The autophagic degradation of cytosolic pools of peroxisomal proteins by a new selective pathway

References

• Ma C, Agrawal G, Subramani S. Peroxisome assembly: matrix and membrane protein biogenesis. J Cell Biol. 2011;193(1):7–16.
   PubMed Web of Science ®Google Scholar
• Dixit E, Boulant S, Zhang Y, et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell. 2010;141(4):668–681.
   PubMed Web of Science ®Google Scholar
• Terlecky SR, Nuttley WM, McCollum D, et al. The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. Embo J. 1995;14(15):3627–3634.
   PubMed Web of Science ®Google Scholar
• Elgersma Y, Elgersma-Hooisma M, Wenzel T, et al. A mobile PTS2 receptor for peroxisomal protein import in Pichia pastoris. J Cell Biol. 1998;140(4):807–820.
   PubMed Web of Science ®Google Scholar
• Marzioch M, Erdmann R, Veenhuis M, et al. PAS7 encodes a novel yeast member of the WD-40 protein family essential for import of 3-oxoacyl-CoA thiolase, a PTS2-containing protein, into peroxisomes. Embo J. 1994;13(20):4908–4918.
   PubMed Web of Science ®Google Scholar
• Zhang JW, Cai X, Lazarow PB. Peb1p (Pas7p) is an intra-peroxisomal receptor for the N-terminal, type 2, peroxisomal targeting signal of thiolase. Ann N Y Acad Sci. 1996;804:654–655.
   PubMed Web of Science ®Google Scholar
• Leon S, Goodman JM, Subramani S. Uniqueness of the mechanism of protein import into the peroxisome matrix: transport of folded, co-factor-bound and oligomeric proteins by shuttling receptors. Biochim Biophys Acta. 2006;1763(12):1552–1564.
   PubMed Web of Science ®Google Scholar
• Purdue PE, Yang X, Lazarow PB. Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J Cell Biol. 1998;143(7):1859–1869.
   PubMed Web of Science ®Google Scholar
• Ma C, Schumann U, Rayapuram N, et al. The peroxisomal matrix import of Pex8p requires only PTS receptors and Pex14p. Mol Biol Cell. 2009;20(16):3680–3689.
   PubMed Web of Science ®Google Scholar
• Meinecke M, Cizmowski C, Schliebs W, et al. The peroxisomal importomer constitutes a large and highly dynamic pore. Nat Cell Biol. 2010;12(3):273–277.
   PubMed Web of Science ®Google Scholar
• Dammai V, Subramani S. The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol. Cell. 2001;105(2):187–196.
   PubMed Web of Science ®Google Scholar
• Nair DM, Purdue PE, Lazarow PB. Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae. J Cell Biol. 2004;167(4):599–604.
   PubMed Web of Science ®Google Scholar
• Grimm I, Saffian D, Platta HW, et al. The AAA-type ATPases Pex1p and Pex6p and their role in peroxisomal matrix protein import in Saccharomyces cerevisiae. Biochim Biophys Acta. 2012;1823(1):150–158.
   PubMed Web of Science ®Google Scholar
• Platta HW, El Magraoui F, Baumer BE, et al. Pex2 and pex12 function as protein-ubiquitin ligases in peroxisomal protein import. Mol Cell Biol. 2009;29(20):5505–5516.
   PubMed Web of Science ®Google Scholar
• Liu X, Subramani S. Unique requirements for mono- and polyubiquitination of the peroxisomal targeting signal co-receptor, Pex20. J Biol Chem. 2013;288(10):7230–7240.
   PubMed Web of Science ®Google Scholar
• Hagstrom D, Ma C, Guha-Polley S, et al. The unique degradation pathway of the PTS2 receptor, Pex7, is dependent on the PTS receptor/coreceptor, Pex5 and Pex20. Mol Biol Cell. 2014;25(17):2634–2643.
   PubMed Web of Science ®Google Scholar
• Zhang L, Leon S, Subramani S. Two independent pathways traffic the intraperoxisomal peroxin PpPex8p into peroxisomes: mechanism and evolutionary implications. Mol Biol Cell. 2006;17(2):690–699.
   PubMed Web of Science ®Google Scholar
• Farré JC, Subramani S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Biol. 2016;17(9):537–552.
   PubMed Web of Science ®Google Scholar
• Oku M, Sakai Y. Pexophagy in yeasts. Biochim Biophys Acta. 2016;1863(5):992–998.
   PubMed Web of Science ®Google Scholar
• Farré JC, Manjithaya R, Mathewson RD, et al. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell. 2008;14(3):365–376.
   PubMed Web of Science ®Google Scholar
• Nazarko TY, Ozeki K, Till A, et al. Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J Cell Biol. 2014;204(4):541–557.
   PubMed Web of Science ®Google Scholar
• Motley AM, Nuttall JM, Hettema EH. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. Embo J. 2012;31(13):2852–2868.
   PubMed Web of Science ®Google Scholar
• Deosaran E, Larsen KB, Hua R, et al. NBR1 acts as an autophagy receptor for peroxisomes. J Cell Sci. 2013;126(4):939.
