The peroxisomal receptor dislocation pathway: To the exportomer and beyond

Biochimie

Volumn 98, Issue 1, 2014, Pages 16-28

  Platta, Harald W ^a   Hagen, Stefanie ^a   Reidick, Christina ^a   Erdmann, Ralf ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

AAA type ATPases; Peroxin; Peroxisome; Protein import; RING type ligase; Ubiquitination

Indexed keywords

AAA-TYPE ATPASES; PEROXIN; PEROXISOME; PROTEIN IMPORT; RING-TYPE LIGASE; UBIQUITINATION;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CYTOSOL; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; PEROXISOMES; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITINATION;

EID: 84895142640     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.12.009     Document Type: Review

References (202)

1. T. Hoppe Multiubiquitylation by E4 enzymes: 'one size' doesn't fit all Trends Biochem. Sci. 30 2005 183 187
2. O. Kerscher, R. Felberbaum, and M. Hochstrasser Modification of proteins by ubiquitin and ubiquitin-like proteins Annu. Rev. Cell Dev. Biol. 22 2006 159 180
3. D.M. Wenzel, A. Lissounov, P.S. Brzovic, and R.E. Klevit UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids Nature 474 2011 105 108
4. A. Williamson, A. Werner, and M. Rape The Colossus of ubiquitylation: decrypting a cellular code Mol. Cell 49 2013 591 600
5. A. Schlüter, A. Real-Chicharro, T. Gabaldón, F. Sánchez-Jiménez, and A. Pujol PeroxisomeDB 2.0: an integrative view of the global peroxisomal metabolome Nucleic Acids Res. 38 2010 (Database issue)
6. R.J. Wanders, and H.R. Waterham Biochemistry of mammalian peroxisomes revisited Annu. Rev. Biochem. 75 2006 295 332
7. A. Baker, I.A. Graham, M. Holdsworth, S.M. Smith, and F.L. Theodoulou Chewing the fat: beta-oxidation in signalling and development Trends Plant Sci. 11 2006 124 132
8. L. Kienow, K. Schneider, M. Bartsch, H.P. Stuible, H. Weng, O. Miersch, C. Wasternack, and E. Kombrink Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana J. Exp. Bot. 59 2008 403 419
9. H.J. Joo, K.Y. Kim, Y.H. Yim, Y.X. Jin, H. Kim, M.Y. Kim, and Y.K. Paik Contribution of the peroxisomal acox gene to the dynamic balance of daumone production in Caenorhabditis elegans J. Biol. Chem. 285 2010 29319 29325
10. C.N. Spiegel, L.G. Batista-Pereira, J.A. Bretas, A.E. Eiras, A.M. Hooper, A.A. Peixoto, and M.J. Soares Pheromone gland development and pheromone production in lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) J. Med. Entomol. 48 2011 489 495
11. P. Magliano, M. Flipphi, B.A. Arpat, S. Delessert, and Y. Poirier Contributions of the peroxisome and ß-oxidation cycle to biotin synthesis in fungi J. Biol. Chem. 286 2011 42133 42140
12. Y. Tanabe, J. Maruyama, S. Yamaoka, D. Yahagi, I. Matsuo, N. Tsutsumi, and K. Kitamoto Peroxisomes are involved in biotin biosynthesis in Aspergillus and Arabidopsis J. Biol. Chem. 286 2011 30455 30461
13. W.H. Meijer, L. Gidijala, S. Fekken, J.A. Kiel, M.A. van den Berg, R. Lascaris, R.A. Bovenberg, and I.J. van der Klei Peroxisomes are required for efficient penicillin biosynthesis in Penicillium chrysogenum Appl. Environ. Micobiol. 76 2010 5702 5709
14. W.H. Müller, T.P. van der Krift, A.J. Krouwer, H.A. Wösten, L.H. van der Voort, E.B. Smaal, and A.J. Verkleij Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum EMBO J. 10 1991 489 495
15. V.I. Titorenko, and S.R. Terlecky Peroxisome metabolism and cellular aging Traffic 12 2011 252 259
16. G. Lizard, O. Rouaud, J. Demarquoy, M. Cherkaoui-Malki, and L. Iuliano Potential roles of peroxisomes in Alzheimer's disease and in dementia of the Alzheimer's type J. Alzheimer's Dis. 29 2012 241 254
17. S. Manivannan, C.Q. Scheckhuber, M. Veenhuis, and I.J. van der Klei The impact of peroxisomes on cellular aging and death Front. Oncol. 2 2012 50
18. S. Nagotu, V.C. Kalel, R. Erdmann, and H.W. Platta Molecular basis of peroxisomal biogenesis disorders caused by defects in peroxisomal matrix protein import Biochim. Biophys. Acta 1822 2012 1326 1336
19. B.T. Poll-The, and J. Gärtner Clinical diagnosis, biochemical findings and MRI spectrum of peroxisomal disorders Biochim. Biophys. Acta 1822 2012 1421 1429
20. H.R. Waterham, and M.S. Ebberink Genetics and molecular basis of human peroxisome biogenesis disorders Biochim. Biophys. Acta 1822 2012 1430 1441
21. R.J. Wanders, and H.R. Waterham Peroxisomal disorders: the single peroxisomal enzyme deficiencies Biochim. Biophys. Acta 1763 2006 1707 1720
22. S.J. Steinberg, G. Dodt, G.V. Raymond, N.E. Braverman, A.B. Moser, and H.W. Moser Peroxisome biogenesis disorders Biochim. Biophys. Acta 1763 2006 1733 1748
23. B. Distel, R. Erdmann, S.J. Gould, G. Blobel, D.I. Crane, J.M. Cregg, G. Dodt, Y. Fujiki, J.M. Goodman, W.W. Just, J.A. Kiel, W.H. Kunau, P.B. Lazarow, G.P. Mannaerts, H.W. Moser, T. Osumi, R.A. Rachubinski, A. Roscher, S. Subramani, H.F. Tabak, T. Tsukamoto, D. Valle, I. van der Klei, P.P. van Veldhoven, and M. Veenhuis A unified nomenclature for peroxisome biogenesis factors J. Cell Biol. 135 1996 1 3
