Control of complement activation by cancer cells and its implications in antibody-mediated cancer immunotherapy

Inmunologia

Volumn 25, Issue 3, 2006, Pages 173-187

  Pio, Ruben ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Antibodies; Complement inactivator proteins; Immunotherapy; Neoplasms

Indexed keywords

ALEMTUZUMAB; BEVACIZUMAB; CETUXIMAB; COMPLEMENT; MONOCLONAL ANTIBODY; REGULATOR PROTEIN; RITUXIMAB; TRASTUZUMAB;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; BREAST CANCER; CANCER CELL; CANCER IMMUNOTHERAPY; CARCINOGENESIS; CELL TRANSFORMATION; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL; COLORECTAL CANCER; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; COMPLEX REGIONAL PAIN SYNDROME TYPE I; DRUG MECHANISM; HUMAN; INNATE IMMUNITY; LUNG CARCINOGENESIS; NONHODGKIN LYMPHOMA; NONHUMAN; PROTEIN EXPRESSION; REVIEW; TARGET CELL;

EID: 33846439007     PISSN: 02139626     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (168)

1. Liszewski MK, Atkinson JP. The complement system. In: Paul WE (ed). Fundamental Immunology. Third edition. New York: Raven Press; 1993. p. 917-939.
2. Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996;271:348-350.
3. Morgan BP, Marchbank KJ, Longhi MP, Harris CL, Gallimore AM. Complement: central to innate immunity and bridging to adaptive responses. Immunol Lett 2005;97:171-179.
4. Carroll MC. The complement system in regulation of adaptive immunity. Nat Immunol 2004;5:981-986.
5. Molina H, Holers VM, Li B, Fung Y, Mariathasan S, Goellner J, et al. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc Natl Acad Sci USA 1996;93:3357-3361.
6. Kaya Z, Afanasyeva M, Wang Y, Dohmen KM, Schlichting J, Tretter T, et al. Contribution of the innate immune system to autoimmune myocarditis: a role for complement. Nat Immunol 2001;2:739-745.
7. Fleming SD, Shea-Donohue T, Guthridge JM, Kulik L, Waldschmidt TJ, Gipson MG, et al. Mice deficient in complement receptors 1 and 2 lack a tissue injury-inducing subset of the natural antibody repertoire. J Immunol 2002;169:2126-2133.
8. Prodeus AP, Goerg S, Shen LM, Pozdnyakova OO, Chu L, Alicot EM, et al. A critical role for complement in maintenance of self-tolerance. Immunity 1998;9:721-731.
9. Carroll MC. The role of complement in B cell activation and tolerance. Adv Immunol 2000;74:61-88.
10. Kishore U, Reid KB. C1q: structure, function, and receptors. Immunopharmacology 2000;49:159-170.
11. Arlaud GJ, Gaboriaud C, Thielens NM, Rossi V. Structural biology of C1. Biochem Soc Trans 2002;30:1001-1006.
12. Sunyer JO, Lambris JD. Evolution and diversity of the complement system of poikilothermic vertebrates. Immunol Rev 1998;166:39-57.
13. Pangburn MK, Schreiber RD, Muller-Eberhard HJ. Formation of the initial C3 convertase of the alternative complement pathway. Acquisition of C3b-like activities by spontaneous hydrolysis of the putative thioester in native C3. J Exp Med 1981;154:856-867.
14. Lu JH, Thiel S, Wiedemann H, Timpl R, Reid KB. Binding of the pentamer/hexamer forms of mannan-binding protein to zymosan activates the proenzyme C1r2C1s2 complex, of the classical pathway of complement, without involvement of C1q. J Immunol 1990;144: 2287-2294.
15. Zhang Y, Suankratay C, Zhang XH, Lint TF, Gewurz H. Lysis via the lectin pathway of complement activation: minireview and lectin pathway enhancement of endotoxin-initiated hemolysis. Immunopharmacology 1999;42:81-90.
16. Bara S, Lint TF. The third component of complement (C3) bound to tumor target cells enhances their sensitivity to killing by activated macrophages. J Immunol 1987;138:1303-1309.
17. Ramos OF, Nilsson B, Nilsson K, Eggertsen G, Yefenof E, Klein E. Elevated NK-mediated lysis of Raji and Daudi cells carrying fixed iC3b fragments. Cell Immunol 1989;119:459-469.
18. 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- 1603.
19. Kohl J. Anaphylatoxins and infectious and non-infectious inflammatory diseases. Mol Immunol 2001;38:175-187.
20. Ziccardi RJ. A new role for C-1-inhibitor in homeostasis: control of activation of the first component of human complement. J Immunol 1982;128:2505-2508.
