Collaboration between tumor-specific CD4+ T cells and B cells in anti-cancer immunity

Oncotarget

Volumn 7, Issue 21, 2016, Pages 30211-30229

  Guy, Thomas V ^a,b   Terry, Alexandra M ^a,b   Bolton, Holly A ^a,b   Hancock, David G ^a,b   Zhu, Erhua ^a,b   Brink, Robert ^c   McGuire, Helen M ^a,b   Shklovskaya, Elena ^a,b   Fazekas De St Groth, Barbara ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Antibody; B cell; CD4 T cell; Immune response; Immunity; Immunology and Microbiology Section; Melanoma

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G3; TRANSCRIPTION FACTOR FOXP3; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CANCER CONTROL; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL LINEAGE; CELL SURVIVAL; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CORRELATION COEFFICIENT; CYTOKINE PRODUCTION; IMMUNOPHENOTYPING; LUNG METASTASIS; MELANOMA; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; TH1 CELL; TUMOR IMMUNITY; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; EXPERIMENTAL MELANOMA; GENE REARRANGEMENT; GENETICS; IMMUNOLOGY; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; TRANSGENIC MOUSE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CYTOKINES; IMMUNOGLOBULIN CLASS SWITCHING; KAPLAN-MEIER ESTIMATE; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; TUMOR BURDEN;

EID: 84971507008     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8797     Document Type: Article

References (51)