24. M. Islinger, S. Grille, H.D. Fahimi, and M. Schrader The peroxisome: an update on mysteries Histochem. Cell Biol. 137 2012 547 574
25. L. Opaliński, M. Veenhuis, and I.J. van der Klei Peroxisomes: membrane events accompanying peroxisome proliferation Int. J. Biochem. Cell Biol. 43 2011 847 851
26. S. Nagotu, M. Veenhuis, and I.J. Van der Klei Divide et impera: the dictum of peroxisomes Traffic 11 2010 175 184
27. A. Fagarasanu, F.D. Mast, B. Knoblach, and R.A. Rachubinski Molecular mechanism of organelle inheritance: lessons from peroxisomes in yeast Nat. Rev. Mol. Cell Biol. 11 2010 644 654
28. S. Hasan, H.W. Platta, and R. Erdmann Import of proteins into the peroxisomal matrix Front. Physiol. 4 2013 261
29. S. Leon, J.M. Goodman, and S. Subramani 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 1763 2006 1552 1564
30. W. Girzalsky, H.W. Platta, and R. Erdmann Protein transport across the peroxisomal membrane Biol. Chem. 390 2009 745 751
31. M.O. Freitas, T. Francisco, T.A. Rodrigues, I.S. Alencastre, M.P. Pinto, C.P. Grou, A.F. Carvalho, M. Fransen, C. Sá-Miranda, and J.E. Azevedo PEX5 protein binds monomeric catalase blocking its tetramerization and releases it upon binding the N-terminal domain of PEX14 J. Biol. Chem. 286 2011 40509 40519
32. H. Otera, and Y. Fujiki Pex5p imports folded tetrameric catalase by interaction with Pex13p Traffic 13 2011 1364 1377
33. P.A. Walton, P.E. Hill, and S. Subramani Import of stably folded proteins into peroxisomes Mol. Biol. Cell 6 1995 675 683
34. A.M. Albiniak, J. Baglieri, and C. Robinson Targeting of lumenal proteins across the thylakoid membrane J. Exp. Bot. 63 2012 1689 1698
35. T. Palmer, and B.C. Berks The twin-arginine translocation (Tat) protein export pathway Nat. Rev. Microbiol. 10 2012 483 964
36. D.J. Schnell, and D.N. Hebert Protein translocons: multifunctional mediators of protein translocation across membranes Cell 112 2003 491 505
37. V. Dammai, and S. Subramani The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol Cell 105 2001 187 196
38. D.M. Nair, P.E. Purdue, and P.B. Lazarow Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae J. Cell Biol. 167 2004 599 604
39. H.W. Platta, S. Hagen, and R. Erdmann The exportomer: the peroxisomal receptor export machinery Cell. Mol. Life Sci. 70 2013 1393 1411
40. C. Brocard, and A. Hartig Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim. Biophys. Acta 1763 2006 1565 1573
41. G. Chowdhary, A.R. Kataya, T. Lingner, and S. Reumann Non-canonical peroxisome targeting signals: identification of novel PTS1 tripeptides and characterization of enhancer elements by computational permutation analysis BMC Plant Biol. 12 2012
42. K. Fodor, J. Wolf, R. Erdmann, W. Schliebs, and M. Wilmanns Molecular requirements for peroxisomal targeting of alanine-glyoxylate aminotransferase as an essential determinant in primary hyperoxaluria type 1 PLoS Biol. 10 2012 e1001309
43. K. Shiozawa, P.V. Konarev, C. Neufeld, M. Wilmanns, and D.I. Svergun Solution structure of human Pex5.Pex14.PTS1 protein complexes obtained by small angle X-ray scattering J. Biol. Chem. 284 2009 25334 25342
44. W.A. Stanley, F.V. Filipp, P. Kursula, N. Schüller, R. Erdmann, W. Schliebs, M. Sattler, and M. Wilmanns Recognition of a functional peroxisome type 1 target by the dynamic import receptor pex5p Mol. Cell 24 2006 653 663
45. P.B. Lazarow The import receptor Pex7p and the PTS2 targeting sequence Biochim. Biophys. Acta 1763 2006 1599 1604
46. O.I. Petriv, L. Tang, V.I. Titorenko, and R.A. Rachubinski A new definition for the consensus sequence of the peroxisome targeting signal type 2 J. Mol. Biol. 341 2004 119 134
47. W. Schliebs, and W.H. Kunau PTS2 co-receptors: diverse proteins with common features Biochim. Biophys. Acta 1763 2006 1606 1612
48. D. Pan, T. Nakatsu, and H. Kato Crystal structure of peroxisomal targeting signal-2 bound to its receptor complex Pex7p-Pex21p Nat. Struct. Mol. Biol. 20 2013 987 993
49. A.M. Gouveia, C.P. Guimaraes, M.E. Oliveira, C. Sa-Miranda, and J.E. Azevedo Insertion of Pex5p into the peroxisomal membrane is cargo protein-dependent J. Biol. Chem. 278 2003 4389 4392
50. S. Grunau, W. Schliebs, R. Linnepe, C. Neufeld, C. Cizmowski, B. Reinartz, H.E. Meyer, B. Warscheid, W. Girzalsky, and R. Erdmann Peroxisomal targeting of PTS2 pre-import complexes in the yeast Saccharomyces cerevisiae Traffic 10 2009 451 460
51. J.A. Kiel, M. Veenhuis, and I.J. van der Klei PEX genes in fungal genomes: common, rare or redundant Traffic 7 2006 1291 1303
52. B. Huhse, P. Rehling, M. Albertini, L. Blank, K. Meller, and W.-H. Kunau Pex17p of Saccharomyces cerevisiae is a novel peroxin and component of the peroxisomal protein translocation machinery J. Cell Biol. 140 1998 49 60
53. D. Managadze, C. Würtz, S. Wiese, M. Schneider, W. Girzalsky, H.E. Meyer, R. Erdmann, B. Warscheid, and H. Rottensteiner Identification of PEX33, a novel component of the peroxisomal docking complex in the filamentous fungus Neurospora crassa Eur. J. Cell Biol. 89 2010 955 964
