CD20 alternative splicing isoform generates immunogenic CD4 helper T epitopes

International Journal of Cancer

Volumn 137, Issue 1, 2015, Pages 116-126

  Vauchy, Charline ^a,b,c   Gamonet, Clementine ^a,b,c   Ferrand, Christophe ^a,b,c   Daguindau, Etienne ^d   Galaine, Jeanne ^a,b,c   Beziaud, Laurent ^a,b,c   Chauchet, Adrien ^d   Henry Dunand, Carole J ^e   Deschamps, Marina ^a,b,c   Rohrlich, Pierre Simon ^a,b,d   Borg, Christophe ^a,b,c,d   Adotevi, Olivier ^a,b,c,d   Godet, Yann ^a,b,c  

^a RIGHT Interactions Hôte Greffon Tumeur Ingénierie Cellulaire et Génique   (France)

^b UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^c ETABLISSEMENT FRANÇAIS DU SANG   (France)

^d UNIVERSITY HOSPITAL OF BESANÇON   (France)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

B cell lymphoma; CD20 antigen; CD4 T cells; immunotherapy; splicing

Indexed keywords

CD20 ANTIGEN; CD4 ANTIGEN; CYTOKINE; EPITOPE; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; PROTEIN D393; RNA ISOFORM; UNCLASSIFIED DRUG; ISOPROTEIN; PEPTIDE; TUMOR ANTIGEN;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; B CELL LYMPHOMA; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CLONING; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TRANSGENIC MOUSE; ANIMAL; GENETICS; IMMUNIZATION; IMMUNOLOGY; LYMPHOMA, B-CELL; METABOLISM; TUMOR CELL LINE;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, CD20; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; EPITOPES, T-LYMPHOCYTE; HUMANS; IMMUNIZATION; LYMPHOMA, B-CELL; MICE; MICE, TRANSGENIC; PEPTIDES; PROTEIN ISOFORMS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84930417033     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29366     Document Type: Article

References (45)

