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Original Research

HLA class I-restricted MYD88 L265P-derived peptides as specific targets for lymphoma immunotherapy

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Article: e1219825 | Received 01 Apr 2016, Accepted 28 Jul 2016, Published online: 03 Mar 2017

References

  • Boon T, Cerottini J-C, Van den Eynde B, van der Bruggen P, Van Pel A. Tumor antigens recognized by T lymphocytes. Annu Rev Immunol 1994; 12:337-65; PMID:8011285; http://dx.doi.org/10.1146/annurev.iy.12.040194.002005
  • Ostrand-Rosenberg S. Tumor immunotherapy: the tumor cell as an antigen-presenting cell. Curr Opin Immunol 1994; 6:722-7; PMID:7826527; http://dx.doi.org/10.1016/0952-7915(94)90075-2
  • Townsend SE, Allison JP. Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science 1993; 259:368-70; PMID:7678351; http://dx.doi.org/10.1126/science.7678351
  • Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, Staehler M, Brugger W, Dietrich PY, Mendrzyk R et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 2012; 18:1254-61; PMID:22842478; http://dx.doi.org/10.1038/nm.2883
  • Perez-Gracia JL, Labiano S, Rodriguez-Ruiz ME, Sanmamed MF, Melero I. Orchestrating immune check-point blockade for cancer immunotherapy in combinations. Curr Opin Immunol 2014; 27:89-97; PMID:24485523; http://dx.doi.org/10.1016/j.coi.2014.01.002
  • Ansell SM. Targeting immune checkpoints in lymphoma. Curr Opin Hematol 2015; 22:337-42; PMID:26049755; http://dx.doi.org/10.1097/MOH.0000000000000158
  • Coulie PG, Lehmann F, Lethe B, Herman J, Lurquin C, Andrawiss M, Boon T. A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma. Proc Natl Acad Sci U S A 1995; 92:7976-80; PMID:7644523; http://dx.doi.org/10.1073/pnas.92.17.7976
  • van Rooij N, van Buuren MM, Philips D, Velds A, Toebes M, Heemskerk B, van Dijk LJ, Behjati S, Hilkmann H, El Atmioui D et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J Clin Oncol 2013; 31:e439-42; PMID:24043743; http://dx.doi.org/10.1200/JCO.2012.47.7521
  • Treon SP, Xu L, Yang G, Zhou Y, Liu X, Cao Y, Sheehy P, Manning RJ, Patterson CJ, Tripsas C et al. MYD88 L265P somatic mutation in Waldenstrom's macroglobulinemia. N Engl J Med 2012; 367:826-33; PMID:22931316; http://dx.doi.org/10.1056/NEJMoa1200710
  • Varettoni M, Arcaini L, Zibellini S, Boveri E, Rattotti S, Riboni R, Corso A, Orlandi E, Bonfichi M, Gotti M et al. Prevalence and clinical significance of the MYD88 (L265P) somatic mutation in Waldenstrom's macroglobulinemia and related lymphoid neoplasms. Blood 2013; 121:2522-8; PMID:23355535; http://dx.doi.org/10.1182/blood-2012-09-457101
  • Xu L, Hunter ZR, Yang G, Zhou Y, Cao Y, Liu X, Morra E, Trojani A, Greco A, Arcaini L et al. MYD88 L265P in Waldenstrom macroglobulinemia, immunoglobulin M monoclonal gammopathy, and other B-cell lymphoproliferative disorders using conventional and quantitative allele-specific polymerase chain reaction. Blood 2013; 121:2051-8; PMID:23321251; http://dx.doi.org/10.1182/blood-2012-09-454355
  • Ngo VN, Young RM, Schmitz R, Jhavar S, Xiao W, Lim KH, Kohlhammer H, Xu W, Yang Y, Zhao H et al. Oncogenically active MYD88 mutations in human lymphoma. Nature 2011; 470:115-9; PMID:21179087; http://dx.doi.org/10.1038/nature09671
  • Pasqualucci L, Trifonov V, Fabbri G, Ma J, Rossi D, Chiarenza A, Wells VA, Grunn A, Messina M, Elliot O et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet 2011; 43:830-7; PMID:21804550; http://dx.doi.org/10.1038/ng.892
  • Puente XS, Pinyol M, Quesada V, Conde L, Ordonez GR, Villamor N, Escaramis G, Jares P, Bea S, Gonzalez-Diaz M et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature 2011; 475:101-5; PMID:21642962; http://dx.doi.org/10.1038/nature10113
  • Landau DA, Carter SL, Stojanov P, McKenna A, Stevenson K, Lawrence MS, Sougnez C, Stewart C, Sivachenko A, Wang L et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 2013; 152:714-26; PMID:23415222; http://dx.doi.org/10.1016/j.cell.2013.01.019
  • Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. GLOBOCAN 2012 v1.0. Cancer Incidence and Mortality Worldwide: IARC CancerBase No 11, 2013:International Agency for Research on Cancer.
