The genomic trajectory of ovarian high-grade serous carcinoma can be observed in STIC lesions.
STIC
evolution
high‐grade serous carcinoma
whole‐genome duplication
Journal
The Journal of pathology
ISSN: 1096-9896
Titre abrégé: J Pathol
Pays: England
ID NLM: 0204634
Informations de publication
Date de publication:
02 Jul 2024
02 Jul 2024
Historique:
revised:
18
04
2024
received:
23
02
2024
accepted:
22
05
2024
medline:
3
7
2024
pubmed:
3
7
2024
entrez:
2
7
2024
Statut:
aheadofprint
Résumé
Ovarian high-grade serous carcinoma (HGSC) originates in the fallopian tube, with secretory cells carrying a TP53 mutation, known as p53 signatures, identified as potential precursors. p53 signatures evolve into serous tubal intraepithelial carcinoma (STIC) lesions, which in turn progress into invasive HGSC, which readily spreads to the ovary and disseminates around the peritoneal cavity. We recently investigated the genomic landscape of early- and late-stage HGSC and found higher ploidy in late-stage (median 3.1) than early-stage (median 2.0) samples. Here, to explore whether the high ploidy and possible whole-genome duplication (WGD) observed in late-stage disease were determined early in the evolution of HGSC, we analysed archival formalin-fixed paraffin-embedded (FFPE) samples from five HGSC patients. p53 signatures and STIC lesions were laser-capture microdissected and sequenced using shallow whole-genome sequencing (sWGS), while invasive ovarian/fallopian tube and metastatic carcinoma samples underwent macrodissection and were profiled using both sWGS and targeted next-generation sequencing. Results showed highly similar patterns of global copy number change between STIC lesions and invasive carcinoma samples within each patient. Ploidy changes were evident in STIC lesions, but not p53 signatures, and there was a strong correlation between ploidy in STIC lesions and invasive ovarian/fallopian tube and metastatic samples in each patient. The reconstruction of sample phylogeny for each patient from relative copy number indicated that high ploidy, when present, occurred early in the evolution of HGSC, which was further validated by copy number signatures in ovarian and metastatic tumours. These findings suggest that aberrant ploidy, suggestive of WGD, arises early in HGSC and is detected in STIC lesions, implying that the trajectory of HGSC may be determined at the earliest stages of tumour development. © 2024 The Author(s). The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Cancer Research UK
ID : A15601
Pays : United Kingdom
Organisme : Cancer Research UK
ID : A15973
Pays : United Kingdom
Organisme : Cancer Research UK
ID : A17197
Pays : United Kingdom
Organisme : Cancer Research UK
ID : A18072
Pays : United Kingdom
Organisme : Cancer Research UK
ID : A19274
Pays : United Kingdom
Organisme : Cancer Research UK
ID : A19694
Pays : United Kingdom
Organisme : National Institute for Health and Care Research (NIHR) Imperial Biomedical Research Centre
ID : P77646
Organisme : La Ligue contre le Cancer
Organisme : La Fondation Nuovo-Soldati
Organisme : Canceropole Lyon Auvergne Rhone-Alpes
Informations de copyright
© 2024 The Author(s). The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.
Références
Piek JM, vanDiest PJ, Zweemer RP, et al. Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 2001; 195: 451–456.
Medeiros F, Muto MG, Lee Y, et al. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am J Surg Pathol 2006; 30: 230–236.
Mehra K, Mehrad M, Ning G, et al. STICS, SCOUTs and p53 signatures; a new language for pelvic serous carcinogenesis. Front Biosci (Elite Ed) 2011; 3: 625–634.
Vang R, Visvanathan K, Gross A, et al. Validation of an algorithm for the diagnosis of serous tubal intraepithelial carcinoma. Int J GynecolPathol 2012; 31: 243–253.
Ducie J, Dao F, Considine M, et al. Molecular analysis of high‐grade serous ovarian carcinoma with and without associated serous tubal intra‐epithelial carcinoma. Nat Commun 2017; 8: 990.
Eckert MA, Pan S, Hernandez KM, et al. Genomics of ovarian cancer progression reveals diverse metastatic trajectories including intraepithelial metastasis to the fallopian tube. Cancer Discov 2016; 6: 1342–1351.
