Tysnd1 deficiency in mice interferes with the peroxisomal localization of PTS2 enzymes, causing lipid metabolic abnormalities and male infertility

PLoS Genet. 2013;9(2):e1003286. doi: 10.1371/journal.pgen.1003286. Epub 2013 Feb 14.

Abstract

Peroxisomes are subcellular organelles involved in lipid metabolic processes, including those of very-long-chain fatty acids and branched-chain fatty acids, among others. Peroxisome matrix proteins are synthesized in the cytoplasm. Targeting signals (PTS or peroxisomal targeting signal) at the C-terminus (PTS1) or N-terminus (PTS2) of peroxisomal matrix proteins mediate their import into the organelle. In the case of PTS2-containing proteins, the PTS2 signal is cleaved from the protein when transported into peroxisomes. The functional mechanism of PTS2 processing, however, is poorly understood. Previously we identified Tysnd1 (Trypsin domain containing 1) and biochemically characterized it as a peroxisomal cysteine endopeptidase that directly processes PTS2-containing prethiolase Acaa1 and PTS1-containing Acox1, Hsd17b4, and ScpX. The latter three enzymes are crucial components of the very-long-chain fatty acids β-oxidation pathway. To clarify the in vivo functions and physiological role of Tysnd1, we analyzed the phenotype of Tysnd1(-/-) mice. Male Tysnd1(-/-) mice are infertile, and the epididymal sperms lack the acrosomal cap. These phenotypic features are most likely the result of changes in the molecular species composition of choline and ethanolamine plasmalogens. Tysnd1(-/-) mice also developed liver dysfunctions when the phytanic acid precursor phytol was orally administered. Phyh and Agps are known PTS2-containing proteins, but were identified as novel Tysnd1 substrates. Loss of Tysnd1 interferes with the peroxisomal localization of Acaa1, Phyh, and Agps, which might cause the mild Zellweger syndrome spectrum-resembling phenotypes. Our data established that peroxisomal processing protease Tysnd1 is necessary to mediate the physiological functions of PTS2-containing substrates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biological Transport
  • Cysteine Endopeptidases / genetics*
  • Humans
  • Infertility, Male / genetics*
  • Infertility, Male / metabolism
  • Lipid Metabolism / genetics*
  • Male
  • Mice
  • Oxidation-Reduction
  • Peroxisomal Targeting Signal 2 Receptor
  • Peroxisomes / metabolism*
  • Protein Sorting Signals / genetics
  • Receptors, Cytoplasmic and Nuclear* / genetics
  • Receptors, Cytoplasmic and Nuclear* / metabolism
  • Serine Endopeptidases
  • Serine Proteases / genetics
  • Serine Proteases / metabolism

Substances

  • Peroxisomal Targeting Signal 2 Receptor
  • Protein Sorting Signals
  • Receptors, Cytoplasmic and Nuclear
  • Serine Proteases
  • Serine Endopeptidases
  • Tysnd1 protein, human
  • Tysnd1 protein, mouse
  • Cysteine Endopeptidases

Grants and funding

This work was supported in part by grants-in-aid of the KAKEN-HI from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT); Genome Network Project; Innovative Cell Biology by Innovative Technology and Support Project; and a grant of Strategic Research Center in Private Universities from the MEXT to Saitama Medical University Research Center for Genomic Medicine and ONO Medical Research Foundation to Yasushi Okazaki. This work was also supported by grants from MEXT commissioned research under LP-RR (Research Revolution) 2002 Program, Ministry of Education Singapore (RG80/07), and Nanyang Technological University (SUG 13/07) to Christian Schönbach, and Saitama Medical University internal grant (23-1-1-10) to Yumi Mizuno. Yumi Mizuno is a recipient of the Saitama Medical University Research Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.