Hepatocellular carcinoma from an immunologic perspective

Clinical Cancer Research

Volumn 19, Issue 24, 2013, Pages 6678-6685

  Greten, Tim F ^a   Duffy, Austin G ^a   Korangy, Firouzeh ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; CYTOKINE; CYTOTOXIC AGENT; GLYPICAN 3; GLYPICAN 3 ANTIBODY; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEPATITIS B VACCINE; IPILIMUMAB; MONOCLONAL ANTIBODY; ONCOLYTIC VIRUS; PEXASTIMOGENE DEVACIREPVEC; PROTEIN ANTIBODY; SORAFENIB; TICILIMUMAB; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ABSENCE OF SIDE EFFECTS; ADVANCED CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER LOCALIZATION; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER SURGERY; CARCINOMA CELL; CD4+ T LYMPHOCYTE; CELL DEATH; CELLULAR IMMUNITY; CHEMOEMBOLIZATION; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG TOLERABILITY; HEPATITIS B; HEPATITIS C; HUMAN; IMMUNE DEFICIENCY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER SURGERY; LOW DRUG DOSE; MELANOMA; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOFREQUENCY ABLATION; REVIEW; SYSTEMIC THERAPY; TUMOR MICROENVIRONMENT;

CARCINOMA, HEPATOCELLULAR; CTLA-4 ANTIGEN; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY; INFLAMMATION; LIVER NEOPLASMS; ONCOLYTIC VIRUSES; TUMOR MICROENVIRONMENT;

EID: 84890577999     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-1721     Document Type: Review

