April 28, 2024
Peroxisome biogenesis initiated by protein phase separation – Nature

Peroxisome biogenesis initiated by protein phase separation – Nature

  • Zalckvar, E. & Schuldiner, M. Beyond rare disorders: a new era for peroxisomal pathophysiology. Mol. Cell 82, 2228–2235 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ganesan, I., Shi, L. X., Labs, M. & Theg, S. M. Evaluating the functional pore size of chloroplast TOC and TIC protein translocons: import of folded proteins. Plant Cell 30, 2161–2173 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Walton, P. A., Hill, P. E. & Subramani, S. Import of stably folded proteins into peroxisomes. Mol. Biol. Cell 6, 675–683 (1995).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meinecke, M. et al. The peroxisomal importomer constitutes a large and highly dynamic pore. Nat. Cell Biol. 12, 273–277 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Martin, E. W. et al. Valence and patterning of aromatic residues determine the phase behavior of prion-like domains. Science 367, 694–699 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, J. et al. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell 174, 688–699 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Erdmann, R. & Schliebs, W. Peroxisomal matrix protein import: the transient pore model. Nat. Rev. Mol. Cell Biol. 6, 738–742 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gatto, G. J. Jr, Geisbrecht, B. V., Gould, S. J. & Berg, J. M. Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat. Struct. Biol. 7, 1091–1095 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Elgersma, Y. et al. The SH3 domain of the Saccharomyces cerevisiae peroxisomal membrane protein Pex13p functions as a docking site for Pex5p, a mobile receptor for the import PTS1-containing proteins. J. Cell Biol. 135, 97–109 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Erdmann, R. & Blobel, G. Identification of Pex13p a peroxisomal membrane receptor for the PTS1 recognition factor. J. Cell Biol. 135, 111–121 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Albertini, M. et al. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 89, 83–92 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Brocard, C., Lametschwandtner, G., Koudelka, R. & Hartig, A. Pex14p is a member of the protein linkage map of Pex5p. EMBO J. 16, 5491–5500 (1997).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Francisco, T. et al. Protein transport into peroxisomes: knowns and unknowns. Bioessays https://doi.org/10.1002/bies.201700047 (2017).

  • Frey, S., Richter, R. P. & Görlich, D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314, 815–817 (2006).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Celetti, G. et al. The liquid state of FG-nucleoporins mimics permeability barrier properties of nuclear pore complexes. J. Cell Biol. https://doi.org/10.1083/jcb.201907157 (2020).

  • Paci, G., Caria, J. & Lemke, E. A. Cargo transport through the nuclear pore complex at a glance. J. Cell Sci. 134, jcs247874 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Barros-Barbosa, A. et al. The intrinsically disordered nature of the peroxisomal protein translocation machinery. FEBS J. 286, 24–38 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Emmanouilidis, L., Gopalswamy, M., Passon, D. M., Wilmanns, M. & Sattler, M. Structural biology of the import pathways of peroxisomal matrix proteins. Biochim. Biophys. Acta 1863, 804–813 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gould, S. J. & Collins, C. S. Opinion: peroxisomal-protein import: is it really that complex. Nat. Rev. Mol. Cell Biol. 3, 382–389 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Carvalho, A. F. et al. The N-terminal half of the peroxisomal cycling receptor Pex5p is a natively unfolded domain. J. Mol. Biol. 356, 864–875 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lancaster, A. K., Nutter-Upham, A., Lindquist, S. & King, O. D. PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition. Bioinformatics 30, 2501–2502 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hoepfner, D., van den Berg, M., Philippsen, P., Tabak, H. F. & Hettema, E. H. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155, 979–990 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yofe, I. et al. Pex35 is a regulator of peroxisome abundance. J. Cell Sci. 130, 791–804 (2017).

    CAS 
    PubMed 

    Google Scholar
     

  • DeLoache, W. C., Russ, Z. N. & Dueber, J. E. Towards repurposing the yeast peroxisome for compartmentalizing heterologous metabolic pathways. Nat. Commun. 7, 11152 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bremer, A. et al. Deciphering how naturally occurring sequence features impact the phase behaviours of disordered prion-like domains. Nat. Chem. 14, 196–207 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Huh, W. K. et al. Global analysis of protein localization in budding yeast. Nature 425, 686–691 (2003).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Nishimasu, H. et al. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156, 935–949 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bergeron-Sandoval, L. P. et al. Endocytic proteins with prion-like domains form viscoelastic condensates that enable membrane remodeling. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.2113789118 (2021).

