Combined Inhibition of IGF-1R/IR and Src Family Kinases Enhances Antitumor Effects in Prostate Cancer by Decreasing Activated Survival Pathways

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Dayyani, Farshid ^a   Parikh, Nila U ^a   Varkaris, Andreas S ^a   Song, Jian H ^a   Moorthy, Shhyam ^a   Chatterji, Tanushree ^a,b   Maity, Sankar N ^a   Wolfe, Adam R ^a   Carboni, Joan M ^c   Gottardis, Marco M ^c   Logothetis, Christopher J ^a   Gallick, Gary E ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [4 [(5 CYCLOPROPYL 1H PYRAZOL 3 YL)AMINO]PYRROLO[2,1 F][1,2,4]TRIAZIN 2 YL] N (6 FLUORO 3 PYRIDINYL) 2 METHYL 2 PYRROLIDINECARBOXAMIDE; DASATINIB; INSULIN RECEPTOR; PROTEIN AKT1; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROSTATE CANCER; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BONE DISEASES; CELL CYCLE; CELL PROLIFERATION; DRUG THERAPY, COMBINATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOPRECIPITATION; MALE; MICE; MICE, NUDE; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZOLES; PYRIMIDINES; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; THIAZOLES; TRIAZINES; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84871588627     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051189     Document Type: Article

References (54)

1. Siegel R, Naishadham D, Jemal A, (2012) Cancer statistics, 2012. CA Cancer J Clin 62: 10-29.
2. de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, et al. (2010) Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 376: 1147-1154.
3. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, et al. (2004) Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 351: 1502-1512.
4. de Bono JS, Logothetis CJ, Molina A, Fizazi K, North S, et al. (2011) Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 364: 1995-2005.
5. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, et al. (2010) Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363: 411-422.
6. Dayyani F, Gallick GE, Logothetis CJ, Corn PG, (2011) Novel therapies for metastatic castrate-resistant prostate cancer. J Natl Cancer Inst 103: 1665-1675.
7. Summy JM, Gallick GE, (2003) Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 22: 337-358.
8. Lombardo LJ, Lee FY, Chen P, Norris D, Barrish JC, et al. (2004) Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4- ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 47: 6658-6661.
9. Nam S, Kim D, Cheng JQ, Zhang S, Lee JH, et al. (2005) Action of the Src family kinase inhibitor, dasatinib (BMS-354825), on human prostate cancer cells. Cancer Res 65: 9185-9189.
10. Logothetis CJ, Lin SH, (2005) Osteoblasts in prostate cancer metastasis to bone. Nat Rev Cancer 5: 21-28.
11. Park SI, Zhang J, Phillips KA, Araujo JC, Najjar AM, et al. (2008) Targeting SRC family kinases inhibits growth and lymph node metastases of prostate cancer in an orthotopic nude mouse model. Cancer Res 68: 3323-3333.
12. Araujo JC, Mathew P, Armstrong AJ, Braud EL, Posadas E, et al. (2012) Dasatinib combined with docetaxel for castration-resistant prostate cancer: Results from a phase 1-2 study. Cancer 118: 63-71.
13. Yu EY, Wilding G, Posadas E, Gross M, Culine S, et al. (2009) Phase II study of dasatinib in patients with metastatic castration-resistant prostate cancer. Clin Cancer Res 15: 7421-7428.
14. Pollak MN, Schernhammer ES, Hankinson SE, (2004) Insulin-like growth factors and neoplasia. Nat Rev Cancer 4: 505-518.
15. Su AI, Welsh JB, Sapinoso LM, Kern SG, Dimitrov P, et al. (2001) Molecular classification of human carcinomas by use of gene expression signatures. Cancer Res 61: 7388-7393.
16. Kimura T, Kuwata T, Ashimine S, Yamazaki M, Yamauchi C, et al. (2010) Targeting of bone-derived insulin-like growth factor-II by a human neutralizing antibody suppresses the growth of prostate cancer cells in a human bone environment. Clin Cancer Res 16: 121-129.
17. Papageorgiou E, Pitulis N, Manoussakis M, Lembessis P, Koutsilieris M, (2008) Rosiglitazone attenuates insulin-like growth factor 1 receptor survival signaling in PC-3 cells. Mol Med 14: 403-411.
