Novel partners of USP6 gene in a spectrum of bone and soft tissue lesions.
Adolescent
Adult
Bone Cysts, Aneurysmal
/ genetics
Child
Databases, Factual
Fasciitis
/ genetics
Female
France
Gene Fusion
Gene Rearrangement
Genetic Predisposition to Disease
Humans
Male
Middle Aged
Myositis Ossificans
/ genetics
Phenotype
Retrospective Studies
Ubiquitin Thiolesterase
/ genetics
Young Adult
Aneurysmal bone cyst
Gene fusion
Nodular fasciitis
USP6
Journal
Virchows Archiv : an international journal of pathology
ISSN: 1432-2307
Titre abrégé: Virchows Arch
Pays: Germany
ID NLM: 9423843
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
15
09
2020
accepted:
28
01
2021
revised:
10
01
2021
pubmed:
10
2
2021
medline:
3
8
2021
entrez:
9
2
2021
Statut:
ppublish
Résumé
Nodular fasciitis, primary aneurysmal bone cyst, myositis ossificans, and their related lesions are benign tumors that share common histological features and a chromosomal rearrangement involving the ubiquitin-specific peptidase 6 (USP6) gene. The identification of an increasing number of new partners implicated in USP6 rearrangements demonstrates a complex tumorogenesis of this tumor spectrum. In this study on a series of 77 tumors (28 nodular fasciitis, 42 aneurysmal bone cysts, and 7 myositis ossificans) from the database of the French Sarcoma Group, we describe 7 new partners of the USP6 gene. For this purpose, rearrangements were first researched by multiplexed RT-qPCRs in the entire population. A targeted RNA sequencing was then used on samples selected according to a high USP6-transcription level expression estimated by RT-qPCR. Thanks to this multistep approach, besides the common USP6 fusions observed, we detected novel USP6 partners: PDLIM7 and MYL12A in nodular fasciitis and TPM4, DDX17, GTF2I, KLF3, and MEF2A in aneurysmal bone cysts. In order to try to bring to light the role played by the recently identified USP6 partners in this lesional spectrum, their functions are discussed. Taking into account that a traumatic participation has long been mentioned in the histogenesis of most of these lesions and because of their morphological resemblance to organizing granulation reparative tissue or callus, a focus is placed on their relationship with tissue remodeling and, to a lesser extent, with bone metabolism.
Identifiants
pubmed: 33558945
doi: 10.1007/s00428-021-03047-z
pii: 10.1007/s00428-021-03047-z
doi:
Substances chimiques
USP6 protein, human
EC 3.4.19.12
Ubiquitin Thiolesterase
EC 3.4.19.12
Types de publication
Journal Article
Multicenter Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
147-156Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature.
Références
Oliveira AM, Wang J, Wang WL (2020) Nodular fasciitis. In: Lokuhetty D, White VA, Cree IA (eds) World Health Organization Classification of Tumours of Soft Tissue and Bone, 5th edn. International Agency for Research on Cancer, Lyon, pp 49–50
Oliveira AM, Rosenberg AE (2020) Myositis ossificans and fibro-osseous pseudotumour of digits. In: Lokuhetty D, White VA, Cree IA (eds) WHO Classification of Tumours of Soft Tissue and Bone, 5th edn. International Agency for Research on Cancer, Lyon, pp 53–54
Agaram NP, Bredella MA (2020) Aneurysmal bone cyst. In: Lokuhetty D, White VA, Cree IA (eds) World Health Organization Classification of Tumours of Soft Tissue and Bone, 5th edn. International Agency for Research on Cancer, Lyon, pp 437–439
Panoutsakopoulos G, Pandis N, Kyriazoglou I, Gustafson P, Mertens F, Mandahl N (1999) Recurrent t(16;17)(q22;p13) in aneurysmal bone cysts. Genes Chromosomes Cancer 26:265–266
