- 1. School of Clinical Medicine, Guizhou Medical University, Guiyang 550000, P. R. China;
- 2. Department of Hepatobiliary Surgery, Affiliated Hospital of Guizhou Medical University, Guiyang 550000, P. R. China;
Citation: YIN Peng, HU Chaoquan. Progress of immune checkpoint inhibitors in treatment of advanced hepatocellular carcinoma. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(4): 524-529. doi: 10.7507/1007-9424.202006125 Copy
1. | Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424. |
2. | Pawlotsky JM. Pathophysiology of hepatitis C virus infection and related liver disease. Trends Microbiol, 2004, 12(2): 96-102. |
3. | Trépo C, Chan HL, Lok A. Hepatitis B virus infection. Lancet, 2014, 384(9959): 2053-2063. |
4. | Morgan TR, Mandayam S, Jamal MM. Alcohol and hepatocellular carcinoma. Gastroenterology, 2004, 127(5 Suppl 1): S87-S96. |
5. | Zhang DY, Friedman SL. Fibrosis-dependent mechanisms of hepatocarcinogenesis. Hepatology, 2012, 56(2): 769-775. |
6. | Bugianesi E, Vanni E, Marchesini G. NASH and the risk of cirrhosis and hepatocellular carcinoma in type 2 diabetes. Curr Diab Rep, 2007, 7(3): 175-180. |
7. | Yang JD, Hainaut P, Gores GJ, et al. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol, 2019, 16(10): 589-604. |
8. | Sangro B, Carpanese L, Cianni R, et al. Survival after yttrium-90 resin microsphere radioembolization of hepatocellular carcinoma across Barcelona clinic liver cancer stages: a European evaluation. Hepatology, 2011, 54(3): 868-878. |
9. | Giannini EG, Farinati F, Ciccarese F, et al. Prognosis of untreated hepatocellular carcinoma. Hepatology, 2015, 61(1): 184-190. |
10. | Meyer T. Treatment of advanced hepatocellular carcinoma: beyond sorafenib. Lancet Gastroenterol Hepatol, 2018, 3(4): 218-220. |
11. | Prieto J, Melero I, Sangro B. Immunological landscape and immunotherapy of hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol, 2015, 12(12): 681-700. |
12. | Nishida N, Kudo M. Immunological microenvironment of hepatocellular carcinoma and its clinical implication. Oncology, 2017, 92 Suppl 1: 40-49. |
13. | Cheng H, Sun G, Chen H, et al. Trends in the treatment of advanced hepatocellular carcinoma: immune checkpoint blockade immunotherapy and related combination therapies. Am J Cancer Res, 2019, 9(8): 1536-1545. |
14. | Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis, 2015, 6(6): e1792. |
15. | Umemoto Y, Okano S, Matsumoto Y, et al. Prognostic impact of programmed cell death 1 ligand 1 expression in human leukocyte antigen class Ⅰ-positive hepatocellular carcinoma after curative hepatectomy. J Gastroenterol, 2015, 50(1): 65-75. |
16. | 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(1): 81-88. |
17. | Huang M, He M, Guo Y, et al. The influence of immune heterogeneity on the effectiveness of immune checkpoint inhibitors in multifocal hepatocellular carcinomas. Clin Cancer Res, 2020, 26(18): 4947-4957. |
18. | Kuang DM, Zhao Q, Peng C, et al. Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J Exp Med, 2009, 206(6): 1327-1337. |
19. | Zhou G, Sprengers D, Boor PPC, et al. Antibodies against immune checkpoint molecules restore functions of tumor-infiltrating T cells in hepatocellular carcinomas. Gastroenterology, 2017, 153(4): 1107-1119.e10. |
20. | Hato T, Goyal L, Greten TF, et al. Immune checkpoint blockade in hepatocellular carcinoma: current progress and future directions. Hepatology, 2014, 60(5): 1776-1782. |
21. | Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res, 2013, 19(19): 5300-5309. |
