Complement in monoclonal antibody therapy of cancer

Immunologic Research

Volumn 59, Issue 1-3, 2014, Pages 203-210

  Rogers, Laura M ^a   Veeramani, Suresh ^a   Weiner, George J ^a,b  

^a UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

ADCC; Cancer therapy; CDC; Complement; Monoclonal antibody

Indexed keywords

ALEMTUZUMAB; ANTIBODY; BEVACIZUMAB; BRENTUXIMAB VEDOTIN; CETUXIMAB; COMPLEMENT; IBRITUMOMAB TIUXETAN; IPILIMUMAB; MONOCLONAL ANTIBODY; OBINUTUZUMAB; OFATUMUMAB; PANITUMUMAB; PERTUZUMAB; RECEPTOR ANTIBODY; RITUXIMAB; TOSITUMOMAB I 131; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; CANCER ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; AUTOIMMUNITY; CANCER THERAPY; COMPLEMENT ACTIVATION; COMPLEMENT DEPENDENT CYTOTOXICITY; CYTOTOXICITY; DRUG DESIGN; DRUG EFFICACY; DRUG MECHANISM; EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR MICROENVIRONMENT; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; NEOPLASMS; PATHOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEOPLASM; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84905749267     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-014-8542-z     Document Type: Review

References (67)

