Genome-wide Analysis of Effectors of Peroxisome Biogenesis

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2010 Aug 10

PMID 20694151

Citations 17

Authors

Ramsey A Saleem

Rose Long-ODonnell

David J Dilworth

Abraham M Armstrong

Arvind P Jamakhandi

Yakun Wan

Theo A Knijnenburg

Antti Niemisto

John Boyle

Richard A Rachubinski

Ilya Shmulevich

John D Aitchison

Affiliations

Soon will be listed here.

Abstract

Peroxisomes are intracellular organelles that house a number of diverse metabolic processes, notably those required for beta-oxidation of fatty acids. Peroxisomes biogenesis can be induced by the presence of peroxisome proliferators, including fatty acids, which activate complex cellular programs that underlie the induction process. Here, we used multi-parameter quantitative phenotype analyses of an arrayed mutant collection of yeast cells induced to proliferate peroxisomes, to establish a comprehensive inventory of genes required for peroxisome induction and function. The assays employed include growth in the presence of fatty acids, and confocal imaging and flow cytometry through the induction process. In addition to the classical phenotypes associated with loss of peroxisomal functions, these studies identified 169 genes required for robust signaling, transcription, normal peroxisomal development and morphologies, and transmission of peroxisomes to daughter cells. These gene products are localized throughout the cell, and many have indirect connections to peroxisome function. By integration with extant data sets, we present a total of 211 genes linked to peroxisome biogenesis and highlight the complex networks through which information flows during peroxisome biogenesis and function.

Citing Articles

Peroxisome prognostications: Exploring the birth, life, and death of an organelle.

Mast F, Rachubinski R, Aitchison J J Cell Biol. 2020; 219(3).

PMID: 32211898 PMC: 7054992. DOI: 10.1083/jcb.201912100.

Contribution of ERMES subunits to mature peroxisome abundance.

Esposito M, Denmat S, Delahodde A PLoS One. 2019; 14(3):e0214287.

PMID: 30908556 PMC: 6433259. DOI: 10.1371/journal.pone.0214287.

ESCRT-III is required for scissioning new peroxisomes from the endoplasmic reticulum.

Mast F, Herricks T, Strehler K, Miller L, Saleem R, Rachubinski R J Cell Biol. 2018; 217(6):2087-2102.

PMID: 29588378 PMC: 5987711. DOI: 10.1083/jcb.201706044.

Peroxisomal biogenesis is genetically and biochemically linked to carbohydrate metabolism in Drosophila and mouse.

Wangler M, Chao Y, Bayat V, Giagtzoglou N, Shinde A, Putluri N PLoS Genet. 2017; 13(6):e1006825.

PMID: 28640802 PMC: 5480855. DOI: 10.1371/journal.pgen.1006825.

Pex35 is a regulator of peroxisome abundance.

Yofe I, Soliman K, Chuartzman S, Morgan B, Weill U, Yifrach E J Cell Sci. 2017; 130(4):791-804.

PMID: 28049721 PMC: 7611368. DOI: 10.1242/jcs.187914.

References

Scholz O, Thiel A, Hillen W, Niederweis M . Quantitative analysis of gene expression with an improved green fluorescent protein. p6. Eur J Biochem. 2000; 267(6):1565-70. DOI: 10.1046/j.1432-1327.2000.01170.x. View

Chan R, Otte C . Isolation and genetic analysis of Saccharomyces cerevisiae mutants supersensitive to G1 arrest by a factor and alpha factor pheromones. Mol Cell Biol. 1982; 2(1):11-20. PMC: 369748. DOI: 10.1128/mcb.2.1.11-20.1982. View

Simon M, Binder M, Adam G, Hartig A, Ruis H . Control of peroxisome proliferation in Saccharomyces cerevisiae by ADR1, SNF1 (CAT1, CCR1) and SNF4 (CAT3). Yeast. 1992; 8(4):303-9. DOI: 10.1002/yea.320080407. View

Hazra P, Suriapranata I, Snyder W, Subramani S . Peroxisome remnants in pex3delta cells and the requirement of Pex3p for interactions between the peroxisomal docking and translocation subcomplexes. Traffic. 2002; 3(8):560-74. DOI: 10.1034/j.1600-0854.2002.30806.x. View

