Mucinous borderline ovarian tumors with BRAF


Journal

Archives of gynecology and obstetrics
ISSN: 1432-0711
Titre abrégé: Arch Gynecol Obstet
Pays: Germany
ID NLM: 8710213

Informations de publication

Date de publication:
08 2020
Historique:
received: 08 10 2019
accepted: 04 06 2020
pubmed: 20 6 2020
medline: 6 11 2020
entrez: 20 6 2020
Statut: ppublish

Résumé

Mucinous ovarian carcinomas (MOCs) are relatively rare. It has been proposed that a subset of mucinous cystadenomas (MCAs) may progress to mucinous borderline tumors (MBTs), and then to MOCs. KRAS is the predominantly mutated gene in MOC; however, other associated mutations and the mechanism underlying carcinogenesis in MOC remain unclear. Here, we assessed molecular genetic alterations in mucinous ovarian tumors and constructed mutation profiles. Using the Sanger sequencing method, we assessed genetic mutations (KRAS, BRAF, TP53, and PIK3CA) in 16 cases of MOC, 10 cases of MBT, and 12 cases of MCA. Among MOC cases, the prevalence of G12D and G13D KRAS mutations was 43.8% (7/16). No MOC cases showed V600E BRAF and TP53 mutations. Among MBT cases, the prevalence of G12D KRAS mutation was 20.0% (2/10), those of TP53 and PIK3CA mutations were nil, and that of V600E BRAF mutation was 40% (4/10). None of the genetic mutations assessed were detected among MCA cases. These results suggest that MBT with V600E BRAF mutation may rarely progress to MOC, while MBT with G12D or G13D KRAS mutation may more commonly progress to MOC.

Identifiants

pubmed: 32556513
doi: 10.1007/s00404-020-05638-8
pii: 10.1007/s00404-020-05638-8
pmc: PMC7321901
doi:

Substances chimiques

BRAF protein, human EC 2.7.11.1
Proto-Oncogene Proteins B-raf EC 2.7.11.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

