Emerging mesenchymal tumor types

2024-10-17   David Papke, MD , Paola Dal Cin, PhD 

1.Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA

Keywords
pseudoendocrine sarcoma,nested glomoid neoplasm,NUTM1-rearranged sarcoma

Classification

Definition

Due in part to the increasingly ubiquitous use of sequencing in sarcoma diagnostics, there has been a recent large increase in the number of described new tumor types with novel gene fusions.1,2 Many of these tumor types remain somewhat ill-defined, with limited clinical follow-up data or limited histopathologic description. Here, we tabulate some of the better-defined emerging tumor types, with references to their descriptions.

Emerging entitiesGenetic event(s)
PRRX1-rearranged mesenchymal tumorPRRX1-rearranged mesenchymal tumor, also described as PRRX1-rearranged fibroblastic tumor, is a rare benign tumor type that occurs in superficial soft tissue.3-5 Fusion partners include NCOA1 and NCOA2, and there is a single report of a tumor harboring PRRX1::KMT2D fusion.5
GLI1-altered mesenchymal tumorsGLI1-altered pericytoma was the first tumor type recognized to harbor GLI1 translocations,6 usually t(7;12)(p22;q13) which correspond to ACTB::GLI1 fusion. GLI1-altered pericytoma is characterized by spindle cell morphology, SMA expression in most cases, and indolent clinical behavior.
GLI1 fusions, including ACTB::GLI1, PTCH1::GLI1, and MALAT1::GLI1, were subsequently described in malignant mesencymal neoplasms with nested morphology.7 Subsequently, GLI1 amplification was shown to drive similar-appearing malignant nested neoplasms, as well as other tumor types falling within a broader morphologic spectrum.8 Most malignant GLI1-rearrranged and GLI1-amplified neoplasms showed morphologic features worrisome for malignancy, including nuclear atypia and high mitotic indices. More recent work has shown that bland-appearing, nested, GLI1-altered tumors behave in an indolent fashion, suggesting that traditional morphologic predictors of malignant behavior might separate this class into benign and malignant groups; these bland tumors were described under the rubric of "nested glomoid neoplasm".9 GLI1 overexpression by immunohistochemistry is a sensitive and specific diagnostic test for this tumor class.10
Pseudoendocrine sarcomaPseudoendocrine sarcoma occurs most commonly in paraspinal soft tissue of older adults, and it give rise to distant metastases in about 20% of patients.11 It morphologically resembles a well-differentiated neuroendocrine tumor, but it does not express keratins or neuroendocrine markers. Pseudoendocrine sarcoma is characterized by CTNNB1 mutations.
NUTM1-rearranged sarcomaNUTM1 fusions with MAD gene family members MGA, MXD1, MXD4, and MXI1 characterize an emerging class of sarcomas that are clinically aggressive, with most patients dying of disease, often within 1-2 years after presentation.12-14 Sarcomas with MGA::NUTM1 fusions are more often spindled and lack rhabdoid morphology, while tumors with MXD1, MXD4, and MXI1 fusions tend to show mixed epithelioid and spindle cell morphology, as well as cells with rhabdoid cytomorphology. More studies are needed to define this tumor class, and to determine whether tumors with MGA fusions are distinct from those with other MAD family member fusions.
PLAG1-rearranged fibroblastic tumorPLAG1-rearranged fibroblastic tumor is a rare tumor type that occurs most commonly in the head and neck region in young children.15 Fusion partners were EEF1A1 and YWHAZ. Tumors show cellular fascicles of bland spindle cells with variably collagenous stroma; characteristically, there are discrete myxoid foci scattered throughout the lesion. Whether these tumors represent a fibroblastic variant of lipoblastoma remains an open question.16
