Ovarian carcinomas: Five distinct diseases with different origins, genetic alterations, and clinicopathological features

Virchows Archiv

Volumn 460, Issue 3, 2012, Pages 237-249

  Prat, Jaime ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

ARID1A; BRCA; Carcinomas; CTNNB1; Histopathological types; HNF 1beta; KRAS; Molecular genetics; Ovary; PIK3CA; PTEN; TP53

Indexed keywords

CANCER CLASSIFICATION; CANCER GRADING; CANCER GROWTH; CLEAR CELL CARCINOMA; CLINICAL FEATURE; ENDOMETRIOID CARCINOMA; EPITHELIUM TUMOR; GENE MUTATION; GENETIC ANALYSIS; HISTOPATHOLOGY; HUMAN; MOLECULAR PATHOLOGY; MUCINOUS CARCINOMA; ONCOGENE; OVARY CARCINOMA; PRIORITY JOURNAL; REVIEW; TUMOR SUPPRESSOR GENE; CARCINOMA; FEMALE; GENETICS; OVARY TUMOR; PATHOLOGY;

CARCINOMA; FEMALE; HUMANS; OVARIAN NEOPLASMS;

EID: 84860336909     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-012-1203-5     Document Type: Review

References (84)

1. Prat J (2004) Pathology of the ovary. Saunders, Philadelphia
2. Lee KR, Tavassoli FA, Prat J et al (2003) Surface epithelialstromal tumours (Ch 2: tumours of the ovary and peritoneum). In: Tavassoli FA, Devilee P (eds) World Health Organization classification of tumours: pathology and genetics of tumours of the breast and female genital organs. IARC Press, Lyon, pp 117-145
3. Shvartsman HS, Sun CC, Bodurka CC, Mahajan V, Crispens M, Lu KH, Deavers MT, Malpica A, Silva EG, Gershenson DM (2007) Comparison of the clinical behavior of newly diagnosed stages II-IV low-grade serous carcinoma of the ovary with that of serous ovarian tumors of low malignant potential that recur as lowgrade serous carcinoma. Gynecol Oncol 105:625-629 (Pubitemid 46734181)
4. Stewart BW, Kleihues P (2003). World Cancer Report (IARC Press)
5. Jass JR (2006) Colorectal cancer: a multipathway disease. Crit Rev Oncog 12:273-287 (Pubitemid 46524134)
6. Gilks CB, Prat J (2009) Ovarian carcinoma pathology and genetics: recent advances. Hum Pathol 40:1213-1223
7. Takano M, Kikuchi Y, Yaegashi N, Kuzuya K, Ueki M, Tsuda H, Suzuki M, Kigawa J, Takeuchi S, Tsuda H, Moriya T, Sugiyama T (2006) Clear cell carcinoma of the ovary: a retrospective multicentre experience of 254 patients with complete surgical staging. Br J Cancer 94:1369-1374 (Pubitemid 43772268)
8. du Bois A, Lück HJ, Meier W, Adams HP, Möbus V, Costa S, Bauknecht T, Richter B, Warm M, Schröder W, Olbricht S, Nitz U, Jackisch C, Emons G, Wagner U, Kuhn W, Pfisterer J (2003) A randomized clinical trial of cisplatin/paclitaxel versus carboplatin/ paclitaxel as first-line treatment of ovarian cancer. J Natl Cancer Inst 95:1320-1329
9. Fountain J, Trimble E, Birrer MJ (2006) Summary and discussion of session recommendations. Gynecol Oncol 103:S23-S25 (Pubitemid 44633413)
10. Köbel M, Kalloger SE, Boyd N, McKinney S, Mehl E, Palmer C, Leung S, Bowen NJ, Ionescu DN, Rajput A, Prentice LM, Miller D, Santos J, Swenerton K, Gilks CB, Huntsman D (2008) Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med 5:e232
11. Kurman RJ, Shih IM (2010) The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 34:433-443
12. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P, Verheijen RH (2001) Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 195:451-456 (Pubitemid 33069670)
13. Piek JM, van Diest PJ, Zweemer RP, Kenemans P, Verheijen RH (2001) Tubal ligation and risk of ovarian cancer. Lancet 358:844
14. Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW, Crum CP (2006) The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 30:230-236 (Pubitemid 43740193)
15. Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C, Berkowitz RS, Muto MG, Crum CP (2007) Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am J Surg Pathol 31:161-169 (Pubitemid 46175016)
16. 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 (Pubitemid 46092026)
17. Folkins AK, Jarboe EA, Saleemuddin A, Lee Y, Callahan MJ, Drapkin R, Garber JE, Muto MG, Tworoger S, Crum CP (2008) A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes from women with BRCA mutations. Gynecol Oncol 109:168-173
18. Jarboe E, Folkins A, Nucci MR, Kindelberger D, Drapkin R, Miron A, Lee Y, Crum CP (2008) Serous carcinogenesis in the fallopian tube: a descriptive classification. Int J Gynecol Pathol 27:1-9 (Pubitemid 351627965)
19. Obata K, Morland SJ, Watson RH, Hitchcock A, Chenevix-Trench G, Thomas EJ, Campbell IG (1998) Frequent PTEN/MMAC mutations in endometrioid but not serous or mucinous epithelial ovarian tumors. Cancer Res 58:2095-2097 (Pubitemid 28232892)
20. Sato N, Tsunoda H, Nishida M, Morishita Y, Takimoto Y, Kubo T, Noguchi M (2000) Loss of heterozygosity on 10q23.3 and mutation of the tumor suppressor gene PTEN in benign endometrial cyst of the ovary: possible sequence progression from benign endometrial cyst to endometrioid carcinoma and clear cell carcinoma of the ovary. Cancer Res 60:7052-7056 (Pubitemid 32059184)
21. Singer G, Oldt R 3rd, Cohen Y, Wang BG, Sidransky D, Kurman RJ, IeM S (2003) Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Nat Cancer Inst 95:484-486 (Pubitemid 36432423)
22. Singer G, Stöhr R, Cope L, Dehari R, Hartmann A, Cao DF, Wang TL, Kurman RJ, IeM S (2005) Patterns of p53 mutations separate ovarian serous borderline tumors and low- and high-grade carcinomas and provide support for a new model of ovarian carcinogenesis. Am J Surg Pathol 29:218-224 (Pubitemid 40170640)
23. Laury AR, Ning G, Quick CM, Nucci MR, Parast MM, McKeon FD, Xian W, Crum CP (2011) Fallopian tube correlates of serous borderline tumors. Am J Surg Pathol 35:1759-1765
24. Kurman RJ, Vang R, Junge J, Hannibal CG, Kjaer SK, Shih Ie M (2011) Papillary tubal hyperplasia: the putative precursor of ovarian atypical proliferative (borderline) serous tumors, noninvasive implants, and endosalpingiosis. Am J Surg Pathol 35:1605-1614
25. Malpica A, Deavers MT, Lu K, Bodurka DC, Atkinson EN, Gershenson DM, Silva EG (2004) Grading ovarian serous carcinoma using a two-tier system. Am J Surg Pathol 28:496-504 (Pubitemid 38436523)
26. Gilks CB, Ionescu DN, Kalloger SE, Köbel M, Irving J, Clarke B, Santos J, Le N, Moravan V, Swenerton K (2008) Tumor cell type can be reproducibly diagnosed and is of independent prognostic significance in patients with maximally debulked ovarian carcinoma. Hum Pathol 39:1239-1251
27. Al-Hussaini M, Stockman A, Foster H, Mc Cluggage WG (2004) WT-1 assists in distinguishing ovarian from uterine serous carcinoma and in distinguishing between serous and endometrioid ovarian carcinoma. Histopathology 44:109-105
28. Köbel M, Kalloger SE, Carrick J, Huntsman D, Asad H, Oliva E, Ewanowich CA, Soslow RA, Gilks CB (2009) A limited panel of immunomarkers can reliably distinguish between clear cell and high-grade serous carcinoma of the ovary. Am J Surg Pathol 33:14-21