  • Lenz G, Wright G, Dave SS, Xiao W, Powell J, Zhao H, Xu W, Tan B, Goldschmidt N, Iqbal J et al. Stromal gene signatures in large-B-cell lymphomas. N Engl J Med 2008; 359:2313-23; PMID:19038878; http://dx.doi.org/10.1056/NEJMoa0802885
  • Tsimberidou A-M, Keating MJ. Treatment of patients with fludarabine-refractory chronic lymphocytic leukemia: need for new treatment options. Leuk Lymphoma 2010; 51:1188-99; PMID:20545582; http://dx.doi.org/10.3109/10428194.2010.486089
  • Schmitt M, Schmitt A, Rojewski MT, Chen J, Giannopoulos K, Fei F, Yu Y, Gotz M, Heyduk M, Ritter G et al. RHAMM-R3 peptide vaccination in patients with acute myeloid leukemia, myelodysplastic syndrome, and multiple myeloma elicits immunologic and clinical responses. Blood 2008; 111:1357-65; PMID:17978170; http://dx.doi.org/10.1182/blood-2007-07-099366
  • Porter DL, Levine BL, Bunin N, Stadtmauer EA, Luger SM, Goldstein S, Loren A, Phillips J, Nasta S, Perl A et al. A phase 1 trial of donor lymphocyte infusions expanded and activated ex vivo via CD3/CD28 costimulation. Blood 2006; 107:1325-31; PMID:16269610; http://dx.doi.org/10.1182/blood-2005-08-3373
  • Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011; 17:4550-7; PMID:21498393; http://dx.doi.org/10.1158/1078-0432.CCR-11-0116
  • Timmerman JM, Czerwinski DK, Davis TA, Hsu FJ, Benike C, Hao ZM, Taidi B, Rajapaksa R, Caspar CB, Okada CY. Idiotype-pulsed dendritic cell vaccination for B-cell lymphoma: clinical and immune responses in 35 patients. Blood 2002; 99:1517-26; PMID:11861263; http://dx.doi.org/10.1182/blood.V99.5.1517
  • Park HJ, Neelapu SS. Developing idiotype vaccines for lymphoma: from preclinical studies to phase III clinical trials. Brit J Haematol 2008; 142:179-91; PMID:18422783; http://dx.doi.org/10.1111/j.1365-2141.2008.07143.x
  • Wilson WH, Young RM, Schmitz R, Yang Y, Pittaluga S, Wright G, Lih C-J, Williams PM, Shaffer AL, Gerecitano J. Targeting B cell receptor signaling with ibrutinib in diffuse large B cell lymphoma. Nat Med 2015; 21:922-6; PMID:26193343; http://dx.doi.org/10.1038/nm.3884
  • Lundegaard C, Lamberth K, Harndahl M, Buus S, Lund O, Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8–11. Nucleic Acids Research 2008; 36:W509-W12; PMID:18463140; http://dx.doi.org/10.1093/nar/gkn202
  • Lundegaard C, Lund O, Nielsen M. Accurate approximation method for prediction of class I MHC affinities for peptides of length 8, 10 and 11 using prediction tools trained on 9mers. Bioinformatics 2008; 24:1397-8; PMID:18413329; http://dx.doi.org/10.1093/bioinformatics/btn128
  • Nielsen M, Lundegaard C, Worning P, Hvid CS, Lamberth K, Buus S, Brunak S, Lund O. Improved prediction of MHC class I and class II epitopes using a novel Gibbs sampling approach. Bioinformatics 2004; 20:1388-97; PMID:14962912; http://dx.doi.org/10.1093/bioinformatics/bth100