487-495

Références

Siegel RL, Miller KD (2019) Cancer statistics. CA Cancer J Clin 69(1):7–34. https://doi.org/10.3322/caac.21551
doi: 10.3322/caac.21551
Shih Ie M, Kurman RJ (2004) Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 164(5):1511–1518
doi: 10.1016/S0002-9440(10)63708-X
Gilks CB (2004) Subclassification of ovarian surface epithelial tumors based on correlation of histologic and molecular pathologic data. Int J Gynecol Pathol 23(3):200–205
doi: 10.1097/01.pgp.0000130446.84670.93
Kurman RJ, Shih Ie M (2011) Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer–shifting the paradigm. Hum Pathol 42(7):918–931. https://doi.org/10.1016/j.humpath.2011.03.003
doi: 10.1016/j.humpath.2011.03.003 pubmed: 21683865 pmcid: 3148026
Tabrizi AD, Kalloger SE, Kobel M, Cipollone J, Roskelley CD, Mehl E, Gilks CB (2010) Primary ovarian mucinous carcinoma of intestinal type: significance of pattern of invasion and immunohistochemical expression profile in a series of 31 cases. Int J Gynecol Pathol 29(2):99–107. https://doi.org/10.1097/PGP.0b013e3181bbbcc1
doi: 10.1097/PGP.0b013e3181bbbcc1
Seidman JD, Horkayne-Szakaly I, Haiba M, Boice CR, Kurman RJ, Ronnett BM (2004) The histologic type and stage distribution of ovarian carcinomas of surface epithelial origin. Int J Gynecol Pathol 23(1):41–44. https://doi.org/10.1097/01.pgp.0000101080.35393.16
doi: 10.1097/01.pgp.0000101080.35393.16 pubmed: 14668549
Ricci F, Affatato R, Carrassa L, Damia G (2018) Recent insights into mucinous ovarian carcinoma. Int J Mol Sci 19:6. https://doi.org/10.3390/ijms19061569
doi: 10.3390/ijms19061569
Vang R, Shih Ie M, Kurman RJ (2009) Ovarian low-grade and high-grade serous carcinoma: pathogenesis, clinicopathologic and molecular biologic features, and diagnostic problems. Adv Anat Pathol 16(5):267–282. https://doi.org/10.1097/PAP.0b013e3181b4fffa
doi: 10.1097/PAP.0b013e3181b4fffa pubmed: 19700937 pmcid: 2745605
Mandai M, Konishi I, Kuroda H, Komatsu T, Yamamoto S, Nanbu K, Matsushita K, Fukumoto M, Yamabe H, Mori T (1998) Heterogeneous distribution of K-ras-mutated epithelia in mucinous ovarian tumors with special reference to histopathology. Hum Pathol 29(1):34–40
doi: 10.1016/S0046-8177(98)90387-2
Takeshima Y, Amatya VJ, Daimaru Y, Nakayori F, Nakano T, Inai K (2001) Heterogeneous genetic alterations in ovarian mucinous tumors: application and usefulness of laser capture microdissection. Hum Pathol 32(11):1203–1208. https://doi.org/10.1053/hupa.2001.28956
doi: 10.1053/hupa.2001.28956 pubmed: 11727259
Mok SC, Bell DA, Knapp RC, Fishbaugh PM, Welch WR, Muto MG, Berkowitz RS, Tsao SW (1993) Mutation of K-ras protooncogene in human ovarian epithelial tumors of borderline malignancy. Cancer Res 53(7):1489–1492
pubmed: 8384077
Mayr D, Hirschmann A, Lohrs U, Diebold J (2006) KRAS and BRAF mutations in ovarian tumors: a comprehensive study of invasive carcinomas, borderline tumors and extraovarian implants. Gynecol Oncol 103(3):883–887. https://doi.org/10.1016/j.ygyno.2006.05.029
doi: 10.1016/j.ygyno.2006.05.029 pubmed: 16806438
Lee YJ, Lee MY, Ruan A, Chen CK, Liu HP, Wang CJ, Chao WR, Han CP (2016) Multipoint Kras oncogene mutations potentially indicate mucinous carcinoma on the entire spectrum of mucinous ovarian neoplasms. Oncotarget 7(50):82097–82103. https://doi.org/10.18632/oncotarget.13449
doi: 10.18632/oncotarget.13449 pubmed: 27888800 pmcid: 5347677