Labidi‐Galy SI, Papp E, Hallberg D, et al. High grade serous ovarian carcinomas originate in the fallopian tube. Nat Commun 2017; 8: 1093.
Bashashati A, Ha G, Tone A, et al. Distinct evolutionary trajectories of primary high‐grade serous ovarian cancers revealed through spatial mutational profiling. J Pathol 2013; 231: 21–34.
Smith P, Bradley T, Gavarró LM, et al. The copy number and mutational landscape of recurrent ovarian high‐grade serous carcinoma. Nat Commun 2023; 14: 4387.
Cheng Z, Mirza H, Ennis DP, et al. The genomic landscape of early‐stage ovarian high‐grade serous carcinoma. Clin Cancer Res 2022; 28: 2911–2922.
Li H, Durbin R. Fast and accurate short read alignment with burrows–wheeler transform. Bioinformatics 2009; 25: 1754–1760.
Sandmann S, deGraaf AO, Karimi M, et al. Evaluating variant calling tools for non‐matched next‐generation sequencing data. Sci Rep 2017; 7: 43169.
Benjamin D, Sato T, Cibulskis K, et al. Calling somatic SNVs and Indels with Mutect2. bioRxiv 2019; 861054. [Not peer reviewed].
Saunders CT, Wong WS, Swamy S, et al. Strelka: accurate somatic small‐variant calling from sequenced tumor‐normal sample pairs. Bioinformatics 2012; 28: 1811–1817.
Scheinin I, Sie D, Bengtsson H, et al. DNA copy number analysis of fresh and formalin‐fixed specimens by shallow whole‐genome sequencing with identification and exclusion of problematic regions in the genome assembly. Genome Res 2014; 24: 2022–2032.
van deWiel MA, Kim KI, Vosse SJ, et al. CGHcall: calling aberrations for array CGH tumor profiles. Bioinformatics 2007; 23: 892–894.
Aujla S, Aloe C, Vannitamby A, et al. Programmed death‐ligand 1 copy number loss in NSCLC associates with reduced programmed death‐ligand 1 tumor staining and a cold Immunophenotype. J Thoracic Oncol 2022; 17: 675–687.
Macintyre G, Goranova T, De Silva D, et al. Copy number signatures and mutational processes in ovarian carcinoma. Nat Genet 2018; 50: 1262–1270.
Steele CD, Abbasi A, Islam SMA, et al. Signatures of copy number alterations in human cancer. Nature 2022; 606: 984–991.
Singh N, Piskorz AM, Bosse T, et al. p53 immunohistochemistry is an accurate surrogate for TP53 mutational analysis in endometrial carcinoma biopsies. J Pathol 2020; 250: 336–345.
Sondka Z, Bamford S, Cole CG, et al. The COSMIC cancer gene census: describing genetic dysfunction across all human cancers. Nat Rev Cancer 2018; 18: 696–705.
Nagasawa S, Ikeda K, Horie‐Inoue K, et al. Systematic identification of characteristic genes of ovarian clear cell carcinoma compared with high‐grade serous carcinoma based on RNA‐sequencing. Int J Mol Sci 2019; 20: 4330.
Akahane T, Masuda K, Hirasawa A, et al. TP53 variants in p53 signatures and the clonality of STICs in RRSO samples. J Gynecol Oncol 2022; 33: e50.
Karst AM, Jones PM, Vena N, et al. Cyclin E1 deregulation occurs early in secretory cell transformation to promote formation of fallopian tube‐derived high‐grade serous ovarian cancers. Cancer Res 2014; 74: 1141–1152.
Bronder D, Tighe A, Wangsa D, et al. TP53 loss initiates chromosomal instability in fallopian tube epithelial cells. Dis Model Mech 2021; 14: dmm049001.
Mei J, Tian H, Huang HS, et al. Cellular models of development of ovarian high‐grade serous carcinoma: a review of cell of origin and mechanisms of carcinogenesis. Cell Prolif 2021; 54: e13029.
Mermel CH, Schumacher SE, Hill B, et al. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy‐number alteration in human cancers. Genome Biol 2011; 12: R41.
Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474: 609–615.
Kim JE, Choi J, Sung CO, et al. High prevalence of TP53 loss and whole‐genome doubling in early‐onset colorectal cancer. Exp Mol Med 2021; 53: 446–456.
