Clear cell carcinoma of the ovary: Molecular insights and future therapeutic perspectives

Journal of Gynecologic Oncology

Volumn 27, Issue 3, 2016, Pages

  Mabuchi, Seiji ^a   Sugiyama, Toru ^b   Kimura, Tadashi ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b IWATE MEDICAL UNIVERSITY   (Japan)

Author keywords

Adenocarcinoma; Antineoplastic agents; ARID1A; Carcinogenesis; Clear cell; Interleukin 6; Salvage therapy

Indexed keywords

CYTOTOXIC AGENT; HEPATOCYTE NUCLEAR FACTOR 1BETA; INTERLEUKIN 6; LURBINECTEDIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; SCATTER FACTOR RECEPTOR; STAT3 PROTEIN; TRABECTEDIN; VASCULOTROPIN; ANTINEOPLASTIC AGENT;

ARTICLE; CANCER PREVENTION; CANCER SURVIVAL; CARCINOGENESIS; CLEAR CELL CARCINOMA; FEMALE; GENETIC ENGINEERING; HUMAN; OVARY CARCINOMA; PROTEIN EXPRESSION; ADENOCARCINOMA, CLEAR CELL; FORECASTING; METABOLISM; OVARIAN NEOPLASMS; PREVENTION AND CONTROL; TUMOR RECURRENCE;

ADENOCARCINOMA, CLEAR CELL; ANTINEOPLASTIC AGENTS; FEMALE; FORECASTING; HUMANS; NEOPLASM RECURRENCE, LOCAL; OVARIAN NEOPLASMS;

EID: 84962343539     PISSN: 20050380     EISSN: 20050399     Source Type: Journal    
DOI: 10.3802/jgo.2016.27.e31     Document Type: Article

References (71)

