Immunomodulation of hematological malignancies using oligonucleotides based-nanomedicines

Journal of Controlled Release

Volumn 244, Issue , 2016, Pages 149-156

  Hazan Halevy, Inbal ^a   Landesman Milo, Dalit ^a   Rosenblum, Daniel ^a   Mizrahy, Shoshy ^a   Ng, Brandon D ^a   Peer, Dan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Hematological malignancies; Nanoparticles; RNAi; Targeted delivery

Indexed keywords

BLOOD; BONE; CONTROLLED DRUG DELIVERY; CYTOLOGY; GENE EXPRESSION; LYMPHOCYTES; MEDICAL NANOTECHNOLOGY; NANOPARTICLES; OLIGONUCLEOTIDES; ONCOGENIC VIRUSES; RNA; STEM CELLS;

ANTISENSE OLIGONUCLEOTIDES; CHROMOSOMAL TRANSLOCATIONS; HEMATOLOGICAL MALIGNANCIES; LYMPHOID MALIGNANCIES; RNAI; SYSTEMIC ADMINISTRATION; TARGETED DELIVERY; TRANSFECTION REAGENTS;

TARGETED DRUG DELIVERY;

ANTISENSE OLIGONUCLEOTIDE; APTAMER; CPG OLIGODEOXYNUCLEOTIDE; LIPOSOME; NANOCARRIER; POLYMER; RNA; SMALL INTERFERING RNA; STABILIZED NUCLEIC ACID LIPID PARTICLE; UNCLASSIFIED DRUG; NANOPARTICLE; OLIGONUCLEOTIDE;

ARTICLE; EX VIVO STUDY; GENE FUNCTION; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNOMODULATION; LEUKOCYTE; NANOMEDICINE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; ANIMAL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; HEMATOLOGIC DISEASE; IMMUNOLOGY;

ANIMALS; DRUG DELIVERY SYSTEMS; HEMATOLOGIC NEOPLASMS; HUMANS; IMMUNOMODULATION; LEUKOCYTES; NANOPARTICLES; OLIGONUCLEOTIDES;

EID: 84994626272     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.07.052     Document Type: Article

References (56)

