Combination with a defucosylated anti-HM1.24 monoclonal antibody plus lenalidomide induces marked ADCC against myeloma cells and their progenitors

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Harada, Takeshi ^a   Ozaki, Shuji ^b   Oda, Asuka ^a   Tsuji, Daisuke ^c   Ikegame, Akishige ^d   Iwasa, Masami ^a   Udaka, Kengo ^a   Fujii, Shiro ^a   Nakamura, Shingen ^a   Miki, Hirokazu ^a   Kagawa, Kumiko ^a   Kuroda, Yoshiaki ^e   Kawai, Shigeto ^f   Itoh, Kohji ^c   Yamada Okabe, Hisafumi ^g   Matsumoto, Toshio ^a   Abe, Masahiro ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b TOKUSHIMA PREFECTURAL CENTRAL HOSPITAL   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d TOKUSHIMA UNIVERSITY HOSPITAL   (Japan)

^e HIROSHIMA UNIVERSITY   (Japan)

^f Research Division   (Japan)

^g CHUGAI PHARMACEUTICAL CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LEN; LENALIDOMIDE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY HM1.24; UNCLASSIFIED DRUG;

ADULT; AGED; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BONE MARROW; CLINICAL ARTICLE; CLONOGENESIS; COLONY FORMATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; MALE; MIDDLE AGED; MONONUCLEAR CELL; MULTIPLE MYELOMA; MYELOMA CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; RECURRENT DISEASE; SIDE POPULATION CELL; STEM CELL; UPREGULATION; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; DRUG SYNERGISM; FEMALE; GLYCOSYLATION; GPI-LINKED PROTEINS; HUMANS; IMMUNOTHERAPY; MALE; MIDDLE AGED; MULTIPLE MYELOMA; NEOPLASTIC STEM CELLS; SIDE-POPULATION CELLS; THALIDOMIDE; UP-REGULATION;

EID: 84891280322     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083905     Document Type: Article

References (44)

