Prenyltransferases regulate CD20 protein levels and influence anti-CD20 monoclonal antibody-mediated activation of complement-dependent cytotoxicity

Journal of Biological Chemistry

Volumn 287, Issue 38, 2012, Pages 31983-31993

  Winiarska, Magdalena ^a   Nowis, Dominika ^a   Bil, Jacek ^a,b   Glodkowska Mrowka, Eliza ^a   Muchowicz, Angelika ^a   Wanczyk, Malgorzata ^a   Bojarczuk, Kamil ^a   Dwojak, Michal ^a   Firczuk, Malgorzata ^a   Wilczek, Ewa ^a   Wachowska, Malgorzata ^a   Roszczenko, Katarzyna ^a   Miaczynska, Marta ^c   Chlebowska, Justyna ^a   Basak, Grzegorz Wladyslaw ^d   Golab, Jakub ^a,e  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b CENTRAL CLINICAL HOSPITAL   (Poland)

^c INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^d MEDICAL UNIVERSITY OF WARSAW   (Poland)

^e INSTITUTE OF PHYSICAL CHEMISTRY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-TUMOR ACTIVITIES; CHROMATIN IMMUNOPRECIPITATION ASSAY; CHRONIC LYMPHOCYTIC LEUKEMIAS; COMPLEMENT-DEPENDENT CYTOTOXICITIES; CONFORMATIONAL CHANGE; FARNESYLTRANSFERASE; MONOCLONAL ANTIBODIES (MABS); NON-HODGKIN LYMPHOMA; PROMOTER SEQUENCES; PROTEIN LEVEL; RAJI CELLS; STATINS; TUMOR CELLS; UP-REGULATION;

DISEASES; MONOCLONAL ANTIBODIES; TUMORS;

CYTOTOXICITY;

2 [[2 [[2 [(2 AMINO 3 MERCAPTOPROPYL)AMINO] 3 METHYLPENTYL]OXY] 1 OXO 3 PHENYLPROPYL]AMINO] 4 (METHYLSULFONYL)BUTANOIC ACID ISOPROPYL ESTER; CD20 ANTIBODY; CD20 ANTIGEN; DIMETHYLALLYLTRANSFERASE; GGTI 2133; GGTI 286; GGTI 298; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; OCTAMER TRANSCRIPTION FACTOR 2; OFATUMUMAB; PROTEIN FARNESYLTRANSFERASE INHIBITOR; RITUXIMAB; TRANSCRIPTION FACTOR PU 1; TRANSFERASE INHIBITOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ISOLATION; CHROMATIN IMMUNOPRECIPITATION; CHRONIC LYMPHATIC LEUKEMIA; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; DRUG EFFICACY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LYMPHOMA CELL; NONHODGKIN LYMPHOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; RAJI CELL; TUMOR CELL; UPREGULATION;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD20; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; COMPLEMENT SYSTEM PROTEINS; DIMETHYLALLYLTRANSTRANSFERASE; ENZYME INHIBITORS; FARNESYLTRANSTRANSFERASE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; LYMPHOMA, B-CELL; METHIONINE; PROMOTER REGIONS, GENETIC;

EID: 84866368767     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.374751     Document Type: Article

References (41)