References (54)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Asghar U, Meyer T. Are there opportunities for chemotherapy in the treatment of hepatocellular cancer? J Hepatol 2012;56:686-95.
3. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc J-F, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-90.
4. Chang MH, Chen CJ, Lai MS, Hsu HM, Wu T-C, Kong MS, et al. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. N Engl J Med 1997;336:1855-9. (Pubitemid 27263972)
5. Park EJ, Lee JH, Yu G-Y, He G, Ali SR, Holzer RG, et al. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010;140:197-208.
6. Starley BQ, Calcagno CJ, Harrison SA. Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology 2010;51:1820-32.
7. Centers for disease control and prevention: overweight and obesity [Internet]. [cited 2013 May 20]. Available from: www.cdc.gov/obesity/data/adult. html
8. Mizukoshi E, Nakamoto Y, Arai K, Yamashita T, Sakai A, Sakai Y, et al. Comparative analysis of various tumor-associated antigen-specific t-cell responses in patients with hepatocellular carcinoma. Hepatology 2011;53:1206-16.
9. Korangy F, Ormandy LA, Bleck JS, Klempnauer J, Wilkens L, Manns MP, et al. Spontaneous tumor-specific humoral and cellular immune responses to NY-ESO-1 in hepatocellular carcinoma. Clin Cancer Res 2004;10:4332-41. (Pubitemid 38878871)
10. Fu J, Xu D, Liu Z, Shi M, Zhao P, Fu B, et al. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 2007;132: 2328-39. (Pubitemid 46890865)
11. Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS, et al. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 2007;25:2586-93. (Pubitemid 47041232)
12. Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009;50:799-807.
13. Arihara F, Mizukoshi E, Kitahara M, Takata Y, Arai K, Yamashita T, et al. Increase in CD14(+)HLA-DR (-/low) myeloid-derived suppressor cells in hepatocellular carcinoma patients and its impact on prognosis. Cancer Immunol Immunother 2013;62:1421-30.
14. Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Impact of an inflammation-based prognostic system on patients undergoing surgery for hepatocellular carcinoma: a retrospective study of 398 Japanese patients. Am J Surg 2012;203:101-6.
15. Pinato DJ, Stebbing J, Ishizuka M, Khan SA, Wasan HS, North BV, et al. A novel and validated prognostic index in hepatocellular carcinoma: The inflammation based index (IBI). J Hepatol 2012; 57:1013-20.
16. Hoshida Y, Moeini A, Alsinet C, Kojima K, Villanueva A. Gene signatures in the management of hepatocellular carcinoma. Semin Oncol 2012;39:473-85.
17. Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 2008;359:1995-2004.
18. Budhu A, Forgues M, Ye Q-H, Jia H-L, He P, Zanetti KA, et al. Prediction of venous metastases, recurrence, and prognosis in hepa-tocellular carcinoma based on a unique immune response signature of the liver microenvironment. Cancer Cell 2006;10:99-111. (Pubitemid 44202603)
19. European Association for the Study of the Liver, European Organisation for Research and Treatment of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012; 56: 908-43.
20. Brok den MH, Sutmuller RP, Nierkens S, Bennink EJ, Frielink C, Toonen LW, et al. Efficient loading of dendritic cells following cryo and radio-frequency ablation in combination with immune modulation induces anti-tumour immunity. Br J Cancer 2006;95:896-905. (Pubitemid 44498106)
21. Zerbini A, Pilli M, Penna A, Pelosi G, Schianchi C, Molinari A, et al. Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses. Cancer Res 2006;66:1139-46. (Pubitemid 43165983)
22. Zerbini A, Pilli M, Fagnoni F, Pelosi G, Pizzi MG, Schivazappa S, et al. Increased immunostimulatory activity conferred to antigen-presenting cells by exposure to antigen extract from hepatocellular carcinoma after radiofrequency thermal ablation. J. Immunother 2008;31:271-82. (Pubitemid 351440997)
23. Hansler J, Wissniowski TT, Schuppan D, Witte A, Bernatik T, Hahn EG, et al. Activation and dramatically increased cytolytic activity of tumor specific T lymphocytes after radio-frequency ablation in patients with hepatocellular carcinoma and colorectal liver metastases. World J Gastroenterol 2006;12:3716-21. (Pubitemid 43958380)
24. Mizukoshi E, Yamashita T, Arai K, Sunagozaka H, Ueda T, Arihara F, et al. Enhancement of tumor-associated antigen-specific T cell responses by radiofrequency ablation of hepatocellular carcinoma. Hepatology 2013;57:1448-57.
25. Zerbini A, Pilli M, Laccabue D, Pelosi G, Molinari A, Negri E, et al. Radio-frequency thermal ablation for hepatocellular carcinoma stimulates autologous NK-cell response. Gastroenterology 2010;138:1931-42.
26. Ayaru L, Pereira SP, Alisa A, Pathan AA, Williams R, Davidson B, et al. Unmasking of alpha-fetoprotein-specific CD4(+) T cell responses in hepatocellular carcinoma patients undergoing embolization. J Immunol 2007;178:1914-22. (Pubitemid 46154664)
