Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016, Article ID 6786245, 11 pages
http://dx.doi.org/10.1155/2016/6786245
Review Article

ABC Transporter Subfamily D: Distinct Differences in Behavior between ABCD1–3 and ABCD4 in Subcellular Localization, Function, and Human Disease

Department of Biological Chemistry, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, 2630 Sugitani, Toyama 930-0194, Japan

Received 24 June 2016; Accepted 29 August 2016

Academic Editor: Hiroshi Nakagawa

Copyright © 2016 Kosuke Kawaguchi and Masashi Morita. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Dassa and P. Bouige, “The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms,” Research in Microbiology, vol. 152, no. 3-4, pp. 211–229, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Vasiliou, K. Vasiliou, and D. W. Nebert, “Human ATP-binding cassette (ABC) transporter family,” Human Genomics, vol. 3, no. 3, pp. 281–290, 2009. View at Google Scholar · View at Scopus
  3. K. Ueda, “ABC proteins protect the human body and maintain optimal health,” Bioscience, Biotechnology, and Biochemistry, vol. 75, no. 3, pp. 401–409, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Kamijo, S. Taketani, S. Yokota, T. Osumi, and T. Hashimoto, “The 70-kDa peroxisomal membrane protein is a member of the Mdr (P-glycoprotein)-related ATP-binding protein superfamily,” The Journal of Biological Chemistry, vol. 265, no. 8, pp. 4534–4540, 1990. View at Google Scholar · View at Scopus
  5. J. Mosser, A.-M. Douart, C.-O. Sarde et al., “Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters,” Nature, vol. 361, no. 6414, pp. 726–730, 1993. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Lombard-Platet, S. Savary, C.-O. Sarde, J.-L. Mandel, and G. Chimini, “A close relative of the adrenoleukodystrophy (ALD) gene codes for a peroxisomal protein with a specific expression pattern,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 3, pp. 1265–1269, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Shani, G. Jimenez-Sanchez, G. Steel, M. Dean, and D. Valle, “Identification of a fourth half ABC transporter in the human peroxisomal membrane,” Human Molecular Genetics, vol. 6, no. 11, pp. 1925–1931, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Morita and T. Imanaka, “Peroxisomal ABC transporters: structure, function and role in disease,” Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease, vol. 1822, no. 9, pp. 1387–1396, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Geillon, C. Gondcaille, S. Charbonnier et al., “Structure-function analysis of peroxisomal ATP-binding cassette transporters using chimeric dimers,” The Journal of Biological Chemistry, vol. 289, no. 35, pp. 24511–24520, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. C. W. T. van Roermund, W. F. Visser, L. Ijlst et al., “The human peroxisomal ABC half transporter ALDP functions as a homodimer and accepts acyl-CoA esters,” The FASEB Journal, vol. 22, no. 12, pp. 4201–4208, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. C. W. T. van Roermund, W. F. Visser, L. Ijlst, H. R. Waterham, and R. J. A. Wanders, “Differential substrate specificities of human ABCD1 and ABCD2 in peroxisomal fatty acid β-oxidation,” Biochimica et Biophysica Acta—Molecular and Cell Biology of Lipids, vol. 1811, no. 3, pp. 148–152, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. C. W. T. van Roermund, L. Ijlst, T. Wagemans, R. J. A. Wanders, and H. R. Waterham, “A role for the human peroxisomal half-transporter ABCD3 in the oxidation of dicarboxylic acids,” Biochimica et Biophysica Acta—Molecular and Cell Biology of Lipids, vol. 1841, no. 4, pp. 563–568, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Ferdinandusse, G. Jimenez-Sanchez, J. Koster et al., “A novel bile acid biosynthesis defect due to a deficiency of peroxisomal ABCD3,” Human Molecular Genetics, vol. 24, no. 2, Article ID ddu448, pp. 361–370, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Kashiwayama, M. Seki, A. Yasui et al., “70-kDa peroxisomal membrane protein related protein (P70R/ABCD4) localizes to endoplasmic reticulum not peroxisomes, and NH2-terminal hydrophobic property determines the subcellular localization of ABC subfamily D proteins,” Experimental Cell Research, vol. 315, no. 2, pp. 190–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Coelho, J. C. Kim, I. R. Miousse et al., “Mutations in ABCD4 cause a new inborn error of vitamin B12 metabolism,” Nature Genetics, vol. 44, no. 10, pp. 1152–1155, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. F. Rutsch, S. Gailus, I. R. Miousse et al., “Identification of a putative lysosomal cobalamin exporter altered in the cblF defect of vitamin B12 metabolism,” Nature Genetics, vol. 41, no. 2, pp. 234–239, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Kawaguchi, T. Okamoto, M. Morita, and T. Imanaka, “Translocation of the ABC transporter ABCD4 from the endoplasmic reticulum to lysosomes requires the escort protein LMBD1,” Scientific Reports, vol. 6, Article ID 30183, 2016. View at Publisher · View at Google Scholar
