The multi-targeted kinase inhibitor sunitinib induces apoptosis in colon cancer cells via PUMA

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Sun, Jing ^a,b   Sun, Quanhong ^a   Brown, Matthew F ^a   Dudgeon, Crissy ^a   Chandler, Julie ^a   Xu, Xiang ^c   Shu, Yongqian ^b   Zhang, Lin ^a   Yu, Jian ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; CASPASE 3; CASPASE 9; CYTOCHROME C; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN P21; PROTEIN P53; PUMA PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SUNITINIB; TRANSCRIPTION FACTOR FOXO; VASCULOTROPIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BINDING SITE; CANCER CELL; CELL FRACTIONATION; CHROMATIN IMMUNOPRECIPITATION; COLON CANCER; COLONY FORMATION; COLORECTAL CANCER; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG RESPONSE; ENZYME ACTIVATION; FEMALE; HISTOPATHOLOGY; MITOCHONDRION; MOUSE; NICK END LABELING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUMOR VOLUME; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; COLONIC NEOPLASMS; DNA PRIMERS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOLOGICAL TECHNIQUES; HUMANS; IN SITU NICK-END LABELING; INDOLES; LUCIFERASES; ONCOGENE PROTEIN V-AKT; PROTO-ONCOGENE PROTEINS; PYRROLES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84865086928     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043158     Document Type: Article

References (48)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2009) Cancer statistics, 2009. CA Cancer J Clin 59: 225-249.
2. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
3. Vogelstein B, Kinzler KW, (2004) Cancer genes and the pathways they control. Nat Med 10: 789-799.
4. Zhang J, Yang PL, Gray NS, (2009) Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 9: 28-39.
5. Hait WN, Hambley TW (2009) Targeted cancer therapeutics. Cancer Res 69: 1263-1267; discussion 1267.
6. Faivre S, Demetri G, Sargent W, Raymond E, (2007) Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov 6: 734-745.
7. Mena AC, Pulido EG, Guillen-Ponce C, (2010) Understanding the molecular-based mechanism of action of the tyrosine kinase inhibitor: sunitinib. Anticancer Drugs 21 Suppl 1: S3-11.
8. Saltz LB, Rosen LS, Marshall JL, Belt RJ, Hurwitz HI, et al. (2007) Phase II trial of sunitinib in patients with metastatic colorectal cancer after failure of standard therapy. J Clin Oncol 25: 4793-4799.
9. Johnstone RW, Ruefli AA, Lowe SW, (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108: 153-164.
10. Yu J, Zhang L, (2004) Apoptosis in human cancer cells. Curr Opin Oncol 16: 19-24.
11. Adams JM, Cory S, (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337.
12. Labi V, Erlacher M, Kiessling S, Villunger A, (2006) BH3-only proteins in cell death initiation, malignant disease and anticancer therapy. Cell Death Differ 13: 1325-1338.
13. Yu J, Zhang L, (2008) PUMA, a potent killer with or without p53. Oncogene 27 Suppl 1: S71-83.
14. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B, (2001) PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7: 673-682.
15. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L, (2003) PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci U S A 100: 1931-1936.
16. Ming L, Wang P, Bank A, Yu J, Zhang L, (2006) PUMA dissociates Bax and BCL-XL to induce apoptosis in colon cancer cells. J Biol Chem 281: 16034-16042.
17. Yu J, Wang P, Ming L, Wood MA, Zhang L, (2007) SMAC/Diablo mediates the proapoptotic function of PUMA by regulating PUMA-induced mitochondrial events. Oncogene 26: 4189-4198.
18. Wang P, Yu J, Zhang L, (2007) The nuclear function of p53 is required for PUMA-mediated apoptosis induced by DNA damage. Proc Natl Acad Sci U S A 104: 4054-4059.
19. Dudgeon C, Wang P, Sun X, Peng R, Sun Q, et al. (2010) PUMA induction by FoxO3a mediates the anticancer activities of the broad-range kinase inhibitor UCN-01. Mol Cancer Ther 9: 2893-2902.
20. Sun Q, Ming L, Thomas SM, Wang Y, Chen ZG, et al. (2009) PUMA mediates EGFR tyrosine kinase inhibitor-induced apoptosis in head and neck cancer cells. Oncogene 18: 2348-2357.
21. You H, Pellegrini M, Tsuchihara K, Yamamoto K, Hacker G, et al. (2006) FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J Exp Med 203: 1657-1663.
22. Wang P, Qiu W, Dudgeon C, Liu H, Huang C, et al. (2009) PUMA is directly activated by NF-kappaB and contributes to TNF-alpha-induced apoptosis. Cell Death Differ 16: 1192-1202.
23. Ming L, Sakaida T, Yue W, Jha A, Zhang L, et al. (2008) Sp1 and p73 Activate PUMA Following Serum Starvation. Carcinogenesis 29: 1878-1884.