29. Karst AM, Levanon K, Duraisamy S, Liu JF, Hirsch MS, Hecht JL, Drapkin R (2011) Stathmin 1, a marker of PI3K pathway activation and regulator of microtubule dynamics, is expressed in early pelvic serous carcinomas. Gynecol Oncol 123:5-12
30. Risch HA, McLaughlin JR, Cole DE, Rosen B, Bradley L, Fan I, Tang J, Li S, Zhang S, Shaw PA, Narod SA (2006) Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin-cohort study in Ontario, Canada. J Natl Cancer Inst 98:1694-1706 (Pubitemid 44942707)
31. Venkitaraman AR (2009) Linking the cellular functions of BRCA genes to cancer pathogenesis and treatment. Annu Rev Pathol 4:461-487
32. Geisler JP, Hatterman-Zogg MA, Rathe JA, Buller RE (2002) Frequency of BRCA1 dysfunction in ovarian cancer. J Natl Cancer Inst 94:61-67 (Pubitemid 34082844)
33. Esteller M, Silva JM, Dominguez G, Bonilla F, Matias-Guiu X, Lerma E, Prat J, Harkes I, Repasky EA, Gabrielson E, Schutte M, Baylin SB, Herman JG (2000) Promoter hypermethylation is a cause of BRCA1 inactivation in sporadic breast and ovarian tumors. J Natl Cancer Inst 92:564-569 (Pubitemid 30212318)
34. Bowtell DD (2010) The genesis and evolution of high-grade serous ovarian cancer. Nat Rev Cancer 10:803-808
35. Levanon K, Ng V, Piao HY, Zhang Y, Chang MC, Roh MH, Kindelberger DW, Hirsch MS, Crum CP, Marto JA, Drapkin R (2010) Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 29:1103-1113
36. Powell CB, Kenley E, Chen LM, Crawford B, McLennan J, Zaloudek C, Komaromy M, Beattie M, Ziegler J (2005) Riskreducing salpingo-oophorectomy in BRCA mutation carriers: role of serial sectioning in the detection of occult malignancy. J Clin Oncol 23:127-132 (Pubitemid 41702631)
37. Pothuri B, Leitao MM, Levine DA, Viale A, Olshen AB, Arroyo C, Bogomolniy F, Olvera N, Lin O, Soslow RA, Robson ME, Offit K, Barakat RR, Boyd J (2010) Genetic analysis of the early natural history of epithelial ovarian carcinoma. PLoS One 5:e10358
38. Norquist BM, Garcia RL, Allison KH, Jokinen CH, Kernochan LE, Pizzi CC, Barrow BJ, Goff BA, Swisher EM (2010) The molecular pathogenesis of hereditary ovarian carcinoma: alterations in the tubal epithelium of women with BRCA1 and BRCA2 mutations. Cancer 116:5261-5271
39. Espinosa I, Catasus L, Canet B, D'Angelo E, Muñoz J, Prat J (2011) Gene expression analysis identifies two groups of ovarian high-grade serous carcinomas with different prognosis. Mod Pathol 24:846-854
40. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A (2005) Targeting the DNA repair defectin BRCA mutant cells as a therapeutic strategy. Nature 434:917-921 (Pubitemid 40559006)
41. Tutt AN, Lord CJ, McCabe N, Farmer H, Turner N, Martin NM, Jackson SP, Smith GC, Ashworth A (2005) Exploiting the DNA repair defectin BRCA mutant cells in the design of new therapeutic strategies for cancer. Cold Spring Harb Symp Quant Biol 70:139-148 (Pubitemid 44124865)
42. Gershenson DM, Sun CC, Lu KH, Coleman RL, Sood AK, Malpica A, Deavers MT, Silva EG, Bodurka DC (2006) Clinical behavior of stage II-IV low-grade serous carcinoma of the ovary. Obstet Gynecol 108:361-368 (Pubitemid 44305678)
43. Malpica A, Deavers MT, Tornos C, Kurman RJ, Soslow R, Seidman JD, Munsell MF, Gaertner E, Frishberg D, Silva EG (2007) Inter-observer and intraobserver variability of a two-tier system for grading ovarian serous carcinoma. Am J Surg Pathol 31:1203-1208
