Efficacy evaluation of combination treatment using gemcitabine and radioimmunotherapy with90 y-labeled fully human anti-CD147 monoclonal antibody 059-053 in a BxPC-3 xenograft mouse model of refractory pancreatic cancer

International Journal of Molecular Sciences

Volumn 19, Issue 10, 2018, Pages

  Sugyo, Aya ^a   Tsuji, Atsushi B ^a   Sudo, Hitomi ^a   Koizumi, Mitsuru ^b   Ukai, Yoshinori ^c   Kurosawa, Gene ^d   Kurosawa, Yoshikazu ^d   Saga, Tsuneo ^a,e   Higashi, Tatsuya ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^b CANCER INSTITUTE HOSPITAL   (Japan)

^c Perseus Proteomics   (Japan)

^d FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e KYOTO UNIVERSITY HOSPITAL   (Japan)

Author keywords

Combination therapy; Extracellular matrix metalloproteinase inducer; Gemcitabine; Pancreatic cancer; Radioimmunotherapy

Indexed keywords

CD147 ANTIGEN; DEOXYCYTIDINE; GELATINASE A; GELATINASE B; GEMCITABINE; MONOCLONAL ANTIBODY; YTTRIUM; YTTRIUM-90;

ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CHEMISTRY; DISEASE MODEL; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOUSE; PANCREAS TUMOR; PROCEDURES; RADIOIMMUNOTHERAPY; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; BASIGIN; CELL LINE, TUMOR; DEOXYCYTIDINE; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; PANCREATIC NEOPLASMS; RADIOIMMUNOTHERAPY; YTTRIUM RADIOISOTOPES;

EID: 85054078261     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms19102979     Document Type: Article

References (41)

1. Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2018. CA Cancer J. Clin. 2018, 68, 7–30. [CrossRef] [PubMed]
2. Gong, J.; Tuli, R.; Shinde, A.; Hendifar, A.E. Meta-analyses of treatment standards for pancreatic cancer. Mol. Clin. Oncol. 2016, 4, 315–325. [CrossRef] [PubMed]
3. Rahib, L.; Smith, B.D.; Aizenberg, R.; Rosenzweig, A.B.; Fleshman, J.M.; Matrisian, L.M. Projecting cancer incidence and deaths to 2030: The unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014, 74, 2913–2921. [CrossRef] [PubMed]
4. Narayanan, V.; Weekes, C.D. Molecular therapeutics in pancreas cancer. World J. Gastrointest. Oncol. 2016, 8, 366–379. [CrossRef] [PubMed]
5. Gnanamony, M.; Gondi, C.S. Chemoresistance in pancreatic cancer: Emerging concepts. Oncol. Lett. 2017, 13, 2507–2513. [CrossRef] [PubMed]
6. Riethdorf, S.; Reimers, N.; Assmann, V.; Kornfeld, J.-W.; Terracciano, L.; Sauter, G.; Pantel, K. High incidence of EMMPRIN expression in human tumors. Int. J. Cancer 2006, 119, 1800–1810. [CrossRef] [PubMed]
7. Weidle, U.H.; Scheuer, W.; Eggle, D.; Klostermann, S.; Stockinger, H. Cancer-related issues of CD147. Cancer Genom. Proteom. 2010, 7, 157–169.
8. Chen, Y.; Gou, X.; Kong, D.K.; Wang, X.; Wang, J.; Chen, Z.; Huang, C.; Zhou, J. EMMPRIN regulates tumor growth and metastasis by recruiting bone marrow-derived cells through paracrine signaling of SDF-1 and VEGF. Oncotarget 2015, 6, 32575–32585. [CrossRef] [PubMed]
9. Guo, H.M.; Li, R.S.; Zucker, S.; Toole, B.P. EMMPRIN (CD147), an inducer of matrix metalloproteinase synthesis, also binds interstitial collagenase to the tumor cell surface. Cancer Res. 2000, 60, 888–891. [PubMed]
10. Koga, K.; Nabeshima, K.; Aoki, M.; Kawakami, T.; Hamasaki, M.; Toole, B.P.; Nakayama, J.; Iwasaki, H. Emmprin in epithelioid sarcoma: Expression in tumor cell membrane and stimulation of MMP-2 production in tumor-associated fibroblasts. Int. J. Cancer 2007, 120, 761–768. [CrossRef] [PubMed]
11. Zucker, S.; Hymowitz, M.; Rollo, E.E.; Mann, R.; Conner, C.E.; Cao, J.; Foda, H.D.; Tompkins, D.C.; Toole, B.P. Tumorigenic potential of extracellular matrix metalloproteinase inducer. Am. J. Pathol. 2001, 158, 1921–1928. [CrossRef]
12. 131 I) metuximab injection: Clinical phase I/II trials. Int. J. Radiat. Oncol. Biol. Phys. 2006, 65, 435–444. [CrossRef] [PubMed]
13. Xu, J.; Shen, Z.-Y.; Chen, X.-G.; Zhang, Q.; Bian, H.-J.; Zhu, P.; Xu, H.-Y.; Song, F.; Yang, X.-M.; Mi, L.; et al. A randomized controlled trial of Licartin for preventing hepatoma recurrence after liver transplantation. Hepatology 2007, 45, 269–276. [CrossRef] [PubMed]
14. Kurosawa, G.; Akahori, Y.; Morita, M.; Sumitomo, M.; Sato, N.; Muramatsu, C.; Eguchi, K.; Matsuda, K.; Takasaki, A.; Tanaka, M.; et al. Comprehensive screening for antigens overexpressed on carcinomas via isolation of human mAbs that may be therapeutic. Proc. Natl. Acad. Sci. USA 2008, 105, 7287–7292. [CrossRef] [PubMed]
15. 89 Zr-labeled human anti-CD147 monoclonal antibody as a positron emission tomography probe in a mouse model of pancreatic cancer. PLoS ONE 2013, 8, e61230. [CrossRef] [PubMed]
16. Graves, S.S.; Dearstyne, E.; Lin, Y.; Zuo, Y.; Sanderson, J.; Schultz, J.; Pantalias, A.; Gray, D.; Axworthy, D.; Jones, H.M.; et al. Combination therapy with Pretarget CC49 radioimmunotherapy and gemcitabine prolongs tumor doubling time in a murine xenograft model of colon cancer more effectively than either monotherapy. Clin. Cancer Res. 2003, 9, 3712–3721. [PubMed]
17. Shibamoto, Y.; Manabe, T.; Baba, N.; Sasai, K.; Takahashi, M.; Tobe, T.; Abe, M. High dose, external beam and intraoperative radiotherapy in the treatment of resectable and unresectable pancreatic cancer. Int. J. Radiat. Oncol. Biol. Phys. 1990, 19, 605–611. [CrossRef]
18. Oonishi, K.; Cui, X.; Hirakawa, H.; Fujimori, A.; Kamijo, T.; Yamada, S.; Yokosuka, O.; Kamada, T. Different effects of carbon ion beams and X-rays on clonogenic survival and DNA repair in human pancreatic cancer stem-like cells. Radiother. Oncol. 2012, 105, 258–265. [CrossRef] [PubMed]
19. 90 Y-Labeled Fully Human Anti-Transferrin Receptor Monoclonal Antibody in Pancreatic Cancer Mouse Models. PLoS ONE 2015, 10, e0123761. [CrossRef] [PubMed]
20. Wolff, R.A.; Evans, D.B.; Gravel, D.M.; Lenzi, R.; Pisters, P.; Lee, J.E.; Janjan, N.A.; Charnsangavej, C.; Abbruzzese, J.L. Phase I trial of gemcitabine combined with radiation for the treatment of locally advanced pancreatic adenocarcinoma. Clin. Cancer Res. 2001, 7, 2246–2253. [PubMed]
