EWSR1-PATZ1 fusion renal cell carcinoma: a recurrent gene fusion characterizing thyroid-like follicular renal cell carcinoma.
Journal
Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc
ISSN: 1530-0285
Titre abrégé: Mod Pathol
Pays: United States
ID NLM: 8806605
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
11
09
2020
accepted:
12
05
2021
revised:
12
05
2021
pubmed:
9
6
2021
medline:
18
3
2022
entrez:
8
6
2021
Statut:
ppublish
Résumé
Thyroid-like follicular renal cell carcinoma is an uncommon kidney tumor with no distinct molecular alteration described to date. This cohort of eight women with mean and median ages of 45 and 46 years, respectively (range 19-65 years), had unencapsulated, well-circumscribed tumors composed of tightly packed anastomosing follicle-like cysts filled with eosinophilic colloid-like material and lined by cuboidal cells with high nuclear to cytoplasmic ratios, oval to elongated nuclei with perpendicular arrangement toward the lumens, and prominent nuclear overlapping. The stroma between these was minimal with the exception of two tumors. Calcifications and necrosis were absent. Immunohistochemically, the tumors were positive for KRT19 (7/7), PAX8 (5/5), cyclin D1 (6/6), KRT7 (5/7), and AMACR (1/5; focal, weak), and were negative for WT1, TTF1 (transcription termination factor-1), and thyroglobulin. In three of three tumors tested molecularly, EWSR1-PATZ1 fusion was identified by RNA sequencing and confirmed by RT-PCR and Sanger sequencing. Over a follow-up period of 1-7 years, no evidence of recurrence or metastasis has been detected. The EWSR1-PATZ1 fusion has been recognized as a recurrent alteration in a subset of round to spindle cell sarcomas with EWSR1-non-ETS fusions (EWSR1-PATZ1 sarcoma) and in several central nervous system tumors. The finding of an EWSR1-PATZ1 fusion in all three of the thyroid-like follicular renal cell carcinomas for which sufficient tissue was available for genomic profiling provides the first distinct molecular abnormality in thyroid-like follicular renal cell carcinomas, supporting its designation as a distinct diagnostic entity.
Identifiants
pubmed: 34099871
doi: 10.1038/s41379-021-00833-7
pii: S0893-3952(22)00537-3
doi:
Substances chimiques
Kruppel-Like Transcription Factors
0
PATZ1 protein, human
0
RNA-Binding Protein EWS
0
Repressor Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1921-1934Informations de copyright
© 2021. The Author(s), under exclusive licence to United States & Canadian Academy of Pathology.
Références
Amin M, Bichal M, Radhakrishman A, Hes O, McKenney JK, Cheville JC. Primary thyroid-like follicular carcinoma of the kidney: a histologically distinctive primary renal epithelial tumor. Mod Pathol. 2004;17:136–7.
doi: 10.1038/modpathol.3800013
Amin MB, Gupta R, Ondrej H, McKenney JK, Michal M, Young AN, et al. Primary thyroid-like follicular carcinoma of the kidney: report of 6 cases of a histologically distinctive adult renal epithelial neoplasm. Am J Surg Pathol. 2009;33:393–400.
pubmed: 19047894
doi: 10.1097/PAS.0b013e31818cb8f5
Srigley JR, Delahunt B, Eble JN, Egevad L, Epstein JI, Grignon D, et al. The International Society of Urological Pathology (ISUP) Vancouver classification of renal neoplasia. Am J Surg Pathol. 2013;37:1469–89.
pubmed: 24025519
doi: 10.1097/PAS.0b013e318299f2d1
Moch H, Cubilla AL, Humphrey PA, Reuter VE, Ulbright TM. The 2016 WHO classification of tumours of the urinary system and male genital organs-Part A: renal, penile, and testicular tumours. Eur Urol. 2016;70:93–105.
pubmed: 26935559
doi: 10.1016/j.eururo.2016.02.029
Eble JN, Delahunt B. Emerging entities in renal cell neoplasia: thyroid-like follicular renal cell carcinoma and multifocal oncocytoma-like tumours associated with oncocytosis. Pathology. 2018;50:24–36.