1. A(2003) Criteria for the classification of monoclonal gammopathies, multiple myeloma and related disorders: a report of the International Myeloma Working Group. Br J Haematol 121: 749-757.
2. Gay F, Larocca A, Wijermans P, Cavallo F, Rossi D, et al. (2011) Complete response correlates with long-term progression-free and overall survival in elderly myeloma treated with novel agents: analysis of 1175 patients. Blood 117: 3025-3031.
3. Kumar SK, Rajkumar SV, Dispenzieri A, Lacy MQ, Hayman SR, et al. (2008) Improved survival in multiple myeloma and the impact of novel therapies. Blood 111: 2516-2520.
4. Palumbo A, Anderson K (2011) Multiple myeloma. N Engl J Med 364: 1046-1060.
5. Anderson KC, Carrasco RD (2011) Pathogenesis of myeloma. Annu Rev Pathol 6: 249-274.
6. Ikegame A, Ozaki S, Tsuji D, Harada T, Fujii S, et al. (2012) Small molecule antibody targeting HLA class I inhibits myeloma cancer stem cells by repressing pluripotency-associated transcription factors. Leukemia 26: 2124-2134.
7. Weiner LM, Dhodapkar MV, Ferrone S (2009) Monoclonal antibodies for cancer immunotherapy. Lancet 373: 1033-1040.
8. Ellis JH, Barber KA, Tutt A, Hale C, Lewis AP, et al. (1995) Engineered anti- CD38 monoclonal antibodies for immunotherapy of multiple myeloma. J Immunol 155: 925-937.
9. de Weers M, Tai YT, van der Veer MS, Bakker JM, Vink T, et al. (2011) Daratumumab, a novel therapeutic human CD38 monoclonal antibody, induces killing of multiple myeloma and other hematological tumors. J Immunol 186: 1840-1848.
10. van der Veer MS, de Weers M, van Kessel B, Bakker JM, Wittebol S, et al. (2011) Towards effective immunotherapy of myeloma: enhanced elimination of myeloma cells by combination of lenalidomide with the human CD38 monoclonal antibody daratumumab. Haematologica 96: 284-290.
11. Plesner T, Lokhorst H, Gimsing P, Nahi H, Lisby S, et al. (2012) Daratumumab, a CD38 Monoclonal Antibody in Patients with Multiple Myeloma - Data From a Dose-Escalation Phase I/II Study. Blood (ASH Annual Meeting Abstracts) 120: 73.
12. Tai YT, Dillon M, Song W, Leiba M, Li XF, et al. (2008) Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibody-dependent cellular cytotoxicity in the bone marrow milieu. Blood 112: 1329-1337.
13. Richardson PG, Jagannath S, Moreau P, Jakubowiak A, Raab MS, et al. (2012) A Phase 2 Study of Elotuzumab (Elo) in Combination with Lenalidomide and Low-Dose Dexamethasone (Ld) in Patients (pts) with Relapsed/Refractory Multiple Myeloma (R/R MM): Updated Results. Blood (ASH Annual Meeting Abstracts) 120: 202.
14. Hsi ED, Steinle R, Balasa B, Szmania S, Draksharapu A, et al. (2008) CS1, a potential new therapeutic antibody target for the treatment of multiple myeloma. Clin Cancer Res 14: 2775-2784.
15. Zonder JA, Mohrbacher AF, Singhal S, van Rhee F, Bensinger WI, et al. (2012) A phase 1, multicenter, open-label, dose escalation study of elotuzumab in patients with advanced multiple myeloma. Blood 120: 552-559.
16. Tai YT, Li XF, Catley L, Coffey R, Breitkreutz I, et al. (2005) Immunomodulatory drug lenalidomide (CC-5013, IMiD3) augments anti-CD40 SGN-40- induced cytotoxicity in human multiple myeloma: clinical implications. Cancer Res 65: 11712-11720. (Pubitemid 41821732)
17. Goto T, Kennel SJ, Abe M, Takishita M, Kosaka M, et al. (1994) A novel membrane antigen selectively expressed on terminally differentiated human B cells. Blood 84: 1922-1930. (Pubitemid 24286144)
18. Cao W, Bover L, Cho M, Wen X, Hanabuchi S, et al. (2009) Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J Exp Med 206: 1603-1614.
19. Cao W, Bover L (2010) Signaling and ligand interaction of ILT7: receptormediated regulatory mechanisms for plasmacytoid dendritic cells. Immunol Rev 234: 163-176.
20. Ozaki S, Kosaka M, Wakatsuki S, Abe M, Koishihara Y, et al. (1997) Immunotherapy of multiple myeloma with a monoclonal antibody directed against a plasma cell-specific antigen, HM1.24. Blood 90: 3179-3186. (Pubitemid 27444214)
21. Ozaki S, Kosaka M, Wakahara Y, Ozaki Y, Tsuchiya M, et al. (1999) Humanized anti-HM1.24 antibody mediates myeloma cell cytotoxicity that is enhanced by cytokine stimulation of effector cells. Blood 93: 3922-3930. (Pubitemid 29249841)
22. Ono K, Ohtomo T, Yoshida K, Yoshimura Y, Kawai S, et al. (1999) The humanized anti-HM1.24 antibody effectively kills multiple myeloma cells by human effector cell-mediated cytotoxicity. Mol Immunol 36: 387-395. (Pubitemid 29331647)
