Conservation of targeting but divergence in function and quality control of peroxisomal ABC transporters: An analysis using cross-kingdom expression

Biochemical Journal

Volumn 436, Issue 3, 2011, Pages 547-557

  Zhang, Xuebin ^a   De Marcos Lousa, Carine ^b   Schutte Lensink, Nellie ^c   Ofman, Rob ^c   Wanders, Ronald J ^c   Baldwin, Stephen A ^b   Baker, Alison ^b   Kemp, Stephan ^c   Theodoulou, Frederica L ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

70 kDa peroxisomal membrane protein (PMP70); Adrenoleukodystrophy protein (ALDP); ATP binding cassette transporter (ABC transporter); Comatose (CTS); Peroxisome; Pex19; X linked adrenoleukodystrophy (X ALD)

Indexed keywords

ABC TRANSPORTER; ADRENOLEUKODYSTROPHY PROTEIN; ADRENOLEUKODYSTROPHY RELATED PROTEIN; PEROXISOMAL MEMBRANE PROTEIN 70 KDA; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FIBROBLAST; GERMINATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; QUALITY CONTROL; TOBACCO;

ADRENOLEUKODYSTROPHY; ADULT; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; ENDOPLASMIC RETICULUM; FIBROBLASTS; HUMANS; MEMBRANE PROTEINS; MIDDLE AGED; PEROXISOMES; SPECIES SPECIFICITY; TOBACCO;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; MAMMALIA; NICOTIANA TABACUM;

EID: 79957728343     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110249     Document Type: Article

References (59)

