Reducing PEX13 expression ameliorates physiological defects of late-acting peroxin mutants

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Volumn 12, Issue 1, 2011, Pages 121-134

  Ratzel, Sarah E ^a   Lingard, Matthew J ^a,b   Woodward, Andrew W ^a,c   Bartel, Bonnie ^a  

^a RICE UNIVERSITY   (United States)

^b St Edward's University ^*  (United States)

^c ST EDWARD'S UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; Indole 3 butyric acid; Organelle targeting; Peroxin recycling; Peroxisome import

Indexed keywords

MATRIX PROTEIN; MEMBRANE PROTEIN; PEROXIN; PROTEIN PEX13; UNCLASSIFIED DRUG;

ALLELE; ARABIDOPSIS; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; GENE INTERACTION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; MODELS, BIOLOGICAL; MUTATION; PEROXISOMES; RNA;

EID: 78649981803     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01136.x     Document Type: Article

References (68)

1. Eckert JH, Erdmann R. Peroxisome biogenesis. Rev Physiol Biochem Pharmacol 2003;147:75-121.
2. Lanyon-Hogg T, Warriner SL, Baker A. Getting a camel through the eye of a needle: the import of folded proteins by peroxisomes. Biol Cell 2010;102:245-263.
3. Mullen RT, Flynn CR, Trelease RN. How are peroxisomes formed? The role of the endoplasmic reticulum and peroxins. Trends Plant Sci 2001;6:256-261.
4. Charlton W, López-Huertas E. PEX genes in plants and other organisms. In: Baker A, Graham IA, editors. Plant Peroxisomes. Biochemistry, Cell Biology and Biotechnological Applications. Dordrecht: Kluwer Academic Publishers; 2002, pp. 385-426.
5. Zolman BK, Yoder A, Bartel B. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 2000;156:1323-1337.
6. Zolman BK, 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.
7. Albertini M, Rehling P, Erdmann R, Girzalsky W, Kiel JAKW, Veenhuis M, Kunau WH. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 1997;89:83-92.
8. 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.
9. Niederhoff K, Meindl-Beinker NM, Kerssen D, Perband U, Schäfer A, Schliebs W, Kunau W-H. Yeast Pex14p possesses two functionally distinct Pex5p and one Pex7p binding sites. J Biol Chem 2005;280:35571-35578.
10. Elgersma Y, Kwast L, Klein A, Voorn-Brouwer T, Van Den Berg M, Metzig B, America T, Tabak HF, Distel B. The SH3 domain of the Saccharomyces cerevisiae peroxisomal membrane protein Pex13p functions as a docking site for Pex5p, a mobile receptor for the import PTS1-containing proteins. J Cell Biol 1996;135:97-109.
11. Erdmann R, Blobel G. Identification of Pex13p a peroxisomal membrane receptor for the PTS1 recognition factor. J Cell Biol 1996;135:111-121.
12. Gould SJ, Kalish JE, Morrell JC, Bjorkman J, Urquhart AJ, Crane DI. Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTs1 receptor. J Cell Biol 1996;135:85-95.
13. Girzalsky W, Rehling P, Stein K, Kipper J, Blank L, Kunau W-H, Erdmann R. Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J Cell Biol 1999;144:1151-1162.
14. Agne B, Meindl NM, Niederhoff K, Einwächter H, Rehling P, Sickmann A, Meyer HE, Girzalsky W, Kunau W-H. Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol Cell 2003;11:635-646.
15. Reguenga C, Oliveira MEM, Gouveia AMM, Sá-Miranda C, Azevedo JE. Characterization of the mammalian peroxisomal import machinery: Pex2p, Pex5p, Pex12p, and Pex14p are subunits of the same protein assembly. J Biol Chem 2001;276:29935-29942.
16. 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.
17. 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.
18. 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.
19. McNew JA, Goodman JM. An oligomeric protein is imported into peroxisomes in vivo. J Cell Biol 1994;127:1245-1257.
20. Erdmann R, Schliebs W. Peroxisomal matrix protein import: the transient pore model. Nat Rev Mol Cell Biol 2005;6:738-742.
21. 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;3:273-277.
22. Williams C, Van Den Berg M, Sprenger RR, Distel B. A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J Biol Chem 2007;282: 22534-22543.
23. Platta HW, Magraoui FE, Baumer BE, 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.
24. Koller A, Snyder WB, Faber KN, Wenzel TJ, Rangell L, Keller GA, Subramani S. Pex22p of Pichia pastoris, essential for peroxisomal matrix protein import, anchors the ubiquitin-conjugating enzyme, Pex4p, on the peroxisomal membrane. J Cell Biol 1999;146:99-112.
25. Zolman BK, Monroe-Augustus M, Silva ID, Bartel B. Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 2005;17:3422-3435.
26. Collins CS, Kalish JE, Morrell JC, McCaffery JM, Gould SJ. The peroxisome biogenesis factors Pex4p, Pex22p, Pex1p, and Pex6p act in the terminal steps of peroxisomal matrix protein import. Mol Cell Biol 2000;20:7516-7526.
27. Miyata N, Fujiki Y. Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export. Mol Cell Biol 2005;25:10822-10832.
28. Platta HW, 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.
29. Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL. Chewing the fat: β-oxidation in signalling and development. Trends Plant Sci 2006;11:124-132.
30. Hayashi M, Nishimura M. Arabidopsis thaliana- a model organism to study plant peroxisomes. Biochim Biophys Acta 2006;1763: 1382-1391.
31. Zolman BK, Nyberg M, Bartel B. IBR3, a novel peroxisomal acyl-CoA dehydrogenase-like protein required for indole-3-butyric acid response. Plant Mol Biol 2007;64:59-72.
