Batf3-dependent dendritic cells in the renal lymph node induce tolerance against circulating antigens

Journal of the American Society of Nephrology

Volumn 24, Issue 4, 2013, Pages 543-549

  Gottschalk, Catherine ^a   Damuzzo, Vera ^a,e   Gotot, Janine ^a   Kroczek, Richard A ^b   Yagita, Hideo ^c   Murphy, Kenneth M ^d   Knolle, Percy A ^a   Ludwig Portugall, Isis ^a   Kurts, Christian ^a  

^a UNIVERSITY OF BONN   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; GAMMA INTERFERON; OVALBUMIN; PROGRAMMED DEATH 1 LIGAND 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BATF3; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; IMMUNOLOGICAL TOLERANCE; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL LYMPH NODE; T LYMPHOCYTE ACTIVATION;

EID: 84875710538     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012101022     Document Type: Article

References (34)

1. Li M, Davey GM, Sutherland RM, Kurts C, Lew AM, Hirst C, Carbone FR, Heath WR: Cellassociated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J Immunol 166: 6099-6103, 2001
2. Gütgemann I, Darling JM, Greenberg HB, Davis MM, Chien YH: A blood-borne antigen induces rapid T-B cell contact: A potential mechanism for tolerance induction. Immunology 107: 420-425, 2002
3. Nolte MA, Beliën JA, Schadee-Eestermans I, Jansen W, Unger WW, van Rooijen N, Kraal G, Mebius RE: A conduit system distributes chemokines and small blood-borne molecules through the splenic white pulp. J Exp Med 198: 505-512, 2003
4. Limmer A, Ohl J, Kurts C, Ljunggren HG, Reiss Y, Groettrup M, Momburg F, Arnold B, Knolle PA: Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 6: 1348-1354, 2000
5. Lukacs-Kornek V, Burgdorf S, Diehl L, Specht S, Kornek M, Kurts C: The kidney-renal lymph node-system contributes to cross-tolerance against innocuous circulating antigen. J Immunol 180: 706-715, 2008
6. Keir ME, Butte MJ, Freeman GJ, Sharpe AH: PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 26: 677-704, 2008
7. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N,Okazaki T, Byrne MC, Horton HF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T: Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 192: 1027-1034, 2000
8. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, Iwai Y, Long AJ, Brown JA, Nunes R, Greenfield EA, Bourque K, Boussiotis VA, Carter LL, Carreno BM, Malenkovich N, Nishimura H, Okazaki T, Honjo T, Sharpe AH, Freeman GJ: PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2: 261-268, 2001
9. Gotot J, Gottschalk C, Leopold S, Knolle PA, Yagita H, Kurts C, Ludwig-Portugall I: Regulatory T cells use programmed death 1 ligands to directly suppress autoreactive B cells in vivo. Proc Natl Acad Sci U S A 109: 10468-10473, 2012
10. Kurts C, Heath WR, Carbone FR, Allison J, Miller JF, Kosaka H: Constitutive class Irestricted exogenous presentation of self antigens in vivo. J Exp Med 184: 923-930, 1996
11. Kurts C, Robinson BW, Knolle PA: Crosspriming in health and disease. Nat Rev Immunol 10: 403-414, 2010
12. Bonifaz L, Bonnyay D, Mahnke K, Rivera M, Nussenzweig MC, Steinman RM: 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: 1627-1638, 2002
13. den Haan JM, Lehar SM, Bevan MJ: CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192: 1685-1696, 2000
14. Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, Caminschi I, Allan RS, Wojtasiak M, Shortman K, Carbone FR, Brooks AG, Heath WR: Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10: 488-495, 2009
15. del Rio ML, Rodriguez-Barbosa JI, Kremmer E, Förster R: CD103- and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J Immunol 178: 6861-6866, 2007
16. Dorner BG, Dorner MB, Zhou X, Opitz C, Mora A, Güttler S, Hutloff A, Mages HW, Ranke K, Schaefer M, Jack RS, Henn V, Kroczek RA: Selective expression of the chemokine receptorXCR1 on cross-presenting dendritic cells determines cooperation with CD8+ T cells. Immunity 31: 823-833, 2009