  18. R. J. A. Wanders, “Metabolic functions of peroxisomes in health and disease,” Biochimie, vol. 98, no. 1, pp. 36–44, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. H. R. Waterham, S. Ferdinandusse, and R. J. A. Wanders, “Human disorders of peroxisome metabolism and biogenesis,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1863, no. 5, pp. 922–933, 2016. View at Publisher · View at Google Scholar
  20. R. J. A. Wanders and H. R. Waterham, “Biochemistry of mammalian peroxisomes revisited,” Annual Review of Biochemistry, vol. 75, pp. 295–332, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Ferdinandusse, S. Denis, P. A. W. Mooyer et al., “Clinical and biochemical spectrum of D-bifunctional protein deficiency,” Annals of Neurology, vol. 59, no. 1, pp. 92–104, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Ferdinandusse, S. Denis, C. W. T. Van Roermund, R. J. A. Wanders, and G. Dacremont, “Identification of the peroxisomal β-oxidation enzymes involved in the degradation of long-chain dicarboxylic acids,” The Journal of Lipid Research, vol. 45, no. 6, pp. 1104–1111, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. R. J. Wanders, H. R. Waterham, and S. Ferdinandusse, “Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum,” Frontiers in Cell and Developmental Biology, vol. 3, article 83, 2016. View at Publisher · View at Google Scholar
  24. E. Dixit, S. Boulant, Y. Zhang et al., “Peroxisomes are signaling platforms for antiviral innate immunity,” Cell, vol. 141, no. 4, pp. 668–681, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. B.-B. Chu, Y.-C. Liao, W. Qi et al., “Cholesterol transport through lysosome-peroxisome membrane contacts,” Cell, vol. 161, no. 2, pp. 291–306, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Appelqvist, P. Wäster, K. Kågedal, and K. Öllinger, “The lysosome: from waste bag to potential therapeutic target,” Journal of Molecular Cell Biology, vol. 5, no. 4, pp. 214–226, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. D. F. Bainton, “The discovery of lysosomes,” The Journal of Cell Biology, vol. 91, no. 3, pp. 66s–76s, 1981. View at Google Scholar · View at Scopus
  28. B. Schröder, C. Wrocklage, C. Pan et al., “Integral and associated lysosomal membrane proteins,” Traffic, vol. 8, no. 12, pp. 1676–1686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. J. W. Callahan, R. D. Bagshaw, and D. J. Mahuran, “The integral membrane of lysosomes: its proteins and their roles in disease,” Journal of Proteomics, vol. 72, no. 1, pp. 23–33, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Lübke, P. Lobel, and D. E. Sleat, “Proteomics of the lysosome,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1793, no. 4, pp. 625–635, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Mizushima and M. Komatsu, “Autophagy: renovation of cells and tissues,” Cell, vol. 147, no. 4, pp. 728–741, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. E. D. Carstea, J. A. Morris, K. G. Coleman et al., “Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis,” Science, vol. 277, no. 5323, pp. 228–231, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Naureckiene, D. E. Sleat, H. Lacklan et al., “Identification of HE1 as the second gene of Niemann-Pick C disease,” Science, vol. 290, no. 5500, pp. 2298–2301, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Martinez, S. Chakrabarti, T. Hellevik, J. Morehead, K. Fowler, and N. W. Andrews, “Synaptotagmin vii regulates Ca2+-dependent exocytosis of lysosomes in fibroblasts,” The Journal of Cell Biology, vol. 148, no. 6, pp. 1141–1149, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Lee, K. Asahina, T. Okamoto et al., “Role of NH2-terminal hydrophobic motif in the subcellular localization of ATP-binding cassette protein subfamily D: common features in eukaryotic organisms,” Biochemical and Biophysical Research Communications, vol. 453, no. 3, pp. 612–618, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Kashiwayama, K. Asahina, H. Shibata et al., “Role of Pex19p in the targeting of PMP70 to peroxisome,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1746, no. 2, pp. 116–128, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. K. A. Sacksteder, J. M. Jones, S. T. South, X. Li, Y. Liu, and S. J. Gould, “PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis,” Journal of Cell Biology, vol. 148, no. 5, pp. 931–944, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Biermanns