54. L. Opaliński, J.A. Kiel, T.G. Homan, M. Veenhuis, and I.J. van der Klei Penicillium chrysogenum Pex14/17p-a novel component of the peroxisomal membrane that is important for penicillin production FEBS J. 277 2010 3203 3218
55. L. Peraza-Reyes, S. Arnaise, D. Zickler, E. Coppin, R. Debuchy, and V. Berteaux-Lecellier The importomer peroxins are differentially required for peroxisome assembly and meiotic development in Podospora anserina: insights into a new peroxisome import pathway Mol. Microbiol. 82 2011 365 377
56. A. Brennand, D.J. Rigden, and P.A. Michels Trypanosomes contain two highly different isoforms of peroxin PEX13 involved in glycosome biogenesis FEBS Lett. 586 2012 1765 1771
57. J.E. Azevedo, and W. Schliebs Pex14p, more than just a docking protein Biochim. Biophys. Acta 1763 2006 1574 1584
58. C. Williams, and B. Distel Pex13p: docking or cargo handling protein? Biochim. Biophys. Acta 1763 2006 1585 1591
59. R. Erdmann, and W. Schliebs Peroxisomal matrix protein import: the transient pore model Nat. Rev. Mol. Cell Biol. 6 2005 738 742
60. A.M. Gouveia, C.P. Guimaraes, M.E. Oliveira, C. Reguenga, C. Sa-Miranda, and J.E. Azevedo Characterization of the peroxisomal cycling receptor, Pex5p, using a cell-free in vitro import system J. Biol. Chem. 278 2002 226 232
61. A.M. Gouveia, C. Reguenga, M.E. Oliveira, C. Sa-Miranda, and J.E. Azevedo Characterization of peroxisomal Pex5p from rat liver: Pex5p in the Pex5p-Pex14p membrane complex is a transmembrane protein J. Biol. Chem. 275 2000 32444 32451
62. D. Kerssen, E. Hambruch, W. Klaas, H.W. Platta, B. de Kruijff, R. Erdmann, W.H. Kunau, and W. Schliebs Membrane association of the cycling peroxisome import receptor Pex5p J. Biol. Chem. 281 2006 27003 27015
63. H.W. Platta, S. Grunau, K. Rosenkranz, W. Girzalsky, and R. Erdmann Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol Nat. Cell Biol. 7 2005 817 822
64. C. Ma, U. Schumann, N. Rayapuram, and S. Subramani The peroxisomal matrix import of Pex8p requires only PTS receptors and Pex14p Mol. Biol. Cell 20 2009 3680 3689
65. R. Natsuyama, K. Okumoto, and Y. Fujiki Pex5p stabilizes Pex14p: a study using a newly isolated pex5 CHO cell mutant, ZPEG101 Biochem. J. 449 2013 195 207
66. N. Cyr, K.P. Madrid, R. Strasser, M. Aurousseau, R. Finn, J. Ausio, and A. Jardim Leishmania donovani peroxin 14 undergoes a marked conformational change following association with peroxin 5 J. Biol. Chem. 283 2008 31488 31499
67. M. Meinecke, C. Cizmowski, W. Schliebs, V. Kruger, S. Beck, R. Wagner, and R. Erdmann The peroxisomal importomer constitutes a large and highly dynamic pore Nat. Cell Biol. 12 2010 273 277
68. D. Wang, N.V. Visser, M. Veenhuis, and I.J. Van Der Klei Physical interactions of the peroxisomal targeting signal 1-receptor, Pex5p, studied by fluorescence correlation spectroscopy J. Biol. Chem. 278 2003 43340 43345
69. C. Ma, D. Hagstrom, S.G. Polley, and S. Subramani Redox regulated cargo binding and release by the peroxisomal targeting signal receptor, Pex5 J. Biol. Chem. 288 2013 27220 27231
70. B. Agne, N.M. Meindl, K. Niederhoff, H. Einwächter, P. Rehling, A. Sickmann, H.E. Meyer, W. Girzalsky, and W.H. Kunau Pex8p. An intraperoxisomal organizer of the peroxisomal import machinery Mol. Cell 11 2003 635 646
71. C.S. Collins, J.E. Kalish, J.C. Morrell, J.M. McCaffery, and S.J. Gould The peroxisome biogenesis factors Pex4p, Pex22p, Pex1p, and Pex6p act in the terminal steps of peroxisomal matrix protein import Mol. Cell. Biol. 20 2000 7516 7526
72. P.P. Hazra, I. Suriapranata, W.B. Snyder, and S. Subramani Peroxisome remnants in pex3Delta cells and the requirement of Pex3p for interactions between the peroxisomal docking and translocation subcomplexes Traffic 3 2002 560 574
73. S. Oeljeklaus, B.S. Reinartz, J. Wolf, S. Wiese, J. Tonillo, K. Podwojski, K. Kuhlmann, C. Stephan, H.E. Meyer, W. Schliebs, C. Brocard, R. Erdmann, and B. Warscheid Identification of core components and transient interactors of the peroxisomal importomer by dual-track stable isotope labeling with amino acids in cell culture analysis J. Proteome Res. 11 2012 2567 2580
74. H.W. Platta, F. El Magraoui, B.E. Baumer, D. Schlee, W. Girzalsky, and R. Erdmann Pex2 and Pex12 function as protein-ubiquitin ligases in peroxisomal protein import Mol. Cell. Biol. 29 2009 5505 5516
75. F. El Magraoui, B.E. Bäumer, H.W. Platta, J.S. Baumann, W. Girzalsky, and R. Erdmann The RING-type ubiquitin ligases Pex2p, Pex10p and Pex12p form a heteromeric complex that displays enhanced activity in an ubiquitin conjugating enzyme-selective manner FEBS J. 279 2012 2060 2070
76. C.P. Grou, A.F. Carvalho, M.P. Pinto, S. Wiese, H. Piechura, H.E. Meyer, B. Warscheid, C. Sa-Miranda, and J.E. Azevedo Members of the E2D (UbcH5) family mediate the ubiquitination of the conserved cysteine of Pex5p, the peroxisomal import receptor J. Biol. Chem. 283 2008 14190 14197