24. Bunz F, Hwang PM, Torrance C, Waldman T, Zhang Y, et al. (1999) Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 104: 263-269.
25. Sun Q, Sakaida T, Yue W, Gollin SM, Yu J, (2007) Chemosensitization of head and neck cancer cells by PUMA. Mol Cancer Ther 6: 3180-3188.
26. Sun Q, Zheng X, Zhang L, Yu J (2011) Smac Modulates Chemosensitivity in Head and Neck Cancer Cells through the Mitochondrial Apoptotic Pathway. Clin Cancer Res.
27. Yu J, Yue W, Wu B, Zhang L, (2006) PUMA sensitizes lung cancer cells to chemotherapeutic agents and irradiation. Clin Cancer Res 12: 2928-2936.
28. Yu J, Zhang L, Hwang PM, Rago C, Kinzler KW, et al. (1999) Identification and classification of p53-regulated genes. Proc Natl Acad Sci U S A 96: 14517-14522.
29. Rolff J, Dorn C, Merk J, Fichtner I, (2009) Response of Patient-Derived Non-Small Cell Lung Cancer Xenografts to Classical and Targeted Therapies Is Not Related to Multidrug Resistance Markers. J Oncol 2009: 814140.
30. Qiu W, Carson-Walter EB, Kuan SF, Zhang L, Yu J, (2009) PUMA suppresses intestinal tumorigenesis in mice. Cancer Res 69: 4999-5006.
31. Leibowitz BJ, Qiu W, Liu H, Cheng T, Zhang L, et al. (2011) Uncoupling p53 Functions in Radiation-Induced Intestinal Damage via PUMA and p21. Mol Cancer Res 9: 616-625.
32. Nakano K, Vousden KH, (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7: 683-694.
33. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, et al. (2003) p53- and Drug-Induced Apoptotic Responses Mediated by BH3-Only Proteins Puma and Noxa. Science 302: 1036-1038.
34. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, et al. (2003) Puma is an essential mediator of p53-dependent and-independent apoptotic pathways. Cancer Cell 4: 321-328.
35. Johnson KD, Bresnick EH, (2002) Dissecting long-range transcriptional mechanisms by chromatin immunoprecipitation. Methods 26: 27-36.
36. Huang D, Ding Y, Li Y, Luo WM, Zhang ZF, et al. (2010) Sunitinib acts primarily on tumor endothelium rather than tumor cells to inhibit the growth of renal cell carcinoma. Cancer Res 70: 1053-1062.
37. Burkitt K, Chun SY, Dang DT, Dang LH, (2009) Targeting both HIF-1 and HIF-2 in human colon cancer cells improves tumor response to sunitinib treatment. Mol Cancer Ther 8: 1148-1156.
38. Xin H, Zhang C, Herrmann A, Du Y, Figlin R, et al. (2009) Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res 69: 2506-2513.
39. Yang F, Jove V, Xin H, Hedvat M, Van Meter TE, et al. (2010) Sunitinib induces apoptosis and growth arrest of medulloblastoma tumor cells by inhibiting STAT3 and AKT signaling pathways. Mol Cancer Res 8: 35-45.
40. Naik E, O'Reilly LA, Asselin-Labat ML, Merino D, Lin A, et al. (2011) Destruction of tumor vasculature and abated tumor growth upon VEGF blockade is driven by proapoptotic protein Bim in endothelial cells. J Exp Med 208: 1351-1358.
41. Arena S, Bardelli A, (2008) Understanding how kinase-targeted therapies work. Cell Cycle 7: 1560-1563.
42. Deng J, Carlson N, Takeyama K, Dal Cin P, Shipp M, et al. (2007) BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents. Cancer Cell 12: 171-185.
43. Ni Chonghaile T, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, et al. (2011) Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 334: 1129-1133.
44. Fesik SW, (2005) Promoting apoptosis as a strategy for cancer drug discovery. Nat Rev Cancer 5: 876-885.
45. Zhang L, Ming L, Yu J, (2007) BH3 mimetics to improve cancer therapy; mechanisms and examples. Drug Resist Updat 10: 207-217.
46. Pinon JD, Labi V, Egle A, Villunger A, (2008) Bim and Bmf in tissue homeostasis and malignant disease. Oncogene 27 Suppl 1: S41-52.
47. Takezawa K, Okamoto I, Nishio K, Janne PA, Nakagawa K, (2011) Role of ERK-BIM and STAT3-survivin signaling pathways in ALK inhibitor-induced apoptosis in EML4-ALK-positive lung cancer. Clin Cancer Res 17: 2140-2148.
48. Faber AC, Li D, Song Y, Liang MC, Yeap BY, et al. (2009) Differential induction of apoptosis in HER2 and EGFR addicted cancers following PI3K inhibition. Proc Natl Acad Sci U S A 106: 19503-19508.