Novel and unusual USP6 fusion partners in aneurysmal bone cyst and their role in pathogenesis and histopathological evaluation of this disease

. 2025 May 25 ; 78 (6) : 399-403. [epub] 20250525

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38429095

AIMS: The purpose of this study is to report novel and unusual USP6 fusion partners in aneurysmal bone cysts (ABCs). These findings may be useful in routine diagnostics as well as in studying the biology of USP6-related disorders. METHODS: A cohort of seven patients diagnosed with ABC examined between 2014 and 2023 at Motol University Hospital in Prague was included into this retrospective non-randomised study. All cases were analysed using histopathological evaluation, immunohistochemistry and Anchored multiplex RNA methods. Demographic characteristics and clinical data were also analysed. RESULTS: We identified two novel (ZFX and IP6K2), three unusual (MEF2A, EIF1 and COL1A2) and two common (CDH11) fusion partners with USP6 gene among all seven cases of ABC. CONCLUSIONS: Cases in our study were diagnosed as ABCs due to characteristic clinical and morphological presentation. However, not all cases are as self-evident, and molecular testing is necessary. The identification of these gene alterations can be useful in distinction between true ABC and ABC-like changes among many benign and malignant bone tumours.

Zobrazit více v PubMed

Jager L, Johnson DN, Sukhanova M, et al. Diagnosis of giant cell-rich bone tumors on core needle biopsy: a practical approach. Pathol Res Pract. 2022;231:153777. doi: 10.1016/j.prp.2022.153777. PubMed DOI

Qian X. Updates in primary bone tumors: current challenges and new opportunities in cytopathology. Surg Pathol Clin. 2018;11:657–68. doi: 10.1016/j.path.2018.06.004. PubMed DOI

Kovacs SK, Manassaporn A, Nielsen GP, et al. Molecular and immunohistochemical testing of bone tumours: review and update. Histopathology. 2023;82:794–811. doi: 10.1111/his.14845. PubMed DOI

Oliveira AM, Perez-Atayde AR, Inwards CY, et al. USP6 and CDH11 oncogenes identify the neoplastic cell in primary aneurysmal bone cysts and are absent in so-called secondary aneurysmal bone cysts. Am J Pathol. 2004;165:1773–80. doi: 10.1016/S0002-9440(10)63432-3. PubMed DOI PMC

Guseva NV, Jaber O, Tanas MR, et al. 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. 2017;56:266–77. doi: 10.1002/gcc.22432. PubMed DOI

Blackburn PR, Davila JI, Jackson RA, et al. RNA sequencing identifies a novel USP9X-Usp6 promoter swap gene fusion in a primary aneurysmal bone cyst. Genes Chromosomes Cancer. 2019;58:589–94. doi: 10.1002/gcc.22742. PubMed DOI

Šekoranja D, Zupan A, Mavčič B, et al. Novel ASAP1-USP6, FAT1-USP6, SAR1A-USP6, and TNC-USP6 fusions in primary aneurysmal bone cyst. Genes Chromosomes Cancer. 2020;59:357–65. doi: 10.1002/gcc.22836. PubMed DOI

Oliveira AM, Perez-Atayde AR, Dal Cin P, et al. Aneurysmal bone Cyst variant Translocations Upregulate Usp6 transcription by promoter swapping with the Znf9, Col1A1, Trap150, and OMD genes. Oncogene. 2005;24:3419–26. doi: 10.1038/sj.onc.1208506. PubMed DOI

Hiemcke-Jiwa LS, van Gorp JM, Fisher C, et al. USP6-associated neoplasms: a rapidly expanding family of lesions. Int J Surg Pathol. 2020;28:816–25. doi: 10.1177/1066896920938878. PubMed DOI

Balko J, Stanek M, Krskova L, et al. Unusual fusion gene rearrangements in patients with nodular fasciitis: a study of rare and novel USP6 fusion partners with a review of the literature. J Clin Pathol. 2024;77:411–6. doi: 10.1136/jcp-2023-208768. PubMed DOI PMC

Legrand M, Jourdan M-L, de Pinieux G. Histopathogenesis of bone- and soft-tissue tumor spectrum with USP6 gene rearrangement: multiple partners involved in the tissue repair process. Histol Histopathol. 2023;38:247–60. doi: 10.14670/HH-18-532. PubMed DOI

Oliveira AM, Chou MM. Usp6-induced neoplasms: the biologic spectrum of aneurysmal bone cyst and nodular Fasciitis. Hum Pathol. 2014;45:1–11. doi: 10.1016/j.humpath.2013.03.005. PubMed DOI

Borni M, Kolsi F, Cherif I, et al. Spontaneous rapid regression of a juvenile primary aneurysmal bone cyst of the skull: a case report and literature review. Radiol Case Rep. 2022;17:1634–9. doi: 10.1016/j.radcr.2022.02.037. PubMed DOI PMC

McQueen MM, Chalmers J, Smith GD. Spontaneous healing of aneurysmal bone cysts. A report of two cases. J Bone Joint Surg Br. 1985;67:310–2. doi: 10.1302/0301-620X.67B2.3980546. PubMed DOI

Erickson-Johnson MR, Chou MM, Evers BR, et al. Nodular fasciitis: a novel model of transient neoplasia induced by Myh9-USP6 gene fusion. Lab Invest. 2011;91:1427–33. doi: 10.1038/labinvest.2011.118. PubMed DOI

