Molecular pathogenesis and therapeutic targets in epithelial ovarian cancer

Journal of Cellular Biochemistry

Volumn 102, Issue 5, 2007, Pages 1117-1129

  Chien, Jeremy R ^a   Aletti, Giovanni ^a   Bell, Debra A ^a   Keeney, Gary L ^a   Shridhar, Viji ^a   Hartmann, Lynn C ^a  

^a MAYO CLINIC   (United States)

Author keywords

Molecular pathogenesis; Ovarian cancer; Therapeutic targets

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2,3 DIHYDRO 2 OXO 3 (4,5,6,7 TETRAHYDRO 1H INDOL 2 YLMETHYLENE) 1H INDOLE 5 SULFONIC ACID DIMETHYLAMIDE; 5 AMINO 1 [3,5 DICHLORO 4 (4 CHLOROBENZOYL)BENZYL] 1H 1,2,3 TRIAZOLE 4 CARBOXAMIDE; BEVACIZUMAB; BORTEZOMIB; BUTHIONINE SULFOXIMINE; CANERTINIB; CARBOPLATIN; CGP 69846A; CYCLOPHOSPHAMIDE; ERLOTINIB; ETACRYNIC ACID; EVEROLIMUS; FLAVOPIRIDOL; GEFITINIB; LAPATINIB; LONAFARNIB; MELPHALAN; PACLITAXEL; PLACEBO; PLATINUM; ROSCOVITINE; SORAFENIB; TEMSIROLIMUS; THALIDOMIDE; THIOTEPA; TIPIFARNIB; TRASTUZUMAB; UNINDEXED DRUG; VALSPODAR;

CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER MODEL; CANCER THERAPY; CARCINOGENESIS; CLINICAL TRIAL; GENE MUTATION; HUMAN; HYPOTHESIS; INTESTINE PERFORATION; METASTASIS; NONHUMAN; OVARY CANCER; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL CELLS; FEMALE; HUMANS; MODELS, BIOLOGICAL; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; PRECANCEROUS CONDITIONS; TREATMENT OUTCOME;

EID: 36849051967     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21552     Document Type: Review

References (79)