Giant cell tumor with HMGA2::NCOR2 fusionIt has been recognized recently that a subset of giant-cell rich soft tissue tumors show keratin expression and harbor recurrent HMGA2::NCOR2 fusions.17-20 These tumors bear resemblance to giant cell tumor of soft tissue; however, they show more circumscribed growth and keratin expression, neither of which would be typical of giant cell tumor of soft tissue, and they lack metaplastic bone formation. Giant cell tumor with HMGA2::NCOR2 fusion appears to be indolent, although there are rare reports of patients developing metastatic disease.21
KMT2A-rearranged sarcomaKMT2A rearrangements seem to define a distinctive sarcoma type with hyalinized to sclerotic stroma.1,22,23 Most harbor KMT2A::YAP1 fusions, but there has been a report of one that harbored KMT2A::PRRX fusion.23 The stroma is reminiscent of sclerosing epithelioid fibrosarcoma, but the neoplastic cells show more histiocytoid morphology, with pale cytoplasm and vesicular nuclei. Despite their bland morphology, these are aggressive sarcomas, with a high risk of local recurrence and a roughly 20-50% risk of distant metastasis.
Acral FibroChondroMyxoid TumorAcral FibroChondroMyxoid tumor is a benign tumor type that has a striking predilection for the distal extremities, especially the digits.24 It is characterized by THBS1::ADGRF5 fusions. Acral FibroChondroMyxoid tumor shows uniform, round-to-ovoid neoplastic cells in a myxoid matrix and are morphologically reminiscent of myoepithelioma of soft tissue. However, in contrast to myoepithelioma, it does not express keratins or neuroectodermal markers. Instead, acral FibroChondroMyxoid tumor expresses ERG, suggesting it might be showing immature cartilaginous differentiation.
Infantile sinonasal myxomaInfantile sinonasal myxoma is a recently described, clinicopathologically distinctive subtype of craniofacial myxoma.25-27 In contrast to other myxomas of the craniofacial bones, which are characterized by locally aggressive behavior and infiltrative margins, infantile sinonasal myxoma shows indolent behavior even when incompletely resected. Infantile sinonasal myxoma harbors APC inactivation and CTNNB1 mutations in most cases, the latter of which are different from the CTNNB1 mutations that characterize most examples of desmoid fibromatosis.25
Calcified chondroid mesenchymal neoplasmCalcified chondroid mesenchymal neoplasm, an umbrella diagnostic term taht also encompasses tumors described previously under the rubric of "chondroblastoma-like soft tissue chondroma",28 is a benign mesenchymal tumor type that most commonly occurs in the soft tisue of the distal extremities. It shows an admixture of regions with spindle cell proliferations, regions with chondroid extracellular matrix that can show grungy calcification, and regions of frank cartilaginous differentiation. It is now recognized that calcified chondroid mesenchymal neoplasm harbors FN1 fusions, with a variety of fusion partners including FGFR2, FGFR1, MERTK, NTRK1, and TEK.29,30 There are recent reports of calcified chondroid mesenchymal neoplasms harboring alternate PDGFRA::USP8 fusion.31,32
Superficial ALK-rearranged myxoid spindle cell neoplasm, also termed epithelioid fibrous histiocytoid, myxoid spindle cell variantSuperficial ALK-rearranged myxoid spindle cell neoplasm is a recently described benign tumor type that occurs in the skin and subcutis.33-38 It is characterized by whorls of spindle cells in a myxoid matrix. Recently, morphologically identical tumors were described that harbored alternate RET and NTRK3 fusions, and some examples were described that showed hybrid features with epithelioid fibrous histiocytoma;39 therefore, because not all tumors in this morphologic class harbored ALK fusions, and because these tumors showed significant clinical overlap with epithelioid fibrous histiocytoma including benign behavior, the alternate term "epithelioid fibrous histiocytoma, myxoid spindle cell variant" was proposed.39