pubmed: 10502326
doi: 10.1002/(SICI)1098-2264(199911)26:3<265::AID-GCC12>3.0.CO;2-#
pmcid: 10502326
Oliveira AM, Hsi BL, Weremowicz S, Rosenberg AE, Dal Cin P, Joseph N et al (2004) USP6 (Tre2) fusion oncogenes in aneurysmal bone cyst. Cancer Res 15(64):1920–1923
doi: 10.1158/0008-5472.CAN-03-2827
Oliveira AM, Perez-Atayde AR, Inwards CY, Medeiros F, Derr V, Hsi BL, Gebhardt MC, Rosenberg AE, Fletcher JA (2004) USP6 and CDH11 oncogenes identify the neoplastic cell in primary aneurysmal bone cysts and are absent in so-called secondary aneurismal bone cysts. Am J Pathol 165:1773–1780
pubmed: 15509545
pmcid: 3278819
doi: 10.1016/S0002-9440(10)63432-3
Oliveira AM, Perez-Atayde AR, Dal Cin P, Gebhardt MC, Chen CJ, Neff JR, Demetri GD, Rosenberg AE, Bridge JA, Fletcher JA (2005) Aneurysmal bone cyst variant translocations upregulate USP6 transcription by promoter swapping with the ZNF9, COL1A1, TRAP150, and OMD genes. Oncogene 24:3419–3426
pubmed: 15735689
doi: 10.1038/sj.onc.1208506
Guseva NV, Jaber O, Tanas MR, Stence AA, Sompallae R, Schade J, Fillman AN, Miller BJ, Bossler AD, Ma D (2017) Anchored multiplex PCR for targeted next-generation sequencing reveals recurrent and novel USP6 fusions and upregulation of USP6 expression in aneurysmal bone cyst. Genes Chromosomes Cancer 56:266–277
pubmed: 27910166
doi: 10.1002/gcc.22432
Šekoranja D, Boštjančič E, Salapura V, Mavčič B, Pižem J (2018) Primary aneurysmal bone cyst with a novel SPARC-USP6 translocation identified by next-generation sequencing. Cancer Gene Ther 228-229:12–16
doi: 10.1016/j.cancergen.2018.07.001
Blackburn PR, Davila JI, Jackson RA, Fadra N, Atiq MA, Pitel BA, Nair AA, VanDeWalker TJ, Hessler MG, Hovel SK, Wehrs RN, Fritchie KJ, Jenkins RB, Halling KC, Geiersbach KB (2019) RNA sequencing identifies a novel USP9X-USP6 promoter swap gene fusion in a primary aneurysmal bone cyst. Genes Chromosomes Cancer 58:589–594
pubmed: 30767316
doi: 10.1002/gcc.22742
pmcid: 30767316
Šekoranja D, Zupan A, Mavčič B, Martinčič D, Salapura V, Snoj Ž et al (2020) Novel ASAP1-USP6, FAT1-USP6, SAR1A-USP6, and TNC-USP6 fusions in primary aneurysmal bone cyst. Genes Chromosomes Cancer 59:357–365.
pubmed: 32011035
doi: 10.1002/gcc.22836
pmcid: 32011035
Erickson-Johnson MR, Chou MM, Evers BR, Roth CW, Seys AR, Jin L, Ye Y, Lau AW, Wang X, Oliveira AM (2011) Nodular fasciitis: a novel model of transient neoplasia induced by MYH9-USP6 gene fusion. Lab Investig 91:1427–1433
pubmed: 21826056
doi: 10.1038/labinvest.2011.118
pmcid: 21826056
Guo R, Wang X, Chou MM, Asmann Y, Wenger DE, Al-Ibraheemi A et al (2016) PPP6R3-USP6 amplification: novel oncogenic mechanism in malignant nodular fasciitis. Genes Chromosomes Cancer 55:640–649
pubmed: 27113271
doi: 10.1002/gcc.22366
pmcid: 27113271
Patel NR, Chrisinger JSA, Demicco EJ, Sarabia SF, Reuther J, Kumar E et al (2017) USP6 activation in nodular fasciitis by promoter-swapping gene fusions. Mod Pathol 30:1577–1588
pubmed: 28752842
doi: 10.1038/modpathol.2017.78
pmcid: 28752842
Lam SW, Cleton-Jansen AM, Cleven AHG, Ruano D, van Wezel T, Szuhai K, Bovée JVMG (2018) Molecular analysis of gene fusions in bone and soft tissue tumors by anchored multiplex PCR-based targeted next-generation sequencing. J Mol Diagn 20:653–663
pubmed: 30139549
doi: 10.1016/j.jmoldx.2018.05.007
pmcid: 30139549
Lenz J, Michal M, Švajdler M, Ptakova N, Lenz D, Konecna P et al (2019) Novel EIF5A-USP6 gene fusion in nodular fasciitis associated with unusual pathologic features: a report of a case and review of the literature [published online ahead of print, 2019 Dec 26]. Am J Dermatopathol 10:1097
