Abstract
Recent developments in the immuno-oncology field strongly support a role for the immune system in both the prevention and progression of melanoma. Melanoma is a highly immunogenic cancer, including its ability to induce tumour antigen-specific B cell and antibody responses through largely unknown mechanisms. This review considers likely hypothetical mechanisms by which anti-tumour surveillance detects pre-cancerous cells and by which immune (including B cell and antibody) responses may be elicited during malignancy. The review further considers potential pro- and anti-tumour functions of B cells and antibodies (including tertiary lymphoid structures) in both the tumour microenvironment and in circulation. Although the vast majority of studies have focused on T cells, recent evidence highlights the important roles of B cells in response to malignancy. B cells and antibodies are also discussed in the context of their potential utility as clinical biomarkers for various applications (as diagnostic, prognostic, therapeutic efficacy, and toxicity proxies), with a particular focus on protein microarray-based antibody detection and quantitation. Although the role of B cells in melanoma is incompletely understood, the measurement of circulating tumour-specific antibodies represents a promising avenue in the search for melanoma-relevant biomarkers.
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Ahmed R, Gray D (1996) Immunological memory and protective immunity: understanding their relation. Science 272:54–60
Akbani R, Akdemir KC, Aksoy BA, Albert M, Ally A, Amin SB, Arachchi H, Arora A, Auman JT, Ayala B, Baboud J, Balasundaram M, Balu S, Barnabas N, Bartlett J, Bartlett P, Bastian BC, Baylin SB, Behera M, Belyaev D, Benz C, Bernard B, Beroukhim R, Bir N, Black AD, Bodenheimer T, Boice L, Boland GM, Bono R, Bootwalla MS, Bosenberg M, Bowen J, Bowlby R, Bristow CA, Brockway-Lunardi L, Brooks D, Brzezinski J, Bshara W, Buda E, Burns WR, Butterfield YSN, Button M, Calderone T, Cappellini GA, Carter C, Carter SL, Cherney L, Cherniack AD, Chevalier A, Chin L, Cho J, Cho RJ, La Choi Y, Chu A, Chudamani S, Cibulskis K, Ciriello G, Clarke A, Coons S, Cope L, Crain D, Curley E, Danilova L, D’Atri S, Davidsen T, Davies MA, Delman KA, Demchok JA, Deng QA, Deribe YL, Dhalla N, Dhir R, Dicara D, Dinikin M, Dubina M, Ebrom JS, Egea S, Eley G, Engel J, Eschbacher JM, Fedosenko KV, Felau I, Fennell T, Ferguson ML, Fisher S, Flaherty KT, Frazer S, Frick J, Fulidou V, Gabriel SB, Gao J, Gardner J, Garraway LA, Gastier-Foster JM, Gaudioso C, Gehlenborg N, Genovese G, Gerken M, Gershenwald JE, Getz G, Gomez-Fernandez C, Gribbin T, Grimsby J, Gross B, Guin R, Gutschner T, Hadjipanayis A, Halaban R, Hanf B, Haussler D, Haydu LE, Hayes DN, Hayward NK, Heiman DI, Herbert L, Herman JG, Hersey P, Hoadley KA, Hodis E, Holt RA, Hoon DS, Hoppough S, Hoyle AP, Huang FW, Huang M, Huang S, Hutter CM, Ibbs M, Iype L, Jacobsen A, Jakrot V, Janning A, Jeck WR, Jefferys SR, Jensen MA, Jones CD, Jones SJM, Ju Z, Kakavand H, Kang H, Kefford RF, Khuri FR, Kim J, Kirkwood JM, Klode J, Korkut A, Korski K, Krauthammer M, Kucherlapati R, Kwong LN, Kycler W, Ladanyi M, Lai PH, Laird PW, Lander E, Lawrence MS, Lazar AJ, Łaźniak R, Lee D, Lee JE, Lee J, Lee K, Lee S, Lee W, Leporowska E, Leraas KM, Li HI, Lichtenberg TM, Lichtenstein L, Lin P, Ling S, Liu J, Liu O, Liu W, Long GV, Lu Y, Ma S, Ma Y, Mackiewicz A, Mahadeshwar HS, Malke J, Mallery D, Manikhas GM, Mann GJ, Marra MA, Matejka B, Mayo M, Mehrabi S, Meng S, Meyerson M, Mieczkowski PA, Miller JP, Miller ML, Mills GB, Moiseenko F, Moore RA, Morris S, Morrison C, Morton D, Moschos S, Mose LE, Muller FL, Mungall AJ, Murawa D, Murawa P, Murray BA, Nezi L, Ng S, Nicholson D, Noble MS, Osunkoya A, Owonikoko TK, Ozenberger BA, Pagani E, Paklina OV, Pantazi A, Parfenov M, Parfitt J, Park PJ, Park WY, Parker JS, Passarelli F, Penny R, Perou CM, Pihl TD, Potapova O, Prieto VG, Protopopov A, Quinn MJ, Radenbaugh A, Rai K, Ramalingam SS, Raman AT, Ramirez NC, Ramirez R, Rao U, Rathmell WK, Ren X, Reynolds SM, Roach J, Robertson AG, Ross MI, Roszik J, Russo G, Saksena G, Saller C, Samuels Y, Sander C, Sander C, Sandusky G, Santoso N, Saul M, Saw RP, Schadendorf D, Schein JE, Schultz N, Schumacher SE, Schwallier C, Scolyer RA, Seidman J, Sekhar PC, Sekhon HS, Senbabaoglu Y, Seth S, Shannon KF, Sharpe S, Sharpless NE, Shaw KRM, Shelton C, Shelton T, Shen R, Sheth M, Shi Y, Shiau CJ, Shmulevich I, Sica GL, Simons JV, Sinha R, Sipahimalani P, Sofia HJ, Soloway MG, Song X, Sougnez C, Spillane AJ, Spychała A, Stretch JR, Stuart J, Suchorska WM, Sucker A, Sumer SO, Sun Y, Synott M, Tabak B, Tabler TR, Tam A, Tan D, Tang J, Tarnuzzer R, Tarvin K, Tatka H, Taylor BS, Teresiak M, Thiessen N, Thompson JF, Thorne L, Thorsson V, Trent JM, Triche TJ, Tsai KY, Tsou P, Van Den Berg DJ, Van Allen EM, Veluvolu U, Verhaak RG, Voet D, Voronina O, Walter V, Walton JS, Wan Y, Wang Y, Wang Z, Waring S, Watson IR, Weinhold N, Weinstein JN, Weisenberger DJ, White P, Wilkerson MD, Wilmott JS, Wise L, Wiznerowicz M, Woodman SE, Wu CJ, Wu CC, Wu J, Wu Y, Xi R, Xu AW, Yang D, Yang L, Yang L, Zack TI, Zenklusen JC, Zhang H, Zhang J, Zhang W, Zhao X, Zhu J, Zhu K, Zimmer L, Zmuda E, Zou L (2015) Genomic classification of cutaneous melanoma. Cell 161:1681–1696. https://doi.org/10.1016/j.cell.2015.05.044
Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SAJR, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Børresen-Dale AL, Boyault S, Burkhardt B, Butler AP, Caldas C, Davies HR, Desmedt C, Eils R, Eyfjörd JE, Foekens JA, Greaves M, Hosoda F, Hutter B, Ilicic T, Imbeaud S, Imielinsk M, Jäger N, Jones DTW, Jonas D, Knappskog S, Koo M, Lakhani SR, López-Otín C, Martin S, Munshi NC, Nakamura H, Northcott PA, Pajic M, Papaemmanuil E, Paradiso A, Pearson JV, Puente XS, Raine K, Ramakrishna M, Richardson AL, Richter J, Rosenstiel P, Schlesner M, Schumacher TN, Span PN, Teague JW, Totoki Y, Tutt ANJ, Valdés-Mas R, Van Buuren MM, Van’T Veer L, Vincent-Salomon A, Waddell N, Yates LR, Zucman-Rossi J, Andrew Futreal P, McDermott U, Lichter P, Meyerson M, Grimmond SM, Siebert R, Campo E, Shibata T, Pfister SM, Campbell PJ, Stratton MR (2013) Signatures of mutational processes in human cancer. Nature 500:415–421. https://doi.org/10.1038/nature12477
Andrews MC, Woods K, Cebon J, Behren A (2014) Evolving role of tumor antigens for future melanoma therapies. Future Oncol 10:1457–1468. https://doi.org/10.2217/fon.14.84
Avram G, Sánchez-Sendra B, Martín JM, Terrádez L, Ramos D, Monteagudo C (2013) The density and type of MECA-79-positive high endothelial venules correlate with lymphocytic infiltration and tumour regression in primary cutaneous melanoma. Histopathology 63:852–861. https://doi.org/10.1111/his.12235
Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, Eggermont AM, Flaherty KT, Gimotty PA, Kirkwood JM, McMasters KM, Mihm MC, Morton DL, Ross MI, Sober AJ, Sondak VK (2009) Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 27:6199–6206. https://doi.org/10.1200/JCO.2009.23.4799
Barrow C, Browning J, MacGregor D, Davis ID, Sturrock S, Jungbluth AA, Cebon J (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771. https://doi.org/10.1158/1078-0432.CCR-05-1544
Batista FD, Neuberger MS (1998) Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity 8:751–759. https://doi.org/10.1016/S1074-7613(00)80580-4
Batista FD, Iber D, Neuberger MS (2001) B cells acquire antigen from target cells after synapse formation. Nature 411:489–494. https://doi.org/10.1038/35078099
Beeton-Kempen N, Duarte J, Shoko A, Serufuri J-M, John T, Cebon J, Blackburn J (2014) Development of a novel, quantitative protein microarray platform for the multiplexed serological analysis of autoantibodies to cancer–testis antigens. Int J cancer 135:1842–1851. https://doi.org/10.1002/ijc.28832
Belousov PV, Kuprash DV, Sazykin AYu, Khlgatian SV, Penkov DN, Shebzukhov YuV, Nedospasov SA (2008) Cancer-associated antigens and antigen arrays in serological diagnostics of malignant tumors. Biochemistry 73:562–572. https://doi.org/10.1134/S000629790805009X
Berkowska MA, Driessen GJA, Bikos V, Grosserichter-Wagener C, Stamatopoulos K, Cerutti A, He B, Biermann K, Lange JF, van der Burg M, van Dongen JJM, van Zelm MC (2011) Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways. Blood 118:2150–2158. https://doi.org/10.1182/blood-2011-04-345579
Bosisio FM, Wilmott JS, Volders N, Mercier M, Wouters J, Stas M, Blokx WAAA, Massi D, Thompson JF, Scolyer RA, Van Baren N, van den Oord JJ (2016) Plasma cells in primary melanoma. Prognostic significance and possible role of IgA. Mod Pathol 29:347–358. https://doi.org/10.1038/modpathol.2016.28
Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M, Förster R (2000) Follicular B helper T cells express Cxc chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med 192:1545–1552. https://doi.org/10.1084/jem.192.11.1545
Caron M, Choquet-Kastylevsky G, Joubert-Caron R (2007) Cancer immunomics using autoantibody signatures for biomarker discovery. Mol Cell Proteomics 6:1115–1122. https://doi.org/10.1074/mcp.R600016-MCP200
Carragher DM, Rangel-Moreno J, Randall TD (2008) Ectopic lymphoid tissues and local immunity. Semin Immunol 20:26–42. https://doi.org/10.1016/j.smim.2007.12.004
Cerutti A, Rescigno M (2008) The biology of intestinal immunoglobulin A responses. Immunity 28:740–750. https://doi.org/10.1016/j.immuni.2008.05.001
Chan CJ, Smyth MJ, Martinet L (2014) Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ 21:5–14. https://doi.org/10.1038/cdd.2013.26
Chen DS, Mellman I (2017) Elements of cancer immunity and the cancer-immune set point. Nature 541:321–330. https://doi.org/10.1038/nature21349
Chiaruttini G, Mele S, Opzoomer J, Crescioli S, Ilieva KM, Lacy KE, Karagiannis SN (2017) B cells and the humoral response in melanoma: the overlooked players of the tumor microenvironment. Oncoimmunology 6:e1294296. https://doi.org/10.1080/2162402X.2017.1294296
Cipponi A, Mercier M, Seremet T, Baurain J-F, Théate I, van den Oord J, Stas M, Boon T, Coulie PG, van Baren N (2012) Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res 72:3997–4007. https://doi.org/10.1158/0008-5472.CAN-12-1377