pubmed: 29132724
doi: 10.1016/j.pathol.2017.09.005
Trpkov K, Hes O. New and emerging renal entities: a perspective post-WHO 2016 classification. Histopathology. 2019;74:31–59.
pubmed: 30565301
doi: 10.1111/his.13727
Tretiakova MS, Kehr EL, Gore JL, Tykodi SS. Thyroid-like follicular renal cell carcinoma arising within benign mixed epithelial and stromal tumor. Int J Surg Pathol. 2020;28:80–6.
pubmed: 31342803
doi: 10.1177/1066896919863478
pmcid: 31342803
Brunelli M, Eble JN, Zhang S, Martignoni G, Cheng L. Gains of chromosomes 7, 17, 12, 16, and 20 and loss of Y occur early in the evolution of papillary renal cell neoplasia: a fluorescent in situ hybridization study. Mod Pathol. 2003;16:1053–9.
pubmed: 14559990
doi: 10.1097/01.MP.0000090924.90762.94
Cossu-Rocca P, Eble JN, Zhang S, Bonsib SM, Martignoni G, Brunelli M, et al. Interphase cytogenetic analysis with centromeric probes for chromosomes 1, 2, 6, 10, and 17 in 11 tumors from a patient with bilateral renal oncocytosis. Mod Pathol. 2008;21:498–504.
pubmed: 18246052
doi: 10.1038/modpathol.2008.16
Cheng L, Zhang S, Wang L, MacLennan GT, Davidson DD. Fluorescence in situ hybridization in surgical pathology: principles and applications. J Pathol Clin Res. 2017;3:73–99.
pubmed: 28451457
pmcid: 5402181
doi: 10.1002/cjp2.64
Kadri S, Long BC, Mujacic I, Zhen CJ, Wurst MN, Sharma S, et al. Clinical validation of a next-generation sequencing genomic oncology panel via cross-platform benchmarking against established amplicon sequencing assays. J Mol Diagn. 2017;19:43–56.
pubmed: 27836695
doi: 10.1016/j.jmoldx.2016.07.012
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60.
pubmed: 2705234
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Mose LE, Wilkerson MD, Hayes DN, Perou CM, Parker JS. ABRA: improved coding indel detection via assembly-based realignment. Bioinformatics. 2014;30:2813–5.
pubmed: 24907369
pmcid: 4173014
doi: 10.1093/bioinformatics/btu376
Li MM, Datto M, Duncavage EJ, Kulkarni S, Lindeman NI, Roy S, et al. Standards and guidelines for the interpretation and reporting of sequence variants in cancer: a joint consensus recommendation of the Association for Molecular Pathology, American Society of Clinical Oncology, and College of American Pathologists. J Mol Diagn. 2017;19:4–23.
pubmed: 27993330
pmcid: 5707196
doi: 10.1016/j.jmoldx.2016.10.002
Talevich E, Shain AH, Botton T, Bastian BC. CNVkit: genome-wide copy number detection and visualization from targeted DNA sequencing. PLoS Comput Biol. 2016;12:e1004873.
pubmed: 27100738
pmcid: 4839673
doi: 10.1371/journal.pcbi.1004873
Parilla M, Alikhan M, Al-Kawaaz M, Patil S, Kadri S, Ritterhouse LL, et al. Genetic underpinnings of renal cell carcinoma with leiomyomatous stroma. Am J Surg Pathol. 2019;43:1135–44.
pubmed: 30986793
doi: 10.1097/PAS.0000000000001255
Benayed R, Offin M, Mullaney K, Sukhadia P, Rios K, Desmeules P, et al. SvABA: genome-wide detection of structural variants and indels by local assembly. Genome Res. 2018;28:581–91.