22. | Tarhini AA, Kirkwood JM. CTLA-4-blocking immunotherapy with ipilimumab for advanced melanoma. Oncology (Williston Park), 2010, 24(14): 1302, 1304. |
23. | Kähler KC, Hauschild A. Treatment and side effect management of CTLA-4 antibody therapy in metastatic melanoma. J Dtsch Dermatol Ges, 2011, 9(4): 277-286. |
24. | Waidmann O. Recent developments with immunotherapy for hepatocellular carcinoma. Expert Opin Biol Ther, 2018, 18(8): 905-910. |
25. | Huz JI, Melis M, Sarpel U. Spontaneous regression of hepatocellular carcinoma is most often associated with tumour hypoxia or a systemic inflammatory response. HPB (Oxford), 2012, 14(8): 500-505. |
26. | Cheng AL, Hsu C, Chan SL, et al. Challenges of combination therapy with immune checkpoint inhibitors for hepatocellular carcinoma. J Hepatol, 2020, 72(2): 307-319. |
27. | Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature, 2006, 439(7077): 682-687. |
28. | Francisco LM, Salinas VH, Brown KE, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med, 2009, 206(13): 3015-3029. |
29. | Nguyen LT, Ohashi PS. Clinical blockade of PD1 and LAG3-potential mechanisms of action. Nat Rev Immunol, 2015, 15(1): 45-56. |
30. | 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(10088): 2492-2502. |
31. | 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, 19(7): 940-952. |
32. | Segal NH, Ou SI, Balmanoukian A, et al. Safety and efficacy of durvalumab in patients with head and neck squamous cell carcinoma: results from a phase Ⅰ/Ⅱ expansion cohort. Eur J Cancer, 2019, 109: 154-161. |
33. | Rexer H, Steiner T, Bergmann L. Nivolumab combined with ipilimumab versus sunitinib monotherapy-SUNNIFORECAST AN 41/16of the AUO: a phase 2, randomized, open-label study in subjects with previously untreated and advanced (unresectable or metastatic) non-clear cell renal cell carcinoma. Urologe A, 2017, 56(6): 802-803. |
34. | Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol, 2015, 33(17): 1974-1982. |
35. | Reck M, Rodríguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med, 2016, 375(19): 1823-1833. |
36. | Kudo M. Immuno-oncology in hepatocellular carcinoma: 2017 update. Oncology, 2017, 93 Suppl 1: 147-159. |
37. | Michot JM, Bigenwald C, Champiat S, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer, 2016, 54: 139-148. |
38. | Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science, 2018, 359(6382): 1350-1355. |
39. | Lin Z, Lu D, Wei X, et al. Heterogeneous responses in hepatocellular carcinoma: the achilles heel of immune checkpoint inhibitors. Am J Cancer Res, 2020, 10(4): 1085-1102. |
40. | Kuo HY, Chiang NJ, Chuang CH, et al. Impact of immune checkpoint inhibitors with or without a combination of tyrosine kinase inhibitors on organ-specific efficacy and macrovascular invasion in advanced hepatocellular carcinoma. Oncol Res Treat, 2020, 43(5): 211-220. |
41. | Cui H, Dai G, Guan J. Programmed cell death protein-1 (PD-1)-targeted immunotherapy for advanced hepatocellular carcinoma in real world. Onco Targets Ther, 2020, 13: 143-149. |
42. | Chen Y, Ramjiawan RR, Reiberger T, et al. CXCR4 inhibition in tumor microenvironment facilitates anti-programmed death receptor-1 immunotherapy in sorafenib-treated hepatocellular carcinoma in mice. Hepatology, 2015, 61(5): 1591-1602. |
43. | Zamarin D, Holmgaard RB, Subudhi SK, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med, 2014, 6(226): 226ra32. |
44. | Duffy AG, Ulahannan SV, Makorova-Rusher O, et al. Tremelimumab in combination with ablation in patients with advanced hepatocellular carcinoma. J Hepatol, 2017, 66(3): 545-551. |
