Neutralization of membrane complement regulators improves complement-dependent effector functions of therapeutic anticancer antibodies targeting leukemic cells

OncoImmunology

Volumn 4, Issue 3, 2015, Pages 1-12

  Mamidi, Srinivas ^a   Höne, Simon ^a   Teufel, Claudia ^a   Sellner, Leopold ^a,b   Zenz, Thorsten ^a,b   Kirschfink, Michael ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Alemtuzumab; Chronic lymphocytic leukemia; Complement regulatory proteins; Complement dependent cytotoxicity; Ofatumumab; Opsonization; Rituximab

Indexed keywords

ALEMTUZUMAB; CD20 ANTIGEN; CD59 ANTIGEN; DECAY ACCELERATING FACTOR; MEMBRANE COFACTOR PROTEIN; NEUTRALIZING ANTIBODY; OFATUMUMAB; RITUXIMAB; TRASTUZUMAB;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; BURKITT LYMPHOMA; CELL PHAGOCYTOSIS; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE SEQUENCE; GENE SILENCING; HUMAN; HUMAN CELL; LEUKEMIA CELL; OPSONIZATION; PROTEIN EXPRESSION; RAJI CELL LINE; SERODIAGNOSIS;

EID: 84951907927     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/2162402X.2014.979688     Document Type: Article

References (54)

