Unravelling undifferentiated soft tissue sarcomas: insights from genomics.
bone and soft tissue
genomics
pathology
sarcoma
Journal
Histopathology
ISSN: 1365-2559
Titre abrégé: Histopathology
Pays: England
ID NLM: 7704136
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
received:
05
07
2021
accepted:
08
07
2021
entrez:
27
12
2021
pubmed:
28
12
2021
medline:
30
3
2022
Statut:
ppublish
Résumé
Undifferentiated pleomorphic sarcoma now falls under the broader rubric of undifferentiated soft tissue sarcoma (USTS) in the 2020 World Health Organization classification of bone and soft tissue tumours. These rare cancers remain a diagnosis of exclusion, and show genomic complexity manifesting as extreme forms of aneuploidy and genetic rearrangement. This review covers some of the recent advances in the diagnosis and treatment of USTS based on genomic sequencing, cancer evolution and heterogeneity studies, and immunotherapy. We highlight the critical role that pathologists have to play in the diagnosis and treatment of patients with USTS, viewed through the lens of the hallmarks of cancer.
Substances chimiques
Biomarkers, Tumor
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
109-121Subventions
Organisme : Cancer Research UK
ID : 18387
Pays : United Kingdom
Organisme : Cancer Research UK
ID : BCCG1C8R
Pays : United Kingdom
Organisme : Sarcoma UK
ID : SGR04.2017
Organisme : University College London
Informations de copyright
© 2021 The Authors. Histopathology published by John Wiley & Sons Ltd.
Références
Steele CD, Pillay N. The genomics of undifferentiated sarcoma of soft tissue: progress, challenges and opportunities. Semin. Cancer Biol. 2020; 61; 42-55.
Fletcher CD. The evolving classification of soft tissue tumours - an update based on the new 2013 who classification. Histopathology 2014; 64; 2-11.
Mitelman F. Catalogue of chromosome aberrations in cancer. Cytogenet. Cell Genet. 1983; 36; 1-515.
Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144; 646-674.
Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature 2009; 458; 719-724.
Pleasance ED, Cheetham RK, Stephens PJ et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010; 463; 191-196.
Steele CD, Tarabichi M, Oukrif D et al. Undifferentiated sarcomas develop through distinct evolutionary pathways. Cancer Cell 2019; 35; 441-456.e8.
Cancer Genome Atlas Research Network. Electronic address edsc, Cancer Genome Atlas Research N. Comprehensive and integrated genomic characterization of adult soft tissue sarcomas. Cell 2017;171;950-965 e928.
Bielski CM, Zehir A, Penson AV et al. Genome doubling shapes the evolution and prognosis of advanced cancers. Nat Genet 2018; 50; 1189-1195.
Yuan Y, Failmezger H, Rueda OM et al. Quantitative image analysis of cellular heterogeneity in breast tumors complements genomic profiling. Sci. Transl. Med. 2012; 4; 157ra143.
Uhler C, Shivashankar GV. Nuclear mechanopathology and cancer diagnosis. Trends Cancer 2018; 4; 320-331.
Pérot G, Chibon F, Montero A et al. Constant p53 pathway inactivation in a large series of soft tissue sarcomas with complex genetics. Am. J. Pathol. 2010; 177; 2080-2090.
Irshad H, Veillard A, Roux L, Racoceanu D. Methods for nuclei detection, segmentation, and classification in digital histopathology: a review-current status and future potential. IEEE Rev. Biomed. Eng. 2014; 7; 97-114.
Stephens PJ, Greenman CD, Fu B et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 2011; 144; 27-40.
Cortes-Ciriano I, Lee JJ, Xi R et al. Comprehensive analysis of chromothripsis in 2,658 human cancers using whole-genome sequencing. Nat. Genet. 2020; 52; 331-341.
Muller HJ. The relation of recombination to mutational advance. Mutat. Res. 1964; 106; 2-9.
Arbajian E, Koster J, Vult von Steyern F, Mertens F. Inflammatory leiomyosarcoma is a distinct tumor characterized by near-haploidization, few somatic mutations, and a primitive myogenic gene expression signature. Mod. Pathol. 2018; 31; 93-100.
