Immunotherapy of hepatocellular carcinoma with small double-stranded RNA

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Kabilova, Tatyana O ^a   Kovtonyuk, Larisa V ^a   Zonov, Evgeniy V ^a   Ryabchikova, Elena I ^a   Popova, Nelly A ^b   Nikolin, Valeriy P ^b   Kaledin, Vasiliy I ^b   Zenkova, Marina A ^a   Vlassov, Valentin V ^a   Chernolovskaya, Elena L ^a  

^a INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^b INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

Author keywords

Hepatocellular carcinoma; Immunostimulatory RNA; Interferon inducer

Indexed keywords

ALPHA INTERFERON; DOUBLE STRANDED RNA; IMMUNOSTIMULATING AGENT; INTERLEUKIN 6; LIPOFECTAMINE; POLYINOSINIC POLYCYTIDYLIC ACID; SMALL INTERFERING RNA; INTERFERON INDUCING AGENT; INTERLEUKIN-6, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GENE THERAPY; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG FORMULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HEART METASTASIS; IMMUNOSTIMULATION; KIDNEY METASTASIS; LIPOSOMAL DELIVERY; LIVER CELL CARCINOMA; LIVER METASTASIS; MALE; METASTASIS INHIBITION; MOUSE; MOUSE MODEL; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; RNA GENE; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; BLOOD; CARCINOMA, HEPATOCELLULAR; CBA MOUSE; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; INNATE IMMUNITY; LIVER NEOPLASMS; MITOSIS; NECROSIS; PATHOLOGY; PROCEDURES; SECONDARY; TIME;

ANIMALS; CARCINOMA, HEPATOCELLULAR; IMMUNITY, INNATE; IMMUNOTHERAPY; INTERFERON INDUCERS; INTERFERON-ALPHA; INTERLEUKIN-6; LIVER NEOPLASMS; MALE; MICE, INBRED CBA; MITOSIS; NECROSIS; RNA, DOUBLE-STRANDED; TIME FACTORS; TUMOR BURDEN;

EID: 84901633190     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-338     Document Type: Article

References (47)

1. Schütte K, Bornschein J, Malfertheiner P. Hepatocellular carcinoma-epidemiological trends and risk factors. Dig Dis 2009, 27:80-92.
2. Makuuchi M, Kosuge T, Takayama T, Yamazaki S, Kakazu T, Miyagawa S, Kawasaki S. Surgery for small liver cancers. Semin Surg Oncol 1993, 9:298-304. 10.1002/ssu.2980090404, 8210909.
3. Livragh T, Lazzaroni S, Pellicano S, Ravasi S, Torzilli G, Vettori C. Percutaneous ethanol injection of hepatic tumours: single-session therapy with general anesthesia. AJR Am J Roentgenol 1993, 161:1065-1069. 10.2214/ajr.161.5.8273612, 8273612.
4. Allgaier HP, Deibert P, Zuber I, Olschewski M, Blum HE. Percutaneous radiofrequency interstitial thermal ablation of small hepatocellular carcinoma. Lancet 1999, 353:1676-1677. 10.1016/S0140-6736(99)00368-2, 10335793.
5. Arii S, Yamaoka Y, Futagawa S, Inoue K, Kobayashi K, Kojiro M, Makuuchi M, Nakamura Y, Okita K, Yamada R. Results of surgical and nonsurgical treatment for small-sized hepatocellular carcinomas: a retrospective and nationwide survey in Japan. Hepatology 2000, 32:1224-1229. 10.1053/jhep.2000.20456, 11093728.
6. Adams S. Toll-like receptor agonists in cancer therapy. Immunotherapy 2009, 1:949-964. 10.2217/imt.09.70, 2886992, 20563267.
7. Gold JE, Masters TR, Osband ME. Autolymphocyte therapy III effective adjuvant adoptive cellular therapy with in vivo anti-tumor specificity against murine melanoma and carcinoma using ex-vivo-activated memory T-lymphocytes. J Surg Res 1995, 59:279-286. 10.1006/jsre.1995.1165, 7543632.
8. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, Xu Y, Frohlich MW, Schellhammer PF. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 2010, 363:411-422. 10.1056/NEJMoa1001294, 20818862.
9. Waldmann TA. Immunotherapy: past, present and future. Nat Med 2003, 9:269-277. 10.1038/nm0303-269, 12612576.
10. Unitt E, Marshall A, Gelson W, Rushbrook SM, Davies S, Vowler SL, Morris LS, Coleman N, Alexander GJ. Tumour lymphocytic infiltrate and recurrence of hepatocellular carcinoma following liver transplantation. J Hepatol 2006, 45:246-253. 10.1016/j.jhep.2005.12.027, 16580084.
11. Cui J, Wang N, Zhao H, Jin H, Wang G, Niu C, Terunuma H, He H, Li W. Combination of radiofrequency ablation and sequential cellular immunotherapy improves progression-free survival for patients with hepatocellular carcinoma. Int J Cancer 2014, 134:342-351. 10.1002/ijc.28372, 23825037.
12. Ishikawa T. Secondary prevention of recurrence by interferon therapy after ablation therapy for hepatocellular carcinoma in chronic hepatitis C patients. World J Gastroenterol 2008, 14:6140-6144. 10.3748/wjg.14.6140, 2761574, 18985803.
13. Mencin A, Kluwe J, Schwabe RF. Toll-like receptors as targets in chronic liver diseases. Gut 2009, 58:704-720. 10.1136/gut.2008.156307, 2791673, 19359436.
14. Ishikawa T, Ichida T. Features of hepatitis B virus-related hepatocellular carcinoma. Nihon Rinsho 2001, 59:435-439.
15. Nishiguchi S, Kuroki T, Nakatani S, Morimoto H, Takeda T, Nakajima S, Shiomi S, Seki S, Kobayashi K, Otani S. Randomised trial of effects of interferon-alpha on incidence of hepatocellular carcinoma in chronic active hepatitis C with cirrhosis. Lancet 1995, 346:1051-1055. 10.1016/S0140-6736(95)91739-X, 7564784.
16. Nishiguchi S, Shiomi S, Nakatani S, Takeda T, Fukuda K, Tamori A, Habu D, Tanaka T. Prevention of hepatocellular carcinoma in patients with chronic active hepatitis C and cirrhosis. Lancet 2001, 357:196-197. 10.1016/S0140-6736(00)03595-9, 11213099.
17. Olejniczak M, Galka-Marciniak P, Polak K, Fligier A, Krzyzosiak WJ. RNAimmuno: a database of the nonspecific immunological effects of RNA interference and microRNA reagents. RNA 2012, 18:930-935. 10.1261/rna.025627.110, 3334701, 22411954.
18. Desmet CJ, Ishii KJ. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol 2012, 12:479-491. 10.1038/nri3247, 22728526.
19. El-Omar EM, Ng MT, Hold GL. Polymorphisms in Toll-like receptor genes and risk of cancer. Oncogene 2008, 27:244-252. 10.1038/sj.onc.1210912, 18176606.
20. McHutchison JG, Bacon BR, Gordon SC, Lawitz E, Shiffman M, Afdhal NH, Jacobson IM, Muir A, Al-Adhami M, Morris ML, Lekstrom-himes JA, Efler SM, Davis HL. Phase 1B, randomized, double-blind, dose-escalation trial of CPG 10101 in patients with chronic hepatitis C virus. Hepatology 2007, 46:1341-1349. 10.1002/hep.21773, 17929306.
21. Horsmans Y, Berg T, Desager JP, Mueller T, Schott E, Fletcher SP, Steffy KR, Bauman LA, Kerr BM, Averett DR. Isatoribine, an agonist of TLR7, reduces plasma virus concentration in chronic hepatitis C infection. Hepatology 2005, 42:724-731. 10.1002/hep.20839, 16116638.
22. Xiang AX, Webber SE, Kerr BM, Rueden EJ, Lennox JR, Haley GJ, Wang T, Ng JS, Herbert MR, Clark DL, Banh VN, Li W, Fletcher SP, Steffy KR, Bartkowski DM, Kirovsky LI, Bauman LA, Averett DR. Discovery of ANA975: an oral prodrug of the TLR-7 agonist isatoribine. Nucleosides Nucleotides Nucleic Acids 2007, 26:635-640. 10.1080/15257770701490472, 18066870.
23. Pappas SC. Good science behind hepatitis C virus antiviral drug development: necessary but not sufficient. Hepatology 2010, 51:1897-1903. 10.1002/hep.23531, 20196118.
24. Kabilova TO, Vladimirova AV, Zenkova MA, Chernolovskaya EL, Vlassov VV. Antiproliferative and interferon-inducing activities of unique short double-stranded RNA. Dokl Biochem Biophys 2011, 436:8-11. 10.1134/S1607672911010042, 21369893.
25. Kabilova TO, Meschaninova MI, Venyaminova AG, Nikolin VP, Zenkova MA, Vlassov VV, Chernolovskaya EL. Short double-stranded RNA with immunostimulatory activity: sequence dependence. Nucleic Acid Ther 2012, 22:196-204.
26. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, Maclachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat Biotechnol 2005, 23:457-462. 10.1038/nbt1081, 15778705.
27. Currie AJ, van der Most RG, Broomfield SA, Prosser AC, Tovey MG, Robinson BW. Targeting the effector site with IFN-alphabeta-inducing TLR ligands reactivates tumor-resident CD8 T cell responses to eradicate established solid tumors. J Immunol 2008, 180:1535-1544. 10.4049/jimmunol.180.3.1535, 18209049.
28. Kaledin VI, Zhukova NA, Nikolin VP, Popova NA, Beliaev MD, Baginskaya NV, Litvinova EA, Tolstikova TG, Lushnikova EL, Semenov DE. Hepatocarcinoma-29, a metastasizing transplantable mouse tumor inducing cachexia. Bull Exp Biol Med 2009, 148:903-908. 10.1007/s10517-010-0848-9, 21116503.
29. Wang H, Chen L. Tumor microenviroment and hepatocellular carcinoma metastasis. J Gastroenterol Hepatol 2013, 28:43-48.
30. Seki S, Nakashima H, Nakashima M, Kinoshita M. Antitumor immunity produced by the Liver Kupffer Cells, NK Cells, NKT Cells, and CD8+ CD122+ TCells. Clin Dev Immunol 2011, 2011:868345. 3235445, 22190974.
31. Wang YC, Xu GL, Jia WD, Han SJ, Ren WH, Wang W, Liu WB, Zhang CH, Chen H. Estrogen suppresses metastasis in rat hepatocellular carcinoma through decreasing interleukin-6 and hepatocyte growth factor expression. Inflammation 2012, 35:143-149. 10.1007/s10753-011-9299-3, 21302136.
32. Hornung V, Guenthner-Biller M, Bourquin C, Ablasser A, Schlee M, Uematsu S, Noronha A, Manoharan M, Akira S, De FA, Endres S, Hartmann G. Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med 2005, 11:263-270. 10.1038/nm1191, 15723075.
33. Shin D, Kim SI, Park M, Kim M. Immunostimulatory properties and antiviral activity of modified HBV-specific siRNAs. Biochem Biophys Res Commun 2007, 364:436-442. 10.1016/j.bbrc.2007.10.012, 17963721.
34. Poeck H, Besch R, Maihoefer C, Renn M, Tormo D, Morskaya SS, Kirschnek S, Gaffal E, Landsberg J, Hellmuth J, Schmidt A, Anz D, Bscheider M, Schwerd T, Berking C, Bourquin C, Kalinke U, Kremmer E, Kato H, Akira S, Meyers R, Hacker G, Neuenhahn M, Busch D, Ruland J, Rothenfusser S, Prinz M, Hornung V, Endres S, Tuting T, et al. 5′-Triphosphate-siRNA: turning gene silencing and Rig-I activation against melanoma. Nat Med 2008, 14:1256-1263. 10.1038/nm.1887, 18978796.
35. Khairuddin N, Gantier MP, Blake SJ, Wu SY, Behlke MA, Williams BR, McMillan NA. siRNA-induced immunostimulation through TLR7 promotes antitumoral activity against HPV-driven tumors in vivo. Immunol Cell Biol 2012, 90:187-196. 10.1038/icb.2011.19, 21423261.
36. Tseng YC, Mozumdar S, Huang L. Lipid-based systemic delivery of siRNA. Adv Drug Deliv Rev 2009, 61:721-731. 10.1016/j.addr.2009.03.003, 3172140, 19328215.
37. Kortylewski M, Swiderski P, Herrmann A, Wang L, Kowolik C, Kujawski M, Lee H, Scuto A, Liu Y, Yang C, Deng J, Soifer HS, Raubitschek A, Forman S, Rossi JJ, Pardoll DM, Jove R, Yu H. In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses. Nat Biotechnol 2009, 27:925-932. 10.1038/nbt.1564, 2846721, 19749770.
38. Zhang Q, Hossain DM, Nechaev S, Kozlowska A, Zhang W, Liu Y, Kowolik CM, Swiderski P, Rossi JJ, 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 2013, 121:1304-1315. 10.1182/blood-2012-07-442590, 3578952, 23287859.
39. Schlee M, Hartmann G. The chase for the RIG-I ligand-recent advances. Mol Ther 2010, 18:1254-1262. 10.1038/mt.2010.90, 2911265, 20461060.
40. Kang DC, Gopalkrishnan RV, Wu Q, Jankowsky E, Pyle AM, Fisher PB. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci U S A 2002, 99:637-642. 10.1073/pnas.022637199, 117358, 11805321.
41. Karikó K, Bhuyan P, Capodici J, Ni H, Lubinski J, Friedman H, Weissman D. Exogenous siRNA mediates sequence-independent gene suppression by signaling through toll-like receptor 3. Cells Tissues Organs 2004, 177:132-138. 10.1159/000079987, 15388987.
42. Reynolds A, Anderson EM, Vermeulen A, Fedorov Y, Robinson K, Leake D, Karpilow J, Marshall WS, Khvorova A. Induction of the interferon response by siRNA is cell type- and duplex length-dependent. RNA 2006, 12:988-993. 10.1261/rna.2340906, 1464853, 16611941.
43. Puthenveetil S, Whitby L, Ren J, Kelnar K, Krebs JF, Beal PA. Controlling activation of the RNA-dependent protein kinase by siRNAs using site-specific chemical modification. Nucleic Acids Res 2006, 34:4900-4911. 10.1093/nar/gkl464, 1635244, 16982647.
44. Zhang Z, Weinschenk T, Guo K, Schluesener HJ. siRNA binding proteins of microglial cells: PKR is an unanticipated ligand. J Cell Biochem 2006, 97:1217-1229. 10.1002/jcb.20716, 16315288.
45. Yang C, Li L, Xue Y, Zhao Z, Zhao T, Jia Y, Rong R, Xu M, Nicholson ML, Zhu T, Yang B. Innate immunity activation involved in unprotected porcine auto-transplant kidneys preserved by naked caspase-3 siRNA. J Transl Med 2013, 11:210. 10.1186/1479-5876-11-210, 3847504, 24034868.
46. Meng Z, Zhang X, Wu J, Pei R, Xu Y, Yang D, Roggendorf M, Lu M. RNAi induces innate immunity through multiple cellular signaling pathways. PLoS One 2013, 8:e64708. 10.1371/journal.pone.0064708, 3659100, 23700487.
47. Hafner M, Zawatzky R, Hirtreiter C, Buurman WA, Echtenacher B, Hehlgans T, Mannel DN. Antimetastatic effect of CpG DNA Mediated by Type I IFN. Cancer Res 2001, 61:5523-5528.