Dendritic cells transfected with heat-shock protein 70 messenger RNA for patients with hepatitis C virus-related hepatocellular carcinoma: A phase 1 dose escalation clinical trial

Cancer Immunology, Immunotherapy

Volumn 64, Issue 8, 2015, Pages 1047-1056

  Maeda, Yoshinari ^a   Yoshimura, Kiyoshi ^a   Matsui, Hiroto ^a   Shindo, Yoshitaro ^a   Tamesa, Takao ^a   Tokumitsu, Yukio ^a   Hashimoto, Noriaki ^a   Tokuhisa, Yoshihiro ^a   Sakamoto, Kazuhiko ^a   Sakai, Kouhei ^a   Suehiro, Yutaka ^a   Hinoda, Yuji ^a   Tamada, Koji ^a   Yoshino, Shigefumi ^a   Hazama, Shoichi ^a   Oka, Masaaki ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Dendritic cell; Electroporation; Heat shock protein 70; Hepatocellular carcinoma; Immunotherapy

Indexed keywords

GAMMA INTERFERON; GRANZYME B; HEAT SHOCK PROTEIN 70; MESSENGER RNA;

ADULT; AGED; ARTICLE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG DOSE ESCALATION; EFFECTOR CELL; ELECTROPORATION; FEMALE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; LIVER ABSCESS; LIVER CELL CARCINOMA; MALE; MIDDLE AGED; PARTIAL HEPATECTOMY; PHASE 1 CLINICAL TRIAL; POPULATION DYNAMICS; PRIORITY JOURNAL; RECOMMENDED DRUG DOSE; RECURRENT DISEASE; SIDE EFFECT; VERY ELDERLY; CARCINOMA, HEPATOCELLULAR; CHRONIC HEPATITIS C; CLINICAL TRIAL; COMPLICATION; CYTOTOXICITY; FOLLOW UP; GENETIC TRANSFECTION; GENETICS; HEPACIVIRUS; IMMUNOLOGY; INTRADERMAL DRUG ADMINISTRATION; LIVER NEOPLASMS; LYMPHOCYTE ACTIVATION; NEOPLASM RECURRENCE, LOCAL; PROCEDURES; REMISSION; TRANSGENE; TRANSPLANTATION; VIROLOGY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, HEPATOCELLULAR; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; FEMALE; FOLLOW-UP STUDIES; HEPACIVIRUS; HEPATITIS C, CHRONIC; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOTHERAPY; INJECTIONS, INTRADERMAL; LIVER NEOPLASMS; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; REMISSION INDUCTION; RNA, MESSENGER; TRANSFECTION; TRANSGENES; YOUNG ADULT;

EID: 84937969182     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1709-1     Document Type: Article

References (33)

1. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55(2):74–108
2. Thorgeirsson SS, Grisham JW (2002) Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31(4):339–346. doi:10.1038/ng0802-339
3. Ohishi W, Kitamoto M, Aikata H, Kamada K, Kawakami Y, Ishihara H, Kamiyasu M, Nakanishi T, Tazuma S, Chayama K (2003) Impact of aging on the development of hepatocellular carcinoma in patients with hepatitis C virus infection in Japan. Scand J Gastroenterol 38(8):894–900
4. Ikai I, Arii S, Ichida T, Okita K, Omata M, Kojiro M, Takayasu K, Nakanuma Y, Makuuchi M, Matsuyama Y, Yamaoka Y (2005) Report of the 16th follow-up survey of primary liver cancer. Hepatol Res 32(3):163–172. doi:10.1016/j.hepres.2005.04.005
5. Thomas MB, Abbruzzese JL (2005) Opportunities for targeted therapies in hepatocellular carcinoma. J Clin Oncol 23(31):8093–8108. doi:10.1200/JCO.2004.00.1537
6. Llovet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362(9399):1907–1917. doi:10.1016/S0140-6736(03)14964-1
7. Iizuka N, Oka M, Yamada-Okabe H, Nishida M, Maeda Y, Mori N, Takao T, Tamesa T, Tangoku A, Tabuchi H, Hamada K, Nakayama H, Ishitsuka H, Miyamoto T, Hirabayashi A, Uchimura S, Hamamoto Y (2003) Oligonucleotide microarray for prediction of early intrahepatic recurrence of hepatocellular carcinoma after curative resection. Lancet 361(9361):923–929. doi:10.1016/S0140-6736(03)12775-4
8. Iizuka N, Hamamoto Y, Oka M (2004) Predicting individual outcomes in hepatocellular carcinoma. Lancet 364(9448):1837–1839. doi:10.1016/S0140-6736(04)17455-2
9. Itoh Y, Ohkubo K, Iuchi H, Michitaka K, Horiike N, Onji M (2002) Chronological changes of causes of death and distant metastasis in hepatocellular carcinoma. Oncol Rep 9(2):331–335
10. Yang Y, Nagano H, Ota H, Morimoto O, Nakamura M, Wada H, Noda T, Damdinsuren B, Marubashi S, Miyamoto A, Takeda Y, Dono K, Umeshita K, Nakamori S, Wakasa K, Sakon M, Monden M (2007) Patterns and clinicopathologic features of extrahepatic recurrence of hepatocellular carcinoma after curative resection. Surgery 141(2):196–202. doi:10.1016/j.surg.2006.06.033
11. Unitt E, Marshall A, Gelson W, Rushbrook SM, Davies S, Vowler SL, Morris LS, Coleman N, Alexander GJ (2006) Tumour lymphocytic infiltrate and recurrence of hepatocellular carcinoma following liver transplantation. J Hepatol 45(2):246–253. doi:10.1016/j.jhep.2005.12.027
12. Takayama T, Sekine T, Makuuchi M, Yamasaki S, Kosuge T, Yamamoto J, Shimada K, Sakamoto M, Hirohashi S, Ohashi Y, Kakizoe T (2000) Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet 356(9232):802–807. doi:10.1016/S0140-6736(00)02654-4
13. Takashima M, Kuramitsu Y, Yokoyama Y, Iizuka N, Toda T, Sakaida I, Okita K, Oka M, Nakamura K (2003) Proteomic profiling of heat shock protein 70 family members as biomarkers for hepatitis C virus-related hepatocellular carcinoma. Proteomics 3(12):2487–2493. doi:10.1002/pmic.200300621
14. Yoshida S, Hazama S, Tokuno K, Sakamoto K, Takashima M, Tamesa T, Torigoe T, Sato N, Oka M (2009) Concomitant overexpression of heat-shock protein 70 and HLA class-I in hepatitis C virus-related hepatocellular carcinoma. Anticancer Res 29(2):539–544
15. Liao X, Li Y, Bonini C, Nair S, Gilboa E, Greenberg PD, Yee C (2004) Transfection of RNA encoding tumor antigens following maturation of dendritic cells leads to prolonged presentation of antigen and the generation of high-affinity tumor-reactive cytotoxic T lymphocytes. Mol Ther 9(5):757–764. doi:10.1016/j.ymthe.2004.02.011
16. Boczkowski D, Nair SK, Snyder D, Gilboa E (1996) Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med 184(2):465–472