Clark WH, Elder DE, Guerry D, Braitman LE, Trock BJ, Schultz D, Synnestvedt M, Halpern AC (1989) Model predicting survival in stage I melanoma based on tumor progression. J Natl Cancer Inst 81:1893–1904. https://doi.org/10.1093/jnci/81.24.1893
Clemente CG, Mihm MC, Bufalino R, Zurrida S, Collini P, Cascinelli N (1996) Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 77:1303–1310. https://doi.org/10.1002/(SICI)1097-0142(19960401)77:7%3C1303::AID-CNCR12%3E3.0.CO;2-5
Colbeck EJ, Ager A, Gallimore A, Jones GW (2017) Tertiary lymphoid structures in cancer: drivers of antitumor immunity, immunosuppression, or Bystander Sentinels in disease? Front Immunol 8:1–18. https://doi.org/10.3389/fimmu.2017.01830
Cyster JG (1999) Chemokines and cell migration in secondary lymphoid organs. Science 286:2098–2102. https://doi.org/10.1126/science.286.5447.2098
Da Gama Duarte J, Parakh S, Andrews MC, Woods K, Pasam A, Tutuka C, Ostrouska S, Blackburn JM, Behren A, Cebon J (2018a) Autoantibodies may predict immune-related toxicity: results from a Phase I study of intralesional Bacillus Calmette–Guérin followed by ipilimumab in patients with advanced metastatic melanoma. Front Immunol 9:411. https://doi.org/10.3389/fimmu.2018.00411
Da Gama Duarte J, Woods K, Andrews MC, Behren A (2018b) The good, the (not so) bad and the ugly of immune homeostasis in melanoma. Immunol Cell Biol. https://doi.org/10.1111/imcb.12001
Das R, Bar N, Ferreira M, Newman AM, Zhang L, Bailur JK, Bacchiocchi A, Kluger H, Wei W, Halaban R, Sznol M, Dhodapkar MV, Dhodapkar KM (2018) Early B cell changes predict autoimmunity following combination immune checkpoint blockade. J Clin Investig 128:2–7. https://doi.org/10.1172/JCI96798
Davis ID, Chen W, Jackson H, Parente P, Shackleton M, Hopkins W, Chen Q, Dimopoulos N, Luke T, Murphy R, Scott AM, Maraskovsky E, McArthur G, MacGregor D, Sturrock S, Tai TY, Green S, Cuthbertson A, Maher D, Miloradovic L, Mitchell SV, Ritter G, Jungbluth AA, Chen Y-T, Gnjatic S, Hoffman EW, Old LJ, Cebon JS (2004) Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc Natl Acad Sci USA 101:10697–10702. https://doi.org/10.1073/pnas.0403572101
De Visser KE, Eichten A, Coussens LM (2006) Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6:24–37. https://doi.org/10.1038/nrc1782
DeFalco J, Harbell M, Manning-Bog A, Baia G, Scholz A, Millare B, Sumi M, Zhang D, Chu F, Dowd C, Zuno-Mitchell P, Kim D, Leung Y, Jiang S, Tang X, Williamson KS, Chen X, Carroll SM, Espiritu Santo G, Haaser N, Nguyen N, Giladi E, Minor D, Tan YC, Sokolove JB, Steinman L, Serafini TA, Cavet G, Greenberg NM, Glanville J, Volkmuth W, Emerling DE, Robinson WH (2017) Non-progressing cancer patients have persistent B cell responses expressing shared antibody paratopes that target public tumor antigens. Clin Immunol 187:37–45. https://doi.org/10.1016/j.clim.2017.10.002
Dieu-Nosjean M-C, Goc J, Giraldo NA, Sautès-Fridman C, Fridman WH (2014) Tertiary lymphoid structures in cancer and beyond. Trends Immunol 35:571–580. https://doi.org/10.1016/j.it.2014.09.006
Dieu-Nosjean MC, Giraldo NA, Kaplon H, Germain C, Fridman WH, Sautès-Fridman C (2016) Tertiary lymphoid structures, drivers of the anti-tumor responses in human cancers. Immunol Rev 271:260–275. https://doi.org/10.1111/imr.12405
DiFronzo LA, Gupta RK, Essner R, Foshag LJ, O’Day SJ, Wanek LA, Stern SL, Morton DL (2002) Enhanced humoral immune response correlates with improved disease-free and overall survival in American Joint Committee on Cancer stage II melanoma patients receiving adjuvant polyvalent vaccine. J Clin Oncol 20:3242–3248. https://doi.org/10.1200/JCO.2002.01.065
Dobbin KK, Cesano A, Alvarez J, Hawtin R, Janetzki S, Kirsch I, Masucci GV, Robbins PB, Selvan SR, Streicher HZ, Zhang J, Butterfield LH, Thurin M (2016) Validation of biomarkers to predict response to immunotherapy in cancer: Volume II—clinical validation and regulatory considerations. J Immunother Cancer 4:77. https://doi.org/10.1186/s40425-016-0179-0
Drayton DL, Liao S, Mounzer RH, Ruddle NH (2006) Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol 7:344–353. https://doi.org/10.1038/ni1330
Duarte JG, Blackburn JM (2017) Advances in the development of human protein microarrays. Expert Rev Proteomics 14:627–641. https://doi.org/10.1080/14789450.2017.1347042
Dunn GP, Old LJ, Schreiber RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21:137–148. https://doi.org/10.1016/j.immuni.2004.07.017
Egbuniwe IU, Karagiannis SN, Nestle FO, Lacy KE (2015) Revisiting the role of B cells in skin immune surveillance. Trends Immunol 36:102–111. https://doi.org/10.1016/j.it.2014.12.006
Elder DE, Rodeck U, Thurin J, Cardillo F, Clark WH, Stewart R, Herlyn M (1989) Antigenic profile of tumor progression stages in human melanocytic nevi and melanomas. Cancer Res 49:5091–5096
Erdag G, Schaefer JT, Smolkin ME, Deacon DH, Shea SM, Dengel LT, Patterson JW, Slingluff CL (2012) Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res 72:1070–1080. https://doi.org/10.1158/0008-5472.CAN-11-3218
Fishman P, Merimski O, Baharav E, Shoenfeld Y (1997) Autoantibodies to tyrosinase. Cancer 79:1461–1464. https://doi.org/10.1002/(SICI)1097-0142(19970415)79:8%3C1461::AID-CNCR3%3E3.0.CO;2-E