18. Ngo TH, Barnard RJ, Leung PS, Cohen P, Aronson WJ, (2003) Insulin-like growth factor I (IGF-I) and IGF binding protein-1 modulate prostate cancer cell growth and apoptosis: possible mediators for the effects of diet and exercise on cancer cell survival. Endocrinology 144: 2319-2324.
19. Miyake H, Nelson C, Rennie PS, Gleave ME, (2000) Overexpression of insulin-like growth factor binding protein-5 helps accelerate progression to androgen-independence in the human prostate LNCaP tumor model through activation of phosphatidylinositol 3′-kinase pathway. Endocrinology 141: 2257-2265.
20. Maloney EK, McLaughlin JL, Dagdigian NE, Garrett LM, Connors KM, et al. (2003) An anti-insulin-like growth factor I receptor antibody that is a potent inhibitor of cancer cell proliferation. Cancer Res 63: 5073-5083.
21. Krueckl SL, Sikes RA, Edlund NM, Bell RH, Hurtado-Coll A, et al. (2004) Increased insulin-like growth factor I receptor expression and signaling are components of androgen-independent progression in a lineage-derived prostate cancer progression model. Cancer Res 64: 8620-8629.
22. Wu JD, Odman A, Higgins LM, Haugk K, Vessella R, et al. (2005) In vivo effects of the human type I insulin-like growth factor receptor antibody A12 on androgen-dependent and androgen-independent xenograft human prostate tumors. Clin Cancer Res 11: 3065-3074.
23. Wahdan-Alaswad RS, Song K, Krebs TL, Shola DT, Gomez JA, et al. (2010) Insulin-like growth factor I suppresses bone morphogenetic protein signaling in prostate cancer cells by activating mTOR signaling. Cancer Res 70: 9106-9117.
24. Gills JJ, Dennis PA, (2009) Perifosine: update on a novel Akt inhibitor. Curr Oncol Rep 11: 102-110.
25. Ligresti G, Militello L, Steelman LS, Cavallaro A, Basile F, et al. (2009) PIK3CA mutations in human solid tumors: role in sensitivity to various therapeutic approaches. Cell Cycle 8: 1352-1358.
26. Carboni JM, Wittman M, Yang Z, Lee F, Greer A, et al. (2009) BMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR. Mol Cancer Ther 8: 3341-3349.
27. Tai S, Sun Y, Squires JM, Zhang H, Oh WK, et al. (2011) PC3 is a cell line characteristic of prostatic small cell carcinoma. Prostate 71: 1668-1679.
28. Kim SJ, Uehara H, Yazici S, Busby JE, Nakamura T, et al. (2006) Targeting platelet-derived growth factor receptor on endothelial cells of multidrug-resistant prostate cancer. J Natl Cancer Inst 98: 783-793.
29. Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, et al. (2004) Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. FASEB J 18: 1240-1242.
30. Lee YC, Cheng CJ, Bilen MA, Lu JF, Satcher RL, et al. (2011) BMP4 promotes prostate tumor growth in bone through osteogenesis. Cancer Res 71: 5194-5203.
31. Zhang J, Park SI, Artime MC, Summy JM, Shah AN, et al. (2007) AFAP-110 is overexpressed in prostate cancer and contributes to tumorigenic growth by regulating focal contacts. J Clin Invest 117: 2962-2973.
32. Park SI, Kim SJ, McCauley LK, Gallick GE, (2010) Pre-clinical mouse models of human prostate cancer and their utility in drug discovery. Curr Protoc Pharmacol Chapter 14: Unit 14 15.
33. Varkaris A, Corn PG, Gaur S, Dayyani F, Logothetis CJ, et al. (2011) The role of HGF/c-Met signaling in prostate cancer progression and c-Met inhibitors in clinical trials. Expert Opin Investig Drugs 20: 1677-1684.
34. Windham TC, Parikh NU, Siwak DR, Summy JM, McConkey DJ, et al. (2002) Src activation regulates anoikis in human colon tumor cell lines. Oncogene 21: 7797-7807.
35. Kopetz S, Lesslie DP, Dallas NA, Park SI, Johnson M, et al. (2009) Synergistic activity of the SRC family kinase inhibitor dasatinib and oxaliplatin in colon carcinoma cells is mediated by oxidative stress. Cancer Res 69: 3842-3849.