  • Cooper, J. T. & Harris, J. M. Imaging fluorescence-correlation spectroscopy for measuring fast surface diffusion at liquid/solid interfaces. Anal. Chem. 86, 7618–7626 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Singh, A. P. & Wohland, T. Applications of imaging fluorescence correlation spectroscopy. Curr. Opin. Chem. Biol. 20, 29–35 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shuang, B., Chen, J., Kisley, L. & Landes, C. F. Troika of single particle tracking programing: SNR enhancement, particle identification, and mapping. Phys. Chem. Chem. Phys. 16, 624–634 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Slaughter, B. D., Schwartz, J. W. & Li, R. Mapping dynamic protein interactions in MAP kinase signaling using live-cell fluorescence fluctuation spectroscopy and imaging. Proc. Natl Acad. Sci. USA 104, 20320–20325 (2007).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cherry, J. M. et al. Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 40, D700–705 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bacia, K., Kim, S. A. & Schwille, P. Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 3, 83–89 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kisley, L. et al. Characterization of porous materials by fluorescence correlation spectroscopy super-resolution optical fluctuation imaging. ACS Nano 9, 9158–9166 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ouyang, M. et al. Liquid-liquid phase transition drives intra-chloroplast cargo sorting. Cell 180, 1144–1159 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gould, S. J. et al. Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTs1 receptor. J. Cell Biol. 135, 85–95 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Girzalsky, W. et al. Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J. Cell Biol. 144, 1151–1162 (1999).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kerssen, D. et al. Membrane association of the cycling peroxisome import receptor Pex5p. J. Biol. Chem. 281, 27003–27015 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Banjade, S. & Rosen, M. K. Phase transitions of multivalent proteins can promote clustering of membrane receptors. Elife 3, e04123 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gaussmann, S. et al. Membrane interactions of the peroxisomal proteins PEX5 and PEX14. Front. Cell Dev. Biol. 9, 651449 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Feng, P. et al. A peroxisomal ubiquitin ligase complex forms a retrotranslocation channel. Nature 607, 374–380 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pedrosa, A. G. et al. Peroxisomal monoubiquitinated PEX5 interacts with the AAA ATPases PEX1 and PEX6 and is unfolded during its dislocation into the cytosol. J. Biol. Chem. 293, 11553–11563 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gao, Y., Skowyra, M. L., Feng, P. & Rapoport, T. A. Protein import into peroxisomes occurs through a nuclear pore-like phase. Science 378, eadf3971 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lazard, M., Blanquet, S., Fisicaro, P., Labarraque, G. & Plateau, P. Uptake of selenite by Saccharomyces cerevisiae involves the high and low affinity orthophosphate transporters. J. Biol. Chem. 285, 32029–32037 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Felice, M. R. et al. Post-transcriptional regulation of the yeast high affinity iron transport system. J. Biol. Chem. 280, 22181–22190 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Salomons, F. A., Kiel, J. A., Faber, K. N., Veenhuis, M. & van der Klei, I. J. Overproduction of Pex5p stimulates import of alcohol oxidase and dihydroxyacetone synthase in a Hansenula polymorpha Pex14 null mutant. J. Biol. Chem. 275, 12603–12611 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Steinberg, S. et al. The PEX Gene Screen: molecular diagnosis of peroxisome biogenesis disorders in the Zellweger syndrome spectrum. Mol. Genet. Metab. 83, 252–263 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ebberink, M. S. et al. Genetic classification and mutational spectrum of more than 600 patients with a Zellweger syndrome spectrum disorder. Hum. Mutat. 32, 59–69 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jansen, R. L. M., Santana-Molina, C., van den Noort, M., Devos, D. P. & van der Klei, I. J. Comparative genomics of peroxisome biogenesis proteins: making sense of the PEX proteins. Front. Cell Dev. Biol. 9, 654163 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yofe, I. et al. One library to make them all: streamlining the creation of yeast libraries via a SWAp-Tag strategy. Nat. Methods 13, 371–378 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sherman, F. Getting started with yeast. Methods Enzymol. 194, 3–21 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shaw, W. M. et al. Engineering a model cell for rational tuning of GPCR signaling. Cell 177, 782–796 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Davis, N. G., Horecka, J. L. & Sprague, G. F. Jr. Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122, 53–65 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mascle, X. H. et al. Acetylation of SUMO1 alters interactions with the SIMs of PML and Daxx in a protein-specific manner. Structure 28 157–168 (2020).

  • Ceballos, A. V., McDonald, C. J. & Elbaum-Garfinkle, S. Methods and strategies to quantify phase separation of disordered proteins. Methods Enzymol. 611, 31–50 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

  • Kisley L. PeroxisomeCorrelationMain_LK20221006.m Zenodo https://doi.org/10.5281/zenodo.7702794 (2023).

  • Xavier-Castellanos-Girouard. Xavier-Castellanos-Girouard/Peroxisome-biogenesis-initiated-by-protein-phase-separation: Droplet_Fusion v0.1. Zenodo https://doi.org/10.5281/zenodo.7702890 (2023).

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