Mesenchymal, non-meningothelial tumors involving the CNS

2024-12-03   Paola Dal Cin, PhD , Scott Ryall, PhD 

1.Brigham and Women's Hospital , Harvard Medical School, Boston , MA (USA)
2.Brigham and Women's Hospital, Harvard Medical School, Boston , MA (USA)

Keywords
Primary intracranial sarcomas, DICER1-mutant,FET::CREB fusion, CIC-rearranged sarcoma

Classification

Definition

The histological features of non-meningothelial tumors involving the central nervous system (CNS) are governed by their bone and soft tissue counterparts as described in WHO 2020 Soft Tissue and Bone Tumours. 1 Collectively, primary mesenchymal CNS tumors are very rare, can arise in patients of any age and are more commonly noted in supratentorial, as opposed to spinal or infratentorial, regions. The WHO 2021 Central Nervous System Tumours focusses on entities with unique histological or molecular features and either occur uniquely, or more frequently, in the CNS. 2 They were all sarcomas grouped in "tumors of uncertain differentiation,” due to their often-ambiguous histological features and immunophenotype e.g., i) intracranial mesenchymal tumor, FET::CREB fusion positive, ii) CIC rearranged sarcoma, iii) Primary intracranial sarcoma, DICER1-mutant, and iv) Ewing sarcoma. Given their rarity and morphologic ambiguity, molecular characterization has become indispensable for their accurate diagnosis and future prognostication. 3 

Mesenchymal tumors relatively common in CNS
Primary intracranial sarcomas in CNS Genetic marker(s)
Primary intracranial sarcoma, DICER1-mutantDICER1-mutant primary intracranial sarcoma are defined by biallelic disruption of the DICER1 gene, typically manifesting as a loss of function variant on one alleles and a missense mutation in the Rnase IIIb domain on the other. 4,5 Other biallelic inactivation combination, including loss of heterozygosity have also been described. The majority of these tumors also harbor inactivating TP53 mutations, mutations or deletions in ATRX, and up-regulation of the RAS/MAPK singaling pathway via mutations in KRAS, NF1, or PDGFRA. 5-7 These tumors do not harbor genetic events associated with fibrous tumors (NAB2::STAT6), alveolar rhabdomyosarcoma (PAX3::FOXO1 and/or PAX7::FOXO1), nor meningioma (NF2, SMARCB1, etc.) DNA methylation analysis reliable segregates DICER1-mutant primary intracranial sarcoma from other CNS tumors. 5,6
FET::CREB family fusion–positiveThis provisional tumor classification is characterized by fusions involving an FET RNA-binding protein family gene (typically EWSR1 but can rarely include FUS) with a member of the CREB family of transcription factors e.g., CREB1, ATF1, or CREM). 8-13 Interestingly, isolated tumors harboring FET::CREB fusions have also been identified with an extracranial presentation, suggesting the need to fully elucidate the spectrum of tumors driven by these rearrangements. 14,15
CIC-rearranged sarcomaCIC-rearranged sarcoma are defined by an oncgenic fusion of the CIC transcriptional repressor with a variety of partners including DUX4, FOXO4, LEUTX, NUTM1, and NUTM2A of which DUX4 is the most common overall and NUTM1 the most common in CNS tumors. 16-20 These tumors primarily affect adolescents and young adults, but are not exclusive to these demograhpics. 21,22 Methylation analysis readily identifies CIC-rearranged sarcoma in the CNS. 23
Emerging entities Dural angioleiomyomas is haracterized by a distinct DNA methylation pattern sand GJA4 p.Gly41Cys mutation. 24
Spindle cell neoplasms with NTRK‑rearrangements and distinct methylation class. 25,26
Sarcoma, MPNST-like , single case of with intracranial mesenchymal tumor with COX14::PTEN rearrangement between chromosome bands 12q13.12 and 10q23.31 . In addition, several copy number variations were observed including gains e.g. 1q, 7, 8 and 21 losses 1p, 10, 14, and 16q, and homozygosis of CDKN2A/ CDKN2B and PTEN. 27