77. H.W. Platta, F. El Magraoui, D. Schlee, S. Grunau, W. Girzalsky, and R. Erdmann Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling J. Cell Biol. 177 2007 197 204
78. C. Williams, M. van den Berg, E. Geers, and B. Distel Pex10p functions as an E3 ligase for the Ubc4p-dependent ubiquitination of Pex5p Biochem. Biophys. Res. Commun. 374 2008 620 624
79. C. Williams, M. van den Berg, R.R. Sprenger, and B. Distel A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p J. Biol. Chem. 282 2007 22534 22543
80. S. Leon, L. Zhang, W.H. McDonald, J. Yates 3rd, J.M. Cregg, and S. Subramani Dynamics of the peroxisomal import cycle of PpPex20p: ubiquitin-dependent localization and regulation J. Cell Biol. 172 2006 67 78
81. N. Miyata, and Y. Fujiki Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export Mol. Cell. Biol. 25 2005 10822 10832
82. N. Miyata, K. Okumoto, S. Mukai, M. Noguchi, and Y. Fujiki AWP1/ZFAND6 functions in Pex5 export by interacting with cys-monoubiquitinated Pex5 and Pex6 AAA ATPase Traffic 13 2011 168 183
83. M.O. Debelyy, H.W. Platta, D. Saffian, A. Hensel, S. Thoms, H.E. Meyer, B. Warscheid, W. Girzalsky, and R. Erdmann Ubp15p, a ubiquitin hydrolase associated with the peroxisomal export machinery J. Biol. Chem. 286 2011 28223 28234
84. X. Wang, R.A. Herr, and T.H. Hansen Ubiquitination of substrates by esterification Traffic 13 2012 19 24
85. A.F. Carvalho, M.P. Pinto, C.P. Grou, I.S. Alencastre, M. Fransen, C. Sa-Miranda, and J.E. Azevedo Ubiquitination of mammalian Pex5p, the peroxisomal import receptor J. Biol. Chem. 282 2007 31267 31272
86. K. Okumoto, S. Misono, N. Miyata, Y. Matsumoto, S. Mukai, and Y. Fujiki Cysteine ubiquitination of PTS1 receptor Pex5p regulates Pex5p recycling Traffic 12 2011 1067 1083
87. F.F. Wiebel, and W.-H. Kunau The PAS2 protein essential for peroxisome biogenesis is related to ubiquitin-conjugating enzymes Nature 359 1992 73 76
88. D.I. Crane, J.E. Kalish, and S.J. Gould The Pichia pastoris PAS4 gene encodes a ubiquitin-conjugation enzyme required for peroxisome assembly J. Biol. Chem. 269 1994 21835 21844
89. I.J. van der Klei, R.E. Hilbrands, J.A.K.W. Kiel, S.W. Rasmussen, J.M. Cregg, and M. Veenhuis The ubiquitin-conjugating enzyme Pex4p of Hansenula polymorpha is required for efficient functioning of the PTS1 import machinery EMBO J. 17 1998 3608 3618
90. B.K. Zolman, M. Monroe-Augustus, I.D. Silva, and B. Bartel Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22 Plant Cell 17 2005 3422 3435
91. A. Koller, W.B. Snyder, K.N. Faber, T.J. Wenzel, L. Rangell, G.A. Keller, and S. Subramani Pex22p of Pichia pastoris, essential for peroxisomal matrix protein import, anchors the ubiquitin-conjugating enzyme, Pex4p, on the peroxisomal membrane J. Cell Biol. 146 1999 99 112
92. C. Williams, M. van den Berg, S. Panjikar, W.A. Stanley, B. Distel, and M. Wilmanns Insights into ubiquitin-conjugating enzyme/co-activator interactions from the structure of the Pex4p:Pex22p complex EMBO J. 31 2012 391 402
93. P.S. Brzovic, and R.E. Klevit Ubiquitin transfer from the E2 perspective: why is UbcH5 so promiscuous? Cell Cycle 5 2006 2867 2873
94. H. Gonen, B. Bercovich, A. Orian, A. Carrano, C. Takizawa, K. Yamanaka, M. Pagano, K. Iwai, and A. Ciechanover Identification of the ubiquitin carrier proteins, E2s, involved in signal-induced conjugation and subsequent degradation of IkappaBalpha J. Biol. Chem. 274 1999 14823 14830
95. M.K. Saville, A. Sparks, D.P. Xirodimas, J. Wardrop, L.F. Stevenson, J.C. Bourdon, Y.L. Woods, and D.P. Lane Regulation of p53 by the ubiquitin-conjugating enzymes UbcH5B/C in vivo J. Biol. Chem. 279 2004 42169 42181
96. M. Gualdrón-López, N. Chevalier, P. Van Der Smissen, P.J. Courtoy, D.J. Rigden, and P.A. Michels Ubiquitination of the glycosomal matrix protein receptor PEX5 in Trypanosoma brucei by PEX4 displays novel features Biochim. Biophys. Acta 1833 2013 3076 3092
97. A. Kragt, T. Voorn-Brouwer, M. van den Berg, and B. Distel The Saccharomyces cerevisiae peroxisomal import receptor Pex5p is monoubiquitinated in wild type cells J. Biol. Chem. 280 2005 7867 7874
98. N. Kaur, Q. Zhao, Q. Xie, and J. Hu Arabidopsis RING peroxins are E3 ubiquitin ligases that interact with two homologous ubiquitin receptor proteins(F) J. Integr. Plant Biol. 55 2013 108 120
99. Y. Fujiki, C. Nashiro, N. Miyata, S. Tamura, and K. Okumoto New insights into dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p in shuttling of PTS1-receptor Pex5p during peroxisome biogenesis Biochim. Biophys. Acta 1823 2012 145 149
100. I. Grimm, D. Saffian, H.W. Platta, and R. Erdmann The AAA-type ATPases Pex1p and Pex6p and their role in peroxisomal matrix protein import in Saccharomyces cerevisiae Biochim. Biophys. Acta 1823 2012 150 158
101. H.W. Platta, M.O. Debelyy, F. El Magraoui, and R. Erdmann The AAA peroxins Pex1p and Pex6p function as dislocases for the ubiquitinated peroxisomal import receptor Pex5p Biochem. Soc. Trans. 36 2008 99 104