Fabjani G, Kriegshaeuser G, Schuetz A, Prix L, Zeillinger R (2005) Biochip for K-ras mutation screening in ovarian cancer. Clin Chem 51(4):784–787. https://doi.org/10.1373/clinchem.2004.041194
doi: 10.1373/clinchem.2004.041194 pubmed: 15788786
Dhomen N, Reis-Filho JS, da Rocha DS, Hayward R, Savage K, Delmas V, Larue L, Pritchard C, Marais R (2009) Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 15(4):294–303. https://doi.org/10.1016/j.ccr.2009.02.022
doi: 10.1016/j.ccr.2009.02.022 pubmed: 19345328
Xing M (2007) BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocr Rev 28(7):742–762. https://doi.org/10.1210/er.2007-0007
doi: 10.1210/er.2007-0007 pubmed: 17940185
Dvorak K, Aggeler B, Palting J, McKelvie P, Ruszkiewicz A, Waring P (2014) Immunohistochemistry with the anti-BRAF V600E (VE1) antibody: impact of pre-analytical conditions and concordance with DNA sequencing in colorectal and papillary thyroid carcinoma. Pathology 46(6):509–517. https://doi.org/10.1097/PAT.0000000000000119
doi: 10.1097/PAT.0000000000000119 pubmed: 25014730 pmcid: 4233678
Taieb J, Le Malicot K, Shi Q, Penault-Llorca F, Bouche O, Tabernero J, Mini E, Goldberg RM, Folprecht G, Luc Van Laethem J, Sargent DJ, Alberts SR, Emile JF, Laurent Puig P, Sinicrope FA (2017) Prognostic value of BRAF and KRAS mutations in MSI and MSS stage III colon cancer. J Natl Cancer Inst 109:5. https://doi.org/10.1093/jnci/djw272
doi: 10.1093/jnci/djw272
Kreitman RJ (2019) Hairy cell leukemia: present and future directions. Leuk Lymphoma 1:11. https://doi.org/10.1080/10428194.2019.1608536
doi: 10.1080/10428194.2019.1608536
Wong KK, Tsang YT, Deavers MT, Mok SC, Zu Z, Sun C, Malpica A, Wolf JK, Lu KH, Gershenson DM (2010) BRAF mutation is rare in advanced-stage low-grade ovarian serous carcinomas. Am J Pathol 177(4):1611–1617. https://doi.org/10.2353/ajpath.2010.100212
doi: 10.2353/ajpath.2010.100212 pubmed: 20802181 pmcid: 2947258
Grisham RN, Iyer G, Garg K, Delair D, Hyman DM, Zhou Q, Iasonos A, Berger MF, Dao F, Spriggs DR, Levine DA, Aghajanian C, Solit DB (2013) BRAF mutation is associated with early stage disease and improved outcome in patients with low-grade serous ovarian cancer. Cancer 119(3):548–554. https://doi.org/10.1002/cncr.27782
doi: 10.1002/cncr.27782 pubmed: 22930283
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(8):1581–1586
doi: 10.1002/(SICI)1097-0142(19970415)79:8<1581::AID-CNCR21>3.0.CO;2-T
Hunter SM, Gorringe KL, Christie M, Rowley SM, Bowtell DD (2012) Australian Ovarian Cancer Study G, Campbell IG Pre-invasive ovarian mucinous tumors are characterized by CDKN2A and RAS pathway aberrations. Clin Cancer Res 18(19):5267–5277. https://doi.org/10.1158/1078-0432.CCR-12-1103
doi: 10.1158/1078-0432.CCR-12-1103 pubmed: 22891197
Ryland GL, Hunter SM, Doyle MA, Rowley SM, Christie M, Allan PE, Bowtell DD (2013) Australian Ovarian Cancer Study G, Gorringe KL, Campbell IG RNF43 is a tumour suppressor gene mutated in mucinous tumours of the ovary. J Pathol. 229(3):469–476. https://doi.org/10.1002/path.4134
doi: 10.1002/path.4134 pubmed: 23096461
Wang Y, Helland A, Holm R, Kristensen GB, Borresen-Dale AL (2005) PIK3CA mutations in advanced ovarian carcinomas. Hum Mutat 25(3):322. https://doi.org/10.1002/humu.9316
doi: 10.1002/humu.9316 pubmed: 15712344
Mackenzie R, Kommoss S, Winterhoff BJ, Kipp BR, Garcia JJ, Voss J, Halling K, Karnezis A, Senz J, Yang W, Prigge ES, Reuschenbach M, Doeberitz MV, Gilks BC, Huntsman DG, Bakkum-Gamez J, McAlpine JN, Anglesio MS (2015) Targeted deep sequencing of mucinous ovarian tumors reveals multiple overlapping RAS-pathway activating mutations in borderline and cancerous neoplasms. BMC Cancer 15:415. https://doi.org/10.1186/s12885-015-1421-8
