Human CD59 inhibitor sensitizes rituximab-resistant lymphoma cells to complement-mediated cytolysis

Cancer Research

Volumn 71, Issue 6, 2011, Pages 2298-2307

  Hu, Weiguo ^a,c   Ge, Xiaowen ^c   You, Tao ^c   Xu, Ting ^d   Zhang, Jinyan ^c,e   Wu, Gongxiong ^a,c   Peng, Zhihai ^e   Chorev, Michael ^a,c   Aktas, Bertal H ^a,c   Halperin, Jose A ^a,c   Brown, Jennifer R ^b   Qin, Xuebin ^a,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Sino Recombi Pharma   (China)

^e SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; C REACTIVE PROTEIN; CD20 ANTIGEN; CD48 ANTIGEN; CD59 ANTIGEN; DECAY ACCELERATING FACTOR; INTERMEDILYSIN DOMAIN 4; MEMBRANE COFACTOR PROTEIN; RITUXIMAB; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; COMPLEMENT DEPENDENT CYTOTOXICITY; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYTOLYSIS; DISTRIBUTION VOLUME; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG ELIMINATION; DRUG HALF LIFE; DRUG RECEPTOR BINDING; DRUG SENSITIZATION; ERYTHROCYTE; FLUORESCENCE ACTIVATED CELL SORTING; HEMOLYSIS; HEMOLYTIC ANEMIA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LARGE CELL LYMPHOMA; LYMPHOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TOXICITY TESTING; TUMOR VOLUME; UPREGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIGENS, CD59; ANTINEOPLASTIC AGENTS; BACTERIOCINS; CELL LINE, TUMOR; COMPLEMENT SYSTEM PROTEINS; CYTOTOXICITY, IMMUNOLOGIC; CYTOTOXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOMA, B-CELL; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, NUDE; RECOMBINANT PROTEINS; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79952759542     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3016     Document Type: Article

References (46)

