Rapid degradation of the complement regulator, CD59, by a novel inhibitor

Journal of Biological Chemistry

Volumn 289, Issue 17, 2014, Pages 12109-12125

  Cai, Bishuang ^a   Xie, Shuwei ^a   Liu, Fengming ^b   Simone, Laura C ^a   Caplan, Steve ^a   Qin, Xuebin ^b   Naslavsky, Naava ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

BACTERIAL TOXIN; CANCER CELLS; GLYCOSYLPHOSPHATIDYLINOSITOL-ANCHORED PROTEINS; INHIBITORY ACTIVITY; LUNG CARCINOMA; NON-TOXIC; RAPID DEGRADATION; SURFACE EXPRESSION;

PROTEINS;

BACTERIAL TOXIN; CD59 ANTIGEN; RECOMBINANT INTERMEDILYSIN 4TH DOMAIN; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BIOTINYLATION; CANCER CELL; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; INTERNALIZATION; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; STREPTOCOCCUS INTERMEDIUS;

BACTERIAL TOXIN; CD59; COMPLEMENT; DEGRADATION; ENDOCYTOSIS; ENDOSOMES; GLYCOSYL PHOSPHATIDYLINOSITOL ANCHORS; INTRACELLULAR TRAFFICKING; LYSOSOMES; SHEDDING;

ANTIGENS, CD59; CELL LINE, TUMOR; ENDOCYTOSIS; HUMANS; HYDROLYSIS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84899447630     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.547083     Document Type: Article

References (47)