1. Wanders, R. J. (2004) Peroxisomes, lipid metabolism, and peroxisomal disorders. Mol. Genet. Metab. 83, 16-27
2. Schumann, U., Wanner, G., Veenhuis, M., Schmid, M. and Gietl, C. (2003) AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 9626-9631
3. Sparkes, I. A., Brandizzi, F., Slocombe, S. P., El-Shami, M., Hawes, C. and Baker, A. (2003) An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol. 133, 1809-1819
4. Fan, J., Quan, S., Orth, T., Awai, C., Chory, J. and Hu, J. (2005) The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol. 139, 231-239 (Pubitemid 43951607)
5. Nito, K., Kamigaki, A., Kondo, M., Hayashi, M. and Nishimura, M. (2007) Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant Cell Physiol. 48, 763-774 (Pubitemid 47356089)
6. Kemp, S. and Wanders, R. J. (2007) X-linked adrenoleukodystrophy: very long-chain fatty acid metabolism, ABC half-transporters and the complicated route to treatment. Mol. Genet. Metab. 90, 268-276
7. Kemp, S. and Wanders, R. (2010) Biochemical aspects of X-linked adrenoleukodystrophy. Brain Pathol. 20, 831-837
8. 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 (Pubitemid 23070480)
9. Rottensteiner, H. and Theodoulou, F. L. (2006) The ins and outs of peroxisomes: co-ordination of membrane transport and peroxisomal metabolism. Biochim. Biophys. Acta 1763, 1527-1540
10. Higgins, C. F. (1992) ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113
11. 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., doi:10.1111/j.1476-5381.2011.01435.x
12. 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
13. 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
14. 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
15. Ofman, R., Dijkstra, I. M., van Roermund, C. W., Burger, N., Turkenburg, M., van Cruchten, A., van Engen, C. E., Wanders, R. J. and Kemp, S. (2010) The role of ELOVL1 in very long-chain fatty acid homeostasis and X-linked adrenoleukodystrophy. EMBO Mol. Med. 2, 90-97
16. 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
17. van Roermund, C. W., Visser, W., 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
18. Fourcade, S., Ruiz, M., Camps, C., Schlüter, A., Houten, S. M., Mooyer, P. A., Pàmpols, T., Dacremont, G., Wanders, R. J., Giròs, M. and Pujol, A. (2009) A key role for the peroxisomal ABCD2 transporter in fatty acid homeostasis. Am. J. Physiol. Endocrinol. Metab. 296, E211-E221
19. Genin, E., Geillon, F., Gondecaille, C., Athias, A., Gambert, P., Trompier, D. and Savary, S. (2011) Substrate specificity overlap and interaction between adrenoleukodystrophy protein (ALDP/ABCD1) and adrenoleukodystrophy- related protein (ALDRP/ABCD2). J. Biol. Chem. 286, 8075-8084
20. Braiterman, L. T., Zheng, S., Watkins, P. A., Geraghty, M. T., Johnson, G., McGuinness, M. C., Moser, A. B. and Smith, K. D. (1998) Suppression of peroxisomal membrane protein defects by peroxisomal ATP binding cassette (ABC) proteins. Hum. Mol. Genet. 7, 239-247
21. Netik, A., Forss-Petter, S., Holzinger, A., Molzer, B., Unterrainer, G. and Berger, J. (1999) Adrenoleukodystrophy-related protein can compensate functionally for adrenoleukodystrophy protein deficiency (X-ALD): implications for therapy. Hum. Mol. Genet. 8, 907-913
22. 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
23. Wanders, R. J., Vreken, P., Ferdinandusse, S., Jansen, G. A., Waterham, H. R., van Roermund, C. W. and van Grunsven, E. G. (2001) Peroxisomal fatty acid α- and β-oxidation in humans: enzymology, peroxisomal metabolite transporters and peroxisomal diseases. Biochem. Soc. Trans. 29, 250-267
24. 2-terminal hydrophobic property determines the subcellular localization of ABC subfamily D proteins. Exp. Cell Res. 315, 190-205
25. Zolman, B. K., Silva, I. D. and Bartel, B. (2001) The Arabidopsis pxa1mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. Plant Physiol. 127, 1266-1278 (Pubitemid 33112184)
26. 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
27. 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)
28. Hooks, M. A., Turner, J. E., Murphy, E. C., Johnston, K. A., Burr, S. and Jaros?awski, S. (2007) The Arabidopsis ALDP protein homologue COMATOSE is instrumental in peroxisomal acetate metabolism. Biochem. J. 406, 399-406 (Pubitemid 47425446)
29. Footitt, S., Marquez, J., Schmuths, H., Baker, A., Theodoulou, F. L. and Holdsworth, M. (2006) Analysis of the role of COMATOSE and peroxisomal β-oxidation in the determination of germination potential in Arabidopsis. J. Exp. Bot. 57, 2805-2814
30. Footitt, S., Dietrich, D., Fait, A., Fernie, A. R., Holdsworth, M. J., Baker, A. and Theodoulou, F. L. (2007) The COMATOSE ATP-binding cassette transporter is required for full fertility in Arabidopsis. Plant Physiol. 144, 1467-1480
31. Kunz, H. H., Scharnewski, M., Feussner, K., Feussner, I., Flügge, U. I., Fulda, M. and Gierth, M. (2009) The ABC transporter PXA1 and peroxisomal β-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell 21, 2733-2749
32. Slocombe, S. P., Cornah, J., Pinfield-Wells, H., Soady, K., Zhang, Q., Gilday, A., Dyer, J. M. and Graham, I. A. (2009) Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol. J. 7, 694-703
33. 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
34. 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
35. 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
