Anticancer activity of the type I insulin-like growth factor receptor antagonist, ganitumab, in combination with the death receptor 5 agonist, conatumumab

Targeted Oncology

Volumn 10, Issue 1, 2015, Pages 65-76

  Tabernero, Josep ^a   Chawla, Sant P ^b   Kindler, Hedy ^c   Reckamp, Karen ^d   Chiorean, E Gabriela ^e   Azad, Nilofer S ^f   Lockhart, A Craig ^g   Hsu, Cheng Pang ^h   Baker, Nigel F ⁱ   Galimi, Francesco ^h   Beltran, Pedro ^h   Baselga, José ^j  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^b Sarcoma Oncology Center   (United States)

^c University of Chicago   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f JOHNS HOPKINS HOSPITAL   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h AMGEN INC   (United States)

ⁱ AMGEN LTD   (United Kingdom)

^j MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

more..

Author keywords

Apoptosis; Death receptor; Insulin like growth factor receptor; Monoclonal antibodies; Targeted therapy; TRAIL

Indexed keywords

ANTINEOPLASTIC AGENT; CONATUMUMAB; GANITUMAB; MONOCLONAL ANTIBODY;

ADULT; AGED; ANIMAL; CLINICAL TRIAL; DRUG SCREENING; FEMALE; HUMAN; MALE; MAXIMUM TOLERATED DOSE; MIDDLE AGED; MOUSE; MULTICENTER STUDY; NEOPLASMS; NUDE MOUSE; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; YOUNG ADULT;

ADULT; AGED; ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; FEMALE; HUMANS; MALE; MAXIMUM TOLERATED DOSE; MICE; MICE, NUDE; MIDDLE AGED; NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 84925319198     PISSN: 17762596     EISSN: 1776260X     Source Type: Journal    
DOI: 10.1007/s11523-014-0315-z     Document Type: Article

References (50)