102. I. Birschmann, K. Rosenkranz, R. Erdmann, and W.H. Kunau Structural and functional analysis of the interaction of the AAA-peroxins Pex1p and Pex6p FEBS J. 272 2005 47 58
103. J.A. Kiel, R.E. Hilbrands, R.A. Bovenberg, and M. Veenhuis Isolation of Penicillium chrysogenum PEX1 and PEX6 encoding AAA proteins involved in peroxisome biogenesis Appl. Microbiol. Biotechnol. 54 2000 238 242
104. J.A. Kiel, R.E. Hilbrands, I.J. van der Klei, S.W. Rasmussen, F.A. Salomons, M. van der Heide, K.N. Faber, J.M. Cregg, and M. Veenhuis Hansenula polymorpha Pex1p and Pex6p are peroxisome-associated AAA proteins that functionally and physically interact Yeast 15 1999 1059 1078
105. S. Tamura, N. Shimozawa, Y. Suzuki, T. Tsukamoto, T. Osumi, and Y. Fujiki A cytoplasmic AAA family peroxin, Pex1p, interacts with Pex6p Biochem. Biophys. Res. Commun. 245 1998 883 886
106. S. Tamura, S. Yasutake, N. Matsumoto, and Y. Fujiki Dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p J. Biol. Chem. 281 2006 27693 27704
107. I. Birschmann, A.K. Stroobants, M. Van Den Berg, A. Schäfer, K. Rosenkranz, W.H. Kunau, and H.F. Tabak Pex15p of Saccharomyces cerevisiae Provides a molecular basis for recruitment of the AAA peroxin Pex6p to peroxisomal membranes Mol. Biol. Cell 14 2003 2226 2236
108. S. Furuki, S. Tamura, N. Matsumoto, N. Miyata, A. Moser, H.W. Moser, and Y. Fujiki Mutations in the peroxin Pex26p responsible for peroxisome biogenesis disorders of complementation group 8 impair its stability, peroxisomal localization, and interaction with the Pex1p x Pex6p complex J. Biol. Chem. 281 2006 1317 1323
109. S. Goto, S. Mano, C. Nakamori, and M. Nishimura Arabidopsis ABERRANT PEROXISOME MORPHOLOGY9 is a peroxin that recruits the PEX1-PEX6 complex to peroxisomes Plant Cell 23 2011 1573 1587
110. N. Matsumoto, S. Tamura, and Y. Fujiki The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes Nat. Cell Biol. 5 2003 454 460
111. N. Matsumoto, S. Tamura, S. Furuki, N. Miyata, A. Moser, N. Shimozawa, H.W. Moser, Y. Suzuki, N. Kondo, and Y. Fujiki Mutations in novel peroxin gene PEX26 that cause peroxisome-biogenesis disorders of complementation group 8 provide a genotype-phenotype correlation Am. J. Hum. Genet. 73 2003 233 246
112. L.M. Iyer, D.D. Leipe, E.V. Koonin, and L. Aravind Evolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol. 146 2004 11 31
113. S.R. White, and B. Lauring AAA+ ATPases: achieving diversity of function with conserved machinery Traffic 8 2007 1657 1667
114. D. Saffian, I. Grimm, W. Girzalsky, and R. Erdmann ATP-dependent assembly of the heteromeric Pex1p-Pex6p-complex of the peroxisomal matrix protein import machinery J. Struct. Biol. 179 2012 126 132
115. C. Bebeacua, A. Förster, C. McKeown, H.H. Meyer, X. Zhang, and P.S. Freemont Distinct conformations of the protein complex p97-Ufd1-Npl4 revealed by electron cryomicroscopy Proc. Natl. Acad. Sci. U. S. A. 109 2012 1098 1103
116. J.M. Davies, A.T. Brunger, and W.I. Weis Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change Structure 16 2008 715 726
117. C. Nashiro, A. Kashiwagi, T. Matsuzaki, S. Tamura, and Y. Fujiki Recruiting mechanism of the AAA peroxins, Pex1p and Pex6p, to Pex26p on peroxisome membrane Traffic 12 2011 774 788
118. K. Rosenkranz, I. Birschmann, S. Grunau, W. Girzalsky, W.H. Kunau, and R. Erdmann Functional association of the AAA complex and the peroxisomal importomer FEBS J. 273 2006 3804 3815
119. B.J. Fenner, M. Scannell, and J.H. Prehn Identification of polyubiquitin binding proteins involved in NF-kappaB signaling using protein arrays Biochim. Biophys. Acta 1794 2009 1010 1016
120. J.A. Kiel, K. Emmrich, H.E. Meyer, and W.H. Kunau Ubiquitination of the peroxisomal targeting signal type 1 receptor, Pex5p, suggests the presence of a quality control mechanism during peroxisomal matrix protein import J. Biol. Chem. 280 2005 1921 1930
121. H.W. Platta, W. Girzalsky, and R. Erdmann Ubiquitination of the peroxisomal import receptor Pex5p Biochem. J. 384 2004 37 45
122. W. Seufert, and S. Jentsch Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins EMBO J. 9 1990 543 550
123. W. Seufert, J.P. McGrath, and S. Jentsch UBC1 encodes a novel member of an essential subfamily of yeast ubiquitin-conjugating enzymes involved in protein degradation EMBO J. 9 1990 4535 4541
124. S. Leon, and S. Subramani A conserved cysteine residue of Pichia pastoris Pex20p is essential for its recycling from the peroxisome to the cytosol J. Biol. Chem. 282 2007 7424 7430
125. G. Dodt, and S.J. Gould 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. 135 1996 1763 1774
126. B.K. Zolman, and B. Bartel An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function Proc. Natl. Acad. Sci. U. S. A. 101 2004 1786 1791
127. C.P. Grou, A.F. Carvalho, M.P. Pinto, S.J. Huybrechts, C. Sa-Miranda, M. Fransen, and J.E. Azevedo Properties of the ubiquitin-Pex5p thiol ester conjugate J. Biol. Chem. 284 2009 10504 10513