21. Sim RB, Day AJ, Moffatt BE, Fontaine M. Complement factor I and cofactors in control of complement system convertase enzymes. Methods Enzymol 1993;223:13-35.
22. Weiler JM, Daha MR, Austen KF, Fearon DT. Control of the amplification convertase of complement by the plasma protein beta1H. Proc Natl Acad Sci USA 1976;73:3268-3272.
23. Whaley K, Ruddy S. Modulation of the alternative complement pathways by beta 1 H globulin. J Exp Med 1976;144:1147-1163.
24. Jenne DE, Tschopp J. Molecular structure and functional characterization of a human complement cytolysis inhibitor found in blood and seminal plasma: identity to sulfated glycoprotein 2, a constituent of rat testis fluid. Proc Natl Acad Sci USA 1989;86: 7123-7127.
25. Podack ER, Muller-Eberhard HJ. Isolation of human S-protein, an inhibitor of the membrane attack complex of complement. J Biol Chem 1979;254:9808-9814.
26. Fearon DT. Regulation of the amplification C3 convertase of human complement by an inhibitory protein isolated from human erythrocyte membrane. Proc Natl Acad Sci USA 1979;76:5867-5871.
27. Iida K, Nussenzweig V. Functional properties of membrane-associated complement receptor CR1. J Immunol 1983;130:1876-1880.
28. Liszewski MK, Post TW, Atkinson JP. Membrane cofactor protein (MCP or CD46): newest member of the regulators of complement activation gene cluster. Annu Rev Immunol 1991;9:431-455.
29. Lublin DM, Atkinson JP. Decay-accelerating factor: biochemistry, molecular biology, and function. Annu Rev Immunol 1989;7:35-58.
30. Meri S, Morgan BP, Davies A, Daniels RH, Olavesen MG, Waldmann H, Lachmann PJ. Human protectin (CD59), an 18,000-20,000 MW complement lysis restricting factor, inhibits C5b-8 catalysed insertion of C9 into lipid bilayers. Immunology 1990;71:1-9.
31. Rollins SA, Sims PJ. The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J Immunol 1990;144:3478-3483.
32. Yamamoto H, Blaas P, Nicholson-Weller A, Hansch GM. Homologous species restriction of the complement-mediated killing of nucleated cells. Immunology 1990;70:422-426.
33. Rodriguez de Cordoba S, Lublin DM, Rubinstein P, Atkinson JP. Human genes for three complement components that regulate the activation of C3 are tightly linked. J Exp Med 1985;161:1189-1195.
34. Rodriguez de Cordoba S, Diaz-Guillen MA, Heine-Suner D. An integrated map of the human regulator of complement activation (RCA) gene cluster on 1q32. Mol Immunol 1999;36:803-808.
35. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100: 57-70.
36. Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 1996;56:5309-5318.
37. Warren L, Buck CA, Tuszynski GP. Glycopeptide changes and malignant transformation. A possible role for carbohydrate in malignant behavior. Biochim Biophys Acta 1978;516:97-127.
38. Pardoll D. Does the immune system see tumors as foreign or self? Annu Rev Immunol 2003;21:807-839.
39. Smyth MJ, Godfrey DI, Trapani JA. A fresh look at tumor immunosurveillance and immunotherapy. Nat Immunol 2001;2: 293-299.
40. Jakobisiak M, Lasek W, Golab J. Natural mechanisms protecting against cancer. Immunol Lett 2003;90:103-122.
41. Guidi L, Baroni R, Bartoloni C, Pellegrino M, Tricerri A, Marciano M, et al. Immune complexes in solid tumours precipitable by 3.5% polyethylene glycol: analysis of some nonspecific components. Diagn Clin Immunol 1988;5:284-288.
42. Zurlo JJ, Schechter GP, Fries LF. Complement abnormalities in multiple myeloma. Am J Med 1989;87:411-420.
43. Baatrup G, Qvist N, Junker A, Larsen KE, Zimmermann-Nielsen C. Activity and activation of the complement system in patients being operated on for cancer of the colon. Eur J Surg 1994;160:503-510.
44. Bjorge L, Hakulinen J, Vintermyr OK, Jarva H, Jensen TS, Iversen OE, Meri S. Ascitic complement system in ovarian cancer. Br J Cancer 2005;92:895-905.
45. Niculescu F, Rus HG, Retegan M, Vlaicu R. Persistent complement activation on tumor cells in breast cancer. Am J Pathol 1992;140: 1039-1043.
