De novo diffuse large B-cell lymphoma with a CD20 immunohistochemistry-positive and flow cytometry-negative phenotype: Molecular mechanisms and correlation with rituximab sensitivity

Cancer Science

Volumn 105, Issue 1, 2014, Pages 35-43

  Tokunaga, Takashi ^a,b   Tomita, Akihiro ^a   Sugimoto, Keiki ^a   Shimada, Kazuyuki ^a   Iriyama, Chisako ^a   Hirose, Tatsuya ^a,c   Shirahata Adachi, Mizuho ^a   Suzuki, Yasuhiro ^a   Mizuno, Hiroki ^a   Kiyoi, Hitoshi ^a   Asano, Naoko ^a   Nakamura, Shigeo ^a   Kinoshita, Tomohiro ^d   Naoe, Tomoki ^a,b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION NAGOYA MEDICAL CENTER   (Japan)

^c MEIJO UNIVERSITY   (Japan)

^d AICHI CANCER CENTER HOSPITAL   (Japan)

Author keywords

CD20; Diffuse large B cell lymphoma; Flow cytometry; Immunohistochemistry; Rituximab

Indexed keywords

CD20 ANTIGEN; CYCLOPHOSPHAMIDE; DOXORUBICIN; ETOPOSIDE; MEMBRANE ANTIGEN; MESSENGER RNA; PREDNISOLONE; RITUXIMAB; VINCRISTINE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CELL SURFACE; CLINICAL FEATURE; CODING; CONTROLLED STUDY; CORRELATIONAL STUDY; DRUG SENSITIVITY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LARGE CELL LYMPHOMA; LYMPHOMA CELL; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION;

CD20; DIFFUSE LARGE B-CELL LYMPHOMA; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; RITUXIMAB;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIGENS, CD20; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MICE; MICE, SCID; MIDDLE AGED; PHENOTYPE; SURVIVAL RATE;

EID: 84892885330     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12307     Document Type: Article

References (34)

