PTBP1 acts as a dominant repressor of the aberrant tissue-specific splicing of ISCU in hereditary myopathy with lactic acidosis

Mol Genet Genomic Med. 2018 Nov;6(6):887-897. doi: 10.1002/mgg3.413. Epub 2018 Sep 12.

Abstract

Background: Hereditary myopathy with lactic acidosis (HML) is an autosomal recessive disease caused by an intron mutation in the iron-sulfur cluster assembly (ISCU) gene. The mutation results in aberrant splicing, where part of the intron is retained in the final mRNA transcript, giving rise to a truncated nonfunctional ISCU protein. Using an ISCU mini-gene system, we have previously shown that PTBP1 can act as a repressor of the mis-splicing of ISCU, where overexpression of PTBP1 resulted in a decrease of the incorrect splicing. In this study, we wanted to, in more detail, analyze the role of PTBP1 in the regulation of endogenous ISCU mis-splicing.

Methods: Overexpression and knockdown of PTBP1 was performed in myoblasts from two HML patients and a healthy control. Quantification of ISCU mis-splicing was done by qRTPCR. Biotinylated ISCU RNA, representing wildtype and mutant intron sequence, was used in a pull-down assay with nuclear extracts from myoblasts. Levels of PTBP1 in human cell lines and mice tissues were analyzed by qRTPCR and western blot.

Results: PTBP1 overexpression in HML patient myoblasts resulted in a substantial decrease of ISCU mis-splicing while knockdown of PTBP1 resulted in a drastic increase. The effect could be observed in both patient and control myoblasts. We could also show that PTBP1 interacts with both the mutant and wild-type ISCU intron sequence, but with a higher affinity to the mutant sequence. Furthermore, low levels of PTBP1 among examined mouse tissues correlated with high levels of incorrect splicing of ISCU.

Conclusion: Our results show that PTBP1 acts as a dominant repressor of ISCU mis-splicing. We also show an inverse correlation between the levels of PTBP1 and ISCU mis-splicing, suggesting that the high level of mis-splicing in the skeletal muscle is primarily due to the low levels of PTBP1.

Keywords: ISCU; PTBP1; alternative splicing; hereditary myopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acidosis, Lactic / congenital*
  • Acidosis, Lactic / genetics
  • Animals
  • Cells, Cultured
  • Genes, Dominant
  • HEK293 Cells
  • Heterogeneous-Nuclear Ribonucleoproteins / genetics*
  • Heterogeneous-Nuclear Ribonucleoproteins / metabolism
  • Humans
  • Iron-Sulfur Proteins / genetics*
  • Iron-Sulfur Proteins / metabolism
  • Mice
  • Mice, Inbred CBA
  • Muscular Diseases / congenital*
  • Muscular Diseases / genetics
  • Myoblasts / metabolism
  • Polypyrimidine Tract-Binding Protein / genetics*
  • Polypyrimidine Tract-Binding Protein / metabolism
  • RNA Splicing*
  • Suppression, Genetic

Substances

  • Heterogeneous-Nuclear Ribonucleoproteins
  • Iron-Sulfur Proteins
  • IscU protein, mouse
  • Ptbp1 protein, mouse
  • Polypyrimidine Tract-Binding Protein

Supplementary concepts

  • Myopathy with Lactic Acidosis, Hereditary