1. [1] Arber, D.A., Orazi, A., Hasserjian, R., Thiele, J., Borowitz, M.J., Le Beau, M.M., Bloomfield, C.D., Cazzola, M., Vardiman, J.W., The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood 127 (2016), 2391–2405.
2. [2] Weinstein, S., Peer, D., RNAi nanomedicines: challenges and opportunities within the immune system. Nanotechnology, 21, 2010, 232001.
3. [3] Davidson, B.L., McCray, P.B. Jr., Current prospects for RNA interference-based therapies. Nat. Rev. Genet. 12 (2011), 329–340.
4. [4] Ling, H., Fabbri, M., Calin, G.A., MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat. Rev. Drug Discov. 12 (2013), 847–865.
5. [5] Wittrup, A., Lieberman, J., Knocking down disease: a progress report on siRNA therapeutics. Nat. Rev. Genet. 16 (2015), 543–552.
6. [6] Dorsett, Y., Tuschl, T., siRNAs: applications in functional genomics and potential as therapeutics. Nat. Rev. Drug Discov. 3 (2004), 318–329.
7. [7] Juliano, R., Alam, M.R., Dixit, V., Kang, H., Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides. Nucleic Acids Res. 36 (2008), 4158–4171.
8. [8] Schlee, M., Hartmann, G., The chase for the RIG-I ligand—recent advances. Mol. Ther. 18 (2010), 1254–1262.
9. [9] Hornung, V., Guenthner-Biller, M., Bourquin, C., Ablasser, A., Schlee, M., Uematsu, S., Noronha, A., Manoharan, M., Akira, S., de Fougerolles, A., Endres, S., Hartmann, G., Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 11 (2005), 263–270.
10. [10] Judge, A.D., Sood, V., Shaw, J.R., Fang, D., McClintock, K., MacLachlan, I., Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23 (2005), 457–462.
11. [11] Meade, B.R., Gogoi, K., Hamil, A.S., Palm-Apergi, C., van den Berg, A., Hagopian, J.C., Springer, A.D., Eguchi, A., Kacsinta, A.D., Dowdy, C.F., Presente, A., Lonn, P., Kaulich, M., Yoshioka, N., Gros, E., Cui, X.S., Dowdy, S.F., Efficient delivery of RNAi prodrugs containing reversible charge-neutralizing phosphotriester backbone modifications. Nat. Biotechnol. 32 (2014), 1256–1261.
12. [12] Wu, S.Y., Yang, X., Gharpure, K.M., Hatakeyama, H., Egli, M., McGuire, M.H., Nagaraja, A.S., Miyake, T.M., Rupaimoole, R., Pecot, C.V., Taylor, M., Pradeep, S., Sierant, M., Rodriguez-Aguayo, C., Choi, H.J., Previs, R.A., Armaiz-Pena, G.N., Huang, L., Martinez, C., Hassell, T., Ivan, C., Sehgal, V., Singhania, R., Han, H.D., Su, C., Kim, J.H., Dalton, H.J., Kovvali, C., Keyomarsi, K., McMillan, N.A., Overwijk, W.W., Liu, J., Lee, J.S., Baggerly, K.A., Lopez-Berestein, G., Ram, P.T., Nawrot, B., Sood, A.K., 2′-OMe-phosphorodithioate-modified siRNAs show increased loading into the RISC complex and enhanced anti-tumour activity. Nat. Commun., 5, 2014, 3459.
13. [13] Peer, D., Park, E.J., Morishita, Y., Carman, C.V., Shimaoka, M., Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target. Science (New York, N.Y.) 319 (2008), 627–630.
14. [14] Peer, D., Shimaoka, M., Systemic siRNA delivery to leukocyte-implicated diseases. Cell Cycle (Georgetown, Tex.) 8 (2009), 853–859.
15. [15] Krieg, A.M., The role of CpG motifs in innate immunity. Curr. Opin. Immunol. 12 (2000), 35–43.
16. [16] Abdi, J., Mutis, T., Garssen, J., Redegeld, F., Characterization of the Toll-like receptor expression profile in human multiple myeloma cells. PLoS One, 8, 2013, e60671.
17. [17] Mongini, P.K., Gupta, R., Boyle, E., Nieto, J., Lee, H., Stein, J., Bandovic, J., Stankovic, T., Barrientos, J., Kolitz, J.E., Allen, S.L., Rai, K., Chu, C.C., Chiorazzi, N., TLR-9 and IL-15 synergy promotes the in vitro clonal expansion of chronic lymphocytic leukemia B cells. J. Immunol. (Baltimore, MD: 1950) 195 (2015), 901–923.
18. [18] Zhang, Q., Hossain, D.M., Nechaev, S., Kozlowska, A., Zhang, W., Liu, Y., Kowolik, C.M., Swiderski, P., Rossi, J.J., Forman, S., Pal, S., Bhatia, R., Raubitschek, A., Yu, H., Kortylewski, M., TLR9-mediated siRNA delivery for targeting of normal and malignant human hematopoietic cells in vivo. Blood 121 (2013), 1304–1315.
19. [19] Kortylewski, M., Swiderski, P., Herrmann, A., Wang, L., Kowolik, C., Kujawski, M., Lee, H., Scuto, A., Liu, Y., Yang, C., Deng, J., Soifer, H.S., Raubitschek, A., Forman, S., Rossi, J.J., Pardoll, D.M., Jove, R., Yu, H., In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses. Nat. Biotechnol. 27 (2009), 925–932.
20. [20] Hossain, D.M., Dos Santos, C., Zhang, Q., Kozlowska, A., Liu, H., Gao, C., Moreira, D., Swiderski, P., Jozwiak, A., Kline, J., Forman, S., Bhatia, R., Kuo, Y.H., Kortylewski, M., Leukemia cell-targeted STAT3 silencing and TLR9 triggering generate systemic antitumor immunity. Blood 123 (2014), 15–25.
21. [21] Uckun, F.M., Qazi, S., Dibirdik, I., Myers, D.E., Rational design of an immunoconjugate for selective knock-down of leukemia-specific E2A-PBX1 fusion gene expression in human Pre-B leukemia. Integr. Biol. 5 (2013), 122–132.
22. [22] Hong, D., Kurzrock, R., Kim, Y., Woessner, R., Younes, A., Nemunaitis, J., Fowler, N., Zhou, T., Schmidt, J., Jo, M., Lee, S.J., Yamashita, M., Hughes, S.G., Fayad, L., Piha-Paul, S., Nadella, M.V., Mohseni, M., Lawson, D., Reimer, C., Blakey, D.C., Xiao, X., Hsu, J., Revenko, A., Monia, B.P., MacLeod, A.R., AZD9150, a next-generation antisense oligonucleotide inhibitor of STAT3 with early evidence of clinical activity in lymphoma and lung cancer. Sci. Transl. Med., 7, 2015, 314ra185.
23. [23] Cortes, J., Kantarjian, H., Ball, E.D., Dipersio, J., Kolitz, J.E., Fernandez, H.F., Goodman, M., Borthakur, G., Baer, M.R., Wetzler, M., Phase 2 randomized study of p53 antisense oligonucleotide (cenersen) plus idarubicin with or without cytarabine in refractory and relapsed acute myeloid leukemia. Cancer 118 (2012), 418–427.
24. [24] O'Brien, S., Moore, J.O., Boyd, T.E., Larratt, L.M., Skotnicki, A., Koziner, B., Chanan-Khan, A.A., Seymour, J.F., Bociek, R.G., Pavletic, S., Rai, K.R., Randomized phase III trial of fludarabine plus cyclophosphamide with or without oblimersen sodium (Bcl-2 antisense) in patients with relapsed or refractory chronic lymphocytic leukemia. J. Clin. Oncol. 25 (2007), 1114–1120.
25. [25] Chanan-Khan, A.A., Niesvizky, R., Hohl, R.J., Zimmerman, T.M., Christiansen, N.P., Schiller, G.J., Callander, N., Lister, J., Oken, M., Jagannath, S., Phase III randomised study of dexamethasone with or without oblimersen sodium for patients with advanced multiple myeloma. Leuk. Lymphoma 50 (2009), 559–565.
26. [26] Lieberman, J., Manipulating the in vivo immune response by targeted gene knockdown. Curr. Opin. Immunol. 35 (2015), 63–72.
27. [27] Wheeler, L.A., Vrbanac, V., Trifonova, R., Brehm, M.A., Gilboa-Geffen, A., Tanno, S., Greiner, D.L., Luster, A.D., Tager, A.M., Lieberman, J., Durable knockdown and protection from HIV transmission in humanized mice treated with gel-formulated CD4 aptamer-siRNA chimeras. Mol. Ther. 21 (2013), 1378–1389.
28. [28] Zhou, J., Satheesan, S., Li, H., Weinberg, M.S., Morris, K.V., Burnett, J.C., Rossi, J.J., Cell-specific RNA aptamer against human CCR5 specifically targets HIV-1 susceptible cells and inhibits HIV-1 infectivity. Chem. Biol. 22 (2015), 379–390.
29. [29] Herrmann, A., Priceman, S.J., Swiderski, P., Kujawski, M., Xin, H., Cherryholmes, G.A., Zhang, W., Zhang, C., Lahtz, C., Kowolik, C., Forman, S.J., Kortylewski, M., Yu, H., CTLA4 aptamer delivers STAT3 siRNA to tumor-associated and malignant T cells. J. Clin. Invest. 124 (2014), 2977–2987.
30. [30] Peer, D., Karp, J.M., Hong, S., Farokhzad, O.C., Margalit, R., Langer, R., Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2 (2007), 751–760.
31. [31] Peer, D., A daunting task: manipulating leukocyte function with RNAi. Immunol. Rev. 253 (2013), 185–197.
32. [32] Landesman-Milo, D., Peer, D., Transforming nanomedicines from lab scale production to novel clinical modality. Bioconjug. Chem. 27 (2016), 855–862.
