Peroxisome biogenesis, protein targeting mechanisms and PEX gene functions in plants

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 5, 2016, Pages 850-862

  Cross, Laura L ^a   Ebeed, Heba Talat ^a,b   Baker, Alison ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b Damietta University   (Egypt)

Author keywords

Biogenesis; Importomer; Membrane; Peroxin; Peroxisome; Plant

Indexed keywords

MATRIX PROTEIN; MEMBRANE PROTEIN; PERIPHERAL MYELIN PROTEIN 22; PEROXIN; PEROXIN 10; PEROXIN 16; PEROXIN 19; PEROXIN 2; PEROXIN 3; TAIL ANCHORED PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ARABIDOPSIS PROTEIN; CELL RECEPTOR; ISOPROTEIN; PEROXISOMAL TARGETING SIGNAL 2 RECEPTOR; PEX13 PROTEIN, ARABIDOPSIS; PEX14 PROTEIN, ARABIDOPSIS; REPRESSOR PROTEIN;

BIOGENESIS; ENDOPLASMIC RETICULUM; GENE FUNCTION; MOLECULAR DOCKING; NONHUMAN; PEROXISOME; PLANT CELL; PLANT GENETICS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; ARABIDOPSIS; CHEMISTRY; EUKARYOTIC CELL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; ORGANELLE BIOGENESIS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE PROTEINS; ORGANELLE BIOGENESIS; PEROXISOMES; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EID: 84961129466     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.09.027     Document Type: Review

References (153)

1. de Duve C., Baudhuin P. Peroxisomes (microbodies and related particles). Physiol. Rev. 1966, 46. (323-&).
2. Kornberg H.L., Beevers H. Mechanism of conversion of fat to carbohydrate in castor beans. Nature 1957, 180:35-36.
3. Beevers H. Metabolic production of sucrose from fat. Nature 1961, 191:433-436.
4. Breidenbach R.W., Kahn A., Beevers H. Characterization of glyoxysomes from castor bean endosperm. Plant Physiol. 1968, 43:705-713.
5. Cooper T.G., Beevers H. β-Oxidation in glyoxysomes from castor bean endosperm. J. Biolumin. Chemilumin. 1969, 244:3515-3520.
6. Tolbert N.E. Microbodies-peroxisomes and glyoxysomes. Annu. Rev. Plant Physiol. 1971, 22. (45-&).
7. Linka N., Esser C. Transport proteins regulate the flux of metabolites and cofactors across the membrane of plants peroxisomes. Front. Plant Sci. 2012, 3.
8. Linka N., Theodoulou F.L. Metabolite transporters of the plant peroxisomal membrane: known and unknown. Subcell. Biochem. 2013, 69:169-194.
9. Pracharoenwattana I., Smith S.M. When is a peroxisome not a peroxisome?. Trends Plant Sci. 2008, 13:522-525.
10. Beevers H. Microbodies in higher plants. Annu. Rev. Plant Physiol. 1979, 30:159-193.
11. Frederick S.E., Newcomb E.H. Cytochemical localisation of catalase in leaf microbodies (peroxisomes). J. Cell Biol. 1969, 43:343-353.
12. Kindl H. The biosynthesis of microbodies (peroxisomes and glyoxysomes). Int. Rev. Cytol. 1982, 80:193-229.
13. Hu J., Baker A., Bartel B., Linka N., Mullen R.T., Reumann S., Zolman B.K. Plant peroxisomes: biogenesis and function. Plant Cell 2012, 24:2279-2303.
14. Collings D.A., Harper J.D.I., Marc J., Overall R.L., Mullen R.T. Life in the fast lane: actin-based motility of plant peroxisomes. Can. J. Bot. 2002, 80:430-441.
15. Jedd G., Chua N.-H. Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol. 2002, 43:384-392.
16. Scott I., Sparkes I.A., Logan D.C. The missing link: inter-organellar connections in mitochondria and peroxisomes?. Trends Plant Sci. 2007, 12:380-381.
17. Sinclair A.M., Trobacher C.P., Mathur N., Greenwood J.S., Mathur J. Peroxule extension over ER-defined paths constitutes a rapid subcellular response to hydroxyl stress. Plant J. 2009, 59:231-242.