Paulson VA, Stojanov IA, Wasman JK, Restrepo T, Cano S, Plunkitt J, Duraisamy S, Harris MH, Chute DJ, al-Ibraheemi A, Church AJ (2020) Recurrent and novel USP6 fusions in cranial fasciitis identified by targeted RNA. Mod Pathol 33(5):775–780
pubmed: 31827231
doi: 10.1038/s41379-019-0422-6
Flucke U, Bekers EM, Creytens D, van Gorp JM (2018) COL1A1 is a fusion partner of USP6 in myositis ossificans—FISH analysis of six cases. Ann Diagn Pathol 36:61–62
pubmed: 29980413
doi: 10.1016/j.anndiagpath.2018.06.009
Švajdler M, Michal M, Martínek P, Ptáková N, Kinkor Z, Szépe P, Švajdler P, Mezencev R, Michal M (2019) Fibro-osseous pseudotumor of digits and myositis ossificans show consistent COL1A1-USP6 rearrangement: a clinicopathological and genetic study of 27 cases. Hum Pathol 88:39–47
pubmed: 30946936
doi: 10.1016/j.humpath.2019.02.009
Oliveira AM, Chou MM (2014) USP6-induced neoplasms: the biologic spectrum of aneurysmal bone cyst and nodular fasciitis. Hum Pathol 45:1–11
pubmed: 23769422
doi: 10.1016/j.humpath.2013.03.005
Paulding CA, Ruvolo M, Haber DA (2003) The Tre2 (USP6) oncogene is a hominoid-specific gene. Proc Natl Acad Sci U S A 100:2507–2511
pubmed: 12604796
pmcid: 151371
doi: 10.1073/pnas.0437015100
Jacquot C, Szymanska J, Nemana LJ, Steinbach LS, Horvai AE (2015) Soft-tissue aneurysmal bone cyst with translocation t(17;17)(p13;q21) corresponding to COL1A1 and USP6 loci. Skeletal Radiol 44:1695–1699
pubmed: 26142538
doi: 10.1007/s00256-015-2205-6
Bekers EM, Eijkelenboom A, Grünberg K, Roverts RC, de Rooy JWJ, van der Geest ICM, van Gorp JM, Creytens D, Flucke U (2018) Myositis ossificans—another condition with USP6 rearrangement, providing evidence of a relationship with nodular fasciitis and aneurysmal bone cyst. Ann Diagn Pathol 34:56–59
pubmed: 29661729
doi: 10.1016/j.anndiagpath.2018.01.006
Meng Y, He Y, Zhang J, Xie Q, Yang M, Chen Y, Wu Y (2019) Association of GTF2I gene polymorphisms with renal involvement of systemic lupus erythematosus in a Chinese population. Medicine (Baltimore) 98(31):e16716
doi: 10.1097/MD.0000000000016716
Arbajian E, Magnusson L, Mertens F, Domanski HA (2013) Vult von Steyern F, Nord KH. A novel GTF2I/NCOA2 fusion gene emphasizes the role of NCOA2 in soft tissue angiofibroma development. Genes Chromosomes Cancer 52(3):330–331
pubmed: 23225380
doi: 10.1002/gcc.22033
Tomić TT, Olausson J, Wilzén A, Sabel M, Truvé K, Sjögren H, Dósa S, Tisell M, Lannering B, Enlund F, Martinsson T, Åman P, Abel F (2017) A new GTF2I-BRAF fusion mediating MAPK pathway activation in pilocytic astrocytoma. PLoS One 12(4):e0175638
pubmed: 28448514
pmcid: 5407815
doi: 10.1371/journal.pone.0175638
Yan W, Li J, Zhang Y, Yin Y, Cheng Z, Wang J, Hu G, Liu S, Wang Y, Xu Y, Peng H, Zhang G (2019) RNF8 is responsible for ATRA resistance in variant acute promyelocytic leukemia with GTF2I/RARA fusion, and inhibition of the ubiquitin-proteasome pathway contributes to the reversion of ATRA resistance. Cancer Cell Int 19:84
pubmed: 30992691
pmcid: 6449960
doi: 10.1186/s12935-019-0803-4
Panagopoulos I, Brunetti M, Stoltenberg M, Strandabø RAU, Staurseth J, Andersen K, Kostolomov I, Hveem TS, Lorenz S, Nystad TA, Flægstad T, Micci F, Heim S (2019) Novel GTF2I-PDFGRB and IKZF1-TYW1 fusions in pediatric leukemia with normal karyotype. Exp Hematol Oncol 8:12
pubmed: 31161074
pmcid: 6542082
doi: 10.1186/s40164-019-0136-y
Pearson RC, Funnell AP, Crossley M (2011) The mammalian zinc finger transcription factor Krüppel-like factor 3 (KLF3/BKLF). IUBMB Life 63(2):86–93
