Deficiency of the exportomer components Pex1, Pex6, and Pex15 causes enhanced pexophagy in Saccharomyces cerevisiae

Autophagy

Volumn 10, Issue 5, 2014, Pages 835-845

  Nuttall, James M ^a   Motley, Alison M ^a   Hettema, Ewald H ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Atg36; Exportomer; Peroxin; Peroxisome; Pex1; Pex6; Pexophagy; Selective autophagy

Indexed keywords

ATG11 PROTEIN; ATG36 PROTEIN; MEMBRANE PROTEIN; PEROXIN; PEX1 PROTEIN; PEX15 PROTEIN; PEX6 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; ATG36 PROTEIN, S CEREVISIAE; PEX1 PROTEIN, S CEREVISIAE; PEX15 PROTEIN, S CEREVISIAE; PEX6 PROTEIN, S CEREVISIAE; PHOSPHOPROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITINATED PROTEIN;

ARTICLE; DELETION MUTANT; ENZYME DEGRADATION; GENE DELETION; GENETIC ANALYSIS; MAMMAL CELL; MEMBRANE STRUCTURE; NONHUMAN; PEROXISOMAL TARGETING SIGNAL; PEROXISOME; PEXOPHAGY; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; SACCHAROMYCES CEREVISIAE; AUTOPHAGY; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSGENIC ORGANISM; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATASES; AUTOPHAGY; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; ORGANISMS, GENETICALLY MODIFIED; PEROXISOMES; PHOSPHOPROTEINS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATED PROTEINS;

EID: 84899719244     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.28259     Document Type: Article

References (47)