1. Abramson N, Stokes PK, Luke M, Marks AR, Harris JM. 2002. Ovarian and papillary-serous peritoneal carcinoma: Pilot study with thalidomide. J Clin Oncol 20: 1147-1149.
2. Adams J. 2002. Proteasome inhibition: A novel approach to cancer therapy. Trends Mol Med 8:S49-S54.
3. Adams AT, Auersperg N. 1981. Transformation of cultured rat ovarian surface epithelial cells by Kirsten murine sarcoma virus. Cancer Res 41:2063-2072.
4. Agarwal R, Kaye SB. 2003. Ovarian cancer: Strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 3:502-516.
5. Aghajanian C, Soignet S, Dizon DS, Pien CS, Adams J, Elliott PJ, Sabbatini P, Miller V, Hensley ML, Pezzulli S, Canales C, Daud A, Spriggs DR. 2002. A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin Cancer Res 8:2505-2511.
6. Aletti GD, Gallenberg MM, Cliby WA, Jatoi A, Hartmann LC. 2007. Current magement strategies for ovarian cancer. Mayo Clin Proc 82:751-770.
7. Bapat SA, Mali AM, Koppikar CB, Kurrey NK. 2005. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 65:3025-3029.
8. Bayani J, Brenton JD, Macgregor PF, Beheshti B, Albert M, Nallainathan D, Karaskova J, Rosen B, Murphy J, Laframboise S, Zanke B, Squire JA. 2002. Parallel analysis of sporadic primary ovarian carcinomas by spectral karyotyping, comparative genomic hybridization, and expression microarrays. Cancer Res 62:3466-3476.
9. Bell DA. 2005. Origins and molecular pathology of ovarian cancer. Mod Pathol 18 (Suppl 2):S19-S32.
10. Benson C, White J, De Bono J, O'Donnell A, Raynaud F, Cruickshank C, McGrath H, Walton M, Workman P, Kaye S, Cassidy J, Gianella-Borradori A, Judson I, Twelves C. 2007. A phase I trial of the selective oral cyclin-dependent kinase inhibitor seliciclib (CYC202; R-Roscovitine), administered twice daily for 7 days every 21 days. Br J Cancer 96:29-37.
11. Berkenblit A, Cannistra SA. 2005. Advances in the management of epithelial ovarian cancer. J Reprod Med 50:426-438.
12. Bernards R, Weinberg RA. 2002. A progression puzzle. Nature 418:823.
13. Bible KC, Lensing JL, Nelson SA, Lee YK, Reid JM, Ames MM, Isham CR, Piens J, Rubin SL, Rubin J, Kaufmann SH, Atherton PJ, Sloan JA, Daiss MK, Adjei AA, Erlichman C. 2005. Phase 1 trial of flavopiridol combined with cisplatin or carboplatin in patients with advanced malignancies with the assessment of pharmacokinetic and pharmacodynamic end points. Clin Cancer Res 11: 5935-5941.
14. Bignotti E, Tassi RA, Calza S, Ravaggi A, Bandiera E, Rossi E, Donzelli C, Pasinetti B, Pecorelli S, Santin AD. 2007. Gene expression profile of ovarian serous papillary carcinomas: Identification of metastasis-associated genes. Am J Obstet Gynecol 196:245.e1-e11.
15. Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, Olson JA Jr, Marks JR, Dressman HK, West M, Nevins JR. 2006. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 439:353-357.
16. Blake RA, Broome MA, Liu X, Wu J, Gishizky M, Sun L, Courtneidge SA. 2000. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol Cell Biol 20:9018-9027.
17. Bookman MA, Darcy KM, Clarke-Pearson D, Boothby RA, Horowitz IR. 2003. Evaluation of monoclonal humanized anti-HER2 antibody, trastuzumab, in patients with recurrent or refractory ovarian or primary peritoneal carcinoma with overexpression of HE R2: A phase II trial of the Gynecologic Oncology Group. J Clin Oncol 21:283-290.
18. Boyd J. 2005. Mouse models of gynecologic pathology. N Engl J Med 352:2240-2242.
19. Burger RA, Sill M, Monk BJ, Greer B, Sorosky J. 2005. Phase II trial of bevacizumab in persistent or recurrent epithelial ovarian cancer (EOC) or primary peritoneal cancer (PPC): A Gynecologic Onocology Group study. Proc Am Soc Clin Oncol 23:457s.
20. Campos S, Hamid O, Seiden MV, Oza A, Plante M, Potkul RK, Lenehan PF, Kaldjian EP, Varterasian ML, Jordan C, Charbonneau C, Hirte H. 2005. Multicenter, randomized phase II trial of oral CI-1033 for previously treated advanced ovarian cancer. J Clin Oncol 23:5597-5604.