1. Yuan J, Adamow M, Ginsberg BA, Rasalan TS, Ritter E, Gallardo HF, Xu Y, Pogoriler E, Terzulli SL, Kuk D, Panageas KS, Ritter G, Sznol M, et al. Integrated NYESO-1 antibody and CD8+ T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab. Proc Natl Acad Sci U S A. 2011; 108:16723-16728. doi: 10.1073/pnas.1110814108
2. Sasada T, Suekane S. Variation of tumor-infiltrating lymphocytes in human cancers: controversy on clinical significance. Immunotherapy. 2011; 3:1235-1251. doi: 10.2217/imt.11.106
3. Reuschenbach M, von Knebel Doeberitz M, Wentzensen N. A systematic review of humoral immune responses against tumor antigens. Cancer Immunol Immunother. 2009; 58:1535-1544. doi: 10.1007/s00262-009-0733-4
4. Hermans IF, Daish A, Moroni-Rawson P, Ronchese F. Tumor-peptide-pulsed dendritic cells isolated from spleen or cultured in vitro from bone marrow precursors can provide protection against tumor challenge. Cancer Immunol Immunother. 1997; 44:341-347. doi:
5. Dobrzanski MJ, Reome JB, Dutton RW. Therapeutic effects of tumor-reactive type 1 and type 2 CD8+ T cell subpopulations in established pulmonary metastases. J Immunol. 1999; 162:6671-6680
6. Hanson HL, Donermeyer DL, Ikeda H, White JM, Shankaran V, Old LJ, Shiku H, Schreiber RD, Allen PM. Eradication of established tumors by CD8+ T cell adoptive immunotherapy. Immunity. 2000; 13:265-276
7. Overwijk WW, Theoret MR, Finkelstein SE, Surman DR, de Jong LA, Vyth-Dreese FA, Dellemijn TA, Antony PA, Spiess PJ, Palmer DC, Heimann DM, Klebanoff CA, Yu Z, et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med. 2003; 198:569-580. doi: 10.1084/jem.20030590
8. Perez-Diez A, Joncker NT, Choi K, Chan WF, Anderson CC, Lantz O, Matzinger P. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood. 2007; 109:5346-5354. doi: 10.1182/blood-2006-10-051318
9. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, Kaiser A, Paulos CM, Palmer DC, Touloukian CE, Ptak K, Gattinoni L, Wrzesinski C, Hinrichs CS, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood. 2008; 112:362-373. doi: blood-2007-11-120998 [pii]10.1182/blood-2007-11-120998
10. Quezada SA, Simpson TR, Peggs KS, Merghoub T, Vider J, Fan X, Blasberg R, Yagita H, Muranski P, Antony PA, Restifo NP, Allison JP. Tumor-reactive CD4+ T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J Exp Med. 2010; 207:637-650. doi: jem.20091918 [pii]10.1084/jem.20091918
11. Shklovskaya E, Terry AM, Guy TV, Buckley A, Bolton HA, Zhu E, Holst J, Fazekas de St Groth B. Tumourspecific CD4 T cells eradicate melanoma via indirect recognition of tumour-derived antigen. Immunol Cell Biol 2016. doi: 10.1038/icb.2016.14
12. Fremd C, Schuetz F, Sohn C, Beckhove P, Domschke C. B cell-regulated immune responses in tumor models and cancer patients. Oncoimmunology. 2013; 2:e25443. doi: 10.4161/onci.25443
13. Linnemann C, van Buuren MM, Bies L, Verdegaal EM, Schotte R, Calis JJ, Behjati S, Velds A, Hilkmann H, Atmioui DE, Visser M, Stratton MR, Haanen JB, et al. High-throughput epitope discovery reveals frequent recognition of neo-antigens by CD4+ T cells in human melanoma. Nat Med. 2015; 21:81-85. doi: 10.1038/nm.3773
14. Ladanyi A, Kiss J, Mohos A, Somlai B, Liszkay G, Gilde K, Fejos Z, Gaudi I, Dobos J, Timar J. Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol Immunother. 2011; 60:1729-1738. doi: 10.1007/s00262-011-1071-x
15. Nielsen JS, Sahota RA, Milne K, Kost SE, Nesslinger NJ, Watson PH, Nelson BH. CD20+ tumor-infiltrating lymphocytes have an atypical CD27-memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res. 2012; 18:3281-3292. doi: 10.1158/1078-0432.CCR-12-0234
16. Schmidt M, Hellwig B, Hammad S, Othman A, Lohr M, Chen Z, Boehm D, Gebhard S, Petry I, Lebrecht A, Cadenas C, Marchan R, Stewart JD, et al. A comprehensive analysis of human gene expression profiles identifies stromal immunoglobulin kappa C as a compatible prognostic marker in human solid tumors. Clin Cancer Res. 2012; 18:2695-2703. doi: 10.1158/1078-0432.CCR-11-2210