1. Serov SF, Scully RE, Sobin LH. Histologic typing of ovarian tumors. Geneva: World Health Organization; 1973.
2. Anglesio MS, Carey MS, Köbel M, Mackay H, Huntsman DG; Vancouver Ovarian Clear Cell Symposium Speakers. Clear cell carcinoma of the ovary: a report from the first Ovarian Clear Cell Symposium, June 24th, 2010. Gynecol Oncol 2011;121:407-15.PUBMED | CROSSREF
3. Oncology Committee of Japan Society of Obstetrics and Gynecology. Annual report of the patients with ovarian cancers. Acta Obstet Gynaecol Jpn 2010;62:827-910.
4. Winter WE III, Maxwell GL, Tian C, Carlson JW, Ozols RF, Rose PG, et al. Prognostic factors for stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol 2007;25:3621-7.PUBMED | CROSSREF
5. Sugiyama T, Kamura T, Kigawa J, Terakawa N, Kikuchi Y, Kita T, et al. Clinical characteristics of clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy. Cancer 2000;88:2584-9.PUBMED | CROSSREF
6. Bamias A, Psaltopoulou T, Sotiropoulou M, Haidopoulos D, Lianos E, Bournakis E, et al. Mucinous but not clear cell histology is associated with inferior survival in patients with advanced stage ovarian carcinoma treated with platinum-paclitaxel chemotherapy. Cancer 2010;116:1462-8.PUBMED | CROSSREF
7. Itamochi H, Kigawa J, Sultana H, Iba T, Akeshima R, Kamazawa S, et al. Sensitivity to anticancer agents and resistance mechanisms in clear cell carcinoma of the ovary. Jpn J Cancer Res 2002;93:723-8.PUBMED | CROSSREF
8. Takakura S, Saito M, Ueda K, Motegi M, Takao M, Yamada K, et al. Irinotecan hydrochloride (CPT-11) and cisplatin as first-line chemotherapy after initial surgery for ovarian clear cell adenocarcinoma. Int Surg 2007;92:202-8. PUBMED
9. Sugiyama T, Yakushiji M, Nishida T, Ushijima K, Okura N, Kigawa J, et al. Irinotecan (CPT-11) combined with cisplatin in patients with refractory or recurrent ovarian cancer. Cancer Lett 1998;128:211-8.PUBMED | CROSSREF
10. Okamoto A, Sugiyama T, Hamano T, Kim JW, Kim BG, Enomoto T, et al. Randomized phase III trial of paclitaxel/carboplatin (PC) versus cisplatin/irinotecan (CPT-P) as first-line chemotherapy in patients with clear cell carcinoma (CCC) of the ovary: a Japanese Gynecologic Oncology Group (JGOG)/GCIG study. J Clin Oncol 2014;32(15 Suppl):abstr 5507.
11. Crotzer DR, Sun CC, Coleman RL, Wolf JK, Levenback CF, Gershenson DM. Lack of effective systemic therapy for recurrent clear cell carcinoma of the ovary. Gynecol Oncol 2007;105:404-8.PUBMED | CROSSREF
12. Takano M, Sugiyama T, Yaegashi N, Sakuma M, Suzuki M, Saga Y, et al. Low response rate of second-line chemotherapy for recurrent or refractory clear cell carcinoma of the ovary: a retrospective Japan Clear Cell Carcinoma Study. Int J Gynecol Cancer 2008;18:937-42.PUBMED | CROSSREF
13. Tan DS, Rye T, Barrie C, Shaw P, Laframboise S, Fyles AW, et al. Analysis of outcomes in patients (pts) with recurrent ovarian clear cell carcinoma (ROCCC): time to rethink our approach to treatment. J Clin Oncol 2014;32(15 Suppl):abstr 5548.
14. Okamoto A, Glasspool RM, Mabuchi S, Matsumura N, Nomura H, Itamochi H, et al. Gynecologic Cancer InterGroup (GCIG) consensus review for clear cell carcinoma of the ovary. Int J Gynecol Cancer 2014;24(9 Suppl 3):S20-5.PUBMED | CROSSREF
15. Alsop K, Fereday S, Meldrum C, deFazio A, Emmanuel C, George J, et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J Clin Oncol 2012;30:2654-63.PUBMED | CROSSREF
16. Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, Zeng T, et al. ARID1A mutations in endometriosisassociated ovarian carcinomas. N Engl J Med 2010;363:1532-43.PUBMED | CROSSREF
17. Kuo KT, Mao TL, Jones S, Veras E, Ayhan A, Wang TL, et al. Frequent activating mutations of PIK3CA in ovarian clear cell carcinoma. Am J Pathol 2009;174:1597-601.PUBMED | CROSSREF
18. McConechy MK, Anglesio MS, Kalloger SE, Yang W, Senz J, Chow C, et al. Subtype-specific mutation of PPP2R1A in endometrial and ovarian carcinomas. J Pathol 2011;223:567-73.PUBMED | CROSSREF
