Peroxisomal ABC transporters: Functions and mechanism

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 959-965

  Baker, Alison ^a   Carrier, David J ^a   Schaedler, Theresia ^b   Waterham, Hans R ^c   Van Roermund, Carlo W ^c   Theodoulou, Frederica L ^b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b ROTHAMSTED RESEARCH   (United Kingdom)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Acyl CoA; Asymmetry; ATP binding cassette (ABC) transporter; Peroxisome; Thioesterase; oxidation

Indexed keywords

ABC TRANSPORTER; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATASE; HETERODIMER; LONG CHAIN FATTY ACID COENZYME A LIGASE; PROTEIN ABCD2; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; COENZYME A LIGASE; FATTY ACID; SACCHAROMYCES CEREVISIAE PROTEIN;

ARABIDOPSIS; ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME SPECIFICITY; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; HUMAN; NONHUMAN; NUCLEOTIDE BINDING SITE; PEROXISOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; CHEMISTRY; METABOLISM; MOLECULAR MODEL; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION;

ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; COENZYME A LIGASES; FATTY ACIDS; HUMANS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PEROXISOMES; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84947228011     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150127     Document Type: Article

References (53)

1. Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R.T., Reumann, S. and Zolman, B.K. (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279-2303 CrossRef PubMed
2. Wanders, R.J.A. and Waterham, H.R. (2006) Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75, 295-332 CrossRef PubMed
3. Block, A., Widhalm, J.R., Fatihi, A., Cahoon, R.E., Wamboldt, Y., Elowsky, C., Mackenzie, S.A., Cahoon, E.B., Chapple, C., Dudareva, N. and Basset, G.J. (2014) The origin and biosynthesis of the benzenoid moiety of ubiquinone (coenzyme Q) in Arabidopsis. Plant Cell 26, 1938-1948 CrossRef PubMed
4. Bussell, J.D., Reichelt, M., Wiszniewski, A.A.G., Gershenzon, J. and Smith, S.M. (2014) Peroxisomal ATP-binding cassette transporter COMATOSE and the multifunctional protein abnormal inflorescence meristem are required for the production of benzoylated metabolites in arabidopsis seeds. Plant Physiol. 164, 48-54 CrossRef PubMed
5. Ferdinandusse, S., Jimenez-Sanchez, G., Koster, J., Denis, S., Van Roermund, C.W., Silva-Zolezzi, I., Moser, A.B., Visser, W.F., Gulluoglu, M., Durmaz, O. et al. (2015) A novel bile acid biosynthesis defect due to a deficiency of peroxisomal ABCD3. Hum. Mol. Genet. 24, 361-370 CrossRef PubMed
6. Theodoulou, F.L., Job, K., Slocombe, S.P., Footitt, S., Holdsworth, M., Baker, A., Larson, T.R. and Graham, I.A. (2005) Jasmonic acid levels are reduced in comatose ATP-binding cassette transporter mutants. Implications for transport of jasmonate precursors into peroxisomes. Plant Physiol. 137, 835-840 CrossRef PubMed
7. Antonenkov, V.D. and Hiltunen, J.K. (2006) Peroxisomal membrane permeability and solute transfer. Biochim. Biophys. Acta 1763, 1697 CrossRef PubMed
8. Rokka, A., Antonenkov, V.D., Soininen, R., Immonen, H.L., Pirila, P.L., Bergmann, U., Sormunen, R.T., Weckstram, M., Benz, R. and Hiltunen, J.K. (2009) Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane. PLoS One 4, e5090 CrossRef PubMed
9. Kunze, M. and Hartig, A. (2013) Permeability of the peroxisomal membrane: lessons from the glyoxylate cycle. Front. Physiol. 4, 204 CrossRef PubMed
10. Linka, N. and Theodoulou, F.L. (2013) Metabolite transporters of the plant peroxisomal membrane: known and unknown. Subcell. Biochem. 69, 169-194 CrossRef PubMed
11. Coelho, D., Kim, J.C., Miousse, I.R., Fung, S., du Moulin, M., Buers, I., Suormala, T., Burda, P., Frapolli, M., Stucki, M. et al. (2012) Mutations in ABCD4 cause a new inborn error of vitamin B-12 metabolism. Nat. Genet. 44, 1152-1155 CrossRef PubMed
12. Hurlock, A.K., Roston, R.L., Wang, K. and Benning, C. (2014) Lipid trafficking in plant cells. Traffic 15, 915-932 CrossRef PubMed
13. Verleur, N., Hettema, E.H., VanRoermund, C.T., Tabak, H.F. and Wanders, R.A. (1997) Transport of activated fatty acids by the peroxisomal ATPbinding-cassette transporter Pxa2 in a semi-intact yeast cell system. Eur. J. Biochem. 249, 657-661 CrossRef PubMed