1. Carroll MC, Fischer MB. Complement and the immune response. Curr Opin Immunol 1997; 9:64-9; PMID:9039785; http://dx.doi.org/10.1016/S0952-7915(97)80160-4
2. Walport MJ. Complement. First of two parts. N Engl J Med 2001; 344:1058-66; PMID:11287977; http://dx.doi.org/10.1056/NEJM200104053441406
3. Muller-Eberhard HJ. The membrane attack complex of complement. Annu Rev Immunol 1986; 4:503-28; PMID:3518749; http://dx.doi.org/10.1146/annurev.iy.04.040186.002443
4. Walport MJ. Complement. Second of two parts. N Engl J Med 2001; 344:1140-4; PMID:11297706; http://dx.doi.org/10.1056/NEJM200104123441506
5. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11:785-97; PMID:20720586; http://dx.doi.org/10.1038/ni.1923
6. Perlmann H, Perlmann P, Schreiber RD, Muller-Eberhard HJ. Interaction of target cell-bound C3bi and C3d with human lymphocyte receptors. Enhancement of antibody-mediated cellular cytotoxicity. J Exp Med 1981; 153:1592-603; PMID:7252421; http://dx.doi.org/10.1084/jem.153.6.1592
7. Markiewski MM, DeAngelis RA, Benencia F, Ricklin-Lichtsteiner SK, Koutoulaki A, Gerard C, Coukos G, Lambris JD. Modulation of the antitumor immune response by complement. Nat Immunol 2008; 9:1225-35; PMID:18820683; http://dx.doi.org/10.1038/ni.1655
8. Gelderman KA, Tomlinson S, Ross GD, Gorter A. Complement function in mAb-mediated cancer immunotherapy. Trends Immunol 2004; 25:158-64; PMID:15036044; http://dx.doi.org/10.1016/j.it.2004.01.008
9. Elvington M, Huang Y, Morgan BP, Qiao F, van Rooijen N, Atkinson C, Tomlinson S. A targeted complement-dependent strategy to improve the outcome of mAb therapy, and characterization in a murine model of metastatic cancer. Blood 2012; 119:6043-51; PMID:22442351; http://dx.doi.org/10.1182/blood-2011-10-383232
10. 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; PMID:12914817; http://dx.doi.org/10.1016/S0161-5890(03)00112-3
11. Jurianz K, Ziegler S, Garcia-Schuler H, Kraus S, Bohana-Kashtan O, Fishelson Z, Kirschfink M. Complement resistance of tumor cells: basal and induced mechanisms. Mol Immunol 1999; 36:929-39; PMID:10698347; http://dx.doi.org/10.1016/S0161-5890(99)00115-7
12. Gorter A, Meri S. Immune evasion of tumor cells using membrane-bound complement regulatory proteins. Immunol Today 1999; 20:576-82; PMID:10562709; http://dx.doi.org/10.1016/S0167-5699(99)01537-6
13. Varsano S, Rashkovsky L, Shapiro H, Ophir D, Mark-Bentankur T. Human lung cancer cell lines express cell membrane complement inhibitory proteins and are extremely resistant to complement-mediated lysis; a comparison with normal human respiratory epithelium in vitro, and an insight into mechanism(s) of resistance. Clin Exp Immunol 1998; 113:173-82; PMID:9717965; http://dx.doi.org/10.1046/j.1365-2249.1998.00581.x
14. Geis N, Zell S, Rutz R, Li W, Giese T, Mamidi S, Schultz S, Kirschfink M. Inhibition of membrane complement inhibitor expression (CD46, CD55, CD59) by siRNA sensitizes tumor cells to complement attack in vitro. Curr Cancer Drug Targets 2010; 10:922-31; PMID:20879979; http://dx.doi.org/10.2174/156800910793357952
15. Jurianz K, Maslak S, Garcia-Schuler H, Fishelson Z, Kirschfink M. Neutralization of complement regulatory proteins augments lysis of breast carcinoma cells targeted with rhumAb anti-HER2. Immunopharmacology 1999; 42:209-18; PMID:10408382; http://dx.doi.org/10.1016/S0162-3109(99)00006-5
16. Zell S, Geis N, Rutz R, Schultz S, Giese T, Kirschfink M. Down-regulation of CD55 and CD46 expression by anti-sense phosphorothioate oligonucleotides (SODNs) sensitizes tumour cells to complement attack. Clin Exp Immunol 2007; 150:576-84; PMID:17903221; http://dx.doi.org/10.1111/j.1365-2249.2007.03507.x
17. Bellone S, Roque D, Cocco E, Gasparrini S, Bortolomai I, Buza N, Abu-Khalaf M, Silasi DA, Ratner E, Azodi M et al. Downregulation of membrane complement inhibitors CD55 and CD59 by siRNA sensitises uterine serous carcinoma overexpressing Her2/neu to complement and antibody-dependent cell cytotoxicity in vitro: implications for trastuzumab-based immunotherapy. Br J Cancer 2012; 106:1543-50; PMID:22531721; http://dx.doi.org/10.1038/bjc.2012.132
18. Scott SD. Rituximab: a new therapeutic monoclonal antibody for non-Hodgkin’s lymphoma. Cancer Pract 1998; 6:195-7; PMID:9652253; http://dx.doi.org/10.1046/j.1523-5394.1998.006003195.x