1. Glennie MJ, French RR, Cragg MS, Taylor RP.Mechanisms of killing by anti-CD20 monoclonal antibodies. Mol Immunol 2007;44: 3823-37. (Pubitemid 47332625)
2. Fishelson Z, Donin N, Zell S, Schultz S, Kirschfink M. Obstacles to cancer immunotherapy: expression of membrane complement regulatory proteins (mCRPs) in tumors. Mol Immunol 2003;40:109-23. (Pubitemid 36959821)
3. Bonavida B. Rituximab-induced inhibition of antiapoptotic cell survival pathways: implications in chemo/immunoresistance, rituximab unresponsiveness, prognostic and novel therapeutic interventions. Oncogene 2007;26:3629-36. (Pubitemid 46842700)
4. Golay J, Lazzari M, Facchinetti V, Bernasconi S, Borleri G, Barbui T, et al. CD20 levels determine the in vitro susceptibility to rituximab and complement of B-cell chronic lymphocytic leukemia: further regulation by CD55 and CD59. Blood 2001;98:3383-9.
5. Kennedy AD, Beum PV, Solga MD, DiLillo DJ, Lindorfer MA, Hess CE, et al. Rituximab infusion promotes rapid complement depletion and acute CD20 loss in chronic lymphocytic leukemia. J Immunol 2004;172:3280-8. (Pubitemid 38263720)
6. Golay J, Cittera E, Di Gaetano N, Manganini M, Mosca M, Nebuloni M, et al. The role of complement in the therapeutic activity of rituximab in a murine B lymphoma model homing in lymph nodes. Haematologica 2006;91:176-83.
7. Beum PV, Lindorfer MA, Beurskens F, Stukenberg PT, Lokhorst HM, Pawluczkowycz AW, et al. Complement activation on B lymphocytes opsonized with rituximab or ofatumumab produces substantial changes in membrane structure preceding cell lysis. J Immunol 2008;181:822-32.
8. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 2000;6: 443-6. (Pubitemid 30208162)
9. Zhou X, Hu W, Qin X. The role of complement in the mechanism of action of rituximab for B-cell lymphoma: implications for therapy. Oncologist 2008;13:954-66.
10. Wang SY, Racila E, Taylor RP, Weiner GJ. NK-cell activation and antibody-dependent cellular cytotoxicity induced by rituximab-coated target cells is inhibited by the C3b component of complement. Blood 2008;111:1456-63. (Pubitemid 351213433)
11. Introna M, Golay J. Complement in antibody therapy: friend or foe? Blood 2009;114:5247-8.
12. 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.
13. Cragg MS, Glennie MJ. Antibody specificity controls in vivo effector mechanisms of anti-CD20 reagents. Blood 2004;103:2738-43. (Pubitemid 38393032)
14. Cittera E, Leidi M, Buracchi C, Pasqualini F, Sozzani S, Vecchi A, et al. The CCL3 family of chemokines and innate immunity cooperate in vivo in the eradication of an established lymphoma xenograft by rituximab. J Immunol 2007;178:6616-23. (Pubitemid 46717446)
15. Di Gaetano N, Cittera E, Nota R, Vecchi A, Grieco V, Scanziani E, et al. Complement activation determines the therapeutic activity of rituximab in vivo. J Immunol 2003;171:1581-7. (Pubitemid 36900094)
16. Winkler U, Jensen M, Manzke O, Schulz H, Diehl V, Engert A. Cytokine-release syndrome in patients with B-cell chronic lymphocytic leukemia and high lymphocyte counts after treatment with an anti-CD20 monoclonal antibody (rituximab, IDEC-C2B8). Blood 1999;94:2217-24. (Pubitemid 29467667)
17. Klepfish A, Gilles L, Ioannis K, Eliezer R, Ami S. Enhancing the action of rituximab in chronic lymphocytic leukemia by adding fresh frozen plasma: complement/rituximab interactions & clinical results in refractory CLL. Ann N Y Acad Sci 2009;1173:865-73.
18. Xu W, Miao KR, Zhu DX, Fang C, Zhu HY, Dong HJ, et al. Enhancing the action of rituximab by adding fresh frozen plasma for the treatment of fludarabine refractory chronic lymphocytic leukemia. Int J Cancer. Epub 2010 Jul 15.
19. Golay J, Zaffaroni L, Vaccari T, Lazzari M, Borleri GM, Bernasconi S, et al. Biologic response of B lymphoma cells to anti-CD20 monoclonal antibody rituximab in vitro: CD55 and CD59 regulate complement-mediated cell lysis. Blood 2000;95:3900-8. (Pubitemid 30412866)
20. Wang H, Liu Y, Li ZY, Fan X, Hemminki A, Lieber A. A recombinant adenovirus type 35 fiber knob protein sensitizes lymphoma cells to rituximab therapy. Blood 2010;115:592-600.
21. Harjunpaa A, Junnikkala S, Meri S. Rituximab (anti-CD20) therapy of B-cell lymphomas: direct complement killing is superior to cellular effector mechanisms. Scand J Immunol 2000;51:634-41. (Pubitemid 30353375)
22. Bellosillo B, Villamor N, López-Guillermo A, Marcé S, Esteve J, Campo E, et al. Complement-mediated cell death induced by rituximab in Bcell lymphoproliferative disorders is mediated in vitro by a caspase-independent mechanism involving the generation of reactive oxygen species. Blood 2001;98:2771-7.
23. Ziller F, Macor P, Bulla R, Sblattero D, Marzari R, Tedesco F. Controlling complement resistance in cancer by using human monoclonal antibodies that neutralize complement-regulatory proteins CD55 and CD59. Eur J Immunol 2005;35:2175-83. (Pubitemid 41015056)