44. Ayhan A, Kurman RJ, Yemelyanova A, Vang R, Logani S, Seidman JD, IeM S (2009) Defining the cut-point between low- and highgrade ovarian serous carcinomas: a clinicopathologic and molecular genetic analysis. Am J Surg Pathol 33:1220-1224
45. Jones S, Wang T-L, Kurman RJ, Nakayama K, Velculescu VE, Vogelstein B, Kinzler KW, Papadopoulos N, Shih I-M (2012) Low-grade serous carcinomas of the ovary contain very few point mutations. J Pathol 226:413-420
46. Bell DA, Longacre TA, Prat J, Kohn EC, Soslow RA, Ellenson LH, Malpica A, Stoler MH, Kurman RJ (2004) Serous borderline (low malignant potential, atypical proliferative) ovarian tumors: workshop perspectives. Hum Pathol 35:934-948 (Pubitemid 39037177)
47. Sieben NL, Roemen GMJM, Oosting J, Fleuren GJ, van Engeland M, Prat J (2006) Clonal analysis favours a monoclonal origin for serous borderline tumours with peritoneal implants. J Pathol 210:405-411 (Pubitemid 44830600)
48. Crispens MA, Bodurka D, Deavers M, Lu K, Silva EG, Gershenson DM (2002) Response and survival in patients with progressive or recurrent serous ovarian tumors of low malignant potential. Obstet Gynecol 99:3-10 (Pubitemid 34075460)
49. Rodriguez IM, Prat J (2002) Mucinous tumors of the ovary: a clinicopathologic analysis of 75 borderline tumors (of intestinal type) and carcinomas. Am J Surg Pathol 26:139-152 (Pubitemid 34127494)
50. Lee KR, Scully RE (2000) Mucinous tumors of the ovary-A clinicopathologic study of 196 borderline tumors (of intestinal type) and carcinomas, including an evaluation of 11 cases with "pseudomyxomaperitonei". Am J Surg Pathol 24:1447-1464
51. Silverberg SG, Bell DA, Kurman RJ, Seidman JD, Prat J, Ronnett BM, Copeland L, Silva E, Gorstein F, Young RH (2004) Borderline ovarian tumors: key points and workshop summary. Hum Pathol 35:910-917 (Pubitemid 39037175)
52. Hoerl HD, Hart WR (1998) Primary ovarian mucinous cystadenocarcinomas: a clinicopathologic study of 49 cases with long term follow-up. Am J Surg Pathol 22:1449-1462
53. Riopel MA, Ronnett BM, Kurman RJ (1999) Evaluation of diagnostic criteria and behavior of ovarian intestinal-type mucinous tumors. Atypical proliferative (borderline) tumors and intraepithelial, microinvasive, invasive and metastatic carcinomas. Am J Surg Pathol 23:617-635 (Pubitemid 29262825)
54. Provenza C, Young RH, Prat J (2008) Anaplastic carcinoma in mucinous ovarian tumors: a clinicopathologic study of 34 cases emphasizing the crucial impact of stage on prognosis, their histologic spectrum, and overlap with sarcoma-like mural nodules. Am J Surg Pathol 32:383-389 (Pubitemid 351398929)
55. Heinzelmann-Schwarz VA, Gardiner-Garden M, Henshall SM, Scurry JP, Scolyer RA, Smith AN, Bali A, Vanden Bergh P, Baron-Hay S, Scott C, Fink D, Hacker NF, Sutherland RL, O'Brien PM (2006) A distinct molecular profile associated with mucinous epithelial ovarian cancer. Br J Cancer 94:904-91353
56. Cuatrecasas M, Villanueva A, Matias-Guiu X, Prat J (1997) K-ras mutations in mucinous ovarian tumors. A clinicopathologic and molecular study of 95 cases. Cancer 79:1581-1586 (Pubitemid 27154791)
57. Park SY, Kim HS, Hong EK, Kim WH (2002) Expression of cytokeratins 7 and 20 in primary carcinomas of the stomach and colorectum and their value in the differential diagnosis of metastatic carcinomas to the ovary. Hum Pathol 33:1078-1085 (Pubitemid 35416704)
