Changes in plasma biomarkers following treatment with cabozantinib in metastatic castration-resistant prostate cancer: A post hoc analysis of an extension cohort of a phase II trial

Journal of Translational Medicine

Volumn 14, Issue 1, 2016, Pages

  Leibowitz Amit, Raya ^a   Pintilie, Melania ^b   Khoja, Leila ^b   Azad, Arun A ^c   Berger, Raanan ^a   Laird, A Douglas ^d   Aftab, Dana T ^d   Chi, Kim N ^c   Joshua, Anthony M ^b  

^a SHEBA MEDICAL CENTER   (Israel)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

^d EXELIXIS INC   (United States)

Author keywords

Biomarker; C MET; Cabozantinib; Prostate cancer; VEFR; VEGF

Indexed keywords

ALKALINE PHOSPHATASE BONE ISOENZYME; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; CABOZANTINIB; CARBONATE DEHYDRATASE IX; CARRIER PROTEINS AND BINDING PROTEINS; CLUSTERIN; FLT3 LIGAND; INTERLEUKIN 8; PEPTIDES AND PROTEINS; PHOSPHATASE; PROTEIN AXL; PROTEIN GAS6A; PROTEIN TRAP5B; SCATTER FACTOR RECEPTOR; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TUMOR MARKER; UNCLASSIFIED DRUG; ANILIDE; PYRIDINE DERIVATIVE;

ARTICLE; BONE METABOLISM; BONE METASTASIS; BONE SCINTISCANNING; CANCER CHEMOTHERAPY; CASTRATION RESISTANT PROSTATE CANCER; COHORT ANALYSIS; CORRELATION COEFFICIENT; CORRELATIONAL STUDY; DRUG RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HYPOXIA; INFLAMMATION; INTRACELLULAR SIGNALING; MAJOR CLINICAL STUDY; PHASE 2 CLINICAL TRIAL (TOPIC); POST HOC ANALYSIS; PROTEIN BLOOD LEVEL; RELIABILITY; BLOOD; CLINICAL TRIAL; MALE; METASTASIS; MIDDLE AGED; NONPARAMETRIC TEST; PATHOLOGY; PHASE 2 CLINICAL TRIAL; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; REPRODUCIBILITY;

ANILIDES; BIOMARKERS, TUMOR; HUMANS; MALE; MIDDLE AGED; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; PYRIDINES; REPRODUCIBILITY OF RESULTS; STATISTICS, NONPARAMETRIC;

EID: 84954461073     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-015-0747-y     Document Type: Article