doi: 10.1186/s12885-015-1421-8 pubmed: 25986173 pmcid: 4494777
Ryland GL, Hunter SM, Doyle MA, Caramia F, Li J, Rowley SM, Christie M, Allan PE, Stephens AN, Bowtell DD (2015) Australian Ovarian Cancer Study G, Campbell IG, Gorringe KL Mutational landscape of mucinous ovarian carcinoma and its neoplastic precursors. Genome Med 7(1):87. https://doi.org/10.1186/s13073-015-0210-y
doi: 10.1186/s13073-015-0210-y pubmed: 26257827 pmcid: 4528310
Vereczkey I, Serester O, Dobos J, Gallai M, Szakacs O, Szentirmay Z, Toth E (2011) Molecular characterization of 103 ovarian serous and mucinous tumors. Pathol Oncol Res 17(3):551–559. https://doi.org/10.1007/s12253-010-9345-8
doi: 10.1007/s12253-010-9345-8 pubmed: 21136228
Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, Hussain J, Reis-Filho JS, Springer CJ, Pritchard C, Marais R (2010) Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140(2):209–221. https://doi.org/10.1016/j.cell.2009.12.040
doi: 10.1016/j.cell.2009.12.040 pubmed: 20141835 pmcid: 2872605
Omholt K, Platz A, Kanter L, Ringborg U, Hansson J (2003) NRAS and BRAF mutations arise early during melanoma pathogenesis and are preserved throughout tumor progression. Clin Cancer Res 9(17):6483–6488
pubmed: 14695152
Beeram M, Patnaik A, Rowinsky EK (2005) Raf: a strategic target for therapeutic development against cancer. J Clin Oncol 23(27):6771–6790. https://doi.org/10.1200/JCO.2005.08.036
doi: 10.1200/JCO.2005.08.036 pubmed: 16170185
Marquette A, Andre J, Bagot M, Bensussan A, Dumaz N (2011) ERK and PDE4 cooperate to induce RAF isoform switching in melanoma. Nat Struct Mol Biol 18(5):584–591. https://doi.org/10.1038/nsmb.2022
doi: 10.1038/nsmb.2022 pubmed: 21478863
Dumaz N, Hayward R, Martin J, Ogilvie L, Hedley D, Curtin JA, Bastian BC, Springer C, Marais R (2006) In melanoma, RAS mutations are accompanied by switching signaling from BRAF to CRAF and disrupted cyclic AMP signaling. Cancer Res 66(19):9483–9491. https://doi.org/10.1158/0008-5472.CAN-05-4227
doi: 10.1158/0008-5472.CAN-05-4227 pubmed: 17018604
Garnett MJ, Rana S, Paterson H, Barford D, Marais R (2005) Wild-type and mutant B-RAF activate C-RAF through distinct mechanisms involving heterodimerization. Mol Cell 20(6):963–969. https://doi.org/10.1016/j.molcel.2005.10.022
doi: 10.1016/j.molcel.2005.10.022 pubmed: 16364920
Terai K, Matsuda M (2006) The amino-terminal B-Raf-specific region mediates calcium-dependent homo- and hetero-dimerization of Raf. EMBO J 25(15):3556–3564. https://doi.org/10.1038/sj.emboj.7601241
doi: 10.1038/sj.emboj.7601241 pubmed: 16858395 pmcid: 1538552
Sullivan RJ, Flaherty K (2013) MAP kinase signaling and inhibition in melanoma. Oncogene 32(19):2373–2379. https://doi.org/10.1038/onc.2012.345
doi: 10.1038/onc.2012.345 pubmed: 22945644
Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA (2002) Mutations of the BRAF gene in human cancer. Nature 417(6892):949–954. https://doi.org/10.1038/nature00766
doi: 10.1038/nature00766
Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, Robbins CM, Moses TY, Hostetter G, Wagner U, Kakareka J, Salem G, Pohida T, Heenan P, Duray P, Kallioniemi O, Hayward NK, Trent JM, Meltzer PS (2003) High frequency of BRAF mutations in nevi. Nat Genet 33(1):19–20. https://doi.org/10.1038/ng1054
doi: 10.1038/ng1054