Flynn NJ, Somasundaram R, Arnold KM, Sims-Mourtada J (2017) The multifaceted roles of B cells in solid tumors: emerging treatment opportunities. Target Oncol 12:139–152. https://doi.org/10.1007/s11523-017-0481-x
Fremd C, Schuetz F, Sohn C, Beckhove P, Domschke C (2013) B cell-regulated immune responses in tumor models and cancer patients. Oncoimmunology 2:e25443. https://doi.org/10.4161/onci.25443
Garg K, Maurer M, Griss J, Brüggen MC, Wolf IH, Wagner C, Willi N, Mertz KD, Wagner SN (2016) Tumor-associated B cells in cutaneous primary melanoma and improved clinical outcome. Hum Pathol 54:157–164. https://doi.org/10.1016/j.humpath.2016.03.022
Garside P, Ingulli E, Merica RR, Johnson JC, Noelle RJ, Jenkins MK (1998) Visualization of specific B and T lymphocyte interactions in the lymph node. Science 281:96–99. https://doi.org/10.1126/science.281.5373.96
Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, Diehn M, West RB, Plevritis SK, Alizadeh AA (2015) The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med 21:938–945. https://doi.org/10.1038/nm.3909
Germain C, Gnjatic S, Dieu-Nosjean MC (2015) Tertiary lymphoid structure-associated B cells are key players in anti-tumor immunity. Front Immunol 6:1–14. https://doi.org/10.3389/fimmu.2015.00067
Gnjatic S, Wheeler C, Ebner M, Ritter E, Murray A, Altorki NK, Ferrara CA, Hepburne-Scott H, Joyce S, Koopman J, Mcandrew MB, Workman N, Ritter G, Fallon R, Old LJ (2009) Seromic analysis of antibody responses in non-small cell lung cancer patients and healthy donors using conformational protein arrays. J Immunol Methods 341:50–58. https://doi.org/10.1016/j.jim.2008.10.016
Goff SL, Robbins PF, El-Gamil M, Rosenberg S (2009) No correlation between clinical response to CTLA-4 blockade and presence of NY-ESO-1 antibody in patients with metastatic melanoma. J Immunother 32:884–885. https://doi.org/10.1097/CJI.0b013e3181affbf0
Gowen MF, Giles KM, Simpson D, Tchack J, Zhou H, Moran U, Dawood Z, Pavlick AC, Hu S, Wilson MA, Zhong H, Krogsgaard M, Kirchhoff T, Osman I (2018) Baseline antibody profiles predict toxicity in melanoma patients treated with immune checkpoint inhibitors. J Transl Med 16:82. https://doi.org/10.1186/s12967-018-1452-4
Halliley JL, Tipton CM, Liesveld J, Rosenberg AF, Darce J, Gregoretti IV, Popova L, Kaminiski D, Fucile CF, Albizua I, Kyu S, Chiang K-Y, Bradley KT, Burack R, Slifka M, Hammarlund E, Wu H, Zhao L, Walsh EE, Falsey AR, Randall TD, Cheung WC, Sanz I, Lee FE-H (2015) Long-lived plasma cells are contained within the CD19(−)CD38(hi)CD138(+) subset in human bone marrow. Immunity 43:132–145. https://doi.org/10.1016/j.immuni.2015.06.016
Harris DP, Vordermeier HM, Arya A, Bogdan K, Moreno C, Ivanyi J (1996) Immunogenicity of peptides for B cells is not impaired by overlapping T-cell epitope topology. Immunology 88:348–354
Haynes BF, Kelsoe G, Harrison SC, Kepler TB (2012) B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat Biotechnol 30:423–433. https://doi.org/10.1038/nbt.2197
He Y, Qian H, Liu Y, Duan L, Li Y, Shi G (2014) The roles of regulatory B cells in cancer. J Immunol Res. https://doi.org/10.1155/2014/215471
Heesters BA, van der Poel CE, Das A, Carroll MC (2016) Antigen presentation to B cells. Trends Immunol 37:844–854. https://doi.org/10.1016/j.it.2016.10.003
Hiraoka N, Ino Y, Yamazaki-Itoh R (2016) Tertiary lymphoid organs in cancer tissues. Front Immunol. https://doi.org/10.3389/fimmu.2016.00244
Hofmann O, Caballero OL, Stevenson BJ, Chen Y-TY, Cohen T, Chua R, Maher CA, Panji S, Schaefer U, Kruger A, Lehvaslaiho M, Carninci P, Hayashizaki Y, Jongeneel CV, Simpson AJG, Old LJ, Hide W (2008) Genome-wide analysis of cancer/testis gene expression. Proc Natl Acad Sci USA 105:20422–20427. https://doi.org/10.1073/pnas.0810777105
Hoon DS, Yuzuki D, Hayashida M, Morton DL (1995) Melanoma patients immunized with melanoma cell vaccine induce antibody responses to recombinant MAGE-1 antigen. J Immunol 154:730–737
Hou W, Zhang Q, Yan Z, Chen R, Zeh HJ, Kang R, Lotze MT, Tang D (2013) Strange attractors: DAMPs and autophagy link tumor cell death and immunity. Cell Death Dis 4:e966–e910. https://doi.org/10.1038/cddis.2013.493
Houghton AN, Gold JS, Blachere NE (2001) Immunity against cancer: lessons learned from melanoma. Curr Opin Immunol 13:134–140. https://doi.org/10.1016/S0952-7915(00)00195-3
Hsueh EC, Gupta RK, Qi K, Morton DL (1998) Correlation of specific immune responses with survival in melanoma patients with distant metastases receiving polyvalent melanoma cell vaccine. J Clin Oncol 16:2913–2920. https://doi.org/10.1200/JCO.1998.16.9.2913
Huang SKS, Okamoto T, Morton DL, Hoon DSB (1998) Antibody responses to melanoma/melanocyte autoantigens in melanoma patients. J Investig Dermatol 111:662–667. https://doi.org/10.1046/j.1523-1747.1998.00354.x
Hussein MR, Elsers DAH, Fadel SA, Omar AEM (2006) Immunohistological characterisation of tumour infiltrating lymphocytes in melanocytic skin lesions. J Clin Pathol 59:316–324. https://doi.org/10.1136/jcp.2005.028860