21. Shinoto, M.; Yamada, S.; Terashima, K.; Yasuda, S.; Shioyama, Y.; Honda, H.; Kamada, T.; Tsujii, H.; Saisho, H.; Working Group for Pancreas Cancer. Carbon Ion Radiation Therapy with Concurrent Gemcitabine for Patients with Locally Advanced Pancreatic Cancer. Int. J. Radiat. Oncol. Biol. Phys. 2016, 95, 498–504. [CrossRef] [PubMed]
22. Malik, N.K.; May, K.S.; Chandrasekhar, R.; Wee, W.; Flaherty, L.; Iyer, R.; Gibbs, J.; Kuvshinoff, B.; Wilding, G.; Warren, G.; et al. Treatment of locally advanced unresectable pancreatic cancer: A 10-year experience. J. Gastrointest. Oncol. 2012, 3, 326–334. [PubMed]
23. Teague, A.; Lim, K.-H.; Wang-Gillam, A. Advanced pancreatic adenocarcinoma: A review of current treatment strategies and developing therapies. Ther. Adv. Med. Oncol. 2015, 7, 68–84. [CrossRef] [PubMed]
24. Sharkey, R.M.; Karacay, H.; Govindan, S.V.; Goldenberg, D.M. Combination radioimmunotherapy and chemoimmunotherapy involving different or the same targets improves therapy of human pancreatic carcinoma xenograft models. Mol. Cancer Ther. 2011, 10, 1072–1081. [CrossRef] [PubMed]
25. Pauwels, B.; Korst, A.E.C.; Lardon, F.; Vermorken, J.B. Combined modality therapy of gemcitabine and radiation. Oncologist 2005, 10, 34–51. [CrossRef] [PubMed]
26. Small, W.; Berlin, J.; Freedman, G.M.; Lawrence, T.; Talamonti, M.S.; Mulcahy, M.F.; Chakravarthy, A.B.; Konski, A.A.; Zalupski, M.M.; Philip, P.A.; et al. Full-dose gemcitabine with concurrent radiation therapy in patients with nonmetastatic pancreatic cancer: A multicenter phase II trial. J. Clin. Oncol. 2008, 26, 942–947. [CrossRef] [PubMed]
27. Tseng, W.W.; Zhou, S.; To, C.A.; Thall, P.F.; Lazar, A.J.; Pollock, R.E.; Lin, P.P.; Cormier, J.N.; Lewis, V.O.; Feig, B.W. et al. Phase 1 adaptive dose-finding study of neoadjuvant gemcitabine combined with radiation therapy for patients with high-risk extremity and trunk soft tissue sarcoma. Cancer 2015, 121, 3659–3667. [CrossRef] [PubMed]
28. Sier, C.F.M.; Zuidwijk, K.; Zijlmans, H.J.M.A.A.; Hanemaaijer, R.; Mulder-Stapel, A.A.; Prins, F.A.; Dreef, E.J.; Kenter, G.G.; Fleuren, G.J.; Gorter, A. EMMPRIN-induced MMP-2 activation cascade in human cervical squamous cell carcinoma. Int. J. Cancer 2006, 118, 2991–2998. [CrossRef] [PubMed]
29. Jin, J.; Teng, C.; Li, T. Combination therapy versus gemcitabine monotherapy in the treatment of elderly pancreatic cancer: A meta-analysis of randomized controlled trials. Drug Des. Dev. Ther. 2018, 12, 475–480. [CrossRef] [PubMed]
30. 90 Y-labeled anti-α6β4 integrin antibody. Oncotarget 2016, 7, 38835–38844. [CrossRef] [PubMed]
31. Tsuji, A.B.; Sogawa, C.; Sugyo, A.; Sudo, H.; Toyohara, J.; Koizumi, M.; Abe, M.; Hino, O.; Harada, Y.-N.; Furukawa, T.; et al. Comparison of conventional and novel PET tracers for imaging mesothelioma in nude mice with subcutaneous and intrapleural xenografts. Nucl. Med. Biol. 2009, 36, 379–388. [CrossRef] [PubMed]
32. Emami, B.; Lyman, J.; Brown, A.; Coia, L.; Goitein, M.; Munzenrier, J.E.; Shank, B.; Solin, L.J.; Wesson, M. Tolerance of normal tissue to therapeutic irradiation. Int. J. Radiat. Oncol. Biol. Phys. 1991, 21, 109–122. [CrossRef]
33. Yu, X.; Di, Y.; Xie, C.; Song, Y.; He, H.; Li, H.; Pu, X.; Lu, W.; Fu, D.; Jin, C. An in vitro and in vivo study of gemcitabine-loaded albumin nanoparticles in a pancreatic cancer cell line. Int. J. Nanomed. 2015, 10, 6825–6834. [CrossRef] [PubMed]
34. Pandit-Taskar, N.; Modak, S. Norepinephrine Transporter as a Target for Imaging and Therapy. J. Nucl. Med. 2017, 58, 39S–53S. [CrossRef] [PubMed]
35. 177 Lu-Dotatate for Midgut Neuroendocrine Tumors. N. Engl. J. Med. 2017, 376, 125–135. [CrossRef] [PubMed]
36. 225 Ac-PSMA-617 for PSMA-Targeted α-Radiation Therapy of Metastatic Castration-Resistant Prostate Cancer. J. Nucl. Med. 2016, 57, 1941–1944. [CrossRef] [PubMed]
37. 225 Ac)-Lintuzumab (Anti-CD33) and Low-Dose Cytarabine (LDAC) in Older Patients with Untreated Acute Myeloid Leukemia (AML). Blood 2015, 126, 3794.
38. Klee, G.G. Human anti-mouse antibodies. Arch. Pathol. Lab. Med. 2000, 124, 921–923. [PubMed]
39. Sogawa, C.; Tsuji, A.B.; Sudo, H.; Sugyo, A.; Yoshida, C.; Odaka, K.; Uehara, T.; Arano, Y.; Koizumi, M.; Saga, T. C-kit-targeted imaging of gastrointestinal stromal tumor using radiolabeled anti-c-kit monoclonal antibody in a mouse tumor model. Nucl. Med. Biol. 2010, 37, 179–187. [CrossRef] [PubMed]
40. Eckerman, K.F.; Endo, A. MIRD: Radionuclide Data and Decay Schemes; Society of Nuclear Medicine and Molecular Imaging: Reston, VA, USA, 2008.
41. Sudo, H.; Tsuji, A.B.; Sugyo, A.; Ogawa, Y.; Sagara, M.; Saga, T. ZDHHC8 knockdown enhances radiosensitivity and suppresses tumor growth in a mesothelioma mouse model. Cancer Sci. 2012, 103, 203–209. [CrossRef] [PubMed]