Going against the flow: A case for peroxisomal protein export

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 7, 2014, Pages 1386-1392

  Williams, Chris ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Peroxisome; Protein degradation; Protein export; Protein transport; Ubiquitination

Indexed keywords

MATRIX PROTEIN; PROTEIN; VEGETABLE PROTEIN; SCLEROPROTEIN;

ACTIVE TRANSPORT; CELL FUNCTION; CELL MEMBRANE; PEROXISOMAL TARGETING SIGNAL; PEROXISOME; PICHIA ANGUSTA; PLANT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; UBIQUITINATION; AGING; ANIMAL; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; HUMAN; INTRACELLULAR MEMBRANE; METABOLIC ENCEPHALOPATHY; METABOLISM; PATHOLOGY; PICHIA;

AGING; ANIMALS; BRAIN DISEASES, METABOLIC, INBORN; ENDOPLASMIC RETICULUM; EUKARYOTIC CELLS; EXTRACELLULAR MATRIX PROTEINS; HUMANS; INTRACELLULAR MEMBRANES; PEROXISOMES; PICHIA; PLANTS; PROTEIN TRANSPORT; PROTEOLYSIS; UBIQUITINATION;

EID: 84899673989     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.04.009     Document Type: Review

References (92)

1. Gabaldon T. Peroxisome diversity and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365:765-773.
2. Islinger M., Cardoso M.J., Schrader M. Be different-the diversity of peroxisomes in the animal kingdom. Biochim. Biophys. Acta 2010, 1803:881-897.
3. Pieuchot L., Jedd G. Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu. Rev. Microbiol. 2012, 66:237-263.
4. Lazarow P.B. The role of peroxisomes in mammalian cellular metabolism. J. Inherit. Metab. Dis. 1987, 10:11-22.
5. Kiel J.A., van der Klei I.J., van den Berg M.A., Bovenberg R.A., Veenhuis M. Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet. Biol. 2005, 42:154-164.
6. Misset O., Bos O.J., Opperdoes F.R. Glycolytic enzymes of Trypanosoma brucei. Simultaneous purification, intraglycosomal concentrations and physical properties. Eur. J. Biochem. 1986, 157:441-453.
7. Mano S., Nishimura M. Plant peroxisomes. Vitam. Horm. 2005, 72:111-154.
8. Steinberg S.J., Dodt G., Raymond G.V., Braverman N.E., Moser A.B., Moser H.W. Peroxisome biogenesis disorders. Biochim. Biophys. Acta 2006, 1763:1733-1748.
9. Wanders R.J., Waterham H.R. Peroxisomal disorders: the single peroxisomal enzyme deficiencies. Biochim. Biophys. Acta 2006, 1763:1707-1720.
10. Terlecky S.R., Koepke J.I., Walton P.A. Peroxisomes and aging. Biochim. Biophys. Acta 2006, 1763:1749-1754.
11. Rottensteiner H., Kramer A., Lorenzen S., Stein K., Landgraf C., Volkmer-Engert R., Erdmann R. Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol. Biol. Cell 2004, 15:3406-3417.
12. Grou C.P., Carvalho A.F., Pinto M.P., Alencastre I.S., Rodrigues T.A., Freitas M.O., Francisco T., Sa-Miranda C., Azevedo J.E. The peroxisomal protein import machinery-a case report of transient ubiquitination with a new flavor. Cell. Mol. Life Sci. 2009, 66:254-262.
13. Williams C., Stanley W.A. Peroxin 5: A cycling receptor for protein translocation into peroxisomes. Int. J. Biochem. Cell Biol. 2010, 42:1771-1774.
14. Brocard C., Hartig A. Peroxisome targeting signal 1: is it really a simple tripeptide?. Biochim. Biophys. Acta 2006, 1763:1565-1573.
15. Lazarow P.B. The import receptor Pex7p and the PTS2 targeting sequence. Biochim. Biophys. Acta 2006, 1763:1599-1604.
16. Schliebs W., Kunau W.H. PTS2 co-receptors: diverse proteins with common features. Biochim. Biophys. Acta 2006, 1763:1605-1612.
17. Braverman N., Dodt G., Gould S.J., Valle D. An isoform of pex5p, the human PTS1 receptor, is required for the import of PTS2 proteins into peroxisomes. Hum. Mol. Genet. 1998, 7:1195-1205.