27. Hiroishi K, Eguchi J, Baba T, Shimazaki T, Ishii S, Hiraide A, et al. Strong CD8(+) T-cell responses against tumor-associated antigens prolong the recurrence-free interval after tumor treatment in patients with hepatocellular carcinoma. J Gastroenterol 2010;45:451-8.
28. Nobuoka D, Motomura Y, Shirakawa H, Yoshikawa T, Kuronuma T, Takahashi M, et al. Radiofrequency ablation for hepatocellular carcinoma induces glypican-3 peptide-specific cytotoxic T lymphocytes. Int J Oncol 2012;40:63-70.
29. Wu F, Wang Z-B, Lu P, Xu Z-L, Chen W-Z, Zhu H, et al. Activated anti-tumor immunity in cancer patients after high intensity focused ultrasound ablation. Ultrasound Med Biol 2004;30:1217-22. (Pubitemid 39531627)
30. Zeng Z, Shi F, Zhou L, Zhang M-N, Chen Y, Chang X-J, et al. Upre-gulation of circulating PD-L1/PD-1 is associated with poor post-cryoablation prognosis in patients with HBV-related hepatocellular carcinoma. Luk J, editor. PLoS ONE 2011;6:e23621.
31. Greten TF, Korangy F. Radiofrequency ablation for the treatment of HCC-maybe much more than simple tumor destruction? J Hepatol 2010;53:775-6.
32. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunos-timulation by anticancer drugs. Nat Rev Drug Discov 2012;11:215-33.
33. Kapanadze T, Gamrekelashvili J, Ma C, Chan C, Zhao F, Hewitt S, et al. Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma. J Hepatol. 2013 Jun 22. [Epub ahead of print].
34. Cabrera R, Ararat M, Xu Y, Brusko T, Wasserfall C, Atkinson MA, et al. Immune modulation of effector CD4+ and regulatory T cell function by sorafenib in patients with hepatocellular carcinoma. Cancer Immunol Immunother 2013;62:737-46.
35. Nagai H, Mukozu T, Matsui D, Kanekawa T, Kanayama M, Waku N, et al. Sorafenib prevents escape from host immunity in liver cirrhosis patients with advanced hepatocellular carcinoma. Clin Dev Immunol 9 ed. Hindawi Publishing Corporation;2012; 2012:1-8.
36. Greten TF, Manns MP, Korangy F. Immunotherapy of HCC. Rev Recent Clin Trials 2008;3:31-9. (Pubitemid 351267024)
37. Greten TF, Manns MP, Korangy F. Immunotherapy of hepatocellular carcinoma. J Hepatol 2006;45:868-78. (Pubitemid 44646691)
38. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer 2009;9:64-71.
39. Mastrangelo MJ, Maguire HC, Eisenlohr LC, Laughlin CE, Monken CE, McCue PA, et al. Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther 1999;6:409-22. (Pubitemid 129667814)
40. Park B-H, Hwang T, Liu T-C, Sze DY, Kim J-S, Kwon H-C, et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol 2008;9:533-42.
41. Heo J, Reid T, Ruo L, Breitbach CJ, Rose S, Bloomston M, et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat Med 2013;19:329-36.
42. Liu T-C, Hwang T, Park B-H, Bell J, Kirn DH. The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol Ther 2008;16:1637-42.
43. Capurro M, Wanless IR, Sherman M, Deboer G, Shi W, Miyoshi E, et al. Glypican-3: a novel serum and histochemical markerfor hepatocellular carcinoma. Gastroenterology 2003;125:89-97. (Pubitemid 36799110)
44. Filmus J, Capurro M. Glypican-3: a marker and a therapeutic target in hepatocellular carcinoma. FEBS J 2013;280:2471-6.
45. International Consensus Group for Hepatocellular Neoplasia The International Consensus Group for Hepatocellular Neoplasia. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology 2009;49:658-64.
46. Capurro MI, Xiang Y-Y, Lobe C, Filmus J. Glypican-3 promotes the growth of hepatocellular carcinoma by stimulating canonical Wnt signaling. Cancer Res 2005;65:6245-54. (Pubitemid 40994410)
47. Sawada Y, Yoshikawa T, Nobuoka D, Shirakawa H, Kuronuma T, Motomura Y, et al. Phase I trial of a glypican-3-derived peptide vaccine for advanced hepatocellular carcinoma: immunologic evidence and potential for improving overall survival. Clin Cancer Res 2012;18: 3686-96.
48. Sawada Y, Yoshikawa T, Fujii S, Mitsunaga S, Nobuoka D, Mizuno S, et al. Remarkable tumor lysis in a hepatocellular carcinoma patient immediately following glypican-3-derived peptide vaccination: An autopsy case. Hum Vaccin Immunother 2013;9:1228-33.
49. Feng M, Gao W, Wang R, Chen W, Man YG, Figg WD, et al. Therapeutically targeting glypican-3 via a conformation-specific single-domain antibody in hepatocellular carcinoma. Proc Natl Acad Sci 2013;110:E1083-91.
50. Melero I, Hervas-Stubbs S, Glennie M, Pardoll DM, Chen L. Immu-nostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 2007;7:95-106. (Pubitemid 46160986)
51. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumabin patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
52. Sangro B, Gomez-Martin C, la Mata de M, Inarrairaegui M, Garralda E, Barrera P, et al. A clinical trial of CTLA-4 blockade with tremelimumab in patients with hepatocellular carcinoma and chronic hepatitis C. J Hepatol 2013;59:81-8.
53. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 2012;366:925-31.
54. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbe C, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009;15: 7412-20.