36. Girzalsky, W., Saffian, D. and Erdmann, R. (2010) Peroxisomal protein translocation. Biochim. Biophys. Acta 1803, 724-731
37. Schmidt, F., Treiber, N., Zocher, G., Bjelic, S., Steinmetz, M. O., Kalbacher, H., Stehle, T. and Dodt, G. (2010) Insights into peroxisome function from the structure of PEX3 in complex with a soluble fragment of PEX19. J. Biol. Chem. 285, 25410-25417
38. Schueller, N., Holton, S. J., Fodor, K., Milewski, M., Konarev, P., Stanley, W. A., Wolf, J., Erdmann, R., Schliebs, W., Song, Y. H. and Wilmanns, M. (2010) The peroxisomal receptor Pex19p forms a helical mPTS recognition domain. EMBO J. 29, 2491-2500
39. Strausberg, R. L., Feingold, E. A., Grouse, L. H., Derge, J. G., Klausner, R. D., Collins, F. S., Wagner, L., Shenmen, C. M., Schuler, G. D., Altschul, S. F. et al. (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc. Natl. Acad. Sci. U.S.A. 99, 16899-16903
40. Sparkes, I. A., Hawes, C. and Baker, A. (2005) AtPEX2 and AtPEX10 are targeted to peroxisomes independently of known endoplasmic reticulum trafficking routes. Plant Physiol. 139, 690-700
41. Hadden, D. A., Phillipson, B. A., Johnston, K. A., Brown, L. A., Manfield, I. W., El-Shami, M., Sparkes, I. A. and Baker, A. (2006) Arabidopsis PEX19 is a dimeric protein that binds the peroxin PEX10. Mol. Membr. Biol. 23, 325-336
42. Boisnard-Lorig, C., Colon-Carmona, A., Bauch, M., Hodge, S., Doerner, P., Bancharel, E., Dumas, C., Haseloff, J. and Berger, F. (2001) Dynamic analyses of the expression of the HISTONE::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 13, 495-509 (Pubitemid 32265371)
43. Unterrainer, G., Molzer, B., Forss-Petter, S. and Berger, J. (2000) Co-expression of mutated and normal adrenoleukodystrophy protein reduces protein function: implications for gene therapy of X-linked adrenoleukodystrophy. Hum. Mol. Genet. 9, 2609-2616
44. Sparkes, I. A., Runions, J., Kearns, A. and Hawes, C. (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1, 2019-2025
45. Clough, S. J. and Bent, A. F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743
46. Dietrich, D., Schmuths, H., De Marcos Lousa, C., 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
47. Linka, N., Theodoulou, F. L., Haslam, R. P., Linka, M., Napier, J. A., Neuhaus, H. E. and Weber, A. P. (2008) Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell 20, 3241-32
48. Engelen, M., Ofman, R., Mooijer, P. A., Poll-The, B. T., Wanders, R. J. and Kemp, S. (2008) Cholesterol-deprivation increases mono-unsaturated very long-chain fatty acids in skin fibroblasts from patients with X-linked adrenoleukodystrophy. Biochim. Biophys. Acta 1781, 105-111
49. Kemp, S., Valianpour, F., Mooyer, P. A., Kulik, W. and Wanders, R. J. (2004) Method for measurement of peroxisomal very-long-chain fatty acid β-oxidation in human skin fibroblasts using stable-isotope-labeled tetracosanoic acid. Clin. Chem. 50, 1824-1826
50. Valianpour, F., Selhorst, J. J., van Lint, L. E., van Gennip, A. H., Wanders, R. J. and Kemp, S. (2003) Analysis of very long-chain fatty acids using electrospray ionization mass spectrometry. Mol. Genet. Metab. 79, 189-196
51. Landrum, M., Smertenko, A., Edwards, R., Hussey, P. J. and Steele, P. G. (2010) BODIPY probes to study peroxisome dynamics in vivo. Plant J. 62, 529-538
52. Halbach, A., Lorenzen, S., Landgraf, C., Volkmer-Engert, R., Erdmann, R. and Rottensteiner, H. (2005) Function of the PEX19-binding site of human adrenoleukodystrophy protein as targeting motif in man and yeast: PMP targeting is evolutionarily conserved. J. Biol. Chem. 280, 21176-21182
53. Yernaux, C., Fransen, M., Brees, C., Lorenzen, S. and Michels, P. A. (2006) Trypanosoma bruceiglycosomal ABC transporters: identification and membrane targeting. Mol. Membr. Biol. 23, 157-172
54. Saveria, T., Halbach, A., Erdmann, R., Volkmer-Engert, R., Landgraf, C., Rottensteiner, H. and Parsons, M. (2007) Conservation of PEX19-binding motifs required for protein targeting to mammalian peroxisomal and trypanosome glycosomal membranes. Eukaryotic Cell 6, 1439-1449 (Pubitemid 47257713)
55. Sacksteder, K. A., Jones, J. M., South, S. T., Li, X., Liu, Y. and Gould, S. J. (2000) PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis. J. Cell Biol. 148, 931-944
56. Kemp, S., Pujol, A., Waterham, H. R., van Geel, B. M., Boehm, C. D., Raymond, G. V., Cutting, G. R., Wanders, R. J. and Moser, H. W. (2001) ABCD1 mutations and the X-linked adrenoleukodystrophy mutation database: role in diagnosis and clinical correlations. Hum. Mutat. 18, 499-515
57. Kemp, S., Wei, H. M., Lu, J. F., Braiterman, L. T., McGuinness, M. C., Moser, A. B., Watkins, P. A. and Smith, K. D. (1998) Gene redundancy and pharmacological gene therapy: implications for X-linked adrenoleukodystrophy. Nat. Med. 4, 1261-1268
58. Takahashi, N., Morita, M., Maeda, T., Harayama, Y., Shimozawa, N., Suzuki, Y., Furuya, H., Sato, R., Kashiwayama, Y. and Imanaka, T. (2007) Adrenoleukodystrophy: subcellular localization and degradation of adrenoleukodystrophy protein (ALDP/ABCD1) with naturally occurring missense mutations. J. Neurochem. 101, 1632-1643 (Pubitemid 46848851)
59. Lemieux, B., Miquel, M., Somerville, C. and Browse, J. (1990) Mutants of Arabidopsis with alterations in seed lipid fatty-acid composition. Theor. Appl. Genet. 80, 234-240