Distinct molecular mechanisms of HTRA1 mutants in manifesting heterozygotes with CARASIL

Neurology. 2016 May 24;86(21):1964-74. doi: 10.1212/WNL.0000000000002694. Epub 2016 Apr 27.

Abstract

Objective: To elucidate the molecular mechanism of mutant HTRA1-dependent cerebral small vessel disease in heterozygous individuals.

Methods: We recruited 113 unrelated index patients with clinically diagnosed cerebral small vessel disease. The coding sequences of the HTRA1 gene were analyzed. We evaluated HTRA1 protease activities using casein assays and oligomeric HTRA1 formation using gel filtration chromatography.

Results: We found 4 heterozygous missense mutations in the HTRA1 gene (p.G283E, p.P285L, p.R302Q, and p.T319I) in 6 patients from 113 unrelated index patients and in 2 siblings in 2 unrelated families with p.R302Q. The mean age at cognitive impairment onset was 51.1 years. Spondylosis deformans was observed in all cases, whereas alopecia was observed in 3 cases; an autopsied case with p.G283E showed arteriopathy in their cerebral small arteries. These mutant HTRA1s showed markedly decreased protease activities and inhibited wild-type HTRA1 activity, whereas 2 of 3 mutant HTRA1s reported in cerebral autosomal-recessive arteriopathy with subcortical infarcts and leukoencephalopathy (CARASIL) (A252T and V297M) did not inhibit wild-type HTRA1 activity. Wild-type HTRA1 forms trimers; however, G283E and T319I HTRA1, observed in manifesting heterozygotes, did not form trimers. P285L and R302Q HTRA1s formed trimers, but their mutations were located in domains that are important for trimer-associated HTRA1 activation; in contrast, A252T and V297M HTRA1s, which have been observed in CARASIL, also formed trimers but had mutations outside the domains important for trimer-associated HTRA1 activation.

Conclusions: The mutant HTRA1s observed in manifesting heterozygotes might result in an impaired HTRA1 activation cascade of HTRA1 or be unable to form stable trimers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alopecia / diagnostic imaging
  • Alopecia / enzymology*
  • Alopecia / genetics*
  • Alopecia / pathology
  • Brain / diagnostic imaging
  • Brain / enzymology
  • Brain / pathology
  • Cerebral Infarction / diagnostic imaging
  • Cerebral Infarction / enzymology*
  • Cerebral Infarction / genetics*
  • Cerebral Infarction / pathology
  • Chromatography, Gel
  • Dimerization
  • Family
  • Heterozygote*
  • High-Temperature Requirement A Serine Peptidase 1
  • Humans
  • Leukoencephalopathies / diagnostic imaging
  • Leukoencephalopathies / enzymology*
  • Leukoencephalopathies / genetics*
  • Leukoencephalopathies / pathology
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Models, Molecular
  • Mutation, Missense*
  • Pedigree
  • Sequence Analysis, DNA
  • Serine Endopeptidases / genetics*
  • Serine Endopeptidases / metabolism*
  • Spinal Diseases / diagnostic imaging
  • Spinal Diseases / enzymology*
  • Spinal Diseases / genetics*
  • Spinal Diseases / pathology

Substances

  • High-Temperature Requirement A Serine Peptidase 1
  • HTRA1 protein, human
  • Serine Endopeptidases

Supplementary concepts

  • Cerebral Autosomal Recessive Arteriopathy with Subcortical Infarcts and Leukoencephalopathy