Immunological efficacy of glypican-3 peptide vaccine in patients with advanced hepatocellular carcinoma

OncoImmunology

Volumn 6, Issue 10, 2017, Pages

  Tsuchiya, Nobuhiro ^a,b   Yoshikawa, Toshiaki ^a   Fujinami, Norihiro ^a   Saito, Keigo ^a   Mizuno, Shoichi ^a   Sawada, Yu ^a,b   Endo, Itaru ^b   Nakatsura, Tetsuya ^a  

^a NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

^b YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

CTL; Glypican 3 (GPC3); HCC; immunological efficacy; Peptide vaccine

Indexed keywords

DECARBOXYPROTHROMBIN; GLYPICAN 3; GLYPICAN 3 PEPTIDE VACCINE; GRANZYME B; HLA ANTIGEN CLASS 1; PEPTIDE VACCINE; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER IMMUNOTHERAPY; CANCER STAGING; CELL INFILTRATION; CHEMILUMINESCENCE IMMUNOASSAY; CHILD PUGH SCORE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DISEASE COURSE; DRUG EFFICACY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FEVER; FLOW CYTOMETRY; FOLLOW UP; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; MALE; MIDDLE AGED; OVERALL SURVIVAL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL; PILOT STUDY; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SKIN MANIFESTATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; VACCINATION;

EID: 85026753655     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2017.1346764     Document Type: Article

References (44)