References (50)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74. doi: 10.1016/j.cell.2011.02.013.
2. Lalonde E, Ishkanian AS, Sykes J, Fraser M, Ross-Adams H, Erho N, et al. Tumour genomic and microenvironmental heterogeneity for integrated prediction of 5-year biochemical recurrence of prostate cancer: a retrospective cohort study. Lancet Oncol. 2014;15(13):1521-32. doi: 10.1016/S1470-2045(14)71021-6.
3. Cooke VG, LeBleu VS, Keskin D, Khan Z, O'Connell JT, Teng Y, et al. Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell. 2012;21(1):66-81. doi: 10.1016/j.ccr.2011.11.024.
4. Ranasinghe WK, Xiao L, Kovac S, Chang M, Michiels C, Bolton D, et al. The role of hypoxia-inducible factor 1alpha in determining the properties of castrate-resistant prostate cancers. PLoS One. 2013;8(1):e54251. doi: 10.1371/journal.pone.0054251.
5. Adamski JK, Estlin EJ, Makin GW. The cellular adaptations to hypoxia as novel therapeutic targets in childhood cancer. Cancer Treat Rev. 2008;34(3):231-46. doi: 10.1016/j.ctrv.2007.11.005.
6. McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget. 2012;3(1):84-97.
7. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 2003;3(4):347-61.
8. Liu T, Mendes DE, Berkman CE. From AR to c-Met: androgen deprivation leads to a signaling pathway switch in prostate cancer cells. Int J Oncol. 2013;43(4):1125-30. doi: 10.3892/ijo.2013.2020.
9. Knudsen BS, Gmyrek GA, Inra J, Scherr DS, Vaughan ED, Nanus DM, et al. High expression of the Met receptor in prostate cancer metastasis to bone. Urology. 2002;60(6):1113-7.
10. Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyronet D, et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell. 2012;22(1):21-35. doi: 10.1016/j.ccr.2012.05.037.
11. Ryan CJ, Smith MR, de Bono JS, Molina A, Logothetis CJ, de Souza P, et al. Abiraterone in metastatic prostate cancer without previous chemotherapy. New Engl J Med. 2013;368(2):138-48. doi: 10.1056/NEJMoa1209096.
12. Smith MR, Sweeney CJ, Corn PG, Rathkopf DE, Smith DC, Hussain M, et al. Cabozantinib in chemotherapy-pretreated metastatic castration-resistant prostate cancer: results of a phase II nonrandomized expansion study. J Clin Oncol: Off J Am Soc Clin Oncol. 2014;32(30):3391-9. doi: 10.1200/JCO.2013.54.5954.
13. Brown MS, Chu GH, Kim HJ, Allen-Auerbach M, Poon C, Bridges J, et al. Computer-aided quantitative bone scan assessment of prostate cancer treatment response. Nucl Med Commun. 2012;33(4):384-94. doi: 10.1097/MNM.0b013e3283503ebf.
14. Murukesh N, Dive C, Jayson GC. Biomarkers of angiogenesis and their role in the development of VEGF inhibitors. Br J Cancer. 2010;102(1):8-18. doi: 10.1038/sj.bjc.6605483.
15. Limaverde-Sousa G, Sternberg C, Ferreira CG. Antiangiogenesis beyond VEGF inhibition: a journey from antiangiogenic single-target to broad-spectrum agents. Cancer Treat Rev. 2014;40(4):548-57. doi: 10.1016/j.ctrv.2013.11.009.
16. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov. 2012;2(3):270-87. doi: 10.1158/2159-8290.CD-11-0240.
17. You WK, Sennino B, Williamson CW, Falcon B, Hashizume H, Yao LC, et al. VEGF and c-Met blockade amplify angiogenesis inhibition in pancreatic islet cancer. Cancer Res. 2011;71(14):4758-68. doi: 10.1158/0008-5472.CAN-10-2527.
18. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P, et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther. 2011;10(12):2298-308. doi: 10.1158/1535-7163.MCT-11-0264.
19. DePrimo S, Wu B, Huang S, Bautista R, Cancilla B, Vysotskaia V, et al. Correlative tumor molecular profiling and plasma biomarker analysis in a phase II study of XL184 in patients with progressive or recurrent glioblastoma multiforme (GBM). ASCO Meet Abstr. 2009;27(15S):2049.