1. Bezombes, C., Fournié, J. J., and Laurent, G. (2011) Direct effect of rituximab in B-cell-derived lymphoid neoplasias: mechanism, regulation, and perspectives. Mol. Cancer Res. 9, 1435-1442
2. Winiarska, M., Glodkowska-Mrowka, E., Bil, J., and Golab, J. (2011) Molecular mechanisms of the antitumor effects of anti-CD20 antibodies. Front. Biosci. 16, 277-306
3. Hainsworth, J. D., Litchy, S., Shaffer, D. W., Lackey, V. L., Grimaldi, M., and Greco, F. A. (2005) Maximizing therapeutic benefit of rituximab: maintenance therapy versus re-treatment at progression in patients with indolent non-Hodgkin's lymphoma - a randomized phase II trial of the Minnie Pearl Cancer Research Network. J. Clin. Oncol. 23, 1088-1095 (Pubitemid 46202263)
4. McLaughlin, P., Grillo-López, A. J., Link, B. K., Levy, R., Czuczman, M. S., Williams, M. E., Heyman, M. R., Bence-Bruckler, I., White, C. A., Cabanillas, F., Jain, V., Ho, A. D., Lister, J., Wey, K., Shen, D., and Dallaire, B. K. (1998) Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J. Clin. Oncol. 16, 2825-2833 (Pubitemid 28363048)
5. Golay, J., Lazzari, M., Facchinetti, V., Bernasconi, S., Borleri, G., Barbui, T., Rambaldi, A., and Introna, M. (2001) CD20 levels determine the in vitro susceptibility to rituximab and complement of B-cell chronic lymphocytic leukemia: further regulation by CD55 and CD59. Blood 98, 3383-3389
6. Bellosillo, B., Villamor, N., López-Guillermo, A., Marcé, S., Esteve, J., Campo, E., Colomer, D., and Montserrat, E. (2001) 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 98, 2771-2777
7. van Meerten, T., van Rijn, R. S., Hol, S., Hagenbeek, A., and Ebeling, S. B. (2006) Complement-induced cell death by rituximab depends on CD20 expression level and acts complementary to antibody-dependent cellular cytotoxicity. Clin. Cancer Res. 12, 4027-4035 (Pubitemid 44078090)
8. Seliem, R. M., Freeman, J. K., Steingart, R. H., and Hasserjian, R. P. (2006) Immunophenotypic changes and clinical outcome in B-cell lymphomas treated with rituximab. Appl. Immunohistochem. Mol. Morphol. 14, 18-23
9. Davis, T. A., Czerwinski, D. K., and Levy, R. (1999) Therapy of B-cell lymphoma with anti-CD20 antibodies can result in the loss of CD20 antigen expression. Clin. Cancer Res. 5, 611-615 (Pubitemid 29131971)
10. Foran, J. M., Norton, A. J., Micallef, I. N., Taussig, D. C., Amess, J. A., Rohatiner, A. Z., and Lister, T. A. (2001) Loss of CD20 expression following treatment with rituximab (chimaeric monoclonal anti-CD20): a retrospective cohort analysis. Br. J. Haematol. 114, 881-883 (Pubitemid 32953749)
11. Schmitz, K., Brugger, W., Weiss, B., Kaiserling, E., and Kanz, L. (1999) Clonal selection of CD20-negative non-Hodgkin's lymphoma cells after treatment with anti-CD20 antibody rituximab. Br. J. Haematol. 106, 571-572 (Pubitemid 29450692)
12. Kinoshita, T., Nagai, H., Murate, T., and Saito, H. (1998) CD20-negative relapse in B-cell lymphoma after treatment with rituximab. J. Clin. Oncol. 16, 3916 (Pubitemid 29001546)
13. Haidar, J. H., Shamseddine, A., Salem, Z., Mrad, Y. A., Nasr, M. R., Zaatari, G., and Bazarbachi, A. (2003) Loss of CD20 expression in relapsed lymphomas after rituximab therapy. Eur. J. Haematol. 70, 330-332 (Pubitemid 36560534)
14. Maeshima, A. M., Taniguchi, H., Nomoto, J., Maruyama, D., Kim, S. W., Watanabe, T., Kobayashi, Y., Tobinai, K., and Matsuno, Y. (2009) Histological and immunophenotypic changes in 59 cases of B-cell non-Hodgkin's lymphoma after rituximab therapy. Cancer Sci. 100, 54-61
15. Hiraga, J., Tomita, A., Sugimoto, T., Shimada, K., Ito, M., Nakamura, S., Kiyoi, H., Kinoshita, T., and Naoe, T. (2009) Down-regulation of CD20 expression in B-cell lymphoma cells after treatment with rituximab-containing combination chemotherapies: its prevalence and clinical significance. Blood 113, 4885-4893