46. Lucas SD, Karlsson-Parra A, Nilsson B, Grimelius L, Akerstrom G, Rastad J, Juhlin C. Tumor-specific deposition of immunoglobulin G and complement in papillary thyroid carcinoma. Hum Pathol 1996;27:1329-1335.
47. Ytting H, Jensenius JC, Christensen IJ, Thiel S, Nielsen HJ. Increased activity of the mannan-binding lectin complement activation pathway in patients with colorectal cancer. Scand J Gastroenterol 2004;39:674-679.
48. Ytting H, Christensen IJ, Thiel S, Jensenius JC, Nielsen HJ. Serum mannan-binding lectin-associated serine protease 2 levels in colorectal cancer: relation to recurrence and mortality. Clin Cancer Res 2005;11:1441-1446.
49. Gelderman KA, Blok VT, Fleuren GJ, Gorter A. The inhibitory effect of CD46, CD55, and CD59 on complement activation after immunotherapeutic treatment of cervical carcinoma cells with monoclonal antibodies or bispecific monoclonal antibodies. Lab Invest 2002;82:483-493.
50. Niehans GA, Cherwitz DL, Staley NA, Knapp DJ, Dalmasso AP. Human carcinomas variably express the complement inhibitory proteins CD46 (membrane cofactor protein), CD55 (decay-accelerating factor), and CD59 (protectin). Am J Pathol 1996;149:129-142.
51. Nishioka K, Kawamura K, Hirayama T, Kawashima T, Shimada K. The complement system in tumor immunity: significance of elevated levels of complement in tumor bearing hosts. Ann N Y Acad Sci 1976;276:303- 315.
52. Gminski I, Mykala-Ciesla J, Machalski M, Drozdz M, Najda J. Immunoglobulins and complement components levels in patients with lung cancer. Rom J Intern Med 1992;30:39-44.
53. Carli M, Bucolo C, Pannunzio MT, Ongaro G, Businaro R, Revoltella R. Fluctuation of serum complement levels in children with neuroblastoma. Cancer 1979;43:2399-2404.
54. Maness PF, Orengo A. Serum complement levels in patients with digestive tract carcinomas and other neoplastic diseases. Oncology 1977;34:87-89.
55. Matsutani M, Suzuki T, Hori T, Terao H, Takakura K, Nishioka K. Cellular immunity and complement levels in hosts with brain tumours. Neurosurg Rev 1984;7:29-35.
56. Fust G, Miszlay Z, Czink E, Varga L, Paloczi K, Szegedi G, Hollan SR. C1 and C4 abnormalities in chronic lymphocytic leukaemia and their significance. Immunol Lett 1987;14:255-259.
57. Schlesinger M, Broman I, Lugassy G. The complement system is defective in chronic lymphatic leukemia patients and in their healthy relatives. Leukemia 1996;10:1509-1513.
58. Varga L, Czink E, Miszlai Z, Paloczi K, Banyai A, Szegedi G, Fust G. Low activity of the classical complement pathway predicts short survival of patients with chronic lymphocytic leukaemia. Clin Exp Immunol 1995;99:112-116.
59. Mangano A, Messina L, Birgillito S, Stivala F, Bernardini A. Complement and its fractions (C3-C4) pattern in subjects with neoplasia. J Immunopharmacol 1984;6:147-162.
60. 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;36:929-939.
61. Varsano S, Frolkis I, Rashkovsky L, Ophir D, Fishelson Z. Protection of human nasal respiratory epithelium from complement-mediated lysis by cell-membrane regulators of complement activation. Am J Respir Cell Mol Biol 1996;15:731-737.
62. 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;113:173-182.
63. Gorter A, Meri S. Immune evasion of tumor cells using membrane-bound complement regulatory proteins. Immunol Today 1999;20: 576-582.
64. 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;40:109-123.
65. Weichenthal M, Siemann U, Neuber K, Breitbart EW. Expression of complement regulator proteins in primary and metastatic malignant melanoma. J Cutan Pathol 1999;26:217-221.
66. Brasoveanu LI, Altomonte M, Fonsatti E, Colizzi F, Coral S, Nicotra MR, et al. Levels of cell membrane CD59 regulate the extent of complement-mediated lysis of human melanoma cells. Lab Invest 1996;74:33-42.
67. Loberg RD, Wojno KJ, Day LL, Pienta KJ. Analysis of membrane-bound complement regulatory proteins in prostate cancer. Urology 2005;66:1321-1326.
