Peroxisomal fatty acid uptake mechanism in saccharomyces cerevisiae

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20144-20153

  Van Roermund, Carlo W T ^a   Ijlst, Lodewijk ^a   Majczak, Wiktor ^a   Waterham, Hans R ^a   Folkerts, Hendrik ^a   Wanders, Ronald J A ^a   Hellingwerf, Klaas J ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACID MOIETY; ACYL-COA; ACYL-COA ESTER; CELLULAR LIPID; EXPERIMENTAL EVIDENCE; INNER SURFACES; LONG CHAINS; MODEL ORGANISMS; MOLECULAR MECHANISM; PEROXISOMAL MEMBRANES; SYNTHETASES; UPTAKE MECHANISM; VERY LONG-CHAIN FATTY ACIDS;

CYTOLOGY; ESTERIFICATION; ESTERS;

YEAST;

ABC TRANSPORTER; ACYL COENZYME A; FATTY ACID TRANSPORTER; FATTY ACID TRANSPORTER 1; LONG CHAIN ACYL COENZYME A; LONG CHAIN FATTY ACID COENZYME A LIGASE; PEROXISOMAL ABC TRANSPORTER 1; PEROXISOMAL ABC TRANSPORTER 2; PEROXISOMAL ACYL COENZYME A SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME RELEASE; ESTERIFICATION; FATTY ACID ANALYSIS; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; HYDROLYSIS; MOLECULAR MECHANICS; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

ADRENOLEUKODYSTROPHY; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT, ACTIVE; COENZYME A LIGASES; FATTY ACID TRANSPORT PROTEINS; FATTY ACIDS; HUMANS; MULTIPROTEIN COMPLEXES; OXIDATION-REDUCTION; PEROXISOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84861667471     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.332833     Document Type: Article

References (42)