16. Jilani, I., O'Brien, S., Manshuri, T., Thomas, D. A., Thomazy, V. A., Imam, M., Naeem, S., Verstovsek, S., Kantarjian, H., Giles, F., Keating, M., and Albitar, M. (2003) Transient down-modulation of CD20 by rituximab in patients with chronic lymphocytic leukemia. Blood 102, 3514-3520 (Pubitemid 37419939)
17. Pickartz, T., Ringel, F., Wedde, M., Renz, H., Klein, A., von Neuhoff, N., Dreger, P., Kreuzer, K. A., Schmidt, C. A., Srock, S., Schoeler, D., and Schriever, F. (2001) Selection of B-cell chronic lymphocytic leukemia cell variants by therapy with anti-CD20 monoclonal antibody rituximab. Exp. Hematol. 29, 1410-1416 (Pubitemid 34013487)
18. Mankaï, A., Bordron, A., Renaudineau, Y., Martins-Carvalho, C., Takahashi, S., Ghedira, I., Berthou, C., and Youinou, P. (2008) Purine-rich box-1-mediated reduced expression of CD20 alters rituximab-induced lysis of chronic lymphocytic leukemia B cells. Cancer Res. 68, 7512-7519
19. Beum, P. V., Kennedy, A. D., Williams, M. E., Lindorfer, M. A., and Taylor, R. P. (2006) The shaving reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. J. Immunol. 176, 2600-2609 (Pubitemid 43201712)
20. Beers, S. A., French, R. R., Chan, H. T., Lim, S. H., Jarrett, T. C., Vidal, R. M., Wijayaweera, S. S., Dixon, S. V., Kim, H., Cox, K. L., Kerr, J. P., Johnston, D. A., Johnson, P. W., Verbeek, J. S., Glennie, M. J., and Cragg, M. S. (2010) Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood 115, 5191-5201
21. Ushmorov, A., Leithäuser, F., Sakk, O., Weinhaüsel, A., Popov, S. W., Möller, P., and Wirth, T. (2006) Epigenetic processes play a major role in B-cell-specific gene silencing in classical Hodgkin lymphoma. Blood 107, 2493-2500 (Pubitemid 43345573)
22. Tomita, A., Hiraga, J., Kiyoi, H., Ninomiya, M., Sugimoto, T., Ito, M., Kinoshita, T., and Naoe, T. (2007) Epigenetic regulation of CD20 protein expression in a novel B-cell lymphoma cell line, RRBL1, established from a patient treated repeatedly with rituximab-containing chemotherapy. Int. J. Hematol. 86, 49-57 (Pubitemid 47204490)
23. Winiarska, M., Bil, J., Wilczek, E., Wilczynski, G. M., Lekka, M., Engelberts, P. J., Mackus, W. J., Gorska, E., Bojarski, L., Stoklosa, T., Nowis, D., Kurzaj, Z., Makowski, M., Glodkowska, E., Issat, T., Mrowka, P., Lasek, W., Dabrowska-Iwanicka, A., Basak, G. W., Wasik, M., Warzocha, K., Sinski, M., Gaciong, Z., Jakobisiak, M., Parren, P. W., and Golab, J. (2008) Statins impair antitumor effects of rituximab by inducing conformational changes of CD20. PLoS Med. 5, e64
24. Berndt, N., Hamilton, A. D., and Sebti, S. M. (2011) Targeting protein prenylation for cancer therapy. Nat. Rev. Cancer 11, 775-791
25. Witzig, T. E., Tang, H., Micallef, I. N., Ansell, S. M., Link, B. K., Inwards, D. J., Porrata, L. F., Johnston, P. B., Colgan, J. P., Markovic, S. N., Nowakowski, G. S., Thompson, C. A., Allmer, C., Maurer, M. J., Gupta, M., Weiner, G., Hohl, R., Kurtin, P. J., Ding, H., Loegering, D., Schneider, P., Peterson, K., Habermann, T. M., and Kaufmann, S. H. (2011) Multi-institutional phase 2 study of the farnesyltransferase inhibitor tipifarnib (R115777) in patients with relapsed and refractory lymphomas. Blood 118, 4882-4889
26. Henry, C., Deschamps, M., Rohrlich, P. S., Pallandre, J. R., Rémy-Martin, J. P., Callanan, M., Traverse-Glehen, A., GrandClément, C., Garnache-Ottou, F., Gressin, R., Deconinck, E., Salles, G., Robinet, E., Tiberghien, P., Borg, C., and Ferrand, C. (2010) Identification of an alternative CD20 transcript variant in B-cell malignancies coding for a novel protein associated to rituximab resistance. Blood 115, 2420-2429
27. Bil, J., Winiarska, M., Nowis, D., Bojarczuk, K., Dabrowska-Iwanicka, A., Basak, G. W., Su?ek, K., Jakobisiak, M., and Golab, J. (2010) Bortezomib modulates surface CD20 in B-cell malignancies and affects rituximab-mediated complement-dependent cytotoxicity. Blood 115, 3745-3755