68. Xu C, Jung M, Burkhardt M, Stephan C, Schnorr D, Loening S, Jung K, et al. Increased CD59 protein expression predicts a PSA relapse in patients after radical prostatectomy. Prostate 2005;62: 224-232.
69. Jarvis GA, Li J, Hakulinen J, Brady KA, Nordling S, Dahiya R, Meri S. Expression and function of the complement membrane attack complex inhibitor protectin (CD59) in human prostate cancer. Int J Cancer 1997;71:1049-1055.
70. Watson NF, Spendlove I, Madjd Z, McGilvray R, Green AR, Ellis IO, et al. Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients. Int J Cancer 2006;118:1445-1452.
71. Bjorge L, Vedeler CA, Ulvestad E, Matre R. Expression and function of CD59 on colonic adenocarcinoma cells. Eur J Immunol 1994;24: 1597-1603.
72. Donin N, Jurianz K, Ziporen L, Schultz S, Kirschfink M, Fishelson Z. Complement resistance of human carcinoma cells depends on membrane regulatory proteins, protein kinases and sialic acid. Clin Exp Immunol 2003;131:254-263.
73. Chen S, Caragine T, Cheung NK, Tomlinson S. CD59 expressed on a tumor cell surface modulates decay-accelerating factor expression and enhances tumor growth in a rat model of human neuroblastoma. Cancer Res 2000;60:3013-3018.
74. 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;185:317-323.
75. Loberg RD, Day LL, Dunn R, Kalikin LM, Pienta KJ. Inhibition of Decay-Accelerating Factor (CD55) Attenuates Prostate Cancer Growth and Survival In Vivo. Neoplasia 2006;8:69-78.
76. Mustafa T, Klonisch T, Hombach-Klonisch S, Kehlen A, Schmutzler C, Koehrle J, et al. Expression of CD97 and CD55 in human medullary thyroid carcinomas. Int J Oncol 2004;24:285-294.
77. Durrant LG, Chapman MA, Buckley DJ, Spendlove I, Robins RA. Armitage NC. Enhanced expression of the complement regulatory protein CD55 predicts a poor prognosis in colorectal cancer patients. Cancer Immunol Immunother 2003;52:638-642.
78. Madjd Z, Durrant LG, Bradley R, Spendlove I, Ellis IO, Pinder SE. Loss of CD55 is associated with aggressive breast tumors. Clin Cancer Res 2004;10:2797-2803.
79. Liu J, Miwa T, Hilliard B, Chen Y, Lambris JD, Wells AD, Song WC. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J Exp Med 2005;201:567-577.
80. Madjd Z, Durrant LG, Pinder SE, Ellis IO, Ronan J, Lewis S, et al. Do poor-prognosis breast tumours express membrane cofactor proteins (CD46)? Cancer Immunol Immunother 2005;54:149-156.
81. Rushmere NK, Knowlden JM, Gee JM, Harper ME, Robertson JF, Morgan BP, Nicholson RI. Analysis of the level of mRNA expression of the membrane regulators of complement, CD59, CD55 and CD46, in breast cancer. Int J Cancer 2004;108:930-936.
82. Medof ME, Walter EI, Rutgers JL, Knowles DM, Nussenzweig V. Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids. J Exp Med 1987;165:848- 864.
83. Davies A, Summons DL, Hale G, Harrison RA, Tighe H, Lachmann PJ, Waldmann H. CD59, an LY-6-like protein expressed in human lymphoid cells, regulates the action of the complement membrane attack complex on homologous cells. J Exp Med 1989;170:637-654.
84. Seya T, Hara T, Iwata K, Kuriyama S, Hasegawa T, Nagase Y, Miyagawa S, et al. Purification and functional properties of soluble forms of membrane cofactor protein (CD46) of complement: identification of forms increased in cancer patients' sera. Int Immunol 1995;7:727-736.
85. Sadallah S, Lach E, Schwarz S, Gratwohl A, Spertini O, Schifferli JA. Soluble complement receptor 1 is increased in patients with leukemia and after administration of granulocyte colony-stimulating factor. J Leukoc Biol 1999;65:94-101.
86. Li L, Spendlove I, Morgan J, Durrant LG. CD55 is over-expressed in the tumour environment. Br J Cancer 2001;84:80-86.
87. Morgan J, Spendlove I, Durrant LG. The role of CD55 in protecting the tumour environment from complement attack. Tissue Antigens 2002;60:213-223.
88. Hakulinen J, Junnikkala S, Sorsa T, Meri S. Complement inhibitor membrane cofactor protein (MCP; CD46) is constitutively shed from cancer cell membranes in vesicles and converted by a metalloproteinase to a functionally active soluble form. Eur J Immunol 2004;34:2620-2629.