20. Corn PG, Varkaris A, Li N, Tapia EM, Araujo JC, Aparicio A, Tu SM, et al. Modulation of soluble c-Met, bone turnover markers, angiogenic factors, and c-Met in men with mCRPC treated with cabozantinib. ASCO Meet Abstr. 2013;31(6_suppl):58.
21. Jahangiri A, Aghi MK, Carbonell WS. Beta1 integrin: critical path to antiangiogenic therapy resistance and beyond. Cancer Res. 2014;74(1):3-7.
22. Bentzien F, Zuzow M, Heald N, Gibson A, Shi Y, Goon L et al. In vitro and in vivo activity of cabozantinib (XL184), an inhibitor of RET, MET, and VEGFR2, in a model of medullary thyroid cancer. Thyroid. 2013;23(12):1569-77.
23. Li C, Wu JJ, Hynes M, Dosch J, Sarkar B, Welling TH et al. c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology. 2011;141(6):2218-27 e5.
24. Navis AC, Bourgonje A, Wesseling P, Wright A, Hendriks W, Verrijp K, et al. Effects of dual targeting of tumor cells and stroma in human glioblastoma xenografts with a tyrosine kinase inhibitor against c-MET and VEGFR2. PLoS One. 2013;8(3):e58262. doi: 10.1371/journal.pone.0058262.
25. Müller T, DePrimo S, McGrath G, Yu P, Wu J, Goon L, et al. Abstract B269: Pharmacodynamic and correlative biomarker analyses in clinical trials of XL184, an oral, potent inhibitor of MET, VEGFR2, and RET. Mol Cancer Ther. 2009;8(12 Supplement):B269. doi: 10.1158/1535-7163.targ-09-b269.
26. Varkaris A, Corn PG, Efstathiou E, Parikh NU, Song JH, Hoang AG et al. Integration of murine and clinical trials links modulation of the tumor-associated microenvironment to cabozantinib efficacy in mCRPC, Abstract, Prostate Cancer Foundation Scientific Retreat. 2013. http://www.pcf.org/atf/cf/(7c77d6a2-5859-4d60-af47-132fd0f85892)/Andreas_Varkaris.pdf
27. Lin H, Jiang X, Zhu H, Jiang W, Dong X, Qiao H, et al. 2ME2 inhibits the activated hypoxia-inducible pathways by cabozantinib and enhances its efficacy against medullary thyroid carcinoma. Tumour Biol. 2015;. doi: 10.1007/s13277-015-3816-1.
28. Grullich C. Cabozantinib: a MET, RET, and VEGFR2 tyrosine kinase inhibitor. Recent results in cancer research Fortschritte der Krebsforschung Progres dans les recherches sur le cancer. 2014;201:207-14. doi: 10.1007/978-3-642-54490-3_12.
29. Shiozawa Y, Pedersen EA, Patel LR, Ziegler AM, Havens AM, Jung Y, et al. GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia. 2010;12(2):116-27.
30. Mishra A, Wang J, Shiozawa Y, McGee S, Kim J, Jung Y, et al. Hypoxia stabilizes GAS6/Axl signaling in metastatic prostate cancer. Mol Cancer Res MCR. 2012;10(6):703-12. doi: 10.1158/1541-7786.MCR-11-0569.
31. Eisen T, Joensuu H, Nathan PD, Harper PG, Wojtukiewicz MZ, Nicholson S, et al. Regorafenib for patients with previously untreated metastatic or unresectable renal-cell carcinoma: a single-group phase 2 trial. Lancet Oncol. 2012;13(10):1055-62. doi: 10.1016/S1470-2045(12)70364-9.
32. Smith MR, De Bono JS, Sternberg CN, Le Moulec S, Oudard S, De Giorgi U et al. Final analysis of COMET-1: Cabozantinib (Cabo) versus prednisone (Pred) in metastatic castration-resistant prostate cancer (mCRPC) patients (pts) previously treated with docetaxel (D) and abiraterone (A) and/or enzalutamide (E). ASCO Meet Abstr. 2015;33(7_suppl):139.
33. Basch EM, Scholz MC, De Bono JS, Vogelzang NJ, De Souza PL, Marx GM et al. Final analysis of COMET-2: Cabozantinib (Cabo) versus mitoxantrone/prednisone (MP) in metastatic castration-resistant prostate cancer (mCRPC) patients (pts) with moderate to severe pain who were previously treated with docetaxel (D) and abiraterone (A) and/or enzalutamide (E). ASCO Meet Abstr. 2015;33(7_suppl):141.
34. Fiaschi T, Giannoni E, Taddei ML, Cirri P, Marini A, Pintus G, et al. Carbonic anhydrase IX from cancer-associated fibroblasts drives epithelial-mesenchymal transition in prostate carcinoma cells. Cell Cycle. 2013;12(11):1791-801. doi: 10.4161/cc.24902.