45. | Cui J, Wang N, Zhao H, et al. Combination of radiofrequency ablation and sequential cellular immunotherapy improves progression-free survival for patients with hepatocellular carcinoma. Int J Cancer, 2014, 134(2): 342-351. |
46. | Lee JH, Tak WY, Lee Y, et al. Adjuvant immunotherapy with autologous dendritic cells for hepatocellular carcinoma, randomized phase Ⅱ study. Oncoimmunology, 2017, 6(7): e1328335. |
47. | Shi L, Lin H, Li G, et al. Cisplatin enhances NK cells immunotherapy efficacy to suppress HCC progression via altering the androgen receptor (AR)-ULBP2 signals. Cancer Lett, 2016, 373(1): 45-56. |
48. | Qin S, Bai Y, Lim HY, et al. Randomized, multicenter, open-label study of oxaliplatin plus fluorouracil/leucovorin versus doxorubicin as palliative chemotherapy in patients with advanced hepatocellular carcinoma from Asia. J Clin Oncol, 2013, 31(28): 3501-3508. |
49. | Murawski M, Weeda VB, Maibach R, et al. Hepatocellular carcinoma in children: does modified platinum- and doxorubicin-based chemotherapy increase tumor resectability and change outcome? Lessons learned from the SIOPEL 2 and 3 studies. J Clin Oncol, 2016, 34(10): 1050-1056. |
50. | Burki TK. Palbociclib improves survival in advanced breast cancer. Lancet Oncol, 2017, 18(1): e1. |
51. | Zhou J, Liu M, Sun H, et al. Hepatoma-intrinsic CCRK inhibition diminishes myeloid-derived suppressor cell immunosuppression and enhances immune-checkpoint blockade efficacy. Gut, 2018, 67(5): 931-944. |
52. | Bollard J, Miguela V, Ruiz de Galarreta M, et al. Palbociclib (PD-0332991), a selective CDK4/6 inhibitor, restricts tumour growth in preclinical models of hepatocellular carcinoma. Gut, 2017, 66(7): 1286-1296. |
53. | Takayama T, Sekine T, Makuuchi M, et al. Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet, 2000, 356(9232): 802-807. |
54. | Lee JH, Lee JH, Lim YS, et al. Adjuvant immunotherapy with autologous cytokine-induced killer cells for hepatocellular carcinoma. Gastroenterology, 2015, 148(7): 1383-1391.e6. |
55. | Wang H, Liu A, Bo W, et al. Adjuvant immunotherapy with autologous cytokine-induced killer cells for hepatocellular carcinoma patients after curative resection, a systematic review and meta-analysis. Dig Liver Dis, 2016, 48(11): 1275-1282. |
56. | Nakagawa H, Mizukoshi E, Kobayashi E, et al. Association between high-avidity T-cell receptors, induced by α-fetoprotein-derived peptides, and anti-tumor effects in patients with hepatocellular carcinoma. Gastroenterology, 2017, 152(6): 1395-1406.e10. |
57. | Butterfield LH, Ribas A, Meng WS, et al. T-cell responses to HLA-A*0201 immunodominant peptides derived from alpha-fetoprotein in patients with hepatocellular cancer. Clin Cancer Res, 2003, 9(16 Pt 1): 5902-5908. |
58. | Shao YY, Liu TH, Hsu C, et al. Early alpha-foetoprotein response associated with treatment efficacy of immune checkpoint inhibitors for advanced hepatocellular carcinoma. Liver Int, 2019, 39(11): 2184-2189. |
59. | Gubin MM, Zhang X, Schuster H, et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature, 2014, 515(7528): 577-581. |
60. | 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(3): 329-336. |
61. | Chon HJ, Lee WS, Yang H, et al. Tumor microenvironment remodeling by intratumoral oncolytic vaccinia virus enhances the efficacy of immune-checkpoint blockade. Clin Cancer Res, 2019, 25(5): 1612-1623. |
- 1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
- 2. Pawlotsky JM. Pathophysiology of hepatitis C virus infection and related liver disease. Trends Microbiol, 2004, 12(2): 96-102.