Article Bibliography

Reference NumberPubmed IDLast YearTitleAuthors
1331796142021The 2020 WHO Classification of Soft Tissue Tumours: news and perspectives.Sbaraglia M et al
2341850762021The 2021 WHO Classification of Tumors of the Central Nervous System: a summary.Louis DN et al
3367377902023Mesenchymal non-meningothelial tumors of the central nervous system: a literature review and diagnostic update of novelties and emerging entities.Tauziède-Espariat A et al
4251763342014DICER1: mutations, microRNAs and mechanisms.Foulkes WD et al
5298819932018Primary intracranial spindle cell sarcoma with rhabdomyosarcoma-like features share a highly distinct methylation profile and DICER1 mutations.Koelsche C et al
6306496062019Primary intracranial sarcomas with DICER1 mutation often contain prominent eosinophilic cytoplasmic globules and can occur in the setting of neurofibromatosis type 1.Lee JC et al
7322913952020DICER1-associated central nervous system sarcoma in children: comprehensive clinicopathologic and genetic analysis of a newly described rare tumor.Kamihara J et al
8280096022017EWSR1 Fusions With CREB Family Transcription Factors Define a Novel Myxoid Mesenchymal Tumor With Predilection for Intracranial Location.Kao YC et al
9282813182018Intracranial myxoid mesenchymal tumors with EWSR1-CREB family gene fusions: myxoid variant of angiomatoid fibrous histiocytoma or novel entity?Bale TA et al
10291434322018Primary myxoid mesenchymal tumour with intracranial location: report of a case with a EWSR1-ATF1 fusion.Sciot R et al
11297881952018ESWR1-CREM Fusion in an Intracranial Myxoid Angiomatoid Fibrous Histiocytoma-Like Tumor: A Case Report and Literature Review.Gareton A et al
12299243412018Molecular and Clinicopathologic Heterogeneity of Intracranial Tumors Mimicking Extraskeletal Myxoid Chondrosarcoma.Velz J et al
13308312992019Intracranial Angiomatoid Fibrous Histiocytoma with EWSR1-CREB Family Fusions: A Report of 2 Pediatric Cases.Konstantinidis A et al
14331414882021Intracranial mesenchymal tumor with FET-CREB fusion-A unifying diagnosis for the spectrum of intracranial myxoid mesenchymal tumors and angiomatoid fibrous histiocytoma-like neoplasms.Sloan EA et al
15361072772023An extracranial CNS presentation of the emerging "intracranial" mesenchymal tumor, FET: CREB-fusion positive.Tauziède-Espariat A et al
16220724392012High prevalence of CIC fusion with double-homeobox (DUX4) transcription factors in EWSR1-negative undifferentiated small blue round cell sarcomas.Italiano A et al
17250071472014A novel CIC-FOXO4 gene fusion in undifferentiated small round cell sarcoma: a genetically distinct variant of Ewing-like sarcoma.Sugita S et al
18267358592016Recurrent CIC Gene Abnormalities in Angiosarcomas: A Molecular Study of 120 Cases With Concurrent Investigation of PLCG1, KDR, MYC, and FLT4 Gene Alterations.Huang SC et al
19281887542017NUTM2A-CIC fusion small round cell sarcoma: a genetically distinct variant of CIC-rearranged sarcoma.Sugita S et al
20304072122019Clinicopathologic Features of CIC-NUTM1 Sarcomas, a New Molecular Variant of the Family of CIC-Fused Sarcomas.Le Loarer F et al
21283463262017Sarcomas With CIC-rearrangements Are a Distinct Pathologic Entity With Aggressive Outcome: A Clinicopathologic and Molecular Study of 115 Cases.Antonescu CR et al
22326508332020Molecular identification of CNS NB-FOXR2, CNS EFT-CIC, CNS HGNET-MN1 and CNS HGNET-BCOR pediatric brain tumors using tumor-specific signature genes.Łastowska M et al
23295396392018DNA methylation-based classification of central nervous system tumours.Capper D et al
24356420472022The dural angioleiomyoma harbors frequent GJA4 mutation and a distinct DNA methylation profile.Tauziède-Espariat A et al
25359000132023A rare case of spindle cell neoplasm with NTRK-fusion in central nervous system.Gong H et al
26364131002023NTRK-rearranged spindle cell neoplasms are ubiquitous tumours of myofibroblastic lineage with a distinct methylation class.Tauziède-Espariat A et al
27373122122023Intracranial mesenchymal tumor with (novel) COX14::PTEN rearrangement.d'Amati A et al

Citation

Paola Dal Cin, PhD ; Scott Ryall, PhD

Mesenchymal, non-meningothelial tumors involving the CNS

Atlas Genet Cytogenet Oncol Haematol. 2024-12-03

Online version: http://atlasgeneticsoncology.org/solid-tumor/209296/mesenchymal-non-meningothelial-tumors-involving-the-cns