TrkB inhibition by GNF-4256 slows growth and enhances chemotherapeutic efficacy in neuroblastoma xenografts

Cancer Chemotherapy and Pharmacology

Volumn 75, Issue 1, 2015, Pages 131-141

  Croucher, Jamie L ^a   Iyer, Radhika ^a   Li, Nanxin ^b   Molteni, Valentina ^b   Loren, Jon ^b   Gordon, W Perry ^b   Tuntland, Tove ^b   Liu, Bo ^b   Brodeur, Garrett M ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

Growth inhibition; Neuroblastoma; Signaling; TrkB

Indexed keywords

ANTINEOPLASTIC AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GNF 4256; IRINOTECAN; PROTEIN TYROSINE KINASE INHIBITOR; TEMOZOLOMIDE; UNCLASSIFIED DRUG; CAMPTOTHECIN; DACARBAZINE; MEMBRANE PROTEIN; NEW DRUG; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE; TROPOMYOSIN-RELATED KINASE-B, HUMAN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; DRUG TUMOR LEVEL; EVENT FREE SURVIVAL; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM PLASMA CONCENTRATION; MOUSE; NEUROBLASTOMA; NEUROBLASTOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TUMOR MODEL; TUMOR VOLUME; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CELL SURVIVAL; COMPARATIVE STUDY; DRUG EFFECTS; DRUG SCREENING; HALF LIFE TIME; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; SURVIVAL ANALYSIS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CAMPTOTHECIN; CELL LINE, TUMOR; CELL SURVIVAL; DACARBAZINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUGS, INVESTIGATIONAL; HALF-LIFE; HUMANS; MEMBRANE GLYCOPROTEINS; MICE, NUDE; NEOPLASM PROTEINS; NEUROBLASTOMA; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; SURVIVAL ANALYSIS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84926486693     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-014-2627-1     Document Type: Article

References (74)

1. Brodeur GM (2003) Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3(3):203-216
2. Brodeur GM, Iyer R, Croucher JL, Zhuang T, Higashi M, Kolla V (2014) Therapeutic targets for neuroblastomas. Expert Opin Ther Targets 18(3):277-292
3. Maris JM, Hogarty MD, Bagatell R, Cohn SL (2007) Neuroblastoma. Lancet 369(9579):2106-2120
4. Brodeur GM, Minturn JE, Ho R, Simpson AM, Iyer R, Varela CR et al (2009) Trk receptor expression and inhibition in neuroblastomas. Clin Cancer Res 15(10):3244-3250
5. Thiele CJ, Li Z, McKee AE (2009) On Trk - the TrkB signal transduction pathway is an increasingly important target in cancer biology. Clin Cancer Res 15(19):5962-5967
6. Nakagawara A (2001) Trk receptor tyrosine kinases: a bridge between cancer and neural development. Cancer Lett 169(2):107-114
7. Brodeur GM, Nakagawara A, Yamashiro DJ, Ikegaki N, Liu XG, Azar CG et al (1997) Expression of TrkA, TrkB and TrkC in human neuroblastomas. J Neurooncol 31(1-2):49-55
8. Kogner P, Barbany G, Dominici C, Castello MA, Raschella G, Persson H (1993) Coexpression of messenger RNA for TRK protooncogene and low affinity nerve growth factor receptor in neuroblastoma with favorable prognosis. Cancer Res 53(9):2044-2050
9. Nakagawara A, Arima M, Azar CG, Scavarda NJ, Brodeur GM (1992) Inverse relationship between trk expression and N-myc amplification in human neuroblastomas. Cancer Res 52(5):1364-1368