128. A.Y. Amerik, and M. Hochstrasser Mechanism and function of deubiquitinating enzymes Biochim. Biophys. Acta 1695 2004 189 207
129. F.E. Reyes-Turcu, K.H. Ventii, and K.D. Wilkinson Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes Annu. Rev. Biochem. 78 2009 363 397
130. C.P. Grou, T. Francisco, T.A. Rodrigues, M.O. Freitas, M.P. Pinto, A.F. Carvalho, P. Domingues, S.A. Wood, J.E. Rodríguez-Borges, C. Sá-Miranda, M. Fransen, and J.E. Azevedo Identification of ubiquitin-specific protease 9X (USP9X) as a deubiquitinase acting on the ubiquitin-peroxin 5 (PEX5) thioester conjugate J. Biol. Chem. 287 2012 12815 12827
131. S. Dupont, A. Mamidi, M. Cordenonsi, M. Montagner, L. Zacchigna, M. Adorno, G. Martello, M.J. Stinchfield, S. Soligo, L. Morsut, M. Inui, S. Moro, N. Modena, F. Argenton, S.J. Newfeld, and S. Piccolo FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination Cell 136 2009 123 135
132. M. Schwickart, X. Huang, J.R. Lill, J. Liu, R. Ferrando, D.M. French, H. Maecker, K. O'Rourke, F. Bazan, J. Eastham-Anderson, P. Yue, D. Dornan, D.C. Huang, and V.M. Dixit Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival Nature 463 2010 103 107
133. J.A. Nathan, S. Sengupta, S.A. Wood, A. Admon, G. Markson, C. Sanderson, and P.J. Lehner The ubiquitin E3 ligase MARCH7 is differentially regulated by the deubiquitylating enzymes USP7 and USP9X Traffic 9 2008 1130 1145
134. P.E. Purdue, and P.B. Lazarow Pex18p is constitutively degraded during peroxisome biogenesis J. Biol. Chem. 276 2001 47684 47689
135. A. Hensel, S. Beck, F. El Magraoui, H.W. Platta, W. Girzalsky, and R. Erdmann Cysteine-dependent ubiquitination of Pex18p is linked to cargo translocation across the peroxisomal membrane J. Biol. Chem. 286 2011 43495 43505
136. F. El Magraoui, R. Brinkmeier, A. Schrötter, W. Girzalsky, T. Müller, K. Marcus, H.E. Meyer, R. Erdmann, and H.W. Platta Distinct ubiquitination cascades act on the peroxisomal targeting signal type 2 co-receptor Pex18p Traffic 14 2013 1290 1301
137. X. Liu, and S. Subramani Unique requirements for mono- and polyubiquitination of the peroxisomal targeting signal co-receptor, Pex20 J. Biol. Chem. 288 2013 7230 7240
138. S. Cui, Y. Fukao, S. Mano, K. Yamada, M. Hayashi, and M. Nishimura Proteomic analysis reveals that the Rab GTPase RabE1c is involved in the degradation of the peroxisomal protein receptor PEX7 (peroxin 7) J. Biol. Chem. 288 2013 6014 6023
139. M. Helm, C. Lück, J. Prestele, G. Hierl, P.F. Huesgen, T. Fröhlich, G.J. Arnold, I. Adamska, A. Görg, F. Lottspeich, and C. Gietl Dual specificities of the glyoxysomal/peroxisomal processing protease Deg15 in higher plants Proc. Natl. Acad. Sci. U. S. A. 104 2007 11501 11506
140. K. Okumoto, Y. Kametani, and Y. Fujiki Two proteases, Tysnd1 and PsLon, cooperatively regulate fatty-acid {beta}-oxidation in the peroxisomal matrix J. Biol. Chem. 286 2011 44367 44379
141. I.V. Kurochkin, Y. Mizuno, A. Konagaya, Y. Sakaki, C. Schönbach, and Y. Okazaki Novel peroxisomal protease Tysnd1 processes PTS1- and PTS2-containing enzymes involved in beta-oxidation of fatty acids EMBO J. 26 2007 835 845
142. M. Bartoszewska, C. Williams, A. Kikhney, Ł. Opaliński, C.W. van Roermund, R. de Boer, M. Veenhuis, and I.J. van der Klei Peroxisomal proteostasis involves a Lon family protein that functions as protease and chaperone J. Biol. Chem. 287 2012 27380 27395
143. O. Ostersetzer, Y. Kato, Z. Adam, and W. Sakamoto Multiple intracellular locations of Lon protease in Arabidopsis: evidence for the localization of AtLon4 to chloroplasts Plant Cell Physiol. 48 2007 881 885
144. M.J. Lingard, and B. Bartel Arabidopsis LON2 is necessary for peroxisomal function and sustained matrix protein import Plant Physiol. 151 2009 1354 1365
145. M.J. Lingard, M. Monroe-Augustus, and B. Bartel Peroxisome-associated matrix protein degradation in Arabidopsis Proc. Natl. Acad. Sci. U. S. A. 106 2009 4561 4566
146. S.E. Burkhart, M.J. Lingard, and B. Bartel Genetic dissection of peroxisome-associated matrix protein degradation in Arabidopsis thaliana Genetics 193 2013 125 141
147. V. Berteaux-Lecellier, M. Picard, C. Thompson-Coffe, D. Zickler, A. Panvier-Adoutte, and J.M. Simonet A nonmammalian homolog of the PAF1 gene (Zellweger syndrome) discovered as a gene involved in caryogamy in the fungus Podospora anserina Cell 81 1995 1043 1051
148. D. Zickler, S. Arnaise, E. Coppin, R. Debuchy, and M. Picard Altered mating-type identity in the fungus Podospora anserina leads to selfish nuclei, uniparental progeny, and haploid meiosis Genetics 140 1995 493 503
149. L. Peraza-Reyes, D. Zickler, and V. Berteaux-Lecellier The peroxisome RING-finger complex is required for meiocyte formation in the fungus Podospora anserina Traffic 9 2008 1998 2009
150. C. Bonnet, E. Espagne, D. Zickler, S. Boisnard, A. Bourdais, and V. Berteaux-Lecellier The peroxisomal import proteins PEX2, PEX5 and PEX7 are differently involved in Podospora anserina sexual cycle Mol. Microbiol. 62 2006 157 169