Purdue P, Yang X, Lazarow P . Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J Cell Biol. 1998; 143(7):1859-69. PMC: 2175223. DOI: 10.1083/jcb.143.7.1859. View

Fagarasanu A, Fagarasanu M, Eitzen G, Aitchison J, Rachubinski R . The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae. Dev Cell. 2006; 10(5):587-600. DOI: 10.1016/j.devcel.2006.04.012. View

Lockshon D, Surface L, Kerr E, Kaeberlein M, Kennedy B . The sensitivity of yeast mutants to oleic acid implicates the peroxisome and other processes in membrane function. Genetics. 2006; 175(1):77-91. PMC: 1774995. DOI: 10.1534/genetics.106.064428. View

Bolstad B, Irizarry R, Astrand M, Speed T . A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003; 19(2):185-93. DOI: 10.1093/bioinformatics/19.2.185. View

Rottensteiner H, Wabnegger L, Erdmann R, Hamilton B, Ruis H, Hartig A . Saccharomyces cerevisiae PIP2 mediating oleic acid induction and peroxisome proliferation is regulated by Adr1p and Pip2p-Oaf1p. J Biol Chem. 2003; 278(30):27605-11. DOI: 10.1074/jbc.M304097200. View

10.

Karpichev I, Durand-Heredia J, Luo Y, Small G . Binding characteristics and regulatory mechanisms of the transcription factors controlling oleate-responsive genes in Saccharomyces cerevisiae. J Biol Chem. 2008; 283(16):10264-75. PMC: 2447635. DOI: 10.1074/jbc.M708215200. View

11.

Kiel J, Emmrich K, Meyer H, Kunau W . 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. 2004; 280(3):1921-30. DOI: 10.1074/jbc.M403632200. View

12.

Platta H, Girzalsky W, Erdmann R . Ubiquitination of the peroxisomal import receptor Pex5p. Biochem J. 2004; 384(Pt 1):37-45. PMC: 1134086. DOI: 10.1042/BJ20040572. View

13.

Wiebel F, Kunau W . The Pas2 protein essential for peroxisome biogenesis is related to ubiquitin-conjugating enzymes. Nature. 1992; 359(6390):73-6. DOI: 10.1038/359073a0. View

14.

Niemisto A, Selinummi J, Saleem R, Shmulevich I, Aitchison J, Yli-Harja O . Extraction of the number of peroxisomes in yeast cells by automated image analysis. Conf Proc IEEE Eng Med Biol Soc. 2007; 2006:2353-6. DOI: 10.1109/IEMBS.2006.259890. View

15.

Platta H, Magraoui F, Baumer B, Schlee D, Girzalsky W, Erdmann R . Pex2 and pex12 function as protein-ubiquitin ligases in peroxisomal protein import. Mol Cell Biol. 2009; 29(20):5505-16. PMC: 2756880. DOI: 10.1128/MCB.00388-09. View

16.

Marzioch M, Erdmann R, Veenhuis M, Kunau W . PAS7 encodes a novel yeast member of the WD-40 protein family essential for import of 3-oxoacyl-CoA thiolase, a PTS2-containing protein, into peroxisomes. EMBO J. 1994; 13(20):4908-18. PMC: 395431. DOI: 10.1002/j.1460-2075.1994.tb06818.x. View

17.

Janke C, Magiera M, Rathfelder N, Taxis C, Reber S, Maekawa H . A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 2004; 21(11):947-62. DOI: 10.1002/yea.1142. View

18.

Irizarry R, Bolstad B, Collin F, Cope L, Hobbs B, Speed T . Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003; 31(4):e15. PMC: 150247. DOI: 10.1093/nar/gng015. View

19.

Okumoto K, Abe I, Fujiki Y . Molecular anatomy of the peroxin Pex12p: ring finger domain is essential for Pex12p function and interacts with the peroxisome-targeting signal type 1-receptor Pex5p and a ring peroxin, Pex10p. J Biol Chem. 2000; 275(33):25700-10. DOI: 10.1074/jbc.M003303200. View

20.

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(4):620-4. DOI: 10.1016/j.bbrc.2008.07.054. View