Sağlik Y, Kapicioğlu MI, Güzel B. Spontaneous regression of aneurysmal bone cyst. A case report. Arch Orthop Trauma Surg. 1993;112:203–4. doi: 10.1007/BF00662291. PubMed DOI

Liu Y, Lei P, Row S, et al. Cadherin-11 binds to PDGFRβ and enhances cell proliferation and tissue regeneration via the PDGFR-AKT signaling axis. FASEB J. 2020;34:3792–804. doi: 10.1096/fj.201902613R. PubMed DOI

Passanha FR, Divinagracia ML, LaPointe VLS. Cadherin-11 regulates cell proliferation via the PDGFRβ-Erk1/2 signaling pathway in human mesenchymal stem cells. Stem Cells. 2022;40:165–74. doi: 10.1093/stmcls/sxab019. PubMed DOI

Chavula T, To S, Agarwal SK. Cadherin-11 and its role in tissue fibrosis. Cells Tissues Organs. 2023;212:293–303. doi: 10.1159/000525359. PubMed DOI

Galan-Caridad JM, Harel S, Arenzana TL, et al. Zfx controls the self-renewal of embryonic and hematopoietic stem cells. Cell. 2007;129:345–57. doi: 10.1016/j.cell.2007.03.014. PubMed DOI PMC

Arenzana TL, Smith-Raska MR, Reizis B. Transcription factor zfx controls BCR-induced proliferation and survival of B lymphocytes. Blood. 2009;113:5857–67. doi: 10.1182/blood-2008-11-188888. PubMed DOI PMC

Feng X, Zhou S, Cai W, et al. The miR-93-3p/Zfp36L1/ZFX axis regulates keratinocyte proliferation and migration during skin wound healing. Mol Ther Nucleic Acids. 2021;23:450–63. doi: 10.1016/j.omtn.2020.11.017. PubMed DOI PMC

Wilson MSC, Livermore TM, Saiardi A. Inositol pyrophosphates: between signalling and metabolism. Biochem J. 2013;452:369–79. doi: 10.1042/BJ20130118. PubMed DOI

Jadav RS, Chanduri MVL, Sengupta S, et al. Inositol pyrophosphate synthesis by inositol hexakisphosphate kinase 1 is required for homologous recombination repair. J Biol Chem. 2013;288:3312–21. doi: 10.1074/jbc.M112.396556. PubMed DOI PMC

Liu B, Ou W-C, Fang L, et al. Myocyte enhancer factor 2A plays a central role in the regulatory networks of cellular physiopathology. Aging Dis. 2023;14:331–49. doi: 10.14336/AD.2022.0825. PubMed DOI PMC

Gao Y, Liu Y, Zheng D, et al. Hdac5-mediated Smad7 silencing through Mef2A is critical for fibroblast activation and hypertrophic scar formation. Int J Biol Sci. 2022;18:5724–39. doi: 10.7150/ijbs.76140. PubMed DOI PMC

Kim EY, Hussain A, Khachemoune A. Evidence-based management of Keloids and hypertrophic scars in dermatology. Arch Dermatol Res. 2023;315:1487–95. doi: 10.1007/s00403-022-02509-x. PubMed DOI

Mitchell SF, Lorsch JR. Should I stay or should I go? Eukaryotic translation initiation factors 1 and 1A control start codon recognition. J Biol Chem. 2008;283:27345–9. doi: 10.1074/jbc.R800031200. PubMed DOI PMC

Šekoranja D, Zupan A, Mavčič B, et al. Novel ASAP1-USP6, FAT1-USP6, SAR1A-USP6, and TNC-USP6 fusions in primary aneurysmal bone cyst. Genes Chromosomes Cancer. 2020;59:357–65. doi: 10.1002/gcc.22836. PubMed DOI

Šekoranja D, Boštjančič E, Salapura V, et al. Primary aneurysmal bone cyst with a novel SPARC-Usp6 translocation identified by next-generation sequencing. Cancer Genet. 2018;228–229:12–6. doi: 10.1016/j.cancergen.2018.07.001. PubMed DOI

Büttner C, Skupin A, Rieber EP. Transcriptional activation of the type I collagen genes Col1A1 and Col1A2 in fibroblasts by interleukin-4: analysis of the functional collagen promoter sequences. J Cell Physiol. 2004;198:248–58. doi: 10.1002/jcp.10395. PubMed DOI

Yoshida H, Miyachi M, Ouchi K, et al. Identification of Col3A1 and Rab2A as novel translocation partner genes of Plag1 in lipoblastoma. Genes Chromosomes Cancer. 2014;53:606–11. doi: 10.1002/gcc.22170. PubMed DOI

Koblizek M, Golas W, Krskova L, et al. Primary cardiac lipoblastoma of the right atrium. Cardiovasc Pathol. 2023;65:107542. doi: 10.1016/j.carpath.2023.107542. PubMed DOI

Wang J-C, Li W-S, Kao Y-C, et al. Clinicopathological and molecular characterisation of USP6-rearranged soft tissue neoplasms: the evidence of genetic relatedness indicates an expanding family with variable bone-forming capacity. Histopathology. 2021;78:676–89. doi: 10.1111/his.14268. PubMed DOI

Opalenik SR, Davidson JM. Fibroblast differentiation of bone marrow-derived cells during wound repair. FASEB J. 2005;19:1561–3. doi: 10.1096/fj.04-2978fje. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...