Phase I study of glypican-3-derived peptide vaccine therapy for patients with refractory pediatric solid tumors

OncoImmunology

Volumn 7, Issue 1, 2018, Pages

  Tsuchiya, Nobuhiro ^a   Hosono, Ako ^a   Yoshikawa, Toshiaki ^a   Shoda, Kayoko ^a   Nosaka, Kazuto ^a   Shimomura, Manami ^a   Hara, Junichi ^b   Nitani, Chika ^b   Manabe, Atsushi ^c   Yoshihara, Hiroki ^c   Hosoya, Yosuke ^c   Kaneda, Hide ^d   Kinoshita, Yoshiaki ^e   Kohashi, Kenichi ^f   Yoshimura, Kenichi ^g   Fujinami, Norihiro ^a   Saito, Keigo ^a   Mizuno, Shoichi ^a   Nakatsura, Tetsuya ^a  

^a NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

^b OSAKA CITY GENERAL HOSPITAL   (Japan)

^c ST LUKE'S INTERNATIONAL HOSPITAL   (Japan)

^d NATIONAL CANCER CENTER HOSPITAL   (Japan)

^e KYUSHU UNIVERSITY HOSPITAL   (Japan)

^f KYUSHU UNIVERSITY   (Japan)

^g KANAZAWA UNIVERSITY   (Japan)

Author keywords

CTL; glypican 3 (GPC3); pediatric solid tumors; peptide vaccine; phase I

Indexed keywords

EID: 85030150293     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2017.1377872     Document Type: Article

References (43)

