Sensitivity of neuroblastoma to the novel kinase inhibitor cabozantinib is mediated by ERK inhibition

Cancer Chemotherapy and Pharmacology

Volumn 76, Issue 5, 2015, Pages 977-987

  Zhang, Linna ^a   Scorsone, Kathleen ^a   Woodfield, Sarah E ^a   Zage, Peter E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cabozantinib; ERK; Neuroblastoma; RET; Retinoic acid; XL184

Indexed keywords

CABOZANTINIB; ISOTRETINOIN; MITOGEN ACTIVATED PROTEIN KINASE; TEMOZOLOMIDE; TOPOTECAN; ANILIDE; ANTINEOPLASTIC AGENT; DACARBAZINE; PROTEIN KINASE INHIBITOR; PROTEIN RET; PYRIDINE DERIVATIVE; RET PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NEUROBLASTOMA; NEUROBLASTOMA CELL; NEUROBLASTOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR XENOGRAFT; WESTERN BLOTTING; ADRENAL GLAND NEOPLASMS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DRUG EFFECTS; DRUG POTENTIATION; DRUG SCREENING; ENZYMOLOGY; IMMUNOCOMPROMIZED PATIENT; ORAL DRUG ADMINISTRATION; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADMINISTRATION, ORAL; ADRENAL GLAND NEOPLASMS; ANILIDES; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CELL SURVIVAL; DACARBAZINE; DRUG SYNERGISM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNOCOMPROMISED HOST; INHIBITORY CONCENTRATION 50; ISOTRETINOIN; MAP KINASE SIGNALING SYSTEM; MICE; NEOPLASM PROTEINS; NEUROBLASTOMA; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-RET; PYRIDINES; TOPOTECAN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84944733990     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-015-2871-z     Document Type: Article

References (57)

