Identification of novel therapeutic targets in microdissected clear cell ovarian cancers

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Stany, Michael P ^a   Vathipadiekal, Vinod ^b   Ozbun, Laurent ^c   Stone, Rebecca L ^d   Mok, Samuel C ^e   Xue, Hui ^f   Kagami, Takashi ^f   Wang, Yuwei ^f   McAlpine, Jessica N ^g   Bowtell, David ^h   Gout, Peter W ^f   Miller, Dianne M ^g   Gilks, C Blake ^f   Huntsman, David G ^f   Ellard, Susan L ^f   Wang, Yu Zhuo ^f,g   Vivas Mejia, Pablo ^d   Lopez Berestein, Gabriel ^d   Sood, Anil K ^d   Birrer, Michael J ^b  

^a WALTER REED ARMY MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

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

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f BRITISH COLUMBIA CANCER AGENCY   (Canada)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^h PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; SUNITINIB; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDOLE DERIVATIVE; PYRROLE DERIVATIVE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; CANCER CELL CULTURE; CELL HYPOXIA; CLEAR CELL OVARIAN CANCER; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SILENCING; GENE TARGETING; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LASER CAPTURE MICRODISSECTION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CANCER; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; ANIMAL; CELL DEATH; CELL SURVIVAL; DISEASE COURSE; DRUG EFFECT; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN GENOME; METABOLISM; MICRODISSECTION; MICROVASCULATURE; MOLECULARLY TARGETED THERAPY; NECROSIS; NUDE MOUSE; OVARY TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VASCULARIZATION;

MUS;

ANIMALS; CELL DEATH; CELL HYPOXIA; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; GLUCOSE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INDOLES; MICE; MICE, NUDE; MICRODISSECTION; MICROVESSELS; MOLECULAR TARGETED THERAPY; NECROSIS; OVARIAN NEOPLASMS; PYRROLES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79959923767     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021121     Document Type: Article

References (53)