1. Wanders, R. J., and Waterham, H. R. (2006) Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75, 295-332 (Pubitemid 44118035)
2. Pillai, B. K., Jasuja, R., Simard, J. R., and Hamilton, J. A. (2009) Fast diffusion of very long chain saturated fatty acids across a bilayer membrane and their rapid extraction by cyclodextrins: implications for adrenoleukodystrophy. J. Biol. Chem. 284, 33296-33304
3. Theodoulou, F. L., Holdsworth, M., and Baker, A. (2006) Peroxisomal ABC transporters. FEBS Lett. 580, 1139-1155 (Pubitemid 43185294)
4. Wanders, R. J., Visser, W. F., van Roermund, C. W., Kemp, S., and Waterham, H. R. (2007) The peroxisomal ABC transporter family. Pflugers Arch. 453, 719-734 (Pubitemid 46192542)
5. Rokka, A., Antonenkov, V. D., Soininen, R., Immonen, H. L., Pirilä, P. L., Bergmann, U., Sormunen, R. T., Weckström, M., Benz, R., and Hiltunen, J. K. (2009) Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane. PLoS One 4, e5090
6. Linton, K. J., and Higgins, C. F. (2007) Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch. 453, 555-567 (Pubitemid 46192529)
7. Procko, E., O'Mara, M. L., Bennett, W. F., Tieleman, D. P., and Gaudet, R. (2009) The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J. 23, 1287-1302
8. Hettema, E. H., van Roermund, C. W., Distel, B., van den Berg, M., Vilela, C., Rodrigues-Pousada, C., Wanders, R. J., and Tabak, H. F. (1996) The ABC transporter proteins Pat1 and Pat2 are required for import of long-chain fatty acids into peroxisomes of Saccharomyces cerevisiae. EMBO J. 15, 3813-3822 (Pubitemid 26289791)
9. Shani, N., Sapag, A., Watkins, P. A., and Valle, D. (1996) An S. cerevisiae peroxisomal transporter, orthologous to the human adrenoleukodystrophy protein, appears to be a heterodimer of two half ABC transporters: Pxa1p and Pxa2p. Ann. N.Y. Acad. Sci. 804, 770-772 (Pubitemid 27056691)
10. Swartzman, E. E., Viswanathan, M. N., and Thorner, J. (1996) The PAL1 gene product is a peroxisomal ATP-binding cassette transporter in the yeast Saccharomyces cerevisiae. J. Cell Biol. 132, 549-563 (Pubitemid 26069237)
11. van Roermund, C. W., Visser, W. F., Ijlst, L., van Cruchten, A., Boek, M., Kulik, W., Waterham, H. R., and Wanders, R. J. (2008) The human peroxisomal ABC half transporter ALDP functions as a homodimer and accepts acyl-CoA esters. FASEB J. 22, 4201-4208
12. Verleur, N., Hettema, E. H., van Roermund, C. W., Tabak, H. F., and Wanders, R. J. (1997) Transport of activated fatty acids by the peroxisomal ATP-binding-cassette transporter Pxa2 in a semi-intact yeast cell system. Eur. J. Biochem. 249, 657-661 (Pubitemid 27479034)
13. van Roermund, C. W., Visser, W. F., Ijlst, L., Waterham, H. R., and Wanders, R. J. A. (2011) Differential substrate specificities of human ABCD1 and ABCD2 in peroxisomal fatty acid β-oxidation. Biochim. Biophys. Acta 1811, 148-152
14. Fulda, M., Shockey, J., Werber, M., Wolter, F. P., and Heinz, E. (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid β-oxidation. Plant J. 32, 93-103 (Pubitemid 35180927)
15. Fulda, M., Schnurr, J., Abbadi, A., Heinz, E., and Browse, J. (2004) Peroxisomal acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16, 394-405
16. Footitt, S., Slocombe, S. P., Larner, V., Kurup, S., Wu, Y., Larson, T., Graham, I., Baker, A., and Holdsworth, M. (2002) Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 21, 2912-2922 (Pubitemid 34670376)
17. Hayashi, M., Nito, K., Takei-Hoshi, R., Yagi, M., Kondo, M., Suenaga, A., Yamaya, T., and Nishimura, M. (2002) Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid β-oxidation. Plant Cell Physiol. 43, 1-11 (Pubitemid 34152452)
18. Hooks, M. A., Turner, J. E., Murphy, E. C., Johnston, K. A., Burr, S., and Jarosławski, S. (2007) The Arabidopsis ALDP protein homologue COMATOSE is instrumental in peroxisomal acetate metabolism. Biochem. J. 406, 399-406 (Pubitemid 47425446)
19. Verrier, P. J., Bird, D., Burla, B., Dassa, E., Forestier, C., Geisler, M., Klein, M., Kolukisaoglu, U., Lee, Y., Martinoia, E., Murphy, A., Rea, P. A., Samuels, L., Schulz, B., Spalding, E. J., Yazaki, K., and Theodoulou, F. L. (2008) Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci. 13, 151-159
20. Zolman, B. K., Silva, I. D., and Bartel, B. (2001) The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. Plant Physiol. 127, 1266-1278 (Pubitemid 33112184)
21. Igoillo-Esteve, M., Mazet, M., Deumer, G., Wallemacq, P., and Michels, P. A. (2011) Glycosomal ABC transporters of Trypanosoma brucei: characterisation of their expression, topology and substrate specificity. Int. J. Parasitol. 41, 429-438