1. McLaughlin P, Grillo-Lopez AJ, Link BK, Levy R, Czuczman MS, Williams ME, et al. Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol Off J Am Soc Clin Oncol. 1998;16(8):2825-33. (Pubitemid 28363048)
2. Sliwkowski MX, Mellman I. Antibody therapeutics in cancer. Science. 2013;341(6151):1192-8. doi:10.1126/science.1241145.
3. Cobleigh MA, Vogel CL, Tripathy D, Robert NJ, Scholl S, Fehrenbacher L, et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol Off J Am Soc Clin Oncol. 1999;17(9):2639-48. (Pubitemid 29415219)
4. Villamor N, Montserrat E, Colomer D. Mechanism of action and resistance to monoclonal antibody therapy. Semin Oncol. 2003;30(4):424-33. (Pubitemid 36999684)
5. Brand TM, Iida M, Wheeler DL. Molecular mechanisms of resistance to the EGFR monoclonal antibody cetuximab. Cancer Biol Ther. 2011;11(9):777-92.
6. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010;11(9):785-97. doi:10.1038/ni.1923.
7. Vetvicka V, Thornton BP, Wieman TJ, Ross GD. Targeting of natural killer cells to mammary carcinoma via naturally occurring tumor cell-bound iC3b and beta-glucan-primed CR3 (CD11b/CD18). J Immunol. 1997;159(2):599-605. (Pubitemid 127484208)
8. Klein E, Di Renzo L, Yefenof E. Contribution of CR3, CD11b/CD18 to cytolysis by human NK cells. Mol Immunol. 1990;27(12):1343-7.
9. Li B, Allendorf DJ, Hansen R, Marroquin J, Ding C, Cramer DE, et al. Yeast beta-glucan amplifies phagocyte killing of iC3b-opsonized tumor cells via complement receptor 3-Syk-phosphatidylinositol 3-kinase pathway. J Immunol. 2006;177(3):1661-9. (Pubitemid 44092502)
10. Liu J, Miwa T, Hilliard B, Chen Y, Lambris JD, Wells AD, et al. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J Exp Med. 2005;201(4):567-77. doi:10.1084/jem.20040863. (Pubitemid 40289547)
11. Varela JC, Imai M, Atkinson C, Ohta R, Rapisardo M, Tomlinson S. Modulation of protective T cell immunity by complement inhibitor expression on tumor cells. Cancer Res. 2008;68(16):6734-42. doi:10.1158/0008-5472.CAN-08-0502.
12. Davis AE 3rd. Biological effects of C1 inhibitor. Drug News Perspect. 2004;17(7):439-46.
13. Skerka C, Chen Q, Fremeaux-Bacchi V, Roumenina LT. Complement factor H related proteins (CFHRs). Mol Immunol. 2013;56(3):170-80. doi:10.1016/j.molimm. 2013.06.001.
14. Heinen S, Hartmann A, Lauer N, Wiehl U, Dahse HM, Schirmer S, et al. Factor H-related protein 1 (CFHR-1) inhibits complement C5 convertase activity and terminal complex formation. Blood. 2009;114(12):2439-47. doi:10.1182/blood-2009-02-205641.
15. Gelderman KA, Kuppen PJ, Okada N, Fleuren GJ, Gorter A. Tumor-specific inhibition of membrane-bound complement regulatory protein Crry with bispecific monoclonal antibodies prevents tumor outgrowth in a rat colorectal cancer lung metastases model. Cancer Res. 2004;64(12):4366-72. doi:10.1158/0008-5472.CAN-03- 2131. (Pubitemid 38802445)
16. Watson NF, Durrant LG, Madjd Z, Ellis IO, Scholefield JH, Spendlove I. Expression of the membrane complement regulatory protein CD59 (protectin) is associated with reduced survival in colorectal cancer patients. Cancer Immunol Immunother (CII). 2006;55(8):973-80. doi:10.1007/s00262-005-0055-0. (Pubitemid 43673588)
17. 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(21):10556-63. doi:10.1158/0008-5472.CAN-07-1811. (Pubitemid 350070832)
18. Williams ME, Densmore JJ, Pawluczkowycz AW, Beum PV, Kennedy AD, Lindorfer MA, et al. Thrice-weekly low-dose rituximab decreases CD20 loss via shaving and promotes enhanced targeting in chronic lymphocytic leukemia. J Immunol. 2006;177(10):7435-43. (Pubitemid 44715114)
19. Beum PV, Lindorfer MA, Taylor RP. Within peripheral blood mononuclear cells, antibody-dependent cellular cytotoxicity of rituximab-opsonized Daudi cells is promoted by NK cells and inhibited by monocytes due to shaving. J Immunol. 2008;181(4):2916-24.
20. Beum PV, Peek EM, Lindorfer MA, Beurskens FJ, Engelberts PJ, Parren PW, et al. Loss of CD20 and bound CD20 antibody from opsonized B cells occurs more rapidly because of trogocytosis mediated by Fc receptor-expressing effector cells than direct internalization by the B cells. J Immunol. 2011;187(6):3438-47. doi:10.4049/jimmunol.1101189.
21. 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(3):1581-7. (Pubitemid 36900094)
22. 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(2):176-83.
23. 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(5):3280-8. (Pubitemid 38263720)
24. Charbonneau B, Maurer MJ, Fredericksen ZS, Zent CS, Link BK, Novak AJ, et al. Germline variation in complement genes and event-free survival in follicular and diffuse large B-cell lymphoma. Am J Hematol. 2012;87(9):880-5. doi:10.1002/ajh.23273.