1. Ladenstein R, Philip T, Lasset C, Hartmann O, Garaventa A, Pinkerton R et al (2009) Multivariate analysis of risk factors in stage 4 neuroblastoma patients over the age of one year treated with megatherapy and stem-cell transplantation: a report from the European Bone Marrow Transplantation Solid Tumor Registry. J Clin Oncol 16:953-965
2. Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, Haas-Kogan D et al (2009) Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a Children's Oncology Group study. J Clin Oncol 27:1007-1013
3. Zage PE, Kletzel M, Murray K, Marcus R, Castleberry R, Zhang Y et al (2008) Outcomes of the POG 9340/9341/9342 trials for children with high-risk neuroblastoma: a report from the Children's Oncology Group. Pediatr Blood Cancer 51:747-753
4. Lau L, Tai D, Weitzman S, Grant R, Baruchel S, Malkin D (2004) Factors influencing survival in children with recurrent neuroblastoma. J Pediatr Hematol Oncol 26:227-232
5. London WB, Castel V, Monclair T, Ambros PF, Pearson ADJ, Cohn SL et al (2011) Clinical and biologic features predictive of survival after relapse of neuroblastoma: a report from the International Neuroblastoma Risk Group project. J Clin Oncol 29:3286-3292
6. Matsui T, Sano K, Tsukamoto T, Ito M, Takaishi T, Nakata H et al (1993) Human neuroblastoma cells express alpha and beta platelet-derived growth factor receptors coupling with neurotrophic and chemotactic signaling. J Clin Invest 92:1153-1160
7. Cohen PS, Chan JP, Lipkunskaya M, Biedler JL, Seeger RC (1994) Expression of stem cell factor and c-kit in human neuroblastoma. The Children's Cancer Group. Blood 84:3465-3472
8. Janet T, Ludecke G, Otten U, Unsicker K (1995) Heterogeneity of human neuroblastoma cell lines in their proliferative responses to basic FGF, NGF, and EGF: correlation with expression of growth factors and growth factor receptors. J Neurosci Res 40:707-715
9. Eggert A, Ikegaki N, Kwiatkowski J, Zhao H, Brodeur GM, Himelstein BP (2000) High-level expression of angiogenic factors is associated with advanced tumor stage in human neuroblastomas. Clin Cancer Res 6:1900-1908
10. Langer I, Vertongen P, Perret J, Fontaine J, Atassi G, Robberecht P (2000) Expression of vascular endothelial growth factor (VEGF) and VEGF receptors in human neuroblastomas. Med Pediatr Oncol 34:386-393
11. Hecht M, Papoutsi M, Tran HD, Wilting J, Schweigerer L (2004) Hepatocyte growth factor/c-Met signaling promotes the progression of experimental human neuroblastomas. Cancer Res 64:6109-6118
12. Meyers MB, Shen WP, Spengler BA, Ciccarone V, O'Brien JP, Donner DB et al (1998) Increased epidermal growth factor receptor in multidrug-resistant human neuroblastoma cells. J Cell Biochem 38:87-97
13. Ho R, Minturn JE, Hishiki T, Zhao H, Wang Q, Cnaan A et al (2005) Proliferation of human neuroblastomas mediated by the epidermal growth factor receptor. Cancer Res 65:9868-9875
14. Meister B, Grunebach F, Bautz F, Brugger W, Fink FM, Kanz L, Mohle R (1999) Expression of vascular endothelial growth factor (VEGF) and its receptors in human neuroblastoma. Eur J Cancer 35:445-449
15. Fakhari M, Pullirsch D, Paya K, Abraham D, Hofbauer R, Aharinejad S (2002) Upregulation of vascular endothelial growth factor receptors is associated with advanced neuroblastoma. J Pediatr Surg 37:582-587
16. Crosswell HE, Dasgupta A, Alvarado CS, Watt T, Christensen JG, De P et al (2009) PHA665752, a small-molecule inhibitor of c-Met, inhibits hepatocyte growth factor-stimulated migration and proliferation of c-Met-positive neuroblastoma cells. BMC Cancer 9:411
17. Grüllich C (2014) Cabozantinib: a MET, RET, and VEGFR2 tyrosine kinase inhibitor. Recent Results Cancer Res 201:207-214
18. Viola D, Cappagli V, Elisei R (2013) Cabozantinib (XL184) for the treatment of locally advanced or metastatic progressive medullary thyroid cancer. Future Oncol 9:1083-1092
19. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P et al (2011) Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 10:2298-2308
20. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V et al (2012) Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2:270-287
21. Kurzrock R, Sherman SI, Ball DW, Forastiere AA, Cohen RB, Mehra R et al (2011) Activity of XL184 (Cabozantinib), an oral tyrosine kinase inhibitor, in patients with medullary thyroid cancer. J Clin Oncol 29:2660-2666
22. Gordon MS, Vogelzang NJ, Schoffski P, Daud A, Spira AI, O'Keeffe BA et al (2011) Cabozantinib (XL184) has activity in both soft tissue and bone: results of a phase II randomized discontinuation trial in patients with advanced solid tumors. J Clin Oncol 29:3010
23. Drilon A, Wang L, Hasanovic A, Suehara Y, Lipson D, Stephens P et al (2013) Response to Cabozantinib in patients with RET fusion-positive lung adenocarcinomas. Cancer Discov 3:630-635
24. Smith MR, Sweeney CJ, Corn PG, Rathkopf DE, Smith DC, Hussain M et al (2014) Cabozantinib in chemotherapy-pretreated metastatic castration-resistant prostate cancer: results of a phase II nonrandomized expansion study. J Clin Oncol 32:3391-3399
25. Choueiri TK, Pal SK, McDermott DF, Morrissey S, Ferguson KC, Holland J et al (2014) A phase I study of cabozantinib (XL184) in patients with renal cell cancer. Ann Oncol 25:1603-1608
26. Elisei R, Schlumberger MJ, Müller SP, Schöffski P, Brose MS, Shah MH et al (2013) Cabozantinib in progressive medullary thyroid cancer. J Clin Oncol 31:3639-3646
27. Zage PE, Zeng L, Palla S, Fang W, Nilsson MB, Heymach JV et al (2010) A novel therapeutic combination for neuroblastoma: the VEGFR/EGFR/RET inhibitor vandetanib with 13-cis-retinoic acid. Cancer 116:2465-2475
28. Yan B, Lim M, Zhou L, Kuick CH, Leong MY, Yong KJ et al (2013) Identification of MET genomic amplification, protein expression, and alternative splice isoforms in neuroblastomas. J Clin Pathol 66:985-991
29. Scorsone K, Zhang L, Woodfield SE, Hicks J, Zage PE (2014) The novel kinase inhibitor EMD1214063 is effective against neuroblastoma. Invest New Drugs 32:815-824
30. Biedler JL, Helson L, Spengler BA (1973) Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res 33:2643-2652
31. Brodeur GM, Green AA, Hayes FA, Williams KJ, Williams DL, Tsiatis AA (1981) Cytogenetic features of human neuroblastomas and cell lines. Cancer Res 41:4678-4686
32. Reynolds CP, Tomayko MM, Donner L, Helson L, Seeger RC, Triche TJ et al (1988) Biological classification of cell lines derived from human extra-cranial neural tumors. Prog Clin Biol Res 271:291-306
33. Schlesinger HR, Gerson JM, Moorhead PS, Maguire H, Hummeler K (1976) Establishment and characterization of human neuroblastoma cell line. Cancer Res 36:3094-3100
34. Keshelava N, Seeger RC, Groshen S, Reynolds CP (1998) Drug resistance patterns of human neuroblastoma cell lines derived from patients at different phases of therapy. Cancer Res 58:5396-5405
35. Tumilowicz JJ, Nichols WW, Cholon JJ, Greene AE (1970) Definition of a continuous human cell line derived from neuroblastoma. Cancer Res 30:2110-2118
36. Ciccarone V, Spengler BA, Meyers MB, Biedler JL, Ross RA (1989) Phenotypic diversification in human neuroblastoma cells: expression of distinct neural crest lineages. Cancer Res 49:219-225
37. Sugimoto T, Tatsumi E, Kemshed JT, Helson L, Green AA, Minowada J (1984) Determination of cell surface membrane antigens common to both human neuroblastoma and leukemia-lymphoma cell lines by a panel of 38 monoclonal antibodies. J Natl Cancer Inst 73:51-57
38. Helson L, Helson C (1985) Human neuroblastoma cells and 13-cis-retinoic acid. J Neurooncol 3:39-41
39. Gilbert F, Feder M, Balaban G, Brangman D, Lurie DK, Podolsky R, Rinaldt V, Vinikoor N, Weisband J (1984) Human neuroblastoma and abnormalities of chromosomes 1 and 17. Cancer Res 44:5444-5449
40. Santana VM, Furman WL, Billups CA, Hoffer F, Davidoff AM, Houghton PJ et al (2005) Improved response in high-risk neuroblastoma with protracted topotecan administration using a pharmacokinetically guided dosing approach. J Clin Oncol 23:4039-4047