19. Mayr D, Hirschmann A, Löhrs U, Diebold J. KRAS and BRAF mutations in ovarian tumors: a comprehensive study of invasive carcinomas, borderline tumors and extraovarian implants. Gynecol Oncol 2006;103:883-7.PUBMED | CROSSREF
20. Sato N, Tsunoda H, Nishida M, Morishita Y, Takimoto Y, Kubo T, et al. 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 2000;60:7052-6. PUBMED
21. Kuo KT, Mao TL, Chen X, Feng Y, Nakayama K, Wang Y, et al. DNA copy numbers profiles in affinitypurified ovarian clear cell carcinoma. Clin Cancer Res 2010;16:1997-2008.PUBMED | CROSSREF
22. Tan DS, Lambros MB, Rayter S, Natrajan R, Vatcheva R, Gao Q, et al. PPM1D is a potential therapeutic target in ovarian clear cell carcinomas. Clin Cancer Res 2009;15:2269-80.PUBMED | CROSSREF
23. Yamashita Y, Akatsuka S, Shinjo K, Yatabe Y, Kobayashi H, Seko H, et al. Met is the most frequently amplified gene in endometriosis-associated ovarian clear cell adenocarcinoma and correlates with worsened prognosis. PLoS One 2013;8:e57724.PUBMED | CROSSREF
24. Yamamoto S, Tsuda H, Takano M, Tamai S, Matsubara O. Loss of ARID1A protein expression occurs as an early event in ovarian clear-cell carcinoma development and frequently coexists with PIK3CA mutations. Mod Pathol 2012;25:615-24.PUBMED | CROSSREF
25. Chandler RL, Damrauer JS, Raab JR, Schisler JC, Wilkerson MD, Didion JP, et al. Coexistent ARID1APIK3CA mutations promote ovarian clear-cell tumorigenesis through pro-tumorigenic inflammatory cytokine signalling. Nat Commun 2015;6:6118.PUBMED | CROSSREF
26. Sasano T, Mabuchi S, Kuroda H, Kawano M, Matsumoto Y, Takahashi R, et al. Preclinical efficacy for AKT targeting in clear cell carcinoma of the ovary. Mol Cancer Res 2015;13:795-806.PUBMED | CROSSREF
27. Mabuchi S, Kawase C, Altomare DA, Morishige K, Sawada K, Hayashi M, et al. mTOR is a promising therapeutic target both in cisplatin-sensitive and cisplatin-resistant clear cell carcinoma of the ovary. Clin Cancer Res 2009;15:5404-13.PUBMED | CROSSREF
28. Hisamatsu T, Mabuchi S, Matsumoto Y, Kawano M, Sasano T, Takahashi R, et al. Potential role of mTORC2 as a therapeutic target in clear cell carcinoma of the ovary. Mol Cancer Ther 2013;12:1367-77.PUBMED | CROSSREF
29. Miyazawa M, Yasuda M, Fujita M, Kajiwara H, Hirabayashi K, Takekoshi S, et al. Therapeutic strategy targeting the mTOR-HIF-1alpha-VEGF pathway in ovarian clear cell adenocarcinoma. Pathol Int 2009;59:19-27.PUBMED | CROSSREF
30. Mabuchi S, Kawase C, Altomare DA, Morishige K, Hayashi M, Sawada K, et al. Vascular endothelial growth factor is a promising therapeutic target for the treatment of clear cell carcinoma of the ovary. Mol Cancer Ther 2010;9:2411-22.PUBMED | CROSSREF
31. Tsuchiya A, Sakamoto M, Yasuda J, Chuma M, Ohta T, Ohki M, et al. Expression profiling in ovarian clear cell carcinoma: identification of hepatocyte nuclear factor-1 beta as a molecular marker and a possible molecular target for therapy of ovarian clear cell carcinoma. Am J Pathol 2003;163:2503-12.PUBMED | CROSSREF
32. Kim A, Enomoto T, Serada S, Ueda Y, Takahashi T, Ripley B, et al. Enhanced expression of Annexin A4 in clear cell carcinoma of the ovary and its association with chemoresistance to carboplatin. Int J Cancer 2009;125:2316-22.PUBMED | CROSSREF
33. Kato N, Motoyama T. Overexpression of osteopontin in clear cell carcinoma of the ovary: close association with HNF-1beta expression. Histopathology 2008;52:682-8.PUBMED | CROSSREF
34. Sugita S, Morishita Y, Kano J, Furuya S, Shiba-Ishii A, Noguchi M. IGFBP-1 is expressed specifically in ovarian clear cell adenocarcinoma. Histopathology 2011;58:729-38.PUBMED | CROSSREF
35. Yanaihara N, Anglesio MS, Ochiai K, Hirata Y, Saito M, Nagata C, et al. Cytokine gene expression signature in ovarian clear cell carcinoma. Int J Oncol 2012;41:1094-100.PUBMED | CROSSREF
