A rare non-gadolinium enhancing sarcoma brain metastasis with microenvironment dominated by tumor-associated macrophages.
Brain metastasis
Brain tumor microenvironment
Sarcoma
Tumor-associated macrophages
Journal
Acta neuropathologica communications
ISSN: 2051-5960
Titre abrégé: Acta Neuropathol Commun
Pays: England
ID NLM: 101610673
Informations de publication
Date de publication:
22 Jan 2024
22 Jan 2024
Historique:
received:
24
08
2023
accepted:
17
12
2023
medline:
23
1
2024
pubmed:
23
1
2024
entrez:
23
1
2024
Statut:
epublish
Résumé
Brain metastases occur in 1% of sarcoma cases and are associated with a median overall survival of 6 months. We report a rare case of a brain metastasis with unique radiologic and histopathologic features in a patient with low grade fibromyxoid sarcoma (LGFMS) previously treated with immune checkpoint inhibitor (ICI) therapy. The lone metastasis progressed in the midbrain tegmentum over 15 months as a non-enhancing, T2-hyperintense lesion with peripheral diffusion restriction, mimicking a demyelinating lesion. Histopathology of the lesion at autopsy revealed a rich infiltrate of tumor-associated macrophages (TAMs) with highest density at the leading edge of the metastasis, whereas there was a paucity of lymphocytes, suggestive of an immunologically cold environment. Given the important immunosuppressive and tumor-promoting functions of TAMs in gliomas and carcinoma/melanoma brain metastases, this unusual case provides an interesting example of a dense TAM infiltrate in a much rarer sarcoma brain metastasis.
Identifiants
pubmed: 38254244
doi: 10.1186/s40478-023-01713-8
pii: 10.1186/s40478-023-01713-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
15Informations de copyright
© 2023. The Author(s).
Références
Chen N, Gong J, Nie L, Chen X, Xu M, Chen M et al (2015) Primary intracranial low-grade fibromyxoid sarcoma with FUS gene rearrangement. Neuropathology 35:348–353. https://doi.org/10.1111/neup.12197
doi: 10.1111/neup.12197
pubmed: 25828939
Chen Q, Boire A, Jin X, Valiente M, Er EE, Lopez-Soto A et al (2016) Carcinoma–astrocyte gap junctions promote brain Metastasis by cGAMP transfer. Nature 533:493–498. https://doi.org/10.1038/nature18268
doi: 10.1038/nature18268
pubmed: 27225120
pmcid: 5021195
DeNardo DG, Ruffell B (2019) Macrophages as regulators of tumour immunity and immunotherapy. Nat Rev Immunol 19:369–382. https://doi.org/10.1038/s41577-019-0127-6
doi: 10.1038/s41577-019-0127-6
pubmed: 30718830
pmcid: 7339861
Friebel E, Kapolou K, Unger S, Núñez NG, Utz S, Rushing EJ et al (2020) Single-cell mapping of Human Brain Cancer reveals tumor-specific instruction of tissue-invading leukocytes. Cell 181:1626–1642e1620. https://doi.org/10.1016/j.cell.2020.04.055
doi: 10.1016/j.cell.2020.04.055
pubmed: 32470397
Gusho CA, Blank AT, Batus M (2021) Outcomes of brain Metastasis in high-grade bone and soft tissue sarcoma: an analysis of clinicopathological characteristics and survival data. Rare Tumors 13:20363613211026151. https://doi.org/10.1177/20363613211026151
doi: 10.1177/20363613211026151
pubmed: 34221290
pmcid: 8221671
Hyland M, Bermel RA, Cohen JA (2013) Restricted diffusion preceding gadolinium enhancement in large or tumefactive demyelinating lesions. Neurol Clin Pract 3:15–21. https://doi.org/10.1212/CPJ.0b013e318283ff8e
doi: 10.1212/CPJ.0b013e318283ff8e
pubmed: 23634380
pmcid: 3613217
Karimi S, Lis E, Gilani S, D’Ambrosio N, Holodny A (2011) Nonenhancing brain metastases. J Neuroimaging 21:184–187. https://doi.org/10.1111/j.1552-6569.2009.00389.x
doi: 10.1111/j.1552-6569.2009.00389.x
pubmed: 19490401
