Sézary syndrome originates from heavily mutated hematopoietic progenitors

•CTCL cells arise from mutated hematopoietic stem cells after thymic egression.•Clonally enriched CTCL cells carry these progenitor mutations. [Display omitted] The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 C...

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Published inBlood advances Vol. 7; no. 18; pp. 5586 - 5602
Main Authors Harro, Carly M., Sprenger, Kimberly B., Chaurio, Ricardo A., Powers, John J., Innamarato, Patrick, Anadon, Carmen M., Zhang, Yumeng, Biswas, Subir, Mandal, Gunjan, Mine, Jessica A., Cortina, Carla, Nagy, Mate Z., Martin, Alexandra L., Handley, Katelyn F., Borjas, Gustavo J., Chen, Pei-Ling, Pinilla-Ibarz, Javier, Sokol, Lubomir, Yu, Xiaoqing, Conejo-Garcia, Jose R.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 26.09.2023
The American Society of Hematology
Subjects
Dipeptidyl Peptidase 4
Humans
Lymphoid Neoplasia
Lymphoma, T-Cell, Cutaneous - genetics
Mycosis Fungoides - genetics
Mycosis Fungoides - pathology
Receptors, Antigen, T-Cell
Sezary Syndrome - genetics
Sezary Syndrome - pathology
Skin Neoplasms - genetics
Skin Neoplasms - pathology
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Abstract •CTCL cells arise from mutated hematopoietic stem cells after thymic egression.•Clonally enriched CTCL cells carry these progenitor mutations. [Display omitted] The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and CD26+/CD7+ and 29 932 CD3+CD4+ and CD26−/CD7− lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3+CD4+ and CD26+/CD7+ and 33 841 CD3+CD4+ and CD26−/CD7− lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.
AbstractList •CTCL cells arise from mutated hematopoietic stem cells after thymic egression.•Clonally enriched CTCL cells carry these progenitor mutations. [Display omitted] The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and CD26+/CD7+ and 29 932 CD3+CD4+ and CD26−/CD7− lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3+CD4+ and CD26+/CD7+ and 33 841 CD3+CD4+ and CD26−/CD7− lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.
• CTCL cells arise from mutated hematopoietic stem cells after thymic egression. • Clonally enriched CTCL cells carry these progenitor mutations. The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3 + CD4 + and CD26 + /CD7 + and 29 932 CD3 + CD4 + and CD26 − /CD7 − lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3 + CD4 + and CD26 + /CD7 + and 33 841 CD3 + CD4 + and CD26 − /CD7 − lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.
The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and CD26+/CD7+ and 29 932 CD3+CD4+ and CD26-/CD7- lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3+CD4+ and CD26+/CD7+ and 33 841 CD3+CD4+ and CD26-/CD7- lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.
The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and CD26+/CD7+ and 29 932 CD3+CD4+ and CD26-/CD7- lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3+CD4+ and CD26+/CD7+ and 33 841 CD3+CD4+ and CD26-/CD7- lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and CD26+/CD7+ and 29 932 CD3+CD4+ and CD26-/CD7- lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3+CD4+ and CD26+/CD7+ and 33 841 CD3+CD4+ and CD26-/CD7- lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.
The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and CD26+/CD7+ and 29 932 CD3+CD4+ and CD26−/CD7− lymphocytes from the peripheral blood of 7 patients with CTCL, coupled to single-cell ATAC-sequencing of 26,411 CD3+CD4+ and CD26+/CD7+ and 33 841 CD3+CD4+ and CD26−/CD7− lymphocytes, we show that tumor cells in Sézary syndrome and mycosis fungoides (MF) exhibit different phenotypes and trajectories of differentiation. When compared to MF, Sézary cells exhibit narrower repertoires of TCRs and exhibit clonal enrichment. Surprisingly, we identified ≥200 mutations in hematopoietic stem cells from multiple patients with Sézary syndrome. Mutations in key oncogenes were also present in peripheral Sézary cells, which also showed the hallmarks of recent thymic egression. Together our data suggest that CTCL arises from mutated lymphocyte progenitors that acquire TCRs in the thymus, which complete their malignant transformation in the periphery.
Author Innamarato, Patrick
Mandal, Gunjan
Yu, Xiaoqing
Nagy, Mate Z.
Anadon, Carmen M.
Pinilla-Ibarz, Javier
Borjas, Gustavo J.
Martin, Alexandra L.
Powers, John J.
Handley, Katelyn F.
Harro, Carly M.
Conejo-Garcia, Jose R.
Zhang, Yumeng
Biswas, Subir
Sprenger, Kimberly B.
Chaurio, Ricardo A.
Cortina, Carla
Chen, Pei-Ling
Mine, Jessica A.
Sokol, Lubomir
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  givenname: Ricardo A.
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  organization: Department of Immunology, H. Lee Moffitt Cancer Center & Research Institute, Tampa, FL
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  givenname: Carla
  orcidid: 0000-0002-4353-4008
  surname: Cortina
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  givenname: Mate Z.
  orcidid: 0000-0001-5845-0926
  surname: Nagy
  fullname: Nagy, Mate Z.
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  givenname: Alexandra L.
  surname: Martin
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  surname: Yu
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2023 by The American Society of Hematology. Licensed under Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0), permitting only noncommercial, nonderivative use with attribution. All other rights reserved. 2023 The American Society of Hematology
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Snippet •CTCL cells arise from mutated hematopoietic stem cells after thymic egression.•Clonally enriched CTCL cells carry these progenitor mutations. [Display...
The pathogenesis of cutaneous T-cell lymphoma (CTCL) remains unclear. Using single-cell RNA or T-cell receptor (TCR) sequencing of 32 619 CD3+CD4+ and...
• CTCL cells arise from mutated hematopoietic stem cells after thymic egression. • Clonally enriched CTCL cells carry these progenitor mutations. The...
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SubjectTerms Dipeptidyl Peptidase 4
Humans
Lymphoid Neoplasia
Lymphoma, T-Cell, Cutaneous - genetics
Mycosis Fungoides - genetics
Mycosis Fungoides - pathology
Receptors, Antigen, T-Cell
Sezary Syndrome - genetics
Sezary Syndrome - pathology
Skin Neoplasms - genetics
Skin Neoplasms - pathology
Title Sézary syndrome originates from heavily mutated hematopoietic progenitors
URI https://www.clinicalkey.com/#!/content/1-s2.0-S2473952923004329
https://dx.doi.org/10.1182/bloodadvances.2022008562
https://www.ncbi.nlm.nih.gov/pubmed/37531660
https://www.proquest.com/docview/2845654083
https://pubmed.ncbi.nlm.nih.gov/PMC10514084
Volume 7
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