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Basic Research Paper

Export-deficient monoubiquitinated PEX5 triggers peroxisome removal in SV40 large T antigen-transformed mouse embryonic fibroblasts

, , , , , , , & show all
Pages 1326-1340 | Received 18 Sep 2015, Accepted 08 Jun 2015, Published online: 14 Aug 2015

References

  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147: 728-41; PMID:22078875; http://dx.doi.org/10.1016/j.cell.2011.10.026
  • Kaushik S, Cuervo AM. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 2012; 22: 407-17; PMID:22748206; http://dx.doi.org/10.1016/j.tcb.2012.05.006
  • Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy. Nat Cell Biol 2013; 15: 713-20; PMID:23817233; http://dx.doi.org/10.1038/ncb2788
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 2011; 27: 107-32; PMID:21801009; http://dx.doi.org/10.1146/annurev-cellbio-092910-154005
  • Araki Y, Ku WC, Akioka M, May AI, Hayashi Y, Arisaka F, Ishihama Y, Ohsumi Y. Atg38 is required for autophagy-specific phosphatidylinositol 3-kinase complex integrity. J Cell Biol 2013; 203: 299-313; PMID:24165940; http://dx.doi.org/10.1083/jcb.201304123
  • Green DR, Levine B. To be or not to be? How selective autophagy and cell death govern cell fate. Cell 2014; 157: 65-75; PMID:24679527; http://dx.doi.org/10.1016/j.cell.2014.02.049
  • Rogov V, Dötsch V, Johansen T, Kirkin V. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell 2014; 53: 167-78; PMID:24462201; http://dx.doi.org/10.1016/j.molcel.2013.12.014
  • Van Veldhoven PP. Biochemistry and genetics of inherited disorders of peroxisomal fatty acid metabolism. J Lipid Res 2010; 51: 2863-95; PMID:20558530; http://dx.doi.org/10.1194/jlr.R005959
  • Braverman NE, Moser AB. Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 2012; 1822: 1442-52; PMID:22627108; http://dx.doi.org/10.1016/j.bbadis.2012.05.008
  • Islinger M, Grille S, Fahimi HD, Schrader M. The peroxisome: an update on mysteries. Histochem Cell Biol 2012; 137: 547-74; PMID:22415027; http://dx.doi.org/10.1007/s00418-012-0941-4
  • Fransen M, Nordgren M, Wang B, Apanasets O. Role of peroxisomes in ROS/RNS-metabolism: implications for human disease. Biochim Biophys Acta 2012; 1822: 1363-73; PMID:22178243; http://dx.doi.org/10.1016/j.bbadis.2011.12.001
  • Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry 2010; 49: 835-42; PMID:20050630; http://dx.doi.org/10.1021/bi9020378
  • Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Río LA. Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. Subcell Biochem 2013; 69: 231-55
  • Nordgren M, Fransen M. Peroxisomal metabolism and oxidative stress. Biochimie 2014; 98: 56-62; PMID:23933092; http://dx.doi.org/10.1016/j.biochi.2013.07.026
  • Brocard C, Hartig A. Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim Biophys Acta 2006; 1763: 1565-73.; PMID:17007944; http://dx.doi.org/10.1016/j.bbamcr.2006.08.022
  • Fransen M. Peroxisome dynamics: molecular players, mechanisms, and (dys)functions. ISRN Cell Biology 2012; Article ID 714192; PMID:24340224
  • Gatto GJ Jr, Geisbrecht BV, Gould SJ, Berg JM. Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat Struct Biol 2000; 7: 1091-5; PMID:11101887; http://dx.doi.org/10.1038/81930
  • Braverman N, Dodt G, Gould SJ, 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: 1195-205; PMID:9668159; http://dx.doi.org/10.1093/hmg/7.8.1195
  • Francisco T, Rodrigues TA, Freitas MO, Grou CP, Carvalho AF, Sá-Miranda C, Pinto MP, Azevedo JE. A cargo-centered perspective on the PEX5 receptor-mediated peroxisomal protein import pathway. J Biol Chem 2013; 288: 29151-9; PMID:23963456; http://dx.doi.org/10.1074/jbc.M113.487140
