Recent developments with immunotherapy for hepatocellular carcinoma

References

• Llovet JM, Ricci S, Mazzaferro V, et al. SHARP investigators study group. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359:378–390.
   PubMed Web of Science ®Google Scholar
• 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;56:908–943.
   PubMed Web of Science ®Google Scholar
• Waidmann O, Trojan J. Novel drugs in clinical development for hepatocellular carcinoma. Expert Opin Investig Drugs. 2015;24:1075–1082.
   PubMed Web of Science ®Google Scholar
• Trojan J, Waidmann O. Role of regorafenib as second-line therapy and landscape of investigational treatment options in advanced hepatocellular carcinoma. J Hepatocell Carcinoma. 2016;3:31–36.
   PubMed Web of Science ®Google Scholar
• Bruix J, Qin S, Merle P, et al. Regorafenib for patients with hepatocellular carcinoma who progressed on sorafenib treatment (RESORCE): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2017;389:56–66.
   PubMed Web of Science ®Google Scholar
• Abou-Alfa GK,Meyer T,Cheng AL, et al. Cabozantinib in patients with advanced and progressing hepatocellular carcinoma.n. Engl J Med. 2018;379:54-63.
   PubMed Web of Science ®Google Scholar
• Kudo M, Finn RS, Qin S, et al. Lenvatinib versus sorafenib in first-line treatment of patients with unresectable hepatocellular carcinoma: a randomised phase 3 non-inferiority trial. Lancet. 2018;391:1163-1173.
   PubMed Web of Science ®Google Scholar
• Prieto J, Melero I, Sangro B. Immunological landscape and immunotherapy of hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol. 2015;12:681–700.
   PubMed Web of Science ®Google Scholar
• Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359:1350–1355.
   PubMed Web of Science ®Google Scholar
• Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378:158–168.
   PubMed Web of Science ®Google Scholar
• Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711–723.
   PubMed Web of Science ®Google Scholar
• Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320–330.
   PubMed Web of Science ®Google Scholar
• Robert C, Schachter J, Long GV, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med. 2015;372:2521–2532.
   PubMed Web of Science ®Google Scholar
• El-Khoueiry AB, Sangro B, Yau T, et al. Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): an open-label, non-comparative, phase 1/2 dose escalation and expansion trial. Lancet. 2017;389:2492–2502.
   PubMed Web of Science ®Google Scholar
• Lee CH, Yelensky R, Jooss K, et al. Update on tumor neoantigens and their utility: why it is good to be different. Trends Immunol. 2018;39:536–548.
   PubMed Web of Science ®Google Scholar
• Hellmann MD, Ciuleanu TE, Pluzanski A, et al. Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 2018;378:2093–2104.
   PubMed Web of Science ®Google Scholar
• Johnson DB, Balko JM, Compton ML, et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med. 2016;375:1749–1755.
   PubMed Web of Science ®Google Scholar
• Loomba R, Liang TJ. Hepatitis B reactivation associated with immune suppressive and biological modifier therapies: current concepts, management strategies, and future directions. Gastroenterology. 2017;152:1297–1309.
   PubMed Web of Science ®Google Scholar
• Lake AC. Hepatitis B reactivation in a long-term nonprogressor due to nivolumab therapy. AIDS. 2017;31:2115–2118.
   PubMed Web of Science ®Google Scholar
• Torres HA, Hosry J, Mahale P, et al. Hepatitis C virus reactivation in patients receiving cancer treatment: A prospective observational study. Hepatology. 2018;67:36–47.
   PubMed Web of Science ®Google Scholar
• Sangro B, Melero I, Yau T, et al. Nivolumab in sorafenib-naive and -experienced patients with advanced hepatocellular carcinoma (HCC): survival, hepatic safety, and biomarker assessments in checkMate 040. Hepatology. 2017;66:82a.abstract141.
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Chiarion-Sileni V, Gonzalez R, et al. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2017;377:1345–1356.
   PubMed Web of Science ®Google Scholar
• Bruix J, Takayama T, Mazzaferro V, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2015;16:1344–1354.
   PubMed Web of Science ®Google Scholar
• Zhu AX, Finn RS, Edeline J, et al. Pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib (KEYNOTE-224): a non-randomised, open-label phase 2 trial. Lancet Oncol. 2018 Jun 1. [Epub ahead of print].
   Web of Science ®Google Scholar
• Sangro B, Gomez-Martin C, de la Mata M, et al. A clinical trial of CTLA-4 blockade with tremelimumab in patients with hepatocellular carcinoma and chronic hepatitis C. J Hepatol. 2013;59:81–88.
   PubMed Web of Science ®Google Scholar
• Duffy AG, Ulahannan SV, Makorova-Rusher O, et al. Tremelimumab in combination with ablation in patients with advanced hepatocellular carcinoma. J Hepatol. 2017;66:545–551.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373:23–34.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Tannir NM, McDermott DF, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018;378:1277–1290.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366:2443–2454.