doi: 10.1101/gr.221028.117
Benayed R, Offin M, Mullaney K, Sukhadia P, Rios K, Desmeules P, et al. High yield of RNA sequencing for targetable kinase fusions in lung adenocarcinomas with no mitogenic driver alteration detected by DNA sequencing and low tumor mutation burden. Clin Cancer Res. 2019;25:4712–22.
pubmed: 31028088
pmcid: 6679790
doi: 10.1158/1078-0432.CCR-19-0225
de Jesus LE, Fulgencio C, Leve T, Dekermacher S. Thyroid-like follicular carcinoma of the kidney presenting on a 10 year-old prepubertal girl. Int Braz J Urol. 2019;45:834–42.
pubmed: 31063281
pmcid: 6837619
doi: 10.1590/s1677-5538.ibju.2018.0471
Sterlacci W, Verdorfer I, Gabriel M, Mikuz G. Thyroid follicular carcinoma-like renal tumor: a case report with morphologic, immunophenotypic, cytogenetic, and scintigraphic studies. Virchows Arch. 2008;452:91–5.
pubmed: 17704942
doi: 10.1007/s00428-008-0600-2
Dhillon J, Tannir NM, Matin SF, Tamboli P, Czerniak BA, Guo CC. Thyroid-like follicular carcinoma of the kidney with metastases to the lungs and retroperitoneal lymph nodes. Hum Pathol. 2011;42:146–50.
pubmed: 20971497
doi: 10.1016/j.humpath.2010.01.026
Dong L, Huang J, Huang L, Shi O, Liu Q, Chen H, et al. Thyroid-like follicular carcinoma of the kidney in a patient with skull and meningeal metastasis: a unique case report and review of the literature. Medicine (Baltim). 2016;95:e3314.
doi: 10.1097/MD.0000000000003314
Jenkins TM, Rosenbaum J, Zhang PJ, Schwartz LE, Nayak A, Cooper K, et al. Thyroid-like follicular carcinoma of the kidney with extensive sarcomatoid differentiation: a case report and review of the literature. Int J Surg Pathol. 2019;27:678–83.
pubmed: 31032708
doi: 10.1177/1066896919845490
Chen X, Dou FX, Cheng XB, Guo AT, Shi HY. [Clinicopathologic characteristics of thyroid-like follicular carcinoma of the kidney: an analysis of five cases and review of literature]. Zhonghua Bing Li Xue Za Zhi. 2016;45:687–91.
pubmed: 27760609
Herlitz L, Hes O, Michal M, Tretiakova M, Reyes-Mugica M, Nguyen JK, et al. “Atrophic kidney”-like lesion: clinicopathologic series of 8 cases supporting a benign entity distinct from thyroid-like follicular carcinoma. Am J Surg Pathol. 2018;42:1585–95.
pubmed: 30285996
doi: 10.1097/PAS.0000000000001157
Mehra R, Smith SC, Divatia M, Amin MB. Emerging entities in renal neoplasia. Surg Pathol Clin. 2015;8:623–56.
pubmed: 26612218
doi: 10.1016/j.path.2015.08.004
Fanelli GN, Fassan M, Dal Moro F, Soligo M, Munari G, Zattoni F, et al. Thyroid-like follicular carcinoma of the kidney: the mutational profiling reveals a BRAF wild type status. Pathol Res Pr. 2019;215:152532.
doi: 10.1016/j.prp.2019.152532
Nikiforova MN, Lynch RA, Biddinger PW, Alexander EK, Dorn GW 2nd, Tallini G, et al. RAS point mutations and PAX8-PPAR gamma rearrangement in thyroid tumors: evidence for distinct molecular pathways in thyroid follicular carcinoma. J Clin Endocrinol Metab. 2003;88:2318–26.
pubmed: 12727991
doi: 10.1210/jc.2002-021907
Alaghehbandan R, Michal M, Kuroda N, Hes O. Thyroid-like follicular carcinoma of the kidney: an emerging renal neoplasm with curiously misplaced histologic features. A case report. Int J Surg Pathol. 2017;25:379–80.