25. Racila E, Link BK, Weng WK, Witzig TE, Ansell S, Maurer MJ, et al. A polymorphism in the complement component C1qA correlates with prolonged response following rituximab therapy of follicular lymphoma. Clin Cancer Res Off J Am Assoc Cancer Res. 2008;14(20):6697-703. doi:10.1158/1078-0432.CCR-08-0745.
26. Baig NA, Taylor RP, Lindorfer MA, Church AK, Laplant BR, Pavey ES, et al. Complement dependent cytotoxicity in chronic lymphocytic leukemia: ofatumumab enhances alemtuzumab complement dependent cytotoxicity and reveals cells resistant to activated complement. Leuk Lymphoma. 2012;53(11):2218-27. doi:10.3109/10428194.2012.681657.
27. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med. 2000;6(4):443-6. doi:10.1038/74704. (Pubitemid 30208162)
28. 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(3):580-94. doi:10.1016/j.molonc.2013.02.011.
29. Idusogie EE, Wong PY, Presta LG, Gazzano-Santoro H, Totpal K, Ultsch M, et al. Engineered antibodies with increased activity to recruit complement. J Immunol. 2001;166(4):2571-5. (Pubitemid 32173494)
30. Li B, Shi S, Qian W, Zhao L, Zhang D, Hou S, et al. Development of novel tetravalent anti-CD20 antibodies with potent antitumor activity. Cancer Res. 2008;68(7):2400-8. doi:10.1158/0008-5472.CAN-07-6663. (Pubitemid 351521815)
31. Barth MJ, Hernandez-Ilizaliturri FJ, Mavis C, Tsai PC, Gibbs JF, Deeb G, et al. Ofatumumab demonstrates activity against rituximab-sensitive and -resistant cell lines, lymphoma xenografts and primary tumour cells from patients with B-cell lymphoma. Br J Haematol. 2012;156(4):490-8. doi:10.1111/j.1365-2141.2011.08966.x.
32. Herter S, Herting F, Mundigl O, Waldhauer I, Weinzierl T, Fauti T, et al. Preclinical activity of the type II CD20 antibody GA101 (obinutuzumab) compared with rituximab and ofatumumab in vitro and in xenograft models. Mol Cancer Ther. 2013;12(10):2031-42. doi:10.1158/1535-7163.MCT-12-1182.
33. Goede V, Fischer K, Busch R, Jaeger U, Dilhuydy MS, Wickham N, et al. Chemoimmunotherapy with GA101 plus chlorambucil in patients with chronic lymphocytic leukemia and comorbidity: results of the CLL11 (BO21004) safety run-in. Leukemia. 2013;27(5):1172-4. doi:10.1038/leu.2012.252.
34. Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity. 2006;24(1):19-28. doi:10.1016/j.immuni.2005.11.010. (Pubitemid 43077197)
35. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood. 2002;99(3):754-8. (Pubitemid 34525533)
36. Weng WK, Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol Off J Am Soc Clin Oncol. 2003;21(21):3940-7. doi:10.1200/JCO.2003.05.013. (Pubitemid 46606207)
37. Veeramani S, Wang SY, Dahle C, Blackwell S, Jacobus L, Knutson T, et al. Rituximab infusion induces NK activation in lymphoma patients with the high-affinity CD16 polymorphism. Blood. 2011;118(12):3347-9. doi:10.1182/blood-2011-05-351411.
38. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol Off J Am Soc Clin Oncol. 2008;26(11):1789-96. doi:10.1200/JCO.2007.14.8957.
39. Bibeau F, Lopez-Crapez E, Di Fiore F, Thezenas S, Ychou M, Blanchard F, et al. Impact of Fc{gamma}RIIa-Fc{gamma}RIIIa polymorphisms and KRAS mutations on the clinical outcome of patients with metastatic colorectal cancer treated with cetuximab plus irinotecan. J Clin Oncol Off J Am Soc Clin Oncol. 2009;27(7):1122-9. doi:10.1200/JCO.2008.18.0463.
40. Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood. 2012;119(24):5640-9. doi:10.1182/blood- 2012-01-380121.
41. Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, Briggs J, et al. High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J Biol Chem. 2001;276(9):6591-604. doi:10.1074/jbc. M009483200.
42. Wright A, Morrison SL. Effect of glycosylation on antibody function: implications for genetic engineering. Trends Biotechnol. 1997;15(1):26-32. doi:10.1016/S0167-7799(96)10062-7. (Pubitemid 27067150)
43. Bowles JA, Wang SY, Link BK, Allan B, Beuerlein G, Campbell MA, et al. Anti-CD20 monoclonal antibody with enhanced affinity for CD16 activates NK cells at lower concentrations and more effectively than rituximab. Blood. 2006;108(8):2648-54. doi:10.1182/blood-2006-04-020057.
44. Finberg RW, White W, Nicholson-Weller A. Decay-accelerating factor expression on either effector or target cells inhibits cytotoxicity by human natural killer cells. J Immunol. 1992;149(6):2055-60.
45. Caragine TA, Imai M, Frey AB, Tomlinson S. Expression of rat complement control protein Crry on tumor cells inhibits rat natural killer cell-mediated cytotoxicity. Blood. 2002;100(9):3304-10. doi:10.1182/blood.V100.9.3304. (Pubitemid 35217081)
46. Hamann J, Vogel B, van Schijndel GM, van Lier RA. The sevenspan transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J Exp Med. 1996;184(3):1185-9. (Pubitemid 26313577)