58. Vang R, Gown AM,Wu LS, Barry TS,Wheeler DT, Yemelyanova A, Seidman JD, Ronnett BM (2006) Immunohistochemical expression ofCDX2 in primary ovarian mucinous tumors and metastatic mucinous carcinomas involving the ovary: comparison with CK20 and correlation with coordinate expression of CK7. Mod Pathol 19:1421-1428 (Pubitemid 44624160)
59. Ji H, Isacson C, Seidman J, Kurman RJ, Ronnett BM (2002) Cytokeratins 7and 20, Dpc4, and MUC5AC in the distinction of metastatic mucinous carcinomas in the ovary from primary ovarian mucinous tumors: Dpc4assists in identifying metastatic pancreatic carcinomas. Int J Gynecol Pathol 21:391-400
60. Ronnett BM, Yemelyanova AV, Vang R, Gilks CB, Miller D, Gravitt PE, Kurman RJ (2008) Endocervical adenocarcinomas with ovarian metastases: analysis of 29 cases with emphasis on minimally invasive cervical tumors and the ability of the metastases to simulate primary ovarian neoplasms. Am J Surg Pathol 32:1835-1853
61. Irving JA, Catasús L, Gallardo A, Bussaglia E, Romero M, Matias- Guiu X, Prat J (2005) Synchronous endometrioid carcinomas of the uterine corpus and ovary: alterations in the beta-catenin (CTNNB1) pathway are associated with independent primary tumors and favorable prognosis. Hum Pathol 36:605-619 (Pubitemid 40922566)
62. Tothill RW, Tinker AV, George J, Brown R, Fox SB, Lade S, Johnson DS, Trivett MK, Etemadmoghadam D, Locandro B, Traficante N, Fereday S, Hung JA, Chiew YE, Haviv I, Australian Ovarian Cancer Study Group, Gertig D, DeFazio A, Bowtell D (2008) Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res 14:5198-5208
63. Sainz de la Cuesta R, Eichhorn JH, Rice LW, Fuller AF Jr, Nikrui N, Goff BA (1996) Histologic transformation of benign endometriosis to early epithelial ovarian cancer. Gynecol Oncol 60:238-244 (Pubitemid 26058768)
64. Jiang X, Morland SJ, Hitchcock A, Thomas EJ, Campbell IG (1998) Allelotyping of endometriosis with adjacent ovarian carcinoma reveals evidence of a common lineage. Cancer Res 58:1707-1712 (Pubitemid 28215097)
65. 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 (Pubitemid 40215839)
66. Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, Zeng T, Senz J, McConechy MK, Anglesio MS, Kalloger SE, Yang W, Heravi- Moussavi A, Giuliany R, Chow C, Fee J, Zayed A, Prentice L, Melnyk N, Turashvili G, Delaney AD, Madore J, Yip S, McPherson AW, Ha G, Bell L, Fereday S, Tam A, Galletta L, Tonin PN, Provencher D, Miller D, Jones SJ, Moore RA, Morin GB, Oloumi A, Boyd N, Aparicio SA, Shih Ie M, Mes-Masson AM, Bowtell DD, Hirst M, Gilks B, Marra MA, Huntsman DG (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 363:1532-1543
67. Lemon B, Inouye C, King DS, Tjian R (2001) Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414:924-928 (Pubitemid 34024745)
68. Birrer MJ (2010) The origin of ovarian cancer-is it getting clearer? N Engl J Med 363:1574-1575
69. Palacios J, Gamallo C (1998) Mutations in the beta-catenin gene (CTNNB1) in endometrioid ovarian carcinomas. Cancer Res 58:1344-1347 (Pubitemid 28193586)
70. Catasús L, Bussaglia E, Rodriguez I, Gallardo A, Pons C, Irving JA, Prat J (2004) Molecular genetic alterations in endometrioid carcinomas of the ovary: similar frequency of beta-catenin abnormalities but lower rate of microsatellite instability and PTEN alterations than in uterine endometrioid carcinomas. Hum Pathol 35:1360-1368 (Pubitemid 39601576)