1. Rodriguez-Galindo C, Friedrich P, Alcasabas P, Antillon F, Banavali S, Castillo L, Israels T, Jeha S, Harif M, Sullivan MJ, et al. Toward the Cure of All Children With Cancer Through Collaborative Efforts: Pediatric Oncology As a Global Challenge. J Clin Oncol. 2015;33:3065-73. doi:10.1200/JCO.2014.60.6376
2. Adamson PC. Improving the outcome for children with cancer: Development of targeted new agents. CA Cancer J Clin. 2015;65:212-20. doi:10.3322/caac.21273
3. Fuchs J, Seitz G, Handgretinger R, Schafer J, Warmann SW. Surgical treatment of lung metastases in patients with embryonal pediatric solid tumors: an update. Semin Pediatr Surg. 2012;21:79-87. doi:10.1053/j.sempedsurg.2011.10.008
4. Heiner JP, Miraldi F, Kallick S, Makley J, Neely J, Smith-Mensah WH, Cheung NK. Localization of GD2-specific monoclonal antibody 3F8 in human osteosarcoma. Cancer Res. 1987;47:5377-81.
5. Roth M, Linkowski M, Tarim J, Piperdi S, Sowers R, Geller D, Gill J, Gorlick R. Ganglioside GD2 as a therapeutic target for antibody-mediated therapy in patients with osteosarcoma. Cancer. 2014;120:548-54. doi:10.1002/cncr.28461
6. Dobrenkov K, Ostrovnaya I, Gu J, Cheung IY, Cheung NK. Oncotargets GD2 and GD3 are highly expressed in sarcomas of children, adolescents, and young adults. Pediatr Blood Cancer. 2016;63:1780-5. doi:10.1002/pbc.26097
7. Wang L, Kang FB, Shan BE. B7-H3-mediated tumor immunology: Friend or foe? Int J Cancer. 2014;134:2764-71. doi:10.1002/ijc.28474
8. Zhou LT, Liu FY, Li Y, Peng YM, Liu YH, Li J. Gpnmb/osteoactivin, an attractive target in cancer immunotherapy. Neoplasma. 2012;59:1-5. doi:10.4149/neo_2012_001
9. Oue T, Uehara S, Yamanaka H, Takama Y, Oji Y, Fukuzawa M. Expression of Wilms tumor 1 gene in a variety of pediatric tumors. J Pediatr Surg. 2011;46:2233-8. doi:10.1016/j.jpedsurg.2011.09.004
10. Kushner BH, Cheung IY, Modak S, Kramer K, Ragupathi G, Cheung NK. Phase I trial of a bivalent gangliosides vaccine in combination with beta-glucan for high-risk neuroblastoma in second or later remission. Clin Cancer Res. 2014;20:1375-82. doi:10.1158/1078-0432.CCR-13-1012
11. Hashii Y, Sato E, Ohta H, Oka Y, Sugiyama H, Ozono K. WT1 peptide immunotherapy for cancer in children and young adults. Pediatr Blood Cancer. 2010;55:352-5. doi:10.1002/pbc.22522
12. Filmus J. Glypicans in growth control and cancer. Glycobiology. 2001;11:19R-23R. doi:10.1093/glycob/11.3.19R
13. Song HH, Filmus J. The role of glypicans in mammalian development. Biochim Biophys Acta. 2002;1573:241-6. doi:10.1016/S0304-4165(02)00390-2
14. Kinoshita Y, Tanaka S, Souzaki R, Miyoshi K, Kohashi K, Oda Y, Nakatsura T, Taguchi T. Glypican 3 expression in pediatric malignant solid tumors. Eur J Pediatr Surg. 2015;25:138-44.
15. 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. doi:10.1158/1078-0432.CCR-11-3044
16. 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. doi:10.1080/2162402X.2015.1129483
17. 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. doi:10.1080/2162402X.2016.1238542
18. Tsuchiya N, Yoshikawa T, Fujinami N, Saito K, Mizuno S, Sawada Y, et al. Immunological efficacy of glypican-3 peptide vaccine in patients with advanced hepatocellular carcinoma. Oncoimmunology. 2017;e1346764 in press. doi:10.1080/2162402X.2017.1346764.
19. Pearson AD, Federico SM, Aerts I, Hargrave DR, DuBois SG, Iannone R, Geschwindt RD, Wang R, Haluska FG, Trippett TM, et al. A phase 1 study of oral ridaforolimus in pediatric patients with advanced solid tumors. Oncotarget. 2016;7:84736-47.
20. Vo KT, Karski EE, Nasholm NM, Allen S, Hollinger F, Gustafson WC, Long-Boyle JR, Shiboski, S3, Matthay KK, DuBois SG. Phase 1 study of sirolimus in combination with oral cyclophosphamide and topotecan in children and young adults with relapsed and refractory solid tumors. Oncotarget. 2017;8:23851-23861. doi:10.18632/oncotarget.12904.
21. Saikali Z, Sinnett D. Expression of glypican 3 (GPC3) in embryonal tumors. Int J Cancer. 2000;89:418-22. doi:10.1002/1097-0215(20000920)89:5%3c418::AID-IJC4%3e3.0.CO;2-I
22. Toretsky JA, Zitomersky NL, Eskenazi AE, Voigt RW, Strauch ED, Sun CC, Huber R, Meltzer SJ, Schlessinger D. Glypican-3 expression in Wilms tumor and hepatoblastoma. J Pediatr Hematol Oncol. 2001;23:496-9. doi:10.1097/00043426-200111000-00006
