Imaging Transcriptomics of Brain Functional Alterations in MS and Neuromyelitis Optica Spectrum Disorder

AJNR Am J Neuroradiol. 2024 Dec 9;45(12):1901-1909. doi: 10.3174/ajnr.A8480.

Abstract

Background and purpose: The underlying transcriptomic signatures driving brain functional alterations in MS and neuromyelitis optica spectrum disorder (NMOSD) are still unclear.

Materials and methods: Regional fractional amplitude of low-frequency fluctuation (fALFF) values were obtained and compared among 209 patients with MS, 90 patients with antiaquaporin-4 antibody (AQP4)+ NMOSD, 49 with AQP4- NMOSD, and 228 healthy controls from a discovery cohort. We used partial least squares (PLS) regression to identify the gene transcriptomic signatures associated with disease-related fALFF alterations. The biologic process and cell type-specific signature of the identified PLS genes were explored by enrichment analysis. The correlation between PLS genes and clinical variables was explored. A prospective independent cohort was used to validate the brain fALFF alterations and the repeatability of identified genes.

Results: MS, AQP4+ NMOSD, and AQP4- NMOSD showed decreased fALFF in cognition-related regions and deep gray matter, while NMOSD (both AQP4+ and AQP4-) additionally demonstrated lower fALFF in the visual region. The overlapping PLS1- genes (indicating that the genes were overexpressed as regional fALFF decreased) were enriched in response to regulation of the immune response in all diseases, and the PLS1- genes were specifically enriched in the epigenetics profile in MS, membrane disruption and cell adhesion in AQP4+ NMOSD, and leukocyte activation in AQP4- NMOSD. For the cell type transcriptional signature, microglia and astrocytes accounted for the decreased fALFF. The fALFF-associated PLS1- genes directly correlated with Expanded Disability Status Scale of MS and disease duration across disorders.

Conclusions: We revealed the functional activity alterations and their underlying shared and specific gene transcriptional signatures in MS, AQP4+ NMOSD, and AQP4- NMOSD.

MeSH terms

  • Adult
  • Aquaporin 4 / genetics
  • Brain / diagnostic imaging
  • Female
  • Gene Expression Profiling
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Multiple Sclerosis* / diagnostic imaging
  • Multiple Sclerosis* / genetics
  • Neuromyelitis Optica* / diagnostic imaging
  • Neuromyelitis Optica* / genetics
  • Neuromyelitis Optica* / physiopathology
  • Prospective Studies
  • Transcriptome*

Substances

  • Aquaporin 4
  • AQP4 protein, human