10. Nakagawara A, Arima-Nakagawara M, Scavarda NJ, Azar CG, Cantor AB, Brodeur GM (1993) Association between high levels of expression of the TRK gene and favorable outcome in human neuroblastoma. N Engl J Med 328(12):847-854
11. Nakagawara A, Brodeur GM (1997) Role of neurotrophins and their receptors in human neuroblastomas: a primary culture study. Eur J Cancer 33(12):2050-2053
12. Suzuki T, Bogenmann E, Shimada H, Stram D, Seeger RC (1993) Lack of high-affinity nerve growth factor receptors in aggressive neuroblastomas. J Natl Cancer Inst 85(5):377-384
13. Acheson A, Conover JC, Fandl JP, DeChiara TM, Russell M, Thadani A et al (1995) A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374(6521):450-453 see comments
14. Ho R, Eggert A, Hishiki T, Minturn JE, Ikegaki N, Foster P et al (2002) Resistance to chemotherapy mediated by TrkB in neuroblastomas. Cancer Res 62(22):6462-6466
15. Jaboin J, Hong A, Kim CJ, Thiele CJ (2003) Cisplatin-induced cytotoxicity is blocked by brain-derived neurotrophic factor activation of TrkB signal transduction path in neuroblastoma. Cancer Lett 193(1):109-114
16. Jaboin J, Kim CJ, Kaplan DR, Thiele CJ (2002) Brain-derived neurotrophic factor activation of TrkB protects neuroblastoma cells from chemotherapy-induced apoptosis via phosphatidylinositol 3′-kinase pathway. Cancer Res 62(22):6756-6763
17. Matsumoto K, Wada RK, Yamashiro JM, Kaplan DR, Thiele CJ (1995) Expression of brain-derived neurotrophic factor and p145TrkB affects survival, differentiation, and invasiveness of human neuroblastoma cells. Cancer Res 55(8):1798-1806
18. Nakagawara A, Azar CG, Scavarda NJ, Brodeur GM (1994) Expression and function of TRK-B and BDNF in human neuroblastomas. Mol Cell Biol 14(1):759-767
19. Nakamura K, Martin KC, Jackson JK, Beppu K, Woo CW, Thiele CJ (2006) Brain-derived neurotrophic factor activation of TrkB induces vascular endothelial growth factor expression via hypoxia-inducible factor-1alpha in neuroblastoma cells. Cancer Res 66(8):4249-4255
20. Evans AE, Kisselbach KD, Liu X, Eggert A, Ikegaki N, Camoratto AM et al (2001) Effect of CEP-751 (KT-6587) on neuroblastoma xenografts expressing TrkB. Med Pediatr Oncol 36(1):181-184
21. Evans AE, Kisselbach KD, Yamashiro DJ, Ikegaki N, Camoratto AM, Dionne CA et al (1999) Antitumor activity of CEP-751 (KT-6587) on human neuroblastoma and medulloblastoma xenografts. Clin Cancer Res 5(11):3594-3602
22. Iyer R, Evans AE, Qi X, Ho R, Minturn JE, Zhao H et al (2010) Lestaurtinib enhances the antitumor efficacy of chemotherapy in murine xenograft models of neuroblastoma. Clin Cancer Res 16(5):1478-1485
23. Minturn JE, Evans AE, Villablanca JG, Yanik GA, Park JR, Shusterman S et al (2011) Phase I trial of lestaurtinib for children with refractory neuroblastoma: a new approaches to neuroblastoma therapy consortium study. Cancer Chemother Pharmacol 68(4):1057-1065
24. Iyer R, Varela CR, Minturn JE, Ho R, Simpson AM, Light JE et al (2012) AZ64 Inhibits TrkB and enhances the efficacy of chemotherapy and local radiation in neuroblastoma xenografts. Cancer Chemother Pharmacol (in press)
25. Thress K, Macintyre T, Wang H, Whitston D, Liu ZY, Hoffmann E et al (2009) Identification and preclinical characterization of AZ-23, a novel, selective, and orally bioavailable inhibitor of the Trk kinase pathway. Mol Cancer Ther 8(7):1818-1827