Khan F, Pang L, Dunterman M, Lesniak MS, Heimberger AB, Chen P (2023) Macrophages and microglia in glioblastoma: heterogeneity, plasticity, and therapy. J Clin Investig 133. https://doi.org/10.1172/JCI163446
Klemm F, Maas RR, Bowman RL, Kornete M, Soukup K, Nassiri S et al (2020) Interrogation of the Microenvironmental Landscape in Brain Tumors reveals Disease-specific alterations of Immune cells. Cell 181:1643–1660e1617. https://doi.org/10.1016/j.cell.2020.05.007
doi: 10.1016/j.cell.2020.05.007
pubmed: 32470396
pmcid: 8558904
Lin GL, Nagaraja S, Filbin MG, Suvà ML, Vogel H, Monje M (2018) Non-inflammatory Tumor microenvironment of diffuse intrinsic pontine glioma. 6 51. https://doi.org/10.1186/s40478-018-0553-x
Linette GP, Carreno BM (2019) Tumor-infiltrating lymphocytes in the checkpoint inhibitor era. Curr Hematol Malig Rep 14:286–291. https://doi.org/10.1007/s11899-019-00523-x
doi: 10.1007/s11899-019-00523-x
pubmed: 31187421
pmcid: 6642683
Lu-Emerson C, Snuderl M, Kirkpatrick ND, Goveia J, Davidson C, Huang Y et al (2013) Increase in tumor-associated macrophages after antiangiogenic therapy is associated with poor survival among patients with recurrent glioblastoma. Neurooncology 15:1079–1087. https://doi.org/10.1093/neuonc/not082
doi: 10.1093/neuonc/not082
Maretty-Nielsen K, Baerentzen S, Keller J, Dyrop HB, Safwat A (2013) Low-Grade Fibromyxoid Sarcoma: incidence, Treatment Strategy of Metastases, and clinical significance of the FUS Gene. Sarcoma 2013:256280. https://doi.org/10.1155/2013/256280
doi: 10.1155/2013/256280
pubmed: 23818812
pmcid: 3683502
Piao Y, Liang J, Holmes L, Zurita AJ, Henry V, Heymach JV et al (2012) Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neurooncology 14:1379–1392. https://doi.org/10.1093/neuonc/nos158
doi: 10.1093/neuonc/nos158
Pukrop T, Dehghani F, Chuang HN, Lohaus R, Bayanga K, Heermann S et al (2010) Microglia promote colonization of brain tissue by Breast cancer cells in a wnt-dependent way. Glia 58:1477–1489. https://doi.org/10.1002/glia.21022
doi: 10.1002/glia.21022
pubmed: 20549749
Schulz M, Sevenich L (2021) TAMs in Brain Metastasis: Molecular signatures in Mouse and Man. Front Immunol 12:716504. https://doi.org/10.3389/fimmu.2021.716504
doi: 10.3389/fimmu.2021.716504
pubmed: 34539650
pmcid: 8447936
Sevenich L, Bowman RL, Mason SD, Quail DF, Rapaport F, Elie BT et al (2014) Analysis of tumour- and stroma-supplied proteolytic networks reveals a brain-metastasis-promoting role for cathepsin S. Nat Cell Biol 16:876–888. https://doi.org/10.1038/ncb3011
doi: 10.1038/ncb3011
pubmed: 25086747
pmcid: 4249762
Solomiia S, Kaylee G, Wengang W, Elana C, Belgin Y, Yin L et al (2023) Neuronal-activity dependent mechanisms of small cell Lung Cancer Progression. bioRxiv: 2023.2001.2019.524430. https://doi.org/10.1101/2023.01.19.524430
Warmke LM, Meis JM (2021) Sclerosing Epithelioid Fibrosarcoma: a distinct sarcoma with aggressive features. Am J Surg Pathol 45:317–328. https://doi.org/10.1097/pas.0000000000001559
doi: 10.1097/pas.0000000000001559
pubmed: 32769431
White IK, Scherer AG, Baumanis MM, Abdulkader M, Fulkerson DH (2015) Rapidly enlarging low-grade fibromyxoid sarcoma with intracranial extension in a 5-year-old girl: case report. J Neurosurg Pediatr 16:372–376. https://doi.org/10.3171/2015.3.peds14564
doi: 10.3171/2015.3.peds14564
pubmed: 26140292
Woods AD, Purohit R, Mitchell LC, Collier JR, Collier KA, Lathara M et al (2021) Metastatic pediatric sclerosing epithelioid fibrosarcoma. 7. https://doi.org/10.1101/mcs.a006093
Zhu C, Kros JM, Cheng C, Mustafa D (2017) The contribution of tumor-associated macrophages in glioma neo-angiogenesis and implications for anti-angiogenic strategies. Neurooncology 19:1435–1446. https://doi.org/10.1093/neuonc/nox081
doi: 10.1093/neuonc/nox081