23. Powles R SB, Morgan G, et al (2001) A Phase I study of the safety, tolerance, pharmacokinetics, antigenicity and efficacy of a single intravenous dose of AHM followed by multiple doses of intravenous AHM in patients with multiple myeloma. Blood (ASH Annual Meeting Abstracts) 98: 165a. (Pubitemid 33786149)
24. Ishiguro T, Kawai S, Habu K, Sugimoto M, Shiraiwa H, et al. (2010) A defucosylated anti-CD317 antibody exhibited enhanced antibody-dependent cellular cytotoxicity against primary myeloma cells in the presence of effectors from patients. Cancer Sci 101: 2227-2233.
25. Dimopoulos MA, Chen C, Spencer A, Niesvizky R, Attal M, et al. (2009) Longterm follow-up on overall survival from the MM-009 and MM-010 phase III trials of lenalidomide plus dexamethasone in patients with relapsed or refractory multiple myeloma. Leukemia 23: 2147-2152.
26. Dimopoulos M, Spencer A, Attal M, Prince HM, Harousseau JL, et al. (2007) Lenalidomide plus dexamethasone for relapsed or refractory multiple myeloma. N Engl J Med 357: 2123-2132. (Pubitemid 350146107)
27. Weber DM, Chen C, Niesvizky R, Wang M, Belch A, et al. (2007) Lenalidomide plus dexamethasone for relapsed multiple myeloma in North America. N Engl J Med 357: 2133-2142. (Pubitemid 350146108)
28. Quach H, Ritchie D, Stewart AK, Neeson P, Harrison S, et al. (2010) Mechanism of action of immunomodulatory drugs (IMiDS) in multiple myeloma. Leukemia 24: 22-32.
29. Nowakowski GS, LaPlant B, Habermann TM, Rivera CE, Macon WR, et al. (2011) Lenalidomide can be safely combined with R-CHOP (R2CHOP) in the initial chemotherapy for aggressive B-cell lymphomas: phase I study. Leukemia 25: 1877-1881.
30. Tai YT, Horton HM, Kong SY, Pong E, Chen H, et al. (2012) Potent in vitro and in vivo activity of an Fc-engineered humanized anti-HM1.24 antibody against multiple myeloma via augmented effector function. Blood 119: 2074-2082.
31. Durie BG, Salmon SE (1975) A clinical staging system for multiple myeloma. Correlation of measured myeloma cell mass with presenting clinical features, response to treatment, and survival. Cancer 36: 842-854.
32. Greipp PR, San Miguel J, Durie BG, Crowley JJ, Barlogie B, et al. (2005) International staging system for multiple myeloma. J Clin Oncol 23: 3412-3420.
33. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806. (Pubitemid 26134320)
34. Hamburger A, Salmon SE (1977) Primary bioassay of human myeloma stem cells. J Clin Invest 60: 846-854. (Pubitemid 8208477)
35. Kawai S, Koishihara Y, Iida S, Ozaki S, Matsumoto T, et al. (2006) Construction of a conventional non-radioisotope method to quantify HM1.24 antigens: correlation of HM1.24 levels and ADCC activity of the humanized antibody against HM1.24. Leuk Res 30: 949-956. (Pubitemid 43841900)
36. Kawai S, Azuma Y, Fujii E, Furugaki K, Ozaki S, et al. (2008) Interferon-alpha enhances CD317 expression and the antitumor activity of anti-CD317 monoclonal antibody in renal cell carcinoma xenograft models. Cancer Sci 99: 2461-2466.
37. Jakubikova J, Adamia S, Kost-Alimova M, Klippel S, Cervi D, et al. (2011) Lenalidomide targets clonogenic side population in multiple myeloma: pathophysiologic and clinical implications. Blood 117: 4409-4419.
38. Weng WK, Levy R (2003) Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 21: 3940-3947. (Pubitemid 46606207)
39. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, et al. (2002) Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 99: 754-758. (Pubitemid 34525533)
40. Koene HR, Kleijer M, Algra J, Roos D, von dem Borne AE, et al. (1997) Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype. Blood 90: 1109-1114. (Pubitemid 27314146)
41. Lapalombella R, Yu B, Triantafillou G, Liu Q, Butchar JP, et al. (2008) Lenalidomide down-regulates the CD20 antigen and antagonizes direct and antibody-dependent cellular cytotoxicity of rituximab on primary chronic lymphocytic leukemia cells. Blood 112: 5180-5189.
42. Ohtomo T, Sugamata Y, Ozaki Y, Ono K, Yoshimura Y, et al. (1999) Molecular cloning and characterization of a surface antigen preferentially overexpressed on multiple myeloma cells. Biochem Biophys Res Commun 258: 583-591. (Pubitemid 29290312)
43. Harada T, Ozaki S, Oda A, Fujii S, Nakamura S, et al. (2013) Association of Th1 and Th2 cytokines with transient inflammatory reaction during lenalidomide plus dexamethasone therapy in multiple myeloma. Int J Hematol 97: 743-748.
44. Challen GA, Little MH (2006) A side order of stem cells: the SP phenotype. Stem Cells 24: 3-12.