Abstract: Primary cutaneous acral CD8-positive T-cell lymphoma consists of slow-growing nodules in acral sites with a histopathology, suggesting high-grade lymphoma despite the indolent clinical course. It has been recently included in WHO-EORTC classification for primary cutaneous lymphomas as a provisional entity. A correct diagnosis of this entity is important because its differential diagnosis include more aggressive cutaneous lymphomas. We present a 53-year-old woman with an indolent solitary nodule on her right leg, which histopathologically showed features of CD8-positive T-cell lymphoma, although with some peculiarities, including epidermotropism, absence of CD68 expression, and positivity for GATA3 and Bcl6 in neoplastic cells. This case could contribute to better define the spectrum of this rare cutaneous lymphoma.
Mycosis fungoides (MF) and Sézary syndrome (SS) are the most common subtypes of cutaneous T-cell lymphomas. The diagnosis of these patients is very challenging and requires an integrated approach, incorporating clinical, morphological, immunophenotypic and molecular features. The molecular substrate of early and advanced stages of MF / SS is still poorly understood and, consequently, treatment selection is mainly based on clinical data. The study aimed to transfer what is known about the molecular pathogenesis of MF / SS to early diagnosis, prognosis, and selection of therapy by identifying molecular markers associated with the course of the disease. Using the NanoString platform for gene-expression analysis, we design a custom panel of 77 genes relevant in the pathogenesis of MF/SS, together with genes known to be therapeutic targets. A series of 81 formalin-fixed, paraffin-embedded (FFPE) samples belonging to 27 MF/SS patients in different phases of the disease are included in the study. The technique was informative in all analyzed cases, independently of the clinical or histological stage or density of the tumor infiltration. For each case or sample the analysis provided an objective measure of the T-cell phenotype (T-cell differentiation gene sets), cellular composition of the infiltrate (dendritic cells, macrophages, B-cells,…) expression of markers used for therapy selection (CD30, CXCR4 and KIR3DL2) and expression level of surrogate markers for the main cell-survival oncogenic pathways. Unexpectedly, non-supervised clustering showed that most of the clustering was dependent of the patient identity, suggesting that MF/SS has a high degree of inter-tumoral heterogeneity and that molecular signature for each patient tends to remain relatively stable along the disease. Samples corresponding to pre-MF lesions tend to cluster with early MF/SS samples, suggesting that pre-MF lesions indeed correspond to early phases of the disease. On the other hand, patients who progress to advanced stages have a tendency to cluster with each other. Several differentially expressed genes were comparing early and advanced stages. FGFR3, NUAK1, FJX1, CXCL12 and RORC were up regulated in early lesions, while CARD11, CD2, CD38, CD3D, CD3E, CD3G, CXCR4, GZMA, IL10 and SELL were up - regulated in tumors (p< 0,005). Gene-expression profiling using a customized NanoString platform can be applied to routine paraffin embedded MF/SS samples and provides data that allow to a better understanding of MF genesis and progression. MF/SS samples show an unexpected high degree of inter-tumoral heterogeneity, suggesting that every patient has some individual molecular signature features that are found in consecutive biopsies. The analysis brings also particular gene signatures associated with early MF and progression, allowing recognizing stage-specific signatures. EA - previously submitted to regional or national meetings (up to 1000 attendees) The research was funded by: The research was supported by grants from Instituto de Salud Carlos III, from Ministerio de Economía, Industria y Competitividad, Asociación Española Contra el Cáncer (AECC), Comunidad Autónoma de Madrid and Centro de Investigación Biomédica en Red de Cáncer (CIBERONC): SAF2013-47416-R, CIBERONC-ISCIII, ISCIII-MINECO-AES-FEDER (Plan Estatal I + D + I 2013-2016), AECC PROYE18054PIRI, CAM B2017/BMD-3778, PIC97/2017_FJD, PIE15/0081, PIE16/01294 and PIE19/00715. L.Tomas-Roca was funded by Marie Skłodowska-Curie Individual Fellowship (No 882597) Conflicts of interests pertinent to the abstract Consultant or advisory role Millenium/Takeda. Celgene. Gilead. Jansen. Nanostring. Kyowa Kirin Research funding: Millenium/Takeda. Gilead. Kura