36. Landen CN Jr, Lu C, Han LY, Coffman KT, Bruckheimer E, et al. (2006) Efficacy and antivascular effects of EphA2 reduction with an agonistic antibody in ovarian cancer. J Natl Cancer Inst 98: 1558-1570.
37. Davies MA, Kim SJ, Parikh NU, Dong Z, Bucana CD, et al. (2002) Adenoviral-mediated expression of MMAC/PTEN inhibits proliferation and metastasis of human prostate cancer cells. Clin Cancer Res 8: 1904-1914.
38. Lee YC, Huang CF, Murshed M, Chu K, Araujo JC, et al. (2010) Src family kinase/abl inhibitor dasatinib suppresses proliferation and enhances differentiation of osteoblasts. Oncogene 29: 3196-3207.
39. Soriano P, Montgomery C, Geske R, Bradley A, (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64: 693-702.
40. Saad F, (2009) Src as a therapeutic target in men with prostate cancer and bone metastases. BJU Int 103: 434-440.
41. Fizazi K, (2007) The role of Src in prostate cancer. Ann Oncol 18: 1765-1773.
42. Mohan S, Baylink DJ, (1991) Bone growth factors. Clin Orthop Relat Res pp. 30-48.
43. Tao Y, Pinzi V, Bourhis J, Deutsch E, (2007) Mechanisms of disease: signaling of the insulin-like growth factor 1 receptor pathway-therapeutic perspectives in cancer. Nat Clin Pract Oncol 4: 591-602.
44. Larsson O, Girnita A, Girnita L, (2005) Role of insulin-like growth factor 1 receptor signalling in cancer. Br J Cancer 92: 2097-2101.
45. Yap TA, Olmos D, Molife LR, de Bono JS, (2011) Targeting the insulin-like growth factor signaling pathway: figitumumab and other novel anticancer strategies. Expert Opin Investig Drugs 20: 1293-1304.
46. Chou TC, (2010) Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 70: 440-446.
47. Brownlow N, Mol C, Hayford C, Ghaem-Maghami S, Dibb NJ, (2009) Dasatinib is a potent inhibitor of tumour-associated macrophages, osteoclasts and the FMS receptor. Leukemia 23: 590-594.
48. Vandyke K, Dewar AL, Diamond P, Fitter S, Schultz CG, et al. (2010) The tyrosine kinase inhibitor dasatinib dysregulates bone remodeling through inhibition of osteoclasts in vivo. J Bone Miner Res 25: 1759-1770.
49. Fagan DH, Uselman RR, Sachdev D, Yee D, (2012) Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor (IGF1R): implications for breast cancer treatment. Cancer Res 72: 3372-3380.
50. Rabbani SA, Valentino ML, Arakelian A, Ali S, Boschelli F, SKI-606 (Bosutinib) blocks prostate cancer invasion, growth, and metastasis in vitro and in vivo through regulation of genes involved in cancer growth and skeletal metastasis. Mol Cancer Ther 9: 1147-1157.
51. Wu Z, Chang PC, Yang JC, Chu CY, Wang LY, et al. (2010) Autophagy Blockade Sensitizes Prostate Cancer Cells towards Src Family Kinase Inhibitors. Genes Cancer 1: 40-49.
52. Kim SJ, Johnson M, Koterba K, Herynk MH, Uehara H, et al. (2003) Reduced c-Met expression by an adenovirus expressing a c-Met ribozyme inhibits tumorigenic growth and lymph node metastases of PC3-LN4 prostate tumor cells in an orthotopic nude mouse model. Clin Cancer Res 9: 5161-5170.
53. Paccez JD, Vasques GJ, Correa RG, Vasconcellos JF, Duncan K, et al. (2012) The receptor tyrosine kinase Axl is an essential regulator of prostate cancer proliferation and tumor growth and represents a new therapeutic target. Oncogene doi: 10.1038/onc.2012.89.
54. Desai BJS J, Davis ID, Lipton LR, Hicks R, Scott AM, Park J, Clemens PL, Gestone TA, Finckenstein FG, (2010) Phase I dose-escalation study of daily BMS-754807, an oral, dual IGF-1R/insulin receptor (IR) inhibitor in subjects with solid tumors. J Clin Oncol 28: 15s.