89. Brasoveanu LI, Fonsatti E, Visintin A, Pavlovic M, Cattarossi I, Colizzi F, et al. Melanoma cells constitutively release an anchor-positive soluble form of protectin (sCD59) that retains functional activities in homologous complement-mediated cytotoxicity. J Clin Invest 1997;100:1248- 1255.
90. Hindmarsh EJ, Marks RM. Decay-accelerating factor is a component of subendothelial extracellular matrix in vitro, and is augmented by activation of endothelial protein kinase C. Eur J Immunol 1998;28:1052-1062.
91. Nasu J, Mizuno M, Uesu T, Takeuchi K, Inaba T, Ohya S, et al. Cytokine-stimulated release of decay-accelerating factor (DAF;CD55) from HT-29 human intestinal epithelial cells. Clin Exp Immunol 1998;113:379- 385.
92. Jurianz K, Ziegler S, Donin N, Reiter Y, Fishelson Z, Kirschfink M. K562 erythroleukemic cells are equipped with multiple mechanisms of resistance to lysis by complement. Int J Cancer 2001;93:848-854.
93. Kawada M, Mizuno M, Nasu J, Uesu T, Okazaki H, Okada H, et al. Release of decay-accelerating factor into stools of patients with colorectal cancer by means of cleavage at the site of glycosylphosphatidylinositol anchor. J Lab Clin Med 2003;142:306-312.
94. Kohno H, Mizuno M, Nasu J, Makidono C, Hiraoka S, Inaba T, et al. Stool decay-accelerating factor as a marker for monitoring the disease activity during leukocyte apheresis therapy in patients with refractory ulcerative colitis. J Gastroenterol Hepatol 2005;20: 73-78.
95. Reiter Y, Fishelson Z. Targeting of complement to tumor cells by heteroconjugates composed of antibodies and of the complement component C3b. J Immunol 1989;142:2771-2777.
96. Ollert MW, David K, Bredehorst R, Vogel CW. Classical complement pathway activation on nucleated cells. Role of factor H in the control of deposited C3b. J Immunol 1995;155:4955-4962.
97. Junnikkala S, Jokiranta TS, Friese MA, Jarva H, Zipfel PF, Meri S. Exceptional resistance of human H2 glioblastoma cells to complement-mediated killing by expression and utilization of factor H and factor H-like protein 1. J Immunol 2000;164:6075-6081.
98. Ajona D, Castano Z, Garayoa M, Zudaire E, Pajares MJ, Martinez A, et al. Expression of complement factor H by lung cancer cells: effects on the activation of the alternative pathway of complement. Cancer Res 2004;64:6310-6308.
99. Pangburn MK, Schreiber RD, Muller-Eberhard HJ. Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein beta1H for cleavage of C3b and C4b in solution. J Exp Med 1977;146: 257-270.
100. Zipfel PF, Skerka C. FHL-1/reconectin: a human complement and immune regulator with cell-adhesive function. Immunol Today 1999;20:135- 140.
101. Rodriguez de Cordoba S, Esparza-Gordillo J, Goicoechea de Jorge E, Lopez-Trascasa M, Sanchez-Corral P. The human complement factor H: functional roles, genetic variations and disease associations. Mol Immunol 2004;41:355-367.
102. Gasque P, Julen N, Ischenko AM, Picot C, Mauger C, Chauzy C, et al. Expression of complement components of the alternative pathway by glioma cell lines. J Immunol 1992;149:1381-1387.
103. Katz Y, Guterman M, Lahat E. Regulation of synthesis of complement proteins in HEp2 cells. Clin Immunol Immunopathol 1993;67:117-123.
104. Legoedec J, Gasque P, Jeanne JF, Fontaine M. Expression of the complement alternative pathway by human myoblasts in vitro: biosynthesis of C3, factor B, factor H and factor I. Eur J Immunol 1995;25:3460-3466.
105. Gasque P, Thomas A, Fontaine M, Morgan BP. Complement activation on human neuroblastoma cell lines in vitro: route of activation and expression of functional complement regulatory proteins. J Neuroimmunol 1996;66:29-40.
106. Kinders R, Jones T, Root R, Bruce C, Murchison H, Corey M, et al. Complement factor H or a related protein is a marker for transitional cell cancer of the bladder. Clin Cancer Res 1998;4:2511-2520.
107. Junnikkala S, Hakulinen J, Jarva H, Manuelian T, Bjorge L, Butzow R, et al. Secretion of soluble complement inhibitors factor H and factor H-like protein (FHL-1) by ovarian tumour cells. Br J Cancer 2002;87:1119- 1127.