71. Gamallo C, Palacios J, Moreno G, Calvo de Mora J, Suárez A, Armas A (1999) Beta-catenin expression pattern in stage I and II ovarian carcinomas: relationship withbeta-catenin gene mutations, clinicopathological features, and clinical outcome. Am J Pathol 155:527-536 (Pubitemid 29370402)
72. Campbell IG, Russell SE, Choong DY, Montgomery KG, Ciavarella ML, Hooi CS, Cristiano BE, Pearson RB, Phillips WA (2004) Mutation of the PIK3CA gene in ovarian and breast cancer. Cancer Res 64:7678-7681 (Pubitemid 39446895)
73. Catasus L, Gallardo A, Cuatrecasas M, Prat J (2008) PIK3CA mutations in the kinase domain (exon 20) of uterine endometrial adenocarcinomas are associated with adverse prognostic parameters. Mod Pathol 21:131-139 (Pubitemid 351172164)
74. Willner J, Wurz K, Allison KH, Galic V, Garcia RL, Goff BA, Swisher EM (2007) Alternate molecular genetic pathways in ovarian carcinomas of common histological types. Hum Pathol 38:607-613 (Pubitemid 46399888)
75. Gras E, Catasus L, Argüelles R, Moreno-Bueno G, Palacios J, Gamallo C, Matias-Guiu X, Prat J (2001) Microsatellite instability, MLH-1 promoter hypermethylation, and frameshift mutations at coding mononucleotide repeat microsatellites in ovarian tumors. Cancer 92:2829-2836 (Pubitemid 33091919)
76. Moreno-Bueno G, Gamallo C, Perez-Gallego L, Calvo de Mora J, Suarez A, Palacios J (2001) Beta-catenin expression pattern, betacatenin gene mutations, and microsatellite instability in endometrioid ovarian carcinomas and synchronous endometrial carcinomas. Diagn Mol Pathol 10:116-122 (Pubitemid 32525880)
77. Sugiyama T, Kamura T, Kigawa J, Terakawa N, Kikuchi Y, Kita T, Suzuki M, Sato I, Taguchi K (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 (Pubitemid 30331967)
78. Komiyama S, Aoki D, Tominaga E, Susumu N, Udagawa Y, Nozawa S (1999) Prognosis of Japanese patients with ovarian clear cell carcinoma associated with pelvic endometriosis: clinicopathologic evaluation. Gynecol Oncol 72:342-346 (Pubitemid 29118191)
79. Press JZ, De Luca A, Boyd N, Young S, Troussard A, Ridge Y, Kaurah P, Kalloger SE, Blood KA, Smith M, Spellman PT, Wang Y, Miller DM, Horsman D, Faham M, Gilks CB, Gray J, Huntsman DG (2008) Ovarian carcinomas with genetic and epigenetic BRCA1 loss have distinct molecular abnormalities. BMC Cancer 8:17
80. Kato N, Sasou S, Motoyama T (2006) Expression of hepatocyte nuclear factor-1beta (HNF-1beta) in clear cell tumors and endometriosis of the ovary. Mod Pathol 19:83-89 (Pubitemid 43250982)
81. Kobayashi H, Yamada Y, Kanayama S, Furukawa N, Noguchi T, Haruta S, Yoshida S, Sakata M, Sado T, Oi H (2009) The role of hepatocyte nuclear factor-1beta in the pathogenesis of clear cell carcinoma of the ovary. Int J Gynecol Cancer 19:471-479
82. Horiuchi A, Imai T, Wang C, Ohira S, Feng Y, Nikaido T, Konishi I (2003) Upregulation of small GTPases, RhoA and RhoC, is associated with tumor progression in ovarian carcinoma. Lab Invest 83:861-870 (Pubitemid 36723695)
83. Canet B, Pons C, Espinosa I, Prat J (2011) Ovarian clear cell carcinomas: RHO GTPases may contribute to explain their singular biologic behavior. Hum Pathol 42:833-839
84. Itamochi H, Kigawa J, Sugiyama T, Kikuchi Y, Suzuki M, Terakawa N (2002) Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstet Gynecol 100:281-287 (Pubitemid 34874791)