Structure-function analysis of peroxisomal ATP-binding cassette transporters using chimeric dimers

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24511-24520

  Geillon, Flore ^a   Gondcaille, Catherine ^a   Charbonnier, Soëli ^a   Van Roermund, Carlo W ^b   Lopez, Tatiana E ^a   Dias, Alexandre M M ^a   De Barros, Jean Paul Pais ^c   Arnould, Christine ^d   Wanders, Ronald J ^b   Trompier, Doriane ^a   Savary, Stéphane ^a  

^a Faculté des Sciences Gabriel   (France)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; FATTY ACIDS; POLYUNSATURATED FATTY ACIDS; PROTEINS;

ATP-BINDING CASSETTE; ATP-BINDING CASSETTE TRANSPORTERS; CO-IMMUNOPRECIPITATION ASSAYS; DOCOSAHEXAENOIC ACID; HUMAN SKIN FIBROBLAST; STRUCTURE-FUNCTION ANALYSIS; SUBSTRATE SPECIFICITY; VERY LONG-CHAIN FATTY ACIDS;

DIMERS;

ABC TRANSPORTER; ABC TRANSPORTER D1; ABC TRANSPORTER D2; DOCOSAHEXAENOIC ACID; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; UNCLASSIFIED DRUG; VERY LONG CHAIN FATTY ACID; PRIMER DNA;

ADRENOLEUKODYSTROPHY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME SPECIFICITY; FATTY ACID METABOLISM; FUNGUS MUTANT; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SKIN FIBROBLAST; STRUCTURE ACTIVITY RELATION; YEAST; ANIMAL; CELL LINE; CHEMISTRY; DIMERIZATION; METABOLISM; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; CELL LINE; DIMERIZATION; DNA PRIMERS; HUMANS; MICE; PEROXISOMES; PLASMIDS; POLYMERASE CHAIN REACTION; RATS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84906888527     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.575506     Document Type: Article

References (51)