1. Janevska D, Chaloska-Ivanova V, Janevski V. Hepatocellular carcinoma: Risk factors, diagnosis and treatment. Open Access Maced J Med Sci 2015; 3:732-6; PMID: 27275318; https://doi.org/10.3889/oamjms.2015.111
2. Altekruse SF, McGlynn KA, Reichman ME. Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol 2009; 27:1485-91; PMID: 19224838; https://doi.org/10.1200/JCO.2008.20.7753
3. Izumi N. Diagnostic and treatment algorithm of the Japanese society of hepatology: A consensus-based practice guideline. Oncology 2010; 78 Suppl 1:78-86; PMID: 20616588; https://doi.org/10.1159/000315234
4. Fitzmorris P, Shoreibah M, Anand BS, Singal AK. Management of hepatocellular carcinoma. J Cancer Res Clin Oncol 2015; 141:861-76; PMID: 25158999; https://doi.org/10.1007/s00432-014-1806-0
5. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, Luo R, Feng J, Ye S, Yang TS, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: A phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009; 10:25-34; PMID: 19095497; https://doi.org/10.1016/S1470-2045(08)70285-7
6. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359:378-90; PMID: 18650514; https://doi.org/10.1056/NEJMoa0708857
7. Morimoto M, Numata K, Kondo M, Hidaka H, Takada J, Shibuya A, Kobayashi S, Ohkawa S, Okuse C, Morita S, et al. Higher discontinuation and lower survival rates are likely in elderly Japanese patients with advanced hepatocellular carcinoma receiving sorafenib. Hepatol Res 2011; 41:296-302; PMID: 21348907; https://doi.org/10.1111/j.1872-034X.2011.00778.x
8. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID: 20525992; https://doi.org/10.1056/NEJMoa1003466
9. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID: 22658127; https://doi.org/10.1056/NEJMoa1200690
10. Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, et al. Nivolumab versus Everolimus in advanced renal-cell carcinoma. N Engl J Med 2015; 373:1803-13; PMID: 26406148; https://doi.org/10.1056/NEJMoa1510665
11. Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 2015; 373:123-35; PMID: 26028407; https://doi.org/10.1056/NEJMoa1504627
12. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, Teng SL, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 2014; 515:558-62; PMID: 25428503; https://doi.org/10.1038/nature13904
13. Hamanishi J, Mandai M, Ikeda T, Minami M, Kawaguchi A, Murayama T, Kanai M, Mori Y, Matsumoto S, Chikuma S, et al. Safety and antitumor activity of Anti-PD-1 antibody, nivolumab, in patients with Platinum-Resistant ovarian cancer. J Clin Oncol 2015; 33:4015-22; PMID: 26351349; https://doi.org/10.1200/JCO.2015.62.3397
14. Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D, et al. PD-1 Blockade in tumors with mismatch-repair deficiency. N Engl J Med 2015; 372:2509-20; PMID: 26028255; https://doi.org/10.1056/NEJMoa1500596
15. Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med 2015; 372:311-9; PMID: 25482239; https://doi.org/10.1056/NEJMoa1411087
16. Nakatsura T, Nishimura Y. Usefulness of the novel oncofetal antigen glypican-3 for diagnosis of hepatocellular carcinoma and melanoma. BioDrugs 2005; 19:71-7; PMID: 15807627; https://doi.org/10.2165/00063030-200519020-00001
17. Nakatsura T, Yoshitake Y, Senju S, Monji M, Komori H, Motomura Y, Hosaka S, Beppu T, Ishiko T, Kamohara H, et al. Glypican-3, overexpressed specifically in human hepatocellular carcinoma, is a novel tumor marker. Biochem Biophys Res Commun 2003; 306:16-25; PMID: 12788060; https://doi.org/10.1016/S0006-291X(03)00908-2
18. Capurro M, Wanless IR, Sherman M, Deboer G, Shi W, Miyoshi E, Filmus J. Glypican-3: A novel serum and histochemical marker for hepatocellular carcinoma. Gastroenterology 2003; 125:89-97; PMID: 12851874; https://doi.org/10.1016/S0016-5085(03)00689-9
19. Shirakawa H, Kuronuma T, Nishimura Y, Hasebe T, Nakano M, Gotohda N, Takahashi S, Nakagohri T, Konishi M, Kobayashi N, et al. Glypican-3 is a useful diagnostic marker for a component of hepatocellular carcinoma in human liver cancer. Int J Oncol 2009; 34:649-56; PMID: 19212669
20. Shirakawa H, Suzuki H, Shimomura M, Kojima M, Gotohda N, Takahashi S, Nakagohri T, Konishi M, Kobayashi N, Kinoshita T, et al. Glypican-3 expression is correlated with poor prognosis in hepatocellular carcinoma. Cancer Sci 2009; 100:1403-7; PMID: 19496787; https://doi.org/10.1111/j.1349-7006.2009.01206.x
21. Sawada Y, Yoshikawa T, Nobuoka D, Shirakawa H, Kuronuma T, Motomura Y, Mizuno S, Ishii H, Nakachi K, Konishi M, 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; PMID: 22577059; https://doi.org/10.1158/1078-0432.CCR-11-3044
22. Nobuoka D, Kato Y, Gotohda N, Takahashi S, Nakagohri T, Konishi M, Kinoshita T, Nakatsura T. Postoperative serum alpha-fetoprotein level is a useful predictor of recurrence after hepatectomy for hepatocellular carcinoma. Oncol Rep 2010; 24:521-8; PMID: 20596642
23. Ofuji K, Saito K, Suzuki S, Shimomura M, Shirakawa H, Nobuoka D, et al. Perioperative plasma glypican-3 level may enable prediction of the risk of recurrence after surgery in patients with stage I hepatocellular carcinoma. Oncotarget 2016; 8:37835-44; PMID: 28035063; https://doi.org/10.18632/oncotarget.14271