21. Cheng PC, Gosewehr JA, Kim TM, Velicescu M, Wan M, Zheng J, Felix JC, Cofer KF, Luo P, Biela BH, Godorov G, Dubeau L. 1996. Potential role of the inactivated X chromosome in ovarian epithelial tumor development. J Natl Cancer Inst 88:510-518.
22. Cheng W, Liu J, Yoshida H, Rosen D, Naora H. 2005. Lineage infidelity of epithelial ovarian cancers is controlled by HOX genes that specify regional identity in the reproductive tract. Nat Med 11:531-537.
23. Christie M, Oehler MK. 2006. Molecular pathology of epithelial ovarian cancer. J Br Menopause Soc 12:57-63.
24. Clark-Knowles KV, Garson K, Jonkers J, Vanderhyden BC. 2007. Conditional inactivation of Brca1 in the mouse ovarian surface epithelium results in an increase in preneoplastic changes. Exp Cell Res 313:133-145.
25. Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, Hua X, Harris SS, Vanderhyden BC, Hamilton TC. 2003. Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res 63:1389-1397.
26. Crum CP, Drapkin R, Miron A, Ince TA, Muto M, Kindelberger DW, Lee Y. 2007. The distal fallopian tube: A new model for pelvic serous carcinogenesis. Curr Opin Obstet Gynecol 19:3-9.
27. Dinulescu DM, Ince TA, Quade BJ, Shafer SA, Crowley D, Jacks T. 2005. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 11:63-70.
28. Dressman HK, Berchuck A, Chan G, Zhai J, Bild A, Sayer R, Cragun J, Clarke J, Whitaker RS, Li L, Gray J, Marks J, Ginsburg GS, Potti A, West M, Nevins JR, Lancaster JM. 2007. An integrated genomic-based approach to individualized treatment of patients with advanced-stage ovarian cancer. J Clin Oncol 25:517-525.
29. Dubeau L. 1999. The cell of origin of ovarian epithelial tumors and the ovarian surface epithelium dogma: Does the emperor have no clothes? Gynecol Oncol 72:437-442.
30. Ferrara N. 2005. VEGF as a therapeutic target in cancer. Oncology 69 (Suppl 3):11-16.
31. Flesken-Nikitin A, Choi KC, Eng JP, Shmidt EN, Nikitin AY. 2003. Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium. Cancer Res 63:3459-3463.
32. Fukumoto M, Nakayama K. 2006. Ovarian epithelial tumors of low malignant potential: Are they precursors of ovarian carcinoma? Pathol Int 56:233-239.
33. Garcia AA, Oza AM, Hirte H, Fleming G, Tsao-Wei D, Roman L. 2005. Interim report of a phase II clinical trial of bevacizumab and low dose metronomic oral cyclophosphamide in recurrent ovarian and primary peritoneal carcinoma: A California Cancer Consortium trial. Proc Am Soc Clin Oncol 23:455s.
34. Garson K, Shaw TJ, Clark KV, Yao DS, Vanderhyden BC. 2005. Models of ovarian cancer-are we there yet? Mol Cell Endocrinol 239:15-126.
35. Gordon AN, Finkler N, Edwards RP, Garcia AA, Crozier M, Irwin DH, Barrett E. 2005. Efficacy and safety of erlotinib HCl, an epidermal growth factor receptor (HER1/EGFR) tyrosine kinase inhibitor, in patients with advanced ovarian carcinoma: Results from a phase II multicenter study. Int J Gynecol Cancer 15:785-792.
36. Gregoire L, Rabah R, Schmelz EM, Munkarah A, Roberts PC, Lancaster WD. 2001. Spontaneous malignant transformation of human ovarian surface epithelial cells in vitro. Clin Cancer Res 7:4280-4287.
37. Gries JM, Bond J, Rodrigues L, et al. 2003. Phase I study of fiavopiridol 24 hour infusion monotherapy in solid tumours (HMR1275/1002). Proc Am Soc Clin Oncol 22: 141.
38. Haas CJ, Diebold J, Hirschmann A, Rohrbach H, Schmid S, Lohrs U. 1999. Microsatellite analysis in serous tumors of the ovary. Int J Gynecol Pathol 18:158-162.
39. Haluska P, Toft D, Steinmetz S. 2004. A phase I trial of gemcitabine, 17-allylaminogeldanamycin and cisplastin in solid tumour patients. J Clin Oncol 22:209.
40. Hartmann LC, Lu KH, Linette GP, Cliby WA, Kalli KR, Gershenson D, Bast RC, Stec J, Iartchouk N, Smith DI, Ross JS, Hoersch S, Shridhar V, Lillie J, Kaufmann SH, Clark EA, Damokosh AI. 2005. Gene expression profiles predict early relapse in ovarian cancer after platinum-paclitaxel chemotherapy. Clin Cancer Res 11:2149-2155.
41. Hibbs K, Skubitz KM, Pambuccian SE, Casey RC, Burleson KM, Oegema TR Jr, Thiele JJ, Grindle SM, Bliss RL, Skubitz AP. 2004. Differential gene expression in ovarian carcinoma: Identification of potential biomarkers. Am J Pathol 165:397-414.