33. [33] Chou, S.T., Mixson, A.J., siRNA nanoparticles: the future of RNAi therapeutics for oncology?. Nanomedicine (London, England) 9 (2014), 2251–2254.
34. [34] Francis, S.M., Taylor, C.A., Tang, T., Liu, Z., Zheng, Q., Dondero, R., Thompson, J.E., SNS01-T modulation of eIF5A inhibits B-cell cancer progression and synergizes with bortezomib and lenalidomide. Mol. Ther. 22 (2014), 1643–1652.
35. [35] Gavrilov, K., Seo, Y.E., Tietjen, G.T., Cui, J., Cheng, C.J., Saltzman, W.M., Enhancing potency of siRNA targeting fusion genes by optimization outside of target sequence. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), E6597–E6605.
36. [36] Babar, I.A., Cheng, C.J., Booth, C.J., Liang, X., Weidhaas, J.B., Saltzman, W.M., Slack, F.J., Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E1695–E1704.
37. [37] Schallon, A., Synatschke, C.V., Jerome, V., Muller, A.H., Freitag, R., Nanoparticulate nonviral agent for the effective delivery of pDNA and siRNA to differentiated cells and primary human T lymphocytes. Biomacromolecules 13 (2012), 3463–3474.
38. [38] Badros, A.Z., Goloubeva, O., Rapoport, A.P., Ratterree, B., Gahres, N., Meisenberg, B., Takebe, N., Heyman, M., Zwiebel, J., Streicher, H., Gocke, C.D., Tomic, D., Flaws, J.A., Zhang, B., Fenton, R.G., Phase II study of G3139, a Bcl-2 antisense oligonucleotide, in combination with dexamethasone and thalidomide in relapsed multiple myeloma patients. J. Clin. Oncol. 23 (2005), 4089–4099.
39. [39] Durig, J., Duhrsen, U., Klein-Hitpass, L., Worm, J., Hansen, J.B., Orum, H., Wissenbach, M., The novel antisense Bcl-2 inhibitor SPC2996 causes rapid leukemic cell clearance and immune activation in chronic lymphocytic leukemia. Leukemia 25 (2011), 638–647.
40. [40] Yu, B., Mao, Y., Bai, L.Y., Herman, S.E., Wang, X., Ramanunni, A., Jin, Y., Mo, X., Cheney, C., Chan, K.K., Jarjoura, D., Marcucci, G., Lee, R.J., Byrd, J.C., Lee, L.J., Muthusamy, N., Targeted nanoparticle delivery overcomes off-target immunostimulatory effects of oligonucleotides and improves therapeutic efficacy in chronic lymphocytic leukemia. Blood 121 (2013), 136–147.
41. [41] Coelho, T., Adams, D., Silva, A., Lozeron, P., Hawkins, P.N., Mant, T., Perez, J., Chiesa, J., Warrington, S., Tranter, E., Munisamy, M., Falzone, R., Harrop, J., Cehelsky, J., Bettencourt, B.R., Geissler, M., Butler, J.S., Sehgal, A., Meyers, R.E., Chen, Q., Borland, T., Hutabarat, R.M., Clausen, V.A., Alvarez, R., Fitzgerald, K., Gamba-Vitalo, C., Nochur, S.V., Vaishnaw, A.K., Sah, D.W., Gollob, J.A., Suhr, O.B., Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N. Engl. J. Med. 369 (2013), 819–829.
42. [42] Tabernero, J., Shapiro, G.I., LoRusso, P.M., Cervantes, A., Schwartz, G.K., Weiss, G.J., Paz-Ares, L., Cho, D.C., Infante, J.R., Alsina, M., Gounder, M.M., Falzone, R., Harrop, J., White, A.C., Toudjarska, I., Bumcrot, D., Meyers, R.E., Hinkle, G., Svrzikapa, N., Hutabarat, R.M., Clausen, V.A., Cehelsky, J., Nochur, S.V., Gamba-Vitalo, C., Vaishnaw, A.K., Sah, D.W., Gollob, J.A., Burris, H.A. III, First-in-humans trial of an RNA interference therapeutic targeting VEGF and KSP in cancer patients with liver involvement. Cancer Discov. 3 (2013), 406–417.
43. [43] Morrissey, D.V., Lockridge, J.A., Shaw, L., Blanchard, K., Jensen, K., Breen, W., Hartsough, K., Machemer, L., Radka, S., Jadhav, V., Vaish, N., Zinnen, S., Vargeese, C., Bowman, K., Shaffer, C.S., Jeffs, L.B., Judge, A., MacLachlan, I., Polisky, B., Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol. 23 (2005), 1002–1007.
44. [44] Akinc, A., Querbes, W., De, S., Qin, J., Frank-Kamenetsky, M., Jayaprakash, K.N., Jayaraman, M., Rajeev, K.G., Cantley, W.L., Dorkin, J.R., Butler, J.S., Qin, L., Racie, T., Sprague, A., Fava, E., Zeigerer, A., Hope, M.J., Zerial, M., Sah, D.W., Fitzgerald, K., Tracy, M.A., Manoharan, M., Koteliansky, V., Fougerolles, A., Maier, M.A., Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol. Ther. 18 (2010), 1357–1364.