Article Bibliography

Reference NumberPubmed IDLast YearTitleAuthors
1349585102022'I Can't Keep Up!': an update on advances in soft tissue pathology occurring after the publication of the 2020 World Health Organization classification of soft tissue and bone tumours.Folpe AL et al
2375500122023Emerging mesenchymal tumour types and biases in the era of ubiquitous sequencing.Towery EA et al
3310085392019PRRX-NCOA1/2 rearrangement characterizes a distinctive fibroblastic neoplasm.Lacambra MD et al
4342727532021PRRX1-NCOA1-rearranged fibroblastic tumour: a clinicopathological, immunohistochemical and molecular genetic study of six cases of a potentially under-recognised, distinctive mesenchymal tumour.Dermawan JK et al
5373386202023"PRRX1-rearranged mesenchymal tumors": expanding the immunohistochemical profile and molecular spectrum of a recently described entity with the proposed revision of nomenclature.Warmke LM et al
6151113112004Activation of the GLI oncogene through fusion with the beta-actin gene (ACTB) in a group of distinctive pericytic neoplasms: pericytoma with t(7;12).Dahlén A et al
7293093072018A Distinct Malignant Epithelioid Neoplasm With GLI1 Gene Rearrangements, Frequent S100 Protein Expression, and Metastatic Potential: Expanding the Spectrum of Pathologic Entities With ACTB/MALAT1/PTCH1-GLI1 Fusions.Antonescu CR et al
8311899982019GLI1-amplifications expand the spectrum of soft tissue neoplasms defined by GLI1 gene fusions.Agaram NP et al
9363954742023Distinctive Nested Glomoid Neoplasm: Clinicopathologic Analysis of 20 Cases of a Mesenchymal Neoplasm With Frequent GLI1 Alterations and Indolent Behavior.Papke DJ Jr et al
10366933632023GLI1 Immunohistochemistry Distinguishes Mesenchymal Neoplasms With GLI1 Alterations From Morphologic Mimics.Parrack PH et al
11340810372022Pseudoendocrine Sarcoma: Clinicopathologic Analysis of 23 Cases of a Distinctive Soft Tissue Neoplasm With Metastatic Potential, Recurrent CTNNB1 Mutations, and a Predilection for Truncal Locations.Papke DJ Jr et al
12305521292018A recurrent novel MGA-NUTM1 fusion identifies a new subtype of high-grade spindle cell sarcoma.Diolaiti D et al
13385950532024Cytomorphology of metastatic colonic MXD4::NUTM1-rearranged sarcoma.Wilkinson ZA et al
14337149832021NUTM1-rearranged colorectal sarcoma: a clinicopathologically and genetically distinctive malignant neoplasm with a poor prognosis.Van Treeck BJ et al
15333001922021Pediatric fibromyxoid soft tissue tumor with PLAG1 fusion: A novel entity?Chung CT et al
16330978262021Lipoblastomas presenting in older children and adults: analysis of 22 cases with identification of novel PLAG1 fusion partners.Fritchie K et al
17337421412021Recurrent novel HMGA2-NCOR2 fusions characterize a subset of keratin-positive giant cell-rich soft tissue tumors.Agaimy A et al
18356906442022Xanthogranulomatous epithelial tumors and keratin-positive giant cell-rich soft tissue tumors: two aspects of a single entity with frequent HMGA2-NCOR2 fusions.Dehner CA et al
19371709072023Giant Cell Tumors With HMGA2::NCOR2 Fusion : Clinicopathologic, Molecular, and Epigenetic Study of a Distinct Entity.Perret R et al
20382786072024Xanthogranulomatous Epithelial Tumors and Keratin-Positive Giant Cell Rich Tumors of Soft Tissue and Bone: Two Sides of the Same Coin.Folpe AL et al
