Investigating the role of filamin C in Belgian patients with frontotemporal dementia linked to GRN deficiency in FTLD-TDP brains

Belgian Neurology BELNEU, Jonathan Janssens, Stephanie Philtjens, Gernot Kleinberger, Sara Van Mossevelde, Julie van der Zee, Rita Cacace, Sebastiaan Engelborghs, Anne Sieben, Julia Banzhaf-Strathmann, Lubina Dillen, Celine Merlin, Ivy Cuijt, Caroline Robberecht, Bettina Schmid, Patrick Santens, Adrian Ivanoiu, Mathieu Vandenbulcke, Rik Vandenberghe, Patrick CrasPeter P. De Deyn, Jean-Jacques Martin, Stuart Maudsley, Christian Haass, Marc Cruts, Christine Van Broeckhoven*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

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Abstract

TAR DNA-binding protein 43 (TDP-43) inclusions are pathological hallmarks of patients with frontotemporal lobar degeneration (FTLD) and amyotrophic lateral sclerosis (ALS). Loss of TDP-43 in zebrafish engenders a severe muscle and vascular phenotype with a concomitant elevation of filamin C (FLNC) levels, an observation confirmed in the frontal cortex of FTLD-TDP patients. Here, we aimed to further assess the contribution of FLNC to frontotemporal dementia (FTD) etiology. We conducted a mutational screening of FLNC in a cohort of 529 unrelated Belgian FTD and FTD-ALS patients, and a control cohort of 920 unrelated and age-matched individuals. Additionally we performed an in-depth characterization of FLNC expression levels in FTD patients and a murine FTD model.

In total 68 missense variants were identified of which 19 (MAF <1 %) were patient-only. Gene burden analysis demonstrated a significant association between the presence of rare variants in FLNC and disease (P = 0.0349, RR = 1.46 [95 % CI 1.03-2.07]). Furthermore, elevated FLNC expression levels, observed previously in FTLD-TDP patients, were mainly attributable to FTD patients with the progranulin (GRN) p.0(IVS1 + 5G > C) loss-of-function mutation. Increased FLNC levels were, to a lesser extent, also identified in a FLNC p.V831I variant carrier and in FTD patients with the p.R159H mutation in valosin-containing protein (VCP). The GRN-associated increase of FLNC was confirmed in the frontal cortex of aged Grn knockout mice starting at 16-18 months of age. Combined quantitative proteomic and bioinformatic analyses of the frontal cortex of FTD patients possessing elevated FLNC levels, identified multiple altered protein factors involved in accelerated aging, neurodegeneration and synaptogenesis.

Our findings further support the involvement of aberrant FLNC expression levels in FTD pathogenesis. Identification of increased FLNC levels in aged Grn mice and impaired pathways related to aging and neurodegeneration, implies a potential role for FLNC in mediating or accelerating the aging process.

Original languageEnglish
Article number68
Number of pages18
JournalActa Neuropathologica Communications
Volume3
DOIs
Publication statusPublished - 10-Nov-2015

Keywords

  • Filamin C
  • Genetics
  • Frontotemporal lobar degeneration
  • Granulin GRN
  • Haploinsufficiency
  • Proteomics
  • AMYOTROPHIC-LATERAL-SCLEROSIS
  • LOBAR DEGENERATION
  • BINDING PROTEIN
  • HYPERTROPHIC CARDIOMYOPATHY
  • ALZHEIMERS-DISEASE
  • VASCULAR DEMENTIA
  • MUTATIONS
  • MYOPATHY
  • IDENTIFICATION
  • NEUROGRANIN

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