  • Platta HW, Hagen S, Reidick C, Erdmann R. The peroxisomal receptor dislocation pathway: to the exportomer and beyond. Biochimie 2014; 98: 16-28; PMID:24345375; http://dx.doi.org/10.1016/j.biochi.2013.12.009
  • 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
  • Oliveira ME, Gouveia AM, Pinto RA, Sá-Miranda C, Azevedo JE. The energetics of Pex5p-mediated peroxisomal protein import. J Biol Chem 2003; 278: 39483-8; PMID:12885776; http://dx.doi.org/10.1074/jbc.M305089200
  • Francisco T, Rodrigues TA, Pinto MP, Carvalho AF, Azevedo JE, Grou CP. Ubiquitin in the peroxisomal protein import pathway. Biochimie 2014; 98: 29-35; PMID:23954799; http://dx.doi.org/10.1016/j.biochi.2013.08.003
  • 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
  • Shiozawa K, Maita N, Tomii K, Seto A, Goda N, Akiyama Y, Shimizu T, Shirakawa M, Hiroaki H. Structure of the N-terminal domain of PEX1 AAA-ATPase. Characterization of a putative adaptor-binding domain. J Biol Chem 2004; 279: 50060-8; PMID:15328346; http://dx.doi.org/10.1074/jbc.M407837200
  • Fujiki Y, Nashiro C, Miyata N, Tamura S, Okumoto K. New insights into dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p in shuttling of PTS1-receptor Pex5p during peroxisome biogenesis. Biochim Biophys Acta 2012; 1823: 145-9; PMID:22079764; http://dx.doi.org/10.1016/j.bbamcr.2011.10.012
  • Yokota S. Formation of autophagosomes during degradation of excess peroxisomes induced by administration of dioctyl phthalate. Eur J Cell Biol 1993; 61: 67-80; PMID:8223709
  • Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, Chiba T, Tanaka K, Kominami E. Excess peroxisomes are degraded by autophagic machinery in mammals. J Biol Chem 2006; 281: 4035-41; PMID:16332691; http://dx.doi.org/10.1074/jbc.M512283200
  • Till A, Lakhani R, Burnett SF, Subramani S. Pexophagy: the selective degradation of peroxisomes. Int J Cell Biol 2012; Article ID 512721; PMID:22536249
  • 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: 939-952; PMID:23239026; http://dx.doi.org/10.1242/jcs.114819
  • Nordgren M, Wang B, Apanasets O, Fransen M. Peroxisome degradation in mammals: mechanisms of action, recent advances, and perspectives. Front Physiol 2013; Article ID 145; PMID:23785334
  • Yamashita SI, Abe K, Tatemichi Y, Fujiki Y. The membrane peroxin PEX3 induces peroxisome-ubiquitination-linked pexophagy. Autophagy 2014; 10: 1549-64; PMID:25007327; http://dx.doi.org/10.4161/auto.29329
  • Kim I, Lemasters JJ. Mitophagy selectively degrades individual damaged mitochondria after photoirradiation. Antioxid Redox Signal 2011; 14: 1919-28; PMID:21126216; http://dx.doi.org/10.1089/ars.2010.3768
  • Rubio N, Verrax J, Dewaele M, Verfaillie T, Johansen T, Piette J, Agostinis P. p38(MAPK)-regulated induction of p62 and NBR1 after photodynamic therapy promotes autophagic clearance of ubiquitin aggregates and reduces reactive oxygen species levels by supporting Nrf2-antioxidant signaling. Free Radic Biol Med 2014; 67: 292-303; PMID:24269898; http://dx.doi.org/10.1016/j.freeradbiomed.2013.11.010
  • Wang Y, Nartiss Y, Steipe B, McQuibban GA, Kim PK. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 2012; 8: 1462-76; PMID:22889933; http://dx.doi.org/10.4161/auto.21211
  • 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
  • Shibata M, Oikawa K, Yoshimoto K, Kondo M, Mano S, Yamada K, Hayashi M, Sakamoto W, Ohsumi Y, Nishimura M. Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell 2013; 25: 4967-83; PMID:24368788; http://dx.doi.org/10.1105/tpc.113.116947
  • Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 2008; 105: 20567-74; PMID:19074260; http://dx.doi.org/10.1073/pnas.0810611105
  • Brown AI, Kim PK, Rutenberg AD. PEX5 and ubiquitin dynamics on mammalian peroxisome membranes. PLoS Comput Biol 2014; Article ID e1003426