1. Ricklin, D., and Lambris, J. D. (2013) Complement in immune and inflammatory disorders: therapeutic interventions. J. Immunol. 190, 3839-3847
2. Gorter, A., and Meri, S. (1999) Immune evasion of tumor cells using membrane- bound complement regulatory proteins. Immunol. Today 20, 576-582
3. Meri, S., Morgan, B. P., Davies, A., Daniels, R. H., Olavesen, M. G., Waldmann, H., and Lachmann, P. J. (1990) Human protectin (CD59), an 18,000-20,000 MW complement lysis restricting factor, inhibits C5b-8 catalysed insertion of C9 into lipid bilayers. Immunology 71, 1-9 (Pubitemid 20296064)
4. Rollins, S. A., and Sims, P. J. (1990) The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J. Immunol. 144, 3478-3483 (Pubitemid 20146382)
5. Zalman, L. S., Wood, L. M., and Müller-Eberhard, H. J. (1987) Inhibition of antibody-dependent lymphocyte cytotoxicity by homologous restriction factor incorporated into target cell membranes. J. Exp. Med. 166, 947-955 (Pubitemid 18024237)
6. Yamashina, M., Ueda, E., Kinoshita, T., Takami, T., Ojima, A., Ono, H., Tanaka, H., Kondo, N., Orii, T., and Okada, N. (1990) Inherited complete deficiency of 20-kilodalton homologous restriction factor (CD59) as a cause of paroxysmal nocturnal hemoglobinuria. N. Engl. J. Med. 323, 1184-1189 (Pubitemid 20347405)
7. Golay, J., Zaffaroni, L., Vaccari, T., Lazzari, M., Borleri, G. M., Bernasconi, S., Tedesco, F., Rambaldi, A., and Introna, M. (2000) Biologic response of B lymphoma cells to anti-CD20 monoclonal antibody rituximab in vitro: CD55 and CD59 regulate complement-mediated cell lysis. Blood 95, 3900-3908 (Pubitemid 30412866)
8. You, T., Hu, W., Ge, X., Shen, J., and Qin, X. (2011) Application of a novel inhibitor of human CD59 for the enhancement of complement-dependent cytolysis on cancer cells. Cell Mol. Immunol. 8, 157-163
9. Bjørge, L., Hakulinen, J., Wahlström, T., Matre, R., and Meri, S. (1997) Complement-regulatory proteins in ovarian malignancies. Int. J. Cancer 70, 14-25 (Pubitemid 27059700)
10. Juhl, H., Helmig, F., Baltzer, K., Kalthoff, H., Henne-Bruns, D., and Kremer, B. (1997) Frequent expression of complement resistance factors CD46, CD55, and CD59 on gastrointestinal cancer cells limits the therapeutic potential of monoclonal antibody 17-1A. J. Surg. Oncol. 64, 222-230 (Pubitemid 27157412)
11. Jarvis, G. A., Li, J., Hakulinen, J., Brady, K. A., Nordling, S., Dahiya, R., and Meri, S. (1997) Expression and function of the complement membrane attack complex inhibitor protectin (CD59) in human prostate cancer. Int. J. Cancer 71, 1049-1055 (Pubitemid 27252889)
12. Coral, S., Fonsatti, E., Sigalotti, L., De Nardo, C., Visintin, A., Nardi, G., Colizzi, F., Colombo, M. P., Romano, G., Altomonte, M., and Maio, M. (2000) Overexpression of protectin (CD59) down-modulates the susceptibility of human melanoma cells to homologous complement. J. Cell. Physiol. 185, 317-323
13. Fonsatti, E., Altomonte, M., Coral, S., De Nardo, C., Lamaj, E., Sigalotti, L., Natali, P. G., and Maio, M. (2000) Emerging role of protectin (CD59) in humoral immunotherapy of solid malignancies. Clin. Ter. 151, 187-193
14. Kolev, M., Towner, L., and Donev, R. (2011) Complement in cancer and cancer immunotherapy. Arch. Immunol. Ther. Exp. (Warsz) 59, 407-419
15. Yan, J., Allendorf, D. J., Li, B., Yan, R., Hansen, R., and Donev, R. (2008) The role of membrane complement regulatory proteins in cancer immunotherapy. Adv. Exp. Med. Biol. 632, 159-174
16. Wang, S. Y., and Weiner, G. (2008) Complement and cellular cytotoxicity in antibody therapy of cancer. Expert Opin. Biol. Ther. 8, 759-768 (Pubitemid 351860205)
17. Zhou, X., Hu, W., and Qin, X. (2008) The role of complement in the mechanism of action of rituximab for B-cell lymphoma: implications for therapy. Oncologist 13, 954-966
18. Ajona, D., Hsu, Y. F., Corrales, L., Montuenga, L. M., and Pio, R. (2007) Down-regulation of human complement factor H sensitizes non-small cell lung cancer cells to complement attack and reduces in vivo tumor growth. J. Immunol. 178, 5991-5998 (Pubitemid 46674397)
19. Johnston, J. B., Navaratnam, S., Pitz, M. W., Maniate, J. M., Wiechec, E., Baust, H., Gingerich, J., Skliris, G. P., Murphy, L. C., and Los, M. (2006) Targeting the EGFR pathway for cancer therapy. Curr. Med. Chem. 13, 3483-3492 (Pubitemid 44873742)
20. Zhao, W. P., Zhu, B., Duan, Y. Z., and Chen, Z. T. (2009) Neutralization of complement regulatory proteins CD55 and CD59 augments therapeutic effect of herceptin against lung carcinoma cells. Oncol. Rep. 21, 1405-1411
21. Ziller, F., Macor, P., Bulla, R., Sblattero, D., Marzari, R., and Tedesco, F. (2005) Controlling complement resistance in cancer by using human monoclonal antibodies that neutralize complement-regulatory proteins CD55 and CD59. Eur. J. Immunol. 35, 2175-2183 (Pubitemid 41015056)
22. Macor, P., Tripodo, C., Zorzet, S., Piovan, E., Bossi, F., Marzari, R., Amadori, A., and Tedesco, F. (2007) In vivo targeting of human neutralizing antibodies against CD55 and CD59 to lymphoma cells increases the antitumor activity of rituximab. Cancer Res. 67, 10556-10563 (Pubitemid 350070832)