and J. Gärtner, “Targeting elements in the amino-terminal part direct the human 70-kDa peroxisomal integral membrane protein (PMP70) to peroxisomes,” Biochemical and Biophysical Research Communications, vol. 285, no. 3, pp. 649–655, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Kashiwayama, K. Asahina, M. Morita, and T. Imanaka, “Hydrophobic regions adjacent to transmembrane domains 1 and 5 are important for the targeting of the 70-kDa peroxisomal membrane protein,” The Journal of Biological Chemistry, vol. 282, no. 46, pp. 33831–33844, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Sakaue, S. Iwashita, Y. Yamashita, Y. Kida, and M. Sakaguchi, “The N-terminal motif of PMP70 suppresses cotranslational targeting to the endoplasmic reticulum,” Journal of Biochemistry, vol. 159, no. 5, pp. 539–551, 2016. View at Publisher · View at Google Scholar
  41. A. Halbach, S. Lorenzen, C. Landgraf, R. Volkmer-Engert, R. Erdmann, and H. Rottensteiner, “Function of the PEX19-binding site of human adrenoleukodystrophy protein as targeting motif in man and yeast. PMP targeting is evolutionarily conserved,” The Journal of Biological Chemistry, vol. 280, no. 22, pp. 21176–21182, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. L. T.-L. Tseng, C.-L. Lin, K.-Y. Tzen, S. C. Chang, and M.-F. Chang, “LMBD1 protein serves as a specific adaptor for insulin receptor internalization,” The Journal of Biological Chemistry, vol. 288, no. 45, pp. 32424–32432, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Cartier, J. Lopez, P. Moullier et al., “Retroviral-mediated gene transfer corrects very-long-chain fatty acid metabolism in adrenoleukodystrophy fibroblasts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 5, pp. 1674–1678, 1995. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Wiesinger, M. Kunze, G. Regelsberger, S. Forss-Petter, and J. Berger, “Impaired very long-chain acyl-CoA β-oxidation in human X-linked adrenoleukodystrophy fibroblasts is a direct consequence of ABCD1 transporter dysfunction,” The Journal of Biological Chemistry, vol. 288, no. 26, pp. 19269–19279, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. C. W. T. van Roermund, L. Ijlst, W. Majczak et al., “Peroxisomal fatty acid uptake mechanism in Saccharomyces cerevisiae,” The Journal of Biological Chemistry, vol. 287, no. 24, pp. 20144–20153, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. C. De Marcos Lousa, C. W. T. Van Roermund, V. L. G. Postis et al., “Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporter is required for transport and metabolism of fatty acids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 4, pp. 1279–1284, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Pujol, I. Ferrer, C. Camps et al., “Functional overlap between ABCD1 (ALD) and ABCD2 (ALDR) transporters: a therapeutic target for X-adrenoleukodystrophy,” Human Molecular Genetics, vol. 13, no. 23, pp. 2997–3006, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Fourcade, M. Ruiz, C. Camps et al., “A key role for the peroxisomal ABCD2 transporter in fatty acid homeostasis,” American Journal of Physiology—Endocrinology and Metabolism, vol. 296, no. 1, pp. E211–E221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. E. C. Genin, F. Geillon, C. Gondcaille et al., “Substrate specificity overlap and interaction between adrenoleukodystrophy protein (ALDP/ABCD1) and adrenoleukodystrophy-related protein (ALDRP/ABCD2),” The Journal of Biological Chemistry, vol. 286, no. 10, pp. 8075–8084, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Berger, S. Albet, M. Bentejac et al., “The four murine peroxisomal ABC-transporter genes differ in constitutive, inducible and developmental expression,” European Journal of Biochemistry, vol. 265, no. 2, pp. 719–727, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Coelho, T. Suormala, M. Stucki et al., “Gene identification for the cblD defect of vitamin B12 metabolism,” The New England Journal of Medicine, vol. 358, no. 14, pp. 1454–1464, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. E. L. Borths, B. Poolman, R. N. Hvorup, K. P. Locher, and D. C. Rees, “In vitro functional characterization of BtuCD-F, the Escherichia coli ABC transporter for vitamin B12 uptake,” Biochemistry, vol. 44, no. 49, pp. 16301–16309, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Beedholm-Ebsen, K. van de Wetering, T. Hardlei, E. Nexø, P. Borst, and S. K. Moestrup, “Identification of multidrug resistance protein 1 (MRP1/ABCC1) as a molecular gate for cellular export of cobalamin,” Blood, vol. 115, no. 8, pp. 1632–1639, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. H. W. Moser, A. Mahmood, and G. V. Raymond, “X-linked adrenoleukodystrophy,” Nature