  • Okumoto K, Noda H, Fujiki Y. Distinct modes of ubiquitination of peroxisome-targeting signal type 1 (PTS1) receptor Pex5p regulate PTS1 protein import. J Biol Chem 2014; 289: 14089-108; PMID:24662292; http://dx.doi.org/10.1074/jbc.M113.527937
  • Bulina ME, Lukyanov KA, Britanova OV, Onichtchouk D, Lukyanov S, Chudakov DM. Chromophore-assisted light inactivation (CALI) using the phototoxic fluorescent protein KillerRed. Nat Protoc 2006; 1: 947-53; PMID:17406328; http://dx.doi.org/10.1038/nprot.2006.89
  • Nordgren M, Wang B, Apanasets O, Brees C, Veldhoven PP, Fransen M. Potential limitations in the use of KillerRed for fluorescence microscopy. J Microsc 2012; 245: 229-35; PMID:22091555; http://dx.doi.org/10.1111/j.1365-2818.2011.03564.x
  • Wang Y, Shyy JY, Chien S. Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing. Annu Rev Biomed Eng 2008; 10: 1-38; PMID:18647110; http://dx.doi.org/10.1146/annurev.bioeng.010308.161731
  • Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152: 657-68; PMID:11266458; http://dx.doi.org/10.1083/jcb.152.4.657
  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
  • Woudenberg J, Rembacz KP, Hoekstra M, Pellicoro A, van den Heuvel FA, Heegsma J, van Ijzendoorn SC, Holzinger A, Imanaka T, Moshage H, et al. Lipid rafts are essential for peroxisome biogenesis in HepG2 cells. Hepatology 2010; 52: 623-33; PMID:20683960; http://dx.doi.org/10.1002/hep.23684
  • Huybrechts SJ, Van Veldhoven PP, Brees C, Mannaerts GP, Los GV, Fransen M. Peroxisome dynamics in cultured mammalian cells. Traffic 2009; 10: 1722-33; PMID:19719477; http://dx.doi.org/10.1111/j.1600-0854.2009.00970.x
  • Grou CP, Carvalho AF, Pinto MP, Huybrechts SJ, Sá-Miranda C, Fransen M, Azevedo JE. Properties of the ubiquitin-Pex5p thiol ester conjugate. J Biol Chem 2009; 284: 10504-13; PMID:19208625; http://dx.doi.org/10.1074/jbc.M808978200
  • Carvalho AF, Grou CP, Pinto MP, Alencastre IS, Costa-Rodrigues J, Fransen M, Sá-Miranda C, Azevedo JE. Functional characterization of two missense mutations in Pex5p - C11S and N526K. Biochim Biophys Acta 2007; 1773: 1141-8; PMID:17532062; http://dx.doi.org/10.1016/j.bbamcr.2007.04.011
  • Wang X, Herr RA, Hansen TH. Ubiquitination of substrates by esterification. Traffic 2012; 13: 19-24; PMID:21883762; http://dx.doi.org/10.1111/j.1600-0854.2011.01269.x
  • Okumoto K, Misono S, Miyata N, Matsumoto Y, Mukai S, Fujiki Y. Cysteine ubiquitination of PTS1 receptor Pex5p regulates Pex5p recycling. Traffic 2011; 12: 1067-83; PMID:21554508; http://dx.doi.org/10.1111/j.1600-0854.2011.01217.x
  • Amery L, Sano H, Mannaerts GP, Snider J, Van Looy J, Fransen M, Van Veldhoven PP. Identification of PEX5-related novel peroxisome-targeting signal 1 (PTS1)-binding proteins in mammals. Biochem J 2001; 357: 635-46; PMID:11463335; http://dx.doi.org/10.1042/0264-6021:3570635
  • Grou CP, Francisco T, Rodrigues TA, Freitas MO, Pinto MP, Carvalho AF, Domingues P, Wood SA, Rodríguez-Borges JE, Sá-Miranda C, et al. Identification of ubiquitin-specific protease 9X (USP9X) as a deubiquitinase acting on ubiquitin-peroxin 5 (PEX5) thioester conjugate. J Biol Chem 2012; 287: 12815-27; PMID:22371489; http://dx.doi.org/10.1074/jbc.M112.340158
  • Miyata N, Okumoto K, Mukai S, Noguchi M, Fujiki Y. AWP1/ZFAND6 functions in Pex5 export by interacting with cys-monoubiquitinated Pex5 and Pex6 AAA ATPase. Traffic 2012; 13: 168-183; PMID:21980954; http://dx.doi.org/10.1111/j.1600-0854.2011.01298.x
  • Ivashchenko O, Van Veldhoven PP, Brees C, Ho YS, Terlecky SR, Fransen M. Intraperoxisomal redox balance in mammalian cells: oxidative stress and interorganellar crosstalk. Mol Biol Cell 2011; 22: 1440-51; PMID:21372177; http://dx.doi.org/10.1091/mbc.E10-11-0919