18. Mano S., Nakamori C., Kondo M., Hayashi M., Nishimura M. An arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J. 2004, 38:487-498.
19. Barton K., Mathur N., Mathur J. Simultaneous live-imaging of peroxisomes and the ER in plant cells suggests contiguity but no lumina' continuity between the two organelles. Front. Physiol. 2013, 4.
20. Kim P.K., Hettema E.H. Multiple pathways for protein transport to peroxisomes. J. Mol. Biol. 2015, 427:1176-1190.
21. Nito K., Kamigaki A., Kondo M., Hayashi M., Nishimura M. Functional classification of arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant Cell Physiol. 2007, 48:763-774.
22. Hadden D.A., Phillipson B.A., Johnston K.A., Brown L.-A., Manfield I.W., El-Shami M., Sparkes I.A., Baker A. Arabidopsis PEX19 is a dimeric protein that binds the peroxin PEX10. Mol. Membr. Biol. 2006, 23:325-336.
23. Nyathi Y., Zhang X., Baldwin J.M., Bernhardt K., Johnson B., Baldwin S.A., Theodoulou F.L., Baker A. Pseudo half-molecules of the ABC transporter, COMATOSE, bind Pex19 and target to peroxisomes independently but are both required for activity. FEBS Lett. 2012, 586:2280-2286.
24. Nyathi Y., Lousa C.D.M., van Roermund C.W., Wanders R.J.A., Johnson B., Baldwin S.A., Theodoulou F.L., Baker A. The arabidopsis peroxisomal ABC transporter, comatose, complements the Saccharomyces cerevisiae pxa1 pxa2 delta mutant for metabolism of long-chain fatty acids and exhibits fatty acyl-CoA-stimulated ATPase activity. J. Biolumin. Chemilumin. 2010, 285:29892-29902.
25. Zhang X., Lousa C.D.M., Schutte-Lensink N., Ofman R., Wanders R.J., Baldwin S.A., Baker A., Kemp S., Theodoulou F.L. Conservation of targeting but divergence in function and quality control of peroxisomal ABC transporters: an analysis using cross-kingdom expression. Biochem. J. 2011, 436:547-557.
26. Theodoulou F.L., Bernhardt K., Linka N., Baker A. Peroxisome membrane proteins: multiple trafficking routes and multiple functions?. Biochem. J. 2013, 451:345-352.
27. Ma C., Hagstrom D., Polley S.G., Subramani S. Redox-regulated cargo binding and release by the peroxisomal targeting signal receptor, Pex5. J. Biolumin. Chemilumin. 2013, 288:27220-27231.
28. Stanley W.A., Filipp F.V., Kursula P., Schueller N., Erdmann R., Schliebs W., Sattler M., Wilmanns M. Recognition of a functional peroxisome type 1 target by the dynamic import receptor Pex5p. Mol. Cell 2006, 24:653-663.
29. Schueller N., Holton S.J., Fodor K., Milewski M., Konarev P., Stanley W.A., Wolf J., Erdmann R., Schliebs W., Song Y.-H., Wilmanns M. The peroxisomal receptor Pex19p forms a helical mPTS recognition domain. EMBO J. 2010, 29:2491-2500.
30. Schliebs W., Saidowsky J., Agianian B., Dodt G., Herberg F.W., Kunau W.H. Recombinant human peroxisomal targeting signal receptor PEX5 - structural basis for interaction of PEX5 with PEX14. J. Biolumin. Chemilumin. 1999, 274:5666-5673.
31. Lanyon-Hogg T., Hooper J., Gunn S., Warriner S.L., Baker A. PEX14 binding to arabidopsis PEX5 has differential effects on PTS1 and PTS2 cargo occupancy of the receptor. FEBS Lett. 2014, 588:2223-2229.
32. Fang Y., Morrell J.C., Jones J.M., Gould S.J. PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins. J. Cell Biol. 2004, 164:863-875.
33. Schmidt F., Treiber N., Zocher G., Bjelic S., Steinmetz M.O., Kalbacher H., Stehle T., Dodt G. Insights into peroxisome function from the structure of PEX3 in complex with a soluble fragment of PEX19. J. Biolumin. Chemilumin. 2010, 285:25410-25417.