108. Cheng ZZ, Corey MJ, Parepalo M, Majno S, Hellwage J, Zipfel PF, et al. Complement factor H as a marker for detection of bladder cancer. Clin Chem 2005;51:856-863.
109. Maenpaa A, Junnikkala S, Hakulinen J, Timonen T, Meri S. Expression of complement membrane regulators membrane cofactor protein (CD46), decay accelerating factor (CD55), and protectin (CD59) in human malignant gliomas. Am J Pathol 1996;148: 1139-1152.
110. Corey MJ, Kinders RJ, Brown LG, Vessella RL. A very sensitive coupled luminescent assay for cytotoxicity and complement-mediated lysis. J Immunol Methods 1997;207:43-51.
111. Fedarko NS, Fohr B, Robey PG, Young MF, Fisher LW. Factor H binding to bone sialoprotein and osteopontin enables tumor cell evasion of complement-mediated attack. J Biol Chem 2000;275: 16666-16672.
112. Jain A, Karadag A, Fohr B, Fisher LW, Fedarko NS. Three SIBLINGs (small integrin-binding ligand, N-linked glycoproteins) enhance factor H's cofactor activity enabling MCP-like cellular evasion of complement-mediated attack. J Biol Chem 2002;277:13700-13708.
113. Gorter A, Blok VT, Haasnoot WH, Ensink NG, Daha MR, Fleuren GJ. Expression of CD46, CD55, and CD59 on renal tumor cell lines and their role in preventing complement-mediated tumor cell lysis. Lab Invest 1996;74:1039-1049.
114. Battistelli S, Victoria A, Cappelli R, Stefanoni M, Roviello F. Protein S in cancer patients with non-metastatic solid tumours. Eur J Surg Oncol 2005;31:798-802.
115. Holmberg MT, Blom AM, Meri S. Regulation of complement classical pathway by association of C4b-binding protein to the surfaces of SK-OV-3 and Caov-3 ovarian adenocarcinoma cells. J Immunol 2001;167:935-939.
116. Morris KM, Aden DP, Knowles BB, Colten HR. Complement biosynthesis by the human hepatoma-derived cell line HepG2. J Clin Invest 1982;70:906-913.
117. Buo L, Karlsrud TS, Dyrhaug G, Jacobsen MB, Bell H, Johansen HT, Aasen AO. Differential diagnosis of human ascites: inhibitors of the contact system and total proteins. Scand J Gastroenterol 1993;28:777-782.
118. Perricone R, De Carolis C, Giacomello F, Giacomelli R, De Sanctis G, Fontana L. Impaired human ovarian follicular fluid complement function in hereditary angioedema. Scand J Immunol 2000;51:104-108.
119. Trougakos IP, Gonos ES. Clusterin/apolipoprotein J in human aging and cancer. Int J Biochem Cell Biol 2002;34:1430-1448.
120. Harris M. Monoclonal antibodies as therapeutic agents for cancer. Lancet Oncol 2004;5:292-302.
121. Adams GP, Weiner LM. Monoclonal antibody therapy of cancer. Nat Biotechnol 2005;23:1147-1157.
122. Trikha M, Yan L, Nakada MT. Monoclonal antibodies as therapeutics in oncology. Curr Opin Biotechnol 2002;13:609-614.
123. Gelderman KA, Tomlinson S, Ross GD, Gorter A. Complement function in mAb-mediated cancer immunotherapy. Trends Immunol 2004;25:158-164.
124. Imai M, Landen C, Ohta R, Cheung NK, Tomlinson S. Complement-mediated mechanisms in anti-GD2 monoclonal antibody therapy of murine metastatic cancer. Cancer Res 2005;65:10562-10568.
125. Dillman RO. Treatment of low-grade B-cell lymphoma with the monoclonal antibody rituximab. Semin Oncol 2003;30:434-447.
126. Maloney DG, Smith B, Rose A. Rituximab: mechanism of action and resistance. Semin Oncol 2002;29:2-9.
127. 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;171:1581-1587.
128. Bellosillo B, Villamor N, Lopez-Guillermo A, Marce S, Esteve J, Campo E, et al. Complement-mediated cell death induced by rituximab in B-cell lymphoproliferative disorders is mediated in vitro by a caspase-independent mechanism involving the generation of reactive oxygen species. Blood 2001;98:2771-2777.