18. Matsuzaki T., Fujiki Y. The peroxisomal membrane protein import receptor Pex3p is directly transported to peroxisomes by a novel Pex19p- and Pex16p-dependent pathway. J. Cell Biol. 2008, 183:1275-1286.
19. Dimitrov L., Lam S.K., Schekman R. The role of the endoplasmic reticulum in peroxisome biogenesis. Cold Spring Harb. Perspect. Biol. 2013, 5.
20. Smith M.H., Ploegh H.L., Weissman J.S. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 2011, 334:1086-1090.
21. Perlmutter D.H. Pathogenesis of chronic liver injury and hepatocellular carcinoma in alpha-1-antitrypsin deficiency. Pediatr. Res. 2006, 60:233-238.
22. Heo J.M., Rutter J. Ubiquitin-dependent mitochondrial protein degradation. Int. J. Biochem. Cell Biol. 2011, 43:1422-1426.
23. Platta H.W., Grunau S., Rosenkranz K., Girzalsky W., Erdmann R. Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat. Cell Biol. 2005, 7:817-822.
24. Leon 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, 282:7424-7430.
25. Platta H.W., Girzalsky W., Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p. Biochem. J. 2004, 384:37-45.
26. Williams C., van den Berg M., Sprenger R.R., Distel B. A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J. Biol. Chem. 2007, 282:22534-22543.
27. Liu X., Subramani S. Unique requirements for mono- and polyubiquitination of the peroxisomal targeting signal co-receptor, Pex20. J. Biol. Chem. 2013, 288:7230-7240.
28. Carvalho A.F., Pinto M.P., Grou C.P., Alencastre I.S., Fransen M., Sa-Miranda C., Azevedo J.E. Ubiquitination of mammalian Pex5p, the peroxisomal import receptor. J. Biol. Chem. 2007, 282:31267-31272.
29. Hensel A., Beck S., El Magraoui F., Platta H.W., Girzalsky W., Erdmann R. Cysteine-dependent ubiquitination of Pex18p is linked to cargo translocation across the peroxisomal membrane. J. Biol. Chem. 2011, 286:43495-43505.
30. Platta H.W., El Magraoui F., Schlee D., Grunau S., Girzalsky W., Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J. Cell Biol. 2007, 177:197-204.
31. Leon S., Zhang L., McDonald W.H., Yates J., Cregg J.M., Subramani S. Dynamics of the peroxisomal import cycle of PpPex20p: ubiquitin-dependent localization and regulation. J. Cell Biol. 2006, 172:67-78.
32. Williams C., van den Berg M., Panjikar S., Stanley W.A., Distel B., Wilmanns M. Insights into ubiquitin-conjugating enzyme/co-activator interactions from the structure of the Pex4p:Pex22p complex. EMBO J. 2012, 31:391-402.
33. Kiel J.A., Emmrich K., Meyer H.E., Kunau W.H. 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. 2005, 280:1921-1930.
34. Grou C.P., Carvalho A.F., Pinto M.P., Wiese S., Piechura H., Meyer H.E., Warscheid B., Sa-Miranda C., Azevedo J.E. Members of the E2D (UbcH5) family mediate the ubiquitination of the conserved cysteine of Pex5p, the peroxisomal import receptor. J. Biol. Chem. 2008, 283:14190-14197.
35. Platta H.W., El Magraoui F., Baumer B.E., Schlee D., Girzalsky W., Erdmann R. Pex2 and pex12 function as protein-ubiquitin ligases in peroxisomal protein import. Mol. Cell. Biol. 2009, 29:5505-5516.
36. Williams C., van den Berg M., Geers E., Distel B. Pex10p functions as an E3 ligase for the Ubc4p-dependent ubiquitination of Pex5p. Biochem. Biophys. Res. Commun. 2008, 374:620-624.
37. El Magraoui F., Baumer B.E., Platta H.W., Baumann J.S., Girzalsky W., Erdmann R. 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. 2012, 279:2060-2070.
