Six1 overexpression in ovarian carcinoma causes resistance to TRAIL-mediated apoptosis and is associated with poor survival

Cancer Research

Volumn 67, Issue 7, 2007, Pages 3036-3042

  Behbakht, Kian ^a,c   Qamar, Lubna ^a   Aldridge, Carrie S ^a   Coletta, Ricardo D ^a,b   Davidson, Susan A ^a   Thorburn, Andrew ^a   Ford, Heide L ^a,c  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c Department of Obstetrics and Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SIX1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; HOMEODOMAIN PROTEIN; MESSENGER RNA; SIX1 PROTEIN, HUMAN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER STAGING; CANCER SURVIVAL; CARCINOGENESIS; CARCINOMA CELL; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; BIOSYNTHESIS; CELL GROWTH; DOSE RESPONSE; DRUG EFFECT; DRUG RESISTANCE; EPITHELIUM CELL; FEMALE; GENETIC TRANSFECTION; GENETICS; METABOLISM; OVARY; OVARY TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; HOMEODOMAIN PROTEINS; HUMANS; OVARIAN NEOPLASMS; OVARY; RNA, MESSENGER; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSFECTION;

EID: 34248162523     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-3755     Document Type: Article

References (49)

1. Abdollahi T, Potential for TRAIL as a therapeutic agent in ovarian cancer. Vitam Horm 2004;67:347-64.
2. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-30.
3. Kelley SK, Ashkenazi A. Targeting death receptors in cancer with Apo2L/TRAIL. Curr Opin Pharmacol 2004;4: 333-9.
4. Nagane M, Huang HJ, Cavenee WK. The potential of TRAIL for cancer chemotherapy. Apoptosis 2001;6: 191-7.
5. Ozoren N, El-Deiry WS. Cell surface Death Receptor signaling in normal and cancer cells. Semin Cancer Biol 2003;13:135-47.
6. Thorburn A. Death receptor-induced cell killing. Cell Signal 2004;16:139-44.
7. Thomas LR, Henson A, Reed JC, Salsbury FR, Thorburn A. Direct binding of Fas-associated death domain (FADD) to the tumor necrosis factor-related apoptosis-inducing ligand receptor DR5 is regulated by the death effector domain of FADD. J Biol Chem 2004; 279:32780-5.
8. Thomas LR, Johnson RL, Reed JC, Thorburn A. The C-terminal tails of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas receptors have opposing functions in Fas-associated death domain (FADD) recruitment and can regulate agonist-specific mechanisms of receptor activation. J Biol Chem 2004; 279:52479-86.
9. Rowinsky EK. Targeted induction of apoptosis in cancer management: the emerging role of tumor necrosis factor-related apoptosis-inducing ligand receptor activating agents. J Clin Oncol 2005;23: 9394-407.
10. Liu P, Mao H, Hou P. Synergistic antitumor effect of tumor necrosis factor-related apoptosis-inducing ligand combined with cisplatin in ovarian carcinoma cell lines in vitro and in vivo. Int J Gynecol Cancer 2006;16:538-48.
11. Cretney E, Takeda K, Yagita H, Glaccum M, Peschon JJ, Smyth MJ. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J Immunol 2002;168:1356-61.
12. Wang S, El-Deiry WS, Requirement of p53 targets in chemosensitization of colonic carcinoma to death ligand therapy. Proc Natl Acad Sci U S A 2003;100: 15095-100.
13. Wang S, El-Deiry WS. Inducible silencing of KILLER/DR5 in vivo promotes bioluminescent colon tumor xenograft growth and confers resistance to chemotherapeutic agent 5-fluorouracil. Cancer Res 2004;64:6666-72.
14. Shin MS, Kim HS, Lee SH, et al. Mutations of tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1) and receptor 2 (TRAIL-R2) genes in metastatic breast cancers. Cancer Res 2001;61:4942-6.
15. Laclef C, Hamard G, Demignon J, Souil E, Houbron C, Maire P. Altered myogenesis in Six1-deficient mice. Development 2003;130:2239-52.
16. Laclef C, Souil E, Demignon J, Maire P. Thymus, kidney and craniofacial abnormalities in Six 1 deficient mice. Mech Dev 2003;120:669-79.
17. Li X, Oghi KA, Zhang J, et al. Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature 2003;426:247-54.
18. Ozaki H, Nakamura K, Funahashi J, et al. Six1 controls patterning of the mouse otic vesicle. Development 2004;131:551-62.
19. Xu PX, Zheng W, Huang L, Maire P, Laclef C, Silvius D. Six1 is required for the early organogenesis of mammalian kidney. Development 2003;130:3085-94.
20. Zheng W, Huang L, Wei ZB, Silvius D, Tang B, Xu PX. The role of Six1 in mammalian auditory system development. Development 2003;130:3989-4000.
21. Oliver G, Wehr R, Jenkins NA, et al. Homeobox genes and connective tissue patterning. Development 1995; 121:693-705.