129. Bannerji R, Kitada S, Flinn IW, Pearson M, Young D, Reed JC, Byrd JC. Apoptotic-regulatory and complement-protecting protein expression in chronic lymphocytic leukemia: relationship to in vivo rituximab resistance. J Clin Oncol 2003;21:1466-1471.
130. 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;98:1352-1357.
131. 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;95:3900-3908.
132. Cardarelli PM, Quinn M, Buckman D, Fang Y, Colcher D, King DJ, et al. Binding to CD20 by anti-B1 antibody or F(ab′)(2) is sufficient for induction of apoptosis in B-cell lines. Cancer Immunol Immunother 2002;51:15-24.
133. Terui Y, Sakurai T, Mishima Y, Mishima Y, Sugimura N, Sasaoka C, et al. Blockade of bulky lymphoma-associated CD55 expression by RNA interference overcomes resistance to complement-dependent cytotoxicity with rituximab. Cancer Sci 2006;97:72-79.
134. Paganelli G, Magnani P, Zito F, Villa E, Sudati F, Lopalco L, et al. Three-step monoclonal antibody tumor targeting in carcinoembryonic antigen-positive patients. Cancer Res 1991;51: 5960-5966.
135. Macor P, Mezzanzanica D, Cossetti C, Alberti P, Figini M, Canevari S, Tedesco F. Complement activated by chimeric anti-folate receptor antibodies is an efficient effector system to control ovarian carcinoma. Cancer Res 2006;66:3876-3883.
136. Gelderman KA, Kuppen PJ, Bruin W, Fleuren GJ, Gorter A. Enhancement of the complement activating capacity of 17-1A mAb to overcome the effect of membrane-bound complement regulatory proteins on colorectal carcinoma. Eur J Immunol 2002;32: 128-135.
137. Gelderman KA, Lam S, Gorter A. Inhibiting complement regulators in cancer immunotherapy with bispecific mAbs. Expert Opin Biol Ther 2005;5:1593-1601.
138. Junnikkala S, Hakulinen J, Meri S. Targeted neutralization of the complement membrane attack complex inhibitor CD59 on the surface of human melanoma cells. Eur J Immunol 1994;24:611-615.
139. Harris CL, Kan KS, Stevenson GT, Morgan BP. Tumour cell killing using chemically engineered antibody constructs specific for tumour cells and the complement inhibitor CD59. Clin Exp Immunol 1997;107:364-371.
140. Blok VT, Daha MR, Tijsma O, Harris CL, Morgan BP, Fleuren GJ, Gorter A. A bispecific monoclonal antibody directed against both the membrane-bound complement regulator CD55 and the renal tumor-associated antigen G250 enhances C3 deposition and tumor cell lysis by complement. J Immunol 1998;160:3437-3443.
141. 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;64:4366-4372.
142. Blok VT, Gelderman KA, Tijsma OH, Daha MR, Gorter A. Cytokines affect resistance of human renal tumour cells to complement-mediated injury. Scand J Immunol 2003;57:591-599.
143. Bjorge L, Jensen TS, Ulvestad E, Vedeler CA, Matre R. The influence of tumour necrosis factor-alpha, interleukin-1 beta and interferon-gamma on the expression and function of the complement regulatory protein CD59 on the human colonic adenocarcinoma cell line HT29. Scand J Immunol 1995;41:350-356.
144. Andoh A, Fujiyama Y, Sumiyoshi K, Sakumoto H, Bamba T. Interleukin 4 acts as an inducer of decay-accelerating factor gene expression in human intestinal epithelial cells. Gastroenterology 1996;111:911-918.
145. Blom DJ, Goslings WR, De Waard-Siebinga I, Luyten GP, Claas FH, Gorter A, Jager MJ. Lack of effect of different cytokines on expression of membrane-bound regulators of complement activity on human uveal melanoma cells. J Interferon Cytokine Res 1997;17: 695-700.
146. Varsano S, Rashkovsky L, Shapiro H, Radnay J. Cytokines modulate expression of cell-membrane complement inhibitory proteins in human lung cancer cell lines. Am J Respir Cell Mol Biol 1998;19: 522-529.
147. Pasch MC, Bos JD, Daha MR, Asghar SS. Transforming growth factor-beta isoforms regulate the surface expression of membrane cofactor protein (CD46) and CD59 on human keratinocytes. Eur J Immunol 1999;29:100-108.
148. Spiller OB, Criado-Garcia O, Rodriguez De Cordoba S, Morgan BP. Cytokine-mediated up-regulation of CD55 and CD59 protects human hepatoma cells from complement attack. Clin Exp Immunol 2000;121:234-241.