Introduction: Peripheral T-cell Lymphomas (PTCLs) are aggressive tumours with unfavourable prognosis, with around 30% overall survival (OS) after 5 years. Histological and molecular studies have revealed a striking degree of heterogeneity, with three major PTCL subtypes defined. Consistent diagnosis and prognostication are still difficult to achieve, because of the difficulty of reproducing results, and the dearth of clinically applicable prognostic biological markers. Methods: We have analyzed a series of 105 PTCL cases (66 angioimmunoblastic T-cell lymphoma, AITL; 21 PTCL-not otherwise specified, PTCL-NOS; and 18 PTCL-with T follicular helper phenotype, PTCL-TFH) patients using a customized NanoString platform that includes 208 genes associated with T-cell differentiation, oncogenes and tumor suppressor genes, deregulated pathways and stromal cell subpopulations. Specifically, the platform includes genes expressed by the multiple cell types present in PTCL specimens, together with normal T-cell populations. These are used to try and enable the deconvolution of the T-cell lymphoma microenvironment, and thereby develop an integrated perspective on the cell composition of PTCL tumor specimens. Results: A comparative analysis of the various histological types of PTCL (AITL, PTCL-NOS and PTCL-TFH) showed specific sets of genes to be associated with each of the diagnoses, including TFH markers, cytotoxic markers and genes whose expression was a surrogate for specific cellular subpopulations, including follicular dendritic cells, mast cells and genes belonging to specific cell-survival pathways (NF-κB). Unsupervised analysis of the expression of the genes here studied revealed clusters of co-regulated genes that identified the main cell components of the tumor. The analysis did not reveal any differences in survival probability associated with the histological sub-classification, but did identify specific genes and gene sets whose expression was associated with changes in survival probability for each of the PTCL subtypes, independently of the clinical variables included in the International Prognostic Index (IPI). These included a B-cell gene set in cases of AITL, the expression of proliferation markers in PTCL-NOS, and the expression of cytotoxic markers in cases with a diagnosis of PTCL-TFH. For each PTCL lymphoma type, a multivariate analysis identified genes that allow the series of cases to be stratified into different risk groups. This was validated for AITL in an independent series of 54 additional cases. Conclusions: In summary, our study supports the current division of PTCL into these three categories (AITL, PTCL-NOS and PTCL-TFH), identifies gene sets potentially useful for this classification and recognizes the expression of B-cell genes as an IPI-independent prognostic factor for AITL subtype. EA – previously submitted to regional or national meetings (up to 1000 attendees). The research was funded by: The research was supported by grants from Instituto de Salud Carlos III, from Ministerio de Economía, Industria y Competitividad, Asociación Española Contra el Cáncer (AECC), Comunidad Autónoma de Madrid and Centre for Biomedical Network Research on Cancer (CIBERONC): SAF2013-47416-R, CIBERONC-ISCIII (CB16/12/00291), ISCIII-MINECO-AES-FEDER (Plan Estatal I + D + I 2013-2016), ISCIII-MINECO AES-FEDER (Plan Estatal I + D + I 2017-2020), AECC PROYE18054PIRI, CAM B2017/BMD-3778, PIC97/2017_FJD, PIE15/0081, PI17/00272, PIE16/01294, GILEAD (GL18/00019) and PIC 041-19. L. Tomas-Roca was funded by Marie Skłodowska-Curie Individual Fellowship (No 882597). Keywords: Genomics, Epigenomics, and Other -Omics, Diagnostic and Prognostic Biomarkers, Aggressive T-cell non-Hodgkin lymphoma Conflicts of interests pertinent to the abstract M. Án. Piris Consultant or advisory role: Millenium/Takeda, Celgene, Gilead, Jansen, NanoString, Kyowa Kirin Research funding: Millenium/Takeda, Gilead, Kura
<div>Abstract<p>Recently, it has been shown that mice deficient in the proapoptotic protein prostate apoptosis response 4 (Par-4) are specifically prone to develop endometrial carcinomas. Based on this, we have examined here the possible role of <i>Par-4</i> as a tumor suppressor gene in human endometrial cancer. Using cDNA arrays, quantitative reverse transcription-PCR, and immunohistochemistry, we detected <i>Par-4</i> down-regulation in ∼40% of endometrial carcinomas. This alteration was not associated with phosphatase and tensin homologue (<i>PTEN</i>), <i>K-RAS</i>, or <i>β-catenin</i> mutations, but was more frequent among tumors showing microsatellite instability (MSI) or among tumors that were estrogen receptor positive. Mutational analysis of the complete coding sequence of <i>Par-4</i> in endometrial cancer cell lines (<i>n</i> = 6) and carcinomas (<i>n</i> = 69) detected a mutation in a single carcinoma, which was localized in exon 3 [Arg (CGA) 189 (TGA) Stop]. Interestingly, <i>Par-4</i> promoter hypermethylation was detected in 32% of the tumors in association with low levels of Par-4 protein and was more common in MSI-positive carcinomas. <i>Par-4</i> promoter hypermethylation and silencing was also detected in endometrial cancer cell lines SKUT1B and AN3CA, and reexpression was achieved by treatment with the demethylating agent 5′-aza-2′-deoxycytidine. Together, these data show that <i>Par-4</i> is a relevant tumor suppressor gene in human endometrial carcinogenesis. [Cancer Res 2007;67(5):1927–34]</p></div>