   PubMed Web of Science ®Google Scholar
• Kim PK, Hailey DW, Mullen RT, et al. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci U S A. 2008;105(52):20567–20574.
   PubMed Web of Science ®Google Scholar
• Sargent G, van Zutphen T, Shatseva T, et al. PEX2 is the E3 ubiquitin ligase required for pexophagy during starvation. J Cell Biol. 2016;214(6):677–690.
   PubMed Web of Science ®Google Scholar
• Gould SJ, Kalish JE, Morrell JC, et al. Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTS1 receptor. J Cell Biol. 1996;135(1):85–95.
   PubMed Web of Science ®Google Scholar
• Leon S, Zhang L, McDonald WH, et al. Dynamics of the peroxisomal import cycle of PpPex20p: ubiquitin-dependent localization and regulation. J Cell Biol. 2006;172(1):67–78.
   PubMed Web of Science ®Google Scholar
• Dodt G, Gould SJ. Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J Cell Biol. 1996;135(6):1763–1774.
   PubMed Web of Science ®Google Scholar
• Titorenko VI, Smith JJ, Szilard RK, et al. Pex20p of the yeast Yarrowia lipolytica is required for the oligomerization of thiolase in the cytosol and for its targeting to the peroxisome. J Cell Biol. 1998;142(2):403–420.
   PubMed Web of Science ®Google Scholar
• Léon S, Subramani S. A conserved cysteine residue of Pichia pastoris Pex20p is essential for its recycling from the peroxisome to the cytosol. J Biol Chem. 2007;282(10):7424–7430.
   PubMed Web of Science ®Google Scholar
• Ma C, Hagstrom D, Polley SG, et al. Redox-regulated cargo binding and release by the peroxisomal targeting signal receptor, Pex5. J Biol Chem. 2013;288(38):27220–27231.
   PubMed Web of Science ®Google Scholar
• Welter E, Thumm M, Krick R. Quantification of nonselective bulk autophagy in S. cerevisiae using Pgk1-GFP. Autophagy. 2010;6(6):794–797.
   PubMed Web of Science ®Google Scholar
• van Zutphen T, Veenhuis M, van der Klei IJ. Damaged peroxisomes are subject to rapid autophagic degradation in the yeast Hansenula polymorpha. Autophagy. 2011;7(8):863–872.
   PubMed Web of Science ®Google Scholar
• Gunkel K, van Dijk R, Veenhuis M, et al. Routing of Hansenula polymorpha alcohol oxidase: an alternative peroxisomal protein-sorting machinery. Mol Biol Cell. 2004;15(3):1347–1355.
   PubMed Web of Science ®Google Scholar
• Hiltunen JK, Wenzel B, Beyer A, et al. Peroxisomal multifunctional beta-oxidation protein of Saccharomyces cerevisiae. Molecular analysis of the FOX2 gene and gene product. J Biol Chem. 1992;267(10):6646–6653.
   PubMed Web of Science ®Google Scholar
• Lu K, Psakhye I, Jentsch S. Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell. 2014;158(3):549–563.
   PubMed Web of Science ®Google Scholar
• Chiang MC, Chiang HL. Vid24p, a novel protein localized to the fructose-1, 6-bisphosphatase-containing vesicles, regulates targeting of fructose-1,6-bisphosphatase from the vesicles to the vacuole for degradation. J Cell Biol. 1998;140(6):1347–1356.
   PubMed Web of Science ®Google Scholar
• El Magraoui F, Brinkmeier R, Schrotter A, et al. Distinct ubiquitination cascades act on the peroxisomal targeting signal type 2 co-receptor Pex18p. Traffic. 2013;14(12):1290–1301.
   PubMed Web of Science ®Google Scholar
• Waterham HR, Ferdinandusse S, Wanders RJ. Human disorders of peroxisome metabolism and biogenesis. Biochim Biophys Acta. 2016;1863(5):922–933.
   PubMed Web of Science ®Google Scholar
• Terlecky SR, Koepke JI, Walton PA. Peroxisomes and aging. Biochim Biophys Acta. 2006;1763(12):1749–1754.
   PubMed Web of Science ®Google Scholar
• Walton PA, Brees C, Lismont C, et al. The peroxisomal import receptor PEX5 functions as a stress sensor, retaining catalase in the cytosol in times of oxidative stress. Biochim Biophys Acta. 2017;1864(10):1833–1843.
   Web of Science ®Google Scholar
• Braverman N, Steel G, Obie C, et al. Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nat Genet. 1997;15(4):369–376.
   PubMed Web of Science ®Google Scholar
• Schliebs W, Saidowsky J, Agianian B, et al. Recombinant human peroxisomal targeting signal receptor PEX5. Structural basis for interaction of PEX5 with PEX14. J Biol Chem. 1999;274(9):5666–5673.
   PubMed Web of Science ®Google Scholar
• Farré JC, Carolino K, Stasyk OV, et al. A new yeast peroxin, Pex36, a functional homolog of mammalian PEX16, functions in the ER-to-peroxisome traffic of peroxisomal membrane proteins. J Mol Biol. 2017;429(23):3743–3762.
   PubMed Web of Science ®Google Scholar