1. Cheever MA, Allison JP, Ferris AS, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res 2009; 15: 5323-37.
2. Faustino NA, Cooper TA,. Pre-mRNA splicing and human disease. Genes Dev 2003; 17: 419-37.
3. Kaida D, Schneider-Poetsch T, Yoshida M,. Splicing in oncogenesis and tumor suppression. Cancer Sci 2012; 103: 1611-6.
4. Gardina PJ, Clark TA, Shimada B, et al. Alternative splicing and differential gene expression in colon cancer detected by a whole genome exon array. BMC Genomics 2006; 7: 325.
5. He C, Zuo Z, Chen H, et al. Genome-wide detection of testis- and testicular cancer-specific alternative splicing. Carcinogenesis 2007; 28: 2484-90.
6. Henry C, Deschamps M, Rohrlich P-S, et al. Identification of an alternative CD20 transcript variant in B-cell malignancies coding for a novel protein associated to rituximab resistance. Blood 2010; 115: 2420-9.
7. Gamonet C, Ferrand C, Colliou N, et al. Lack of expression of an alternative CD20 transcript variant in circulating B cells from patients with pemphigus. Exp Dermatol 2014; 23: 66-7.
8. Small GW, McLeod HL, Richards KL,. Analysis of innate and acquired resistance to anti-CD20 antibodies in malignant and nonmalignant B cells. PeerJ 2013; 1: e31.
9. Kennedy R, Celis E,. Multiple roles for CD4+ T cells in anti-tumor immune responses. Immunol Rev 2008; 222: 129-44.
10. Bos R, Sherman LA,. CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 2010; 70: 8368-77.
11. Dosset M, Godet Y, Vauchy C, et al. Universal cancer peptide-based therapeutic vaccine breaks tolerance against telomerase and eradicates established tumor. Clin Cancer Res Off J Am Assoc Cancer Res 2012; 18: 6284-95.
12. Aarntzen EHJG, De Vries IJM, Lesterhuis WJ, et al. Targeting CD4(+) T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res 2013; 73: 19-29.
13. Slingluff CL Jr, Lee S, Zhao F, et al. A randomized phase II trial of multiepitope vaccination with melanoma peptides for cytotoxic T cells and helper T cells for patients with metastatic melanoma (E1602). Clin Cancer Res Off J Am Assoc Cancer Res 2013; 19: 4228-38.
14. Godet Y, Fabre E, Dosset M, Lamuraglia M, et al. Analysis of spontaneous tumor-specific CD4 T-cell immunity in lung cancer using promiscuous HLA-DR telomerase-derived epitopes: potential synergistic effect with chemotherapy response. Clin Cancer Res Off J Am Assoc Cancer Res 2012; 18: 2943-53.
15. Pajot A, Michel M-L, Fazilleau N, et al. A mouse model of human adaptive immune functions: HLA-A2.1-/HLA-DR1-transgenic H-2 class I-/class II-knockout mice. Eur J Immunol 2004; 34: 3060-9.
16. Tedder TF, Schlossman SF,. Phosphorylation of the B1 (CD20) molecule by normal and malignant human B lymphocytes. J Biol Chem 1988; 263: 10009-15.
17. Pfeiffer C, Stein J, Southwood S, et al. Altered peptide ligands can control CD4 T lymphocyte differentiation in vivo. J Exp Med 1995; 181: 1569-74.
18. Doherty DG, Penzotti JE, Koelle DM, et al. Structural basis of specificity and degeneracy of T cell recognition: pluriallelic restriction of T cell responses to a peptide antigen involves both specific and promiscuous interactions between the T cell receptor, peptide, and HLA-DR. J Immunol Baltim Md 1950 1998; 161: 3527-35.
19. Mycko MP, Waldner H, Anderson DE, et al. Cross-reactive TCR responses to self antigens presented by different MHC class II molecules. J Immunol Baltim Md 1950 2004; 173: 1689-98.
20. Hennecke J, Wiley DC,. Structure of a complex of the human alpha/beta T cell receptor (TCR) HA1.7, influenza hemagglutinin peptide, and major histocompatibility complex class II molecule, HLA-DR4 (DRA0101 and DRB10401): insight into TCR cross-restriction and alloreactivity. J Exp Med 2002; 195: 571-81.
21. Maccalli C, Li YF, El-Gamil M, et al. Identification of a Colorectal Tumor-Associated Antigen (COA-1) Recognized by CD4+ T Lymphocytes. Cancer Res 2003; 63: 6735-43.
22. Guo Y, Niiya H, Azuma T, et al. Direct recognition and lysis of leukemia cells by WT1-specific CD4+ T lymphocytes in an HLA class II-restricted manner. Blood 2005; 106: 1415-8.
23. Akhmetzyanova I, Zelinskyy G, Schimmer S, et al. Tumor-specific CD4+ T cells develop cytotoxic activity and eliminate virus-induced tumor cells in the absence of regulatory T cells. Cancer Immunol Immunother CII 2013; 62: 257-71.