21374612322024Keratin-Positive Giant Cell-Rich Tumor of Bone Harboring an HMGA2::NCOR2 Fusion: Two Cases, Including a Patient With Metastatic Disease, and Review of the Literature.Patton A et al
22315927982020Recurrent YAP1 and KMT2A Gene Rearrangements in a Subset of MUC4-negative Sclerosing Epithelioid Fibrosarcoma.Kao YC et al
23319131562020Recurrent Fusions Between YAP1 and KMT2A in Morphologically Distinct Neoplasms Within the Spectrum of Low-grade Fibromyxoid Sarcoma and Sclerosing Epithelioid Fibrosarcoma.Puls F et al
24320472332020Recurrent novel THBS1-ADGRF5 gene fusion in a new tumor subtype "Acral FibroChondroMyxoid Tumors".Bouvier C et al
25376783432023Infantile Sinonasal Myxoma Is Clinically and Genetically Distinct From Other Myxomas of the Craniofacial Bones and From Desmoid Fibromatosis.Odintsov I et al
26370592292023Sinonasal Myxoma: A Distinct Entity or a Myxoid Variant of Desmoid Fibromatosis?Velez Torres JM et al
27375892772023CTNNB1 and APC Mutations in Sinonasal Myxoma : Expanding the Spectrum of Tumors Driven By WNT/β-catenin Pathway.Chen S et al
28113427802001Chondroblastoma-like chondroma of soft tissue: an underrecognized variant and its differential diagnosis.Cates JM et al
29337276962021Calcified chondroid mesenchymal neoplasms with FN1-receptor tyrosine kinase gene fusions including FGFR2, FGFR1, MERTK, NTRK1, and TEK: a molecular and clinicopathologic analysis.Liu YJ et al
30371025742023Calcified Chondroid Mesenchymal Neoplasm: Exploring the Morphologic and Clinical Features of an Emergent Entity With a Series of 33 Cases.Kallen ME et al
31376424402024Expanding the spectrum of tyrosine kinase fusions in calcified chondroid mesenchymal neoplasms: Identification of a novel PDGFRA::USP8 gene fusion.Fisher Y et al
32386705912024Fusion of Platelet Derived Growth Factor Receptor Alpha (PDGFRA) With Ubiquitin Specific Peptidase 8 (USP8) in a Calcified Chondroid Mesenchymal Neoplasm Harboring t(4;15)(q12;q21) as a Sole Aberration.Panagopoulos I et al
33340889972021Superficial ALK-rearranged myxoid spindle cell neoplasm: a cutaneous soft tissue tumor with distinctive morphology and immunophenotypic profile.Dermawan JK et al
34349379022022Superficial ALK-rearranged myxoid spindle cell neoplasm with a novel FMR1-ALK fusion gene.Kao YC et al
35361258532023ALK-rearranged Mesenchymal Neoplasms: A Report of 9 cases Further Expanding the Clinicopathologic Spectrum of Emerging Kinase Fusion Positive Group of Tumors.Dermawan JK et al
36363258852023A novel case of cutaneous myxoid spindle cell neoplasm with FMR1-ALK gene fusion and CD34/S100 co-expression.Kasago I et al
37377260672023ALK-Rearranged Epithelioid Mesenchymal Neoplasm: Expanding the Spectrum of Tyrosine Kinase-Altered Mesenchymal Tumors.Gestrich CK et al
38388390882024ALK-rearranged mesenchymal neoplasms: a clinicopathological and molecular study of eight additional cases of an emerging group of tyrosine kinase fusion mesenchymal tumours.Zhao M et al
39393292542024Epithelioid Fibrous Histiocytoma Is on a Continuum With Superficial ALK -rearranged Myxoid Spindle Cell Neoplasm : A Clinicopathologic Series of 35 Cases Including Alternate RET and NTRK3 Fusions.DeSimone MS et al

Citation

David Papke, MD ; Paola Dal Cin, PhD

Emerging mesenchymal tumor types

Atlas Genet Cytogenet Oncol Haematol. 2024-10-17

Online version: http://atlasgeneticsoncology.org/solid-tumor/209275/emerging-mesenchymal-tumor-types