Anaplastic large cell lymphoma arises in thymocytes and requires transient TCR expression for thymic egress

Tim I.M. Malcolm, Patrick Villarese, Camilla J. Fairbairn, Laurence Lamant, Amélie Trinquand, C. Elizabeth Hook, G. A. Amos Burke, Laurence Brugières, Katherine Hughes, Dominique Payet, Olaf Merkel, Ana Iris Schiefer, Ibraheem Ashankyty, Shahid Mian, Mariusz A. Wasik, Martin Turner, Lukas Kenner, Vahid Asnafi, Elizabeth Macintyre, Suzanne D. Turner

Research output: Contribution to journalArticlepeer-review

67 Scopus citations

Abstract

Anaplastic large cell lymphoma (ALCL) is a peripheral T-cell lymphoma presenting mostly in children and young adults. The natural progression of this disease is largely unknown as is the identity of its true cell of origin. Here we present a model of peripheral ALCL pathogenesis where the malignancy is initiated in early thymocytes, before T-cell receptor (TCR) β-rearrangement, which is bypassed in CD4/NPM-ALK transgenic mice following Notch1 expression. However, we find that a TCR is required for thymic egress and development of peripheral murine tumours, yet this TCR must be downregulated for T-cell lymphomagenesis. In keeping with this, clonal TCR rearrangements in human ALCL are predominantly in-frame, but often aberrant, with clonal TCRα but no comparable clonal TCRβ rearrangement, yielding events that would not normally be permissive for survival during thymic development. Children affected by ALCL may thus harbour thymic lymphoma-initiating cells capable of seeding relapse after chemotherapy.

Original languageEnglish
Article number10087
Pages (from-to)10087
JournalNature Communications
Volume7
DOIs
StatePublished - Jan 12 2016

Keywords

  • Adult
  • Animals
  • CD4 Antigens/metabolism
  • Cell Line, Tumor
  • Child
  • Disease Models, Animal
  • Female
  • Flow Cytometry
  • Gene Rearrangement, T-Lymphocyte
  • Genes, RAG-1/genetics
  • Genes, T-Cell Receptor alpha
  • Genes, T-Cell Receptor beta
  • Humans
  • Immunohistochemistry
  • Jurkat Cells
  • Lymphoma, Large-Cell, Anaplastic/metabolism
  • Male
  • Mice
  • Mice, Transgenic
  • Protein-Tyrosine Kinases/metabolism
  • Receptor, Notch1/metabolism
  • Receptors, Antigen, T-Cell, alpha-beta/genetics
  • Receptors, Antigen, T-Cell/metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Thymocytes/metabolism
  • Thymus Gland/cytology

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