pubmed: 28381154
doi: 10.1177/1066896917696748
Muscara MJ, Simper NB, Gandia E. Thyroid-like follicular carcinoma of the kidney. Int J Surg Pathol. 2017;25:73–7.
pubmed: 27474044
doi: 10.1177/1066896916662153
Delahunt B, Eble JN. Papillary renal cell carcinoma: a clinicopathologic and immunohistochemical study of 105 tumors. Mod Pathol. 1997;10:537–44.
pubmed: 9195569
Tosi AL, de Biase D, Leonardi E, Eusebi V. Thyroid-like metastases to the scalp from a papillary renal cell carcinoma: a case report. Tumori. 2012;98:79e–81e.
pubmed: 22825524
doi: 10.1177/030089161209800324
Delahunt B, Eble JN, McCredie MR, Bethwaite PB, Stewart JH, Bilous AM. Morphologic typing of papillary renal cell carcinoma: comparison of growth kinetics and patient survival in 66 cases. Hum Pathol. 2001;32:590–5.
pubmed: 11431713
doi: 10.1053/hupa.2001.24984
Ricketts CJ, De Cubas AA, Fan H, Smith CC, Lang M, Reznik E, et al. The Cancer Genome Atlas comprehensive molecular characterization of renal cell carcinoma. Cell Rep. 2018;23:3698.
pubmed: 29925010
doi: 10.1016/j.celrep.2018.06.032
Quddus MB, Pratt N, Nabi G. Chromosomal aberrations in renal cell carcinoma: an overview with implications for clinical practice. Urol Ann. 2019;11:6–14.
pubmed: 30787564
pmcid: 6362797
doi: 10.4103/UA.UA_32_18
Al-Obaidy KI, Eble JN, Nassiri M, Cheng L, Eldomery MK, Williamson SR, et al. Recurrent KRAS mutations in papillary renal neoplasm with reverse polarity. Mod Pathol. 2020;33:1157–64.
pubmed: 31534204
doi: 10.1038/s41379-019-0362-1
Speicher MR, Schoell B, du Manoir S, Schrock E, Ried T, Cremer T, et al. Specific loss of chromosomes 1, 2, 6, 10, 13, 17, and 21 in chromophobe renal cell carcinomas revealed by comparative genomic hybridization. Am J Pathol. 1994;145:356–64.
pubmed: 7519827
pmcid: 1887405
Alessandrini L, Fassan M, Gardiman MP, Guttilla A, Zattoni F, Galletti TP, et al. Thyroid-like follicular carcinoma of the kidney: report of two cases with detailed immunohistochemical profile and literature review. Virchows Arch. 2012;461:345–50.
pubmed: 22898790
doi: 10.1007/s00428-012-1298-8
Chougule A, Bal A, Das A, Nayak B. Thyroid-like follicular renal cell carcinoma: an emerging morphological variant. Pathology. 2014;46:657–60.
pubmed: 25393263
doi: 10.1097/PAT.0000000000000176
Wu WW, Chu JT, Nael A, Rezk SA, Romansky SG, Shane L. Thyroid-like follicular carcinoma of the kidney in a young patient with history of pediatric acute lymphoblastic leukemia. Case Rep. Pathol. 2014;2014:313974.
pubmed: 25133003
pmcid: 4123569
Jung SJ, Chung JI, Park SH, Ayala AG, Ro JY. Thyroid follicular carcinoma-like tumor of kidney: a case report with morphologic, immunohistochemical, and genetic analysis. Am J Surg Pathol. 2006;30:411–5.
pubmed: 16538064
doi: 10.1097/01.pas.0000194745.10670.dd
Dawane R, Grindstaff A, Parwani AV, Brock T, White WM, Nodit L. Thyroid-like follicular carcinoma of the kidney: one case report and review of the literature. Am J Clin Pathol. 2015;144:796–804.
pubmed: 26486745
doi: 10.1309/AJCP6P0STAAHOTTG
Le Loarer F, Szuhai K, Tirode F. Round cell sarcoma with EWSR1-non ETS fusions. In: Antonescu CR, Bovee J, Bridge JA, Cunha IW, Dei Tos AP, Flanagan A, et al., editors. WHO classification of tumours of soft tissue and bone, 5th edition. Lyon, France: IARC Press; 2020. p. 326–9.