Iglesia MD, Vincent BG, Parker JS, Hoadley KA, Carey LA, Perou CM, Serody JS (2014) Prognostic B-cell signatures using mRNA-seq in patients with subtype-specific breast and ovarian cancer. Clin Cancer Res 20:3818–3829. https://doi.org/10.1158/1078-0432.CCR-13-3368
Iglesia MD, Parker JS, Hoadley KA, Serody JS, Perou CM, Vincent BG (2016) Genomic analysis of immune cell infiltrates across 11 tumor types. J Natl Cancer Inst 108:1–11. https://doi.org/10.1093/jnci/djw144
Jäger E, Chen YT, Drijfhout JW, Karbach J, Ringhoffer M, Jäger D, Arand M, Wada H, Noguchi Y, Stockert E, Old LJ, Knuth A (1998) Simultaneous humoral and cellular immune response against cancer–testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med 187:265–270. https://doi.org/10.1084/jem.187.2.265
Jäger E, Stockert E, Zidianakis Z, Chen YT, Karbach J, Jäger D, Arand M, Ritter G, Old LJ, Knuth A (1999) Humoral immune responses of cancer patients against “Cancer-Testis” antigen NY-ESO-1: correlation with clinical events. Int J Cancer 84:506–510
Jäger E, Gnjatic S, Nagata Y, Stockert E, Jäger D, Karbach J, Neumann A, Rieckenberg J, Chen YT, Ritter G, Hoffman E, Arand M, Old LJ, Knuth A (2000a) Induction of primary NY-ESO-1 immunity: CD8+ T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers. Proc Natl Acad Sci USA 97:12198–12203. https://doi.org/10.1073/pnas.220413497
Jäger E, Nagata Y, Gnjatic S, Wada H, Stockert E, Karbach J, Dunbar PR, Lee SY, Jungbluth A, Jäger D, Arand M, Ritter G, Cerundolo V, Dupont B, Chen YT, Old LJ, Knuth A (2000b) Monitoring CD8 T cell responses to NY-ESO-1: correlation of humoral and cellular immune responses. Proc Natl Acad Sci USA 97:4760–4765
Jäger E, Karbach J, Gnjatic S, Neumann A, Bender A, Valmori D, Ayyoub M, Ritter E, Ritter G, Jäger D, Panicali D, Hoffman E, Pan L, Oettgen H, Old LJ, Knuth A (2006) Recombinant vaccinia/fowlpox NY-ESO-1 vaccines induce both humoral and cellular NY-ESO-1-specific immune responses in cancer patients. Proc Natl Acad Sci USA 103:14453–14458. https://doi.org/10.1073/pnas.0606512103
Janssen WJ, Bratton DL, Jakubzick CV, Henson PM (2016) Myeloid cell turnover and clearance. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.MCHD-0005-2015
Karagiannis P, Gilbert AE, Josephs DH, Ali N, Dodev T, Saul L, Correa I, Roberts L, Beddowes E, Koers A, Hobbs C, Ferreira S, Geh JLC, Healy C, Harries M, Acland KM, Blower PJ, Mitchell T, Fear DJ, Spicer JF, Lacy KE, Nestle FO, Karagiannis SN (2013) IgG4 subclass antibodies impair antitumor immunity in melanoma. J Clin Investig 123:1457–1474. https://doi.org/10.1172/JCI65579
Karagiannis P, Villanova F, Josephs DH, Correa I, Van Hemelrijck M, Hobbs C, Saul L, Egbuniwe IU, Tosi I, Ilieva KM, Kent E, Calonje E, Harries M, Fentiman I, Taylor-Papadimitriou J, Burchell J, Spicer JF, Lacy KE, Nestle FO, Karagiannis SN (2015) Elevated IgG4 in patient circulation is associated with the risk of disease progression in melanoma. Oncoimmunology 4:e1032492. https://doi.org/10.1080/2162402X.2015.1032492
Kometani K, Kurosaki T (2015) Differentiation and maintenance of long-lived plasma cells. Curr Opin Immunol 33:64–69. https://doi.org/10.1016/j.coi.2015.01.017
Kumar V, Abbas AK, Aster JC (2015) Robbins and Cotran pathologic basis of disease, 9th edn. Elsevier Saunders, Philadelphia
Kunkel EJ, Butcher EC (2003) Plasma-cell homing. Nat Rev Immunol 3:822–829. https://doi.org/10.1038/nri1203
Kurosaki T, Kometani K, Ise W (2015) Memory B cells. Nat Rev Immunol 15:149–159. https://doi.org/10.1038/nri3802
Ladányi A, Kiss J, Mohos A, Somlai B, Liszkay G, Gilde K, Fejös Z, Gaudi I, Dobos J, Tímár J (2011) Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol Immunother 60:1729–1738. https://doi.org/10.1007/s00262-011-1071-x
Ladányi A, Sebestyén T, Mohos A, Liszkay G, Somlai B, Tóth E, Tímár J (2014) Ectopic lymphoid structures in primary cutaneous melanoma. Pathol Oncol Res 20:981–985. https://doi.org/10.1007/s12253-014-9784-8
Ladd JJ, Chao T, Johnson MM, Qiu J, Chin A, Israel R, Pitteri SJ, Mao J, Wu M, Amon LM, McIntosh M, Li C, Prentice R, Disis N, Hanash S (2013) Autoantibody signatures involving glycolysis and spliceosome proteins precede a diagnosis of breast cancer among postmenopausal women. Cancer Res 73:1502–1513. https://doi.org/10.1158/0008-5472.CAN-12-2560
Lee SK, Rigby RJ, Zotos D, Tsai LM, Kawamoto S, Marshall JL, Ramiscal RR, Chan TD, Gatto D, Brink R, Yu D, Fagarasan S, Tarlinton DM, Cunningham AF, Vinuesa CG (2011) B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J Exp Med 208:1377–1388. https://doi.org/10.1084/jem.20102065
Linnebacher M, Maletzki C (2012) Tumor-infiltrating B cells: the ignored players in tumor immunology. Oncoimmunology 1:1186–1188. https://doi.org/10.4161/onci.20641
Litvak DA, Gupta RK, Yee R, Wanek LA, Ye W, Morton DL (2004) Endogenous immune response to early- and intermediate-stage melanoma is correlated with outcomes and is independent of locoregional relapse and standard prognostic factors. J Am Coll Surg 198:27–35. https://doi.org/10.1016/j.jamcollsurg.2003.08.012