  • Nielsen M, Lundegaard C, Worning P, Lauemoller SL, Lamberth K, Buus S, Brunak S, Lund O. Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci 2003; 12:1007-17; PMID:12717023; http://dx.doi.org/10.1110/ps.0239403
  • Schuler MM, Nastke MD, Stevanovikc S. SYFPEITHI: database for searching and T-cell epitope prediction. Methods Mol Biol 2007; 409:75-93; PMID:18449993; http://dx.doi.org/10.1007/978-1-60327-118-9_5
  • Duan F, Duitama J, Al Seesi S, Ayres CM, Corcelli SA, Pawashe AP, Blanchard T, McMahon D, Sidney J, Sette A et al. Genomic and bioinformatic profiling of mutational neoepitopes reveals new rules to predict anticancer immunogenicity. J Exp Med 2014; 211:2231-48; PMID:25245761; http://dx.doi.org/10.1084/jem.20141308
  • Peper JK, Bösmüller H-C, Schuster H, Gückel B, Hörzer H, Roehle K, Schäfer R, Wagner P, Rammensee H-G, Stevanović S et al. HLA ligandomics identifies Histone Deacetylase 1 as target for Ovarian Cancer immunotherapy. OncoImmunology 2016; 5(5):e1065369; PMID:27467910; http://dx.doi.org/10.1080/2162402X.2015.1065369
  • Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-33; PMID:23724867; http://dx.doi.org/10.1056/NEJMoa1302369
  • Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
  • Robert C, Ribas A, Wolchok JD, Hodi FS, Hamid O, Kefford R, Weber JS, Joshua AM, Hwu WJ, Gangadhar TC et al. Anti-programmed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet 2014; 384:1109-17; PMID:25034862; http://dx.doi.org/10.1016/S0140-6736(14)60958-2
  • Lynch TJ, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, Sebastian M, Neal J, Lu H, Cuillerot JM et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol 2012; 30:2046-54; PMID:22547592; http://dx.doi.org/10.1200/JCO.2011.38.4032
  • Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, Schuster SJ, Millenson MM, Cattry D, Freeman GJ et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med 2015; 372:311-9; PMID:25482239; http://dx.doi.org/10.1056/NEJMoa1411087
  • Martin P, Furman RR, Rutherford S, Ruan J, Ely S, Greenberg J, Coleman M, Goldsmith SJ, Leonard JP. Phase I study of the anti-CD74 monoclonal antibody milatuzumab (hLL1) in patients with previously treated B-cell lymphomas. Leuk Lymphoma 2015; 56(11):3065-70; PMID:25754579; http://dx.doi.org/10.3109/10428194.2015.1028052
  • Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014; 371:2189-99; PMID:25409260; http://dx.doi.org/10.1056/NEJMoa1406498
  • Brossart P, Schneider A, Dill P, Schammann T, Grunebach F, Wirths S, Kanz L, Buhring HJ, Brugger W. The epithelial tumor antigen MUC1 is expressed in hematological malignancies and is recognized by MUC1-specific cytotoxic T-lymphocytes. Cancer Res 2001; 61:6846-50; PMID:11559560.