38. El Magraoui F., Brinkmeier R., Schrotter A., Girzalsky W., Muller T., Marcus K., Meyer H.E., Erdmann R., Platta H.W. Distinct ubiquitination cascades act on the peroxisomal targeting signal type 2 co-receptor Pex18p. Traffic 2013, 14:1290-1301.
39. Platta H.W., Debelyy M.O., El Magraoui F., Erdmann R. The AAA peroxins Pex1p and Pex6p function as dislocases for the ubiquitinated peroxisomal import receptor Pex5p. Biochem. Soc. Trans. 2008, 36:99-104.
40. Debelyy M.O., Platta H.W., Saffian D., Hensel A., Thoms S., Meyer H.E., Warscheid B., Girzalsky W., Erdmann R. Ubp15p, a ubiquitin hydrolase associated with the peroxisomal export machinery. J. Biol. Chem. 2011, 286:28223-28234.
41. Grou C.P., Francisco T., Rodrigues T.A., Freitas M.O., Pinto M.P., Carvalho A.F., Domingues P., Wood S.A., Rodriguez-Borges J.E., Sa-Miranda C., Fransen M., Azevedo J.E. Identification of ubiquitin-specific protease 9X (USP9X) as a deubiquitinase acting on ubiquitin-peroxin 5 (PEX5) thioester conjugate. J. Biol. Chem. 2012, 287:12815-12827.
42. Platta H.W., Hagen S., Erdmann R. The exportomer: the peroxisomal receptor export machinery. Cell. Mol. Life Sci. 2013, 70:1393-1411.
43. Platta H.W., Hagen S., Reidick C., Erdmann R. The peroxisomal receptor dislocation pathway: to the exportomer and beyond. Biochimie 2013, 98:16-28.
44. Titus D.E., Becker W.M. Investigation of the glyoxysome-peroxisome transition in germinating cucumber cotyledons using double-label immunoelectron microscopy. J. Cell Biol. 1985, 101:1288-1299.
45. Beevers H. Microbodies in higher-plants. Annu. Rev. Plant Physiol. 1979, 30:159-193.
46. Burke J.J., Trelease R.N. Cytochemical demonstration of malate synthase and glycolate oxidase in microbodies of cucumber cotyledons. Plant Physiol. 1975, 56:710-717.
47. Burkhart S.E., Lingard M.J., Bartel B. Genetic dissection of peroxisome-associated matrix protein degradation in Arabidopsis thaliana. Genetics 2013, 193:125-141.
48. Farmer L.M., Rinaldi M.A., Young P.G., Danan C.H., Burkhart S.E., Bartel B. Disrupting autophagy restores peroxisome function to an arabidopsis LON2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation. Plant Cell 2013, 25:4085-4100.
49. Lingard M.J., Monroe-Augustus M., Bartel B. Peroxisome-associated matrix protein degradation in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4561-4566.
50. Zolman B.K., Monroe-Augustus M., Silva I.D., Bartel B. Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 2005, 17:3422-3435.
51. Kim D.Y., Scalf M., Smith L.M., Vierstra R.D. Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis. Plant Cell 2013, 25:1523-1540.
52. Okumoto K., Kametani Y., Fujiki Y. Two proteases, trypsin domain-containing 1 (Tysnd1) and peroxisomal lon protease (PsLon), cooperatively regulate fatty acid beta-oxidation in peroxisomal matrix. J. Biol. Chem. 2011, 286:44367-44379.
53. Bartoszewska M., Williams C., Kikhney A., Opalinski L., van Roermund C.W., de Boer R., Veenhuis M., van der Klei I.J. Peroxisomal proteostasis involves a Lon family protein that functions as protease and chaperone. J. Biol. Chem. 2012, 287:27380-27395.
54. Lingard M.J., Bartel B. Arabidopsis LON2 is necessary for peroxisomal function and sustained matrix protein import. Plant Physiol. 2009, 151:1354-1365.
55. Omi S., Nakata R., Okamura-Ikeda K., Konishi H., Taniguchi H. Contribution of peroxisome-specific isoform of Lon protease in sorting PTS1 proteins to peroxisomes. J. Biochem. 2008, 143:649-660.
56. Bellu A.R., Salomons F.A., Kiel J.A., Veenhuis M., Van Der Klei I.J. Removal of Pex3p is an important initial stage in selective peroxisome degradation in Hansenula polymorpha. J. Biol. Chem. 2002, 277:42875-42880.