Pasquali S, Braglia L, Chibon F et al. The prognostic value of CINSARC in a randomised trial comparing histotype-tailored neoadjuvant chemotherapy versus standard chemotherapy in patients with high-risk soft-tissue sarcomas (ISG-STS 1001). J. Clin. Oncol. 2020; 38; e23531.
Chibon F, Lagarde P, Salas S et al. Validated prediction of clinical outcome in sarcomas and multiple types of cancer on the basis of a gene expression signature related to genome complexity. Nat. Med. 2010; 16; 781-787.
Davies H, Glodzik D, Morganella S et al. Hrdetect is a predictor of BRCA1 and BRCA2 deficiency based on mutational signatures. Nat Med 2017; 23; 517-525.
Macintyre G, Goranova TE, De Silva D et al. Copy number signatures and mutational processes in ovarian carcinoma. Nat. Genet. 2018; 50; 1262-1270.
Simons A, Schepens M, Jeuken J et al. Frequent loss of 9p21 (p16(INK4a)) and other genomic imbalances in human malignant fibrous histiocytoma. Cancer Genet. Cytogenet. 2000; 118; 89-98.
Chibon F, Mairal A, Freneaux P et al. The RB1 gene is the target of chromosome 13 deletions in malignant fibrous histiocytoma. Cancer Res. 2000; 60; 6339-6345.
Gibault L, Pérot G, Chibon F et al. New insights in sarcoma oncogenesis: a comprehensive analysis of a large series of 160 soft tissue sarcomas with complex genomics. J. Pathol. 2011; 223; 64-71.
Kastenhuber ER, Lowe SW. Putting p53 in context. Cell 2017; 170; 1062-1078.
Mantovani F, Collavin L, Del Sal G. Mutant p53 as a guardian of the cancer cell. Cell Death Differ. 2019; 26; 199-212.
Knudsen ES, Nambiar R, Rosario SR, Smiraglia DJ, Goodrich DW, Witkiewicz AK. Pan-cancer molecular analysis of the RB tumor suppressor pathway. Commun. Biol. 2020; 3; 158.
Li GZ, Okada T, Kim Y-M et al. Rb and p53-deficient myxofibrosarcoma and undifferentiated pleomorphic sarcoma require Skp2 for survival. Cancer Res. 2020; 80; 2461-2471.
May CD, Landers SM, Bolshakov S et al. Co-targeting PI3K, mTOR, and IGF1R with small molecule inhibitors for treating undifferentiated pleomorphic sarcoma. Cancer Biol. Ther. 2017; 18; 816-826.
Hélias-Rodzewicz Z, Pérot G, Chibon F et al. YAP1 and VGLL3, encoding two cofactors of TEAD transcription factors, are amplified and overexpressed in a subset of soft tissue sarcomas. Genes Chromosomes Cancer 2010; 49; 1161-1171.
Harvey KF, Zhang X, Thomas DM. The Hippo pathway and human cancer. Nat. Rev. Cancer 2013; 13; 246-257.
Hori N, Okada K, Takakura Y, Takano H, Yamaguchi N, Yamaguchi N. Vestigial-like family member 3 (VGLL3), a cofactor for TEAD transcription factors, promotes cancer cell proliferation by activating the Hippo pathway. J. Biol. Chem. 2020; 295; 8798-8807.
Eisinger-Mathason TSK, Mucaj V, Biju KM et al. Deregulation of the Hippo pathway in soft-tissue sarcoma promotes FOXM1 expression and tumorigenesis. Proc. Natl. Acad. Sci. USA. 2015; 112; E3402-E3411.
Barthel FP, Wei W, Tang M et al. Systematic analysis of telomere length and somatic alterations in 31 cancer types. Nat. Genet. 2017; 49; 349-357.
Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. Telomere end-replication problem and cell aging. J. Mol. Biol. 1992; 225; 951-960.
Maciejowski J, Li Y, Bosco N, Campbell PJ, de Lange T. Chromothripsis and kataegis induced by telomere crisis. Cell 2015; 163; 1641-1654.
von Morgen P, Maciejowski J. The ins and outs of telomere crisis in cancer. Genome. Med. 2018; 10; 89.
Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA. Highly recurrent TERT promoter mutations in human melanoma. Science 2013; 339; 957-959.
Zhang A, Zheng C, Lindvall C et al. Frequent amplification of the telomerase reverse transcriptase gene in human tumors. Cancer Res. 2000; 60; 6230-6235.
Bahrami A, Lee S, Schaefer I-M et al. TERT promoter mutations and prognosis in solitary fibrous tumor. Mod. Pathol. 2016; 29; 1511-1522.
Ventura Ferreira M, Crysandt M, Braunschweig T et al. Presence of TERT promoter mutations is a secondary event and associates with elongated telomere length in myxoid liposarcomas. Int. J. Mol. Sci. 2018; 19; 608.
Killela PJ, Reitman ZJ, Jiao Y et al. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc. Natl. Acad. Sci. USA. 2013; 110; 6021-6026.
Griewank KG, Schilling B, Murali R et al. TERT promoter mutations are frequent in atypical fibroxanthomas and pleomorphic dermal sarcomas. Mod. Pathol. 2014; 27; 502-508.
Koelsche C, Renner M, Hartmann W et al. TERT promoter hotspot mutations are recurrent in myxoid liposarcomas but rare in other soft tissue sarcoma entities. J. Exp. Clin. Cancer Res. 2014; 33; 33.
Saito T, Akaike K, Kurisaki-arakawa A et al. TERT promoter mutations are rare in bone and soft tissue sarcomas of Japanese patients. Mol. Clin. Oncol. 2016; 4; 61-64.
Peifer M, Hertwig F, Roels F et al. Telomerase activation by genomic rearrangements in high-risk neuroblastoma. Nature 2015; 526; 700-704.
Delespaul L, Lesluyes T, Perot G et al. Recurrent TRIO fusion in nontranslocation-related sarcomas. Clin. Cancer Res. 2017; 23; 857-867.
Ramamoorthy M, Smith S. Loss of ATRX suppresses resolution of telomere cohesion to control recombination in ALT cancer cells. Cancer Cell 2015; 28; 357-369.
Liau JY, Lee JC, Tsai JH et al. Comprehensive screening of alternative lengthening of telomeres phenotype and loss of ATRX expression in sarcomas. Mod. Pathol. 2015; 28; 1545-1554.
O'Sullivan RJ, Almouzni G. Assembly of telomeric chromatin to create ALTernative endings. Trends Cell Biol. 2014; 24; 675-685.
Pan X, Drosopoulos WC, Sethi L, Madireddy A, Schildkraut CL, Zhang D. FANCM, BRCA1, and BLM cooperatively resolve the replication stress at the ALT telomeres. Proc. Natl. Acad. Sci. USA 2017; 114; E5940-E5949.
Flynn RL, Cox KE, Jeitany M et al. Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors. Science 2015; 347; 273-277.
Lawlor RT, Veronese N, Pea A et al. Alternative lengthening of telomeres (ALT) influences survival in soft tissue sarcomas: a systematic review with meta-analysis. BMC Cancer 2019; 19; 232.
Slijepcevic P. Telomere length measurement by Q-FISH. Methods Cell Sci. 2001; 23; 17-22.
Montpetit AJ, Alhareeri AA, Montpetit M et al. Telomere length: a review of methods for measurement. Nurs. Res. 2014; 63; 289-299.
Yeager TR, Neumann AA, Englezou A, Huschtscha LI, Noble JR, Reddel RR. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res 1999; 59; 4175-4179.
Heaphy CM, Subhawong AP, Hong S-M et al. Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am. J. Pathol. 2011; 179; 1608-1615.
Henson JD, Cao Y, Huschtscha LI et al. DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat. Biotechnol. 2009; 27; 1181-1185.
Idilli AI, Segura-Bayona S, Lippert TP, Boulton SJ. A C-circle assay for detection of alternative lengthening of telomere activity in FFPE tissue. STAR Protoc. 2021; 2; 100569.
Ding Z, Mangino M, Aviv A, Spector T, Durbin R. Estimating telomere length from whole genome sequence data. Nucleic. Acids Res. 2014; 42; e75.
