Schumacher T.N. Antigen bias in T cell cross-priming. Science 304 (2004) 1314-1317
71. Zehn D., and Bevan M.J. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity 25 (2006) 261-270