34. Sato Y., Shibata H., Nakatsu T., Nakano H., Kashiwayama Y., Imanaka T., Kato H. Structural basis for docking of peroxisomal membrane protein carrier Pex19p onto its receptor Pex3p. EMBO J. 2010, 29:4083-4093.
35. Nordgren M., Fransen M. Peroxisomal metabolism and oxidative stress. Biochimie 2014, 98C:56-62.
36. Hunt J.E., Trelease R.N. Sorting pathway and molecular targeting signals for the arabidopsis peroxin 3. Biochem. Biophys. Res. Commun. 2004, 314:586-596.
37. Banjoko A., Trelease R.N. Development and application of an in-vivo plant peroxisome import system. Plant Physiol. 1995, 107:1201-1208.
38. Fakieh M.H., Drake P.J.M., Lacey J., Munck J.M., Motley A.M., Hettema E.H. Intra-ER sorting of the peroxisomal membrane protein Pex3 relies on its luminal domain. Biology Open 2013, 2:829-837.
39. Tam Y.Y.C., Fagarasanu A., Fagarasanu M., Rachubinski R.A. Pex3p initiates the formation of a preperoxisomal compartment from a subdomain of the endoplasmic reticulum in Saccharomyces cerevisiae. J. Biolumin. Chemilumin. 2005, 280:34933-34939.
40. Halbach A., Rucktaeschel R., Rottensteiner H., Erdmann R. The N-domain of Pex22p can functionally replace the Pex3p N-domain in targeting and peroxisome formation. J. Biolumin. Chemilumin. 2009, 284:3906-3916.
41. 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.
42. Lin Y., Sun L., Nguyen L.V., Rachubinski R.A., Goodman H.M. The pex16p homolog SSE1 and storage organelle formation in arabidopsis seeds. Science 1999, 284:328-330.
43. Lin Y., Cluette-Brown J.E., Goodman H.M. The peroxisome deficient arabidopsis mutant sse1 exhibits impaired fatty acid synthesis. Plant Physiol. 2004, 135:814-827.
44. Karnik S.K., Trelease R.N. Arabidopsis peroxin 16 coexists at steady state in peroxisomes and endoplasmic reticulum. Plant Physiol. 2005, 138:1967-1981.
45. Karnik S.K., Trelease R.N. Arabidopsis peroxin 16 trafficks through the ER and an intermediate compartment to pre-existing peroxisomes via overlapping molecular targeting signals. J. Exp. Bot. 2007, 58:1677-1693.
46. Hua R., Gidda S.K., Aranovich A., Mullen R.T., Kim P.K. Multiple domains in PEX16 mediate its trafficking and recruitment of peroxisomal proteins to the ER. Traffic 2015, 16:832-852.
47. Titorenko V.I., Ogrydziak D.M., Rachubinski R.A. Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 1997, 17:5210-5226.
48. Sparkes I.A., Hawes C., Baker A. AtPEX2 and AtPEX10 are targeted to peroxisomes independently of known endoplasmic reticulum trafficking routes. Plant Physiol. 2005, 139:690-700.
49. Flynn C.R., Heinze M., Schumann U., Gietl C., Trelease R.N. Compartmentalization of the plant peroxin, AtPex10p, within subdomain(s) of ER. Plant Sci. 2005, 168:635-652.
50. Rokka A., Antonenkov V.D., Soininen R., Immonen H.L., Pirilä P.I.L., Bergmann U., Sormunen R.T., Weckström M., Benz R., Hiltunen J.K. Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane. PLoS One 2009, 4.
51. Tugal H.B., Pool M., Baker A. Arabidopsis 22-kilodalton peroxisomal membrane protein. Nucleotide sequence analysis and biochemical characterization. Plant Physiol. 1999, 120:309-320.
52. Murphy M.A., Phillipson B.A., Baker A., Mullen R.T. Characterization of the targeting signal of the arabidopsis 22-kD integral peroxisomal membrane protein. Plant Physiol. 2003, 133:813-828.
53. Pause B., Saffrich R., Hunziker A., Ansorge W., Just W.W. Targeting of the 22 kDa integral peroxisomal membrane protein. FEBS Lett. 2000, 471:23-28.
54. Abell B.M., Mullen R.T. Tail-anchored membrane proteins: exploring the complex diversity of tail-anchored-protein targeting in plant cells. Plant Cell Rep. 2011, 30:137-151.