23. Giddings, K. S., Zhao, J., Sims, P. J., and Tweten, R. K. (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat. Struct. Mol. Biol. 11, 1173-1178
24. Wickham, S. E., Hotze, E. M., Farrand, A. J., Polekhina, G., Nero, T. L., Tomlinson, S., Parker, M. W., and Tweten, R. K. (2011) Mapping the intermedilysin-human CD59 receptor interface reveals a deep correspondence with the binding site on CD59 for complement binding proteins C8α and C9. J. Biol. Chem. 286, 20952-20962
25. Hu, W., Yu, Q., Hu, N., Byrd, D., Amet, T., Shikuma, C., Shiramizu, B., Halperin, J. A., and Qin, X. (2010) A high-affinity inhibitor of human CD59 enhances complement-mediated virolysis of HIV-1: implications for treatment of HIV-1/AIDS. J. Immunol. 184, 359-368
26. Hu, W., Ge, X., You, T., Xu, T., Zhang, J., Wu, G., Peng, Z., Chorev, M., Aktas, B. H., Halperin, J. A., Brown, J. R., and Qin, X. (2011) Human CD59 inhibitor sensitizes rituximab-resistant lymphoma cells to complementmediated cytolysis. Cancer Res. 71, 2298-2307
27. Ge, X., Wu, L., Hu, W., Fernandes, S., Wang, C., Li, X., Brown, J. R., and Qin, X. (2011) rILYd4, a human CD59 inhibitor, enhances complementdependent cytotoxicity of ofatumumab against rituximab-resistant B-cell lymphoma cells and chronic lymphocytic leukemia. Clin. Cancer Res. 17, 6702-6711
28. Cai, B., Caplan, S., and Naslavsky, N. (2012) cPLA2α and EHD1 interact and regulate the vesiculation of cholesterol-rich, GPI-anchored, proteincontaining endosomes. Mol. Biol. Cell 23, 1874-1888
29. Cai, B., Katafiasz, D., Horejsi, V., and Naslavsky, N. (2011) Pre-sorting endosomal transport of the GPI-anchored protein, CD59, is regulated by EHD1. Traffic 12, 102-120
30. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232 (Pubitemid 46010930)
31. Wu, L., Su, S., Liu, F., Xu, T., Wang, X., Huang, Y., Sun, X., Ge, X., Chen, T., Liu, H., Wang, C., Chorev, M., Xu, T., and Qin, X. (2012) Removal of the tag from His-tagged ILYd4, a human CD59 inhibitor, significantly improves its physical properties and its activity. Curr. Pharm. Des. 18, 4187-4196
32. Lauc, G., and Heffer-Lauc, M. (2006) Shedding and uptake of gangliosides and glycosylphosphatidylinositol-anchored proteins. Biochim. Biophys. Acta 1760, 584-602
33. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S., and Parton, R. G. (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465-476 (Pubitemid 40205068)
34. Doherty, G. J., and McMahon, H. T. (2009) Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902
35. Brown, D. A. (2007) Analysis of raft affinity of membrane proteins by detergent-insolubility. Methods Mol. Biol. 398, 9-20
36. Lundmark, R., Doherty, G. J., Howes, M. T., Cortese, K., Vallis, Y., Parton, R. G., and McMahon, H. T. (2008) The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr. Biol. 18, 1802-1808
37. Sabharanjak, S., Sharma, P., Parton, R. G., and Mayor, S. (2002) GPIanchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411-423 (Pubitemid 34436571)
38. Chadda, R., Howes, M. T., Plowman, S. J., Hancock, J. F., Parton, R. G., and Mayor, S. (2007) Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8, 702-717 (Pubitemid 46785152)
39. Cohen, D., Müsch, A., and Rodriguez-Boulan, E. (2001) Selective control of basolateral membrane protein polarity by cdc42. Traffic 2, 556-564 (Pubitemid 32725400)
40. Müsch, A., Cohen, D., Kreitzer, G., and Rodriguez-Boulan, E. (2001) cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J. 20, 2171-2179 (Pubitemid 32410587)
41. Naslavsky, N., Weigert, R., and Donaldson, J. G. (2004) Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15, 3542-3552 (Pubitemid 38989695)
42. Kalia, M., Kumari, S., Chadda, R., Hill, M. M., Parton, R. G., and Mayor, S. (2006) Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol- 3'-kinase-dependent machinery. Mol. Biol. Cell 17, 3689-3704 (Pubitemid 44156459)
43. Ullrich, O., Reinsch, S., Urbé, S., Zerial, M., and Parton, R. G. (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924 (Pubitemid 26403768)
44. Mohrmann, K., and van der Sluijs, P. (1999) Regulation of membrane transport through the endocytic pathway by rabGTPases. Mol. Membr. Biol. 16, 81-87 (Pubitemid 29179341)
45. Perez-Torres, M., Valle, B. L., Maihle, N. J., Negron-Vega, L., Nieves- Alicea, R., and Cora, E. M. (2008) Shedding of epidermal growth factor receptor is a regulated process that occurs with overexpression in malignant cells. Exp. Cell Res. 314, 2907-2918
46. Hayashi, H., and Yamashita, Y. (2012) Role of N-glycosylation in cell surface expression and protection against proteolysis of the intestinal anion exchanger SLC26A3. Am. J. Physiol. Cell Physiol. 302, C781-795
47. van Veen, H. A., Geerts, M. E., van Berkel, P. H., and Nuijens, J. H. (2004) The role of N-linked glycosylation in the protection of human and bovine lactoferrin against tryptic proteolysis. Eur. J. Biochem. 271, 678-684 (Pubitemid 38250910)