Lu B, Curtius K, Graham TA, et al. CNETML: maximum likelihood inference of phylogeny from copy number profiles of multiple samples. Genome Biol 2023; 24: 144.
Baslan T, Morris JP, Zhao Z, et al. Ordered and deterministic cancer genome evolution after p53 loss. Nature 2022; 608: 795–802.
Ahmed AA, Etemadmoghadam D, Temple J, et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol 2010; 221: 49–56.
Köbel M, Kang EY, Weir A, et al. p53 and ovarian carcinoma survival: an ovarian tumor tissue analysis consortium study. J Pathol Clin Res 2023; 9: 208–222.
McGranahan N, Favero F, deBruin EC, et al. Clonal status of actionable driver events and the timing of mutational processes in cancer evolution. Sci Transl Med 2015; 7: 283ra254.
Bielski CM, Zehir A, Penson AV, et al. Genome doubling shapes the evolution and prognosis of advanced cancers. Nat Genet 2018; 50: 1189–1195.
Zeng J, Hills SA, Ozono E, et al. Cyclin E‐induced replicative stress drives p53‐dependent whole‐genome duplication. Cell 2023; 186: 528–542.e14.
Nichols CA, Gibson WJ, Brown MS, et al. Loss of heterozygosity of essential genes represents a widespread class of potential cancer vulnerabilities. Nat Commun 2020; 11: 2517.
Ciriello G, Miller ML, Aksoy BA, et al. Emerging landscape of oncogenic signatures across human cancers. Nat Genet 2013; 45: 1127–1133.
Moore K, Colombo N, Scambia G, et al. Maintenance olaparib in patients with newly diagnosed advanced ovarian cancer. N Engl J Med 2018; 379: 2495–2505.
Monk BJ, Parkinson C, Lim MC, et al. A randomized, phase III trial to evaluate rucaparib monotherapy as maintenance treatment in patients with newly diagnosed ovarian cancer (ATHENA–MONO/GOG‐3020/ENGOT‐ov45). J Clin Oncol 2022; 40: 3952–3964.
Shih IM, Wang Y, Wang TL. The origin of ovarian cancer species and precancerous landscape. Am J Pathol 2021; 191: 26–39.
Engqvist H, Parris TZ, Biermann J, et al. Integrative genomics approach identifies molecular features associated with early‐stage ovarian carcinoma histotypes. Sci Rep 2020; 10: 7946.
Saotome K, Chiyoda T, Aimono E, et al. Clinical implications of next‐generation sequencing‐based panel tests for malignant ovarian tumors. Cancer Med 2020; 9: 7407–7417.
Iyer S, Zhang S, Yucel S, et al. Genetically defined syngeneic mouse models of ovarian cancer as tools for the discovery of combination immunotherapy. Cancer Discov 2020; 11: 384–407.
Knudson AG Jr. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci U S A 1971; 68: 820–823.
Wang Y, Douville C, Chien Y‐W, et al. Aneuploidy landscape in precursors of ovarian cancer. Clin Cancer Res 2023; 30: 600–615.
Visvanathan K, Shaw P, May BJ, et al. Fallopian tube lesions in women at high risk for ovarian cancer: a multicenter study. Cancer Prev Res (Phila) 2018; 11: 697–706.
Ruel‐Laliberté J, Kasasni SM, Oprea D, et al. Outcome and management of serous tubal intraepithelial carcinoma following opportunistic salpingectomy: systematic review and meta‐analysis. J Obstet Gynaecol Can 2022; 44: 1174–1180.
Poell JB, Mendeville M, Sie D, et al. ACE: absolute copy number estimation from low‐coverage whole‐genome sequencing data. Bioinformatics 2019; 35: 2847–2849.
Adalsteinsson VA, Ha G, Freeman SS, et al. Scalable whole‐exome sequencing of cell‐free DNA reveals high concordance with metastatic tumors. Nat Commun 2017; 8: 1324.
Kyo S, Ishikawa N, Nakamura K, et al. The fallopian tube as origin of ovarian cancer: change of diagnostic and preventive strategies. Cancer Med 2020; 9: 421–431.
Goranova T, Ennis D, Piskorz AM, et al. Safety and utility of image‐guided research biopsies in relapsed high‐grade serous ovarian carcinoma‐experience of the BriTROC consortium. Br J Cancer 2017; 116: 1294–1301.