35. Kalin M, Cima I, Schiess R, Fankhauser N, Powles T, Wild P, et al. Novel prognostic markers in the serum of patients with castration-resistant prostate cancer derived from quantitative analysis of the pten conditional knockout mouse proteome. Eur Urol. 2011;60(6):1235-43. doi: 10.1016/j.eururo.2011.06.038.
36. Escaff S, Fernandez JM, Gonzalez LO, Suarez A, Gonzalez-Reyes S, Gonzalez JM, et al. Study of matrix metalloproteinases and their inhibitors in prostate cancer. Br J Cancer. 2010;102(5):922-9. doi: 10.1038/sj.bjc.6605569.
37. Fiaschi T, Marini A, Giannoni E, Taddei ML, Gandellini P, De Donatis A, et al. Reciprocal metabolic reprogramming through lactate shuttle coordinately influences tumor-stroma interplay. Cancer Res. 2012;72(19):5130-40. doi: 10.1158/0008-5472.CAN-12-1949.
38. Codony-Servat J, Marin-Aguilera M, Visa L, Garcia-Albeniz X, Pineda E, Fernandez PL, et al. Nuclear factor-kappa B and interleukin-6 related docetaxel resistance in castration-resistant prostate cancer. Prostate. 2013;73(5):512-21. doi: 10.1002/pros.22591.
39. Herman JG, Meadows GG. Increased class 3 semaphorin expression modulates the invasive and adhesive properties of prostate cancer cells. Int J Oncol. 2007;30(5):1231-8.
40. Sharma J, Gray KP, Harshman LC, Evan C, Nakabayashi M, Fichorova R, et al. Elevated IL-8, TNF-alpha, and MCP-1 in men with metastatic prostate cancer starting androgen-deprivation therapy (ADT) are associated with shorter time to castration-resistance and overall survival. Prostate. 2014;74(8):820-8. doi: 10.1002/pros.22788.
41. Culig Z. CXCL8, an underestimated "bad guy" in prostate cancer. Eur Urol. 2013;64(2):189-90. doi: 10.1016/j.eururo.2012.09.024(discussion 90-2).
42. Koltai T. Clusterin: a key player in cancer chemoresistance and its inhibition. OncoTargets Ther. 2014;7:447-56. doi: 10.2147/OTT.S58622.
43. Hegele A, Wahl HG, Varga Z, Sevinc S, Koliva L, Schrader AJ, et al. Biochemical markers of bone turnover in patients with localized and metastasized prostate cancer. BJU Int. 2007;99(2):330-4. doi: 10.1111/j.1464-410X.2006.06604.x.
44. Miyata Y, Sakai H. Thrombospondin-1 in urological cancer: pathological role, clinical significance, and therapeutic prospects. Int J Mol Sci. 2013;14(6):12249-72. doi: 10.3390/ijms140612249.
45. Nassar ZD, Hill MM, Parton RG, Parat MO. Caveola-forming proteins caveolin-1 and PTRF in prostate cancer. Nature Rev Urol. 2013;10(9):529-36. doi: 10.1038/nrurol.2013.168.
46. Vidal SJ, Rodriguez-Bravo V, Quinn SA, Rodriguez-Barrueco R, Lujambio A, Williams E, et al. A targetable GATA2-IGF2 axis confers aggressiveness in lethal prostate cancer. Cancer Cell. 2015;27(2):223-39. doi: 10.1016/j.ccell.2014.11.013.
47. Heidegger I, Kern J, Ofer P, Klocker H, Massoner P. Oncogenic functions of IGF1R and INSR in prostate cancer include enhanced tumor growth, cell migration and angiogenesis. Oncotarget. 2014;5(9):2723-35.
48. Lind AJ, Wikstrom P, Granfors T, Egevad L, Stattin P, Bergh A. Angiopoietin 2 expression is related to histological grade, vascular density, metastases, and outcome in prostate cancer. Prostate. 2005;62(4):394-9. doi: 10.1002/pros.20163.
49. Thoms JW, Dal Pra A, Anborgh PH, Christensen E, Fleshner N, Menard C, et al. Plasma osteopontin as a biomarker of prostate cancer aggression: relationship to risk category and treatment response. Br J Cancer. 2012;107(5):840-6. doi: 10.1038/bjc.2012.345.
50. Doran MG, Spratt DE, Wongvipat J, Ulmert D, Carver BS, Sawyers CL, Evans MJ. Cabozantinib resolves bone scans in tumor-naïve mice harboring skeletal metastasis. Mol Imaging. 2014;13:1-5. doi: 10.2310/7290.2014.00026.