Qaddoumi I, Orisme W, Wen J, Santiago T, Gupta K, Dalton JD, et al. Genetic alterations in uncommon low-grade neuroepithelial tumors: BRAF, FGFR1, and MYB mutations occur at high frequency and align with morphology. Acta Neuropathol. 2016;131:833–45.
pubmed: 26810070
pmcid: 4866893
doi: 10.1007/s00401-016-1539-z
Johnson A, Severson E, Gay L, Vergilio JA, Elvin J, Suh J, et al. Comprehensive genomic profiling of 282 pediatric low- and high-grade gliomas reveals genomic drivers, tumor mutational burden, and hypermutation signatures. Oncologist. 2017;22:1478–90.
pubmed: 28912153
pmcid: 5728033
doi: 10.1634/theoncologist.2017-0242
Alvarez-Breckenridge C, Miller JJ, Nayyar N, Gill CM, Kaneb A, D’Andrea M, et al. Clinical and radiographic response following targeting of BCAN-NTRK1 fusion in glioneuronal tumor. NPJ Precis Oncol. 2017;1:5.
pubmed: 29872694
pmcid: 5871889
doi: 10.1038/s41698-017-0009-y
Siegfried A, Rousseau A, Maurage CA, Pericart S, Nicaise Y, Escudie F, et al. EWSR1-PATZ1 gene fusion may define a new glioneuronal tumor entity. Brain Pathol. 2019;29:53–62.
pubmed: 29679497
doi: 10.1111/bpa.12619
ridge JA, Sumegi J, Druta M, Bui MM, Henderson-Jackson E, Linos K, et al. Clinical, pathological, and genomic features of EWSR1-PATZ1 fusion sarcoma. Mod Pathol. 2019;32:1593–604.
doi: 10.1038/s41379-019-0301-1
Watson S, Perrin V, Guillemot D, Reynaud S, Coindre JM, Karanian M, et al. Transcriptomic definition of molecular subgroups of small round cell sarcomas. J Pathol. 2018;245:29–40.
pubmed: 29431183
doi: 10.1002/path.5053
Cantile M, Marra L, Franco R, Ascierto P, Liguori G, De Chiara A, et al. Molecular detection and targeting of EWSR1 fusion transcripts in soft tissue tumors. Med Oncol. 2013;30:412.
pubmed: 23329308
pmcid: 3586390
doi: 10.1007/s12032-012-0412-8
Fedele M, Crescenzi E, Cerchia L. The POZ/BTB and AT-hook-containing Zinc finger 1 (PATZ1) transcription regulator: physiological functions and disease involvement. Int J Mol Sci. 2017;18:2524.
Zhu B, Poeta ML, Costantini M, Zhang T, Shi J, Sentinelli S, et al. The genomic and epigenomic evolutionary history of papillary renal cell carcinomas. Nat Commun. 2020;11:3096.
pubmed: 32555180
pmcid: 7303129
doi: 10.1038/s41467-020-16546-5
Argani P, Lewin JR, Edmonds P, Netto GJ, Prieto-Granada C, Zhang L, et al. Primary renal sclerosing epithelioid fibrosarcoma: report of 2 cases with EWSR1-CREB3L1 gene fusion. Am J Surg Pathol. 2015;39:365–73.
pubmed: 25353281
pmcid: 4326586
doi: 10.1097/PAS.0000000000000338
Ertoy Baydar D, Kosemehmetoglu K, Aydin O, Bridge JA, Buyukeren B, Aki FT. Primary sclerosing epithelioid fibrosarcoma of kidney with variant histomorphologic features: report of 2 cases and review of the literature. Diagn Pathol. 2015;10:186.
pubmed: 26449317
pmcid: 4599747
doi: 10.1186/s13000-015-0420-z