26. Zage PE, Graham TC, Zeng L, Fang W, Pien C, Thress K et al (2011) The selective Trk inhibitor AZ623 inhibits brain-derived neurotrophic factor-mediated neuroblastoma cell proliferation and signaling and is synergistic with topotecan. Cancer 117(6):1321-1391
27. Blackwell LJ, Birkos S, Hallam R, Van De Carr G, Arroway J, Suto CM et al (2009) High-throughput screening of the cyclic AMP-dependent protein kinase (PKA) using the caliper microfluidic platform. Methods Mol Biol 565:225-237
28. Thompson J, Zamboni WC, Cheshire PJ, Richmond L, Luo X, Houghton JA et al (1997) Efficacy of oral irinotecan against neuroblastoma xenografts. Anticancer Drugs 8(4):313-322
29. Stewart CF, Zamboni WC, Crom WR, Houghton PJ (1997) Disposition of irinotecan and SN-38 following oral and intravenous irinotecan dosing in mice. Cancer Chemother Pharmacol 40(3):259-265
30. Greco A, Mariani C, Miranda C, Pagliardini S, Pierotti MA (1993) Characterization of the NTRK1 genomic region involved in chromosomal rearrangements generating TRK oncogenes. Genomics 18(2):397-400
31. Greco A, Miranda C, Pagliardini S, Fusetti L, Bongarzone I, Pierotti MA (1997) Chromosome 1 rearrangements involving the genes TPR and NTRK1 produce structurally different thyroid-specific TRK oncogenes. Genes Chromosomes Cancer 19(2):112-123
32. Greco A, Roccato E, Pierotti MA (2004) TRK oncogenes in papillary thyroid carcinoma. Cancer Treat Res 122:207-219
33. Pierotti MA, Bongarzone I, Borrello MG, Mariani C, Miranda C, Sozzi G et al (1995) Rearrangements of TRK proto-oncogene in papillary thyroid carcinomas. J Endocrinol Invest 18(2):130-133
34. Vaishnavi A, Capelletti M, Le AT, Kako S, Butaney M, Ercan D et al (2013) Oncogenic and drug-sensitive NTRK1 rearrangements in lung cancer. Nat Med 19(11):1469-1472
35. Davidson B, Reich R, Lazarovici P, Ann Florenes V, Nielsen S, Nesland JM (2004) Altered expression and activation of the nerve growth factor receptors TrkA and p75 provide the first evidence of tumor progression to effusion in breast carcinoma. Breast Cancer Res Treat 83(2):119-128
36. Descamps S, Lebourhis X, Delehedde M, Boilly B, Hondermarck H (1998) Nerve growth factor is mitogenic for cancerous but not normal human breast epithelial cells. J Biol Chem 273(27):16659-16662
37. Descamps S, Pawlowski V, Revillion F, Hornez L, Hebbar M, Boilly B et al (2001) Expression of nerve growth factor receptors and their prognostic value in human breast cancer. Cancer Res 61(11):4337-4340
38. Dolle L, Adriaenssens E, El Yazidi-Belkoura I, Le Bourhis X, Nurcombe V, Hondermarck H (2004) Nerve growth factor receptors and signaling in breast cancer. Curr Cancer Drug Targets 4(6):463-470
39. Dolle L, El Yazidi-Belkoura I, Adriaenssens E, Nurcombe V, Hondermarck H (2003) Nerve growth factor overexpression and autocrine loop in breast cancer cells. Oncogene 22(36):5592-5601
40. Jin W, Kim GM, Kim MS, Lim MH, Yun C, Jeong J et al (2010) TrkC plays an essential role in breast tumor growth and metastasis. Carcinogenesis 31(11):1939-1947
41. Lagadec C, Meignan S, Adriaenssens E, Foveau B, Vanhecke E, Romon R et al (2009) TrkA overexpression enhances growth and metastasis of breast cancer cells. Oncogene 28(18):1960-1970
42. George DJ, Suzuki H, Bova GS, Isaacs JT (1998) Mutational analysis of the TrkA gene in prostate cancer. Prostate 36(3):172-180