1. Rodon J, DeSantos V, Ferry RJ Jr, Kurzrock R (2008) Early drug development of inhibitors of the insulin-like growth factor-I receptor pathway: lessons from the first clinical trials. Mol Cancer Ther 7(9):2575–2588. doi:10.1158/1535-7163.MCT-08-0265
2. Molife LR, Fong PC, Paccagnella L, Reid AH, Shaw HM, Vidal L, Arkenau HT, Karavasilis V, Yap TA, Olmos D, Spicer J, Postel-Vinay S, Yin D, Lipton A, Demers L, Leitzel K, Gualberto A, de Bono JS (2010) The insulin-like growth factor-I receptor inhibitor figitumumab (CP-751,871) in combination with docetaxel in patients with advanced solid tumours: results of a phase Ib dose-escalation, open-label study. Br J Cancer 103(3):332–339. doi:10.1038/sj.bjc.6605767
3. Tolcher AW, Sarantopoulos J, Patnaik A, Papadopoulos K, Lin CC, Rodon J, Murphy B, Roth B, McCaffery I, Gorski KS, Kaiser B, Zhu M, Deng H, Friberg G, Puzanov I (2009) Phase I, pharmacokinetic, and pharmacodynamic study of AMG 479, a fully human monoclonal antibody to insulin-like growth factor receptor 1. J Clin Oncol 27(34):5800–5807. doi:10.1200/JCO.2009.23.6745
4. Atzori F, Tabernero J, Cervantes A, Prudkin L, Andreu J, Rodriguez-Braun E, Domingo A, Guijarro J, Gamez C, Rodon J, Di Cosimo S, Brown H, Clark J, Hardwick JS, Beckman RA, Hanley WD, Hsu K, Calvo E, Rosello S, Langdon RB, Baselga J (2011) A phase I pharmacokinetic and pharmacodynamic study of dalotuzumab (MK-0646), an anti-insulin-like growth factor-1 receptor monoclonal antibody, in patients with advanced solid tumors. Clin Cancer Res 17(19):6304–6312. doi:10.1158/1078-0432.CCR-10-3336
5. Sachdev D, Yee D (2007) Disrupting insulin-like growth factor signaling as a potential cancer therapy. Mol Cancer Ther 6(1):1–12. doi:10.1158/1535-7163.MCT-06-0080
6. Flanigan SA, Pitts TM, Eckhardt SG, Tentler JJ, Tan AC, Thorburn A, Leong S (2010) The insulin-like growth factor I receptor/insulin receptor tyrosine kinase inhibitor PQIP exhibits enhanced antitumor effects in combination with chemotherapy against colorectal cancer models. Clin Cancer Res 16(22):5436–5446. doi:10.1158/1078-0432.CCR-10-2054
7. Sabbatini P, Rowand JL, Groy A, Korenchuk S, Liu Q, Atkins C, Dumble M, Yang J, Anderson K, Wilson BJ, Emmitte KA, Rabindran SK, Kumar R (2009) Antitumor activity of GSK1904529A, a small-molecule inhibitor of the insulin-like growth factor-I receptor tyrosine kinase. Clin Cancer Res 15(9):3058–3067. doi:10.1158/1078-0432.CCR-08-2530
8. Beltran PJ, Mitchell P, Chung YA, Cajulis E, Lu J, Belmontes B, Ho J, Tsai MM, Zhu M, Vonderfecht S, Baserga R, Kendall R, Radinsky R, Calzone FJ (2009) AMG 479, a fully human anti-insulin-like growth factor receptor type I monoclonal antibody, inhibits the growth and survival of pancreatic carcinoma cells. Mol Cancer Ther 8(5):1095–1105. doi:10.1158/1535-7163.MCT-08-1171
9. Guix M, Faber AC, Wang SE, Olivares MG, Song Y, Qu S, Rinehart C, Seidel B, Yee D, Arteaga CL, Engelman JA (2008) Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 118(7):2609–2619. doi:10.1172/JCI34588
10. Jones HE, Gee JM, Barrow D, Tonge D, Holloway B, Nicholson RI (2006) Inhibition of insulin receptor isoform-A signalling restores sensitivity to gefitinib in previously de novo resistant colon cancer cells. Br J Cancer 95(2):172–180. doi:10.1038/sj.bjc.6603237
11. Hilmi C, Larribere L, Giuliano S, Bille K, Ortonne JP, Ballotti R, Bertolotto C (2008) IGF1 promotes resistance to apoptosis in melanoma cells through an increased expression of BCL2, BCL-X(L), and survivin. J Investig Dermatol 128(6):1499–1505. doi:10.1038/sj.jid.5701185
12. Mendivil A, Zhou C, Cantrell LA, Gehrig PA, Malloy KM, Blok LJ, Burger CW, Bae-Jump VL (2011) AMG 479, a novel IGF-1-R antibody, inhibits endometrial cancer cell proliferation through disruption of the PI3K/Akt and MAPK pathways. Reprod Sci 18(9):832–841. doi:10.1177/1933719111398501
13. Beltran PJ, Chung YA, Moody G, Mitchell P, Cajulis E, Vonderfecht S, Kendall R, Radinsky R, Calzone FJ (2011) Efficacy of ganitumab (AMG 479), alone and in combination with rapamycin, in Ewing's and osteogenic sarcoma models. J Pharmacol Exp Ther. doi:10.1124/jpet.110.178400
14. Chung CH, Pohlmann PR, Rothenberg ML, Burkey BB, Parker J, Palka K, Aulino J, Puzanov I, Murphy B (2011) Insulin-like growth factor-1 receptor inhibitor, AMG-479, in cetuximab-refractory head and neck squamous cell carcinoma. Head Neck 33(12):1804–1808. doi:10.1002/hed.21478
