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

References

• 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
   PubMed Web of Science ®Google Scholar
• Walport MJ. Complement. First of two parts. N Engl J Med 2001; 344:1058-66; PMID:11287977; http://dx.doi.org/10.1056/NEJM200104053441406
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Walport MJ. Complement. Second of two parts. N Engl J Med 2001; 344:1140-4; PMID:11297706; http://dx.doi.org/10.1056/NEJM200104123441506
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Zell S, Geis N, Rutz R, Schultz S, Giese T, Kirschfink M. Down-regulation of CD55 and CD46 expression by anti-sense phosphorothioate oligonucleotides (S-ODNs) 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Dyer MJ. The role of CAMPATH-1 antibodies in the treatment of lymphoid malignancies. Semin Oncol 1999; 26:52-7; PMID:10561018
   PubMed Web of Science ®Google Scholar
• Golay J, Manganini M, Rambaldi A, Introna M. Effect of alemtuzumab on neoplastic B cells. Haematologica 2004; 89:1476-83; PMID:15590398
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Sliwkowski MX, Mellman I. Antibody therapeutics in cancer. Science 2013; 341:1192-8; PMID:24031011; http://dx.doi.org/10.1126/science.1241145
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Pawluczkowycz AW, Beurskens FJ, Beum PV, Lindorfer MA, van de Winkel JG, Parren PW, Taylor RP. Binding of submaximal C1q promotes complement-dependent 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• 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; PMID:18024795; http://dx.doi.org/10.1182/blood-2007-02-074716
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   Google Scholar
• 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
   PubMed Web of Science ®Google Scholar