Imaging correlates of leukocyte accumulation and CXCR4/CXCL12 in multiple sclerosis

Arch Neurol. 2009 Jan;66(1):44-53. doi: 10.1001/archneurol.2008.512.

Abstract

Objective: To compare leukocyte accumulation and expression of the chemokine receptor/ligand pair CXCR4/CXCL12 in magnetic resonance imaging-defined regions of interest (ROIs) in brains from patients with chronic multiple sclerosis. We studied the following ROIs: normal-appearing white matter (NAWM); regions abnormal only on T2-weighted images (T2 only); and regions abnormal on T2- and T1-weighted images with an abnormal magnetization transfer ratio (T2/T1/MTR).

Design: Case-control study.

Setting: Cleveland Clinic.

Patients: Brain tissue was acquired from 5 patients with secondary progressive multiple sclerosis (MS) and 5 nonneurological controls.

Intervention: Magnetic resonance imaging pathological correlations were performed on the 5 cases. Based on imaging characteristics, 30 ROIs were excised.

Main outcome measure: Using immunohistochemical analysis, we evaluated myelin status, leukocyte accumulation, and CXCR4/CXCL12 expression in the MS ROIs and white matter regions from the 5 nonneurological controls.

Results: Eight of 10 T2/T1/MTR regions were chronic active or chronic inactive demyelinated lesions, whereas only 2 of 10 T2-only regions were demyelinated and characterized as active or chronic active lesions. Equivalent numbers of CD68+ leukocytes (the predominant cell type) were present in myelinated T2-only regions as compared with NAWM. Parenchymal T cells were significantly increased in T2/T1/MTR ROIs as compared with T2-only regions and NAWM. Expression of CXCR4 and phospho-CXCR4 were found on reactive microglia and macrophages in T2-only and T2/T1/MTR lesions. CXCL12 immunoreactivity was detected in astrocytes, astrocytic processes, and vascular elements in inflamed MS lesions.

Conclusions: Inflammatory leukocyte accumulation was not increased in myelinated MS ROIs with abnormal T2 signal as compared with NAWM. Robust expression of CXCR4/CXCL12 on inflammatory elements in MS lesions highlights a role of this chemokine/receptor pair in central nervous system inflammation.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Aged
  • Aged, 80 and over
  • Astrocytes / immunology
  • Astrocytes / pathology
  • Biomarkers
  • Central Nervous System / immunology
  • Central Nervous System / pathology*
  • Central Nervous System / physiopathology
  • Chemokine CXCL12 / analysis
  • Chemokine CXCL12 / immunology*
  • Chemotaxis, Leukocyte / immunology*
  • Disease Progression
  • Female
  • Humans
  • Inflammation / immunology
  • Inflammation / pathology
  • Leukocytes / pathology*
  • Macrophages / immunology
  • Macrophages / pathology
  • Magnetic Resonance Imaging
  • Male
  • Microglia / immunology
  • Microglia / pathology
  • Middle Aged
  • Multiple Sclerosis / diagnosis*
  • Multiple Sclerosis / immunology
  • Multiple Sclerosis / physiopathology
  • Nerve Fibers, Myelinated / immunology
  • Nerve Fibers, Myelinated / pathology
  • Predictive Value of Tests
  • Receptors, CXCR4 / analysis
  • Receptors, CXCR4 / immunology*

Substances

  • Biomarkers
  • CXCL12 protein, human
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Receptors, CXCR4