17. Van Tendeloo VF, Ponsaerts P, Lardon F, Nijs G, Lenjou M, Van Broeckhoven C, Van Bockstaele DR, Berneman ZN (2001) Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood 98(1):49–56
18. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45(2):228–247. doi:10.1016/j.ejca.2008.10.026
19. Tan A, Aucejo F, Kim R (2010) Is there a role for adjuvant treatment after hepatic resection for hepatocellular carcinoma? Oncology 78(3–4):161–171. doi:10.1159/000315577
20. Litzow MR, Dietz AB, Bulur PA, Butler GW, Gastineau DA, Hoering A, Fink SR, Letendre L, Padley DJ, Paternoster SF, Tefferi A, Vuk-Pavlovic S (2006) Testing the safety of clinical-grade mature autologous myeloid DC in a phase I clinical immunotherapy trial of CML. Cytotherapy 8(3):290–298. doi:10.1080/14653240600735743
21. Olin MR, Low W, McKenna DH, Haines SJ, Dahlheimer T, Nascene D, Gustafson MP, Dietz AB, Clark HB, Chen W, Blazar B, Ohlfest JR, Moertel C (2014) Vaccination with dendritic cells loaded with allogeneic brain tumor cells for recurrent malignant brain tumors induces a CD4(+)IL17(+) response. J Immunother Cancer 2:4. doi:10.1186/2051-1426-2-4
22. Xie F, Zhang X, Li H, Zheng T, Xu F, Shen R, Yan L, Yang J, He J (2012) Adoptive immunotherapy in postoperative hepatocellular carcinoma: a systemic review. PLoS One 7(8):e42879. doi:10.1371/journal.pone.0042879
23. Tada F, Abe M, Hirooka M, Ikeda Y, Hiasa Y, Lee Y, Jung NC, Lee WB, Lee HS, Bae YS, Onji M (2012) Phase I/II study of immunotherapy using tumor antigen-pulsed dendritic cells in patients with hepatocellular carcinoma. Int J Oncol 41(5):1601–1609. doi:10.3892/ijo.2012.1626
24. Palmer DH, Midgley RS, Mirza N, Torr EE, Ahmed F, Steele JC, Steven NM, Kerr DJ, Young LS, Adams DH (2009) A phase II study of adoptive immunotherapy using dendritic cells pulsed with tumor lysate in patients with hepatocellular carcinoma. Hepatology 49(1):124–132. doi:10.1002/hep.22626
25. Ferrarini M, Heltai S, Zocchi MR, Rugarli C (1992) Unusual expression and localization of heat-shock proteins in human tumor cells. Int J Cancer 51(4):613–619
26. Chuma M, Sakamoto M, Yamazaki K, Ohta T, Ohki M, Asaka M, Hirohashi S (2003) Expression profiling in multistage hepatocarcinogenesis: identification of HSP70 as a molecular marker of early hepatocellular carcinoma. Hepatology 37(1):198–207. doi:10.1053/jhep.2003.50022
27. Elsner L, Muppala V, Gehrmann M, Lozano J, Malzahn D, Bickeboller H, Brunner E, Zientkowska M, Herrmann T, Walter L, Alves F, Multhoff G, Dressel R (2007) The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J Immunol 179(8):5523–5533
28. Takemoto S, Nishikawa M, Guan X, Ohno Y, Yata T, Takakura Y (2010) Enhanced generation of cytotoxic T lymphocytes by heat shock protein 70 fusion proteins harboring both CD8(+) T cell and CD4(+) T cell epitopes. Mol Pharm 7(5):1715–1723. doi:10.1021/mp1001069
29. Ciocca DR, Cayado-Gutierrez N, Maccioni M, Cuello-Carrion FD (2012) Heat shock proteins (HSPs) based anti-cancer vaccines. Curr Mol Med 12(9):1183–1197
30. Calderwood SK, Theriault JR, Gong J (2005) Message in a bottle: role of the 70-kDa heat shock protein family in anti-tumor immunity. Eur J Immunol 35(9):2518–2527. doi:10.1002/eji.200535002
31. Zhang HM, Zhang LW, Ren J, Fan L, Si XM, Liu WC (2006) Induction of alpha-fetoprotein-specific CD4- and CD8-mediated T-cell response using RNA-transfected dendritic cells. Cell Immunol 239(2):144–150. doi:10.1016/j.cellimm.2006.05.004
32. Gilboa E, Vieweg J (2004) Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol Rev 199:251–263. doi:10.1111/j.0105-2896.2004.00139.x
33. Binder RJ (2009) CD40-independent engagement of mammalian hsp70 by antigen-presenting cells. J Immunol 182(11):6844–6850. doi:10.4049/jimmunol.0900026