Dual functional BAFF receptor aptamers inhibit ligand-induced proliferation and deliver siRNAs to NHL cells

Nucleic Acids Research

Volumn 41, Issue 7, 2013, Pages 4266-4283

  Zhou, Jiehua ^a   Tiemann, Katrin ^a   Chomchan, Pritsana ^a   Alluin, Jessica ^a   Swiderski, Piotr ^a   Burnett, John ^a   Zhang, Xizhe ^a   Forman, Stephen ^a   Chen, Robert ^a   Rossi, John ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; B CELL ACTIVATING FACTOR RECEPTOR; DICER; MESSENGER RNA; SMALL INTERFERING RNA; STAT3 PROTEIN;

ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL; NONHODGKIN LYMPHOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING;

APTAMERS, NUCLEOTIDE; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; CELL LINE; CELL PROLIFERATION; HUMANS; L-SELECTIN; LIGANDS; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR;

EID: 84876526812     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt125     Document Type: Article

References (58)

1. Thompson, J.S., Bixler, S.A., Qian, F., Vora, K., Scott, M.L., Cachero, T.G., Hession, C., Schneider, P., Sizing, I.D., Mullen, C. et al. (2001) BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science, 293, 2108-2111. (Pubitemid 32848062)
2. Moore, P.A., Belvedere, O., Orr, A., Pieri, K., LaFleur, D.W., Feng, P., Soppet, D., Charters, M., Gentz, R., Parmelee, D. et al. (1999) BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science, 285, 260-263. (Pubitemid 29330000)
3. Gross, J.A., Johnston, J., Mudri, S., Enselman, R., Dillon, S.R., Madden, K., Xu, W., Parrish-Novak, J., Foster, D., Lofton-Day, C. et al. (2000) TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature, 404, 995-999. (Pubitemid 30243593)
4. Craxton, A., Magaletti, D., Ryan, E.J. and Clark, E.A. (2003) Macrophage-and dendritic cell-dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF. Blood, 101, 4464-4471. (Pubitemid 36857815)
5. Nimmanapalli, R., Lyu, M.A., Du, M., Keating, M.J., Rosenblum, M.G. and Gandhi, V. (2007) The growth factor fusion construct containing B-lymphocyte stimulator (BLyS) and the toxin rGel induces apoptosis specifically in BAFF-R-positive CLL cells. Blood, 109, 2557-2564. (Pubitemid 46425902)
6. Lyu, M.A., Cheung, L.H., Hittelman, W.N., Marks, J.W., Aguiar, R.C. and Rosenblum, M.G. (2007) The rGel/BLyS fusion toxin specifically targets malignant B-cells expressing the BLyS receptors BAFF-R, TACI, and BCMA. Mol. Cancer Ther., 6, 460-470. (Pubitemid 46332448)
7. Shulga-Morskaya, S., Dobles, M., Walsh, M.E., Ng, L.G., MacKay, F., Rao, S.P., Kalled, S.L. and Scott, M.L. (2004) Bcell-activating factor belonging to the TNF family acts through separate receptors to support B-cell survival and T cell-independent antibody formation. J. Immunol., 173, 2331-2341. (Pubitemid 39063089)
8. Thompson, J.S., Schneider, P., Kalled, S.L., Wang, L., Lefevre, E.A., Cachero, T.G., MacKay, F., Bixler, S.A., Zafari, M., Liu, Z.Y. et al. (2000) BAFF binds to the tumor necrosis factor receptor-like molecule B-cell maturation antigen and is important for maintaining the peripheral B-cell population. J. Exp. Med., 192, 129-135. (Pubitemid 30470814)
9. Batten, M., Groom, J., Cachero, T.G., Qian, F., Schneider, P., Tschopp, J., Browning, J.L. and Mackay, F. (2000) BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med., 192, 1453-1466.