14. 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 PubMed
15. Shani, N. and Valle, D. (1996) A Saccharomyces cerevisiae homolog of the human adrenoleukodystrophy transporter is a heterodimer of two half ATP-binding cassette transporters. Proc. Natl. Acad. Sci. U.S.A. 93, 11901-11906 CrossRef PubMed
16. 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 CrossRef PubMed
17. Chuang, C.Y., Chen, L.Y., Fu, R.H., Chen, S.M., Ho, M.H., Huang, J.M., Hsu, C.C., Wang, C.C., Chen, M.S. and Tsai, R.T. (2014) Involvement of the carboxyl-terminal region of the yeast peroxisomal half ABC transporter Pxa2p in its interaction with Pxa1p and in transporter function. PLoS One 9, e104892 CrossRef PubMed
18. van Roermund, C.W.T., Drissen, R., van den Berg, M., Ijlst, L., Hettema, E.H., Tabak, H.F., Waterham, H.R. and Wanders, R.J.A. (2001). Identification of a peroxisomal ATP carrier required for medium-chain fatty acid beta-oxidation and normal peroxisome proliferation in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 4321-4329 CrossRef PubMed
19. Palmieri, L., Rottensteiner, H., Girzalsky, W., Scarcia, P., Palmieri, F. and Erdmann, R. (2001) Identification and functional reconstitution of the yeast peroxisomal adenine nucleotide transporter. EMBO J. 20, 5049-5059 CrossRef PubMed
20. Dulermo, R., Gamboa-Melendez, H., Ledesma-Amaro, R., Thevenieau, F. and Nicaud, J.M. (2015) Unraveling fatty acid transport and activation mechanisms in Yarrowia lipolytica. Biochim. Biophys. Acta 1851, 1202-1217 CrossRef PubMed
21. 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 beta-oxidation. Plant Cell Physiol. 43, 1-11 CrossRef PubMed
22. Footitt, S., Slocombe, S.P., Larner, V., Kurup, S., Wu, Y.S., 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 CrossRef PubMed
23. 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 beta-oxidation. Plant Physiol. 127, 1266-1278 CrossRef PubMed
24. Hooks, M.A., Turner, J.E., Murphy, E.C., Johnston, K.A., Burr, S. and Jaroslawski, S. (2007) The Arabidopsis ALDP protein homologue COMATOSE is instrumental in peroxisomal acetate metabolism. Biochem. J. 406, 399-406 CrossRef PubMed
25. Dave, A., Hernandez, M.L., He, Z., Andriotis, V.M.E., Vaistij, F.E., Larson, T.R. and Graham, I.A. (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in arabidopsis. Plant Cell 23, 583-599 CrossRef PubMed
26. Kanai, M., Nishimura, M. and Hayashi, M. (2010) A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J. 62, 936-947 PubMed
27. Nyathi, Y., Zhang, X., Baldwin, J.M., Bernhardt, K., Johnson, B., Baldwin, S.A., Theodoulou, F.L. and Baker, A. (2012) Pseudo half-molecules of the ABC transporter, COMATOSE, bind Pex19 and target to peroxisomes independently but are both required for activity. FEBS Lett. 586, 2280-2286 CrossRef PubMed
28. Mendiondo, G.M., Medhurst, A., van Roermund, C.W., Zhang, X., Devonshire, J., Scholefield, D., Fernández, J., Axcell, B., Ramsay, L., Waterham, H.R. et al. (2014) Barley has two peroxisomal ABC transporters with multiple functions in β-oxidation. J. Exp. Bot. 65, 4833-4847 CrossRef PubMed
29. Orsi, C.H. and Tanksley, S.D. (2009) Natural variation in an ABC transporter gene associated with seed size evolution in tomato species. PLos Genet 5, e1000347 CrossRef PubMed
30. Mosser, J., Douar, A.M., Sarde, C.O., Kioschis, P., Feil, R., Moser, H., Poustka, A.M., Mandel, J.L. and Aubourg, P. (1993) Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361, 726-730 CrossRef PubMed
31. Lombard-Platet, G., Savary, S., Sarde, C.O., Mandel, J.L. and Chimini, G. (1996) A close relative of the adrenoleukodystrophy (ALD) gene codes for a peroxisomal protein with a specific expression pattern. Proc. Natl. Acad. Sci. U.S.A. 93, 1265-1269 CrossRef PubMed
32. Kamijo, K., Taketani, S., Yokota, S., Osumi, T. and Hashimoto, T. (1990). The 70-kDa peroxisomal membrane protein is a member of the Mdr (P-glycoprotein)-related ATP-binding protein superfamily. J. Biol. Chem. 265, 4534-4540 PubMed
33. Geillon, F., Gondcaille, C., Charbonnier, S., Van Roermund, C.W., Lopez, T.E., Dias, A.M.M., Pais de Barros, J.-P., Arnould, C., Wanders, R.J., Trompier, D. and Savary, S. (2014) Structure-function analysis of peroxisomal ATP-binding cassette transporters using chimeric dimers. J. Biol. Chem. 289, 24511-24520 CrossRef PubMed