1. Schiller W, (1939) Mesonephroma ovarii. Am J Cancer 35: 1-21.
2. Genton CY, (1979) Ultrastructure of clear cell carcinoma of the ovary. Case report and review of the literature. Virchows Arch A Pathol Anat Histol 385: 77-91.
3. Silverberg SG, (1973) Ultrastructure and histogenesis of clear cell carcinoma of the ovary. Am J Obstet Gynecol 115: 394-400.
4. Jenison EL, Montag AG, Griffiths CT, Welch WR, Lavin PT, et al. (1989) Clear cell adenocarcinoma of the ovary: a clinical analysis and comparison with serous carcinoma. Gynecol Oncol 32: 65-71.
5. Kennedy AW, Biscotti CV, Hart WR, Webster KD, (1989) Ovarian clear cell adenocarcinoma. Gynecol Oncol 32: 342-349.
6. Crozier MA, Copeland LJ, Silva EG, Gershenson DM, Stringer CA, (1989) Clear cell carcinoma of the ovary: a study of 59 cases. Gynecol Oncol 35: 199-203.
7. Kobel M, Kalloger SE, Huntsman DG, Santos JL, Swenerton KD, et al. (2010) Differences in tumor type in low-stage versus high-stage ovarian carcinomas. Int J Gynecol Pathol 29: 203-211.
8. Sugiyama T, Kamura T, Kigawa J, Terakawa N, Kikuchi Y, et al. (2000) Clinical characteristics of clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy. Cancer 88: 2584-2589.
9. Pectasides D, Pectasides E, Psyrri A, Economopoulos T, (2006) Treatment issues in clear cell carcinoma of the ovary: a different entity? Oncologist 11: 1089-1094.
10. Matsuura Y, Robertson G, Marsden DE, Kim SN, Gebski V, et al. (2007) Thromboembolic complications in patients with clear cell carcinoma of the ovary. Gynecol Oncol 104: 406-410.
11. Nordback I, Lauslahti K, (1980) Clinicopathologic and histochemical study of ovarian clear cell carcinoma. Int J Gynaecol Obstet 18: 85-89.
12. Dickersin GR, Welch WR, Erlandson R, Robboy SJ, (1980) Ultrastructure of 16 cases of clear cell adenocarcinoma of the vagina and cervix in young women. Cancer 45: 1615-1624.
13. Zorn KK, Bonome T, Gangi L, Chandramouli GV, Awtrey CS, et al. (2005) Gene expression profiles of serous, endometrioid, and clear cell subtypes of ovarian and endometrial cancer. Clin Cancer Res 11: 6422-6430.
14. Schwartz DR, Kardia SL, Shedden KA, Kuick R, Michailidis G, et al. (2002) Gene expression in ovarian cancer reflects both morphology and biological behavior, distinguishing clear cell from other poor-prognosis ovarian carcinomas. Cancer Res 62: 4722-4729.
15. Zorn KK, Jazaeri AA, Awtrey CS, Gardner GJ, Mok SC, et al. (2003) Choice of normal ovarian control influences determination of differentially expressed genes in ovarian cancer expression profiling studies. Clin Cancer Res 9: 4811-4818.
16. Bonome T, Lee JY, Park DC, Radonovich M, Pise-Masison C, et al. (2005) Expression profiling of serous low malignant potential, low-grade, and high-grade tumors of the ovary. Cancer Res 65: 10602-10612.
17. Donninger H, Bonome T, Radonovich M, Pise-Masison CA, Brady J, et al. (2004) Whole genome expression profiling of advance stage papillary serous ovarian cancer reveals activated pathways. Oncogene 23: 8065-8077.
18. Aponte M, Jiang W, Lakkis M, Li MJ, Edwards D, et al. (2008) Activation of platelet-activating factor receptor and pleiotropic effects on tyrosine phospho-EGFR/Src/FAK/paxillin in ovarian cancer. Cancer Res 68: 5839-5848.
19. Landen CN Jr, Chavez-Reyes A, Bucana C, Schmandt R, Deavers MT, et al. (2005) Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res 65: 6910-6918.
20. Halder J, Kamat AA, Landen CN Jr, Han LY, Lutgendorf SK, et al. (2006) Focal adhesion kinase targeting using in vivo short interfering RNA delivery in neutral liposomes for ovarian carcinoma therapy. Clin Cancer Res 12: 4916-4924.
21. Landen CN Jr, Lin YG, Armaiz Pena GN, Das PD, Arevalo JM, et al. (2007) Neuroendocrine modulation of signal transducer and activator of transcription-3 in ovarian cancer. Cancer Res 67: 10389-10396.
22. Ebos JM, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS, (2007) Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci U S A 104: 17069-17074.
23. Sun L, Liang C, Shirazian S, Zhou Y, Miller T, et al. (2003) Discovery of 5-[5-fluoro-2-oxo-1,2- dihydroindol-(3Z)-ylidenemethyl]-2,4- dimethyl-1H-pyrrole-3-carboxylic acid (2-diethylaminoethyl)amide, a novel tyrosine kinase inhibitor targeting vascular endothelial and platelet-derived growth factor receptor tyrosine kinase. J Med Chem 46: 1116-1119.
24. Lee CH, Xue H, Sutcliffe M, Gout PW, Huntsman DG, et al. (2005) Establishment of subrenal capsule xenografts of primary human ovarian tumors in SCID mice: potential models. Gynecol Oncol 96: 48-55.
25. Press JZ, Kenyon JA, Xue H, Miller MA, De Luca A, et al. (2008) Xenografts of primary human gynecological tumors grown under the renal capsule of NOD/SCID mice show genetic stability during serial transplantation and respond to cytotoxic chemotherapy. Gynecol Oncol 110: 256-264.
26. Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, et al. (2003) In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 9: 327-337.
27. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, et al. (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 271: 32529-32537.
28. Kilic M, Kasperczyk H, Fulda S, Debatin KM, (2007) Role of hypoxia inducible factor-1 alpha in modulation of apoptosis resistance. Oncogene 26: 2027-2038.
29. Kelly BD, Hackett SF, Hirota K, Oshima Y, Cai Z, et al. (2003) Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93: 1074-1081.
30. Tsao MS, Liu N, Nicklee T, Shepherd F, Viallet J, (1997) Angiogenesis correlates with vascular endothelial growth factor expression but not with Ki-ras oncogene activation in non-small cell lung carcinoma. Clin Cancer Res 3: 1807-1814.
31. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, et al. (2006) Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol 291: R1085-1093.
32. Cuadrado MJ, Buendia P, Velasco F, Aguirre MA, Barbarroja N, et al. (2006) Vascular endothelial growth factor expression in monocytes from patients with primary antiphospholipid syndrome. J Thromb Haemost 4: 2461-2469.
33. Crutchley DJ, Que BG, (1995) Copper-induced tissue factor expression in human monocytic THP-1 cells and its inhibition by antioxidants. Circulation 92: 238-243.
34. Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y, et al. (2006) Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 66: 2778-2784.
35. Ciofani M, Zuniga-Pflucker JC, (2005) Notch promotes survival of pre-T cells at the beta-selection checkpoint by regulating cellular metabolism. Nat Immunol 6: 881-888.
36. Wu R, Hendrix-Lucas N, Kuick R, Zhai Y, Schwartz DR, et al. (2007) Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/beta-catenin and PI3K/Pten signaling pathways. Cancer Cell 11: 321-333.
37. Yamaguchi K, Mandai M, Oura T, Matsumura N, Hamanishi J, et al. (2010) Identification of an ovarian clear cell carcinoma gene signature that reflects inherent disease biology and the carcinogenic processes. Oncogene 29: 1741-1752.
38. Mok SC, Bonome T, Vathipadiekal V, Bell A, Johnson ME, et al. (2009) A gene signature predictive for outcome in advanced ovarian cancer identifies a survival factor: microfibril-associated glycoprotein 2. Cancer Cell 16: 521-532.
39. Sprecher CA, Kisiel W, Mathewes S, Foster DC, (1994) Molecular cloning, expression, and partial characterization of a second human tissue-factor-pathway inhibitor. Proc Natl Acad Sci U S A 91: 3353-3357.
40. Cappellini MD, (2007) Coagulation in the pathophysiology of hemolytic anemias. Hematology Am Soc Hematol Educ Program pp. 74-78.
41. Medina P, Navarro S, Estelles A, Espana F, (2007) Polymorphisms in the endothelial protein C receptor gene and thrombophilia. Thromb Haemost 98: 564-569.
42. Maeshima K, Maeshima A, Hayashi Y, Kishi S, Kojima I, (2004) Crucial role of activin a in tubulogenesis of endothelial cells induced by vascular endothelial growth factor. Endocrinology 145: 3739-3745.
43. Poulaki V, Joussen AM, Mitsiades N, Mitsiades CS, Iliaki EF, et al. (2004) Insulin-like growth factor-I plays a pathogenetic role in diabetic retinopathy. Am J Pathol 165: 457-469.
44. Frede S, Freitag P, Otto T, Heilmaier C, Fandrey J, (2005) The proinflammatory cytokine interleukin 1beta and hypoxia cooperatively induce the expression of adrenomedullin in ovarian carcinoma cells through hypoxia inducible factor 1 activation. Cancer Res 65: 4690-4697.
45. Ito N, Huang K, Claesson-Welsh L, (2001) Signal transduction by VEGF receptor-1 wild type and mutant proteins. Cell Signal 13: 849-854.
46. Pollard PJ, El-Bahrawy M, Poulsom R, Elia G, Killick P, et al. (2006) Expression of HIF-1alpha, HIF-2alpha (EPAS1), and their target genes in paraganglioma and pheochromocytoma with VHL and SDH mutations. J Clin Endocrinol Metab 91: 4593-4598.
47. Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, et al. (2002) Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J Biol Chem 277: 29936-29944.
48. Gwak GY, Yoon JH, Kim KM, Lee HS, Chung JW, et al. (2005) Hypoxia stimulates proliferation of human hepatoma cells through the induction of hexokinase II expression. J Hepatol 42: 358-364.
49. Welsh S, Williams R, Kirkpatrick L, Paine-Murrieta G, Powis G, (2004) Antitumor activity and pharmacodynamic properties of PX-478, an inhibitor of hypoxia-inducible factor-1alpha. Mol Cancer Ther 3: 233-244.
50. Chen J, Zhao S, Nakada K, Kuge Y, Tamaki N, et al. (2003) Dominant-negative hypoxia-inducible factor-1 alpha reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism. Am J Pathol 162: 1283-1291.
51. Gitlits VM, Toh BH, Sentry JW, (2001) Disease association, origin, and clinical relevance of autoantibodies to the glycolytic enzyme enolase. J Investig Med 49: 138-145.
52. Walter M, Berg H, Leidenberger FA, Schweppe KW, Northemann W, (1995) Autoreactive epitopes within the human alpha-enolase and their recognition by sera from patients with endometriosis. J Autoimmun 8: 931-945.
53. Wu MH, Chen KF, Lin SC, Lgu CW, Tsai SJ, (2007) Aberrant expression of leptin in human endometriotic stromal cells is induced by elevated levels of hypoxia inducible factor-1alpha. Am J Pathol 170: 590-598.