151. J. Zhang, J. Kim, A. Alexander, S. Cai, D.N. Tripathi, R. Dere, A.R. Tee, J. Tait-Mulder, A. Di Nardo, J.M. Han, E. Kwiatkowski, E.A. Dunlop, K.M. Dodd, R.D. Folkerth, P.L. Faust, M.B. Kastan, M. Sahin, and C.L. Walker A tuberous sclerosis complex signalling node at the peroxisome regulates mTORC1 and autophagy in response to ROS Nat. Cell Biol. 15 2013 1186 1196
152. E. Dixit, S. Boulant, Y. Zhang, A.S. Lee, C. Odendall, B. Shum, N. Hacohen, Z.J. Chen, S.P. Whelan, M. Fransen, M.L. Nibert, G. Superti-Furga, and J.C. Kagan Peroxisomes are signaling platforms for antiviral innate immunity Cell 141 2010 668 681
153. K. Nito, A. Kamigaki, M. Kondo, M. Hayashi, and M. Nishimura Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants Plant Cell Physiol. 48 2007 763 774
154. J. Prestele, G. Hierl, C. Scherling, S. Hetkamp, C. Schwechheimer, E. Isono, W. Weckwerth, G. Wanner, and C. Gietl Different functions of the C3HC4 zinc RING finger peroxins PEX10, PEX2, and PEX12 in peroxisome formation and matrix protein import Proc. Natl. Acad. Sci. U. S. A. 107 2010 14915 14920
155. U. Schumann, J. Prestele, H. O'Geen, R. Brueggeman, G. Wanner, and C. Gietl Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts Proc. Natl. Acad. Sci. U. S. A. 104 2007 1069 1074
156. H. Meyer, M. Bug, and S. Bremer Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system Nat. Cell Biol. 14 2012 117 123
157. K. Bolte, N. Gruenheit, G. Felsner, M.S. Sommer, U.G. Maier, and F. Hempel Making new of old: recycling and modification of an ancient protein translocation system during eukaryotic evolution. Mechanistic comparison and phylogenetic analysis of ERAD, SELMA and the peroxisomal importomer Bioessays 33 2011 368 376
158. K. Yamanaka, Y. Sasagawa, and T. Ogura Recent advances in p97/VCP/Cdc48 cellular functions Biochim. Biophys. Acta 1823 2012 130 137
159. W. Schliebs, W. Girzalsky, and R. Erdmann Peroxisomal protein import and ERAD: variations on a common theme Nat. Rev. Mol. Cell Biol. 11 2010 885 890
160. V.I. Titorenko, and R.A. Rachubinski Peroxisomal membrane fusion requires two AAA family ATPases, Pex1p and Pex6p J. Cell Biol. 150 2000 881 886
161. A. van der Zand, J. Gent, I. Braakman, and H.F. Tabak Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes Cell 149 2012 397 409
162. C. Zhao, E.C. Smith, and S.W. Whiteheart Requirements for the catalytic cycle of the N-ethylmaleimide-sensitive factor (NSF) Biochim. Biophys. Acta 1823 2012 159 171
163. H.F. Tabak, I. Braakman, and A. van der Zand Peroxisome formation and maintenance are dependent on the endoplasmic reticulum Annu. Rev. Biochem. 82 2013 723 744
164. F.L. Theodoulou, K. Bernhardt, N. Linka, and A. Baker Peroxisome membrane proteins: multiple trafficking routes and multiple functions? Biochem. J. 451 2013 345 352
165. D.R. Warner, E.A. Roberts, R.M. Greene, and M.M. Pisano Identification of novel Smad binding proteins Biochem. Biophys. Res. Commun. 312 2003 1185 1190
166. J.G. Seo, C.Y. Lai, M.V. Miceli, and S.M. Jazwinski A novel role of peroxin PEX6: suppression of aging defects in mitochondria Aging Cell 6 2007 405 413
167. H. Jungwirth, J. Ring, T. Mayer, A. Schauer, S. Buttner, T. Eisenberg, D. Carmona-Gutierrez, K. Kuchler, and F. Madeo Loss of peroxisome function triggers necrosis FEBS Lett. 582 2008 2882 2886
168. D. Dietrich, F. Seiler, F. Essmann, and G. Dodt Identification of the kinesin KifC3 as a new player for positioning of peroxisomes and other organelles in mammalian cells Biochim. Biophys. Acta 1833 2013 3013 3024
169. A.M. Choi, S.W. Ryter, and B. Levine Autophagy in human health and disease N. Engl. J. Med. 368 2013 651 662
170. M. Nordgren, B. Wang, O. Apanasets, and M. Fransen Peroxisome degradation in mammals: mechanisms of action, recent advances, and perspectives Front. Physiol. 4 2013 145
171. A. Till, R. Lakhani, S.F. Burnett, and S. Subramani Pexophagy: the selective degradation of peroxisomes Int. J. Cell Biol. 2012 2012 512721
172. H. Abrahamsen, H. Stenmark, and H.W. Platta Ubiquitination and phosphorylation of Beclin 1 and its binding partners: tuning class III phosphatidylinositol 3-kinase activity and tumor suppression FEBS Lett. 586 2012 1584 1591
173. S. Shaid, C.H. Brandts, H. Serve, and I. Dikic Ubiquitination and selective autophagy Cell. Death Differ. 20 2013 21 30
174. J.C. Farré, A. Burkenroad, S.F. Burnett, and S. Subramani Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11 EMBO Rep. 14 2013 441 449
175. J.C. Farré, R.D. Mathewson, R. Manjithaya, and S. Subramani Roles of Pichia pastoris Uvrag in vacuolar protein sorting and the phosphatidylinositol 3-kinase complex in phagophore elongation in autophagy pathways Autophagy 6 2010 86 99
176. S. Grunau, D. Lay, S. Mindthoff, H.W. Platta, W. Girzalsky, W.W. Just, and R. Erdmann The Phosphoinositide-3-kinase Vps34p is required for pexophagy in Saccharomyces cerevisae Biochem. J. 434 2011 161 170