55. van der Zand A., Braakman I., Tabak H.F. Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol. Biol. Cell 2010, 21:2057-2065.
56. Chen Y., Pieuchot L., Loh R.A., Yang J., Kari T.M.A., Wong J.Y., Jedd G. Hydrophobic handoff for direct delivery of peroxisome tail-anchored proteins. Nat. Commun. 2014, 5:1-12.
57. Halbach A., Landgraf C., Lorenzen S., Rosenkranz K., Volkmer-Engert R., Erdmann R., Rottensteiner H. Targeting of the tail-anchored peroxisomal membrane proteins PEX26 and PEX15 occurs through C-terminal PEX19-binding sites. J. Cell Sci. 2006, 119:2508-2517.
58. Mullen R.T., Lisenbee C.S., Miernyk J.A., Trelease R.N. Peroxisomal membrane ascorbate peroxidase is sorted to a membranous network that resembles a subdomain of the endoplasmic reticulum. Plant Cell 1999, 11:2167-2185.
59. Nito K., Yamaguchi K., Kondo M., Hayashi M., Nishimura M. Pumpkin peroxisomal ascorbate peroxidase is localized on peroxisomal membranes and unknown membranous structures. Plant Cell Physiol. 2001, 42:20-27.
60. Lisenbee C.S., Karnik S.K., Trelease R.N. Overexpression and mislocalization of a tail-anchored GFP redefines the identity of peroxisomal ER. Traffic 2003, 4:491-501.
61. Mullen R.T., Trelease R.N. The ER-peroxisome connection in plants: development of the "ER semi-autonomous peroxisome maturation and replication" model for plant peroxisome biogenesis. Biochim. Biophys. Acta, Mol. Cell Res. 1763, 2006:1655.
62. Mullen R.T., Trelease R.N. The sorting signals for peroxisomal membrane-bound ascorbate peroxidase are within its C-terminal tail. J. Biolumin. Chemilumin. 2000, 275:16337-16344.
63. Shen G., Kuppu S., Venkataramani S., Wang J., Yan J., Qiu X., Zhang H. Ankyrin repeat-containing protein 2A is an essential molecular chaperone for peroxisomal membrane-bound ASCORBATE PEROXIDASE3 in arabidopsis. Plant Cell 2010, 22:811-831.
64. Bae W., Lee Y.J., Kim D.H., Lee J., Kim S., Sohn E.J., Hwang I. AKr2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat. Cell Biol. 2008, 10:220-227.
65. Zhang H., Li X., Zhang Y., Kuppu S., Shen G. Is AKR2A an essential molecular chaperone for a class of membrane-bound proteins in plants?. Plant Signal. Behav. 2010, 5:1520-1522.
66. McCartney A.W., Greenwood J.S., Fabian M.R., White K.A., Mullen R.T. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 2005, 17:3513-3531.
67. Rochon D.A., Singh B., Reade R., Theilmann J., Ghoshal K., Alam S.B., Maghodia A. The p33 auxiliary replicase protein of cucumber necrosis virus targets peroxisomes and infection induces de novo peroxisome formation from the endoplasmic reticulum. Virology 2014, 452-453:133-142.
68. Pathak K.B., Sasvari Z., Nagy P.D. The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology 2008, 379:294-305.
69. Sasvari Z., Gonzalez P.A., Rachubinski R.A., Nagy P.D. Tombusvirus replication depends on Sec39p endoplasmic reticulum-associated transport protein. Virology 2013, 447:21-31.
70. Perry R.J., Mast F.D., Rachubinski R.A. Endoplasmic reticulum-associated secretory proteins Sec20p, Sec39p, and Dsl1p are involved in peroxisome biogenesis. Eukaryot. Cell 2009, 8:830-843.
71. Nito K., Hayashi M., Nishimura M. Direct interaction and determination of binding domains among peroxisomal import factors in Arabidopsis thaliana. Plant Cell Physiol. 2002, 43:355-366.
72. Woodward A.W., Bartel B. The arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol. Biol. Cell 2005, 16:573-583.
73. N.M. Ramon, B. Bartel, Interdependence of the Peroxisome-targeting Receptors in Arabidopsis thaliana: PEX7 Facilitates PEX5 Accumulation and Import of PTS1 Cargo into Peroxisomes, Mol. Biol. Cell, 21 1263-1271.