43. MacGrogan D, Saint-Andre JP, Dicou E (1992) Expression of nerve growth factor and nerve growth factor receptor genes in human tissues and in prostatic adenocarcinoma cell lines. J Neurochem 59(4):1381-1391
44. Pflug BR, Dionne C, Kaplan DR, Lynch J, Djakiew D (1995) Expression of a Trk high affinity nerve growth factor receptor in the human prostate. Endocrinology 136(1):262-268
45. Walch ET, Marchetti D (1999) Role of neurotrophins and neurotrophins receptors in the in vitro invasion and heparanase production of human prostate cancer cells. Clin Exp Metastasis 17(4):307-314
46. Weeraratna AT, Arnold JT, George DJ, DeMarzo A, Isaacs JT (2000) Rational basis for Trk inhibition therapy for prostate cancer. Prostate 45(2):140-148
47. Miknyoczki SJ, Wan W, Chang H, Dobrzanski P, Ruggeri BA, Dionne CA et al (2002) The neurotrophin-trk receptor axes are critical for the growth and progression of human prostatic carcinoma and pancreatic ductal adenocarcinoma xenografts in nude mice. Clin Cancer Res 8(6):1924-1931
48. Miknyoczki SJ, Chang H, Klein-Szanto A, Dionne CA, Ruggeri BA (1999) The Trk tyrosine kinase inhibitor CEP-701 (KT-5555) exhibits significant antitumor efficacy in preclinical xenograft models of human pancreatic ductal adenocarcinoma. Clin Cancer Res 5(8):2205-2212
49. Miknyoczki SJ, Dionne CA, Klein-Szanto AJ, Ruggeri BA (1999) The novel Trk receptor tyrosine kinase inhibitor CEP-701 (KT-5555) exhibits antitumor efficacy against human pancreatic carcinoma (Panc1) xenograft growth and in vivo invasiveness. Ann N Y Acad Sci 880:252-262
50. Miknyoczki SJ, Lang D, Huang L, Klein-Szanto AJ, Dionne CA, Ruggeri BA (1999) Neurotrophins and Trk receptors in human pancreatic ductal adenocarcinoma: expression patterns and effects on in vitro invasive behavior. Int J Cancer 81(3):417-427
51. Sakamoto Y, Kitajima Y, Edakuni G, Sasatomi E, Mori M, Kitahara K et al (2001) Expression of Trk tyrosine kinase receptor is a biologic marker for cell proliferation and perineural invasion of human pancreatic ductal adenocarcinoma. Oncol Rep 8(3):477-484
52. Euhus DM, Timmons CF, Tomlinson GE (2002) ETV6-NTRK3 - Trk-ing the primary event in human secretory breast cancer. Cancer Cell 2(5):347-348
53. Makretsov N, He M, Hayes M, Chia S, Horsman DE, Sorensen PH et al (2004) A fluorescence in situ hybridization study of ETV6-NTRK3 fusion gene in secretory breast carcinoma. Genes Chromosom Cancer 40(2):152-157
54. Tognon C, Knezevich SR, Huntsman D, Roskelley CD, Melnyk N, Mathers JA et al (2002) Expression of the ETV6-NTRK3 gene fusion as a primary event in human secretory breast carcinoma. Cancer Cell 2(5):367-376
55. Knezevich SR, McFadden DE, Tao W, Lim JF, Sorensen PH (1998) A novel ETV6-NTRK3 gene fusion in congenital fibrosarcoma. Nat Genet 18(2):184-187
56. Liu Q, Schwaller J, Kutok J, Cain D, Aster JC, Williams IR et al (2000) Signal transduction and transforming properties of the TEL-TRKC fusions associated with t(12, 15)(p13;q25) in congenital fibrosarcoma and acute myelogenous leukemia. EMBO J 19(8):1827-1838
57. Rubin BP, Chen CJ, Morgan TW, Xiao S, Grier HE, Kozakewich HP et al (1998) Congenital mesoblastic nephroma t(12, 15) is associated with ETV6-NTRK3 gene fusion: cytogenetic and molecular relationship to congenital (infantile) fibrosarcoma. Am J Pathol 153(5):1451-1458