45. [45] Novobrantseva, T.I., Borodovsky, A., Wong, J., Klebanov, B., Zafari, M., Yucius, K., Querbes, W., Ge, P., Ruda, V.M., Milstein, S., Speciner, L., Duncan, R., Barros, S., Basha, G., Cullis, P., Akinc, A., Donahoe, J.S., Narayanannair Jayaprakash, K., Jayaraman, M., Bogorad, R.L., Love, K., Whitehead, K., Levins, C., Manoharan, M., Swirski, F.K., Weissleder, R., Langer, R., Anderson, D.G., de Fougerolles, A., Nahrendorf, M., Koteliansky, V., Systemic RNAi-mediated gene silencing in nonhuman primate and rodent myeloid cells. Mol. Ther. Nucleic Acids, 1, 2012, e4.
46. [46] Zimmermann, T.S., Lee, A.C., Akinc, A., Bramlage, B., Bumcrot, D., Fedoruk, M.N., Harborth, J., Heyes, J.A., Jeffs, L.B., John, M., Judge, A.D., Lam, K., McClintock, K., Nechev, L.V., Palmer, L.R., Racie, T., Rohl, I., Seiffert, S., Shanmugam, S., Sood, V., Soutschek, J., Toudjarska, I., Wheat, A.J., Yaworski, E., Zedalis, W., Koteliansky, V., Manoharan, M., Vornlocher, H.P., MacLachlan, I., RNAi-mediated gene silencing in non-human primates. Nature 441 (2006), 111–114.
47. [47] Ramishetti, S., Kedmi, R., Goldsmith, M., Leonard, F., Sprague, A.G., Godin, B., Gozin, M., Cullis, P.R., Dykxhoorn, D.M., Peer, D., Systemic gene silencing in primary T lymphocytes using targeted lipid nanoparticles. ACS Nano 9 (2015), 6706–6716.
48. [48] Weinstein, S., Toker, I.A., Emmanuel, R., Ramishetti, S., Hazan-Halevy, I., Rosenblum, D., Goldsmith, M., Abraham, A., Benjamini, O., Bairey, O., Raanani, P., Nagler, A., Lieberman, J., Peer, D., Harnessing RNAi-based nanomedicines for therapeutic gene silencing in B-cell malignancies. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E16–E22.
49. [49] Cohen, Z.R., Ramishetti, S., Peshes-Yaloz, N., Goldsmith, M., Wohl, A., Zibly, Z., Peer, D., Localized RNAi therapeutics of chemoresistant grade IV glioma using hyaluronan-grafted lipid-based nanoparticles. ACS Nano 9 (2015), 1581–1591.
50. [50] Ramishetti, S., Landesman-Milo, D., Peer, D., Advances in RNAi therapeutic delivery to leukocytes using lipid nanoparticles. J. Drug Target., 2016, 1–7.
51. [51] O'Brien, S.M., Cunningham, C.C., Golenkov, A.K., Turkina, A.G., Novick, S.C., Rai, K.R., Phase I to II multicenter study of oblimersen sodium, a Bcl-2 antisense oligonucleotide, in patients with advanced chronic lymphocytic leukemia. J. Clin. Oncol. 23 (2005), 7697–7702.
52. [52] Moore, J., Seiter, K., Kolitz, J., Stock, W., Giles, F., Kalaycio, M., Zenk, D., Marcucci, G., A phase II study of Bcl-2 antisense (oblimersen sodium) combined with gemtuzumab ozogamicin in older patients with acute myeloid leukemia in first relapse. Leuk. Res. 30 (2006), 777–783.
53. [53] O'Brien, S., Moore, J.O., Boyd, T.E., Larratt, L.M., Skotnicki, A.B., Koziner, B., Chanan-Khan, A.A., Seymour, J.F., Gribben, J., Itri, L.M., Rai, K.R., 5-year survival in patients with relapsed or refractory chronic lymphocytic leukemia in a randomized, phase III trial of fludarabine plus cyclophosphamide with or without oblimersen. J. Clin. Oncol. 27 (2009), 5208–5212.
54. [54] Carter, B.Z., Mak, D.H., Morris, S.J., Borthakur, G., Estey, E., Byrd, A.L., Konopleva, M., Kantarjian, H., Andreeff, M., XIAP antisense oligonucleotide (AEG35156) achieves target knockdown and induces apoptosis preferentially in CD34 + 38 − cells in a phase 1/2 study of patients with relapsed/refractory AML. Apoptosis 16 (2011), 67–74.
55. [55] Ramon, A.L., Malvy, C., Anticancer oligonulceotides. Reddy, L.H., Couvreur, P., (eds.) Macromolecular Anticancer Therapeutics, 2010, Springer, New York, 539–568.
56. [56] Wilhelm, S., Tavares, A.J., dai, Q., Ohta, S., Audet, J., Dvorak, H.F., Chan, W.C.W., Analysis of nanoparticles delivery to tumors. Nat. Rev. Mater., 2016, 1–12.