74. Purdue P.E., Yang X.D., Lazarow P.B. Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J. Cell Biol. 1998, 143:1859-1869.
75. Einwachter H., Sowinski S., Kunau W.H., Schliebs W. Yarrowia lipolytica Pex20p, Saccharomyces cerevisiae Pex18p/Pex21p and mammalian Pex5pL fulfil a common function in the early steps of the peroxisomal PTS2 import pathway. EMBO Rep. 2001, 2:1035-1039.
76. Lee J.R., Jang H.H., Park J.H., Jung J.H., Lee S.S., Park S.K., Chi Y.H., Moon J.C., Lee Y.M., Kim S.Y., Kim J.-Y., Yun D.-J., Cho M.J., Lee K.O., Lee S.Y. Cloning of two splice variants of the rice PTS1 receptor, OsPex5pL and OsPex5pS, and their functional characterization using pex5-deficient yeast and arabidopsis. Plant J. 2006, 47:457-466.
77. 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.
78. Mullen R.T., Lee M.S., Flynn C.R., Trelease R.N. Diverse amino acid residues function within the type 1 peroxisomal targeting signal. Implications for the role of accessory residues upstream of the type 1 peroxisomal targeting signal. Plant Physiol. 1997, 115:881-889.
79. Maynard E.L., Gatto G.J., Berg J.M. Pex5p binding affinities for canonical and noncanonical PTS1 peptides. Proteins: Struct., Funct., Bioinf. 2004, 55:856-861.
80. Reumann S. Toward a definition of the complete proteome of plant peroxisomes: where experimental proteomics must be complemented by bioinformatics. Proteomics 2011, 11:1764-1779.
81. Lingner T., Kataya A.R., Antonicelli G.E., Benichou A., Nilssen K., Chen X.Y., Siemsen T., Morgenstern B., Meinicke P., Reumann S. Identification of novel plant peroxisomal targeting signals by a combination of machine learning methods and in vivo subcellular targeting analyses. Plant Cell 2011, 23:1556-1572.
82. Chowdhary G., Kataya A.R.A., Lingner T., Reumann S. Non-canonical peroxisome targeting signals: identification of novel PTS1 tripeptides and characterization of enhancer elements by computational permutation Analysis. BMC Plant Biol. 2012, 12. 10.1186/1471-2229-1112-1142.
83. Ramirez R.A., Espinoza B., Kwok E.Y. Identification of two novel type 1 peroxisomal targeting signals in Arabidopsis thaliana. Acta Histochem. 2014, 116:1307-1312.
84. Kataya A.R.A., Schei E., Lillo C. MAP kinase phosphatase 1 harbors a novel PTS1 and is targeted to peroxisomes following stress treatments. J. Plant Physiol. 2015, 179:12-20.
85. Reumann S., Buchwald D., Lingner T. PredPlantPTS1: a web server for the prediction of plant peroxisomal proteins. Front. Plant Sci. 2012, 3.
86. Skoulding N.S., Chowdhary G., Deus M.J., Baker A., Reumann S., Warriner S.L. Experimental validation of plant peroxisomal targeting prediction algorithms by systematic comparison of in vivo import efficiency and in vitro PTS1 binding affinity. J. Mol. Biol. 2015, 427:1085-1101.
87. Rachubinski R.A., Subramani S. How proteins penetrate peroxisomes. Cell 1995, 83:525-528.
88. Gonzalez N.H., Felsner G., Schramm F.D., Klingl A., Maier U.-G., Bolte K. A single peroxisomal targeting signal mediates matrix protein import in diatoms. PLoS One 2011, 6. 10.1371/journal.pone.0025316.
89. Zolman B.K., Yoder A., Bartel B. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 2000, 156:1323-1337.
90. Matsumura T., Otera H., Fujiki Y. Disruption of the interaction of the longer isoform of Pex5p, Pex5pL, with Pex7p abolishes peroxisome targeting signal type 2 - study with a novel PEX5-impaired Chinese hamster ovary cell mutant. J. Biolumin. Chemilumin. 2000, 275:21715-21721.