- 3. Trépo C, Chan HL, Lok A. Hepatitis B virus infection. Lancet, 2014, 384(9959): 2053-2063.
- 4. Morgan TR, Mandayam S, Jamal MM. Alcohol and hepatocellular carcinoma. Gastroenterology, 2004, 127(5 Suppl 1): S87-S96.
- 5. Zhang DY, Friedman SL. Fibrosis-dependent mechanisms of hepatocarcinogenesis. Hepatology, 2012, 56(2): 769-775.
- 6. Bugianesi E, Vanni E, Marchesini G. NASH and the risk of cirrhosis and hepatocellular carcinoma in type 2 diabetes. Curr Diab Rep, 2007, 7(3): 175-180.
- 7. Yang JD, Hainaut P, Gores GJ, et al. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol, 2019, 16(10): 589-604.
- 8. Sangro B, Carpanese L, Cianni R, et al. Survival after yttrium-90 resin microsphere radioembolization of hepatocellular carcinoma across Barcelona clinic liver cancer stages: a European evaluation. Hepatology, 2011, 54(3): 868-878.
- 9. Giannini EG, Farinati F, Ciccarese F, et al. Prognosis of untreated hepatocellular carcinoma. Hepatology, 2015, 61(1): 184-190.
- 10. Meyer T. Treatment of advanced hepatocellular carcinoma: beyond sorafenib. Lancet Gastroenterol Hepatol, 2018, 3(4): 218-220.
- 11. Prieto J, Melero I, Sangro B. Immunological landscape and immunotherapy of hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol, 2015, 12(12): 681-700.
- 12. Nishida N, Kudo M. Immunological microenvironment of hepatocellular carcinoma and its clinical implication. Oncology, 2017, 92 Suppl 1: 40-49.
- 13. Cheng H, Sun G, Chen H, et al. Trends in the treatment of advanced hepatocellular carcinoma: immune checkpoint blockade immunotherapy and related combination therapies. Am J Cancer Res, 2019, 9(8): 1536-1545.
- 14. Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis, 2015, 6(6): e1792.
- 15. Umemoto Y, Okano S, Matsumoto Y, et al. Prognostic impact of programmed cell death 1 ligand 1 expression in human leukocyte antigen class Ⅰ-positive hepatocellular carcinoma after curative hepatectomy. J Gastroenterol, 2015, 50(1): 65-75.
- 16. 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(1): 81-88.
- 17. Huang M, He M, Guo Y, et al. The influence of immune heterogeneity on the effectiveness of immune checkpoint inhibitors in multifocal hepatocellular carcinomas. Clin Cancer Res, 2020, 26(18): 4947-4957.
- 18. Kuang DM, Zhao Q, Peng C, et al. Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J Exp Med, 2009, 206(6): 1327-1337.
- 19. Zhou G, Sprengers D, Boor PPC, et al. Antibodies against immune checkpoint molecules restore functions of tumor-infiltrating T cells in hepatocellular carcinomas. Gastroenterology, 2017, 153(4): 1107-1119.e10.
- 20. Hato T, Goyal L, Greten TF, et al. Immune checkpoint blockade in hepatocellular carcinoma: current progress and future directions. Hepatology, 2014, 60(5): 1776-1782.
- 21. Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res, 2013, 19(19): 5300-5309.
- 22. Tarhini AA, Kirkwood JM. CTLA-4-blocking immunotherapy with ipilimumab for advanced melanoma. Oncology (Williston Park), 2010, 24(14): 1302, 1304.