58. Chou TT, Trojanowski JQ, Lee VM (2000) A novel apoptotic pathway induced by nerve growth factor-mediated TrkA activation in medulloblastoma. J Biol Chem 275(1):565-570
59. Grotzer MA, Janss AJ, Fung K, Biegel JA, Sutton LN, Rorke LB et al (2000) TrkC expression predicts good clinical outcome in primitive neuroectodermal brain tumors. J Clin Oncol 18(5):1027-1035
60. Kim JY, Sutton ME, Lu DJ, Cho TA, Goumnerova LC, Goritchenko L et al (1999) Activation of neurotrophin-3 receptor TrkC induces apoptosis in medulloblastomas. Cancer Res 59(3):711-719
61. Segal RA, Goumnerova LC, Kwon YK, Stiles CD, Pomeroy SL (1994) Expression of the neurotrophin receptor TrkC is linked to a favorable outcome in medulloblastoma. Proc Natl Acad Sci USA 91(26):12867-12871
62. Ng YK, Wong EY, Lau CP, Chan JP, Wong SC, Chan AS et al (2012) K252a induces anoikis-sensitization with suppression of cellular migration in Epstein-Barr virus (EBV) - associated nasopharyngeal carcinoma cells. Invest New Drugs 30(1):48-58
63. McGregor LM, McCune BK, Graff JR, McDowell PR, Romans KE, Yancopoulos GD et al (1999) Roles of trk family neurotrophin receptors in medullary thyroid carcinoma development and progression. Proc Natl Acad Sci USA 96(8):4540-4545
64. Eggert A, Grotzer MA, Ikegaki N, Zhao H, Cnaan A, Brodeur GM et al (2001) Expression of the neurotrophin receptor TrkB is associated with unfavorable outcome in Wilms' tumor. J Clin Oncol 19(3):689-696
65. Martin-Zanca D, Oskam R, Mitra G, Copeland T, Barbacid M (1989) Molecular and biochemical characterization of the human trk proto-oncogene. Mol Cell Biol 9(1):24-33
66. Mitra G, Martin-Zanca D, Barbacid M (1987) Identification and biochemical characterization of p70TRK, product of the human TRK oncogene. Proc Natl Acad Sci U S A 84(19):6707-6711
67. Yu Y, Zhang S, Wang X, Yang Z, Ou G (2010) Overexpression of TrkB promotes the progression of colon cancer. Apmis 118(3):188-195
68. Okugawa Y, Tanaka K, Inoue Y, Kawamura M, Kawamoto A, Hiro J et al (2013) Brain-derived neurotrophic factor/tropomyosin-related kinase B pathway in gastric cancer. Br J Cancer 108(1):121-130
69. Guo D, Hou X, Zhang H, Sun W, Zhu L, Liang J et al (2011) More expressions of BDNF and TrkB in multiple hepatocellular carcinoma and anti-BDNF or K252a induced apoptosis, suppressed invasion of HepG2 and HCCLM3 cells. J Exp Clin Cancer Res 30:97
70. Jin W, Lee JJ, Kim MS, Son BH, Cho YK, Kim HP (2011) DNA methylation-dependent regulation of TrkA, TrkB, and TrkC genes in human hepatocellular carcinoma. Biochem Biophys Res Commun 406(1):89-95
71. Harada T, Yatabe Y, Takeshita M, Koga T, Yano T, Wang Y et al (2011) Role and relevance of TrkB mutations and expression in non-small cell lung cancer. Clin Cancer Res 17(9):2638-2645
72. Doebele R, Vaishnavi A, Capelletti M, Le A, Kako S, Butaney M et al (2013) NTRK1 gene fusions as a novel oncogene target in lung cancer. American Society of Clinical Oncology Annual Meeting 2013. ASCO University, Chicago, IL, p. suppl: abstr 8023
73. Yu X, Liu L, Cai B, He Y, Wan X (2008) Suppression of anoikis by the neurotrophic receptor TrkB in human ovarian cancer. Cancer Sci 99(3):543-552
74. Desmet CJ, Peeper DS (2006) The neurotrophic receptor TrkB: a drug target in anti-cancer therapy? Cell Mol Life Sci 63(7-8):755-759