57. van der Klei I.J., Veenhuis M. Yeast and filamentous fungi as model organisms in microbody research. Biochim. Biophys. Acta 2006, 1763:1364-1373.
58. Sibirny A.A. Mechanisms of autophagy and pexophagy in yeasts. Biochemistry (Mosc) 2011, 76:1279-1290.
59. Yorimitsu T., Klionsky D.J. Autophagy: molecular machinery for self-eating. Cell Death Differ. 2005, 12:1542-1552.
60. Huybrechts S.J., Van Veldhoven P.P., Brees C., Mannaerts G.P., Los G.V., Fransen M. Peroxisome dynamics in cultured mammalian cells. Traffic 2009, 10:1722-1733.
61. Williams C., van der Klei I.J. Pexophagy-linked degradation of the peroxisomal membrane protein Pex3p involves the ubiquitin-proteasome system. Biochem. Biophys. Res. Commun. 2013, 438:395-401.
62. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., Harper J.W., Gygi S.P. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
63. Kim P.K., Mullen R.T., Schumann U., Lippincott-Schwartz J. The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER. J. Cell Biol. 2006, 173:521-532.
64. Fagarasanu A., Fagarasanu M., Rachubinski R.A. Maintaining peroxisome populations: a story of division and inheritance. Annu. Rev. Cell Dev. Biol. 2007, 23:321-344.
65. Fagarasanu M., Fagarasanu A., Tam Y.Y., Aitchison J.D., Rachubinski R.A. Inp1p is a peroxisomal membrane protein required for peroxisome inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2005, 169:765-775.
66. Fagarasanu A., Fagarasanu M., Eitzen G.A., Aitchison J.D., Rachubinski R.A. The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae. Dev. Cell 2006, 10:587-600.
67. Garcia-Alai M.M., Gallo M., Salame M., Wetzler D.E., McBride A.A., Paci M., Cicero D.O., de Prat-Gay G. Molecular basis for phosphorylation-dependent, PEST-mediated protein turnover. Structure 2006, 14:309-319.
68. Horiguchi H., Yurimoto H., Kato N., Sakai Y. Antioxidant system within yeast peroxisome. Biochemical and physiological characterization of CbPmp20 in the methylotrophic yeast Candida boidinii. J. Biol. Chem. 2001, 276:14279-14288.
69. Yamashita H., Avraham S., Jiang S., London R., Van Veldhoven P.P., Subramani S., Rogers R.A., Avraham H. Characterization of human and murine PMP20 peroxisomal proteins that exhibit antioxidant activity in vitro. J. Biol. Chem. 1999, 274:29897-29904.
70. Bener Aksam E., Jungwirth H., Kohlwein S.D., Ring J., Madeo F., Veenhuis M., van der Klei I.J. Absence of the peroxiredoxin Pmp20 causes peroxisomal protein leakage and necrotic cell death. Free Radic. Biol. Med. 2008, 45:1115-1124.
71. Nur E.K.A., Gross S.R., Pan Z., Balklava Z., Ma J., Liu L.F. Nuclear translocation of cytochrome c during apoptosis. J. Biol. Chem. 2004, 279:24911-24914.
72. Fahrenkrog B. The nuclear pore complex, nuclear transport, and apoptosis. Can. J. Physiol. Pharmacol. 2006, 84:279-286.
73. Tagwerker C., Flick K., Cui M., Guerrero C., Dou Y., Auer B., Baldi P., Huang L., Kaiser P. A tandem affinity tag for two-step purification under fully denaturing conditions: application in ubiquitin profiling and protein complex identification combined with in vivocross-linking. Mol. Cell. Proteomics 2006, 5:737-748.
74. Mayor T., Graumann J., Bryan J., MacCoss M.J., Deshaies R.J. Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell. Proteomics 2007, 6:1885-1895.
75. Seyfried N.T., Xu P., Duong D.M., Cheng D., Hanfelt J., Peng J. Systematic approach for validating the ubiquitinated proteome. Anal. Chem. 2008, 80:4161-4169.