10. Ju, Z.L., Shi, G.Y., Zuo, J.X. and Zhang, J.W. (2007) Unexpected development of autoimmunity in BAFF-R-mutant MRL-lpr mice. Immunology, 120, 281-289. (Pubitemid 46046326)
11. He, B., Chadburn, A., Jou, E., Schattner, E.J., Knowles, D.M. and Cerutti, A. (2004) Lymphoma B-cells evade apoptosis through the TNF family members BAFF/BLyS and APRIL. J. Immunol., 172, 3268-3279. (Pubitemid 38263719)
12. Novak, A.J., Grote, D.M., Stenson, M., Ziesmer, S.C., Witzig, T.E., Habermann, T.M., Harder, B., Ristow, K.M., Bram, R.J., Jelinek, D.F. et al. (2004) Expression of BLyS and its receptors in B-cell non-Hodgkin lymphoma: correlation with disease activity and patient outcome. Blood, 104, 2247-2253. (Pubitemid 39331819)
13. Kern, C., Cornuel, J.F., Billard, C., Tang, R., Rouillard, D., Stenou, V., Defrance, T., Ajchenbaum-Cymbalista, F., Simonin, P.Y., Feldblum, S. et al. (2004) Involvement of BAFF and APRIL in the resistance to apoptosis of B-CLL through an autocrine pathway. Blood, 103, 679-688. (Pubitemid 38145555)
14. Tecchio, C., Nadali, G., Scapini, P., Bonetto, C., Visco, C., Tamassia, N., Vassilakopoulos, T.P., Pangalis, G.A., Calzetti, F., Nardelli, B. et al. (2007) High serum levels of B-lymphocyte stimulator are associated with clinical-pathological features and outcome in classical Hodgkin lymphoma. Br. J. Haematol., 137, 553-559. (Pubitemid 46817342)
15. Siegel, R., Naishadham, D. and Jemal, A. (2012) Cancer statistics 2012. CA Cancer J. Clin., 62, 10-29.
16. Mackay, F. and Schneider, P. (2009) Cracking the BAFF code. Nat. Rev. Immunol., 9, 491-502.
17. Friedberg, J.W. and Fisher, R.I. (2008) Diffuse large B-cell lymphoma. Hematol. Oncol. Clin. North Am., 22, 941-952, ix.
18. Coiffier, B. (2005) Current strategies for the treatment of diffuse large B-cell lymphoma. Curr. Opin. Hematol., 12, 259-265. (Pubitemid 41058389)
19. Feugier, P., Van Hoof, A., Sebban, C., Solal-Celigny, P., Bouabdallah, R., Ferme, C., Christian, B., Lepage, E., Tilly, H., Morschhauser, F. et al. (2005) Long-term results of the R-CHOP study in the treatment of elderly patients with diffuse large B-cell lymphoma: a study by the Groupe d'Etude des Lymphomes de l'Adulte. J. Clin. Oncol., 23, 4117-4126. (Pubitemid 46211317)
20. Friedberg, J.W. and Fisher, R.I. (2006) Diffuse large B-cell NHL. Cancer Treat. Res., 131, 121-140.
21. Campo, E., Raffeld, M. and Jaffe, E.S. (1999) Mantle-cell lymphoma. Semin. Hematol., 36, 115-127. (Pubitemid 29214065)
22. Nakamura, N., Hase, H., Sakurai, D., Yoshida, S., Abe, M., Tsukada, N., Takizawa, J., Aoki, S., Kojima, M., Nakamura, S. et al. (2005) Expression of BAFF-R (BR 3) in normal and neoplastic lymphoid tissues characterized with a newly developed monoclonal antibody. Virchows Arch., 447, 53-60. (Pubitemid 41126240)
23. Monti, S., Savage, K.J., Kutok, J.L., Feuerhake, F., Kurtin, P., Mihm, M., Wu, B., Pasqualucci, L., Neuberg, D., Aguiar, R.C. et al. (2005) Molecular profiling of diffuse large B-cell lymphoma identifies robust subtypes including one characterized by host inflammatory response. Blood, 105, 1851-1861. (Pubitemid 40731764)
24. Shaffer, A.L., Wright, G., Yang, L., Powell, J., Ngo, V., Lamy, L., Lam, L.T., Davis, R.E. and Staudt, L.M. (2006) A library of gene expression signatures to illuminate normal and pathological lymphoid biology. Immunol. Rev., 210, 67-85.