17. Bachem A, Hartung E, Güttler S, Mora A, Zhou X, Hegemann A, Plantinga M, Mazzini E, Stoitzner P, Gurka S, Henn V, Mages HW, Kroczek RA: Expression of XCR1 characterizes the Batf3-dependent lineage of dendritic cells capable of antigen cross-presentation. Front Immunol 3: 214, 2012
18. Kurts C, Kosaka H, Carbone FR, Miller JF, Heath WR: Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J Exp Med 186: 239-245, 1997
19. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, Calderon B, Schraml BU, Unanue ER, Diamond MS, Schreiber RD, Murphy TL, Murphy KM: Batf3 deficiency reveals a critical role for CD8alpha + dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100, 2008
20. Selenko-Gebauer N, Majdic O, Szekeres A, Höfler G, Guthann E, Korthäuer U, Zlabinger G, Steinberger P, Pickl WF, Stockinger H, Knapp W, Stöckl J: B7-H1 (programmed death-1 ligand) on dendritic cells is involved in the induction and maintenance of T cell anergy. J Immunol 170: 3637-3644, 2003
21. Yamazaki T, Akiba H, Iwai H,Matsuda H, Aoki M, Tanno Y, Shin T, Tsuchiya H, Pardoll DM, Okumura K, Azuma M, Yagita H: Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 169: 5538-5545, 2002
22. Belz GT, Behrens GM, Smith CM, Miller JF, Jones C, Lejon K, Fathman CG, Mueller SN, Shortman K, Carbone FR, Heath WR: The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissueassociated antigens. J Exp Med 196: 1099-1104, 2002
23. Probst HC, McCoy K, Okazaki T, Honjo T, van den Broek M: Resting dendritic cells induce peripheral CD8+ T cell tolerance through PD-1 and CTLA-4. Nat Immunol 6: 280-286, 2005
24. Tadagavadi RK, Reeves WB: Renal dendritic cells ameliorate nephrotoxic acute kidney injury. J Am Soc Nephrol 21: 53-63, 2010
25. Macconi D, Chiabrando C, Schiarea S, Aiello S, Cassis L, Gagliardini E, Noris M, Buelli S, Zoja C, Corna D, Mele C, Fanelli R, Remuzzi G, Benigni A: Proteasomal processing of albumin by renal dendritic cells generates antigenic peptides. J Am Soc Nephrol 20: 123-130, 2009
26. Hochheiser K, Engel DR, Hammerich L, Heymann F, Knolle PA, Panzer U, Kurts C: Kidney dendritic cells become pathogenic during crescentic glomerulonephritis with proteinuria. J Am Soc Nephrol 22: 306-316, 2011
27. Nelson PJ, Rees AJ, Griffin MD, Hughes J, Kurts C, Duffield J: The renalmononuclear phagocytic system. J Am Soc Nephrol 23: 194-203, 2012
28. Teteris SA, Engel DR, Kurts C: Homeostatic and pathogenic role of renal dendritic cells. Kidney Int 80: 139-145, 2011
29. Larrubia JR, Benito-Martínez S, Miquel J, Calvino M, Sanz-de-Villalobos E, González-Praetorius A, Albertos S, García-Garzón S, Lokhande M, Parra-Cid T: Bim-mediated apoptosisandPD-1/PD-L1pathway impair reactivity of PD1(+)/CD127(-) HCV-specific CD8(+) cells targeting the virus in chronic hepatitis C virus infection. Cell Immunol 269: 104-114, 2011
30. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366: 2443-2454, 2012
31. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC,Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF,Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM: Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366: 2455-2465, 2012
32. Rees A: Cross dendritic cells anger T cells after kidney injury. J Am Soc Nephrol 20: 3-5, 2009
33. Tsushima F, Iwai H, Otsuki N, Abe M, Hirose S, Yamazaki T, Akiba H, Yagita H, Takahashi Y, Omura K, Okumura K, Azuma M: Preferential contribution of B7-H1 to programmed death-1-mediated regulation of haptenspecific allergic inflammatory responses. Eur J Immunol 33: 2773-2782, 2003
34. Heymann F, Meyer-Schwesinger C, Hamilton-Williams EE, Hammerich L, Panzer U, Kaden S, Floege J, Gröne HJ, Kurts C: Kidney dendritic cell activation is required for progression of renal disease in amousemodel of glomerular injury. J Clin Invest 119: 1286-1297, 2009