   PubMed Web of Science ®Google Scholar
• Bendell JC, Kim TW, Goh BC, et al. Clinical activity and safety of cobimetinib (cobi) and atezolizumab in colorectal cancer (CRC). J Clin Oncol. 2016 May;34(15_suppl):3502.
   PubMed Web of Science ®Google Scholar
• Hoseini SS, Cheung NV. Immunotherapy of hepatocellular carcinoma using chimeric antigen receptors and bispecific antibodies. Cancer Lett. 2017;399:44–52.
   PubMed Web of Science ®Google Scholar
• Eshhar Z, Waks T, Gross G, et al. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S. 1993;90:720–724.
   PubMed Web of Science ®Google Scholar
• Schuster SJ, Svoboda J, Chong EA, et al. Chimeric antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med. 2017;377:2545–2554.
   PubMed Web of Science ®Google Scholar
• Hsu HC, Cheng W, Lai PL. Cloning and expression of a developmentally regulated transcript MXR7 in hepatocellular carcinoma: biological significance and temporospatial distribution. Cancer Res. 1997;57:5179–5184.
   PubMed Web of Science ®Google Scholar
• D´Aloia MM, Zizzari IG, Sacchetti B, et al. CAR-T cells: the long and winding road to solid tumors. Cell Death Dis. 2018;9:282.
   PubMed Web of Science ®Google Scholar
• Carter PJ, Lazar GA. Next generation antibody drugs: pursuit of the ‘high-hanging fruit’. Nat Rev Drug Discov. 2018;17:197–223.
   PubMed Web of Science ®Google Scholar
• Topp MS, Gökbuget N, Zugmaier G, et al. Phase II trial of the anti-CD19 bispecific T cell-engager blinatumomab shows hematologic and molecular remissions in patients with relapsed or refractory B-precursor acute lymphoblastic leukemia. J Clin Oncol. 2014;32:4134–4140.
   PubMed Web of Science ®Google Scholar
• Ishiguro T, Sano Y, Komatsu SI, et al. An anti-glypican 3/CD3 bispecific T cell-redirecting antibody for treatment of solid tumors. Sci Transl Med. 2017;9:410.
   Web of Science ®Google Scholar
• Mariathasan S, Turley SJ, Nickles D, et al. TGFβ attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018;554:544–548.
   PubMed Web of Science ®Google Scholar
• Tauriello DVF, Palomo-Ponce S, Stork D, et al. TGFβ drives immune evasion in genetically reconstituted colon cancer metastasis. Nature. 2018;554:538–543.
   PubMed Web of Science ®Google Scholar
• Ravi R, Noonan KA, Pham V, et al. Bifunctional immune checkpoint-targeted antibody-ligand traps that simultaneously disable TGFβ enhance the efficacy of cancer immunotherapy. Nat Commun. 2018;9:741.
   PubMed Web of Science ®Google Scholar
• Lan Y, Zhang D, Xu C, et al. Enhanced preclinical antitumor activity of M7824, a bifunctional fusion protein simultaneously targeting PD-L1 and TGF-β. Sci Transl Med. 2018;10:424.
   Web of Science ®Google Scholar
• Strauss J, Heery CR, Schlom J, et al. Phase I trial of M7824 (MSB0011359C), a bifunctional fusion protein targeting PD-L1 and TGFβ, in advanced solid tumors. Clin Cancer Res. 2018;24:1287–1295.
   PubMed Web of Science ®Google Scholar
• Melcher A, Parato K, Rooney CM, et al. Thunder and lightning: immunotherapy and oncolytic viruses collide. Mol Ther: Journal Am Soc Gene Ther. 2011;19:1008–1016.
   PubMed Web of Science ®Google Scholar
• Jebar AH, Errington F, Vile RG, et al. Progress in clinical oncolytic virus-based therapy for hepatocellular carcinoma. J Gen Virol. 2015;96:1533–1550.
   PubMed Web of Science ®Google Scholar
• Heo J, Breitbach CJ, Moon A, et al. Sequential therapy with JX-594, a targeted oncolytic poxvirus, followed by sorafenib in hepatocellular carcinoma: preclinical and clinical demonstration of combination efficacy. Mol Ther. 2011;19:1170–1179.
   PubMed Web of Science ®Google Scholar
• Habib NA, Mitry RR, Sarraf CE, et al. Assessment of growth inhibition and morphological changes in in vitro and in vivo hepatocellular carcinoma models post treatment with dl1520 adenovirus. Cancer Gene Ther. 2002;9:414–420.
   PubMed Web of Science ®Google Scholar
• Heo J, Reid T, Ruo L, et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat Med. 2013;19:329–336.
   PubMed Web of Science ®Google Scholar