91. Khan B.R., Zolman B.K. PEX5 mutants that differentially disrupt PTS1 and PTS2 peroxisomal matrix protein import in arabidopsis. Plant Physiol. 2010, 154:1602-1615.
92. Hayashi M., Yagi M., Nito K., Kamada T., Nishimura M. Differential contribution of two peroxisomal protein receptors to the maintenance of peroxisomal functions in arabidopsis. J. Biolumin. Chemilumin. 2005, 280:14829-14835.
93. Gatto G.J., Geisbrecht B.V., Gould S.J., Berg J.M. Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat. Struct. Biol. 2000, 7:1091-1095.
94. Pan D., Nakatsu T., Kato H. Crystal structure of peroxisomal targeting signal-2 bound to its receptor complex Pex7p-Pex21p. Nat. Struct. Mol. Biol. 2013, 20. (987 - +).
95. Carvalho A.F., Costa-Rodrigues J., Correia I., Pessoa J.C., Faria T.Q., Martins C.L., Fransen M., Sa-Miranda C., Azevedo J.E. The N-terminal half of the peroxisomal cycling receptor Pex5p is a natively unfolded domain. J. Mol. Biol. 2006, 356:864-875.
96. McNew J.A., Goodman H.M. An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 1994, 127:1245-1257.
97. Glover J.R., Andrews D.W., Rachubinski R.A. Saccharomyces-cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10541-10545.
98. Kataya A.R.A., Heidari B., Hagen L., Kommedal R., Slupphaug G., Lillo C. Protein phosphatase 2A holoenzyme is targeted to peroxisomes by piggybacking and positively affects peroxisomal beta-oxidation. Plant Physiol. 2015, 167. (493-U335).
99. Hayashi M., Nito K., Toriyama-Kato K., Kondo M., Yamaya T., Nishimura M. AtPex14p maintains peroxisomal functions by determining protein targeting to three kinds of plant peroxisomes. EMBO J. 2000, 19:5701-5710.
100. Monroe-Augustus M., Ramon N.M., Ratzel S.E., Lingard M.J., Christensen S.E., Murali C., Bartel B. Matrix proteins are inefficiently imported into arabidopsis peroxisomes lacking the receptor-docking peroxin PEX14. Plant Mol. Biol. 2011, 77:1-15.
101. Burkhart S.E., Lingard M.J., Bartel B. Genetic dissection of peroxisome-associated matrix protein degradation in Arabidopsis thaliana. Genetics 2013, 193:125-141.
102. Woodward A.W., Fleming W.A., Burkhart S.E., Ratzel S.E., Bjornson M., Bartel B. A viable arabidopsis pex13 missense allele confers severe peroxisomal defects and decreases PEX5 association with peroxisomes. Plant Mol. Biol. 2014, 86:201-214.
103. Mano S., Nakamori C., Nito K., Kondo M., Nishimura M. The arabidopsis pex12 and pex13 mutants are defective in both PTS1- and PTS2-dependent protein transport to peroxisomes. Plant J. 2006, 47:604-618.
104. Boisson-Dernier A., Frietsch S., Kim T.-H., Dizon M.B., Schroeder J.I. The peroxin loss-of-function mutation abstinence by mutual consent disrupts male-female gametophyte recognition. Curr. Biol. 2008, 18:63-68.
105. Ratzel S.E., Lingard M.J., Woodward A.W., Bartel B. Reducing PEX13 expression ameliorates physiological defects of late-acting peroxin mutants. Traffic 2011, 12:121-134.
106. 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.
107. Salomons F.A., Kiel J., 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. Biolumin. Chemilumin. 2000, 275:12603-12611.
108. Freitas M.O., Francisco T., Rodrigues T.A., Alencastre I.S., Pinto M.P., Grou C.P., Carvalho A.F., Fransen M., Sa-Miranda C., Azevedo J.E. PEX5 protein binds monomeric catalase blocking its tetrarnerization and releases it upon binding the N-terminal domain of PEX14. J. Biolumin. Chemilumin. 2011, 286:40509-40519.
109. Brown L.-A., O'Leary-Steele C., Brookes P., Armitage L., Kepinski S., Warriner S.L., Baker A. A small molecule with differential effects on the PTS1 and PTS2 peroxisome matrix import pathways. Plant J. 2011, 65:980-990.