Liudahl SM, Coussens LM (2018) B cells as biomarkers: predicting immune checkpoint therapy adverse events. J Clin Investig 55:199–204. https://doi.org/10.1172/JCI99036
Lo JA, Fisher DE (2014) The melanoma revolution: from UV carcinogenesis to a new era in therapeutics. Science 346:945–949. https://doi.org/10.1126/science.1253735
Lohr M, Edlund K, Botling J, Hammad S, Hellwig B, Othman A, Berglund A, Lambe M, Holmberg L, Ekman S, Bergqvist M, Pontén F, Cadenas C, Marchan R, Hengstler JG, Rahnenführer J, Micke P (2013) The prognostic relevance of tumour-infiltrating plasma cells and immunoglobulin kappa C indicates an important role of the humoral immune response in non-small cell lung cancer. Cancer Lett 333:222–228. https://doi.org/10.1016/j.canlet.2013.01.036
Lu YC, Robbins PF (2016) Cancer immunotherapy targeting neoantigens. Semin Immunol 28:22–27. https://doi.org/10.1016/j.smim.2015.11.002
MacLennan IC (1994) Germinal centers. Annu Rev Immunol 12:117–139. https://doi.org/10.1146/annurev.iy.12.040194.001001
Maecker HT, McCoy JP, Nussenblatt R (2012) Standardizing immunophenotyping for the human immunology project. Nat Rev Immunol 12:191–200. https://doi.org/10.1038/nri3158
Mahmoud SMA, Lee AHS, Paish EC, Macmillan RD, Ellis IO, Green AR (2012) The prognostic significance of B lymphocytes in invasive carcinoma of the breast. Breast Cancer Res Treat 132:545–553. https://doi.org/10.1007/s10549-011-1620-1
Maio M (2012) Melanoma as a model tumour for immuno-oncology. Ann Oncol Off J Eur Soc Med Oncol 23(Suppl 8):viii10-14. https://doi.org/10.1093/annonc/mds257
Maire C, Vercambre-Darras S, Devos P, D’Herbomez M, Dubucquoi S, Mortier L (2013) Metastatic melanoma: spontaneous occurrence of auto antibodies is a good prognosis factor in a prospective cohort. J Eur Acad Dermatol Venereol 27:92–96. https://doi.org/10.1111/j.1468-3083.2011.04364.x
Martin F, Chan AC (2006) B cell immunobiology in disease: evolving concepts from the clinic. Annu Rev Immunol 24:467–496. https://doi.org/10.1146/annurev.immunol.24.021605.090517
Martinet L, Le Guellec S, Filleron T, Lamant L, Meyer N, Rochaix P, Garrido I, Girard J-PP (2012) High endothelial venules (HEVs) in human melanoma lesions: major gateways for tumor-infiltrating lymphocytes. Oncoimmunology 1:829–839. https://doi.org/10.4161/onci.20492
Martinez-Rodriguez M, Thompson AK, Monteagudo C (2014) A significant percentage of CD20-positive TILs correlates with poor prognosis in patients with primary cutaneous malignant melanoma. Histopathology 65:726–728. https://doi.org/10.1111/his.12437
Mascaro JM, Molgo M, Castel T, Castro J (1987) Plasma cells within the infiltrate of primary cutaneous malignant melanoma of the skin. A confirmation of its histoprognostic value. Am J Dermatopathol 9:497–499
Masucci GV, Cesano A, Hawtin R, Janetzki S, Zhang J, Kirsch I, Dobbin KK, Alvarez J, Robbins PB, Selvan SR, Streicher HZ, Butterfield LH, Thurin M (2016) Validation of biomarkers to predict response to immunotherapy in cancer: Volume I—pre-analytical and analytical validation. J Immunother Cancer 4:76. https://doi.org/10.1186/s40425-016-0178-1
Messina JL, Fenstermacher DA, Eschrich S, Qu X, Berglund AE, Lloyd MC, Schell MJ, Sondak VK, Weber JS, Mulé JJ (2012) 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy? Sci Rep 2:1–6. https://doi.org/10.1038/srep00765
Michot JM, Bigenwald C, Champiat S, Collins M, Carbonnel F, Postel-Vinay S, Berdelou A, Varga A, Bahleda R, Hollebecque A, Massard C, Fuerea A, Ribrag V, Gazzah A, Armand JP, Amellal N, Angevin E, Noel N, Boutros C, Mateus C, Robert C, Soria JC, Marabelle A, Lambotte O (2016) Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer 54:139–148. https://doi.org/10.1016/j.ejca.2015.11.016
Mihm MC, Clemente CG, Cascinelli N (1996) Tumor infiltrating lymphocytes in lymph node melanoma metastases: a histopathologic prognostic indicator and an expression of local immune response. Lab Investig 74:43–47
Mukherji B (2013) Immunology of melanoma. Clin Dermatol 31:156–165. https://doi.org/10.1016/j.clindermatol.2012.08.017
Nelson BH (2010) CD20+ B cells: the other tumor-infiltrating lymphocytes. J Immunol 185:4977–4982. https://doi.org/10.4049/jimmunol.1001323
Nielsen JS, Nelson BH (2012) Tumor-infiltrating B cells and T cells. Oncoimmunology 1:1623–1625. https://doi.org/10.4161/onci.21650
Nishimura EK (2011) Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell Melanoma Res 24:401–410. https://doi.org/10.1111/j.1755-148X.2011.00855.x
Nsengimana J, Laye J, Filia A, O’Shea S, Muralidhar S, Poźniak J, Droop A, Chan M, Walker C, Parkinson L, Gascoyne J, Mell T, Polso M, Jewell R, Randerson-Moor J, Cook GP, Bishop DT, Newton-Bishop J (2018) β-Catenin-mediated immune evasion pathway frequently operates in primary cutaneous melanomas. J Clin Investig 128:2048–2063. https://doi.org/10.1172/JCI95351
Pennock ND, White JT, Cross EW, Cheney EE, Tamburini BA, Kedl RM (2013) T cell responses: naive to memory and everything in between. AJP Adv Physiol Educ 37:273–283. https://doi.org/10.1152/advan.00066.2013
Punt CJA, Barbuto JAM, Zhang H, Grimes WJ, Hatch KD, Hersh EM (1994) Anti-tumor antibody produced by human tumor-infiltrating and peripheral blood B lymphocytes. Cancer Immunol Immunother 38:225–232. https://doi.org/10.1007/BF01533513
Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, Kammula US, Hughes MS, Restifo NP, Raffeld M, Lee CCR, Levy CL, Li YF, El-Gamil M, Schwarz SL, Laurencot C, Rosenberg SA (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29:917–924. https://doi.org/10.1200/JCO.2010.32.2537
Rodrigues M (2017) Skin cancer risk (nonmelanoma skin cancers/melanoma) in vitiligo patients. Dermatol Clin 35:129–134. https://doi.org/10.1016/j.det.2016.11.003
Roth K, Oehme L, Zehentmeier S, Zhang Y, Niesner R, Hauser AE (2014) Tracking plasma cell differentiation and survival. Cytometry A 85:15–24. https://doi.org/10.1002/cyto.a.22355
Ruprecht CR, Lanzavecchia A (2006) Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 36:810–816. https://doi.org/10.1002/eji.200535744
Saul L, Ilieva KM, Bax HJ, Karagiannis P, Correa I, Rodriguez-Hernandez I, Josephs DH, Tosi I, Egbuniwe IU, Lombardi S, Crescioli S, Hobbs C, Villanova F, Cheung A, Geh JLC, Healy C, Harries M, Sanz-Moreno V, Fear DJ, Spicer JF, Lacy KE, Nestle FO, Karagiannis SN (2016) IgG subclass switching and clonal expansion in cutaneous melanoma and normal skin. Sci Rep 6:1–12. https://doi.org/10.1038/srep29736
Sautès-Fridman C, Lawand M, Giraldo NA, Kaplon H, Germain C, Fridman WH, Dieu-Nosjean M-C (2016) Tertiary lymphoid structures in cancers: prognostic value, regulation, and manipulation for therapeutic intervention. Front Immunol 7:407. https://doi.org/10.3389/fimmu.2016.00407
Scanlan MJ, Gure AO, Jungbluth AA, Old LJ, Chen Y (2002) Cancer/testis antigens: an expanding family of targets for cancer immunotherapy. Immunol Rev 188:22–32
Scanlan MJ, Simpson AJG, Old LJ (2004) The cancer/testis genes: review, standardization, and commentary. Cancer Immun 4:1–15
Schadendorf D, Fisher DE, Garbe C, Gershenwald JE, Grob J-J, Halpern A, Herlyn M, Marchetti M, McArthur G, Ribas A, Roesch A, Hauschild A (2015) Melanoma. Nat Rev Dis Primer. https://doi.org/10.1038/nrdp.2015.3
Schmidt M, Böhm D, Von Törne C, Steiner E, Puhl A, Pilch H, Lehr HA, Hengstler JG, Kölbl H, Gehrmann M (2008) The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res 68:5405–5413. https://doi.org/10.1158/0008-5472.CAN-07-5206
Schumacher TN, Schreiber RD (2015) Realising the Promise: neoantigens in cancer immunotherapy. Science. https://doi.org/10.1126/science.aaa4971
Sebestyén T, Mohos A, Liszkay G, Somlai B, Gaudi I, Ladányi A (2018) Correlation with lymphocyte infiltration, but lack of prognostic significance of MECA-79-positive high endothelial venules in primary malignant melanoma. Melanoma Res. https://doi.org/10.1097/CMR.0000000000000457
Sharon J, Rynkiewicz MJ, Lu Z, Yang C-Y (2014) Discovery of protective B-cell epitopes for development of antimicrobial vaccines and antibody therapeutics. Immunology 142:1–23. https://doi.org/10.1111/imm.12213
Simpson AJG, Caballero OL, Jungbluth A, Chen Y-T, Old LJ (2005) Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 5:615–625. https://doi.org/10.1038/nrc1669
Spaner D, Bahlo A (2011) B lymphocytes in cancer immunology. In: Medin J, Fowler D (eds) Experimental and applied immunotherapy. Springer, New York, p 37–57
Stockert E, Jäger E, Chen YT, Scanlan MJ, Gout I, Karbach J, Arand M, Knuth A, Old LJ (1998) A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J Exp Med 187:1349–1354
Stowman AM, Hickman AW, Mauldin IS, Mahmutovic A, Gru AA, Slingluff CL (2018) Lymphoid aggregates in desmoplastic melanoma have features of tertiary lymphoid structures. Melanoma Res. https://doi.org/10.1097/CMR.0000000000000439
Svobodová S, Browning J, MacGregor D, Pollara G, Scolyer RA, Murali R, Thompson JF, Deb S, Azad A, Davis ID, Cebon JS (2011) Cancer–testis antigen expression in primary cutaneous melanoma has independent prognostic value comparable to that of Breslow thickness, ulceration and mitotic rate. Eur J Cancer 47:460–469. https://doi.org/10.1016/j.ejca.2010.09.042
Swann JB, Smyth MJ (2007) Immune surveillance of tumors. J Clin Investig 117:1137–1146. https://doi.org/10.1172/JCI31405
Tan EM (2001) Autoantibodies as reporters identifying aberrant cellular mechanisms in tumorigenesis. J Clin Investig 108:1411–1415. https://doi.org/10.1172/JCI200114451
Tan HT, Low J, Lim SG, Chung MCM (2009) Serum autoantibodies as biomarkers for early cancer detection. FEBS J 276:6880–6904. https://doi.org/10.1111/j.1742-4658.2009.07396.x
Tefany FJ, Barnetson RS, Halliday GM, McCarthy SW, McCarthy WH (1991) Immunocytochemical analysis of the cellular infiltrate in primary regressing and non-regressing malignant melanoma. J Investig Dermatol 97:197–202
Teillaud JL, Dieu-Nosjean MC (2017) Tertiary lymphoid structures: an anti-tumor school for adaptive immune cells and an antibody factory to fight cancer? Front Immunol 8:1–6. https://doi.org/10.3389/fimmu.2017.00830
Teulings HE, Limpens J, Jansen SN, Zwinderman AH, Reitsma JB, Spuls PI, Luiten RM (2015) Vitiligo-like depigmentation in patients with stage III–IV melanoma receiving immunotherapy and its association with survival: a systematic review and meta-analysis. J Clin Oncol 33:773–781. https://doi.org/10.1200/JCO.2014.57.4756