Peripheral T-cell lymphomas (PTCLs) are a heterogeneous group of non-Hodgkin lymphomas (NHLs), characterized by their striking clinical and biological heterogeneity and non-specific therapeutic regimens. JAK proteins (Janus kinases, JAK1-3 and TYK2) exhibit tyrosine kinase activity and are associated with cytokine receptors. After ligand binding, JAKs bind to the receptors, allowing their phosphorylation, resulting in the activation of members of the STAT family (signal transducer and activator of transcription, STAT1 – STAT4, 5A, 5B and 6) (Heim, 1999). Most of these dimmers are related to proliferation, differentiation and survival. Alterations of the JAK/STAT-pathway are frequent in diverse subtypes of PTCL. Moreover, the use of JAK/STAT-inhibitors in cell lines and/or patients with haematological malignancies and solid tumours causes inhibition of cell proliferation, improvement of symptoms and increased survival, respectively (Perez et al, 2015). This study aimed to analyse the activation of the JAK/STAT-pathway in nodal PTCL-not otherwise specified (NOS) and establish its potential clinical implication. Tissue microarrays of 98 nodal PTCL-NOS, comprising 57 angioimmunoblastic T-cell lymphoma (AITL) and 41 PTCL-NOS patients were constructed. The expression of phosphorylated (p)-STAT3, p-STAT6 as well as NF-KB-pathway proteins, Follicular helper T-cell phenotype (TFH markers) and Ki67 was analysed by immunohistochemistry (IHC) (Table S1). Next Generation Sequencing (NGS) was used to identify whether mutations in genes of the JAK/STAT pathway could be involved in its activation (Table S2). Clinical data of all patients was collected. Conventional statistical tools were used to establish correlations between biological and/or clinical features (see Supplementary Information). Twenty-eight (28/98, 28·6%) and 26 cases (26/98, 26·5%) were positive (i.e., when more than 10% and 20%, respectively, of the tumoural cells showed nuclear staining) for p-STAT3 and p-STAT6, respectively (Fig 1). Overall, 6·1% (6/98) of the tumours (3 AITL and 3 PTCL-NOS) showed mutations in one gene of this pathway (Table 1). Mutations were mutually exclusive. There were three JAK1 (G1097V, T901R, K696E), one STAT1 (E563K), one STAT3 (D566N) and one CCR4 (Y331*) gene mutations. No correlations were found between p-STAT3 or p-STAT6 expression and JAK/STAT pathway gene mutations. p-STAT3 and p-STA6 expression was associated with the presence of AITL morphology and TFH phenotype (P = 0·047 and 0·001, respectively). p-STAT3 expression was directly associated with the presence of ICOS (P = 0·013), CXCL13 (P = 0·005) and p52 (also termed NFKB2; P < 0·001). Moreover, p-STAT6 expression was significantly and positively correlated with the level of Ki67 expression (P = 0·012) and nuclear expression of p52 (P < 0·001). No correlations were found between either p50 (NFKB1) immunoreactivity or p-STAT3/p-STAT6 expression. In this series, p-STAT6 expression was related to shorter survival (P = 0·008) (Fig 1). Interestingly, 2/3 patients (66·7%) with mutations in genes of the JAK/STAT-pathway (Cases 24 and 53) showed a worse prognosis (P = 0·016) (Figure S1). A tendency for JAK1 and/or STAT3 mutations to be present in the cutaneous T-cell lymphoma (CTCL) and ALK-negative ALCL subgroup, as well as the overrepresentation of STAT5B and/or JAK3 mutations in subgroups of epitheliotropic intestinal T-cell lymphoma (EATL) type II, hepatosplenic T-cell lymphoma (HPTSP), primary cutaneous γδ T-cell lymphoma (γδ-TCL) and Natural Killer/T-cell lymphomas, has been reported in previous studies (Nicolae et al, 2014; Crescenzo et al, 2015; Perez et al, 2015). In contrast to the present report, a large subset of these tumours harboured concurrent activating mutations in two members of the same pathway (Crescenzo et al, 2015). Here, JAK1 was the most frequently mutated gene (found in 1 AITL and 2 PTCL-NOS cases), with mutations taking place in the kinase and pseudo-kinase domains of the gene, conferring a potentially harmful function (Figure S2). Two patients showed mutations in the DNA binding domain of both STAT1 (E563K) and STAT3 (D566N) genes. STAT1-E563K is a non-synonymous single nucleotide variation (SNV) that has been reported in PTCL-NOS, where it is associated with p-STAT6 expression and has been