  • Walz S, Stickel J, Kowalewski DJ, Schuster H, Weisel K, Backert L, Kahn S, Nelde A, Stroh T, Handel M et al. The antigenic landscape of multiple myeloma: mass spectrometry (re-)defines targets for T-cell based immunotherapy. Blood 2015; 126(10):1203-13; PMID:26138685; http://dx.doi.org/10.1182/blood-2015-04-640532
  • Berlin C, Kowalewski DJ, Schuster H, Mirza N, Walz S, Handel M, Schmid-Horch B, Salih HR, Kanz L, Rammensee HG et al. Mapping the HLA ligandome landscape of acute myeloid leukemia: a targeted approach toward peptide-based immunotherapy. Leukemia 2015; 29, 647-59; PMID:25092142; http://dx.doi.org/10.1038/leu.2014.233
  • Greiner J, Ono Y, Hofmann S, Schmitt A, Mehring E, Gotz M, Guillaume P, Dohner K, Mytilineos J, Dohner H et al. Mutated regions of nucleophosmin 1 elicit both CD4(+) and CD8(+) T-cell responses in patients with acute myeloid leukemia. Blood 2012; 120:1282-9; PMID:22592607; http://dx.doi.org/10.1182/blood-2011-11-394395
  • Greiner J, Schneider V, Schmitt M, Götz M, Döhner K, Wiesneth M, Döhner H, Hofmann S. Immune responses against the mutated region of cytoplasmatic NPM1 might contribute to the favorable clinical outcome of AML patients with NPM1 mutations (NPM1mut). Blood 2013; 122:1087-8; PMID:23929838; http://dx.doi.org/10.1182/blood-2013-04-496844
  • Martinez-Trillos A, Pinyol M, Navarro A, Aymerich M, Jares P, Juan M, Rozman M, Colomer D, Delgado J, Gine E et al. Mutations in TLR/MYD88 pathway identify a subset of young chronic lymphocytic leukemia patients with favorable outcome. Blood 2014; 123:3790-6; PMID:24782504; http://dx.doi.org/10.1182/blood-2013-12-543306
  • Stanke J, Hoffmann C, Erben U, von Keyserling H, Stevanovic S, Cichon G, Schneider A, Kaufmann AM. A flow cytometry-based assay to assess minute frequencies of CD8+ T cells by their cytolytic function. J Immunological Methods 2010; 360:56-65; PMID:20558172; http://dx.doi.org/10.1016/j.jim.2010.06.005
  • Andersen MH, Reker S, Kvistborg P, Becker JC, Straten Pt. Spontaneous Immunity against Bcl-xL in Cancer Patients. J Immunol 2005; 175:2709-14; PMID:16081848; http://dx.doi.org/10.4049/jimmunol.175.4.2709
  • Avbelj M, Wolz O-O, Fekonja O, Benčina M, Repič M, Mavri J, Krüger J, Schärfe C, Garcia MD, Panter G. Activation of lymphoma-associated MyD88 mutations via allostery-induced TIR-domain oligomerization. Blood 2014; 124:3896-904; PMID:25359991; http://dx.doi.org/10.1182/blood-2014-05-573188
  • Ansell S, Hodge L, Secreto F, Manske M, Braggio E, Price-Troska T, Ziesmer S, Li Y, Johnson S, Hart S. Activation of TAK1 by MYD88 L265P drives malignant B-cell Growth in non-Hodgkin lymphoma. Blood Cancer J 2014; 4:e183; PMID:24531446; http://dx.doi.org/10.1038/bcj.2014.4
  • Rittig SM, Haentschel M, Weimer KJ, Heine A, Muller MR, Brugger W, Horger MS, Maksimovic O, Stenzl A, Hoerr I. Intradermal Vaccinations With RNA Coding for TAA Generate CD8+ and CD4+ Immune Responses and Induce Clinical Benefit in Vaccinated Patients. Molecular Therapy 2011; 19:990-9; PMID:21189474; http://dx.doi.org/10.1038/mt.2010.289
  • Rapoport AP, Stadtmauer EA, Binder-Scholl GK, Goloubeva O, Vogl DT, Lacey SF, Badros AZ, Garfall A, Weiss B, Finklestein J et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat Med 2015; 21:914-21; PMID:26193344; http://dx.doi.org/10.1038/nm.3910
  • Bonzheim I, Giese S, Deuter C, Süsskind D, Zierhut M, Waizel M, Szurman P, Federmann B, Schmidt J, Quintanilla-Martinez L et al. High frequency of MYD88 mutations in vitreoretinal B-cell lymphoma: a valuable tool to improve diagnostic yield of vitreous aspirates. Blood 2015; 126:76-9; PMID:25900979; http://dx.doi.org/10.1182/blood-2015-01-620518