28. Venugopal, P., Sivaraman, S., Huang, X. K., Nayini, J., Gregory, S. A., and Preisler, H. D. (2000) Effects of cytokines on CD20 antigen expression on tumor cells from patients with chronic lymphocytic leukemia. Leuk. Res. 24, 411-415 (Pubitemid 30227241)
29. Sivaraman, S., Venugopal, P., Ranganathan, R., Deshpande, C. G., Huang, X., Jajeh, A., Gregory, S. A., O'Brien, T., and Preisler, H. D. (2000) Effect of interferon-α on CD20 antigen expression of B-cell chronic lymphocytic leukemia. Cytokines Cell. Mol. Ther. 6, 81-87
30. Wojciechowski, W., Li, H., Marshall, S., Dell'Agnola, C., and Espinoza-Delgado, I. (2005) Enhanced expression of CD20 in human tumor B cells is controlled through ERK-dependent mechanisms. J. Immunol. 174, 7859-7868 (Pubitemid 40806295)
31. Mankaï, A., Buhé, V., Hammadi, M., Youinou, P., Ghedira, I., Berthou, C., and Bordron, A. (2009) Improvement of rituximab efficiency in chronic lymphocytic leukemia by CpG-mediated upregulation of CD20 expression independently of PU.1. Ann. N.Y. Acad. Sci. 1173, 721-728
32. Czuczman, M. S., Olejniczak, S., Gowda, A., Kotowski, A., Binder, A., Kaur, H., Knight, J., Starostik, P., Deans, J., and Hernandez-Ilizaliturri, F. J. (2008) Acquirement of rituximab resistance in lymphoma cell lines is associated with both global CD20 gene and protein down-regulation regulated at the pretranscriptional and posttranscriptional levels. Clin. Cancer Res. 14, 1561-1570 (Pubitemid 351413941)
33. Efuet, E. T., and Keyomarsi, K. (2006) Farnesyl and geranylgeranyl transferase inhibitors induceG1 arrest by targeting the proteasome. Cancer Res. 66, 1040-1051 (Pubitemid 43165972)
34. Michel, R. B., and Mattes, M. J. (2002) Intracellular accumulation of the anti-CD20 antibody 1F5 in B-lymphoma cells. Clin. Cancer Res. 8, 2701-2713 (Pubitemid 34856360)
35. Michel, R. B., Ochakovskaya, R., and Mattes, M. J. (2002) Antibody localization to B-cell lymphoma xenografts in immunodeficient mice: importance of using residualizing radiolabels. Clin. Cancer Res. 8, 2632-2639 (Pubitemid 34856351)
36. Turzanski, J., Daniels, I., and Haynes, A. P. (2008) Internalisation of uncross-linked rituximab is not essential for the induction of caspase-independent killing in Burkitt lymphoma cell lines. Leuk. Lymphoma 49, 1578-1591
37. Anolik, J., Looney, R. J., Bottaro, A., Sanz, I., and Young, F. (2003) Downregulation of CD20 on B cells upon CD40 activation. Eur. J. Immunol. 33, 2398-2409 (Pubitemid 37138972)
38. Lapalombella, R., Yu, B., Triantafillou, G., Liu, Q., Butchar, J. P., Lozanski, G., Ramanunni, A., Smith, L. L., Blum, W., Andritsos, L., Wang, D. S., Lehman, A., Chen, C. S., Johnson, A. J., Marcucci, G., Lee, R. J., Lee, L. J., Tridandapani, S., Muthusamy, N., and Byrd, J. C. (2008) Lenalidomide down-regulates the CD20 antigen and antagonizes direct and antibody-dependent cellular cytotoxicity of rituximab on primary chronic lymphocytic leukemia cells. Blood 112, 5180-5189
39. Tsai, P. C., Hernandez-Ilizaliturri, F. J., Bangia, N., Olejniczak, S. H., and Czuczman, M. S. (2012) Regulation of CD20 in rituximab-resistant cell lines and B-cell non-Hodgkin lymphoma. Clin. Cancer Res. 18, 1039-1050
40. Adjei, A. A., Mauer, A., Bruzek, L., Marks, R. S., Hillman, S., Geyer, S., Hanson, L. J., Wright, J. J., Erlichman, C., Kaufmann, S. H., and Vokes, E. E. (2003) Phase II study of the farnesyl transferase inhibitor R115777 in patients with advanced non-small-cell lung cancer. J. Clin. Oncol. 21, 1760-1766 (Pubitemid 46638589)
41. Alsina, M., Fonseca, R., Wilson, E. F., Belle, A. N., Gerbino, E., Price-Troska, T., Overton, R. M., Ahmann, G., Bruzek, L. M., Adjei, A. A., Kaufmann, S. H., Wright, J. J., Sullivan, D., Djulbegovic, B., Cantor, A. B., Greipp, P. R., Dalton, W. S., and Sebti, S. M. (2004) Farnesyltransferase inhibitor tipifarnib is well tolerated, induces stabilization of disease, and inhibits farnesylation and oncogenic/tumor survival pathways in patients with advanced multiple myeloma. Blood 103, 3271-3277 (Pubitemid 38525650)