19. Maloney DG, Grillo-Lopez AJ, White CA, Bodkin D, Schilder RJ, Neidhart JA, Janakiraman N, Foon KA, Liles TM, Dallaire BK et al. IDEC-C2B8 (Rituximab) anti-CD20 monoclonal antibody therapy in patients with relapsed low-grade non-Hodgkin’s lymphoma. Blood 1997; 90:2188-95; PMID:9310469
20. Cheson BD, Leonard JP. Monoclonal antibody therapy for B-cell non-Hodgkin’s lymphoma. N Engl J Med 2008; 359:613-26; PMID:18687642; http://dx.doi.org/10.1056/NEJMra0708875
21. Golay J, Zaffaroni L, Vaccari T, Lazzari M, Borleri GM, Bernasconi S, Tedesco F, Rambaldi A, Introna M. 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; PMID:10845926
22. Huhn D, von Schilling C, Wilhelm M, Ho AD, Hallek M, Kuse R, Knauf W, Riedel U, Hinke A, Srock S et al. Rituximab therapy of patients with B-cell chronic lymphocytic leukemia. Blood 2001; 98:1326-31; PMID:11520778; http://dx.doi.org/10.1182/blood.V98.5.1326
23. 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. Leuk Res 2006; 30:625-31; PMID:16289746; http://dx.doi.org/10.1016/j.leukres.2005.09.008
24. Treon SP, Mitsiades C, Mitsiades N, Young G, Doss D, Schlossman R, Anderson KC. Tumor cell expression of CD59 is associated with resistance to CD20 serotherapy in patients with B-cell malignancies. J Immunother (1991) 2001; 24:263-71; PMID:11395643; http://dx.doi.org/10.1097/00002371-200105000-00011
25. Macor P, Tripodo C, Zorzet S, Piovan E, Bossi F, Marzari R, Amadori A, Tedesco F. 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; PMID:17975000; http://dx.doi.org/10.1158/0008-5472.CAN-07-1811
26. Hu W, Ge X, You T, Xu T, Zhang J, Wu G, Peng Z, Chorev M, Aktas BH, Halperin JA et al. Human CD59 inhibitor sensitizes rituximab-resistant lymphoma cells to complement-mediated cytolysis. Cancer Res 2011; 71:2298-307; PMID:21252115; http://dx.doi.org/10.1158/0008-5472.CAN-10-3016
27. Teeling JL, French RR, Cragg MS, van den Brakel J, Pluyter M, Huang H, Chan C, Parren PW, Hack CE, Dechant M et al. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood 2004; 104:1793-800; PMID:15172969; http://dx.doi.org/10.1182/blood-2004-01-0039
28. Teeling JL, Mackus WJ, Wiegman LJ, van den Brakel JH, Beers SA, French RR, van Meerten T, Ebeling S, Vink T, Slootstra JW et al. The biological activity of human CD20 monoclonal antibodies is linked to unique epitopes on CD20. J Immunol 2006; 177:362-71; PMID:16785532; http://dx.doi.org/10.4049/jimmunol.177.1.362
29. Bologna L, Gotti E, Da Roit F, Intermesoli T, Rambaldi A, Introna M, Golay J. Ofatumumab is more efficient than rituximab in lysing B chronic lymphocytic leukemia cells in whole blood and in combination with chemotherapy. J Immunol 2013; 190:231-9; PMID:23225880; http://dx.doi.org/10.4049/jimmunol.1202645
30. Horl S, Banki Z, Huber G, Ejaz A, Windisch D, Muellauer B, Willenbacher E, Steurer M, Stoiber H. Reduction of complement factor H binding to CLL cells improves the induction of rituximab-mediated complement-dependent cytotoxicity. Leukemia 2013; 27:2200-8; PMID:23760402; http://dx.doi.org/10.1038/leu.2013.169
31. Horl S, Banki Z, Huber G, Ejaz A, Mullauer B, Willenbacher E, Steurer M, Stoiber H. Complement factor H-derived short consensus repeat 18-20 enhanced complement-dependent cytotoxicity of ofatumumab on chronic lymphocytic leukemia cells. Haematologica 2013; 98:1939-47; PMID:23850806; http://dx.doi.org/10.3324/haematol.2013.089615
32. Keating MJ, Flinn I, Jain V, Binet JL, Hillmen P, Byrd J, Albitar M, Brettman L, Santabarbara P, Wacker B et al. Therapeutic role of alemtuzumab (Campath-1H) in patients who have failed fludarabine: results of a large international study. Blood 2002; 99:3554-61; PMID:11986207; http://dx.doi.org/10.1182/blood.V99.10.3554
33. Osterborg A, Mellstedt H, Keating M. Clinical effects of alemtuzumab (Campath-1H) in B-cell chronic lymphocytic leukemia. Med Oncol 2002; 19 Suppl:S21-6; PMID:12180488; http://dx.doi.org/10.1385/MO:19:2S:S21
34. Fiegl M, Stauder R, Steurer M, Mian M, Hopfinger G, Brychtova Y, Skrabs C, Zabernigg A, Schmid F, Haslbaur F et al. Alemtuzumab in chronic lymphocytic leukemia: final results of a large observational multicenter study in mostly pretreated patients. Ann Hematol 2014; 93:267-77; PMID:24292560; http://dx.doi.org/10.1007/s00277-013-1966-z
35. Dyer MJ. The role of CAMPATH-1 antibodies in the treatment of lymphoid malignancies. Semin Oncol 1999; 26:52-7; PMID:10561018
36. Golay J, Manganini M, Rambaldi A, Introna M. Effect of alemtuzumab on neoplastic B cells. Haematologica 2004; 89:1476-83; PMID:15590398