15. Tap WD, Demetri G, Barnette P, Desai J, Kavan P, Tozer R, Benedetto PW, Friberg G, Deng H, McCaffery I, Leitch I, Badola S, Chang S, Zhu M, Tolcher A (2012) Phase II study of ganitumab, a fully human anti-type-1 insulin-like growth factor receptor antibody, in patients with metastatic Ewing family tumors or desmoplastic small round cell tumors. J Clin Oncol. doi:10.1200/JCO.2011.37.2359
16. Kelley SK, Ashkenazi A (2004) Targeting death receptors in cancer with Apo2L/TRAIL. Curr Opin Pharmacol 4(4):333–339. doi:10.1016/j.coph.2004.02.006
17. Rosevear HM, Lightfoot AJ, Griffith TS (2010) Conatumumab, a fully human mAb against death receptor 5 for the treatment of cancer. Curr Opin Investig Drugs 11(6):688–698
18. Wiezorek J, Holland P, Graves J (2010) Death receptor agonists as a targeted therapy for cancer. Clin Cancer Res 16(6):1701–1708. doi:10.1158/1078-0432.CCR-09-1692
19. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104(2):155–162. doi:10.1172/JCI6926
20. Zoog SJ, Ma CY, Kaplan-Lefko PJ, Hawkins JM, Moriguchi J, Zhou L, Pan Y, Hsu CP, Friberg G, Herbst R, Hill J, Juan G (2010) Measurement of conatumumab-induced apoptotic activity in tumors by fine needle aspirate sampling. Cytometry A 77(9):849–860. doi:10.1002/cyto.a.20940
21. Kaplan-Lefko PJ, Graves JD, Zoog SJ, Pan Y, Wall J, Branstetter DG, Moriguchi J, Coxon A, Huard JN, Xu R, Peach ML, Juan G, Kaufman S, Chen Q, Bianchi A, Kordich JJ, Ma M, Foltz IN, Gliniak BC (2010) Conatumumab, a fully human agonist antibody to death receptor 5, induces apoptosis via caspase activation in multiple tumor types. Cancer Biol Ther 9(8):618–631
22. Herbst RS, Kurzrock R, Hong DS, Valdivieso M, Hsu CP, Goyal L, Juan G, Hwang YC, Wong S, Hill JS, Friberg G, LoRusso PM (2010) A first-in-human study of conatumumab in adult patients with advanced solid tumors. Clin Cancer Res 16(23):5883–5891. doi:10.1158/1078-0432.CCR-10-0631
23. Doi T, Murakami H, Ohtsu A, Fuse N, Yoshino T, Yamamoto N, Boku N, Onozawa Y, Hsu CP, Gorski KS, Friberg G, Kawaguchi T, Sasaki T (2011) Phase 1 study of conatumumab, a pro-apoptotic death receptor 5 agonist antibody, in Japanese patients with advanced solid tumors. Cancer Chemother Pharmacol 68(3):733–741. doi:10.1007/s00280-010-1544-1
24. Goetsch L, Gonzalez A, Leger O, Beck A, Pauwels PJ, Haeuw JF, Corvaia N (2005) A recombinant humanized anti-insulin-like growth factor receptor type I antibody (h7C10) enhances the antitumor activity of vinorelbine and anti-epidermal growth factor receptor therapy against human cancer xenografts. Int J Cancer 113(2):316–328. doi:10.1002/ijc.20543
25. Mitsiades CS, Treon SP, Mitsiades N, Shima Y, Richardson P, Schlossman R, Hideshima T, Anderson KC (2001) TRAIL/Apo2L ligand selectively induces apoptosis and overcomes drug resistance in multiple myeloma: therapeutic applications. Blood 98(3):795–804
26. Poulaki V, Mitsiades CS, Kotoula V, Tseleni-Balafouta S, Ashkenazi A, Koutras DA, Mitsiades N (2002) Regulation of Apo2L/tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in thyroid carcinoma cells. Am J Pathol 161(2):643–654. doi:10.1016/S0002-9440(10)64220-4
27. Fischer-Posovszky P, Tornqvist H, Debatin KM, Wabitsch M (2004) Inhibition of death-receptor mediated apoptosis in human adipocytes by the insulin-like growth factor I (IGF-I)/IGF-I receptor autocrine circuit. Endocrinology 145(4):1849–1859. doi:10.1210/en.2003-0985
28. Wang Q, Wang X, Hernandez A, Hellmich MR, Gatalica Z, Evers BM (2002) Regulation of TRAIL expression by the phosphatidylinositol 3-kinase/Akt/GSK-3 pathway in human colon cancer cells. J Biol Chem 277(39):36602–36610. doi:10.1074/jbc.M206306200
29. Pennarun B, Kleibeuker JH, Oenema T, Stegehuis JH, de Vries EG, de Jong S (2011) Inhibition of IGF-1R-dependent PI3K activation sensitizes colon cancer cells specifically to DR5-mediated apoptosis but not to rhTRAIL. Cell Oncol (Dordr) 34(3):245–259. doi:10.1007/s13402-011-0033-9
30. Ashkenazi A, Herbst RS (2008) To kill a tumor cell: the potential of proapoptotic receptor agonists. J Clin Invest 118(6):1979–1990. doi:10.1172/JCI34359
31. Larsson O, Girnita A, Girnita L (2005) Role of insulin-like growth factor 1 receptor signalling in cancer. Br J Cancer 92(12):2097–2101. doi:10.1038/sj.bjc.6602627
32. Samani AA, Yakar S, LeRoith D, Brodt P (2007) The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocr Rev 28(1):20–47. doi:10.1210/er.2006-0001
33. Ewing GP, Goff LW (2010) The insulin-like growth factor signaling pathway as a target for treatment of colorectal carcinoma. Clin Colorectal Cancer 9(4):219–223. doi:10.3816/CCC.2010.n.032