177. J.A. Kiel, K.B. Rechinger, I.J. van der Klei, F.A. Salomons, V.I. Titorenko, and M. Veenhuis The Hansenula polymorpha PDD1 gene product, essential for the selective degradation of peroxisomes, is a homologue of Saccharomyces cerevisiae Vps34p Yeast 15 1999 741 754
178. P.K. Kim, D.W. Hailey, R.T. Mullen, and J. Lippincott-Schwartz Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes Proc. Natl. Acad. Sci. U. S. A. 105 2008 20567 20574
179. S. Yamashita, M. Oku, Y. Wasada, Y. Ano, and Y. Sakai PI4P-signaling pathway for the synthesis of a nascent membrane structure in selective autophagy J. Cell Biol. 173 2006 709 717
180. E. Deosaran, K.B. Larsen, R. Hua, G. Sargent, Y. Wang, S. Kim, T. Lamark, M. Jauregui, K. Law, J. Lippincott-Schwartz, A. Brech, T. Johansen, and P.K. Kim NBR1 acts as an autophagy receptor for peroxisomes J. Cell Sci. 126 2013 939 952
181. V. Kirkin, T. Lamark, Y.S. Sou, G. Bjørkøy, J.L. Nunn, J.A. Bruun, E. Shvets, D.G. McEwan, T.H. Clausen, P. Wild, I. Bilusic, J.P. Theurillat, A. Overvatn, T. Ishii, Z. Elazar, M. Komatsu, I. Dikic, and T. Johansen A role for NBR1 in autophagosomal degradation of ubiquitinated substrates Mol. Cell 33 2009 505 516
182. S. Pankiv, T.H. Clausen, T. Lamark, A. Brech, J.A. Bruun, H. Outzen, A. Overvatn, G. Bjørkøy, and T. Johansen p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy J. Biol. Chem. 282 2007 24131 24145
183. A.R. Bellu, F.A. Salomons, J.A. Kiel, M. Veenhuis, and I.J. Van Der Klei Removal of Pex3p is an important initial stage in selective peroxisome degradation in Hansenula polymorpha J. Biol. Chem. 277 2002 42875 42880
184. C. Williams, and I.J. van der Klei Pexophagy-linked degradation of the peroxisomal membrane protein Pex3p involves the ubiquitin-proteasome system Biochem. Biophys. Res. Commun. 438 2013 395 401
185. J. Kallijärvi, U. Lahtinen, R. Hämäläinen, M. Lipsanen-Nyman, J.J. Palvimo, and A.E. Lehesjoki TRIM37 defective in mulibrey nanism is a novel RING finger ubiquitin E3 ligase Exp. Cell Res. 308 2005 146 155
186. J. Kallijarvi, K. Avela, M. Lipsanen-Nyman, I. Ulmanen, and A.E. Lehesjoki The TRIM37 gene encodes a peroxisomal RING-B-Box-coiled-coil protein: classification of mulibrey nanism as a new peroxisomal disorder Am. J. Hum. Genet. 70 2002
187. M.M. Molusky, D. Ma, K. Buelow, L. Yin, and J.D. Lin Peroxisomal localization and circadian regulation of ubiquitin-specific protease 2 PLoS One 7 2012 e47970
188. M.M. Molusky, S. Li, D. Ma, L. Yu, and J.D. Lin Ubiquitin-specific protease 2 regulates hepatic gluconeogenesis and diurnal glucose metabolism through 11β-hydroxysteroid dehydrogenase 1 Diabetes 61 2012 1025 1035
189. H.W. Platta, and H. Stenmark Endocytosis and signaling Curr. Opin. Cell Biol. 23 2011 393 403
190. V.F. Taelman, R. Dobrowolski, J.-L. Plouhinec, L.C. Fuentealba, P.P. Vorwald, I. Gumper, D.D. Sabatini, and E.M. De Robertis Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes Cell 143 2010 1136 1148
191. F.J. Vizeacoumar, J.C. Torres-Guzman, Y.Y. Tam, J.D. Aitchison, and R.A. Rachubinski YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size, and distribution in Saccharomyces cerevisiae J. Cell Biol. 161 2003 321 332
192. Y. Li, J. Yan, I. Kim, C. Liu, K. Huo, and H. Rao Rad4 regulates protein turnover at a postubiquitylation step Mol. Biol. Cell 21 2010 177 185
193. C. Liu, D. van Dyk, P. Xu, V. Choe, H. Pan, J. Peng, B. Andrews, and H. Rao Ubiquitin chain elongation enzyme Ufd2 regulates a subset of Doa10 substrates J. Biol. Chem. 285 2010 10265 10272
194. T. Ravid, S.G. Kreft, and M. Hochstrasser Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways EMBO J. 25 2006 533 543
195. M. Fransen, M. Nordgren, B. Wang, and O. Apanasets Role of peroxisomes in ROS/RNS-metabolism: implications for human disease Biochim. Biophys. Acta 1822 2012 1363 1373
196. J. Wei, L. Zhai, J. Xu, and H. Wang Role of Bmi1 in H2A ubiquitylation and Hox gene silencing J. Biol. Chem. 281 2006 22537 22544
197. I. Alchanati, C. Teicher, G. Cohen, V. Shemesh, H.M. Barr, P. Nakache, D. Ben-Avraham, A. Idelevich, I. Angel, N. Livnah, S. Tuvia, Y. Reiss, D. Taglicht, and O. Erez The E3 ubiquitin-ligase Bmi1/Ring1A controls the proteasomal degradation of Top2alpha cleavage complex - a potentially new drug target PLoS One 4 2009 e8104
198. B. Eisenhaber, N. Chumak, F. Eisenhaber, and M.T. Hauser The ring between ring fingers (RBR) protein family Genome Biol. 8 2007 209
199. S.E. Ratzel, M.J. Lingard, A.W. Woodward, and B. Bartel Reducing PEX13 expression ameliorates physiological defects of late-acting peroxin mutants Traffic 12 2011 121 134
200. I.S. Alencastre, T.A. Rodrigues, C.P. Grou, M. Fransen, C. Sá-Miranda, and J.E. Azevedo Mapping the cargo protein membrane translocation step into the PEX5 cycling pathway J. Biol. Chem. 284 2009 27243 27251
201. N. Miyata, K. Hosoi, S. Mukai, and Y. Fujiki In vitro import of peroxisome-targeting signal type 2 (PTS2) receptor Pex7p into peroxisomes Biochim. Biophys. Acta 1793 2009 860 870
202. C. Dingell, W.A. Johns, and J.K. White To the moon and beyond Sci. Am. 297 2007 62 68