34. van Roermund, C.W.T., Ijlst, L., Wagemans, T., Wanders, R.J.A. and Waterham, H.R. (2014) A role for the human peroxisomal half-transporter ABCD3 in the oxidation of dicarboxylic acids. Biochim. Biophys. Acta 1841, 563-568 CrossRef PubMed
35. Kemp, S., Theodoulou, F.L. and Wanders, R.J.A. (2011) Mammalian peroxisomal ABC transporters: from endogenous substrates to pathology and clinical significance. Br. J. Pharmacol. 164, 1753-1766 CrossRef PubMed
36. Di Benedetto, R., Denti, M.A., Salvati, S., Sanchez, M., Attorri, L., David, G. and Di Biase, A. (2008) RNAi-mediated silencing of ABCD3 gene expression in rat C6 glial cells: a model system to study PMP70 function. Neurochem. Int. 52, 1106-1113 CrossRef PubMed
37. 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 CrossRef PubMed
38. van Roermund, C.W., Visser, W.F., Ijlst, L., Waterham, H.R. and Wanders, R.J. (2011) Differential substrate specificities of human ABCD1 and ABCD2 in peroxisomal fatty acid beta-oxidation. Biochim. Biophys. Acta 1811, 148-152 CrossRef PubMed
39. 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 pxa2Delta mutant for metabolism of long-chain fatty acids and exhibits fatty acyl-CoA-stimulated ATPase activity. J. Biol. Chem. 285, 29892-29902 CrossRef PubMed
40. Zhang, X., De Marcos Lousa, C., Schutte-Lensink, N., Ofman, R., Wanders, R.J., Baldwin, S.A., Baker, A., Kemp, S. and Theodoulou, F.L. (2011). Conservation of targeting but divergence in function and quality control of peroxisomal ABC transporters: an analysis using cross-kingdom expression. Biochem. J. 436, 547-557 CrossRef PubMed
41. 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 CrossRef PubMed
42. Wiesinger, C., Kunze, M., Regelsberger, G., Forss-Petter, S. and Berger, J. (2013) Impaired very long-chain acyl-coA β-oxidation in human X-linked adrenoleukodystrophy fibroblasts is a direct consequence of ABCD1 transporter dysfunction. J. Biol. Chem. 288, 19269-19279 CrossRef PubMed
43. van Roermund, C.W., Ijlst, L., Majczak, W., Waterham, H.R., Folkerts, H., Wanders, R.J. and Hellingwerf, K.J. (2012) Peroxisomal fatty acid uptake mechanism in Saccharomyces cerevisiae. J. Biol. Chem. 287, 20144-20153 CrossRef PubMed
44. 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 CrossRef PubMed
45. De Marcos Lousa, C., van Roermund, C.W., Postis, V.L., Dietrich, D., Kerr, I.D., Wanders, R.J., Baldwin, S.A., Baker, A. and Theodoulou, F.L. (2013). Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids. Proc. Natl. Acad. Sci. U.S.A. 110, 1279-1284 CrossRef PubMed
46. Park, S., Gidda, S.K., James, C.N., Horn, P.J., Khuu, N., Seay, D.C., Keereetaweep, J., Chapman, K.D., Mullen, R.T. and Dyer, J.M. (2013) The α/β hydrolase CGI-58 and peroxisomal transport protein PXA1 coregulate lipid homeostasis and signaling in arabidopsis. Plant Cell 25, 1726-1739 CrossRef PubMed
47. Smith, P.C., Karpowich, N., Millen, L., Moody, J.E., Rosen, J., Thomas, P.J. and Hunt, J.F. (2002) ATP Binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10, 139-149 CrossRef PubMed
48. Dietrich, D., Schmuths, H., Lousa, C.D.M., Baldwin, J.M., Baldwin, S.A., Baker, A., Theodoulou, F.L. and Holdsworth, M.J. (2009) Mutations in the arabidopsis peroxisomal ABC Transporter COMATOSE allow differentiation between multiple functions in planta: insights from an allelic series. Mol. Biol. Cell 20, 530-543 CrossRef PubMed
49. Procko, E., O'Mara, M.L., Bennett, W.F.D., 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 CrossRef PubMed
50. Hou, Y.-x., Cui, L., Riordan, J.R. and Chang, X.-B. (2000) Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein MRP1. J. Biol. Chem. 275, 20280-20287 CrossRef PubMed
51. Aleksandrov, L., Aleksandrov, A.A., Chang, X.-B. and Riordan, J.R. (2002). The first nucleotide binding domain of cystic fibrosis transmembrane conductance regulator is a site of stable nucleotide interaction, whereas the second is a site of rapid turnover. J. Biol. Chem. 277, 15419-15425 CrossRef PubMed
52. Shintre, C.A., Pike, A.C.W., Li, Q., Kim, J.-I., Barr, A.J., Goubin, S., Shrestha, L., Yang, J., Berridge, G., Ross, J. et al. (2013) Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states. Proc. Natl. Acad. Sci. U.S.A. 110, 9710-9715 CrossRef PubMed
53. Dawson, R.J.P. and Locher, K.P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 CrossRef PubMed