24. Attallah AM, El-Far M, Omran MM, Abdelrazek MA, Attallah AA, Saeed AM, Farid K. GPC-HCC model: A combination of glybican-3 with other routine parameters improves the diagnostic efficacy in hepatocellular carcinoma. Tumour Biol 2016; 37:12571-7; PMID: 27380057; https://doi.org/10.1007/s13277-016-5127-6
25. Sawada Y, Yoshikawa T, Fujii S, Mitsunaga S, Nobuoka D, Mizuno S, Takahashi M, Yamauchi C, Endo I, Nakatsura T. 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; PMID: 23466818; https://doi.org/10.4161/hv.24179
26. Oquinena S, Guillen-Grima F, Inarrairaegui M, Zozaya JM, Sangro B. Spontaneous regression of hepatocellular carcinoma: A systematic review. Eur J Gastroenterol Hepatol 2009; 21:254-7; PMID: 19279469; https://doi.org/10.1097/MEG.0b013e328324b6a2
27. Suzuki S, Sakata J, Utsumi F, Sekiya R, Kajiyama H, Shibata K, Kikkawa F, Nakatsura T. Efficacy of glypican-3-derived peptide vaccine therapy on the survival of patients with refractory ovarian clear cell carcinoma. Oncoimmunology 2016; 5:e1238542; PMID: 27999758; https://doi.org/10.1080/2162402X.2016.1238542
28. Sawada Y, Sakai M, Yoshikawa T, Ofuji K, Nakatsura T. A glypican-3-derived peptide vaccine against hepatocellular carcinoma. Oncoimmunology 2012; 1:1448-50; PMID: 23243625; https://doi.org/10.4161/onci.21351
29. Sawada Y, Yoshikawa T, Ofuji K, Yoshimura M, Tsuchiya N, Takahashi M, Nobuoka D, Gotohda N, Takahashi S, Kato Y, et al. Phase II study of the GPC3-derived peptide vaccine as an adjuvant therapy for hepatocellular carcinoma patients. Oncoimmunology 2016; 5:e1129483; PMID: 27467945; https://doi.org/10.1080/2162402X.2015.1129483
30. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006; 314:126-9; PMID: 16946036; https://doi.org/10.1126/science.1129003
31. Thomas S, Stauss HJ, Morris EC. Molecular immunology lessons from therapeutic T-cell receptor gene transfer. Immunology 2010; 129:170-7; PMID: 20561357; https://doi.org/10.1111/j.1365-2567.2009.03227.x
32. Coccoris M, Straetemans T, Govers C, Lamers C, Sleijfer S, Debets R. T cell receptor (TCR) gene therapy to treat melanoma: Lessons from clinical and preclinical studies. Expert Opin Biol Ther 2010; 10:547-62; PMID: 20146634; https://doi.org/10.1517/14712591003614756
33. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, Kammula US, Royal RE, Sherry RM, Wunderlich JR, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009; 114:535-46; PMID: 19451549; https://doi.org/10.1182/blood-2009-03-211714
34. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DN, Feldman SA, Davis JL, Morgan RA, Merino MJ, Sherry RM, et al. T Cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 2011; 19:620-6; https://doi.org/10.1038/mt.2010.272
35. Morgan RA, Chinnasamy N, Abate-Daga D, Gros A, Robbins PF, Zheng Z, Dudley ME, Feldman SA, Yang JC, Sherry RM, et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 2013; 36:133-51; PMID: 23377668; https://doi.org/10.1097/CJI.0b013e3182829903
36. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 2011; 29:917-24; PMID: 21282551; https://doi.org/10.1200/JCO.2010.32.2537
37. Johnson LA, Heemskerk B, Powell DJ, Jr., Cohen CJ, Morgan RA, Dudley ME, Robbins PF, Rosenberg SA. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J Immunol 2006; 177:6548-59; PMID: 17056587; https://doi.org/10.4049/jimmunol.177.9.6548
38. Vonderheide RH, Nathanson KL. Immunotherapy at large: The road to personalized cancer vaccines. Nat Med 2013; 19:1098-100; PMID: 24013748; https://doi.org/10.1038/nm.3317
39. Fritsch EF, Hacohen N, Wu CJ. Personal neoantigen cancer vaccines: The momentum builds. Oncoimmunology 2014; 3:e29311; PMID: 25101225; https://doi.org/10.4161/onci.29311
40. Trajanoski Z, Maccalli C, Mennonna D, Casorati G, Parmiani G, Dellabona P. Somatically mutated tumor antigens in the quest for a more efficacious patient-oriented immunotherapy of cancer. Cancer Immunol Immunother 2015; 64:99-104; PMID: 25164877; https://doi.org/10.1007/s00262-014-1599-7
41. Chapuis AG, Roberts IM, Thompson JA, Margolin KA, Bhatia S, Lee SM, Sloan HL, Lai IP, Farrar EA, Wagener F, et al. T-Cell therapy using Interleukin-21-Primed Cytotoxic T-Cell lymphocytes combined with Cytotoxic T-Cell Lymphocyte Antigen-4 blockade results in long-term cell persistence and durable tumor regression. J Clin Oncol 2016; 34:3787-95; PMID: 27269940; https://doi.org/10.1200/JCO.2015.65.5142
42. Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis 2010; 30:52-60; PMID: 20175033; https://doi.org/10.1055/s-0030-1247132
43. Yoshikawa T, Nakatsugawa M, Suzuki S, Shirakawa H, Nobuoka D, Sakemura N, Motomura Y, Tanaka Y, Hayashi S, Nakatsura T. HLA-A2-restricted glypican-3 peptide-specific CTL clones induced by peptide vaccine show high avidity and antigen-specific killing activity against tumor cells. Cancer Sci 2011; 102:918-25; PMID: 21281401; https://doi.org/10.1111/j.1349-7006.2011.01896.x
44. Tanaka-Harada Y, Kawakami M, Oka Y, Tsuboi A, Katagiri T, Elisseeva OA, Nishida S, Shirakata T, Hosen N, Fujiki F, et al. Biased usage of BV gene families of T-cell receptors of WT1 (Wilms' tumor gene)-specific CD8+ T cells in patients with myeloid malignancies. Cancer Sci 2010; 101:594-600; PMID: 20132220; https://doi.org/10.1111/j.1349-7006.2009.01453.x