IgE/FcεRI-mediated antigen cross-presentation by dendritic cells enhances anti-tumor immune responses

Cell Reports

Volumn 10, Issue 9, 2015, Pages 1487-1495

  Platzer, Barbara ^a   Elpek, KutluG ^b   Cremasco, Viviana ^b   Baker, Kristi ^a   Stout, MadeleineM ^a   Schultz, Cornelia ^a   Dehlink, Eleonora ^a,c   Shade, Kai TingC ^a   Anthony, RobertM ^a   Blumberg, RichardS ^a   Turley, ShannonJ ^b,d   Fiebiger, Edda ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c UNIV KLIN KINDER JUGENDHEILKUNDE   (Austria)

^d GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC EPSILON RECEPTOR; FC RECEPTOR; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E RECEPTOR; INTERLEUKIN 12; MYELOID DIFFERENTIATION FACTOR 88; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CONCENTRATION RESPONSE; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; IN VIVO STUDY; LYMPHOCYTOPOIESIS; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TUMOR IMMUNITY;

EID: 84924545972     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.015     Document Type: Article

References (39)

1. Bachem A., Güttler S., Hartung E., Ebstein F., Schaefer M., Tannert A., Salama A., Movassaghi K., Opitz C., Mages H.W., et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J.Exp. Med. 2010, 207:1273-1281.
2. Baker K., Qiao S.W., Kuo T.T., Aveson V.G., Platzer B., Andersen J.T., Sandlie I., Chen Z., de Haar C., Lencer W.I., et al. Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b+ dendritic cells. Proc. Natl. Acad. Sci. USA 2011, 108:9927-9932.
3. Baker K., Rath T., Flak M.B., Arthur J.C., Chen Z., Glickman J.N., Zlobec I., Karamitopoulou E., Stachler M.D., Odze R.D., et al. Neonatal Fc receptor expression in dendritic cells mediates protective immunity against colorectal cancer. Immunity 2013, 39:1095-1107.
4. Burgdorf S., Schölz C., Kautz A., Tampé R., Kurts C. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 2008, 9:558-566.
5. Chatterjee B., Smed-Sörensen A., Cohn L., Chalouni C., Vandlen R., Lee B.C., Widger J., Keler T., Delamarre L., Mellman I. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 2012, 120:2011-2020.
6. Daniels T.R., Leuchter R.K., Quintero R., Helguera G., Rodríguez J.A., Martínez-Maza O., Schultes B.C., Nicodemus C.F., Penichet M.L. Targeting HER2/neu with a fully human IgE to harness the allergic reaction against cancer cells. Cancer Immunol. Immunother. 2012, 61:991-1003.
7. Daniels-Wells T.R., Helguera G., Leuchter R.K., Quintero R., Kozman M., Rodríguez J.A., Ortiz-Sánchez E., Martínez-Maza O., Schultes B.C., Nicodemus C.F., Penichet M.L. A novel IgE antibody targeting the prostate-specific antigen as a potential prostate cancer therapy. BMC Cancer 2013, 13:195.
8. den Haan J.M., Lehar S.M., Bevan M.J. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic Tcells invivo. J.Exp. Med. 2000, 192:1685-1696.
9. Dhodapkar M.V., Sznol M., Zhao B., Wang D., Carvajal R.D., Keohan M.L., Chuang E., Sanborn R.E., Lutzky J., Powderly J., et al. Induction of antigen-specific immunity with a vaccine targeting NY-ESO-1 to the dendritic cell receptor DEC-205. Sci. Transl. Med. 2014, 6:232ra251.
10. Falo L.D., Kovacsovics-Bankowski M., Thompson K., Rock K.L. Targeting antigen into the phagocytic pathway invivo induces protective tumour immunity. Nat. Med. 1995, 1:649-653.
11. Fu S.L., Pierre J., Smith-Norowitz T.A., Hagler M., Bowne W., Pincus M.R., Mueller C.M., Zenilman M.E., Bluth M.H. Immunoglobulin E antibodies from pancreatic cancer patients mediate antibody-dependent cell-mediated cytotoxicity against pancreatic cancer cells. Clin. Exp. Immunol. 2008, 153:401-409.
12. Galli S.J., Tsai M. IgE and mast cells in allergic disease. Nat. Med. 2012, 18:693-704.
13. Guilliams M., Bruhns P., Saeys Y., Hammad H., Lambrecht B.N. The function of Fcγ receptors in dendritic cells and macrophages. Nat. Rev. Immunol. 2014, 14:94-108.
14. Haniffa M., Collin M., Ginhoux F. Ontogeny and functional specialization of dendritic cells in human and mouse. Adv. Immunol. 2013, 120:1-49.
15. Jensen-Jarolim E., Achatz G., Turner M.C., Karagiannis S., Legrand F., Capron M., Penichet M.L., Rodríguez J.A., Siccardi A.G., Vangelista L., et al. AllergoOncology: the role of IgE-mediated allergy in cancer. Allergy 2008, 63:1255-1266.
16. Joffre O.P., Segura E., Savina A., Amigorena S. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 2012, 12:557-569.
17. Josephs D.H., Spicer J.F., Corrigan C.J., Gould H.J., Karagiannis S.N. Epidemiological associations of allergy, IgE and cancer. Clin. Exp. Allergy 2013, 43:1110-1123.