17. Zornig I, Halama N, Lorenzo Bermejo J, Ziegelmeier C, Dickes E, Migdoll A, Kaiser I, Waterboer T, Pawlita M, Grabe N, Ugurel S, Schadendorf D, Falk C, et al. Prognostic significance of spontaneous antibody responses against tumor-associated antigens in malignant melanoma patients. Int J Cancer. 2015; 136:138-151. doi: 10.1002/ijc.28980
18. Yamaguchi T, Takii Y, Maruyama S. Usefulness of serum p53 antibody measurement in colorectal cancer: an examination of 1384 primary colorectal cancer patients. Surg Today. 2014; 44:1529-1535. doi: 10.1007/s00595-013-0703-5
19. Qin Z, Richter G, Schuler T, Ibe S, Cao X, Blankenstein T. B cells inhibit induction of T cell-dependent tumor immunity. Nat Med. 1998; 4:627-630
20. Shah S, Divekar AA, Hilchey SP, Cho HM, Newman CL, Shin SU, Nechustan H, Challita-Eid PM, Segal BM, Yi KH, Rosenblatt JD. Increased rejection of primary tumors in mice lacking B cells: inhibition of anti-tumor CTL and TH1 cytokine responses by B cells. Int J Cancer. 2005; 117:574-586. doi: 10.1002/ijc.21177
21. Horikawa M, Minard-Colin V, Matsushita T, Tedder TF. Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice. J Clin Invest. 2011; 121:4268-4280. doi: 10.1172/JCI59266
22. Nimmerjahn F, Ravetch JV. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 2005; 310:1510-1512. doi: 10.1126/science.1118948
23. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell. 2005; 7:411-423. doi: 10.1016/j.ccr.2005.04.014
24. Phan TG, Amesbury M, Gardam S, Crosbie J, Hasbold J, Hodgkin PD, Basten A, Brink R. B cell receptorindependent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J Exp Med. 2003; 197(7):845-860
25. Seder RA, Paul WE, Davis MM, Fazekas de St Groth B. The presence of interleukin 4 during in vitro priming determines the lymphokine-producing potential of CD4+ T cells from T cell receptor transgenic mice. J Exp Med. 1992; 176:1091-1098
26. Xie Y, Akpinarli A, Maris C, Hipkiss EL, Lane M, Kwon EK, Muranski P, Restifo NP, Antony PA. Naive tumorspecific CD4+ T cells differentiated in vivo eradicate established melanoma. J Exp Med. 2010; 207:651-667. doi: jem.20091921 [pii]10.1084/jem.20091921
27. Macaulay AE, DeKruyff RH, Goodnow CC, Umetsu DT. Antigen-specific B cells preferentially induce CD4+ T cells to produce IL-4. J Immunol. 1997; 158:4171-4179
28. Lindner S, Dahlke K, Sontheimer K, Hagn M, Kaltenmeier C, Barth TF, Beyer T, Reister F, Fabricius D, Lotfi R, Lunov O, Nienhaus GU, Simmet T, et al. Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013; 73:2468-2479. doi: 10.1158/0008-5472.CAN-12-3450
29. Balkwill F, Montfort A, Capasso M. B regulatory cells in cancer. Trends in immunology. 2013; 34:169-173. doi: 10.1016/j.it.2012.10.007
30. Martin RM, Brady JL, Lew AM. The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J Immunol Methods. 1998; 212:187-192
31. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, Huhn RD, Song W, Li D, Sharp LL, Torigian DA, O'Dwyer PJ, Vonderheide RH. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science. 2011; 331:1612-1616. doi: 10.1126/science.1198443
32. Candolfi M, Curtin JF, Yagiz K, Assi H, Wibowo MK, Alzadeh GE, Foulad D, Muhammad AK, Salehi S, Keech N, Puntel M, Liu C, Sanderson NR, et al. B cells are critical to T-cell-mediated antitumor immunity induced by a combined immune-stimulatory/conditionally cytotoxic therapy for glioblastoma. Neoplasia. 2011; 13:947-960
33. Bolton HA, Zhu E, Terry AM, Guy TV, Koh W-P, Tan S-Y, Power CA, Bertolino P, Lahl K, Sparwasser T, Shklovskaya E, Fazekas de St Groth B. Selective Treg reconstitution during lymphopenia normalizes DC costimulation and prevents graft-versus-host disease. J Clin Invest. 2015; 125:3627-3641. doi: 10.1172/JCI76031
34. Linton PJ, Bautista B, Biederman E, Bradley ES, Harbertson J, Kondrack RM, Padrick RC, Bradley LM. Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J Exp Med. 2003; 197:875-883. doi: 10.1084/jem.20021290
