Conservation of targeting but divergence in function and quality control of peroxisomal ABC transporters: An analysis using cross-kingdom expression
Open accessAbstract
ABC (ATP-binding cassette) subfamily D transporters are found in all eukaryotic kingdoms and are known to play essential roles in mammals and plants; however, their number, organization and physiological contexts differ. Via cross-kingdom expression experiments, we have explored the conservation of targeting, protein stability and function between mammalian and plant ABCD transporters. When expressed in tobacco epidermal cells, the mammalian ABCD proteins ALDP (adrenoleukodystrophy protein), ALDR (adrenoleukodystrophy-related protein) and PMP70 (70 kDa peroxisomal membrane protein) targeted faithfully to peroxisomes and P70R (PMP70-related protein) targeted to the ER (endoplasmic reticulum), as in the native host. The Arabidopsis thaliana peroxin AtPex19_1 interacted with human peroxisomal ABC transporters both in vivo and in vitro, providing an explanation for the fidelity of targeting. The fate of X-linked adrenoleukodystrophy disease-related mutants differed between fibroblasts and plant cells. In fibroblasts, levels of ALDP in some ‘protein-absent’ mutants were increased by low-temperature culture, in some cases restoring function. In contrast, all mutant ALDP proteins examined were stable and correctly targeted in plant cells, regardless of their fate in fibroblasts. ALDR complemented the seed germination defect of the Arabidopsis cts-1 mutant which lacks the peroxisomal ABCD transporter CTS (Comatose), but neither ALDR nor ALDP was able to rescue the defect in fatty acid β-oxidation in establishing seedlings. Taken together, our results indicate that the mechanism for trafficking of peroxisomal membrane proteins is shared between plants and mammals, but suggest differences in the sensing and turnover of mutant ABC transporter proteins and differences in substrate specificity and/or function.
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The pathogenic variant p.Ser606Leu reduced the amount of detectable ALD protein to 25% that of control cells in patient cell lines.
“Other ALD-related research studies using patient cell lines revealed that this pathogenic variant reduced the amount of detectable ALD protein to 25% that of control cells (Database Ref 97) [21].”
From Structure and Function of the ABCD1 Variant Database: 20 Years, 940 Pathogenic Variants, and 3400 Cases of Adrenoleukodystrophy (2022) · cites this paper as [21]
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X-linked adrenoleukodystrophy: Clinical, metabolic, genetic and pathophysiological aspects
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Peroxisomal ABC Transporters: An Update
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“thaliana CTS mutant cannot restore the germination and establishment, whereas human ABCD2 only restores the germination phenotype [113].”
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Self-citationStructure-Function Analysis of Peroxisomal ATP-binding Cassette Transporters Using Chimeric Dimers
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- Authors
- Zhang, X., De Marcos Lousa, C., Schutte-Lensink, N., Ofman, R., Wanders, R. J., Baldwin, S. A., Baker, A., Kemp, S., & Theodoulou, F. L.
- Affiliations
- Rothamsted Research (GB)
- Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, U.K.
- Amsterdam UMC Location University of Amsterdam (NL)
- University of Leeds (GB)
- Corresponding author
- Zhang, Xuebin
- Venue
- Biochemical Journal
- Publisher
- Portland Press Ltd.
- Published
- 2011-05-27
- Volume
- 436
- Issue
- 3
- Pages
- 547-557
- ISSN
- 0264-6021 (ISSN-L)
- 1470-8728
- OpenAlex
- W1999282198
- Cited by
- 43
- References
- 10
- Citations by year
- 2023: 2 · 2022: 2 · 2021: 3 · 2020: 5 · 2019: 3 · 2018: 2 · 2017: 2 · 2016: 4 · 2015: 3 · 2014: 6 · 2013: 3 · 2012: 6
- FWCI
- 3.09
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- Locations
- Biochemical Journal (publishedVersion, other-oa)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- HAL (submittedVersion, other-oa)
- Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
- Funders
- European Commission (241622)
- Biotechnology and Biological Sciences Research Council (BB/F007299/1, BB/F007108/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- peroxisomal membrane proteins, protein targeting, protein quality control, ALDP, PMP70, adrenoleukodystrophy, seed germination, fatty acid beta-oxidation, peroxisome biogenesis, cross-species complementation, Arabidopsis thaliana, protein stability
- MeSH terms
- ATP Binding Cassette Transporter, Subfamily D, ATP Binding Cassette Transporter, Subfamily D, Member 1, Adrenoleukodystrophy, Adult, Animals, Endoplasmic Reticulum, Fibroblasts, Humans, Membrane Proteins, Middle Aged, Species Specificity, Nicotiana, Arabidopsis, ATP-Binding Cassette Transporters, Peroxisomes, Arabidopsis Proteins
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