predicted to have a deleterious function (Palomero et al, 2014). Recently, Abate et al (2017) reported STAT6 gene mutations in 8·3% (5/60) of AITL cases. This series features a single case with a STAT3 mutation, which also showed p-STAT3 nuclear expression and CD30-positivity (Figure S3). Nevertheless, it was considered PTCL-NOS-positive for TFH markers lacking anaplastic morphology, thus showing that STAT3 mutations can be also found in non-anaplastic T-cell lymphomas (Crescenzo et al, 2015). C-C chemokine receptor type 4 (CCR4) is a chemokine receptor belonging to the G protein-coupled receptor (GPCR) family. It has been frequently found mutated in ATLL patients, conferring poor prognosis and activating the PI3K-pathway. It has been found mutated in a series of 9% of PTCL-NOS cases, and is overexpressed in AITL patients with a RHOA mutation (Nagao et al, 2016). We found one AITL case with the most frequently mutated amino acid so far reported (Y331*). The frequency of JAK/STAT mutations identified here is slightly higher than that reported by Vallois et al (2016) (4/85). Furthermore, the results of this study also draw attention to the importance of JAK/STAT pathway activation in PTCL and AITL, whereby there are close associations between mutations in this pathway and a TFH phenotype (P < 0·001), and between shorter survival for both p-STA6 expression and JAK-STAT pathway mutation. Additionally, a close relationship was found between p-STAT6 expression and a high proliferation index (Ki67), which is a feature related to poor outcome in this and other series (Rodriguez-Pinilla et al, 2013). Furthermore, p-STAT3 and p-STAT6 expression correlated with the presence of p52, a member of the alternative NF-kB-pathway that plays an important role in PTCL pathogenesis. Simultaneous activation of the NF-kB and JAK/STAT pathways has also been found in other T-cell lymphoma subtypes, such as CTCL (Odqvist et al, 2013). In the present series, which mainly comprises AITL and nodal PTCL-NOS, the proportion of mutated cases is lower than that of cases showing activation of the pathway, as indicated by the phosphorylation of either JAK or STAT proteins. This implies the existence of additional alternative mechanisms of JAK/STAT-pathway activation, a finding also observed in other studies performed in other T-cell lymphoma subtypes (Nicolae et al, 2014; Crescenzo et al, 2015; Perez et al, 2015). Considered together, these results indicate that JAK/STAT-pathway activation in nodal PTCL patients could be mechanistically and clinically significant, and suggest there may be a potential benefit from the specific inhibition of these targets. This needs further investigation in larger series of patients. We are indebted to the patients who contributed to this study and to the hospitals who supplied the samples. We acknowledge the Biobanks of the CNIO (RD09/0076/00113), IDIVAL-HUMV (RD09/0076/00076), Hospital Universitario 12 de Octubre (RD09/0076/00118), CHUVI (RD09/0076/00011) and FJD (PT13/0010/0012) for their help in collecting the samples, especially Laura Cereceda. We thank Valentín Calvo for his efficiency in providing us with important papers as background to our work. This work was supported by grants from the Instituto de Salud Carlos III, from Ministerio de Economía, Industria y Competitividad (RTICC RD06/0020/0107, RD12/0036/0060, PI 12/1682, PT13/0010/0007, PI16/01294, SAF2013-47416-R, CIBERONC-ISCIII, PIE15/0081, ISCIII-MINECO AES-FEDER (Plan Estatal I+D+I 2013-2016): PI14/00221 and PIE14/0064)) and the Asociación Española Contra el Cáncer, Spain. JG-R is a recipient of an iPFIS predoctoral fellowship (IFI14/00003) from ISCIII-MINECO-AES-FEDER (Plan Estatal I+D+I 2013-2016). MSB was supported by a Miguel Servet contract (CP11/00018) from the ISCIII-MINECO-AES-FEDER (Plan Nacional I+D+I 2008-2011), and currently holds a Miguel Servet II contract (CPII16/00024), supported by ISCIII-MINECO-AES-FEDER (Plan Estatal I+D+I 2013-2016) and the Fundación de Investigación Biomédica Puerta de Hierro. The Instituto de Investigación Marqués de Valdecilla (IDIVAL) is partly funded by the Sociedad para el Desarrollo Regional de Cantabria (SODERCAN). None of the authors reports any conflict of interest. MAP and SMR-P conceived the study. MAP and SMR-P designed the study. FR, MM, MG-C and JM provided samples and/or patients' clinical data. RM, MS-B, JG-R, SG, MAP and SMR-P performed the experiments and/or analysed data. RM, MAP and SMR-P wrote the manuscript. The authors declare no competing financial interests. Table SI. Panel of antibodies used in this series. Table SII. Genes analyzed using the AmpliSeq tool and the Ion Proton sequencer. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
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