  • Schmidt J, Federmann B, Schindler N, Steinhilber J, Bonzheim I, Fend F, Quintanilla-Martinez L. MYD88 L265P and CXCR4 mutations in lymphoplasmacytic lymphoma identify cases with high disease activity. Brit J Haematol 2015; 169:795-803; PMID:25819228; http://dx.doi.org/10.1111/bjh.13361
  • Lundegaard C, Lamberth K, Harndahl M, Buus S, Lund O, Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8–11. Nucleic Acids Res 2008; 1;36:W509-12; PMID:18463140; http://dx.doi.org/10.1093/nar/gkn202
  • Merrifield B. Solid phase synthesis. Science 1986; 232:341-7; PMID:3961484; http://dx.doi.org/10.1126/science.3961484
  • Atherton E, Fox H, Harkiss D, Logan C, Sheppard R, Williams B. A mild procedure for solid phase peptide synthesis: use of fluorenylmethoxycarbonylamino-acids. J Chem Soc Chem Commun 1978; 13:537-9; http://dx.doi.org/10.1039/c39780000537
  • Garboczi DN, Hung DT, Wiley DC. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc Natl Acad Sci U S A 1992; 89:3429-33; PMID:1565634; http://dx.doi.org/10.1073/pnas.89.8.3429
  • Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, Bell JI, McMichael AJ, Davis MM. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996; 274:94-6; PMID:8810254; http://dx.doi.org/10.1126/science.274.5284.94
  • Kowalewski DJ, Schuster H, Backert L, Berlin C, Kahn S, Kanz L, Salih HR, Rammensee HG, Stevanovic S, Stickel JS. HLA ligandome analysis identifies the underlying specificities of spontaneous antileukemia immune responses in chronic lymphocytic leukemia (CLL). Proc Natl Acad Sci U S A 2015; 112.2:E166-E75; PMID:25548167; http://dx.doi.org/10.1073/pnas.1416389112
  • Widenmeyer M, Griesemann H, Stevanovic S, Feyerabend S, Klein R, Attig S, Hennenlotter J, Wernet D, Kuprash DV, Sazykin AY et al. Promiscuous survivin peptide induces robust CD4+ T-cell responses in the majority of vaccinated cancer patients. Int J Cancer 2012; 131:140-9; PMID:21858810; http://dx.doi.org/10.1002/ijc.26365
  • Britten CM, Gouttefangeas C, Welters MJ, Pawelec G, Koch S, Ottensmeier C, Mander A, Walter S, Paschen A, Muller-Berghaus J et al. The CIMT-monitoring panel: a two-step approach to harmonize the enumeration of antigen-specific CD8+ T lymphocytes by structural and functional assays. Cancer Immunol Immunother 2008; 57:289-302; PMID:17721783; http://dx.doi.org/10.1007/s00262-007-0378-0
  • Rudolf D, Silberzahn T, Walter S, Maurer D, Engelhard J, Wernet D, Buhring HJ, Jung G, Kwon BS, Rammensee HG et al. Potent costimulation of human CD8 T cells by anti-4-1BB and anti-CD28 on synthetic artificial antigen presenting cells. Cancer Immunol Immunother 2008; 57:175-83; PMID:17657490; http://dx.doi.org/10.1007/s00262-007-0360-x
  • Neumann A, Horzer H, Hillen N, Klingel K, Schmid-Horch B, Buhring HJ, Rammensee HG, Aebert H, Stevanovic S. Identification of HLA ligands and T-cell epitopes for immunotherapy of lung cancer. Cancer Immunol Immunother 2013; 62:1485-97; PMID:23817722; http://dx.doi.org/10.1007/s00262-013-1454-2
  • Hermans IF, Silk JD, Yang J, Palmowski MJ, Gileadi U, McCarthy C, Salio M, Ronchese F, Cerundolo V. The VITAL assay: a versatile fluorometric technique for assessing CTL- and NKT-mediated cytotoxicity against multiple targets in vitro and in vivo. J Immunol Methods 2004; 285:25-40; PMID:14871532; http://dx.doi.org/10.1016/j.jim.2003.10.017