Morphological precursors of high-grade serous ovarian cancer

Novikov F.V.; Efremov G.D.

doi:https://doi.org/10.17116/patol20238501174

Close metadata

Abstract:

At the beginning of this century, there was a paradigm shift in understanding the histogenesis of high-grade serous carcinomas. The theory of the origin of these tumors from the ovarian surface epithelium was replaced by the concept of their origin from the secretory epithelium of the fallopian tubes. In recent years, researchers have put forward the hypothesis of the “escape” of the precursor of high-grade serous carcinomas. It allows looking at the carcinogenesis of these neoplasms as a natural history of tumor transformation of the serous epithelium without reference to a specific localization.

Keywords:

high-grade serous carcinoma

STIC

p53 signature

precursor escape

serous carcinogenesis

Authors:

Novikov F.V.

Kursk State Medical University of the Ministry of Health of Russia

Efremov G.D.

N.A. Lopatkin Scientific Research Institute of Urology and Interventional Radiology — branch of the National Medical Research Radiological Center

Received:

20.09.2022

Accepted:

26.10.2022

Close metadata

References:

Soong TR, Dinulescu DM, Xian W, Crum CP. Frontiers in the pathology and pathogenesis of ovarian cancer: cancer precursors and «precursor escape». Hematol Oncol Clin North Am. 2018;32(6):915-928. https://doi.org/10.1016/j.hoc.2018.07.013
Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev. 2001;22(2):255-288. https://doi.org/10.1210/edrv.22.2.0422
Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, Gille JJ, Jongsma AP, Pals G, Kenemans P, et al. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol. 2001;195(4):451-456. https://doi.org/10.1002/path.1000
Medeiros F, Muto MG, Lee Y, Elvin JA, Callahan MJ, Feltmate C, Garber JE, Cramer DW, Crum CP. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol. 2006;30(2):230-236. https://doi.org/10.1097/01.pas.0000180854.28831.77
Bijron JG, Seldenrijk CA, Zweemer RP, Lange JG, Verheijen RH, van Diest PJ. Fallopian tube intraluminal tumor spread from noninvasive precursor lesions: a novel metastatic route in early pelvic carcinogenesis. Am J Surg Pathol. 2013;37(8):1123-1130. https://doi.org/10.1097/PAS.0b013e318282da7f
Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474(7353):609-615. https://doi.org/10.1038/nature10166
Kuhn E, Kurman RJ, Vang R, Sehdev AS, Han G, Soslow R, Wang TL, Shih IeM. TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma — evidence supporting the clonal relationship of the two lesions. J Pathol. 2012;226(3):421-426. https://doi.org/10.1002/path.3023
Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, Stewart C, Fereday S, Caldas C, Defazio A, et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol. 2010;221(1):49-56. https://doi.org/10.1002/path.2696
Kurman RJ, Shih IeM. The dualistic model of ovarian carcinogenesis: revisited, revised, and expanded. Am J Pathol. 2016;186(4):733-747. https://doi.org/10.1016/j.ajpath.2015.11.011
WHO Classification of Tumours Editorial Board. WHO Classification of Tumours. Female genital tumours. 5th ed. Vol. 4. Lyon, France: IARC; 2020.
Kroeger PT Jr, Drapkin R. Pathogenesis and heterogeneity of ovarian cancer. Curr Opin Obstet Gynecol. 2017;29(1):26-34. https://doi.org/10.1097/GCO.0000000000000340
Eckert MA, Pan S, Hernandez KM, Loth RM, Andrade J, Volchenboum SL, Faber P, Montag A, Lastra R, Peter ME, et al. Genomics of ovarian cancer progression reveals diverse metastatic trajectories including intraepithelial metastasis to the Fallopian tube. Cancer Discov. 2016;6(12):1342-1351. https://doi.org/10.1158/2159-8290.CD-16-0607
Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, Gordon RW, et al. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol. 2007;211(1):26-35. https://doi.org/10.1002/path.2091
Jarboe E, Folkins A, Nucci MR, Kindelberger D, Drapkin R, Miron A, Lee Y, Crum CP. Serous carcinogenesis in the fallopian tube: a descriptive classification. Int J Gynecol Pathol. 2008;27(1):1-9. https://doi.org/10.1097/pgp.0b013e31814b191f
Soong TR, Howitt BE, Miron A, Horowitz NS, Campbell F, Feltmate CM, Muto MG, Berkowitz RS, Nucci MR, Xian W, et al. Evidence for lineage continuity between early serous proliferations (ESPs) in the Fallopian tube and disseminated high-grade serous carcinomas. J Pathol. 2018;246(3):344-351. https://doi.org/10.1002/path.5145