42. Hidalgo M, Rowinsky EK. 2000. The rapamycin-sensitive signal transduction pathway as a target for cancer therapy. Oncogene 19:6680-6686.
43. Hussain MM, Kotz H, Minasian L, Premkumar A, Sarosy G, Reed E, Zhai S, Steinberg SM, Raggio M, Oliver VK, Figg WD, Kohn EC. 2003. Phase II trial of carboxyamidotriazole in patients with relapsed epithelial ovarian cancer. J Clin Oncol 21:4356-4363.
44. Israeli O, Gotlieb WH, Friedman E, Korach J, Friedman E, Goldman B, Zeltser A, Ben-Baruch G, Rienstein S, Aviram-Goldring A. 2004. Genomic analyses of primary and metastatic serous epithelial ovarian cancer. Cancer Genet Cytogenet 154:16-21.
45. Jazaeri AA, Awtrey CS, Chandramouli GV, Chuang YE, Khan J, Sotiriou C, Aprelikova O, Yee CJ, Zorn KK, Birrer MJ, Barrett JC, Boyd J. 2005. Gene expression profiles associated with response to chemotherapy in epithelial ovarian cancers. Clin Cancer Res 11:6300-6310.
46. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. 2007. Cancer statistics, 2007. CA Cancer J Clin 57:43-66.
47. Johnston SR. 2001. Farnesyl transferase inhibitors: A novel targeted therapy for cancer. Lancet Oncol 2:18-26.
48. JoIy F, Mangioni C, Nicoletto M, Manikhas GM, Walker J, Mietlowski W, Jones G, Wysowskyi H, Dugan M. 2002. A phase 3 study of PSC 833 in combination with paclitaxel and carboplatin (PC-PSC) versus paclitaxel and carboplatin (PC) alone in patients with stage IV or suboptimally debulked stage III epithelial ovarian cancer or primary cancer of the peritoneum. Proc Am Soc Clin Oncol 21(Pt 1 of 2):202a. Abstract 806.
49. Lancaster JM, Dressman HK, Clarke JP, Sayer RA, Martino MA, Cragun JM, Henriott AH, Gray J, Sutphen R, Elahi A, Whitaker RS, West M, Marks JR, Nevins JR, Berchuck A. 2006. Identification of genes associated with ovarian cancer metastasis using microarray expression analysis. Int J Gynecol Cancer 16:1733-1745.
50. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, Cramer DW, McKeon FD, Crum CP. 2007. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 211:26-35.
51. Leung EH, Leung PC, Auersperg N. 2001. Differentiation and growth potential of human ovarian surface epithelial cells expressing temperature-sensitive SV40 T antigen. In Vitro Cell Dev Biol Anim 37:515-521.
52. Liotta LA, Kohn EC. 2005. Cancer biology: Invasion and metastases. In: Kufe D, Pollock R, Weichselbaum R, Bast R Jr, Gansler T, Holland J, Frei EF III, editors. Cancer medicine. Hamilton, Ontario L8N 3K7: BC Decker.
53. Liu J, Yang G, Thompson-Lanza JA, Glassman A, Hayes K, Patterson A, Marquez RT, Auersperg N, Yu Y, Hahn WC, Mills GB, Bast RC Jr. 2004. A genetically defined model for human ovarian cancer. Cancer Res 64:1655-1663.
54. Liu TC, Galanis E, Kirn D. 2007. Clinical trial results with oncolytic virotherapy: A century of promise, a decade of progress. Nat Clin Pract Oncol 4:101-117.
55. Lu HK, Broaddus RR. 2005. Gynecologic cancers in Lynch syndrome/HNPCC. Fam Cancer 4:249-254.
56. Mabuchi S, Altomare DA, Connolly DC, Klein-Szanto A, Litwin S, Hoelzle MK, Hensley HH, Hamilton TC, Testa JR. 2007. RAD001 (Everolimus) delays tumor onset and progression in a transgenic mouse model of ovarian cancer. Cancer Res 67:2408-2413.
57. Maines-Bandiera SL, Kruk PA, Auersperg N. 1992. Simian virus 40-transformed human ovarian surface epithelial cells escape normal growth controls but retain morphogenetic responses to extracellular matrix. Am J Obstet Gynecol 167:729-735.
58. O'Dwyer PJ, LaCreta F, Nash S, Tinsley PW, Schilder R, Clapper ML, Tew KD, Panting L, Litwin S, Comis RL, et al. 1991. Phase I study of thiotepa in combination with the glutathione transferase inhibitor ethacrynic acid. Cancer Res 51:6059-6065.
59. O'Dwyer PJ, Hamilton TC, LaCreta FP, Gallo JM, Kilpatrick D, Halbherr T, Brennan J, Bookman MA, Hoffman J, Young RC, Comis RL, Ozols RF. 1996. Phase I trial of buthionine sulfoximine in combination with melphalan in patients with cancer. J Clin Oncol 14: 249-256.