36. Yanaihara N, Hirata Y, Yamaguchi N, Noguchi Y, Saito M, Nagata C, et al. Antitumor effects of interleukin-6 (IL-6)/interleukin-6 receptor (IL-6R) signaling pathway inhibition in clear cell carcinoma of the ovary. Mol Carcinog 2015 Apr 9 [Epub].PUBMED | CROSSREF
37. Bobbs AS, Cole JM, Cowden Dahl KD. Emerging and evolving ovarian cancer animal models. Cancer Growth Metastasis 2015;8(Suppl 1):29-36.PUBMED | CROSSREF
38. Köbel M, Kalloger SE, Carrick J, Huntsman D, Asad H, Oliva E, et al. A limited panel of immunomarkers can reliably distinguish between clear cell and high-grade serous carcinoma of the ovary. Am J Surg Pathol 2009;33:14-21.PUBMED | CROSSREF
39. Hall M, Gourley C, McNeish I, Ledermann J, Gore M, Jayson G, et al. Targeted anti-vascular therapies for ovarian cancer: current evidence. Br J Cancer 2013;108:250-8.PUBMED | CROSSREF
40. Clinical Trials.gov. Sunitinib in patients with recurrent ovarian clear cell carcinoma [Internet]. Bethesda, MD: U.S. National Institute of Health; 2013 [cited 2016 Jan 16]. Available from: https://clinicaltrials.gov/ct2/show/NCT01824615
41. Chan J, Brady WE, Brown J, Shahin MS, Rose PG, Kim JH, et al. A phase II evaluation of sunitinib (SU11248) in the treatment of persistent or recurrent clear cell ovarian carcinoma: an NRG Oncology/ Gynecologic Oncology Group (GOG) study. Gynecol Oncol 2015;138(Suppl 1):3.PUBMED | CROSSREF
42. Mabuchi S, Kuroda H, Takahashi R, Sasano T. The PI3K/AKT/mTOR pathway as a therapeutic target in ovarian cancer. Gynecol Oncol 2015;137:173-9.PUBMED | CROSSREF
43. Hashiguchi Y, Tsuda H, Inoue T, Berkowitz RS, Mok SC. PTEN expression in clear cell adenocarcinoma of the ovary. Gynecol Oncol 2006;101:71-5.PUBMED | CROSSREF
44. Yamamoto S, Tsuda H, Miyai K, Takano M, Tamai S, Matsubara O. Gene amplification and protein overexpression of MET are common events in ovarian clear-cell adenocarcinoma: their roles in tumor progression and prognostication of the patient. Mod Pathol 2011;24:1146-55.PUBMED | CROSSREF
45. Clinical Trials.gov. Clinical trial of lurbinectedin (PM01183) in platinum resistant ovarian cancer patients (CORAIL) [Internet]. Bethesda, MD: U.S. National Institute of Health; 2013 [cited 2016 Jan 16]. Available from: https://www.clinicaltrials.gov/ct2/show/NCT02421588?term=NCT02421588&rank=1
46. Hennessy BT, Timms KM, Carey MS, Gutin A, Meyer LA, Flake DD II, et al. Somatic mutations in BRCA1 and BRCA2 could expand the number of patients that benefit from poly (ADP ribose) polymerase inhibitors in ovarian cancer. J Clin Oncol 2010;28:3570-6.PUBMED | CROSSREF
47. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med 2012;366:1382-92.PUBMED | CROSSREF
48. Pejovic T, Yates JE, Liu HY, Hays LE, Akkari Y, Torimaru Y, et al. Cytogenetic instability in ovarian epithelial cells from women at risk of ovarian cancer. Cancer Res 2006;66:9017-25.PUBMED | CROSSREF
49. Saal LH, Gruvberger-Saal SK, Persson C, Lövgren K, Jumppanen M, Staaf J, et al. Recurrent gross mutations of the PTEN tumor suppressor gene in breast cancers with deficient DSB repair. Nat Genet 2008;40:102-7.PUBMED | CROSSREF
50. Ibrahim YH, García-García C, Serra V, He L, Torres-Lockhart K, Prat A, et al. PI3K inhibition impairs BRCA1/2 expression and sensitizes BRCA-proficient triple-negative breast cancer to PARP inhibition. Cancer Discov 2012;2:1036-47.PUBMED | CROSSREF
51. Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med 2009;361:1475-85.PUBMED | CROSSREF
52. Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: the role of DNA repair pathways. Clin Cancer Res 2008;14:1291-5.PUBMED | CROSSREF
53. Dabholkar M, Vionnet J, Bostick-Bruton F, Yu JJ, Reed E. Messenger RNA levels of XPAC and ERCC1 in ovarian cancer tissue correlate with response to platinum-based chemotherapy. J Clin Invest 1994;94:703-8.PUBMED | CROSSREF