Meserve EEK, Brouwer J, Crum CP. Serous tubal intraepithelial neoplasia: the concept and its application. Mod Pathol. 2017;30(5):710-721. https://doi.org/10.1038/modpathol.2016.238
Soong TR, Kolin DL, Teschan NJ, Crum CP. Back to the Future? The Fallopian tube, precursor escape and a dualistic model of high-grade serous carcinogenesis. Cancers (Basel). 2018;10(12):468. https://doi.org/10.3390/cancers10120468
Soong TR, Howitt BE, Horowitz N, Nucci MR, Crum CP. The fallopian tube, «precursor escape» and narrowing the knowledge gap to the origins of high-grade serous carcinoma. Gynecol Oncol. 2019;152(2):426-433. https://doi.org/10.1016/j.ygyno.2018.11.033
Yoon JY, Chapel DB, Goebel E, Qian X, Mito JK, Horowitz NS, Miron A, Soong TR, Xian W, et al. Genomic catastrophe, the peritoneal cavity and ovarian cancer prevention. J Pathol. 2022;257(3):255-261. https://doi.org/10.1002/path.5891
Quartuccio SM, Karthikeyan S, Eddie SL, Lantvit DD, Ó hAinmhire E, Modi DA, Wei JJ, Burdette JE. Mutant p53 expression in fallopian tube epithelium drives cell migration. Int J Cancer. 2015;137(7):1528-1538. https://doi.org/10.1002/ijc.29528
Horn LC, Kafkova S, Leonhardt K, Kellner C, Einenkel J. Serous tubal in situ carcinoma (STIC) in primary peritoneal serous carcinomas. Int J Gynecol Pathol. 2013;32(4):339-344. https://doi.org/10.1097/PGP.0b013e31826a629b
Hutson R, Ramsdale J, Wells M. p53 protein expression in putative precursor lesions of epithelial ovarian cancer. Histopathology. 1995;27(4):367-371. https://doi.org/10.1111/j.1365-2559.1995.tb01528.x
Pothuri B, Leitao MM, Levine DA, Viale A, Olshen AB, Arroyo C, Bogomolniy F, Olvera N, Lin O, Soslow RA, et al. Genetic analysis of the early natural history of epithelial ovarian carcinoma. PLoS One. 2010;5(4):e10358. https://doi.org/10.1371/journal.pone.0010358
Craig E, Clarke R, Rushton G, McCluggage WG. Serous tubal intraepithelial carcinoma (STIC)-like lesions arising in ovarian serous cystadenofibroma: report of 2 cases. Int J Gynecol Pathol. 2015;34(6):535-540. https://doi.org/10.1097/PGP.0000000000000195
Ramanayake N, Russell P, Yang V. High grade serous intraepithelial carcinoma arising in a benign ovarian serous cyst — a bridge too far? Pathology. 2018;50(5):485-489. https://doi.org/10.1016/j.pathol.2018.03.009
Asaturova AV. Sources of highly-malignant serous ovarian carcinomas. Zlokachestvennye opukholi = Malignant Tumors. 2019;9(3s1):9-14. (In Russ.).
Chen EY, Mehra K, Mehrad M, Ning G, Miron A, Mutter GL, Monte N, Quade BJ, McKeon FD, Yassin Y, et al. Secretory cell outgrowth, PAX2 and serous carcinogenesis in the Fallopian tube. J Pathol. 2010;222(1):110-116. https://doi.org/10.1002/path.2739
Asaturova AV, Ezhova LS, Faĭzullina NM, Sannikova MV, Khabas GN. The morphological and immunohistochemical characteristics of changes in the fallopian tube mucosa in ovarian epithelial tumors. Arkhiv Patologii. 2016;78(2):3-9. (In Russ.). https://doi.org/10.17116/patol20167823-9
Mehra KK, Chang MC, Folkins AK, Raho CJ, Lima JF, Yuan L, Mehrad M, Tworoger SS, Crum CP, Saleemuddin A. The impact of tissue block sampling on the detection of p53 signatures in fallopian tubes from women with BRCA 1 or 2 mutations (BRCA+) and controls. Mod Pathol. 2011;24(1):152-156. https://doi.org/10.1038/modpathol.2010.171
Akahane T, Masuda K, Hirasawa A, Kobayashi Y, Ueki A, Kawaida M, Misu K, Nakamura K, Nagai S, Chiyoda T, et al. TP53 variants in p53 signatures and the clonality of STICs in RRSO samples. J Gynecol Oncol. 2022;33(4):e50. https://doi.org/10.3802/jgo.2022.33.e50
Schultheis AM, Martelotto LG, De Filippo MR, Piscuglio S, Ng CK, Hussein YR, Reis-Filho JS, Soslow RA, Weigelt B. TP53 mutational spectrum in endometrioid and serous endometrial cancers. Int J Gynecol Pathol. 2016;35(4):289-300. https://doi.org/10.1097/PGP.0000000000000243
Labidi-Galy SI, Papp E, Hallberg D, Niknafs N, Adleff V, Noe M, Bhattacharya R, Novak M, Jones S, Phallen J, et al. High-grade serous ovarian carcinomas originate in the fallopian tube. Nat Commun. 2017;8(1):1093. https://doi.org/10.1038/s41467-017-00962-1
Bashashati A, Ha G, Tone A, Ding J, Prentice LM, Roth A, Rosner J, Shumansky K, Kalloger S, Senz J, et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J Pathol. 2013;231(1):21-34. https://doi.org/10.1002/path.4230
Wu RC, Wang P, Lin SF, Zhang M, Song Q, Chu T, Wang BG, Kurman RJ, Vang R, Kinzler K, et al. Genomic landscape and evolutionary trajectories of ovarian cancer precursor lesions. J Pathol. 2019;248(1):41-50. https://doi.org/10.1002/path.5219