22. 2 cell cycle checkpoint associated with overexpression of HSLX1: a possible mechanism of breast carcinogenesis. Proc Natl Acad Sci U S A 1998;95:12608-13.
23. Coletta RD, Christensen K, Reichenberger KJ, et al. The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1. Proc Natl Acad Sci U S A 2004; 101:6478-83.
24. Reichenberger KJ, Coletta RD, Schulte AP, Varella-Garcia M, Ford HL. Gene amplification is a mechanism of Six1 overexpression in breast cancer. Cancer Res 2005;65:2668-75.
25. Khan J, Bittner ML, Saal LH, et al. cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. Proc Natl Acad Sci U S A 1999;96:13264-9.
26. Yu Y, Khan J, Khanna C, Herman L, Meltzer PS, Merlino G. Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators. Nat Med 2004;10: 175-81.
27. Yuan Y, Kim WH, Han HS, et al. Establishment and characterization of human ovarian carcinoma cell lines. Gynecol Oncol 1997;66:378-87.
28. Auersperg N, Siemens CH, Myrdal SE. Human ovarian surface epithelium in primary culture. In Vitro 1984;20: 743-55.
29. Ford HL, Zain SB. Interaction of metastasis associated Mts1 protein with nonmuscle myosin. Oncogene 1995;10:1597-605.
30. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983;11:1475-89.
31. Waterborg JH, Matthews HR. The Lowry method for protein quantitation. Methods Mol Biol 1994;32:1-4.
32. Ford HL, Landesman-Bollag E, Dacwag CS, Stukenberg PT, Pardee AB, Seldin DC. Cell cycle-regulated phosphorylation of the human SIX1 homeodomain protein. J Biol Chem 2000;275:22245-54.
33. Ng KT, Man K, Sun CK, et al. Clinicopathological significance of homeoprotein Six1 in hepatocellular carcinoma. Br J Cancer 2006;95:1050-5.
34. Yu Y, Davicioni E, Triche TJ, Merlino G. The homeoprotein six1 transcriptionally activates multiple protumorigenic genes but requires ezrin to promote metastasis. Cancer Res 2006;66:1982-9.
35. Li CM, Guo M, Borczuk A, et al. Gene expression in Wilms' tumor mimics the earliest committed stage in the metanephric mesenchymal-epithelial transition. Am J Pathol 2002;160:2181-90.
36. Slamon DJ, Godolphin W, Jones LA, et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989;244:707-12.
37. Wooster R, Weber BL. Breast and ovarian cancer. N Engl J Med 2003;348:2339-47.
38. Lane D, Cartier A, L'Esperance S, Cote M, Rancourt C, Piche A. Differential induction of apoptosis by tumor necrosis factor-related apoptosis-inducing ligand in human ovarian carcinoma cells. Gynecol Oncol 2004; 93:594-604.
39. Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature 2004;432:307-15.
40. Szegezdi E, Cahill S, Meyer M, O'Dwyer M, Samali A. TRAIL sensitisation by arsenic trioxide is caspase-8 dependent and involves modulation of death receptor components and Akt. Br J Cancer 2006;94: 398-406.
41. Nyakern M, Cappellini A, Mantovani I, Martelli AM. Synergistic induction of apoptosis in human leukemia T cells by the Akt inhibitor perifosine and etoposide through activation of intrinsic and Fas-mediated extrinsic cell death pathways. Mol Cancer Ther 2006;5: 1559-70.
42. Takeda K, Hayakawa Y, Smyth MJ, et al. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat Med 2001;7:94-100.
43. Cross SS, Harrison RF, Balasubramanian SP, et al. Expression of receptor activator of nuclear factor kappabeta ligand (RANKL) and tumour necrosis factor related, apoptosis inducing ligand (TRAIL) in breast cancer, and their relations with osteoprotegerin, oestrogen receptor, and clinicopathological variables. J Clin Pathol 2006;59:716-20.
44. Lancaster JM, Sayer R, Blanchette C, et al. High expression of tumor necrosis factor-related apoptosis-inducing ligand is associated with favorable ovarian cancer survival. Clin Cancer Res 2003;9:762-6.
45. Lin T, Zhang L, Davis J, et al. Combination of TRAIL gene therapy and chemotherapy enhances antitumor and antimetastasis effects in chemosensitive and chemoresistant breast cancers. Mol Ther 2003;8: 441-8.
46. Ma H, Liu Y, Liu S, et al. Recombinant adeno-associated virus-mediated TRAIL gene therapy suppresses liver metastatic tumors. Int J Cancer 2005;116: 314-21.
47. Zhang L, Yang N, Huang J, et al. Transcriptional coactivator Drosophila eyes absent homologue 2 is up-regulated in epithelial ovarian cancer and promotes tumor growth. Cancer Res 2005;65:925-32.
48. Heanue TA, Reshef R, Davis RJ, et al. Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev 1999;13:3231-43.
49. Zou D, Silvius D, Fritzsch B, Xu PX. Eya1 and Six1 are essential for early steps of sensory neurogenesis in mammalian cranial placodes. Development 2004;131: 5561-72.