Dong J, Phelps RG, Qiao R, Yao S, Benard O, Ronai Z, Aaronson SA (2003) BRAF oncogenic mutations correlate with progression rather than initiation of human melanoma. Cancer Res 63(14):3883–3885
pubmed: 12873977
Damsky W, Micevic G, Meeth K, Muthusamy V, Curley DP, Santhanakrishnan M, Erdelyi I, Platt JT, Huang L, Theodosakis N, Zaidi MR, Tighe S, Davies MA, Dankort D, McMahon M, Merlino G, Bardeesy N, Bosenberg M (2015) mTORC1 activation blocks BrafV600E-induced growth arrest but is insufficient for melanoma formation. Cancer Cell 27(1):41–56. https://doi.org/10.1016/j.ccell.2014.11.014
doi: 10.1016/j.ccell.2014.11.014 pubmed: 25584893 pmcid: 4295062
Mueller JJ, Schlappe BA, Kumar R, Olvera N, Dao F, Abu-Rustum N, Aghajanian C, DeLair D, Hussein YR, Soslow RA, Levine DA, Weigelt B (2018) Massively parallel sequencing analysis of mucinous ovarian carcinomas: genomic profiling and differential diagnoses. Gynecol Oncol 150(1):127–135. https://doi.org/10.1016/j.ygyno.2018.05.008
doi: 10.1016/j.ygyno.2018.05.008 pubmed: 29793804 pmcid: 6105459
Dankner M, Rose AAN, Rajkumar S, Siegel PM, Watson IR (2018) Classifying BRAF alterations in cancer: new rational therapeutic strategies for actionable mutations. Oncogene 37(24):3183–3199. https://doi.org/10.1038/s41388-018-0171-x
doi: 10.1038/s41388-018-0171-x pubmed: 29540830
McCormick F (2018) c-Raf in KRas mutant cancers: a moving target. Cancer Cell 33(2):158–159. https://doi.org/10.1016/j.ccell.2018.01.017
doi: 10.1016/j.ccell.2018.01.017 pubmed: 29438690 pmcid: 6464632
Cheasley D, Wakefield MJ, Ryland GL, Allan PE, Alsop K, Amarasinghe KC, Ananda S, Anglesio MS, Au-Yeung G, Bohm M, Bowtell DDL, Brand A, Chenevix-Trench G, Christie M, Chiew YE, Churchman M, DeFazio A, Demeo R, Dudley R, Fairweather N, Fedele CG, Fereday S, Fox SB, Gilks CB, Gourley C, Hacker NF, Hadley AM, Hendley J, Ho GY, Hughes S, Hunstman DG, Hunter SM, Jobling TW, Kalli KR, Kaufmann SH, Kennedy CJ, Kobel M, Le Page C, Li J, Lupat R, McNally OM, McAlpine JN, Mes-Masson AM, Mileshkin L, Provencher DM, Pyman J, Rahimi K, Rowley SM, Salazar C, Samimi G, Saunders H, Semple T, Sharma R, Sharpe AJ, Stephens AN, Thio N, Torres MC, Traficante N, Xing Z, Zethoven M, Antill YC, Scott CL, Campbell IG, Gorringe KL (2019) The molecular origin and taxonomy of mucinous ovarian carcinoma. Nat Commun 10(1):3935. https://doi.org/10.1038/s41467-019-11862-x
doi: 10.1038/s41467-019-11862-x pubmed: 31477716 pmcid: 6718426

Auteurs

Kaori Ohnishi (K)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Kentaro Nakayama (K)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan. kn88@med.shimane-u.ac.jp.

Masako Ishikawa (M)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Tomoka Ishibashi (T)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Hitomi Yamashita (H)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Kohei Nakamura (K)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Toshiko Minamoto (T)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Kouji Iida (K)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Sultana Razia (S)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

Noriyoshi Ishikawa (N)

Department of Organ Pathology, Shimane University School of Medicine, Izumo, 6938501, Japan.

Satoru Kyo (S)

Department of Obstetrics and Gynecology, Shimane University School of Medicine, Enyacho 89-1, Izumo, Shimane, 6938501, Japan.

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