1. Tedder TF, Engel P. CD20: a regulator of cell-cycle progression of B lymphocytes. Immunol Today 1994; 15: 450-4.
2. Maloney DG. Anti-CD20 antibody therapy for B-cell lymphomas. N Engl J Med 2012; 366: 2008-16.
3. Lim SH, Beers SA, French RR, Johnson PW, Glennie MJ, Cragg MS. Anti-CD20 monoclonal antibodies: historical and future perspectives. Haematologica 2010; 95: 135-43.
4. Coiffier B, Thieblemont C, Van Den Neste E, et al. Long-term outcome of patients in the LNH-98.5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d'Etudes des Lymphomes de l'Adulte. Blood 2010; 116: 2040-5.
5. Salles G, Seymour JF, Offner F, et al. Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial. Lancet 2011; 377: 42-51.
6. Hiddemann W, Kneba M, Dreyling M, et al. Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood 2005; 106: 3725-32.
7. Smith MR. Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Oncogene 2003; 22: 7359-68.
8. Rezvani AR, Maloney DG. Rituximab resistance. Best Pract Res Clin Haematol 2011; 24: 203-16.
9. Tomita A, Hiraga J, Kiyoi H, et al. Epigenetic regulation of CD20 protein expression in a novel B-cell lymphoma cell line, RRBL1, established from a patient treated repeatedly with rituximab-containing chemotherapy. Int J Hematol 2007; 86: 49-57.
10. Hiraga J, Tomita A, Sugimoto T, et al. Down-regulation of CD20 expression in B-cell lymphoma cells after treatment with rituximab-containing combination chemotherapies: its prevalence and clinical significance. Blood 2009; 113: 4885-93.
11. Sugimoto T, Tomita A, Hiraga J, et al. Escape mechanisms from antibody therapy to lymphoma cells: downregulation of CD20 mRNA by recruitment of the HDAC complex and not by DNA methylation. Biochem Biophys Res Commun 2009; 390: 48-53.
12. Beum PV, Kennedy AD, Williams ME, Lindorfer MA, Taylor RP. The shaving reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. J Immunol 2006; 176: 2600-9.
13. Beum PV, Lindorfer MA, Taylor RP. Within peripheral blood mononuclear cells, antibody-dependent cellular cytotoxicity of rituximab-opsonized Daudi cells is promoted by NK cells and inhibited by monocytes due to shaving. J Immunol 2008; 181: 2916-24.
14. Terui Y, Mishima Y, Sugimura N, et al. Identification of CD20 C-terminal deletion mutations associated with loss of CD20 expression in non-Hodgkin's lymphoma. Clin Cancer Res 2009; 15: 2523-30.
15. Mishima Y, Terui Y, Takeuchi K, et al. The identification of irreversible rituximab-resistant lymphoma caused by CD20 gene mutations. Blood Cancer J 2011; 1: e15.
16. Nakamaki T, Fukuchi K, Nakashima H, et al. CD20 gene deletion causes a CD20-negative relapse in diffuse large B-cell lymphoma. Eur J Haematol 2012; 89: 350-5.
17. Henry C, Deschamps M, Rohrlich PS, 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.
18. Lim SH, Vaughan AT, Ashton-Key M, et al. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood 2011; 118: 2530-40.
19. Beum PV, Peek EM, Lindorfer MA, et al. Loss of CD20 and bound CD20 antibody from opsonized B cells occurs more rapidly because of trogocytosis mediated by Fc receptor-expressing effector cells than direct internalization by the B cells. J Immunol 2011; 187: 3438-47.
20. Beers SA, French RR, Chan HT, et al. Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood 2010; 115: 5191-201.
21. Miyoshi H, Arakawa F, Sato K, et al. Comparison of CD20 expression in B-cell lymphoma between newly diagnosed, untreated cases and those after rituximab treatment. Cancer Sci 2012; 103: 1567-73.
22. Horvat M, Kloboves Prevodnik V, Lavrencak J, Jezersek Novakovic B. Predictive significance of the cut-off value of CD20 expression in patients with B-cell lymphoma. Oncol Rep 2010; 24: 1101-7.
23. van Meerten T, van Rijn RS, Hol S, Hagenbeek A, Ebeling SB. Complement-induced cell death by rituximab depends on CD20 expression level and acts complementary to antibody-dependent cellular cytotoxicity. Clin Cancer Res 2006; 12: 4027-35.
24. van Meerten T, Rozemuller H, Hol S, et al. HuMab-7D8, a monoclonal antibody directed against the membrane-proximal small loop epitope of CD20 can effectively eliminate CD20 low expressing tumor cells that resist rituximab-mediated lysis. Haematologica 2010; 95: 2063-71.
25. Johnson NA, Boyle M, Bashashati A, et al. Diffuse large B-cell lymphoma: reduced CD20 expression is associated with an inferior survival. Blood 2009; 113: 3773-80.
26. Sonoki T, Li Y, Miyanishi S, et al. Establishment of a novel CD20 negative mature B-cell line, WILL2, from a CD20 positive diffuse large B-cell lymphoma patient treated with rituximab. Int J Hematol 2009; 89: 400-2.
27. Goto E, Tomita A, Hayakawa F, Atsumi A, Kiyoi H, Naoe T. Missense mutations in PML-RARA are critical for the lack of responsiveness to arsenic trioxide treatment. Blood 2011; 118: 1600-9.
28. Shipp MA. A predictive model for aggressive non-Hodgkin's lymphoma. The International Non-Hodgkin's Lymphoma Prognostic Factors Project. N Engl J Med 1993; 329: 987-94.
29. Binder M, Otto F, Mertelsmann R, Veelken H, Trepel M. The epitope recognized by rituximab. Blood 2006; 108: 1975-8.
30. Niederfellner G, Lammens A, Mundigl O, et al. Epitope characterization and crystal structure of GA101 provide insights into the molecular basis for type I/II distinction of CD20 antibodies. Blood 2011; 118: 358-67.
31. Himmelmann A, Riva A, Wilson GL, Lucas BP, Thevenin C, Kehrl JH. PU.1/Pip and basic helix loop helix zipper transcription factors interact with binding sites in the CD20 promoter to help confer lineage- and stage-specific expression of CD20 in B lymphocytes. Blood 1997; 90: 3984-95.
32. Kawabata KC, Ehata S, Komuro A, Takeuchi K, Miyazono K. TGF-beta-induced apoptosis of B-cell lymphoma Ramos cells through reduction of MS4A1/CD20. Oncogene 2013; 32: 2096-106.
33. Teeling JL, Mackus WJ, Wiegman LJ, et al. The biological activity of human CD20 monoclonal antibodies is linked to unique epitopes on CD20. J Immunol 2006; 177: 362-71.
34. Patz M, Isaeva P, Forcob N, et al. Comparison of the in vitro effects of the anti-CD20 antibodies rituximab and GA101 on chronic lymphocytic leukaemia cells. Br J Haematol 2011; 152: 295-306.