1. Reggiori F, Klionsky DJ. Autophagic processes in yeast: mechanism, machinery and regulation. Genetics 2013; 194:341-61; PMID:23733851; http://dx.doi.org/10.1534/genetics.112.149013
2. Hutchins MU, Veenhuis M, Klionsky DJ. Peroxisome degradation in Saccharomyces cerevisiae is dependent on machinery of macroautophagy and the Cvt pathway. J Cell Sci 1999; 112:4079-87; PMID:10547367
3. Manivannan S, de Boer R, Veenhuis M, van der Klei IJ. Lumenal peroxisomal protein aggregates are removed by concerted fission and autophagy events. Autophagy 2013; 9:1044-56; PMID:23614977; http://dx.doi.org/10.4161/auto.24543
4. van Zutphen T, Veenhuis M, van der Klei IJ. Damaged peroxisomes are subject to rapid autophagic degradation in the yeast Hansenula polymorpha. Autophagy 2011; 7:863-72; PMID:21490428; http://dx.doi.org/10.4161/auto.7.8. 15697
5. Motley AM, Nuttall JM, Hettema EH. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J 2012; 31:2852-68; PMID:22643220; http://dx.doi.org/10.1038/emboj.2012.151
6. Yorimitsu T, Klionsky DJ. Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol Biol Cell 2005; 16:1593-605; PMID:15659643; http://dx.doi.org/10.1091/mbc.E04-11-1035
7. Lynch-Day MA, Klionsky DJ. The Cvt pathway as a model for selective autophagy. FEBS Lett 2010; 584:1359-66; PMID:20146925; http://dx.doi.org/10. 1016/j.febslet.2010.02.013
8. Farré JC, Burkenroad A, Burnett SF, Subramani S. Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep 2013; 14:441-9; PMID:23559066; http://dx.doi.org/10.1038/embor. 2013.40
9. Farré JC, Manjithaya R, Mathewson RD, Subramani S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell 2008; 14:365-76; PMID:18331717; http://dx.doi.org/10.1016/j.devcel.2007.12.011
10. Kanki T, Kurihara Y, Jin X, Goda T, Ono Y, Aihara M, Hirota Y, Saigusa T, Aoki Y, Uchiumi T, et al. Casein kinase 2 is essential for mitophagy. EMBO Rep 2013; 14:788-94; PMID:23897086; http://dx.doi.org/10.1038/embor.2013.114
11. Kondo-Okamoto N, Noda NN, Suzuki SW, Nakatogawa H, Takahashi I, Matsunami M, Hashimoto A, Inagaki F, Ohsumi Y, Okamoto K. Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J Biol Chem 2012; 287:10631-8; PMID:22308029; http://dx.doi.org/10.1074/jbc.M111.299917
12. Aoki Y, Kanki T, Hirota Y, Kurihara Y, Saigusa T, Uchiumi T, Kang D. Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol Biol Cell 2011; 22:3206-17; PMID:21757540; http://dx.doi.org/10.1091/mbc.E11-02-0145
13. Platta HW, Hagen S, Erdmann R. The exportomer: the peroxisomal receptor export machinery. Cell Mol Life Sci 2013; 70:1393-411; PMID:22983384; http://dx.doi.org/10.1007/s00018-012-1136-9
14. 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; 135:1763-74; PMID:8991089; http://dx.doi.org/10.1083/jcb.135.6.1763
15. 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; 20:7516-26; PMID:11003648; http://dx.doi.org/10.1128/MCB.20.20.7516-7526.2000
16. 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; 7:817-22; PMID:16007078; http://dx.doi.org/10. 1038/ncb1281
17. 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; 25:10822-32; PMID:16314507; http://dx.doi.org/10.1128/MCB.25.24. 10822-10832.2005
18. Platta HW, Girzalsky W, Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p. Biochem J 2004; 384:37-45; PMID:15283676; http://dx.doi.org/10.1042/BJ20040572
19. Kiel JA, 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; 280:1921-30; PMID:15536088; http://dx.doi.org/10.1074/jbc.M403632200
20. Kragt A, Voorn-Brouwer T, van den Berg M, Distel B. The Saccharomyces cerevisiae peroxisomal import receptor Pex5p is monoubiquitinated in wild type cells. J Biol Chem 2005; 280:7867-74; PMID:15632140; http://dx.doi.org/10.1074/ jbc.M413553200
21. Williams C, van den Berg M, Sprenger RR, Distel B. A conserved cysteine is essential for Pex4pdependent ubiquitination of the peroxisomal import receptor Pex5p. J Biol Chem 2007; 282:22534-43; PMID:17550898; http://dx.doi.org/10.1074/jbc.M702038200
22. Carvalho AF, Pinto MP, Grou CP, Alencastre IS, Fransen M, Sá-Miranda C, Azevedo JE. Ubiquitination of mammalian Pex5p, the peroxisomal import receptor. J Biol Chem 2007; 282:31267-72; PMID:17726030; http://dx.doi.org/10.1074/jbc.M706325200
23. Magraoui FE, Brinkmeier R, Schrotter A, Girzalsky W, Muller T, Marcus K, Meyer HE, Erdmann R, Platta HW. Distinct ubiquitination cascades act on the peroxisomal targeting signal type 2 co-receptor Pex18p. Traffic (Copenhagen, Denmark) 2013.