18. Karagiannis S.N., Josephs D.H., Karagiannis P., Gilbert A.E., Saul L., Rudman S.M., Dodev T., Koers A., Blower P.J., Corrigan C., et al. Recombinant IgE antibodies for passive immunotherapy of solid tumours: from concept towards clinical application. Cancer Immunol. Immunother. 2012, 61:1547-1564.
19. Kinet J.P. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu. Rev. Immunol. 1999, 17:931-972.
20. Kreer C., Rauen J., Zehner M., Burgdorf S. Cross-presentation: how to get there - or how to get the ER. Front. Immunol. 2011, 2:87.
21. Marichal T., Starkl P., Reber L.L., Kalesnikoff J., Oettgen H.C., Tsai M., Metz M., Galli S.J. A beneficial role for immunoglobulin E in host defense against honeybee venom. Immunity 2013, 39:963-975.
22. Mende I., Engleman E.G. Breaking tolerance to tumors with dendritic cell-based immunotherapy. Ann. N Y Acad. Sci. 2005, 1058:96-104.
23. Nigro E.A., Brini A.T., Soprana E., Ambrosi A., Dombrowicz D., Siccardi A.G., Vangelista L. Antitumor IgE adjuvanticity: key role of Fc epsilon RI. J.Immunol. 2009, 183:4530-4536.
24. Palm N.W., Rosenstein R.K., Yu S., Schenten D.D., Florsheim E., Medzhitov R. Bee venom phospholipase A2 induces a primary type 2 response that is dependent on the receptor ST2 and confers protective immunity. Immunity 2013, 39:976-985.
25. Palucka K., Banchereau J. Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 2012, 12:265-277.
26. Platzer B., Ruiter F., van der Mee J., Fiebiger E. Soluble IgE receptors-elements of the IgE network. Immunol. Lett. 2011, 141:36-44.
27. Platzer B., Baker K., Vera M.P., Singer K., Panduro M., Lexmond W.S., Turner D., Vargas S.O., Kinet J.P., Maurer D., et al. Dendritic cell-bound IgE functions to restrain allergic inflammation at mucosal sites. Mucosal Immunol. 2014, Published online September 17, 2014. 10.1038/mi.2014.85.
28. Platzer B., Stout M., Fiebiger E. Antigen cross-presentation of immune complexes. Front. Immunol. 2014, 5:140.
29. Regnault A., Lankar D., Lacabanne V., Rodriguez A., Théry C., Rescigno M., Saito T., Verbeek S., Bonnerot C., Ricciardi-Castagnoli P., Amigorena S. Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J.Exp. Med. 1999, 189:371-380.
30. Sasaki K., Pardee A.D., Okada H., Storkus W.J. IL-4 inhibits VLA-4 expression on Tc1 cells resulting in poor tumor infiltration and reduced therapy benefit. Eur. J. Immunol. 2008, 38:2865-2873.
31. Schuette V., Burgdorf S. The ins-and-outs of endosomal antigens for cross-presentation. Curr. Opin. Immunol. 2014, 26:63-68.
32. Schuurhuis D.H., Ioan-Facsinay A., Nagelkerken B., van Schip J.J., Sedlik C., Melief C.J., Verbeek J.S., Ossendorp F. Antigen-antibody immune complexes empower dendritic cells to efficiently prime specific CD8+ CTL responses invivo. J.Immunol. 2002, 168:2240-2246.
33. Segura E., Durand M., Amigorena S. Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J.Exp. Med. 2013, 210:1035-1047.
34. Sharma R.K., Elpek K.G., Yolcu E.S., Schabowsky R.H., Zhao H., Bandura-Morgan L., Shirwan H. Costimulation as a platform for the development of vaccines: a peptide-based vaccine containing a novel form of 4-1BB ligand eradicates established tumors. Cancer Res. 2009, 69:4319-4326.
35. Staff C., Magnusson C.G., Hojjat-Farsangi M., Mosolits S., Liljefors M., Frödin J.E., Wahrén B., Mellstedt H., Ullenhag G.J. Induction of IgM, IgA and IgE antibodies in colorectal cancer patients vaccinated with a recombinant CEA protein. J.Clin. Immunol. 2012, 32:855-865.
36. Tacken P.J., de Vries I.J., Torensma R., Figdor C.G. Dendritic-cell immunotherapy: from exvivo loading to invivo targeting. Nat. Rev. Immunol. 2007, 7:790-802.
37. Tomita Y., Yuno A., Tsukamoto H., Senju S., Kuroda Y., Hirayama M., Irie A., Kawahara K., Yatsuda J., Hamada A., et al. Identification of promiscuous KIF20A long peptides bearing both CD4+ and CD8+ T-cell epitopes: KIF20A-specific CD4+ T-cell immunity in patients with malignant tumor. Clin. Cancer Res. 2013, 19:4508-4520.
38. Weimershaus M., Maschalidi S., Sepulveda F., Manoury B., van Endert P., Saveanu L. Conventional dendritic cells require IRAP-Rab14 endosomes for efficient cross-presentation. J.Immunol. 2012, 188:1840-1846.
39. Zwart W., Griekspoor A., Kuijl C., Marsman M., van Rheenen J., Janssen H., Calafat J., van Ham M., Janssen L., van Lith M., et al. Spatial separation of HLA-DM/HLA-DR interactions within MIIC and phagosome-induced immune escape. Immunity 2005, 22:221-233.