54. Reed E, Yu JJ, Davies A, Gannon J, Armentrout SL. Clear cell tumors have higher mRNA levels of ERCC1 and XPB than other histological types of epithelial ovarian cancer. Clin Cancer Res 2003;9:5299-305. PUBMED
55. Carter NJ, Keam SJ. Trabectedin: a review of its use in the management of soft tissue sarcoma and ovarian cancer. Drugs 2007;67:2257-76.PUBMED | CROSSREF
56. Monk BJ, Herzog TJ, Kaye SB, Krasner CN, Vermorken JB, Muggia FM, et al. Trabectedin plus pegylated liposomal doxorubicin in recurrent ovarian cancer. J Clin Oncol 2010;28:3107-14.PUBMED | CROSSREF
57. Takebayashi Y, Pourquier P, Zimonjic DB, Nakayama K, Emmert S, Ueda T, et al. Antiproliferative activity of ecteinascidin 743 is dependent upon transcription-coupled nucleotide-excision repair. Nat Med 2001;7:961-6.PUBMED | CROSSREF
58. Erba E, Bergamaschi D, Bassano L, Damia G, Ronzoni S, Faircloth GT, et al. Ecteinascidin-743 (ET-743), a natural marine compound, with a unique mechanism of action. Eur J Cancer 2001;37:97-105.PUBMED | CROSSREF
59. Mabuchi S, Hisamatsu T, Kawase C, Hayashi M, Sawada K, Mimura K, et al. The activity of trabectedin as a single agent or in combination with everolimus for clear cell carcinoma of the ovary. Clin Cancer Res 2011;17:4462-73.PUBMED | CROSSREF
60. Kawano M, Mabuchi S, Kishimoto T, Hisamatsu T, Matsumoto Y, Sasano T, et al. Combination treatment with trabectedin and irinotecan or topotecan has synergistic effects against ovarian clear cell carcinoma cells. Int J Gynecol Cancer 2014;24:829-37.PUBMED | CROSSREF
61. Takano M, Kouta H, Kudoh K, Kita T, Kikuchi R, Miyamoto M, et al. Combination therapy with temsirolimus and trabectedin for recurrent clear cell carcinoma of the ovary: a phase II study with biomarker analysis. J Clin Oncol 2015;33(15 Suppl):abstr 5583.
62. Leal JF, Martínez-Díez M, García-Hernández V, Moneo V, Domingo A, Bueren-Calabuig JA, et al. PM01183, a new DNA minor groove covalent binder with potent in vitro and in vivo anti-tumour activity. Br J Pharmacol 2010;161:1099-110.PUBMED | CROSSREF
63. Elez ME, Tabernero J, Geary D, Macarulla T, Kang SP, Kahatt C, et al. First-in-human phase I study of Lurbinectedin (PM01183) in patients with advanced solid tumors. Clin Cancer Res 2014;20:2205-14.PUBMED | CROSSREF
64. Poveda A, Berton-Rigaud D, Ray-Coquard IL, Alexandre J, Provansal M, Soto A, et al. Lurbinectedin (PM01183), an active compound in platinum-resistant/refractory ovarian cancer (PRROC) patients: results of a two-stage, controlled phase II study. J Clin Oncol 2014;32(15 Suppl):abstr 5505.
65. Yagyu T, Tsuji Y, Haruta S, Kitanaka T, Yamada Y, Kawaguchi R, et al. Activation of mammalian target of rapamycin in postmenopausal ovarian endometriosis. Int J Gynecol Cancer 2006;16:1545-51.PUBMED | CROSSREF
66. Mabuchi S, Altomare DA, Connolly DC, Klein-Szanto A, Litwin S, Hoelzle MK, et al. RAD001 (Everolimus) delays tumor onset and progression in a transgenic mouse model of ovarian cancer. Cancer Res 2007;67:2408-13.PUBMED | CROSSREF
67. Taubes G. Cancer research. Cancer prevention with a diabetes pill? Science 2012;335:29.PUBMED | CROSSREF
68. Dowling RJ, Zakikhani M, Fantus IG, Pollak M, Sonenberg N. Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells. Cancer Res 2007;67:10804-12.PUBMED | CROSSREF
69. Hamanishi J, Mandai M, Ikeda T, Minami M, Kawaguchi A, Murayama T, et al. Safety and antitumor activity of anti-PD-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol 2015;33:4015-22.PUBMED | CROSSREF
70. Disis ML, Patel MR, Pant S, Infante JR, Lockhart AC, Kelly K, et al. Avelumab (MSB0010718C), an anti-PD-L1 antibody, in patients with previously treated, recurrent or refractory ovarian cancer: a phase Ib, open-label expansion trial. J Clin Oncol 2015;33(15 Suppl):abstr 5509.
71. Tan DS, Iravani M, McCluggage WG, Lambros MB, Milanezi F, Mackay A, et al. Genomic analysis reveals the molecular heterogeneity of ovarian clear cell carcinomas. Clin Cancer Res 2011;17:1521-34.PUBMED | CROSSREF