  • Hosokawa N, Hara Y, Mizushima N. Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett 2006; 580: 2623-9; PMID:16647067; http://dx.doi.org/10.1016/j.febslet.2006.04.008
  • Verfaillie T, Rubio N, Garg AD, Bultynck G, Rizzuto R, Decuypere JP, Piette J, Linehan C, Gupta S, Samali A, Agostinis P. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ 2012; 19: 1880-91; PMID:22705852; http://dx.doi.org/10.1038/cdd.2012.74
  • Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131: 1149-63; PMID:18083104; http://dx.doi.org/10.1016/j.cell.2007.10.035
  • Deegan S, Saveljeva S, Gorman AM, Samali A. Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic reticulum stress. Cell Mol Life Sci 2013; 70: 2425-41; PMID:23052213; http://dx.doi.org/10.1007/s00018-012-1173-4
  • Campello S, Strappazzon F, Cecconi F. Mitochondrial dismissal in mammals, from protein degradation to mitophagy. Biochim Biophys Acta 2014; 1837: 451-60; PMID:24275087; http://dx.doi.org/10.1016/j.bbabio.2013.11.010
  • Michaeli S, Galili G. Degradation of organelles or specific organelle components via selective autophagy in plant cells. Int J Mol Sci 2014; 15: 7624-38; PMID:24802874; http://dx.doi.org/10.3390/ijms15057624
  • Aksam EB, de Vries B, van der Klei IJ, Kiel JA. Preserving organelle vitality: peroxisomal quality control mechanisms in yeast. FEMS Yeast Res 2009; 9: 808-20; PMID:19538506; http://dx.doi.org/10.1111/j.1567-1364.2009.00534.x
  • Oku M, Sakai Y. Peroxisomes as dynamic organelles: autophagic degradation. FEBS J 2010; 277: 3289-94; PMID:20629742; http://dx.doi.org/10.1111/j.1742-4658.2010.07741.x
  • Manjithaya R, Nazarko TY, Farré JC, Subramani S. Molecular mechanism and physiological role of pexophagy. FEBS Lett 2010; 584: 1367-73; PMID:20083110; http://dx.doi.org/10.1016/j.febslet.2010.01.019
  • Nuttall JM, Motley AM, Hettema EH. Deficiency of the exportomer components Pex1, Pex6, and Pex15 causes enhanced pexophagy in Saccharomyces cerevisiae. Autophagy 2014; 10: 835-45; PMID:24657987; http://dx.doi.org/10.4161/auto.28259
  • Tomko RJ, Funakoshi M, Schneider K, Wang J, Hochstrasser M. Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: implications for proteasome structure and assembly. Mol Cell 2010; 38: 393-403; PMID:20471945; http://dx.doi.org/10.1016/j.molcel.2010.02.035
  • Alencastre IS, Rodrigues TA, Grou CP, Fransen M, Sá-Miranda C, Azevedo JE. Mapping the cargo protein membrane translocation step into the PEX5 cycling pathway. J Biol Chem 2009; 284: 27243-51; PMID:19632994; http://dx.doi.org/10.1074/jbc.M109.032565
  • Rodrigues TA, Alencastre IS, Francisco T, Brites P, Fransen M, Grou CP, Azevedo JE. A PEX7-centered perspective on the peroxisomal targeting signal type 2-mediated protein import pathway. Mol Cell Biol 2014; 34: 2917-28; PMID:24865970; http://dx.doi.org/10.1128/MCB.01727-13
  • Grou CP, Carvalho AF, Pinto MP, Alencastre IS, Rodrigues TA, Freitas MO, Francisco T, Sá-Miranda C, Azevedo JE. The peroxisomal protein import machinery - a case report of transient ubiquitination with a new flavor. Cell Mol Life Sci 2009; 66: 254-62; PMID:18810320; http://dx.doi.org/10.1007/s00018-008-8415-5
  • Gouveia AM, Guimarães CP, Oliveira ME, Reguenga C, Sá-Miranda C, Azevedo JE. Characterization of the peroxisomal cycling receptor, Pex5p, using a cell-free in vitro import system. J Biol Chem 2003; 278: 226-32; PMID:12411433; http://dx.doi.org/10.1074/jbc.M209498200
  • Gouveia AM, Guimarães CP, Oliveira ME, Sá-Miranda C, Azevedo JE. Insertion of Pex5p into the peroxisomal membrane is cargo protein-dependent. J Biol Chem 2003; 278: 4389-92; PMID:12502712; http://dx.doi.org/10.1074/jbc.C200650200