24. Bijker MS, van den Eeden SJF, Franken KL, et al. CD8+ CTL priming by exact peptide epitopes in incomplete Freund's adjuvant induces a vanishing CTL response, whereas long peptides induce sustained CTL reactivity. J Immunol Baltim Md 1950 2007; 179: 5033-40.
25. Zhang L, Vlad A, Milcarek C, Finn OJ,. Human mucin MUC1 RNA undergoes different types of alternative splicing resulting in multiple isoforms. Cancer Immunol Immunother CII 2013; 62: 423-35.
26. Lin J, Lin L, Thomas DG, et al. Melanoma-associated antigens in esophageal adenocarcinoma: identification of novel MAGE-A10 splice variants. Clin Cancer Res Off J Am Assoc Cancer Res 2004; 10: 5708-16.
27. Kobayashi J, Torigoe T, Hirohashi Y, et al. Comparative study on the immunogenicity between an HLA-A24-restricted cytotoxic T-cell epitope derived from survivin and that from its splice variant survivin-2B in oral cancer patients. J Transl Med 2009; 7: 1.
28. Volpe G, Cignetti A, Panuzzo C, et al. Alternative BCR/ABL splice variants in Philadelphia chromosome-positive leukemias result in novel tumor-specific fusion proteins that may represent potential targets for immunotherapy approaches. Cancer Res 2007; 67: 5300-7.
29. Lupetti R, Pisarra P, Verrecchia A, v. Translation of a retained intron in tyrosinase-related protein (TRP) 2 mRNA generates a new cytotoxic T lymphocyte (CTL)-defined and shared human melanoma antigen not expressed in normal cells of the melanocytic lineage. J Exp Med 1998; 188: 1005-16.
30. Guilloux Y, Lucas S, Brichard VG, et al. A peptide recognized by human cytolytic T lymphocytes on HLA-A2 melanomas is encoded by an intron sequence of the N-acetylglucosaminyltransferase V gene. J Exp Med 1996; 183: 1173-83.
31. Robbins PF, El-Gamil M, Li YF, et al. The intronic region of an incompletely spliced gp100 gene transcript encodes an epitope recognized by melanoma-reactive tumor-infiltrating lymphocytes. J Immunol Baltim Md 1950 1997; 159: 303-8.
32. Andersen RS, Andersen SR, Hjortsø MD, et al. High frequency of T cells specific for cryptic epitopes in melanoma patients. Oncoimmunology 2013; 2: e25374.
33. Slager EH, van der Minne CE, Krüse M, et al. Identification of multiple HLA-DR-restricted epitopes of the tumor-associated antigen CAMEL by CD4+ Th1/Th2 lymphocytes. J Immunol Baltim Md 1950 2004; 172: 5095-102.
34. Friedman KM, Prieto PA, Devillier LE, et al. Tumor-specific CD4+ melanoma tumor-infiltrating lymphocytes. J Immunother Hagerstown Md 1997 2012; 35: 400-8.
35. Matsuzaki J, Tsuji T, Luescher I, et al. Nonclassical antigen-processing pathways are required for MHC class II-restricted direct tumor recognition by NY-ESO-1-specific CD4(+) T cells. Cancer Immunol Res 2014; 2: 341-50.
36. Zhu J, Paul WE,. Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol Rev 2010; 238: 247-62.
37. Muranski P, Restifo NP,. Essentials of Th17 cell commitment and plasticity. Blood 2013; 121: 2402-14.
38. Hamaï A, Pignon P, Raimbaud I, et al. Human T(H)17 immune cells specific for the tumor antigen MAGE-A3 convert to IFN-γ-secreting cells as they differentiate into effector T cells in vivo. Cancer Res 2012; 72: 1059-63.
39. Cecil DL, Holt GE, Park KH, et al. Elimination of IL-10-inducing T-helper epitopes from an IGFBP-2 vaccine ensures potent antitumor activity. Cancer Res 2014; 74: 2710-8.
40. Van Panhuys N, Klauschen F, Germain RN,. T-cell-receptor-dependent signal intensity dominantly controls CD4(+) T cell polarization in vivo. Immunity 2014; 41: 63-74.
41. Speetjens FM, Kuppen PJK, Welters MJP, et al. Induction of p53-specific immunity by a p53 synthetic long peptide vaccine in patients treated for metastatic colorectal cancer. Clin Cancer Res Off J Am Assoc Cancer Res 2009; 15: 1086-95.
42. Melief CJM, van der Burg SH,. Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat Rev Cancer 2008; 8: 351-60.
43. Koscielny G, Le Texier V, Gopalakrishnan C, et al. ASTD: The Alternative Splicing and Transcript Diversity database. Genomics 2009; 93: 213-20.
44. Stranzl T, Larsen MV, Lund O, et al. The cancer exome generated by alternative mRNA splicing dilutes predicted HLA class I epitope density. PloS One 2012; 7: e38670.
45. Bae J, Martinson JA, Klingemann HG,. Identification of CD19 and CD20 peptides for induction of antigen-specific CTLs against B-cell malignancies. Clin Cancer Res Off J Am Assoc Cancer Res 2005; 11: 1629-38.