23. Maeda D, Ota S, Takazawa Y, Aburatani H, Nakagawa S, Yano T, Taketani Y, Kodama T, Fukayama M. Glypican-3 expression in clear cell adenocarcinoma of the ovary. Mod Pathol. 2009;22:824-32.
24. Aviel-Ronen S, Lau SK, Pintilie M, Lau D, Liu N, Tsao MS, Jothy S. Glypican-3 is overexpressed in lung squamous cell carcinoma, but not in adenocarcinoma. Mod Pathol. 2008;21:817-25. doi:10.1038/modpathol.2008.37
25. Zynger DL, Gupta A, Luan C, Chou PM, Yang GY, Yang XJ. Expression of glypican 3 in hepatoblastoma: an immunohistochemical study of 65 cases. Hum Pathol. 2008;39:224-30. doi:10.1016/j.humpath.2007.06.006
26. 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. doi:10.1016/S0006-291X(03)00908-2
27. Nakatsura T, Nishimura Y. Usefulness of the novel oncofetal antigen glypican-3 for diagnosis of hepatocellular carcinoma and melanoma. BioDrugs. 2005;19:71-7. doi:10.2165/00063030-200519020-00001
28. 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.
29. 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. doi:10.1111/j.1349-7006.2009.01206.x
30. Trobaugh-Lotrario AD, Katzenstein HM. Chemotherapeutic approaches for newly diagnosed hepatoblastoma: past, present, and future strategies. Pediatr Blood Cancer. 2012;59:809-12. doi:10.1002/pbc.24219
31. Semeraro M, Branchereau S, Maibach R, Zsiros J, Casanova M, Brock P, Domerg C, Aronson DC, Zimmermann A, Laithier V, et al. Relapses in hepatoblastoma patients: clinical characteristics and outcome–experience of the International Childhood Liver Tumour Strategy Group (SIOPEL). Eur J Cancer. 2013;49:915-22. doi:10.1016/j.ejca.2012.10.003
32. Frazier AL, Hale JP, Rodriguez-Galindo C, Dang H, Olson T, Murray MJ, Amatruda JF, Thornton C, Arul GS, Billmire D, et al. Revised risk classification for pediatric extracranial germ cell tumors based on 25 years of clinical trial data from the United Kingdom and United States. J Clin Oncol. 2015;33:195-201. doi:10.1200/JCO.2014.58.3369
33. Sawada A, Inoue M, Kondo O, Yamada-Nakata K, Ishihara T, Kuwae Y, Nishikawa M, Ammori Y, Tsuboi A, Oji Y, et al. Feasibility of Cancer Immunotherapy with WT1 Peptide Vaccination for Solid and Hematological Malignancies in Children. Pediatr Blood Cancer. 2016;63:234-41. doi:10.1002/pbc.25792
34. Ortega JA, Douglass EC, Feusner JH, Reynolds M, Quinn JJ, Finegold MJ, Haas JE, King DR, Liu-Mares W, Sensel MG, et al. Randomized comparison of cisplatin/vincristine/fluorouracil and cisplatin/continuous infusion doxorubicin for treatment of pediatric hepatoblastoma: A report from the Children's Cancer Group and the Pediatric Oncology Group. J Clin Oncol. 2000;18:2665-75. doi:10.1200/JCO.2000.18.14.2665
35. Meyers RL, Tiao G, de Ville de Goyet J, Superina R, Aronson DC. Hepatoblastoma state of the art: pre-treatment extent of disease, surgical resection guidelines and the role of liver transplantation. Curr Opin Pediatr. 2014;26:29-36. doi:10.1097/MOP.0000000000000042
36. Zsiros J, Maibach R, Shafford E, Brugieres L, Brock P, Czauderna P, Roebuck D, Childs M, Zimmermann A, Laithier V, et al. Successful treatment of childhood high-risk hepatoblastoma with dose-intensive multiagent chemotherapy and surgery: final results of the SIOPEL-3HR study. J Clin Oncol. 2010;28:2584-90. doi:10.1200/JCO.2009.22.4857
37. Zsiros J, Brugieres L, Brock P, Roebuck D, Maibach R, Zimmermann A, Childs M, Pariente D, Laithier V, Otte JB, et al. Dose-dense cisplatin-based chemotherapy and surgery for children with high-risk hepatoblastoma (SIOPEL-4): a prospective, single-arm, feasibility study. Lancet Oncol. 2013;14:834-42. doi:10.1016/S1470-2045(13)70272-9
38. Heczey A, Louis CU. Advances in chimeric antigen receptor immunotherapy for neuroblastoma. Discovery medicine. 2013;16:287-94.
39. Kopp LM, Katsanis E. Targeted immunotherapy for pediatric solid tumors. Oncoimmunology. 2016;5:e1087637. doi:10.1080/2162402X.2015.1087637
40. Ofuji K, Saito K, Suzuki S, Shimomura M, Shirakawa H, Nobuoka D, Sawada Y, Yoshimura M, Tsuchiya N, Takahashi M, 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. 2017;8:37835-37844. doi:10.18632/oncotarget.14271.
41. 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. doi:10.1007/s13277-016-5127-6
42. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228-47. doi:10.1016/j.ejca.2008.10.026
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. doi:10.1111/j.1349-7006.2011.01896.x