47. Shenoy-Scaria AM, Kwong J, Fujita T, Olszowy MW, Shaw AS, Lublin DM. Signal transduction through decay-accelerating factor. Interaction of glycosyl-phosphatidylinositol anchor and protein tyrosine kinases p56lck and p59fyn 1. J Immunol. 1992;149(11):3535-41.
48. Losse J, Zipfel PF, Jozsi M. Factor H and factor H-related protein 1 bind to human neutrophils via complement receptor 3, mediate attachment to Candida albicans, and enhance neutrophil antimicrobial activity. J Immunol. 2010;184(2):912-21. doi:10.4049/jimmunol.0901702.
49. Wang SY, Veeramani S, Racila E, Cagley J, Fritzinger DC, Vogel CW, et al. Depletion of the C3 component of complement enhances the ability of rituximab-coated target cells to activate human NK cells and improves the efficacy of monoclonal antibody therapy in an in vivo model. Blood. 2009;114(26):5322-30. doi:10.1182/blood-2009-01-200469.
50. 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 Off J Am Assoc Cancer Res. 2006;12(13):4027-35. doi:10.1158/1078-0432.CCR-06- 0066. (Pubitemid 44078090)
51. Pohlmann PR, Mayer IA, Mernaugh R. Resistance to trastuzumab in breast cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2009;15(24):7479-91. doi:10.1158/1078-0432.CCR-09-0636.
52. Farag SS, Flinn IW, Modali R, Lehman TA, Young D, Byrd JC. Fc gamma RIIIa and Fc gamma RIIa polymorphisms do not predict response to rituximab in B-cell chronic lymphocytic leukemia. Blood. 2004;103(4):1472-4. doi:10.1182/blood-2003- 07-2548. (Pubitemid 38168664)
53. Bolger MS, Ross DS, Jiang H, Frank MM, Ghio AJ, Schwartz DA, et al. Complement levels and activity in the normal and LPS-injured lung. Am J Physiol Lung Cell Mol Physiol. 2007;292(3):L748-59. doi:10.1152/ajplung.00127.2006. (Pubitemid 46376993)
54. Devaud C, Westwood JA, John LB, Flynn JK, Paquet-Fifield S, Duong CP, et al. Tissues in different anatomical sites can sculpt and vary the tumor microenvironment to affect responses to therapy. Mol Ther J Am Soc Gene Ther. 2014;22(1):18-27. doi:10.1038/mt.2013.219.
55. Kerbel RS. Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived-but they can be improved. Cancer Biol Ther. 2003;2(4 Suppl 1):S134-9.
56. Racila DM, Sontheimer CJ, Sheffield A, Wisnieski JJ, Racila E, Sontheimer RD. Homozygous single nucleotide polymorphism of the complement C1QA gene is associated with decreased levels of C1q in patients with subacute cutaneous lupus erythematosus. Lupus. 2003;12(2):124-32. (Pubitemid 36240846)
57. Sontheimer RD, Racila E, Racila DM. C1q: its functions within the innate and adaptive immune responses and its role in lupus autoimmunity. J Invest Dermatol. 2005;125(1):14-23. doi:10.1111/j.0022-202X.2005.23673.x. (Pubitemid 40981419)
58. Chen M, Daha MR, Kallenberg CG. The complement system in systemic autoimmune disease. J Autoimmun. 2010;34(3):J276-86. doi:10.1016/j.jaut.2009.11. 014.
59. Carroll MC. The complement system in regulation of adaptive immunity. Nat Immunol. 2004;5(10):981-6. doi:10.1038/ni1113. (Pubitemid 41057714)
60. Carroll MC. The complement system in B cell regulation. Mol Immunol. 2004;41(2-3):141-6. doi:10.1016/j.molimm.2004.03.017. (Pubitemid 38668623)
61. Strainic MG, Shevach EM, An F, Lin F, Medof ME. Absence of signaling into CD4(+) cells via C3aR and C5aR enables autoinductive TGF-beta1 signaling and induction of Foxp3(+) regulatory T cells. Nat Immunol. 2013;14(2):162-71. doi:10.1038/ni.2499.
62. Gunn L, Ding C, Liu M, Ma Y, Qi C, Cai Y, et al. Opposing roles for complement component C5a in tumor progression and the tumor microenvironment. J Immunol. 2012;189(6):2985-94. doi:10.4049/jimmunol.1200846.
63. Wagner C, Ochmann C, Schoels M, Giese T, Stegmaier S, Richter R, et al. The complement receptor 1, CR1 (CD35), mediates inhibitory signals in human T-lymphocytes. Mol Immunol. 2006;43(6):643-51. doi:10.1016/j.molimm.2005.04.006. (Pubitemid 41785392)
64. Markiewski MM, DeAngelis RA, Benencia F, Ricklin-Lichtsteiner SK, Koutoulaki A, Gerard C, et al. Modulation of the antitumor immune response by complement. Nat Immunol. 2008;9(11):1225-35. doi:10.1038/ni.1655.
65. Barchet W, Price JD, Cella M, Colonna M, MacMillan SK, Cobb JP, et al. Complement-induced regulatory T cells suppress T-cell responses but allow for dendritic-cell maturation. Blood. 2006;107(4):1497-504. doi:10.1182/blood-2005- 07-2951. (Pubitemid 43242387)
66. Weaver DJ Jr, Reis ES, Pandey MK, Kohl G, Harris N, Gerard C, et al. C5a receptor-deficient dendritic cells promote induction of Treg and Th17 cells. Eur J Immunol. 2010;40(3):710-21. doi:10.1002/eji.200939333.
67. Ricklin D, Lambris JD. Progress and trends in complement therapeutics. Adv Exp Med Biol. 2013;735:1-22.