Mitochondrial PITRM1 peptidase loss-of-function in childhood cerebellar atrophy

  • J Med Genet. 2018 Sep;55(9):599-606. doi: 10.1136/jmedgenet-2018-105330.
Yeshaya Langer  #  1 Adi Aran  #  2 Suleyman Gulsuner  3 Bassam Abu Libdeh  4 Paul Renbaum  5 Dario Brunetti  6  7 Pedro-Filipe Teixeira  8 Tom Walsh  3 Sharon Zeligson  5 Roberta Ruotolo  9 Rachel Beeri  5 Imad Dweikat  4 Maher Shahrour  4 Ariella Weinberg-Shukron  5 Fouad Zahdeh  5 Enrico Baruffini  9 Elzbieta Glaser  8 Mary-Claire King  3 Ephrat Levy-Lahad  10 Massimo Zeviani  6 Reeval Segel  11
Affiliations
  • 1. Department of Pediatrics, Shaare Zedek Medical Center, Jerusalem, Israel.
  • 2. Department of Pediatrics, Neuropediatrics Unit, Shaare Zedek Medical Center and Hebrew University-Hadassah School of Medicine, Jerusalem, Israel.
  • 3. Departments of Medicine and Genome Sciences, University of Washington, Seattle, Washington, USA.
  • 4. Departments of Pediatrics and Genetics, Makassed Hospital, Al-Quds University, Jerusalem, Israel.
  • 5. Medical Genetics Institute, Shaare Zedek Medical Center, Jerusalem, Israel.
  • 6. MRC Mitochondrial Biology Unit, University of Cambridge, Cambridge, UK.
  • 7. Department of Medical Biotechnology and Translational Medicine, University of Milan, Milan, Italy.
  • 8. Department of Biochemistry and Biophysics, Arrhenius Laboratories for Natural Sciences, Stockholm University, Stockholm, Sweden.
  • 9. Department of Chemistry, Life Sciences, and Environmental Sustainability, University of Parma, Parma, Italy.
  • 10. Medical Genetics Institute, Shaare Zedek Medical Center, Hebrew University-Hadassah School of Medicine, Jerusalem, Israel.
  • 11. Department of Pediatrics, Medical Genetics Institute, Shaare Zedek Medical Center, Hebrew University-Hadassah School of Medicine, Jerusalem, Israel.
  • # Contributed equally.
Abstract

Objective: To identify the genetic basis of a childhood-onset syndrome of variable severity characterised by progressive spinocerebellar ataxia, mental retardation, psychotic episodes and cerebellar atrophy.

Methods: Identification of the underlying mutations by whole exome and whole genome Sequencing. Consequences were examined in patients' cells and in yeast.

Results: Two brothers from a consanguineous Palestinian family presented with progressive spinocerebellar ataxia, mental retardation and psychotic episodes. Serial brain imaging showed severe progressive cerebellar atrophy. Whole exome Sequencing revealed a novel mutation: pitrilysin metallopeptidase 1 (PITRM1) c.2795C>T, p.T931M, homozygous in the affected children and resulting in 95% reduction in PITRM1 protein. Whole genome Sequencing revealed a chromosome X structural rearrangement that also segregated with the disease. Independently, two siblings from a second Palestinian family presented with similar, somewhat milder symptoms and the same PITRM1 mutation on a shared haplotype. PITRM1T931M carrier frequency was 0.027 (3/110) in the village of the first family evaluated, and 0/300 among Palestinians from Other locales. PITRM1 is a mitochondrial matrix enzyme that degrades 10-65 amino acid oligopeptides, including the mitochondrial fraction of amyloid-beta peptide. Analysis of peptide cleavage activity by the PITRM1T931M protein revealed a significant decrease in the degradation capacity specifically of peptides ≥40 Amino acids.

Conclusion: PITRM1T931M results in childhood-onset recessive cerebellar pathology. Severity of PITRM1-related disease may be affected by the degree of impairment in cleavage of mitochondrial long peptides. Disruption and deletion of X linked regulatory segments may also contribute to severity.

Keywords
PITML; cerebellar atrophy; mitochondria; next generation sequencing; whole exome sequencing.