Peripheral T-cell lymphoma emerging in a patient with aggressive polymyositis: molecular evidence for neoplastic transformation of an oligoclonal T-cell infiltrate

Acta Neuropathol. 2013 Oct;126(4):595-601. doi: 10.1007/s00401-013-1164-z. Epub 2013 Aug 13.

Abstract

We report a rare case of peripheral T-cell lymphoma arising in a 52-year-old man with biopsy-proven aggressive polymyositis, who had cardiac involvement, progressive bulbar symptoms, and died 11 months post diagnosis due to multiorgan failure. Using a multimodality approach including immunohistochemistry, genome-wide single nucleotide polymorphism (SNP)-array analysis, and high-throughput sequencing of the complementary determining region 3 (CDR3) of T-cell receptor beta (TCRβ) genes, our study demonstrates a molecular link between polymyositis and T-cell lymphoma, and provides evidence of the rapid and possibly late occurrence of genomic instability during neoplastic transformation of an oligoclonal T-cell population. Immunohistochemical analysis revealed loss of CD5, CD7, and CD8 antigen expression in autopsy tissue samples, as well as the occurrence of aberrant CD56 expression, not seen in pre-mortem biopsies, supporting the emergence of a neoplastic T-cell population. Multiplex polymerase chain reaction and next-generation sequencing of the TCRβ CDR3 region displayed two unique T-cell clones in both the diagnostic biopsy confirming polymyositis and the autopsy muscle tissue exhibiting T-cell lymphoma, linking the two pathological processes. SNP-array analysis revealed complex genomic abnormalities at autopsy but not in the pre-mortem muscle biopsies displaying polymyositis, confirming malignant transformation of the oligoclonal T-cell infiltrate. Our findings raise the possibility that clinically aggressive polymyositis might represent a preneoplastic condition in some instances, similar to certain other autoimmune and inflammatory disorders.

Publication types

  • Case Reports

MeSH terms

  • Antigens, CD / biosynthesis
  • Antigens, CD / genetics
  • Autopsy
  • Base Sequence
  • Brain / pathology
  • Cardiomegaly / pathology
  • Cell Transformation, Neoplastic / pathology*
  • Fatal Outcome
  • Humans
  • Immunohistochemistry
  • Lymphoma, T-Cell, Peripheral / complications*
  • Lymphoma, T-Cell, Peripheral / pathology*
  • Male
  • Middle Aged
  • Molecular Sequence Data
  • Muscle Weakness / etiology
  • Muscle, Skeletal / pathology
  • Muscular Atrophy / pathology
  • Myocardium / pathology
  • Polymerase Chain Reaction
  • Polymorphism, Single Nucleotide
  • Polymyositis / complications*
  • Polymyositis / pathology
  • Sequence Analysis, DNA
  • T-Lymphocytes / pathology*

Substances

  • Antigens, CD