Feuerbach L, Sieverling L, Deeg KI et al. Telomerehunter - in silico estimation of telomere content and composition from cancer genomes. BMC Bioinformatics 2019; 20; 272.
D'Incalci M, Galmarini CM. A review of trabectedin (ET-743): a unique mechanism of action. Mol. Cancer Ther. 2010; 9; 2157-2163.
Pompili L, Leonetti C, Biroccio A, Salvati E. Diagnosis and treatment of ALT tumors: is trabectedin a new therapeutic option? J. Exp. Clin. Cancer Res. 2017; 36; 189.
De Sanctis R, Marrari A, Marchetti S et al. Efficacy of trabectedin in advanced soft tissue sarcoma: beyond lipo- and leiomyosarcoma. Drug Des. Devel. Ther. 2015; 9; 5785-5791.
Nowell PC. The clonal evolution of tumor cell populations. Science 1976; 194; 23-28.
Thorsson V, Gibbs DL, Brown SD et al. The immune landscape of cancer. Immunity 2018; 48; 812-830 e814.
Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu. Rev. Immunol. 2004; 22; 329-360.
Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271; 1734-1736.
Ishida Y, Agata Y, Shibahara K, Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 1992; 11; 3887-3895.
Fourcade J, Sun Z, Benallaoua M et al. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J. Exp. Med. 2010; 207; 2175-2186.
Davis AA, Patel VG. The role of PD-L1 expression as a predictive biomarker: an analysis of all US food and drug administration (FDA) approvals of immune checkpoint inhibitors. J. Immunother. Cancer 2019; 7; 278.
Tawbi HA, Burgess M, Bolejack V et al. Pembrolizumab in advanced soft-tissue sarcoma and bone sarcoma (SARC028): a multicentre, two-cohort, single-arm, open-label, phase 2 trial. Lancet Oncol. 2017; 18; 1493-1501.
Petitprez F, de Reyniès A, Keung EZ et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature 2020; 577; 556-560.
Wustrack RL, Shao E, Sheridan J et al. Tumor morphology and location associate with immune cell composition in pleomorphic sarcoma. Cancer Immunol. Immunother. 2021.
Pollack SM, He Q, Yearley JH et al. T-cell infiltration and clonality correlate with programmed cell death protein 1 and programmed death-ligand 1 expression in patients with soft tissue sarcomas. Cancer 2017; 123; 3291-3304.
Devalaraja S, To TKJ, Folkert IW et al. Tumor-derived retinoic acid regulates intratumoral monocyte differentiation to promote immune suppression. Cell 2020; 180; 1098-1114 e16.
Rosenthal R, Cadieux EL, Salgado R et al. Neoantigen-directed immune escape in lung cancer evolution. Nature 2019; 567; 479-485.
Budczies J, Bockmayr M, Denkert C et al. Pan-cancer analysis of copy number changes in programmed death-ligand 1 (Pd-L1, CD274) - associations with gene expression, mutational load, and survival. Genes Chromosomes Cancer 2016; 55; 626-639.
Barrett MT, Anderson KS, Lenkiewicz E et al. Genomic amplification of 9p24.1 targeting JAK2, PD-L1, and PD-L2 is enriched in high-risk triple negative breast cancer. Oncotarget 2015; 6; 26483-26493.
Inoue Y, Yoshimura K, Mori K et al. Clinical significance of PD-L1 and PD-L2 copy number gains in non-small-cell lung cancer. Oncotarget 2016; 7; 32113-32128.
Goodman AM, Piccioni D, Kato S et al. Prevalence of PDL1 amplification and preliminary response to immune checkpoint blockade in solid tumors. JAMA Oncol. 2018; 4; 1237-1244.
Budczies J, Mechtersheimer G, Denkert C et al. Pd-L1 (CD274) copy number gain, expression, and immune cell infiltration as candidate predictors for response to immune checkpoint inhibitors in soft-tissue sarcoma. Oncoimmunology 2017; 6; e1279777.
Saunders G, Baudis M, Becker R et al. Leveraging european infrastructures to access 1 million human genomes by 2022. Nat. Rev. Genet. 2019; 20; 693-701.