Clinical Practice Neurology, vol. 3, no. 3, pp. 140–151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Kemp, A. Pujol, H. R. Waterham et al., “ABCD1 mutations and the X-linked adrenoleukodystrophy mutation database: role in diagnosis and clinical correlations,” Human Mutation, vol. 18, no. 6, pp. 499–515, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Takahashi, M. Morita, T. Maeda et al., “Adrenoleukodystrophy: subcellular localization and degradation of adrenoleukodystrophy protein (ALDP/ABCD1) with naturally occurring missense mutations,” Journal of Neurochemistry, vol. 101, no. 6, pp. 1632–1643, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Hillebrand, S. E. Verrier, A. Ohlenbusch et al., “Live cell FRET microscopy: homo- and heterodimerization of two human peroxisomal ABC transporters, the adrenoleukodystrophy protein (ALDP, ABCD1) and PMP70 (ABCD3),” The Journal of Biological Chemistry, vol. 282, no. 37, pp. 26997–27005, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. P. C. Smith, N. Karpowich, L. Millen et al., “ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer,” Molecular Cell, vol. 10, no. 1, pp. 139–149, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. K. D. Smith, S. Kemp, L. T. Braiterman et al., “X-linked adrenoleukodystrophy: genes, mutations, and phenotypes,” Neurochemical Research, vol. 24, no. 4, pp. 521–535, 1999. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Holzinger, E. Maier, S. Stöckler-Ipsiroglu, A. Braun, and A. A. Roscher, “Characterization of a novel mutation in exon 10 of the adrenoleukodystrophy gene,” Clinical Genetics, vol. 53, no. 6, pp. 482–487, 1998. View at Google Scholar · View at Scopus
  61. C.-Y. Chuang, L.-Y. Chen, R.-H. Fu et al., “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, vol. 9, no. 8, Article ID e104892, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. D. S. Froese and R. A. Gravel, “Genetic disorders of vitamin B12 metabolism: eight complementation groups—eight genes,” Expert Reviews in Molecular Medicine, vol. 12, article e37, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. T. Takeichi, C.-K. Hsu, H.-S. Yang et al., “Progressive hyperpigmentation in a Taiwanese child due to an inborn error of vitamin B12 metabolism (cblJ),” British Journal of Dermatology, vol. 172, no. 4, pp. 1111–1115, 2016. View at Publisher · View at Google Scholar · View at Scopus
  64. G. C. Korenke, S. Fuchs, E. Krasemann et al., “Cerebral adrenoleukodystrophy (ALD) in only one of monozygotic twins with an identical ALD genotype,” Annals of Neurology, vol. 40, no. 2, pp. 254–257, 1996. View at Publisher · View at Google Scholar · View at Scopus
  65. T. Matsukawa, M. Asheuer, Y. Takahashi et al., “Identification of novel SNPs of ABCD1, ABCD2, ABCD3, and ABCD4 genes in patients with X-linked adrenoleukodystrophy (ALD) based on comprehensive resequencing and association studies with ALD phenotypes,” Neurogenetics, vol. 12, no. 1, pp. 41–50, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Peters, L. R. Charnas, Y. Tan et al., “Cerebral X-linked adrenoleukodystrophy: the international hematopoietic cell transplantation experience from 1982 to 1999,” Blood, vol. 104, no. 3, pp. 881–888, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Cartier, S. Hacein-Bey-Abina, C. C. Bartholomae et al., “Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy,” Science, vol. 326, no. 5954, pp. 818–823, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Morita, N. Shimozawa, Y. Kashiwayama, Y. Suzuki, and T. Imanaka, “ABC subfamily d proteins and very long chain fatty acid metabolism as novel targets in adrenoleukodystrophy,” Current Drug Targets, vol. 12, no. 5, pp. 694–706, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. E. C. Genin, C. Gondcaille, D. Trompier, and S. Savary, “Induction of the adrenoleukodystrophy-related gene (ABCD2) by thyromimetics,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 116, no. 1-2, pp. 37–43, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Morita, M. Kanai, S. Mizuno et al., “Baicalein 5,6,7-trimethyl ether activates peroxisomal but not mitochondrial fatty acid β-oxidation,” Journal of Inherited Metabolic Disease, vol. 31, no. 3, pp. 442–449, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Engelen, L. Tran, R. Ofman et al., “Bezafibrate for X-linked adrenoleukodystrophy,” PLoS ONE, vol. 7, no. 7, Article ID e41013, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. R. V. Kartha, J. Zhou, L. Basso, H. Schröder, P. J. Orchard, and J. Cloyd, “Mechanisms of antioxidant induction with high-dose N-acetylcysteine in childhood cerebral adrenoleukodystrophy,” CNS Drugs, vol. 29, no. 12, pp. 1041–1047, 2015. View at Publisher · View at Google Scholar · View at Scopus