34. Olmos D, Martins AS, Jones RL, Alam S, Scurr M, Judson IR (2011) Targeting the insulin-like growth factor 1 receptor in Ewing's sarcoma: reality and expectations. Sarcoma 2011:402508. doi:10.1155/2011/402508
35. Ho AL, Schwartz GK (2011) Targeting of insulin-like growth factor type 1 receptor in Ewing sarcoma: unfulfilled promise or a promising beginning? J Clin Oncol 29(34):4581–4583. doi:10.1200/JCO.2011.38.2374
36. Rieder S, Michalski CW, Friess H, Kleeff J (2011) Insulin-like growth factor signaling as a therapeutic target in pancreatic cancer. Anticancer Agents Med Chem 11(5):427–433
37. Beauchamp MC, Yasmeen A, Knafo A, Gotlieb WH (2010) Targeting insulin and insulin-like growth factor pathways in epithelial ovarian cancer. J Oncol 2010: doi:10.1155/2010/257058
38. Karp DD, Paz-Ares LG, Novello S, Haluska P, Garland L, Cardenal F, Blakely LJ, Eisenberg PD, Langer CJ, Blumenschein G Jr, Johnson FM, Green S, Gualberto A (2009) Phase II study of the anti-insulin-like growth factor type 1 receptor antibody CP-751,871 in combination with paclitaxel and carboplatin in previously untreated, locally advanced, or metastatic non-small-cell lung cancer. J Clin Oncol 27(15):2516–2522. doi:10.1200/JCO.2008.19.9331
39. Olmos D, Postel-Vinay S, Molife LR, Okuno SH, Schuetze SM, Paccagnella ML, Batzel GN, Yin D, Pritchard-Jones K, Judson I, Worden FP, Gualberto A, Scurr M, de Bono JS, Haluska P (2010) Safety, pharmacokinetics, and preliminary activity of the anti-IGF-1R antibody figitumumab (CP-751,871) in patients with sarcoma and Ewing's sarcoma: a phase 1 expansion cohort study. Lancet Oncol 11(2):129–135. doi:10.1016/S1470-2045(09)70354-7
40. Clopper CJ, Pearson ES (1934) The use of confidence or fiducial limits illustrated in the case of the binomial. Biometricka 26(4):404–413
41. Gombos A, Metzger-Filho O, Dal Lago L, Awada-Hussein A (2012) Clinical development of insulin-like growth factor receptor-1 (IGF-1R) inhibitors: at the crossroad? Investig New Drugs. doi:10.1007/s10637-10012-19811-10630
42. Boone DN, Lee AV (2012) Targeting the insulin-like growth factor receptor: developing biomarkers from gene expression profiling. Crit Rev Oncog 17(2):161–173
43. Camidge DR, Herbst RS, Gordon MS, Eckhardt SG, Kurzrock R, Durbin B, Ing J, Tohnya TM, Sager J, Ashkenazi A, Bray G, Mendelson D (2010) A phase I safety and pharmacokinetic study of the death receptor 5 agonistic antibody PRO95780 in patients with advanced malignancies. Clin Cancer Res 16(4):1256–1263. doi:10.1158/1078-0432.CCR-09-1267
44. Pan Y, Haddad V, Sabin T, Baker N, Hei YJ, Galimi F, Graves J, Huang C, Cottrell S (2011) Predictive value of Fc gamma receptor IIIa genotype in response to conatumumab in three phase II studies. J Clin Oncol 29(suppl):Abstract 3103
45. De Roock W, Biesmans B, De Schutter J, Tejpar S (2009) Clinical biomarkers in oncology: focus on colorectal cancer. Mol Diagn Ther 13(2):103–114. doi:10.2165/01250444-200913020-00004
46. Tan DS, Thomas GV, Garrett MD, Banerji U, de Bono JS, Kaye SB, Workman P (2009) Biomarker-driven early clinical trials in oncology: a paradigm shift in drug development. Cancer J 15(5):406–420. doi:10.1097/PPO.0b013e3181bd0445
47. Haluska P, Shaw HM, Batzel GN, Yin D, Molina JR, Molife LR, Yap TA, Roberts ML, Sharma A, Gualberto A, Adjei AA, de Bono JS (2007) Phase I dose escalation study of the anti insulin-like growth factor-I receptor monoclonal antibody CP-751,871 in patients with refractory solid tumors. Clin Cancer Res 13(19):5834–5840. doi:10.1158/1078-0432.CCR-07-1118
48. Hidalgo M, Tirado Gomez M, Lewis N, Vuky JL, Taylor G (2008) A phase I study of MK-0646, a humanized monoclonal antibody against the insulin-like growth factor receptor type 1 (IGF1R) in advanced solid tumor patients in a q2 wk schedule. J Clin Oncol 26(Suppl):3520
49. Tolcher AW, Mita M, Meropol NJ, von Mehren M, Patnaik A, Padavic K, Hill M, Mays T, McCoy T, Fox NL, Halpern W, Corey A, Cohen RB (2007) Phase I pharmacokinetic and biologic correlative study of mapatumumab, a fully human monoclonal antibody with agonist activity to tumor necrosis factor-related apoptosis-inducing ligand receptor-1. J Clin Oncol 25(11):1390–1395. doi:10.1200/JCO.2006.08.8898
50. Plummer R, Attard G, Pacey S, Li L, Razak A, Perrett R, Barrett M, Judson I, Kaye S, Fox NL, Halpern W, Corey A, Calvert H, de Bono J (2007) Phase 1 and pharmacokinetic study of lexatumumab in patients with advanced cancers. Clin Cancer Res 13(20):6187–6194. doi:10.1158/1078-0432.CCR-07-0950