110. 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.
111. Deshaies R.J., Joazeiro C.A.P. RING Domain E3 Ubiquitin Ligases. Annu Rev Biochem 2009, vol. 78:399-434.
112. 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.
113. Platta H.W., Magraoui F.E., 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.
114. 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.
115. El Magraoui F., Schroetter A., Brinkmeier R., Kunst L., Mastalski T., Mueller T., Marcus K., Meyer H.E., Girzalsky W., Erdmann R., Platta H.W. The cytosolic domain of Pex22p stimulates the Pex4p-dependent ubiquitination of the PTS1-Receptor. PLoS ONE 2014, 9. 10.1371/journal.pone.0105894.
116. Kaur N., Zhao Q., Xie Q., Hu J. Arabidopsis RING peroxins are E3 ubiquitin ligases that interact with two homologous ubiquitin receptor proteins. J. Integr. Plant Biol. 2013, 55:108-120.
117. Burkhart S.E., Kao Y.-T., Bartel B. Peroxisomal ubiquitin-protein ligases Peroxin2 and Peroxin10 have distinct but synergistic roles in matrix protein import and Peroxin5 retrotranslocation in arabidopsis. Plant Physiol. 2014, 166:1329-1344.
118. Desai M., Kaur N., Hu J. Ectopic expression of the RING domain of the arabidopsis Peroxin2 protein partially suppresses the phenotype of the photomorphogenic mutant de-etiolated1. PLoS ONE 2014, 9.
119. Hu J.P., Aguirre M., Peto C., Alonso J., Ecker J., Chory J. A role for peroxisomes in photomorphogenesis and development of arabidopsis. Science 2002, 297:405-409.
120. Kamigaki A., Kondo M., Mano S., Hayashi M., Nishimura M. Suppression of peroxisome biogenesis factor 10 reduces cuticular wax accumulation by disrupting the ER network in Arabidopsis thaliana. Plant Cell Physiol. 2009, 50:2034-2046.
121. Prestele J., Hierl G., Scherling C., Hetkamp S., Schwechheimer C., Isono E., Weckwerth W., Wanner G., Gietl C. Different functions of the C(3)HC(4) zinc RING finger peroxins PEX10, PEX2, and PEX12 in peroxisome formation and matrix protein import. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14915-14920.
122. Schumann U., Wanner G., Veenhuis M., Schmid M., Gietl C. AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during arabidopsis embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9626-9631.
123. Sparkes I.A., Brandizzi F., Slocombe S.P., El-Shami M., Hawes C., Baker A. An arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol. 2003, 133:1809-1819.
124. Fan J.L., Quan S., Orth T., Awai C., Chory J., Hu J.P. The arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol. 2005, 139:231-239.
125. Cui S., Fukao Y., Mano S., Yamada K., Hayashi M., Nishimura M. Proteomic analysis reveals that the Rab GTPase RabE1c is involved in the degradation of the peroxisomal protein receptor PEX7 (peroxin 7). J. Biolumin. Chemilumin. 2013, 288:6014-6023.
126. Goto S., Mano S., Nakamori C., Nishimura M. Arabidopsis aberrant peroxisome morphology9 is a peroxin that recruits the PEX1-PEX6 complex to peroxisomes. Plant Cell 2011, 23:1573-1587.
127. Li X.-R., Li H.-J., Yuan L., Liu M., Shi D.-Q., Liu J., Yang W.-C. Arabidopsis DAYU/ABERRANT PEROXISOME MORPHOLOGY9 is a key regulator of peroxisome biogenesis and plays critical roles during pollen maturation and germination in planta. Plant Cell 2014, 26:619-635.
128. Zolman B.K., Bartel B. 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. 2004, 101:1786-1791.
129. Ciniawsky S., Grimm I., Saffian D., Girzalsky W., Erdmann R., Wendler P. Molecular snapshots of the Pex1/6 AAA+ complex in action. Nat. Commun. 2015, 6. (7331-7331).
130. Delille H.K., Alves R., Schrader M. Biogenesis of peroxisomes and mitochondria: linked by division. Histochem. Cell Biol. 2009, 131:441-446.