  • Cantalupo PG, Sáenz-Robles MT, Rathi AV, Beerman RW, Patterson WH, Whitehead RH, Pipas JM. Cell-type specific regulation of gene expression by simian virus 40 T antigens. Virology 2009; 386: 183-91; PMID:19201438; http://dx.doi.org/10.1016/j.virol.2008.12.038
  • Rathi AV, Sáenz Robles MT, Cantalupo PG, Whitehead RH, Pipas JM. Simian virus 40 T-antigen-mediated gene regulation in enterocytes is controlled primarily by the Rb-E2F pathway. J Virol 2009; 83: 9521-31; PMID:19570859; http://dx.doi.org/10.1128/JVI.00583-09
  • Legakis JE, Koepke JI, Jedeszko C, Barlaskar F, Terlecky LJ, Edwards HJ, Walton PA, Terlecky SR. Peroxisome senescence in human fibroblasts. Mol Biol Cell 2002; 13: 4243-55; PMID:12475949; http://dx.doi.org/10.1091/mbc.E02-06-0322
  • Muller M. Cellular senescence: molecular mechanisms, in vivo significance, and redox considerations. Antioxid Redox Signal 2009; 11: 59-98; PMID:18976161; http://dx.doi.org/10.1089/ars.2008.2104
  • Apanasets O, Grou CP, Van Veldhoven PP, Brees C, Wang B, Nordgren M, Dodt G, Azevedo JE, Fransen M. PEX5, the shuttling import receptor for peroxisomal matrix proteins, is a redox-sensitive protein. Traffic 2014; 15: 94-103; PMID:24118911; http://dx.doi.org/10.1111/tra.12129
  • Yokota S, Oda T, Fahimi HD. The role of 15-lipoxygenase in disruption of the peroxisomal membrane and in programmed degradation of peroxisomes in normal rat liver. J Histochem Cytochem 2001; 49: 613-22; PMID:11304799; http://dx.doi.org/10.1177/002215540104900508
  • Juenemann K, Reits EA. Alternative macroautophagic pathways. Int J Cell Biol 2012; 2012: Article ID 189794; PMID:22536246; http://dx.doi.org/10.1155/2012/189794
  • 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
  • Léon S1, 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: 7424-30; http://dx.doi.org/10.1074/jbc.M611627200
  • Feutz AC, Pham-Dinh D, Allinquant B, Miehe M, Ghandour MS. An immortalized jimpy oligodendrocyte cell line: defects in cell cycle and cAMP pathway. Glia 2001; 34: 241-52; PMID:11360297; http://dx.doi.org/10.1002/glia.1058
  • Brees C, Fransen M. A cost-effective approach to microporate mammalian cells with the Neon Transfection System. Anal Biochem 2014; 466: 49-50; PMID:25172131; http://dx.doi.org/10.1016/j.ab.2014.08.017
  • Amery L, Fransen M, De Nys K, Mannaerts GP, Van Veldhoven PP. Mitochondrial and peroxisomal targeting of 2-methylacyl-CoA racemase in humans. J Lipid Res 2000; 41: 1752-9; PMID:11060344
  • Huybrechts SJ, Van Veldhoven PP, Hoffman I, Zeevaert R, de Vos R, Demaerel P, Brams M, Jaeken J, Fransen M, Cassiman D. Identification of a novel PEX14 mutation in Zellweger syndrome. J Med Genet 2008; 45: 376-83; PMID:18285423; http://dx.doi.org/10.1136/jmg.2007.056697
  • Fransen M, Van Veldhoven PP, Subramani S. Identification of peroxisomal proteins by using M13 phage protein VI phage display: molecular evidence that mammalian peroxisomes contain a 2,4-dienoyl-CoA reductase. Biochem J 1999; 340: 561-8; PMID:10333503; http://dx.doi.org/10.1042/0264-6021:3400561
  • Fransen M. HaloTag as a tool to investigate peroxisome dynamics in cultured mammalian cells. Methods Mol Biol 2014; 1174: 157-70; PMID:24947380
  • Wilkinson KD, Gan-Erdene T, Kolli N. Derivitization of the C-terminus of ubiquitin and ubiquitin-like proteins using intein chemistry: methods and uses. Methods Enzymol 2005; 399: 37-51; PMID:16338347
  • Fransen M, Vastiau I, Brees C, Brys V, Mannaerts GP, Van Veldhoven PP. Potential role for Pex19p in assembly of PTS-receptor docking complexes. J Biol Chem 2004; 279: 12615-24; PMID:14715663; http://dx.doi.org/10.1074/jbc.M304941200

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