CNS Langerhans cell histiocytosis: Common hematopoietic origin for LCH-associated neurodegeneration and mass lesions

Cancer. 2018 Jun 15;124(12):2607-2620. doi: 10.1002/cncr.31348. Epub 2018 Apr 6.

Abstract

Background: Central nervous system Langerhans cell histiocytosis (CNS-LCH) brain involvement may include mass lesions and/or a neurodegenerative disease (LCH-ND) of unknown etiology. The goal of this study was to define the mechanisms of pathogenesis that drive CNS-LCH.

Methods: Cerebrospinal fluid (CSF) biomarkers including CSF proteins and extracellular BRAFV600E DNA were analyzed in CSF from patients with CNS-LCH lesions compared with patients with brain tumors and other neurodegenerative conditions. Additionally, the presence of BRAFV600E was tested in peripheral mononuclear blood cells (PBMCs) as well as brain biopsies from LCH-ND patients, and the response to BRAF-V600E inhibitor was evaluated in 4 patients with progressive disease.

Results: Osteopontin was the only consistently elevated CSF protein in patients with CNS-LCH compared with patients with other brain pathologies. BRAFV600E DNA was detected in CSF of only 2/20 (10%) cases, both with LCH-ND and active lesions outside the CNS. However, BRAFV600E+ PBMCs were detected with significantly higher frequency at all stages of therapy in LCH patients who developed LCH-ND. Brain biopsies of patients with LCH-ND demonstrated diffuse perivascular infiltration by BRAFV600E+ cells with monocyte phenotype (CD14+ CD33+ CD163+ P2RY12- ) and associated osteopontin expression. Three of 4 patients with LCH-ND treated with BRAF-V600E inhibitor experienced significant clinical and radiologic improvement.

Conclusion: In LCH-ND patients, BRAFV600E+ cells in PBMCs and infiltrating myeloid/monocytic cells in the brain is consistent with LCH-ND as an active demyelinating process arising from a mutated hematopoietic precursor from which LCH lesion CD207+ cells are also derived. Therapy directed against myeloid precursors with activated MAPK signaling may be effective for LCH-ND. Cancer 2018;124:2607-20. © 2018 American Cancer Society.

Keywords: BRAF-V600E; CNS neoplasms; Langerhans cell histiocytosis; neurodegeneration; osteopontin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Biomarkers / blood
  • Biomarkers / cerebrospinal fluid
  • Biopsy
  • Brain / pathology
  • Brain Neoplasms / cerebrospinal fluid
  • Brain Neoplasms / diagnosis*
  • Brain Neoplasms / genetics
  • Brain Neoplasms / pathology
  • Child
  • Child, Preschool
  • Diagnosis, Differential
  • Female
  • Hematopoietic Stem Cells / pathology
  • Histiocytosis, Langerhans-Cell / cerebrospinal fluid
  • Histiocytosis, Langerhans-Cell / diagnosis*
  • Histiocytosis, Langerhans-Cell / genetics
  • Histiocytosis, Langerhans-Cell / pathology
  • Humans
  • Infant
  • Infant, Newborn
  • Leukocytes, Mononuclear / pathology
  • MAP Kinase Signaling System
  • Male
  • Neurodegenerative Diseases / cerebrospinal fluid
  • Neurodegenerative Diseases / diagnosis*
  • Neurodegenerative Diseases / genetics
  • Neurodegenerative Diseases / pathology
  • Osteopontin / cerebrospinal fluid*
  • Proto-Oncogene Proteins B-raf / antagonists & inhibitors
  • Proto-Oncogene Proteins B-raf / genetics*
  • Retrospective Studies
  • Young Adult

Substances

  • Biomarkers
  • SPP1 protein, human
  • Osteopontin
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf