Interleukin-21 Enhances Rituximab Activity in a Cynomolgus Monkey Model of B Cell Depletion and in Mouse B Cell Lymphoma Models

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Krejsa, Cecile M ^a   Holly, Rick D ^a   Heipel, Mark ^a   Bannink, Ken M ^a   Johnson, Rebecca ^a   Roque, Richard ^a   Heffernan, Jane ^a   Hill, Julie ^a   Chin, Lay ^a   Wagener, Felecia ^a   Shiota, Faith ^a   Henderson, Katherine ^a   Sivakumar, Pallavur V ^a   Ren, Hong Ping ^a   Barahmand pour, Fariba ^a   Foster, Don ^a   Clegg, Chris ^a   Kindsvogel, Wayne ^a   Ponce, Rafael ^a   Hughes, Steven D ^a   Waggie, Kim ^a   more..

^a BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIGEN; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 21; RITUXIMAB; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; CANCER INHIBITION; CANCER SURVIVAL; CELL CULTURE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; HAPLORHINI; HUMAN; HUMAN CELL; HUMORAL IMMUNE DEFICIENCY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA CELL LINE; MALE; MONOTHERAPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; UPREGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTINEOPLASTIC AGENTS; B-LYMPHOCYTES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; FEMALE; HUMANS; IMMUNITY, INNATE; INTERLEUKINS; LYMPHOMA, B-CELL; MACACA FASCICULARIS; MALE; MICE; SURVIVAL ANALYSIS;

MACACA FASCICULARIS; MURINAE;

EID: 84879367551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067256     Document Type: Article

References (41)