- 23. Kähler KC, Hauschild A. Treatment and side effect management of CTLA-4 antibody therapy in metastatic melanoma. J Dtsch Dermatol Ges, 2011, 9(4): 277-286.
- 24. Waidmann O. Recent developments with immunotherapy for hepatocellular carcinoma. Expert Opin Biol Ther, 2018, 18(8): 905-910.
- 25. Huz JI, Melis M, Sarpel U. Spontaneous regression of hepatocellular carcinoma is most often associated with tumour hypoxia or a systemic inflammatory response. HPB (Oxford), 2012, 14(8): 500-505.
- 26. Cheng AL, Hsu C, Chan SL, et al. Challenges of combination therapy with immune checkpoint inhibitors for hepatocellular carcinoma. J Hepatol, 2020, 72(2): 307-319.
- 27. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature, 2006, 439(7077): 682-687.
- 28. Francisco LM, Salinas VH, Brown KE, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med, 2009, 206(13): 3015-3029.
- 29. Nguyen LT, Ohashi PS. Clinical blockade of PD1 and LAG3-potential mechanisms of action. Nat Rev Immunol, 2015, 15(1): 45-56.
- 30. 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(10088): 2492-2502.
- 31. 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, 19(7): 940-952.
- 32. Segal NH, Ou SI, Balmanoukian A, et al. Safety and efficacy of durvalumab in patients with head and neck squamous cell carcinoma: results from a phase Ⅰ/Ⅱ expansion cohort. Eur J Cancer, 2019, 109: 154-161.
- 33. Rexer H, Steiner T, Bergmann L. Nivolumab combined with ipilimumab versus sunitinib monotherapy-SUNNIFORECAST AN 41/16of the AUO: a phase 2, randomized, open-label study in subjects with previously untreated and advanced (unresectable or metastatic) non-clear cell renal cell carcinoma. Urologe A, 2017, 56(6): 802-803.
- 34. Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol, 2015, 33(17): 1974-1982.
- 35. Reck M, Rodríguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med, 2016, 375(19): 1823-1833.
- 36. Kudo M. Immuno-oncology in hepatocellular carcinoma: 2017 update. Oncology, 2017, 93 Suppl 1: 147-159.
- 37. Michot JM, Bigenwald C, Champiat S, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer, 2016, 54: 139-148.
- 38. Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science, 2018, 359(6382): 1350-1355.
- 39. Lin Z, Lu D, Wei X, et al. Heterogeneous responses in hepatocellular carcinoma: the achilles heel of immune checkpoint inhibitors. Am J Cancer Res, 2020, 10(4): 1085-1102.
- 40. Kuo HY, Chiang NJ, Chuang CH, et al. Impact of immune checkpoint inhibitors with or without a combination of tyrosine kinase inhibitors on organ-specific efficacy and macrovascular invasion in advanced hepatocellular carcinoma. Oncol Res Treat, 2020, 43(5): 211-220.
- 41. Cui H, Dai G, Guan J. Programmed cell death protein-1 (PD-1)-targeted immunotherapy for advanced hepatocellular carcinoma in real world. Onco Targets Ther, 2020, 13: 143-149.
- 42. Chen Y, Ramjiawan RR, Reiberger T, et al. CXCR4 inhibition in tumor microenvironment facilitates anti-programmed death receptor-1 immunotherapy in sorafenib-treated hepatocellular carcinoma in mice. Hepatology, 2015, 61(5): 1591-1602.
- 43. Zamarin D, Holmgaard RB, Subudhi SK, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med, 2014, 6(226): 226ra32.
- 44. Duffy AG, Ulahannan SV, Makorova-Rusher O, et al. Tremelimumab in combination with ablation in patients with advanced hepatocellular carcinoma. J Hepatol, 2017, 66(3): 545-551.