1. Trompier, D., and Savary, S. (2013) X-linked Adrenoleukodystrophy, Vol. 2, pp. 1-134, Morgan & Claypool Life Sciences, Princeton, NJ
2. 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)
3. 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 (Pubitemid 26052877)
4. 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
5. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 (Pubitemid 44387602)
6. Guimarães, C. P., Domingues, P., Aubourg, P., Fouquet, F., Pujol, A., Jime-nez- Sanchez, G., Sá-Miranda, C., and Azevedo, J. E. (2004) Mouse liver PMP70 and ALDP: homomeric interactions prevail in vivo. Biochim. Biophys. Acta 1689, 235-243
7. 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 perox-isomal ABC half-transporter ALDP functions as a homodimer and accepts acyl-CoA esters. FASEB J. 22, 4201-4208
8. 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 β-oxidation. Biochim. Biophys. Acta 1811, 148-152
9. van Roermund, C. W., Ijlst, L., Wagemans, T., Wanders, R. J., 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
10. Genin, E. C., Geillon, F., Gondcaille, C., Athias, A., Gambert, P., Trompier, D., and Savary, S. (2011) Substrate specificity overlap and interaction between adrenoleukodystrophy protein (ALDP/ABCD1) and adrenoleu-kodystrophy-related protein (ALDRP/ABCD2). J. Biol. Chem. 286, 8075-8084
11. Smith, K. D., Kemp, S., Braiterman, L. T., Lu, J. F., Wei, H. M., Geraghty, M., Stetten, G., Bergin, J. S., Pevsner, J., and Watkins, P. A. (1999) X-linked adrenoleukodystrophy: genes, mutations, and phenotypes. Neurochem. Res. 24, 521-535 (Pubitemid 29187404)
12. Liu, L. X., Janvier, K., Berteaux-Lecellier, V., Cartier, N., Benarous, R., and Aubourg, P. (1999) Homo- and heterodimerization of peroxisomal ATP-binding cassette half-transporters. J. Biol. Chem. 274, 32738-32743 (Pubitemid 129535304)
13. Tanaka, A. R., Tanabe, K., Morita, M., Kurisu, M., Kasiwayama, Y., Matsuo, M., Kioka, N., Amachi, T., Imanaka, T., and Ueda, K. (2002) ATP binding/hydrolysis by and phosphorylation of peroxisomal ATP-binding cassette proteins PMP70 (ABCD3) and adrenoleukodystrophy protein (ABCD1). J. Biol. Chem. 277, 40142-40147 (Pubitemid 35191006)
14. Hillebrand, M., Verrier, S. E., Ohlenbusch, A., Schäfer, A., Söling, H. D., Wouters, F. S., and Gärtner, J. (2007) Live cell FRET microscopy: homoand heterodimerization of two human peroxisomal ABC transporters, the adrenoleukodystrophy protein (ALDP, ABCD1) and PMP70 (ABCD3). J. Biol. Chem. 282, 26997-27005 (Pubitemid 47501958)
15. Berger, J., Albet, S., Bentejac, M., Netik, A., Holzinger, A., Roscher, A. A., Bugaut, M., and Forss-Petter, S. (1999) The four murine peroxisomal ABC-transporter genes differ in constitutive, inducible and developmental expression. Eur. J. Biochem. 265, 719-727 (Pubitemid 29489005)
16. Troffer-Charlier, N., Doerflinger, N., Metzger, E., Fouquet, F., Mandel, J. L., and Aubourg, P. (1998) Mirror expression of adrenoleukodystrophy and adrenoleukodystrophy related genes in mouse tissues and human cell lines. Eur. J. Cell Biol. 75, 254-264 (Pubitemid 28174650)
17. Trompier, D., Gondcaille, C., Lizard, G., and Savary, S. (2014) Regulation of the adrenoleukodystrophy-related gene (ABCD2): Focus on oxysterols and LXR antagonists. Biochem. Biophys. Res. Commun. 446, 651-655
18. 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 (Pubitemid 29189059)
19. Flavigny, E., Sanhaj, A., Aubourg, P., and Cartier, N. (1999) Retroviralmediated adrenoleukodystrophy-related gene transfer corrects very long chain fatty acid metabolism in adrenoleukodystrophy fibroblasts: implications for therapy. FEBS Lett. 448, 261-264 (Pubitemid 29168499)
20. Pujol, A., Ferrer, I., Camps, C., Metzger, E., Hindelang, C., Callizot, N., Ruiz, M., Pàmpols, T., Giròs, M., and Mandel, J. L. (2004) Functional overlap between ABCD1 (ALD) and ABCD2 (ALDR) transporters: a therapeutic target for X-adrenoleukodystrophy. Hum. Mol. Genet. 13, 2997-3006 (Pubitemid 39585232)
21. Weber, F. D., Wiesinger, C., Forss-Petter, S., Regelsberger, G., Einwich, A., Weber, W. H., Köhler, W., Stockinger, H., and Berger, J. (2014) X-linked adrenoleukodystrophy: very long-chain fatty acid metabolism is severely impaired in monocytes but not in lymphocytes. Hum. Mol. Genet. 23, 2542-2550
22. Liu, J., Liang, S., Liu, X., Brown, J. A., Newman, K. E., Sunkara, M., Morris, A. J., Bhatnagar, S., Li, X., Pujol, A., and Graf, G. A. (2012) The absence of ABCD2 sensitizes mice to disruptions in lipid metabolism by dietary erucic acid. J. Lipid Res. 53, 1071-1079
23. Liu, J., Sabeva, N. S., Bhatnagar, S., Li, X. A., Pujol, A., and Graf, G. A. (2010) ABCD2 is abundant in adipose tissue and opposes the accumulation of dietary erucic acid (C22:1) in fat. J. Lipid Res. 51, 162-168
24. Jimenez-Sanchez, G., Hebron, K. J., Thomas, G., and Valle, D. (1999) Targeted disruption of the 70kDa peroxisomal membrane protein (PMP70) in mouse is associated with an increase in the related P70R protein, deficiency of hepatic glycogen and a dicarboxylic aciduria. Pediatr. Res. 45, 139A
25. Jimenez-Sanchez, G., Silva-Zolezzi, I., Hebron, K. J., Mihalik, S., Watkins, P., Moser, A., Thomas, G., Wood, P. A., and Valle, D. (2000) Defective phytanic and pristanic acids metabolism in PMP70 deficient mice results in defective nonshivering thermogenesis and dicarboxylic aciduria. J. Inherited Metab. Dis. 23, 256