25. Kuppers, R. (2005) Mechanisms of B-cell lymphoma pathogenesis. Nat. Rev. Cancer, 5, 251-262. (Pubitemid 40488631)
26. Yu, H. and Jove, R. (2004) The STATs of cancer-new molecular targets come of age. Nat. Rev. Cancer, 4, 97-105. (Pubitemid 38198738)
27. Yu, H., Pardoll, D. and Jove, R. (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer, 9, 798-809.
28. Ding, B.B., Yu, J.J., Yu, R.Y., Mendez, L.M., Shaknovich, R., Zhang, Y., Cattoretti, G. and Ye, B.H. (2008) Constitutively activated STAT3 promotes cell proliferation and survival in the activated B-cell subtype of diffuse large B-cell lymphomas. Blood, 111, 1515-1523. (Pubitemid 351213441)
29. Lai, R., Rassidakis, G.Z., Medeiros, L.J., Leventaki, V., Keating, M. and McDonnell, T.J. (2003) Expression of STAT3 and its phosphorylated forms in mantle cell lymphoma cell lines and tumours. J. Pathol., 199, 84-89. (Pubitemid 36054732)
30. Do, R.K., Hatada, E., Lee, H., Tourigny, M.R., Hilbert, D. and Chen-Kiang, S. (2000) Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med., 192, 953-964.
31. Khare, S.D., Sarosi, I., Xia, X.Z., McCabe, S., Miner, K., Solovyev, I., Hawkins, N., Kelley, M., Chang, D., Van, G. et al. (2000) Severe B-cell hyperplasia and autoimmune disease in TALL-1 transgenic mice. Proc. Natl Acad. Sci. USA, 97, 3370-3375. (Pubitemid 30183309)
32. Zhou, J. and Rossi, J.J. (2009) The therapeutic potential of cell-internalizing aptamers. Curr. Top Med. Chem, 9, 1144-1157.
33. Zhou, J., Li, H., Li, S., Zaia, J. and Rossi, J.J. (2008) Novel dual inhibitory function aptamer-siRNA delivery system for HIV-1 therapy. Mol. Ther., 16, 1481-1489.
34. McNamara, J.O. II, Andrechek, E.R., Wang, Y., Viles, K.D., Rempel, R.E., Gilboa, E., Sullenger, B.A. and Giangrande, P.H. (2006) Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat. Biotechnol., 24, 1005-1015. (Pubitemid 44215395)
35. Briones, J., Timmerman, J.M., Hilbert, D.M. and Levy, R. (2002) BLyS and BLyS receptor expression in non-Hodgkin's lymphoma. Exp. Hematol., 30, 135-141. (Pubitemid 34081224)
36. Zhou, J., Swiderski, P., Li, H., Zhang, J., Neff, C.P., Akkina, R. and Rossi, J.J. (2009) Selection, characterization and application of new RNA HIV gp 120 aptamers for facile delivery of Dicer substrate siRNAs into HIV infected cells. Nucleic Acids Res., 37, 3094-3109.
37. Tuerk, C. and Gold, L. (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science, 249, 505-510.
38. Fu, L., Lin-Lee, Y.C., Pham, L.V., Tamayo, A.T., Yoshimura, L.C. and Ford, R.J. (2009) BAFF-R promotes cell proliferation and survival through interaction with IKKbeta and NF-kappaB/c-Rel in the nucleus of normal and neoplastic B-lymphoid cells. Blood, 113, 4627-4636.
39. Kortylewski, M. and Yu, H. (2008) Role of Stat3 in suppressing anti-tumor immunity. Curr. Opin. Immunol., 20, 228-233.
40. Bowman, T., Garcia, R., Turkson, J. and Jove, R. (2000) STATs in oncogenesis. Oncogene, 19, 2474-2488. (Pubitemid 30339203)
41. Dassie, J.P., Liu, X.Y., Thomas, G.S., Whitaker, R.M., Thiel, K.W., Stockdale, K.R., Meyerholz, D.K., McCaffrey, A.P., McNamara, J.O. II and Giangrande, P.H. (2009) Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat. Biotechnol., 27, 839-849.
42. Matranga, C., Tomari, Y., Shin, C., Bartel, D.P. and Zamore, P.D. (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell, 123, 607-620. (Pubitemid 41608464)
43. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G. and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell, 15, 185-197. (Pubitemid 38950966)
44. Zhou, J., Song, M.S., Jacobi, A.M., Behlke, M.A., Wu, X. and Rossi, J.J. (2012) Deep Sequencing Analyses of DsiRNAs Reveal the Influence of 3' Terminal Overhangs on Dicing Polarity, Strand Selectivity, and RNA Editing of siRNAs. Mol. Ther. Nucleic Acids, 1, e17.
45. Zhou, J., Neff, C.P., Swiderski, P., Li, H., Smith, D.D., Aboellail, T., Remling-Mulder, L., Akkina, R. and Rossi, J.J. (2013) Functional in vivo delivery of multiplexed anti-HIV-1 siRNAs via a chemically synthesized aptamer with a sticky bridge. Mol. Ther., 21, 192-200.
46. Laubli, H. and Borsig, L. (2010) Selectins promote tumor metastasis. Semin Cancer Biol, 20, 169-177.
47. Laubli, H., Spanaus, K.S. and Borsig, L. (2009) Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes. Blood, 114, 4583-4591.
48. Kneuer, C., Ehrhardt, C., Radomski, M.W. and Bakowsky, U. (2006) Selectins-potential pharmacological targets Drug Discov. Today, 11, 1034-1040.
49. Ng, E.W., Shima, D.T., Calias, P., Cunningham, E.T. Jr, Guyer, D.R. and Adamis, A.P. (2006) Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat. Rev. Drug Discov., 5, 123-132.
50. Zhou, J. and Rossi, J.J. Aptamer-targeted cell-specific RNA interference. Silence, 1, 4.
51. Mackay, F., Woodcock, S.A., Lawton, P., Ambrose, C., Baetscher, M., Schneider, P., Tschopp, J. and Browning, J.L. (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med., 190, 1697-1710. (Pubitemid 30002351)
52. Bromberg, J.F., Wrzeszczynska, M.H., Devgan, G., Zhao, Y., Pestell, R.G., Albanese, C. and Darnell, J.E. Jr (1999) Stat3 as an oncogene. Cell, 98, 295-303. (Pubitemid 29380565)
53. Campbell, C.L., Jiang, Z., Savarese, D.M. and Savarese, T.M. (2001) Increased expression of the interleukin-11 receptor and evidence of STAT3 activation in prostate carcinoma. Am. J. Pathol., 158, 25-32. (Pubitemid 32096467)
54. Gouilleux-Gruart, V., Gouilleux, F., Desaint, C., Claisse, J.F., Capiod, J.C., Delobel, J., Weber-Nordt, R., Dusanter-Fourt, I., Dreyfus, F., Groner, B. et al. (1996) STAT-related transcription factors are constitutively activated in peripheral blood cells from acute leukemia patients. Blood, 87, 1692-1697. (Pubitemid 26068885)
55. Kube, D., Holtick, U., Vockerodt, M., Ahmadi, T., Haier, B., Behrmann, I., Heinrich, P.C., Diehl, V. and Tesch, H. (2001) STAT3 is constitutively activated in Hodgkin cell lines. Blood, 98, 762-770.
56. Tiemann, K., Alluin, J.V., Honegger, A., Chomchan, P., Gaur, S., Yun, Y., Forman, S.J., Rossi, J.J. and Chen, R.W. (2011) Small interfering RNAs targeting cyclin D1 and cyclin D2 enhance the cytotoxicity of chemotherapeutic agents in mantle cell lymphoma cell lines. Leuk Lymphoma, 52, 2148-2154.
57. Chu, T.C., Marks, J.W. III, Lavery, L.A., Faulkner, S., Rosenblum, M.G., Ellington, A.D. and Levy, M. (2006) Aptamer:toxin conjugates that specifically target prostate tumor cells. Cancer Res., 66, 5989-5992.
58. Wen, X., Lyu, M.A., Zhang, R., Lu, W., Huang, Q., Liang, D., Rosenblum, M.G. and Li, C. (2011) Biodistribution, pharmacokinetics, and nuclear imaging studies of (111)in-labeled rGel/BLyS fusion toxin in SCID mice bearing B-cell lymphoma. Mol. Imaging Biol., 13, 721-729.