32. Zolman BK, Martinez N, Millius A, Adham AR, Bartel B. Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics 2008;180:237-251.
33. Strader L, Culler Hendrickson A, Cohen J, Bartel B. Conversion of endogenous indole-3-butyric acid to indole-3-acetic acid drives cell expansion in Arabidopsis seedlings. Plant Physiol 2010;153: 1577-1586.
34. Zolman BK, Silva ID, Bartel B. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. Plant Physiol 2001;127:1266-1278.
35. Footitt S, Dietrich D, Fait A, Fernie AR, Holdsworth MJ, Baker A, Theodoulou FL. The COMATOSE ATP-binding cassette transporter is required for full fertility in Arabidopsis. Plant Physiol 2007;144:1467-1480.
36. Strader L, Bartel B. The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 2009;21:1992-2007.
37. Ramón NM, Bartel B. Interdependence of the peroxisome-targeting receptors in Arabidopsis thaliana: PEX7 facilitates PEX5 accumulation and import of PTS1 cargo into peroxisomes. Mol Cell Biol 2010;21:1263-1271.
38. Hayashi M, Toriyama K, Kondo M, Nishimura M. 2, 4-Dichloro phenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid β-oxidation. Plant Cell 1998;10:183-195.
39. Monroe-Augustus M, Martínez Ramón N, Ratzel SE, Lingard MJ, Murali C, Bartel B. Differential PTS1 and PTS2 import defects reveal a distinct role for Arabidopsis PEX14 in the PTS1 pathway of peroxisomal matrix protein import. 2010; submitted.
40. Woodward AW, 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.
41. Boisson-Dernier A, Frietsch S, Kim T-H, Dizon MB, Schroeder JI. The peroxin loss-of-function mutation abstinence by mutual consent disrupts recognition between male and female gametophytes. Curr Biol 2008;18:63-68.
42. Hu J, 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.
43. 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.
44. Sparkes IA, Brandizzi F, Slocombe SP, 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.
45. Fan J, Quan S, Orth T, Awai C, Chory J, Hu J. The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol 2005;139:231-239.
46. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003;301: 653-657.
47. Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC. The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 2003;20:735-747.
48. Schumann H, Huesgen PF, Gietl C, Adamska I. The DEG15 serine protease cleaves peroxisomal targeting signal 2-containing proteins in Arabidopsis. Plant J 2008;148:1847-1856.
49. Lingard MJ, Monroe-Augustus M, Bartel B. Peroxisome-associated matrix protein degradation in Arabidopsis. Proc Natl Acad Sci U S A 2009;106:4561-4566.
50. Pracharoenwattana I, Cornah JE, Smith SM. Arabidopsis peroxisomal malate dehydrogenase functions in β-oxidation but not in the glyoxylate cycle. Plant J 2007;50:381-390.
51. Platta HW, Girzalsky W, Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p. Biochem J 2004;384:37-45.
52. Oshima Y, Kamigaki A, Nakamori C, Mano S, Hayashi M, Nishimura M, Esaka M. Plant catalase is imported into peroxisomes by Pex5p but is distinct from typical PTS1 import. Plant Cell Physiol 2008;49:671-677.
53. Platta HW, 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.
54. Grou CP, Carvalho AF, Pinto MP, Wiese S, Piechura H, Meyer HE, Warscheid B, Sá-Miranda C, Azevedo JE. 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.
55. Kiel JAKW, Emmrich K, Meyer HE, Kunau WH. 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.
56. 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;135:1763-1774.
57. Kiel JAKW, Otzen M, Veenhuis M, Van Der Klei IJ. Obstruction of polyubiquitination affects PTS1 peroxisomal matrix protein import. Biochim Biophys Acta 2005;1745:176-186.
58. Zhang Z, Suzuki Y, Shimozawa N, Fukuda S, Imamura A, Tsukamoto T, Osumi T, Fujiki Y, Orii T, Wanders RJ, Barth PG, Moser HW, Paton BC, Besley GT, Kondo N. Genomic structure and identification of 11 novel mutations of the PEX6 (peroxisome assembly factor-2) gene in patients with peroxisome biogenesis disorders. Hum Mutat 1999;13:487-496.
59. 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 protein import in mammals. Study with a novel PEX5-impaired Chinese hamster ovary cell mutant. J Biol Chem 2000;275:21715-21721.
60. Crane DI, Maxwell MA, Paton BC. PEX1 mutations in the Zellweger spectrum of the peroxisome biogenesis disorders. Hum Mutat 2005;26:167-175.
61. Ebberink MS, Koster J, Wanders RJA, Waterham HR. Spectrum of PEX6 mutations in Zellweger syndrome spectrum patients. Hum Mutat 2010;31:1058-1070.
62. Haughn GW, Somerville C. Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol Gen Genet 1986;204:430-434.
63. Stasinopoulos TC, Hangarter RP. Preventing photochemistry in culture media by long-pass light filters alters growth of cultured tissues. Plant Physiol 1990;93:1365-1369.
64. Ausubel F, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current Protocols in Molecular Biology. New York: Greene Publishing Associates and Wiley-Interscience; 1999.
65. Lingard MJ, Bartel B. Arabidopsis LON2 is necessary for peroxisomal function and sustained matrix protein import. Plant Physiol 2009;151:1354-1365.
66. Olsen LJ, Ettinger WF, Damsz B, Matsudaira K, Webb MA, Harada JJ. Targeting of glyoxysomal proteins to peroxisomes in leaves and roots of a higher plant. Plant Cell 1993;5:941-952.
67. Kunce CM, Trelease RN, Turley RB. Purification and biosynthesis of cottonseed (Gossypium hirsutum L.) catalase. Biochem J 1988;251:147-155.
68. Dugas D, Bartel B. Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 2008;67: 403-417.