pubmed: 21360637
Chen X, Gao B, Ponnusamy M, Lin Z, Liu J (2017) MEF2 signaling and human diseases. Oncotarget 8(67):112152–112165
pubmed: 29340119
pmcid: 5762387
doi: 10.18632/oncotarget.22899
Park I, Han C, Jin S, Lee B, Choi H, Kwon JT, Kim D, Kim J, Lifirsu E, Park WJ, Park ZY, Kim DH, Cho C (2011) Myosin regulatory light chains are required to maintain the stability of myosin II and cellular integrity. Biochem J 434(1):171–180
pubmed: 21126233
doi: 10.1042/BJ20101473
pmcid: 21126233
Zheng Q, Zhao Y (2007) The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein-protein interaction. Biol Cell 99(9):489–502
pubmed: 17696879
doi: 10.1042/BC20060126
pmcid: 17696879
Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, Ogryzko V et al (2006) The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 11(4):547–560
pubmed: 17011493
doi: 10.1016/j.devcel.2006.08.003
pmcid: 17011493
Germann S, Gratadou L, Zonta E, Dardenne E, Gaudineau B, Fougère M, Samaan S, Dutertre M, Jauliac S, Auboeuf D (2012) Dual role of the ddx5/ddx17 RNA helicases in the control of the pro-migratory NFAT5 transcription factor. Oncogene. 31(42):4536–4549
pubmed: 22266867
doi: 10.1038/onc.2011.618
pmcid: 22266867
Lawrence B, Perez-Atayde A, Hibbard MK, Rubin BP, Dal Cin P, Pinkus JL, Pinkus GS, Xiao S, Yi ES, Fletcher CDM, Fletcher JA (2000) TPM3-ALK and TPM4-ALK oncogenes in inflammatory myofibroblastic tumors. Am J Pathol 157(2):377–384
pubmed: 10934142
pmcid: 10934142
doi: 10.1016/S0002-9440(10)64550-6
Warren M, Xu D, Li X (2017) Gene fusions PAFAH1B1-USP6 and RUNX2-USP6 in aneurysmal bone cysts identified by next generation sequencing. Cancer Gene Ther 212–213:13–18
doi: 10.1016/j.cancergen.2017.03.007
McMichael BK, Kotadiya P, Singh T, Holliday LS, Lee BS (2006) Tropomyosin isoforms localize to distinct microfilament populations in osteoclasts. Bone 39:694–705
pubmed: 16765662
doi: 10.1016/j.bone.2006.04.031
pmcid: 16765662
Pan H, Li X, Wang J, Zhang K, Yang H, Li Z, Zheng Z, Liu H (2015) LIM mineralization protein-1 enhances bone morphogenetic protein-2-mediated osteogenesis through activation of ERK1/2 MAPK pathway and upregulation of Runx2 transactivity. J Bone Miner Res 30:1523–1535
pubmed: 25677945
doi: 10.1002/jbmr.2481
pmcid: 25677945
Pola E, Gao W, Zhou Y, Pola R, Lattanzi W, Sfeir C, Gambotto A, Robbins PD (2004) Efficient bone formation by gene transfer of human LIM mineralization protein-3. Gene Ther 11:683–693
pubmed: 14724674
doi: 10.1038/sj.gt.3302207
Håkelien AM, Bryne JC, Harstad KG, Lorenz S, Paulsen J, Sun J, Mikkelsen TS, Myklebost O, Meza-Zepeda LA (2014) The regulatory landscape of osteogenic differentiation. Stem Cells 32:2780–2793
pubmed: 24898411
doi: 10.1002/stem.1759
Fuller-Pace FV (1829) The DEAD box proteins DDX5 (p68) and DDX17 (p72): multi-tasking transcriptional regulators. Biochim Biophys Acta 2013:756–763
Ma M, Huang DG, Liang X, Zhang L, Cheng S, Cheng B, Qi X, Li P, du Y, Liu L, Zhao Y, Ding M, Wen Y, Guo X, Zhang F (2019) Integrating transcriptome-wide association study and mRNA expression profiling identifies novel genes associated with bone mineral density. Osteoporos Int 30:1521–1528
pubmed: 30993394
doi: 10.1007/s00198-019-04958-z
Rosset EM, Trombetta-eSilva J, Hepfer G, Yao H, Bradshaw AD (2017) SPARC and the N-propeptide of collagen I influence fibroblast proliferation and collagen assembly in the periodontal ligament. PLoS One 12:e0173209
pubmed: 28245286
pmcid: 5330531
doi: 10.1371/journal.pone.0173209