24. Macor P, Tripodo C, Zorzet S, Piovan E, Bossi F, Marzari R, et al. In vivo targeting of human neutralizing antibodies against CD55 and CD59 to lymphoma cells increases the antitumor activity of rituximab. Cancer Res 2007;67:10556-63.
25. Fisicaro N, Aminian A, Hinchliffe SJ, Morgan BP, Pearse MJ, D'Apice AJ, et al. The pig analogue of CD59 protects transgenic mouse hearts from injury by human complement. Transplantation 2000;70:963-8.
26. Sugita Y, Tobe T, Oda E, Tomita M, Yasukawa K, Yamaji N, et al. Molecular cloning and characterization of MACIF, an inhibitor of membrane channel formation of complement. J Biochem 1989;106: 555-7. (Pubitemid 19241820)
27. Medof ME, Lublin DM, Holers VM, Ayers DJ, Getty RR, Leykam JF, et al. Cloning and characterization of cDNAs encoding the complete sequence of decay-accelerating factor of human complement. Proc Natl Acad Sci U S A 1987;84:2007-11. (Pubitemid 17054138)
28. Davitz MA, Low MG, Nussenzweig V. Release of decay-accelerating factor (DAF) from the cell membrane by phosphatidylinositol-specific phospholipase C (PIPLC). J Exp Med 1986;163:1150-61. (Pubitemid 16000414)
29. Nicholson-Weller A, Spicer DB, Austen KF. Deficiency of the complement regulatory protein, "decay-accelerating factor," on membranes of granulocytes, monocytes, and platelets in paroxysmal nocturnal hemoglobinuria. N Engl J Med 1985;312:1091-7.
30. Brodbeck WG, Mold C, Atkinson JP, Medof ME. Cooperation between decay-accelerating factor and membrane cofactor protein in protecting cells from autologous complement attack. J Immunol 2000;165: 3999-4006. (Pubitemid 32057311)
31. Takei K, Yamazaki T, Sawada U, Ishizuka H, Aizawa S. Analysis of changes in CD20, CD55, and CD59 expression on established rituximab- resistant B-lymphoma cell lines. Leukoc Res 2006;30: 625-31.
32. Dalle S, Dupire S, Brunet-Manquat S, Reslan L, Plesa A, Dumontet C. In vivo model of follicular lymphoma resistant to rituximab. Clin Cancer Res 2009;15:851-7.
33. Bannerji R, Kitada S, Flinn IW, Pearson M, Young D, Reed JC, et al. Apoptotic-regulatory and complement-protecting protein expression in chronic lymphocytic leukemia: relationship to in vivo rituximab resistance. J Clin Oncol 2003;21:1466-71. (Pubitemid 46594097)
34. Coral S, Fonsatti E, Sigalotti L, De Nardo C, Visintin A, Nardi G, et al. Overexpression of protectin (CD59) down-modulates the susceptibility of human melanoma cells to homologous complement. J Cell Physiol 2000;185:317-23.
35. Fonsatti E, Altomonte M, Coral S, De Nardo C, Lamaj E, Sigalotti L, et al. Emerging role of protectin (CD59) in humoral immunotherapy of solid malignancies. Clin Ther 2000;151:187-93.
36. Hu W, Yu Q, Hu N, Byrd D, Amet T, Shikuma C, et al. A high-affinity inhibitor of human CD59 enhances complement-mediated virolysis of HIV-1: implications for treatment of HIV-1/AIDS. J Immunol 2010; 184:359-68.
37. Qin X, Hu W, Song W, Grubissich L, Hu X, Wu G, et al. Generation and phenotyping of mCd59a and mCd59b double-knockout mice. Am J Hematol 2009;84:65-70.
38. Hu W, Ferris SP, Tweten RK, Wu G, Radaeva S, Gao B, et al. Rapid conditional targeted ablation of cells expressing human CD59 in transgenic mice by intermedilysin. Nat Med 2008;14:98-103.
39. DiJoseph JF, Dougher MM, Kalyandrug LB, Armellino DC, Boghaert ER, Hamann PR, et al. Antitumor efficacy of a combination of CMC- 544 (inotuzumab ozogamicin), a CD22-targeted cytotoxic immunoconjugate of calicheamicin, and rituximab against non-Hodgkin's Bcell lymphoma. Clin Cancer Res 2006;12:242-9. (Pubitemid 43166200)
40. Dijoseph JF, Dougher MM, Armellino DC, Kalyandrug L, Kunz A, Boghaert ER, et al. CD20-specific antibody-targeted chemotherapy of non-Hodgkin's B-cell lymphoma using calicheamicin-conjugated rituximab. Cancer Immunol Immunother 2007;56:1107-17. (Pubitemid 46675304)
41. Giddings KS, Zhao J, Sims PJ, Tweten RK. Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat Struct Mol Biol 2004;11:1173-8.
42. You T, Hu W, Ge X, Shen J, Qin X. Application of a novel inhibitor of human CD59 for the enhancement of complement-dependent cytolysis on cancer cells. Cell Mol Immunol. Epub 2011 Jan 24.
43. Weng WK, Levy R. Expression of complement inhibitors CD46, CD55, and CD59 on tumor cells does not predict clinical outcome after rituximab treatment in follicular non-Hodgkin lymphoma. Blood 2001;98:1352-7.
44. 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. (Pubitemid 44078090)
45. Ohkura K, Nagamune H, Kourai H. Structural analysis of human specific cytolysin intermedilysin aiming application to cancer immunotherapy. Anticancer Res 2004;24:3343-53. (Pubitemid 39390950)
46. Nagamune H, Ohkura K, Umezu K, Shouji H, Kourai H. A cell membrane modification technique using domain 4 of intermedilysin for immunotherapy against cancer. Anticancer Res 2004;24:3367-72. (Pubitemid 39390953)