76. Williams C., van den Berg M., Distel B. Saccharomyces cerevisiae Pex14p contains two independent Pex5p binding sites, which are both essential for PTS1 protein import. FEBS Lett. 2005, 579:3416-3420.
77. Saidowsky J., Dodt G., Kirchberg K., Wegner A., Nastainczyk W., Kunau W.H., Schliebs W. The di-aromatic pentapeptide repeats of the human peroxisome import receptor PEX5 are separate high affinity binding sites for the peroxisomal membrane protein PEX14. J. Biol. Chem. 2001, 276:34524-34529.
78. Stein K., Schell-Steven A., Erdmann R., Rottensteiner H. Interactions of Pex7p and Pex18p/Pex21p with the peroxisomal docking machinery: implications for the first steps in PTS2 protein import. Mol. Cell. Biol. 2002, 22:6056-6069.
79. Meinecke M., Cizmowski C., Schliebs W., Kruger V., Beck S., Wagner R., Erdmann R. The peroxisomal importomer constitutes a large and highly dynamic pore. Nat. Cell Biol. 2010, 12:273-277.
80. Azevedo J.E., Schliebs W. Pex14p, more than just a docking protein. Biochim. Biophys. Acta 2006, 1763:1574-1584.
81. Koek A., Komori M., Veenhuis M., van der Klei I.J. A comparative study of peroxisomal structures in Hansenula polymorpha pex mutants. FEMS Yeast Res. 2007, 7:1126-1133.
82. Van der Klei I.J., Hilbrands R.E., Kiel J.A., Rasmussen S.W., Cregg J.M., Veenhuis M. The ubiquitin-conjugating enzyme Pex4p of Hansenula polymorpha is required for efficient functioning of the PTS1 import machinery. EMBO J. 1998, 17:3608-3618.
83. Jung S., Smith J.J., von Haller P.D., Dilworth D.J., Sitko K.A., Miller L.R., Saleem R.A., Goodlett D.R., Aitchison J.D. Global analysis of condition-specific subcellular protein distribution and abundance. Mol. Cell. Proteomics 2013, 12:1421-1435.
84. Authier F., Bergeron J.J., Ou W.J., Rachubinski R.A., Posner B.I., Walton P.A. Degradation of the cleaved leader peptide of thiolase by a peroxisomal proteinase. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:3859-3863.
85. Koepke J.I., Wood C.S., Terlecky L.J., Walton P.A., Terlecky S.R. Progeric effects of catalase inactivation in human cells. Toxicol. Appl. Pharmacol. 2008, 232:99-108.
86. Mbonye U.R., Wada M., Rieke C.J., Tang H.Y., Dewitt D.L., Smith W.L. The 19-amino acid cassette of cyclooxygenase-2 mediates entry of the protein into the endoplasmic reticulum-associated degradation system. J. Biol. Chem. 2006, 281:35770-35778.
87. Dubois R.N., Abramson S.B., Crofford L., Gupta R.A., Simon L.S., Van De Putte L.B., Lipsky P.E. Cyclooxygenase in biology and disease. Faseb J. 1998, 12:1063-1073.
88. Goldstein J.L., Brown M.S. Regulation of the mevalonate pathway. Nature 1990, 343:425-430.
89. Jo Y., Debose-Boyd R.A. Control of cholesterol synthesis through regulated ER-associated degradation of HMG CoA reductase. Crit. Rev. Biochem. Mol. Biol. 2010, 45:185-198.
90. Baerends R.J., Salomons F.A., Faber K.N., Kiel J.A., Van der Klei I.J., Veenhuis M. Deviant Pex3p levels affect normal peroxisome formation in Hansenula polymorpha: high steady-state levels of the protein fully abolish matrix protein import. Yeast 1997, 13:1437-1448.
91. Bascom R.A., Chan H., Rachubinski R.A. Peroxisome biogenesis occurs in an unsynchronized manner in close association with the endoplasmic reticulum in temperature-sensitive Yarrowia lipolytica Pex3p mutants. Mol. Biol. Cell 2003, 14:939-957.
92. Kaur N., Zhao Q., Xie Q., Hu J. Arabidopsis RING peroxins are E3 ubiquitin ligases that interact with two homologous ubiquitin receptor proteins(F). J. Integr. Plant Biol. 2013, 55:108-120.