37. Golay J, Cortiana C, Manganini M, Cazzaniga G, Salvi A, Spinelli O, Bassan R, Barbui T, Biondi A, Rambaldi A et al. The sensitivity of acute lymphoblastic leukemia cells carrying the t(12;21) translocation to campath-1H-mediated cell lysis. Haematologica 2006; 91:322-30; PMID:16531255
38. Boross P, Leusen JH. Boosting antibody therapy with complement. Blood 2012; 119:5945-7; PMID:22730521; http://dx.doi.org/10.1182/blood-2012-04-420760
39. Mamidi S, Cinci M, Hasmann M, Fehring V, Kirschfink M. Lipoplex mediated silencing of membrane regulators (CD46, CD55 and CD59) enhances complement-dependent anti-tumor activity of trastuzumab and pertuzumab. Mol Oncol 2013; 7:580-94; PMID:23474221; http://dx.doi.org/10.1016/j.molonc.2013.02.011
40. Seiffert M, Stilgenbauer S, Dohner H, Lichter P. Efficient nucleofection of primary human B cells and B-CLL cells induces apoptosis, which depends on the microenvironment and on the structure of transfected nucleic acids. Leukemia 2007; 21:1977-83; PMID:17637809; http://dx.doi.org/10.1038/sj.leu.2404863
41. Weiner LM, Surana R, Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol 2010; 10:317-27; PMID:20414205; http://dx.doi.org/10.1038/nri2744
42. Sliwkowski MX, Mellman I. Antibody therapeutics in cancer. Science 2013; 341:1192-8; PMID:24031011; http://dx.doi.org/10.1126/science.1241145
43. Macor P, Tedesco F. Complement as effector system in cancer immunotherapy. Immunol Lett 2007; 111:6-13; PMID:17572509; http://dx.doi.org/10.1016/j.imlet.2007.04.014
44. Gancz D, Fishelson Z. Cancer resistance to complement-dependent cytotoxicity (CDC): problem-oriented research and development. Mol Immunol 2009; 46:2794-800; PMID:19501402; http://dx.doi.org/10.1016/j.molimm.2009.05.009
45. Pawluczkowycz AW, Beurskens FJ, Beum PV, Lindorfer MA, van de Winkel JG, Parren PW, Taylor RP. Binding of submaximal C1q promotes complementdependent cytotoxicity (CDC) of B cells opsonized with anti-CD20 mAbs ofatumumab (OFA) or rituximab (RTX): considerably higher levels of CDC are induced by OFA than by RTX. J Immunol 2009; 183:749-58; PMID:19535640; http://dx.doi.org/10.4049/jimmunol.0900632
46. Ge X, Wu L, Hu W, Fernandes S, Wang C, Li X, Brown JR, Qin X. rILYd4, a human CD59 inhibitor, enhances complement-dependent cytotoxicity of ofatumumab against rituximab-resistant B-cell lymphoma cells and chronic lymphocytic leukemia. Clin Cancer Res 2011; 17:6702-11; PMID:21918174; http://dx.doi.org/10.1158/1078-0432.CCR-11-0647
47. Baig NA, Taylor RP, Lindorfer MA, Church AK, Laplant BR, Pavey ES, Nowakowski GS, Zent CS. Complement dependent cytotoxicity in chronic lymphocytic leukemia: ofatumumab enhances alemtuzumab complement dependent cytotoxicity and reveals cells resistant to activated complement. Leuk Lymphoma 2012; 53:2218-27; PMID:22475085; http://dx.doi.org/10.3109/10428194.2012.681657
48. Aagaard L, Rossi JJ. RNAi therapeutics: principles, prospects and challenges. Adv Drug Deliv Rev 2007; 59:75-86; PMID:17449137; http://dx.doi.org/10.1016/j.addr.2007.03.005
49. Schakowski F, Buttgereit P, Mazur M, Marten A, Schottker B, Gorschluter M, Schmidt-Wolf IG. Novel non-viral method for transfection of primary leukemia cells and cell lines. Genet Vaccines Ther 2004; 2:1; PMID:14715084; http://dx.doi.org/10.1186/1479-0556-2-1
50. Wang SY, Racila E, Taylor RP, Weiner GJ. NKcell 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; PMID:18024795; http://dx.doi.org/10.1182/blood-2007-02-074716
51. Glennie MJ, French RR, Cragg MS, Taylor RP. Mechanisms of killing by anti-CD20 monoclonal antibodies. Mol Immunol 2007; 44:3823-37; PMID:17768100; http://dx.doi.org/10.1016/j.molimm.2007.06.151
52. Montalvao F, Garcia Z, Celli S, Breart B, Deguine J, Van Rooijen N, Bousso P. The mechanism of anti-CD20-mediated B cell depletion revealed by intravital imaging. J Clin Invest 2013; 123:5098-103; PMID:24177426; http://dx.doi.org/10.1172/JCI70972
53. Cinci M, Mamidi S, Li W, Fehring V, Kirschfink M. Targeted delivery of siRNA using transferrin-coupled lipoplexes specifically sensitizes CD71 high expressing malignant cells to antibody-mediated complement attack. Target Oncol 2014 Nov 15. [Epub ahead of print]. PMID:25395366
54. Czauderna F, Fechtner M, Dames S, Aygun H, Klippel A, Pronk GJ, Giese K, Kaufmann J. Structural variations and stabilising modifications of synthetic siRNAs in mammalian cells. Nucleic Acids Res 2003; 31:2705-16; PMID:12771196; http://dx.doi.org/10.1093/nar/gkg393