26. Gueugnon, F., Volodina, N., Taouil, J. E., Lopez, T. E., Gondcaille, C., Grand, A. S., Mooijer, P. A., Kemp, S., Wanders, R. J., and Savary, S. (2006) A novel cell model to study the function of the adrenoleukodystrophyrelated protein. Biochem. Biophys. Res. Commun. 341, 150-157 (Pubitemid 43117399)
27. 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)
28. Fouquet, F., Zhou, J. M., Ralston, E., Murray, K., Troalen, F., Magal, E., Robain, O., Dubois-Dalcq, M., and Aubourg, P. (1997) Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system. Neurobiol. Dis. 3, 271-285 (Pubitemid 27180757)
29. Bons, J. A., Michielsen, E. C., de Boer, D., Bouwman, F. G., Jaeken, J., van Dieijen-Visser, M. P., Rubio-Gozalbo, M. E., and Wodzig, W. K. (2008) A specific immunoprecipitation method for isolating isoforms of insulinlike growth factor binding protein-3 from serum. Clin. Chim. Acta 387, 59-65 (Pubitemid 350050931)
30. Baarine, M., Andréoletti, P., Athias, A., Nury, T., Zarrouk, A., Ragot, K., Vejux, A., Riedinger, J. M., Kattan, Z., Bessede, G., Trompier, D., Savary, S., Cherkaoui-Malki, M., and Lizard, G. (2012) Evidence of oxidative stress in very long chain fatty acid-treated oligodendrocytes and potentialization of ROS production using RNA interference-directed knockdown of ABCD1 and ACOX1 peroxisomal proteins. Neuroscience 213, 1-18
31. Hashimoto, T., Kuwabara, T., Usuda, N., and Nagata, T. (1986) Purification of membrane polypeptides of rat liver peroxisomes. J. Biochem. 100, 301-310
32. Ewart, G. D., Cannell, D., Cox, G. B., and Howells, A. J. (1994) Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster. Implications for structure-function relationships. J. Biol. Chem. 269, 10370-10377
33. Bhatia, A., Schäfer, H. J., and Hrycyna, C. A. (2005) Oligomerization of the human ABC transporter ABCG2: evaluation of the native protein and chimeric dimers. Biochemistry 44, 10893-10904 (Pubitemid 41153650)
34. 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)
35. 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 longchain fatty acids and exhibits fatty acyl-CoA-stimulated ATPase activity. J. Biol. Chem. 285, 29892-29902
36. 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
37. 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
38. Xu, J., Liu, Y., Yang, Y., Bates, S., and Zhang, J. T. (2004) Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. J. Biol. Chem. 279, 19781-19789 (Pubitemid 38623417)
39. Rosenberg, M. F., Mao, Q., Holzenburg, A., Ford, R. C., Deeley, R. G., and Cole, S. P. (2001) The structure of the multidrug resistance protein 1 (MRP1/ABCC1). crystallization and single-particle analysis. J. Biol. Chem. 276, 16076-16082
40. Landgraf, P., Mayerhofer, P. U., Polanetz, R., Roscher, A. A., and Holzinger, A. (2003) Targeting of the human adrenoleukodystrophy protein to the peroxisomal membrane by an internal region containing a highly conserved motif. Eur. J. Cell Biol. 82, 401-410 (Pubitemid 37168661)
41. Rottensteiner, H., Kramer, A., Lorenzen, S., Stein, K., Landgraf, C., Volkmer-Engert, R., and Erdmann, R. (2004) Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol. Biol. Cell 15, 3406-3417 (Pubitemid 38850133)
42. Kashiwayama, Y., Asahina, K., Shibata, H., Morita, M., Muntau, A. C., Roscher, A. A., Wanders, R. J., Shimozawa, N., Sakaguchi, M., Kato, H., and Imanaka, T. (2005) Role of Pex19p in the targeting of PMP70 to peroxisome. Biochim. Biophys. Acta 1746, 116-128 (Pubitemid 41774286)
43. Pinto, M. P., Grou, C. P., Alencastre, I. S., Oliveira, M. E., Sá-Miranda, C., Fransen, M., and Azevedo, J. E. (2006) The import competence of a peroxisomal membrane protein is determined by Pex19p before the docking step. J. Biol. Chem. 281, 34492-34502 (Pubitemid 46036657)
44. Shibata, H., Kashiwayama, Y., Imanaka, T., and Kato, H. (2004) Domain architecture and activity of human Pex19p, a chaperone-like protein for intracellular trafficking of peroxisomal membrane proteins. J. Biol. Chem. 279, 38486-38494 (Pubitemid 39296001)
45. Zoghbi, M. E., and Altenberg, G. A. (2014) ATP binding to two sites is necessary for dimerization of nucleotide-binding domains of ABC proteins. Biochem. Biophys. Res. Commun. 443, 97-102
46. 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
47. Guimarães, C. P., Sá-Miranda, C., and Azevedo, J. E. (2005) Probing sub-strate- induced conformational alterations in adrenoleukodystrophy protein by proteolysis. J. Hum. Genet. 50, 99-105
48. Ward, A. B., Szewczyk, P., Grimard, V., Lee, C. W., Martinez, L., Doshi, R., Caya, A., Villaluz, M., Pardon, E., Cregger, C., Swartz, D. J., Falson, P. G., Urbatsch, I. L., Govaerts, C., Steyaert, J., and Chang, G. (2013) Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain. Proc. Natl. Acad. Sci. U.S.A. 110, 13386-13391
49. 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
50. Leclercq, S., Skrzypski, J., Courvoisier, A., Gondcaille, C., Bonnetain, F., André, A., Chardigny, J. M., Bellenger, S., Bellenger, J., Narce, M., and Savary, S. (2008) Effect of dietary polyunsaturated fatty acids on the expression of peroxisomal ABC transporters. Biochimie 90, 1602-1607
51. Ferdinandusse, S., Denis, S., Mooijer, P. A., Zhang, Z., Reddy, J. K., Spector, A. A., and Wanders, R. J. (2001) Identification of the peroxisomal betaoxidation enzymes involved in the biosynthesis of docosahexaenoic acid. J. Lipid Res. 42, 1987-1995 (Pubitemid 34001047)