- 45. Cui J, Wang N, Zhao H, et al. Combination of radiofrequency ablation and sequential cellular immunotherapy improves progression-free survival for patients with hepatocellular carcinoma. Int J Cancer, 2014, 134(2): 342-351.
- 46. Lee JH, Tak WY, Lee Y, et al. Adjuvant immunotherapy with autologous dendritic cells for hepatocellular carcinoma, randomized phase Ⅱ study. Oncoimmunology, 2017, 6(7): e1328335.
- 47. Shi L, Lin H, Li G, et al. Cisplatin enhances NK cells immunotherapy efficacy to suppress HCC progression via altering the androgen receptor (AR)-ULBP2 signals. Cancer Lett, 2016, 373(1): 45-56.
- 48. Qin S, Bai Y, Lim HY, et al. Randomized, multicenter, open-label study of oxaliplatin plus fluorouracil/leucovorin versus doxorubicin as palliative chemotherapy in patients with advanced hepatocellular carcinoma from Asia. J Clin Oncol, 2013, 31(28): 3501-3508.
- 49. Murawski M, Weeda VB, Maibach R, et al. Hepatocellular carcinoma in children: does modified platinum- and doxorubicin-based chemotherapy increase tumor resectability and change outcome? Lessons learned from the SIOPEL 2 and 3 studies. J Clin Oncol, 2016, 34(10): 1050-1056.
- 50. Burki TK. Palbociclib improves survival in advanced breast cancer. Lancet Oncol, 2017, 18(1): e1.
- 51. Zhou J, Liu M, Sun H, et al. Hepatoma-intrinsic CCRK inhibition diminishes myeloid-derived suppressor cell immunosuppression and enhances immune-checkpoint blockade efficacy. Gut, 2018, 67(5): 931-944.
- 52. Bollard J, Miguela V, Ruiz de Galarreta M, et al. Palbociclib (PD-0332991), a selective CDK4/6 inhibitor, restricts tumour growth in preclinical models of hepatocellular carcinoma. Gut, 2017, 66(7): 1286-1296.
- 53. Takayama T, Sekine T, Makuuchi M, et al. Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet, 2000, 356(9232): 802-807.
- 54. Lee JH, Lee JH, Lim YS, et al. Adjuvant immunotherapy with autologous cytokine-induced killer cells for hepatocellular carcinoma. Gastroenterology, 2015, 148(7): 1383-1391.e6.
- 55. Wang H, Liu A, Bo W, et al. Adjuvant immunotherapy with autologous cytokine-induced killer cells for hepatocellular carcinoma patients after curative resection, a systematic review and meta-analysis. Dig Liver Dis, 2016, 48(11): 1275-1282.
- 56. Nakagawa H, Mizukoshi E, Kobayashi E, et al. Association between high-avidity T-cell receptors, induced by α-fetoprotein-derived peptides, and anti-tumor effects in patients with hepatocellular carcinoma. Gastroenterology, 2017, 152(6): 1395-1406.e10.
- 57. Butterfield LH, Ribas A, Meng WS, et al. T-cell responses to HLA-A*0201 immunodominant peptides derived from alpha-fetoprotein in patients with hepatocellular cancer. Clin Cancer Res, 2003, 9(16 Pt 1): 5902-5908.
- 58. Shao YY, Liu TH, Hsu C, et al. Early alpha-foetoprotein response associated with treatment efficacy of immune checkpoint inhibitors for advanced hepatocellular carcinoma. Liver Int, 2019, 39(11): 2184-2189.
- 59. Gubin MM, Zhang X, Schuster H, et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature, 2014, 515(7528): 577-581.
- 60. 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(3): 329-336.
- 61. Chon HJ, Lee WS, Yang H, et al. Tumor microenvironment remodeling by intratumoral oncolytic vaccinia virus enhances the efficacy of immune-checkpoint blockade. Clin Cancer Res, 2019, 25(5): 1612-1623.
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