22. Nyathi, Y., De Marcos Lousa, C., van Roermund, C. W., Wanders, R. J., Johnson, B., Baldwin, S. A., Theodoulou, F. L., and Baker, A. (2010) The Arabidopsis peroxisomal ABC transporter, comatose, complements the Saccharomyces cerevisiae pxa1 pxa2Δ mutant for metabolism of long-chain fatty acids and exhibits fatty acyl-CoA-stimulated ATPase activity. J. Biol. Chem. 285, 29892-29902
23. Shockey, J. M., Fulda, M. S., and Browse, J. A. (2002) Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol. 129, 1710-1722 (Pubitemid 34923235)
24. van Roermund, C. W., Hettema, E. H., van den Berg, M., Tabak, H. F., and Wanders, R. J. (1999) Molecular characterization of carnitine-dependent transport of acetyl-CoA from peroxisomes to mitochondria in Saccharomyces cerevisiae and identification of a plasma membrane carnitine transporter, Agp2p. EMBO J. 18, 5843-5852 (Pubitemid 29515661)
25. Elgersma, Y., Vos, A., van den Berg, M., van Roermund, C. W., van der Sluijs P., Distel, B., and Tabak, H. F. (1996) Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J. Biol. Chem. 271, 26375-26382 (Pubitemid 26347492)
26. Arai, R., Ueda, H., Kitayama, A., Kamiya, N., and Nagamune, T. (2001) Design of the linkers which effectively separate domains of a bifunctional fusion protein. Protein Eng. 14, 529-532 (Pubitemid 32959476)
27. van Vlies, N., Tian, L., Overmars, H., Bootsma, A. H., Kulik, W., Wanders, R. J., Wood, P. A., and Vaz, F. M. (2005) Characterization of carnitine and fatty acid metabolism in the long-chain acyl-CoA dehydrogenase-deficient mouse. Biochem. J. 387, 185-193 (Pubitemid 40524088)
28. Vreken, P., van Lint, A. E., Bootsma, A. H., Overmars, H., Wanders, R. J., and van Gennip, A. H. (1999) Quantitative plasma acylcarnitine analysis using electrospray tandem mass spectrometry for the diagnosis of organic acidaemias and fatty acid oxidation defects. J. Inherit. Metab. Dis. 22, 302-306 (Pubitemid 29259500)
29. van Roermund, C. W., Drissen, R., van Den Berg, M., IJlst, L., Hettema, E. H., Tabak, H. F., Waterham, H. R., and Wanders, R. J. (2001) Identification of a peroxisomal ATP carrier required for medium-chain fatty acid β-oxidation and normal peroxisome proliferation in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 4321-4329 (Pubitemid 32565313)
30. Knoll, L. J., Johnson, D. R., and Gordon, J. I. (1994) Biochemical studies of three Saccharomyces cerevisiae acyl-CoA synthetases, Faa1p, Faa2p, and Faa3p. J. Biol. Chem. 269, 16348-16356 (Pubitemid 24209333)
31. Wanders, R. J., IJlst, L., Poggi, F., Bonnefont, J. P., Munnich, A., Brivet, M., Rabier, D., and Saudubray, J. M. (1992) Human trifunctional protein deficiency: a new disorder of mitochondrial fatty acid β-oxidation. Biochem. Biophys. Res. Commun. 188, 1139-1145
32. Strømhaug, P. E., Berg, T. O., Fengsrud, M., and Seglen, P. O. (1998) Purification and characterization of autophagosomes from rat hepatocytes. Biochem. J. 335, 217-224 (Pubitemid 28491054)
33. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85 (Pubitemid 16258399)
34. Wieser, T., Deschauer, M., Olek, K., Hermann, T., and Zierz, S. (2003) Carnitine palmitoyltransferase II deficiency: molecular and biochemical analysis of 32 patients. Neurology 60, 1351-1353 (Pubitemid 36460994)
35. Athenstaedt, K., Zweytick, D., Jandrositz, A., Kohlwein, S. D., and Daum, G. (1999) Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J. Bacteriol. 181, 6441-6448 (Pubitemid 29512955)
36. Choi, J. Y., and Martin, C. E. (1999) The Saccharomyces cerevisiae FAT1 gene encodes an acyl-CoA synthetase that is required for maintenance of very long chain fatty acid levels. J. Biol. Chem. 274, 4671-4683
37. Obermeyer, T., Fraisl, P., DiRusso, C. C., and Black, P. N. (2007) Topology of the yeast fatty acid transport protein Fat1p: mechanistic implications for functional domains on the cytosolic surface of the plasma membrane. J. Lipid Res. 48, 2354-2364 (Pubitemid 350058747)
38. Watkins, P. A., Lu, J. F., Braiterman, L. T., Steinberg, S. J., and Smith, K. D. (2000) Disruption of a yeast very-long-chain acyl-CoA synthetase gene simulates the cellular phenotype of X-linked adrenoleukodystrophy. Cell Biochem. Biophys. 32, 333-337
39. Lolkema, J. S., Poolman, B., and Konings, W. N. (1998) Bacterial solute uptake and efflux systems. Curr. Opin. Microbiol. 1, 248-253 (Pubitemid 128428067)
40. Deutscher, J., Francke, C., and Postma, P. W. (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70, 939-1031 (Pubitemid 44958262)
41. Steinberg, S. J., Kemp, S., Braiterman, L. T., and Watkins, P. A. (1999) Role of very-long-chain acyl-coenzyme A synthetase in X-linked adrenoleukodystrophy. Ann. Neurol. 46, 409-412 (Pubitemid 29416280)
42. +. Biochem. J. 443, 241-247