Triozzi PL, Aldrich W, Crabb JW, Singh AD (2015) Spontaneous cellular and humoral tumor antigen responses in patients with uveal melanoma. Melanoma Res 25:510–518. https://doi.org/10.1097/CMR.0000000000000207
Tsou P, Katayama H, Ostrin EJ, Hanash SM (2016) The emerging role of B cells in tumor immunity. Cancer Res 76:5591–5601. https://doi.org/10.1158/0008-5472.CAN-16-0431
Valmori D, Souleimanian NE, Tosello V, Bhardwaj N, Adams S, O’Neill D, Pavlick A, Escalon JB, Cruz CM, Angiulli A, Angiulli F, Mears G, Vogel SM, Pan L, Jungbluth AA, Hoffmann EW, Venhaus R, Ritter G, Old LJ, Ayyoub M (2007) Vaccination with NY-ESO-1 protein and CpG in Montanide induces integrated antibody/Th1 responses and CD8 T cells through cross-priming. Proc Natl Acad Sci USA 104:8947–8952. https://doi.org/10.1073/pnas.0703395104
Vanderleyden I, Linterman MA, Smith KGC (2014) Regulatory T cells and control of the germinal centre response. Arthritis Res Ther 16:1–9. https://doi.org/10.1186/s13075-014-0471-7
Vigneron N (2015) Human tumor antigens and cancer immunotherapy. Biomed Res Int 2015:1–17. https://doi.org/10.1155/2015/948501
Vigneron N, Stroobant V, Van den Eynde BJ, van der Bruggen P (2013) Database of T cell-defined human tumor antigens: the 2013 update. Cancer Immun 13:15
Vujanovic L, Butterfield LH (2007) Melanoma cancer vaccines and anti-tumor T cell responses. J Cell Biochem 102:301–310. https://doi.org/10.1002/jcb.21473
Weber JS, Hamid O, Chasalow SD, Wu DY, Parker SM, Galbraith S, Gnjatic S, Berman D (2012) Ipilimumab increases activated T cells and enhances humoral immunity in patients with advanced melanoma. J Immunother 35:89–97. https://doi.org/10.1097/CJI.0b013e31823aa41c
Weill J-C, Weller S, Reynaud C-A (2009) Human marginal zone B cells. Annu Rev Immunol 27:267–285. https://doi.org/10.1146/annurev.immunol.021908.132607
Weissmann A, Roses DF, Harris MN, Dubin N (1984) Prediction of lymph node metastases from the histologic features of primary cutaneous malignant melanomas. Am J Dermatopathol 6(Suppl):35–41
Wieczorek M, Abualrous ET, Sticht J, Álvaro-Benito M, Stolzenberg S, Noé F, Freund C (2017) Major histocompatibility complex (MHC) class I and MHC class II proteins: conformational plasticity in antigen presentation. Front Immunol 8:1–16. https://doi.org/10.3389/fimmu.2017.00292
Yuan J, Gnjatic S, Li H, Powel S, Gallardo HF, Ritter E, Ku GY, Jungbluth AA, Segal NH, Rasalan TS, Manukian G, Xu Y, Roman R-A, Terzulli SL, Heywood M, Pogoriler E, Ritter G, Old LJ, Allison JP, Wolchok JD (2008) CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit. Proc Natl Acad Sci USA 105:20410–20415. https://doi.org/10.1073/pnas.0810114105
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, Halaban R, Jungbluth AA, Allison JP, Old LJ, Wolchok JD, Gnjatic S (2011) Integrated NY-ESO-1 antibody and CD8+ T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab. Proc Natl Acad Sci USA 108:16723–16728. https://doi.org/10.1073/pnas.1110814108
Yuan J, Hegde PS, Clynes R, Foukas PG, Harari A, Kleen TO, Kvistborg P, Maccalli C, Maecker HT, Page DB, Robins H, Song W, Stack EC, Wang E, Whiteside TL, Zhao Y, Zwierzina H, Butterfield LH, Fox BA (2016) Novel technologies and emerging biomarkers for personalized cancer immunotherapy. J Immunother Cancer 4:3. https://doi.org/10.1186/s40425-016-0107-3
Yuen GJ, Demissie E, Pillai S (2016) B lymphocytes and cancer: a love–hate relationship. Trends Cancer 2:747–757. https://doi.org/10.1016/j.trecan.2016.10.010
Zaenker P, Gray ES, Ziman MR (2016) Autoantibody production in cancer—the humoral immune response toward autologous antigens in cancer patients. Autoimmun Rev 15:477–483. https://doi.org/10.1016/j.autrev.2016.01.017
Zhang Y, Gallastegui N, Rosenblatt JD (2015) Regulatory B cells in anti-tumor immunity. Int Immunol 27:521–530. https://doi.org/10.1093/intimm/dxv034
Zörnig 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, Eichmüller SB, Jäger D (2015) Prognostic significance of spontaneous antibody responses against tumor-associated antigens in malignant melanoma patients. Int J Cancer 136:138–151. https://doi.org/10.1002/ijc.28980
Zhang Y, Schreiber TH, Rosenblatt JD (2014) The role of B cells in shaping the antitumor immune response. In: Current cancer research. Humana Press, Inc., New York, p 19–35
Acknowledgements
JDGD is supported by a Tour de Cure Scott Canner Young Research Grant. JMP is supported by the National Health Scholars Programme administered by the South African Medical Research Council. JMB is supported by a South African National Research Foundation Research Chair Grant (#64760). The Olivia Newton-John Cancer Research Institute acknowledges the support of the Victorian Government Operational Infrastructure Support Program.
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Da Gama Duarte, J., Peyper, J.M. & Blackburn, J.M. B cells and antibody production in melanoma. Mamm Genome 29, 790–805 (2018). https://doi.org/10.1007/s00335-018-9778-z
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DOI: https://doi.org/10.1007/s00335-018-9778-z