35. Berg LJ, Pullen AM, Fazekas de St Groth B, Mathis D, Benoist C, Davis MM. Antigen/MHC-specific T cells are preferentially exported from the thymus in the presence of their MHC ligand. Cell. 1989; 58:1035-1046
36. Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol. 2009; 182:7459-7472. doi: 10.4049/jimmunol.0900270
37. Han Y, Wu J, Bi L, Xiong S, Gao S, Yin L, Jiang L, Chen C, Yu K, Zhang S. Malignant B cells induce the conversion of CD4+CD25-T cells to regulatory T cells in B-cell non-Hodgkin lymphoma. PloS one. 2011; 6:e28649. doi: 10.1371/journal.pone.0028649
38. Olkhanud PB, Damdinsuren B, Bodogai M, Gress RE, Sen R, Wejksza K, Malchinkhuu E, Wersto RP, Biragyn A. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res. 2011; 71:3505-3515. doi: 10.1158/0008-5472.CAN-10-4316
39. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS, Hollmann TJ, Bruggeman C, Kannan K, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014; 371:2189-2199. doi: 10.1056/NEJMoa1406498
40. Kvistborg P, Philips D, Kelderman S, Hageman L, Ottensmeier C, Joseph-Pietras D, Welters MJ, van der Burg S, Kapiteijn E, Michielin O, Romano E, Linnemann C, Speiser D, et al. Anti-CTLA-4 therapy broadens the melanoma-reactive CD8+ T cell response. Sci Transl Med. 2014; 6:254ra128. doi: 10.1126/scitranslmed.3008918
41. Schenkel JM, Fraser KA, Beura LK, Pauken KE, Vezys V, Masopust D. T cell memory. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science. 2014; 346:98-101. doi: 10.1126/science.1254536
42. Ly LV, Sluijter M, van der Burg SH, Jager MJ, van Hall T. Effective cooperation of monoclonal antibody and peptide vaccine for the treatment of mouse melanoma. J Immunol. 2013; 190:489-496. doi: 10.4049/jimmunol.1200135
43. Hirschhorn-Cymerman D, Budhu S, Kitano S, Liu C, Zhao F, Zhong H, Lesokhin AM, Avogadri-Connors F, Yuan J, Li Y, Houghton AN, Merghoub T, Wolchok JD. Induction of tumoricidal function in CD4+ T cells is associated with concomitant memory and terminally differentiated phenotype. J Exp Med. 2012; 209:2113-2126. doi: 10.1084/jem.20120532
44. Aklilu M, Stadler WM, Markiewicz M, Vogelzang NJ, Mahowald M, Johnson M, Gajewski TF. Depletion of normal B cells with rituximab as an adjunct to IL-2 therapy for renal cell carcinoma and melanoma. Ann Oncol. 2004; 15:1109-1114. doi: 10.1093/annonc/mdh280
45. Barbera-Guillem E, Nelson MB, Barr B, Nyhus JK, May KF, Jr., Feng L, Sampsel JW. B lymphocyte pathology in human colorectal cancer. Experimental and clinical therapeutic effects of partial B cell depletion. Cancer Immunol Immunother. 2000; 48:541-549
46. Tarella C, Passera R, Magni M, Benedetti F, Rossi A, Gueli A, Patti C, Parvis G, Ciceri F, Gallamini A, Cortelazzo S, Zoli V, Corradini P, et al. Risk factors for the development of secondary malignancy after high-dose chemotherapy and autograft, with or without rituximab: a 20-year retrospective follow-up study in patients with lymphoma. J Clin Oncol. 2011; 29:814-824. doi: 10.1200/JCO.2010.28.9777
47. Nelson BH. CD20+ B cells: the other tumor-infiltrating lymphocytes. J Immunol. 2010; 185(9):4977-4982. doi: 10.4049/jimmunol.1001323
48. Shinkai Y, Rathbun G, Lam K-P, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM, Alt FW. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 1992; 68:855-867
49. Spanopoulou E, Roman CAJ, Corcoran LM, Schlissel MS, Silver DP, Nemazee D, Nussenzweig MC, Shinton SA, Hardy RR, Baltimore D. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-deficient mice. Genes Dev. 1994; 8:1030-1042
50. Shklovskaya E, Roediger B, Fazekas de St Groth B. Epidermal and dermal dendritic cells display differential activation and migratory behavior while sharing the ability to stimulate CD4+ T cell proliferation in vivo. J Immunol. 2008; 181:418-430
51. Overwijk WW, Restifo NP. B16 as a mouse model for human melanoma. Curr Protoc Immunol. 2001; Chapter 20:Unit 20 21. doi: 10.1002/0471142735.im2001s39