1. Asao H, Okuyama C, Kumaki S, Ishii N, Tsuchiya S, et al. (2001) Cutting edge: the common gamma-chain is an indispensable subunit of the IL-21 receptor complex. J Immunol 167: 1-5.
2. Habib T, Senadheera S, Weinberg K, Kaushansky K, (2002) The common gamma chain (gamma c) is a required signaling component of the IL-21 receptor and supports IL-21-induced cell proliferation via JAK3. Biochemistry 41: 8725-8731.
3. Parrish-Novak J, Dillon SR, Nelson A, Hammond A, Sprecher C, et al. (2000) Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 408: 57-63.
4. Ettinger R, Sims GP, Fairhurst AM, Robbins R, da Silva YS, et al. (2005) IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 175: 7867-7879.
5. Jin H, Carrio R, Yu A, Malek TR, (2004) Distinct activation signals determine whether IL-21 induces B cell costimulation, growth arrest, or Bim-dependent apoptosis. J Immunol 173: 657-665.
6. Kuchen S, Robbins R, Sims GP, Sheng G, Phillips TM, et al. (2007) Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD4+ T cell-B cell collaboration. J Immunol 179: 5886-5896.
7. de Totero D, Meazza R, Zupo S, Cutrona G, Matis S, et al. (2006) Interleukin-21 receptor (IL-21R) is up-regulated by CD40 triggering and mediates proapoptotic signals in chronic lymphocytic leukemia B cells. Blood 107: 3708-3715.
8. Sarosiek KA, Malumbres R, Nechushtan H, Gentles AJ, Avisar E, et al. (2010) Novel IL-21 signaling pathway up-regulates c-Myc and induces apoptosis of diffuse large B-cell lymphomas. Blood 115: 570-580.
9. Brady J, Hayakawa Y, Smyth MJ, Nutt SL, (2004) IL-21 induces the functional maturation of murine NK cells. J Immunol 172: 2048-2058.
10. Wang G, Tschoi M, Spolski R, Lou Y, Ozaki K, et al. (2003) In vivo antitumor activity of interleukin 21 mediated by natural killer cells. Cancer Res 63: 9016-9022.
11. Sondergaard H, Frederiksen KS, Thygesen P, Galsgaard ED, Skak K, et al. (2007) Interleukin 21 therapy increases the density of tumor infiltrating CD8(+) T cells and inhibits the growth of syngeneic tumors. Cancer Immunol Immunother 56: 1417-1428.
12. Andorsky DJ, Timmerman JM. Interleukin-21: biology and application to cancer therapy (2008) Expert Opinion on Biological Therapy. 8: 1295-1307.
13. Hashmi MH, Van Veldhuizen PJ, (2010) Interleukin-21: updated review of Phase I and II clinical trials in metastatic renal cell carcinoma, metastatic melanoma and relapsed/refractory indolent non-Hodgkin's lymphoma. Expert Opinion on Biological Therapy 10: 807-817.
14. Shan D, Ledbetter JA, Press OW, (1998) Apoptosis of malignant human B cells by ligation of CD20 with monoclonal antibodies. Blood 91: 1644-1652.
15. Manches O, Lui G, Chaperot L, Gressin R, Molens JP, et al. (2003) In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas. Blood 101: 949-954.
16. Boye J, Elter T, Engert A, (2003) An overview of the current clinical use of the anti-CD20 monoclonal antibody rituximab. Ann Oncol 14: 520-535.
17. Rastetter W, Molina A, White CA, (2004) Rituximab: expanding role in therapy for lymphomas and autoimmune diseases. Annu Rev Med 55: 477-503.
18. Khan KD, Emmanouilides C, Benson DM Jr, Hurst D, Garcia P, et al. (2006) A phase 2 study of rituximab in combination with recombinant interleukin-2 for rituximab-refractory indolent non-Hodgkin's lymphoma. Clin Cancer Res 12: 7046-7053.
19. Ansell SM, Geyer SM, Maurer MJ, Kurtin PJ, Micallef IN, et al. (2006) Randomized phase II study of interleukin-12 in combination with rituximab in previously treated non-Hodgkin's lymphoma patients. Clin Cancer Res 12: 6056-6063.
20. Fraser CC, Chen BP, Webb S, van Rooijen N, Kraai G, (1995) Circulation of human hematopoietic cells in severe combined immunodeficient mice after Cl2MDP-liposome-mediated macrophage depletion. Blood 86: 183-192.
21. Lopes de Menezes DE, Denis-Mize K, Tang Y, Ye H, Kunich JC, et al. (2007) Recombinant interleukin-2 significantly augments activity of rituximab in human tumor xenograft models of B-cell non-Hodgkin lymphoma. J Immunother 30: 64-74.
22. Vugmeyster Y, Howell K, McKeever K, Combs D, Canova-Davis E, (2003) Differential in vivo effects of rituximab on two B-cell subsets in cynomolgus monkeys. Int Immunopharmacol 3: 1477-1481.
23. Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, et al. (1994) Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood 83: 435-445.
24. Vugmeyster Y, Howell K, Bakshl A, Flores C, Canova-Davis E, (2003) Effect of anti-CD20 monoclonal antibody, Rituxan, on cynomolgus monkey and human B cells in a whole blood matrix. Cytometry A 52: 101-109.
25. Vugmeyster Y, Howell K, Bakshi A, Flores C, Hwang O, et al. (2004) B-cell subsets in blood and lymphoid organs in Macaca fascicularis. Cytometry A 61: 69-75.
26. Shultz LD, Schweitzer PA, Christianson SW, Gott B, Schweitzer IB, et al. (1995) Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 154: 180-191.
27. Eskelund CW, Nederby L, Thysen AH, Skovbo A, Roug AS, et al. (2011) Interleukin-21 and rituximab enhance NK cell functionality in patients with B-cell chronic lymphocytic leukaemia. Leukemia Research 35: 914-920.
28. Waggie KS, Holdren MS, Byrnes-Blake K, Pedersen S, Ponce R, et al. (2012) Preclinical safety, pharmacokinetics, and pharmacodynamics of recombinant human IL-21 in Cynomolgus macaques (Macaca fascicularis). Intl J Toxicol 31: 303-316.
29. Hamaguchi Y, Uchida J, Cain DW, Venturi GM, Poe JC, et al. (2005) The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J Immunol 174: 4389-4399.
30. Hernandez-Ilizaliturri FJ, Jupudy V, Ostberg J, Oflazoglu E, Huberman A, et al. (2003) Neutrophils contribute to the biological antitumor activity of rituximab in a non-Hodgkin's lymphoma severe combined immunodeficiency mouse model. Clin Cancer Res 9: 5866-5873.
31. Roda JM, Parihar R, Lehman A, Mani A, Tridandapani S, et al. (2006) Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J Immunol 177: 120-129.
32. McEarchern JA, Oflazoglu E, Francisco L, McDonagh CF, Gordon KA, et al. (2007) Engineered anti-CD70 antibody with multiple effector functions exhibits in vitro and in vivo antitumor activities. Blood. 109: 1185-1192.
33. Tedder TF, Baras A, Xiu Y, (2006) Fcgamma receptor-dependent effector mechanisms regulate CD19 and CD20 antibody immunotherapies for B lymphocyte malignancies and autoimmunity. Springer Semin Immunopathol 28: 351-364.
34. Pelletier M, Bouchard A, Girard D, (2004) In vivo and in vitro roles of IL-21 in inflammation. J Immunol 173: 7521-7530.
35. Mordue DG, Sibley LD, (2003) A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J Leukoc Biol 74: 1015-1025.
36. Landsman L, Varol C, Jung S, (2007) Distinct differentiation potential of blood monocyte subsets in the lung. J Immunol 178: 2000-2007.
37. Uchida J, Hamaguchi Y, Oliver JA, Ravetch JF, Poe JC, et al. (2004) The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 199: 1659-1669.
38. Strengell M, Lehtonen A, Matikainen S, Julkunen I, (2006) IL-21 enhances SOCS gene expression and inhibits LPS-induced cytokine production in human monocyte-derived dendritic cells. J Leukoc Biol 79: 1279-1285.
39. Pesce J, Kaviratne M, Ramalingam TR, Thompson RW, Urban JF, et al. (2006) The IL-21 receptor augments Th2 effector function and alternative macrophage activation. J Clin Invest 116: 2044-2055.
40. Jungel A, Distler JH, Kurowska-Stolarska M, Seemayer CA, Seibl R, et al. (2004) Expression of interleukin-21 receptor, but not interleukin-21, in synovial fibroblasts and synovial macrophages of patients with rheumatoid arthritis. Arthritis Rheum 50: 1468-1476.
41. Timmerman JM, Byrd JC, Andorsky DJ, Yamada RE, Kramer J, et al. (2012) A Phase I dose-finding trial of recombinant interleukin-21 and rituximab in relapsed and refractory low grade B-cell lymphoproliferative disorders. Clin Cancer Res 18: 5752-5760.