149. Varsano S, Kaminsky M, Kaiser M, Rashkovsky L. Generation of complement C3 and expression of cell membrane complement inhibitory proteins by human bronchial epithelium cell line. Thorax 2000;55:364-369.
150. Bjorge L, Matre R. Down-regulation of CD59 (protectin) expression on human colorectal adenocarcinoma cell lines by levamisole. Scand J Immunol 1995;42:512-516.
151. Di Gaetano N, Xiao Y, Erba E, Bassan R, Rambaldi A, Golay J, Introna M. Synergism between fludarabine and rituximab revealed in a follicular lymphoma cell line resistant to the cytotoxic activity of either drug alone. Br J Haematol 2001;114:800-809.
152. Andoh A, Shimada M, Araki Y, Fujiyama Y, Bamba T. Sodium butyrate enhances complement-mediated cell injury via down-regulation of decay-accelerating factor expression in colonic cancer cells. Cancer Immunol Immunother 2002;50:663-672.
153. Nagajothi N, Matsui WH, Mukhina GL, Brodsky RA. Enhanced cytotoxicity of rituximab following genetic and biochemical disruption of glycosylphosphatidylinositol anchored proteins. Leuk Lymphoma 2004;45:795-799.
154. Kock MA, Hew BE, Bammert H, Fritzinger DC, Vogel CW. Structure and function of recombinant cobra venom factor. J Biol Chem 2004;279:30836-30843.
155. Juhl H, Petrella EC, Cheung NK, Bredehorst R, Vogel CW. Complement killing of human neuroblastoma cells: a cytotoxic monoclonal antibody and its F(ab′)2-cobra venom factor conjugate are equally cytotoxic. Mol Immunol 1990;27:957-964.
156. Juhl H, Petrella EC, Cheung NK, Bredehorst R, Vogel CW. Additive cytotoxicity of different monoclonal antibody-cobra venom factor conjugates for human neuroblastoma cells. Immunobiology 1997;197:444-459.
157. Juhl H, Sievers M, Baltzer K, Helmig F, Wolf H, Brenner W, Kalthoff H. A monoclonal antibody-cobra venom factor conjugate increases the tumor-specific uptake of a 99mTc-labeled anti-carcinoembryonic antigen antibody by a two-step approach. Cancer Res 1995;55: 5749s-5755s.
158. Yefenof E, Zehavi-Feferman R, Guy R. Control of primary and secondary antibody responses by cytotoxic T lymphocytes specific for a soluble antigen. Eur J Immunol 1990;20:1849-1853.
159. Kennedy AD, Solga MD, Schuman TA, CM AW, Lindorfer MA, Sutherland WM, et al. An anti-C3b(i) mAb enhances complement activation, C3b(i) deposition, and killing of CD20+ cells by rituximab. Blood 2003;101:1071-1079.
160. Holliger P, Wing M, Pound JD, Bohlen H, Winter G. Retargeting serum immunoglobulin with bispecific diabodies. Nat Biotechnol 1997;15:632-636.
161. 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;98:3383-3389.
162. 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;30:625-631.
163. Spiridon CI, Ghetie MA, Uhr J, Marches R, Li JL, Shen GL, Vitetta ES. Targeting multiple Her-2 epitopes with monoclonal antibodies results in improved antigrowth activity of a human breast cancer cell line in vitro and in vivo. Clin Cancer Res 2002;8:1720-1730.
164. Schuster M, Umana P, Ferrara C, Brunker P, Gerdes C, Waxenecker G, et al.
165. Ragupathi G, Liu NX, Musselli C, Powell S, Lloyd K, Livingston PO. Antibodies against tumor cell glycolipids and proteins, but not mucins, mediate complement-dependent cytotoxicity. J Immunol 2005;174:5706-5712.
166. Livingston PO, Hood C, Krug LM, Warren N, Kris MG, Brezicka T, Ragupathi G. Selection of GM2, fucosyl GM1, globo H and polysialic acid as targets on small cell lung cancers for antibody mediated immunotherapy. Cancer Immunol Immunother 2005;54: 1018-1025.
167. Imai M, Ohta R, Okada N, Tomlinson S. Inhibition of a complement regulator in vivo enhances antibody therapy in a model of mammary adenocarcinoma. Int J Cancer 2004;110:875-881.
168. Gelderman KA, Hakulinen J, Hagenaars M, Kuppen PJ, Meri S, Gorter A. Membrane-bound complement regulatory proteins inhibit complement activation by an immunotherapeutic mAb in a syngeneic rat colorectal cancer model. Mol Immunol 2003;40:13-23.