60. Orsulic S. 2002. An RCAS-TVA-based approach to designer mouse models. Mamm Genome 13:543-547.
61. Orsulic S, Li Y, Soslow RA, Vitale-Cross LA, Gutkind JS, Varmus HE. 2002. Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell 1:53-62.
62. Oza AM, Elit L, Swenerton K, Faught W, Ghatage P, Carey M, McIntosh L, Dorr A, Holmlund JT, Eisenhauer E. 2003. Phase II study of CGP 69846A (ISIS 5132) in recurrent epithelial ovarian cancer: An NCIC clinical trials group study (NCIC IND.116). Gynecol Oncol 89: 129-133.
63. Peng KW, TenEyck CJ, Galanis E, Kalli KR, Hartmann LC, Russell SJ. 2002. Intraperitoneal therapy of ovarian cancer using an engineered measles virus. Cancer Res 62:4656-4662.
64. Roberts PC, Mottillo EP, Baxa AC, Heng HH, Doyon-Reale N, Gregoire L, Lancaster WD, Rabah R, Schmelz EM. 2005. Sequential molecular and cellular events during neoplastic progression: A mouse syngeneic ovarian cancer model. Neoplasia 7:944-956.
65. Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, Tawfik O, Persons DL, Smith PG, Terranova PF. 2000. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 21:585-591.
66. Scambia G, Masciullo V, Benedetti Panici P, Marone M, Ferrandina G, Todaro N, Bellacosa A, Jain SK, Neri G, Piffanelli A, Mancuso S. 1997. Prognostic significance of ras/p21 alterations in human ovarian cancer. Br J Cancer 75:1547-1553.
67. Schilder RJ, Sill MW, Chen X, Darcy KM, Decesare SL, Lewandowski G, Lee RB, Arciero CA, Wu H, Godwin AK. 2005. Phase II study of gefitinib in patients with relapsed or persistent ovarian or primary peritoneal carcinoma and evaluation of epidermal growth factor receptor mutations and immunohistochemical expression: A Gynecologic Oncology Group Study. Clin Cancer Res 11:5539-5548.
68. Shih Ie M, Kurman RJ. 2004. Ovarian tumorigenesis: A proposed model based on morphological and molecular genetic analysis. Am J Pathol 164:1511-1518.
69. Shridhar V, Lee J, Pandita A, Iturria S, Avula R, Staub J, Morrissey M, Calhoun E, Sen A, Kalli K, Keeney G, Roche P, Cliby W, Lu K, Schmandt R, Mills GB, Bast RC Jr, James CD, Couch FJ, Hartmann LC, Lillie J, Smith DI. 2001. Genetic analysis of early- versus late-stage ovarian tumors. Cancer Res 61:5895-5904.
70. Singer G, Oldt R 3rd, Cohen Y, Wang BG, Sidransky D, Kurman RJ, Shih Ie M. 2003. Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst 95:484-486.
71. Spentzos D, Levine DA, Kolia S, Otu H, Boyd J, Libermann TA, Cannistra SA. 2005. Unique gene expression profile based on pathologic response in epithelial ovarian cancer. J Clin Oncol 23:7911-7918.
72. Strumberg D, Awada A, Piccard M. 2003. Final report of the phase I clinical program of the novel raf kinase inhibitor BAY 43-9006 in patients with refractory solid tumours. Proc Am Soc Clin Oncol 22:203.
73. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. 2006. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5:219-234.
74. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin DT, Donahoe PK. 2006. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci USA 103:11154-11159.
75. Tewari KS, Mehta RS, Burger RA, Yu IR, Kyshtoobayeva AS, Monk BJ, Manetta A, Berman ML, Disaia PJ, Fruehauf JP. 2005. Conservation of in vitro drug resistance patterns in epithelial ovarian carcinoma. Gynecol Oncol 98:360-368.
76. Tolcher AW, Mita M, Patnaik A. 2004. A phase I pharmacokinetic study of HGS-ETR1 (TRM1), a human monoclonal against-antibody to TRAIL-R1, in patients with advanced solid tumours. J Clin Oncol 22:210.
77. Wright JD, Hagemann A, Rader JS, Viviano D, Gibb RK, Norris L, Mutch DG, Powell MA. 2006. Bevacizumab combination therapy in recurrent, platinum-refractory, epithelial ovarian carcinoma: A retrospective analysis. Cancer 107:83-839.
78. Xing D, Orsulic S. 2005a. A genetically defined mouse ovarian carcinoma model for the molecular characterization of pathway-targeted therapy and tumor resistance. Proc Natl Acad Sci USA 102:6936-6941.
79. Xing D, Orsulic S. 2005b. Modeling resistance to pathway-targeted therapy in ovarian cancer. Cell Cycle 4:1004-1006.