131. Novikoff A., Shin W.Y. The endoplasmic reticulum in the golgi zone and its relation to microbodies, golgi apparatus and autophagic vacuoles in rat liver cells. J. Microsc. 1964, 3:187-206.
132. Lazarow P.B., Fujiki Y. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1985, 1:489-530.
133. Gabaldon T., Snel B., van Zimmeren F., Hemrika W., Tabak H., Huynen M.A. Origin and evolution of the peroxisomal proteome. Biol. Direct 2006, 1. 10.1186/1745-6150-1181-1188.
134. Schluter A., Fourcade S., Ripp R., Mandel J.L., Poch O., Pujol A. The evolutionary origin of peroxisomes: an ER-peroxisome connection. Mol. Biol. Evol. 2006, 23:838-845.
135. Gabaldon T. A metabolic scenario for the evolutionary origin of peroxisomes from the endomembranous system. Cell. Mol. Life Sci. 2014, 71:2373-2376.
136. Sprecher H., Luthria D.L., Mohammed B.S., Baykousheva S.P. Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J. Lipid Res. 1995, 36:2471-2477.
137. Jarosch E., Lenk U., Sommer T. Endoplasmic reticulum-associated protein degradation. Int. Rev. Cytol. 2003, 223(223):39-81.
138. Codd G., Schmid G., Kowallik W. Enzymic evidence for peroxisomes in a mutant of Chlorella vulgaris. Arch. Mikrobiol. 1972, 81:264-272.
139. Shinozaki A., Sato N., Hayashi Y. Peroxisomal targeting signals in green algae. Protoplasma 2009, 235:57-66.
140. Kiel J.A.K.W., Hilbrands R.E., Bovenberg R.A.L., Veenhuis M. Isolation of Penicillium chrysogenum PEX1 and PEX6 encoding AAA proteins involved in peroxisome biogenesis. Appl. Microbiol. Biotechnol. 2000, 54:238-242.
141. van der Klei I.J., Veenhuis M. Yeast and filamentous fungi as model organisms in microbody research. Biochim. Biophys. Acta, Mol. Cell Res. 1763, 2006:1364.
142. Backeshoff K., Stabenau H. Peroxisomes in the alga Vaucheria are neither the leaf peroxisomal or the glyoxysomal type. Bot. Acta 1990, 103:190-196.
143. Winkler U., Saftel W., Stabenau H. Compartmentation of enzymes of the beta-oxidation pathway in algae. Biol. Chem. Hoppe Seyler 1989, 370. (794-794).
144. Stabenau H., Winkler U., Säftel W. Mitochondrial metabolism of glycolate in the alga Eremosphaera viridis. Z. Pflanzenphysiol. 1984, 29:1377-1388.
145. Kiel J.A.K.W., Veenhuis M., van der Klei I.J. PEX genes in fungal genomes: common, rare or redundant. Traffic 2006, 7:1291-1303.
146. Hayashi M. Plant peroxisomes: molecular basis of the regulation of their functions. J. Plant Res. 2000, 113:103-109.
147. Brown A.I., Kim P.K., Rutenberg A.D. PEX5 and ubiquitin dynamics on mammalian peroxisome membranes. PLoS Comput. Biol. 2014, 10. (e1003426-e1003426).
148. 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.
149. Gouveia A.M.M., Reguenga C., Oliveira M.E.M., Sa-Miranda C., Azevedo J.E. Characterization of peroxisomal Pex5p from rat liver - Pex5p in the Pex5p-Pex14p membrane complex is a transmembrane protein. J. Biolumin. Chemilumin. 2000, 275:32444-32451.
150. Hoepfner D., Schildknegt D., Braakman I., Philippsen P., Tabak H.F. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 2005, 122:85-95.
151. Thazar-Poulot N., Miquel M., Fobis-Loisy I., Gaude T. Peroxisome extensions deliver the arabidopsis SDP1 lipase to oil bodies. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:4158-4163.
152. Schwacke R., Schneider A., van der Graaff E., Fischer K., Catoni E., Desimone M., Frommer W.B., Flügge U.-I., Kunze R. ARAMEMNON, a novel database for arabidopsis integral membrane proteins. Plant Physiol. 2003, 131:16-26.
153. Hofman K. Tmbase-A database of membrane spanning protein segments. Biol. Chem. Hoppe Seyler 1993, 374.