24. Deosaran E, Larsen KB, Hua R, Sargent G, Wang Y, Kim S, Lamark T, Jauregui M, Law K, Lippincott-Schwartz J, et al. NBR1 acts as an autophagy receptor for peroxisomes. J Cell Sci 2013; 126:939-52; PMID:23239026; http://dx.doi.org/10.1242/jcs.114819
25. Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci U S A 2008; 105:20567-74; PMID:19074260; http://dx.doi.org/10.1073/pnas. 0810611105
26. Schreiber A, Peter M. Substrate recognition in selective autophagy and the ubiquitin-proteasome system. Biochim Biophys Acta 2014; 1843:163-81; PMID:23545414; http://dx.doi.org/10.1016/j.bbamcr.2013.03.019.
27. Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ 2013; 20:21-30; PMID:22722335; http://dx.doi.org/ 10.1038/cdd.2012.72
28. Hara-Kuge S, Fujiki Y. The peroxin Pex14p is involved in LC3-dependent degradation of mammalian peroxisomes. Exp Cell Res 2008; 314:3531-41; PMID:18848543; http://dx.doi.org/10.1016/j.yexcr.2008.09.015
29. Bellu AR, Salomons FA, Kiel JA, Veenhuis M, Van Der Klei IJ. Removal of Pex3p is an important initial stage in selective peroxisome degradation in Hansenula polymorpha. J Biol Chem 2002; 277:42875-80; PMID:12221086; http://dx.doi.org/10.1074/jbc.M205437200
30. Bellu AR, Komori M, van der Klei IJ, Kiel JA, Veenhuis M. Peroxisome biogenesis and selective degradation converge at Pex14p. J Biol Chem 2001; 276:44570-4; PMID:11564741; http://dx.doi.org/10.1074/jbc.M107599200
31. Kanki T, Klionsky DJ. Mitophagy in yeast occurs through a selective mechanism. J Biol Chem 2008; 283:32386-93; PMID:18818209; http://dx.doi.org/10. 1074/jbc.M802403200
32. Okamoto K, Kondo-Okamoto N, Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 2009; 17:87-97; PMID:19619494; http://dx.doi.org/10.1016/j.devcel.2009.06.013
33. Noda T, Klionsky DJ. The quantitative Pho8Delta60 assay of nonspecific autophagy. Methods Enzymol 2008; 451:33-42; PMID:19185711; http://dx.doi.org/10. 1016/S0076-6879(08)03203-5
34. Suzuki K, Kubota Y, Sekito T, Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 2007; 12:209-18; PMID:17295840; http://dx.doi.org/10.1111/j.1365-2443.2007.01050.x
35. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods 2009; 6:917-22; PMID:19915560; http://dx.doi.org/10.1038/nmeth.1401
36. Ebberink MS, Mooijer PA, Gootjes J, Koster J, Wanders RJ, Waterham HR. Genetic classification and mutational spectrum of more than 600 patients with a Zellweger syndrome spectrum disorder. Hum Mutat 2011; 32:59-69; PMID:21031596; http://dx.doi.org/10.1002/humu.21388
37. Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 2009; 34:259-69; PMID:19450525; http://dx.doi.org/10.1016/j. molcel.2009.04.026
38. van der Zand A, Gent J, Braakman I, Tabak HF. Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes. Cell 2012; 149:397-409; PMID:22500805; http://dx.doi.org/10.1016/j.cell.2012.01.054
39. Motley AM, Nuttall JM, Hettema EH. Atg36: the Saccharomyces cerevisiae receptor for pexophagy. Autophagy 2012; 8:1680-1; PMID:22874561; http://dx.doi.org/10.4161/auto.21485
40. Heinemeyer W, Kleinschmidt JA, Saidowsky J, Escher C, Wolf DH. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J 1991; 10:555-62; PMID:2001673
41. Ohashi Y, Munro S. Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol Biol Cell 2010; 21:3998-4008; PMID:20861302; http://dx.doi.org/10.1091/mbc.E10-05-0457
42. Vida TA, Emr SD. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 1995; 128:779-92; PMID:7533169; http://dx.doi.org/10.1083/jcb.128.5.779
43. Gietz RD, Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 1988; 74:527-34; PMID:3073106; http://dx.doi.org/10. 1016/0378-1119(88)90185-0
44. Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, et al. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 2000; 403:623-7; PMID:10688190; http://dx.doi.org/10.1038/35001009
45. rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998; 14:953-61; PMID:9717241; http://dx.doi.org/10.1002/(SICI) 1097-0061(199807)14:10 〈953: :AIDYEA293〉 3.0.CO;2-U
46. Boeke JD, Trueheart J, Natsoulis G, Fink GR. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 1987; 154:164-75; PMID:3323810; http://dx.doi.org/10.1016/0076-6879(87)54076-9
47. Kanki T, Kang D, Klionsky DJ. Monitoring mitophagy in yeast: the Om45-GFP processing assay. Autophagy 2009; 5:1186-9; PMID:19806021; http://dx.doi.org/ 10.4161/auto.5.8.9854