41. Rubie H, Chisholm J, Defachelles AS, Morland B, Munzer C, Valteau-Couanet D et al (2006) Phase II study of temozolomide in relapsed or refractory high-risk neuroblastoma: a joint Societe Francaise des Cancers de l'Enfant and United Kingdom Children Cancer Study Group-New Agents Group Study. J Clin Oncol 24:5259-5264
42. Miller WH (1998) The emerging role of retinoids and retinoic acid metabolism blocking agents in the treatment of cancer. Cancer 83:1471-1482
43. Sidell N (1982) Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J Natl Cancer Inst 68:589-596
44. Sidell N, Altman A, Haussler MR, Seeger RC (1983) Effects of retinoic acid (RA) on the growth and phenotypic expression of several human neuroblastoma cell lines. Exp Cell Res 148:21-30
45. Thiele CJ, Reynolds CP, Israel MA (1985) Decreased expression of N-myc precedes retinoic acid-induced morphological differentiation of human neuroblastoma. Nature 313:404-406
46. Hishiki T, Nimura Y, Isogai E, Kondo K, Ichimiya S, Nakamura Y et al (1998) Glial cell line-derived neurotrophic factor/neurturin-induced differentiation and its enhancement by retinoic acid in primary human neuroblastomas expressing c-Ret, GFR alpha-1, and GFR alpha-2. Cancer Res 58:2158-2165
47. Oppenheimer O, Cheung N-K, Gerald WL (2007) The RET oncogene is a critical component of transcriptional programs associated with retinoic acid-induced differentiation in neuroblastoma. Mol Cancer Ther 6:1300-1309
48. Bunone G, Borrello MG, Picetti R, Bongarzone I, Peverali FA, de Franciscis V et al (1995) Induction of RET proto-oncogene expression in neuroblastoma cells precedes neuronal differentiation and is not mediated by protein synthesis. Exp Cell Res 217:92-99
49. D'Aleesio A, De Vita G, Cali G, Nitsch L, Fusco A, Vecchio G et al (1995) Expression of the RET oncogene induces differentiation of SK-N-BE neuroblastoma cells. Cell Growth Differ 6:1387-1394
50. Encinas M, Iglesias M, Liu Y, Wang H, Muhaisen A, Cena V et al (2000) Sequential treatment of SH-SY5Y Cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J Neurochem 75:991-1003
51. Takada N, Isogai E, Kawamoto Nakanishi H, Todo S, Nakagawara A (2001) Retinoic acid-induced apoptosis of the CHP134 neuroblastoma cell line is associated with nuclear accumulation of p53 and is rescued by the GDNF/Ret signal. Med Pediatr Oncol 36:122-126
52. Carol H, Houghton PJ, Morton CL, Kolb EA, Gorlick R, Reynolds CP, Kang MH, Maris JM, Keir ST, Watkins A, Smith MA, Lock RB (2010) Initial testing of topotecan by the pediatric preclinical testing program. Pediatr Blood Cancer 54:707-715
53. Keir ST, Maris JM, Reynolds CP, Kang MH, Kolb EA, Gorlick R, Lock R, Carol H, Morton CL, Wu J, Kurmasheva RT, Houghton PJ, Smith MA (2013) Initial testing (stage 1) of temozolomide by the pediatric preclinical testing program. Pediatr Blood Cancer 60:783-790
54. Donfrancesco A, Jenkner A, Castellano A, Ilari I, Milano GM, De Sio L, Cozza R, Fifani P, Deb G, De Laurentis C, Inserra A, Dominici C (2004) Ifosfamide/carboplatin/etoposide (ICE) as front-line, topotecan/cyclophosphamide as second-line and oral temozolomide as third-line treatment for advanced neuroblastoma over one year of age. Acta Pediatr 445:6-11
55. London WB, Frantz CN, Campbell LA, Seeger RC, Brumback BA, Cohn SL, Matthay KK, Castleberry RP, Diller L (2010) Phase II randomized comparison of topotecan plus cyclophosphamide versus topotecan alone in children with recurrent or refractory neuroblastoma: a children's oncology group study. J Clin Oncol 28:3808-3815
56. Kushner BH, Kramer K, Modak S, Cheung N-KV (2006) Irinotecan plus temozolomide for relapsed or refractory neuroblastoma. J Clin Oncol 24:5271-5276
57. Bagatell R, London WB, Wagner LM, Voss SD, Stewart CF, Maris JM, Kretschmar C, Cohn SL (2011) Phase II study of irinotecan and temozolomide in children with relapsed or refractory neuroblastoma: a children's oncology group study. J Clin Oncol 29:208-213