Dysfunction of Oskyddad causes Harlequin-type ichthyosis-like defects in Drosophila melanogaster


Autoři: Yiwen Wang aff001;  Michaela Norum aff001;  Kathrin Oehl aff001;  Yang Yang aff001;  Renata Zuber aff001;  Jing Yang aff001;  Jean-Pierre Farine aff004;  Nicole Gehring aff001;  Matthias Flötenmeyer aff005;  Jean-François Ferveur aff004;  Bernard Moussian aff001
Působiště autorů: Section Animal Genetics, Interfaculty Institute of Cell Biology, University of Tübingen, Tübingen, Germany aff001;  School of Pharmaceutical Science and Technology, Tianjin University, Tianjin, China aff002;  Applied Zoology, Technical University of Dresden, Dresden, Germany aff003;  Centre des Sciences du Goût et de l'Alimentation, UMR-CNRS 6265, Université de Bourgogne, Dijon, France aff004;  Microscopy Unit, Max-Planck-Institut für Entwicklungsbiologie, Tübingen, Germany aff005;  Institute of Biology Valrose, CNRS, Inserm, Université Côte d’Azur, Nice, France aff006
Vyšlo v časopise: Dysfunction of Oskyddad causes Harlequin-type ichthyosis-like defects in Drosophila melanogaster. PLoS Genet 16(1): e32767. doi:10.1371/journal.pgen.1008363
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008363

Souhrn

Prevention of desiccation is a constant challenge for terrestrial organisms. Land insects have an extracellular coat, the cuticle, that plays a major role in protection against exaggerated water loss. Here, we report that the ABC transporter Oskyddad (Osy)—a human ABCA12 paralog—contributes to the waterproof barrier function of the cuticle in the fruit fly Drosophila melanogaster. We show that the reduction or elimination of Osy function provokes rapid desiccation. Osy is also involved in defining the inward barrier against xenobiotics penetration. Consistently, the amounts of cuticular hydrocarbons that are involved in cuticle impermeability decrease markedly when Osy activity is reduced. GFP-tagged Osy localises to membrane nano-protrusions within the cuticle, likely pore canals. This suggests that Osy is mediating the transport of cuticular hydrocarbons (CHC) through the pore canals to the cuticle surface. The envelope, which is the outermost cuticle layer constituting the main barrier, is unaffected in osy mutant larvae. This contrasts with the function of Snu, another ABC transporter needed for the construction of the cuticular inward and outward barriers, that nevertheless is implicated in CHC deposition. Hence, Osy and Snu have overlapping and independent roles to establish cuticular resistance against transpiration and xenobiotic penetration. The osy deficient phenotype parallels the phenotype of Harlequin ichthyosis caused by mutations in the human abca12 gene. Thus, it seems that the cellular and molecular mechanisms of lipid barrier assembly in the skin are conserved during evolution.

Klíčová slova:

Animal wings – Cell membranes – Drosophila melanogaster – Embryos – Epidermis – Insects – Larvae – Lipids


Zdroje

1. Rabionet M, Gorgas K, Sandhoff R. Ceramide synthesis in the epidermis. Biochim Biophys Acta. 2014;1841(3):422–34. doi: 10.1016/j.bbalip.2013.08.011 23988654.

2. Zaki T, Choate K. Recent advances in understanding inherited disorders of keratinization. F1000Res. 2018;7. doi: 10.12688/f1000research.13350.2 30002814; PubMed Central PMCID: PMC6024232.

3. Akiyama M. Corneocyte lipid envelope (CLE), the key structure for skin barrier function and ichthyosis pathogenesis. J Dermatol Sci. 2017;88(1):3–9. doi: 10.1016/j.jdermsci.2017.06.002 28623042.

4. Akiyama M. The roles of ABCA12 in keratinocyte differentiation and lipid barrier formation in the epidermis. Dermato-endocrinology. 2011;3(2):107–12. doi: 10.4161/derm.3.2.15136 21695020; PubMed Central PMCID: PMC3117010.

5. Akiyama M. The roles of ABCA12 in epidermal lipid barrier formation and keratinocyte differentiation. Biochim Biophys Acta. 2014;1841(3):435–40. doi: 10.1016/j.bbalip.2013.08.009 23954554.

6. Akiyama M, Sugiyama-Nakagiri Y, Sakai K, McMillan JR, Goto M, Arita K, et al. Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest. 2005;115(7):1777–84. doi: 10.1172/JCI24834 16007253; PubMed Central PMCID: PMC1159149.

7. Kelsell DP, Norgett EE, Unsworth H, Teh MT, Cullup T, Mein CA, et al. Mutations in ABCA12 underlie the severe congenital skin disease harlequin ichthyosis. Am J Hum Genet. 2005;76(5):794–803. doi: 10.1086/429844 15756637; PubMed Central PMCID: PMC1199369.

8. Rajpar SF, Cullup T, Kelsell DP, Moss C. A novel ABCA12 mutation underlying a case of Harlequin ichthyosis. Br J Dermatol. 2006;155(1):204–6. doi: 10.1111/j.1365-2133.2006.07291.x 16792777.

9. Scott CA, Rajpopat S, Di WL. Harlequin ichthyosis: ABCA12 mutations underlie defective lipid transport, reduced protease regulation and skin-barrier dysfunction. Cell Tissue Res. 2013;351(2):281–8. doi: 10.1007/s00441-012-1474-9 22864982.

10. Thomas AC, Cullup T, Norgett EE, Hill T, Barton S, Dale BA, et al. ABCA12 is the major harlequin ichthyosis gene. J Invest Dermatol. 2006;126(11):2408–13. doi: 10.1038/sj.jid.5700455 16902423.

11. Moussian B. Recent advances in understanding mechanisms of insect cuticle differentiation. Insect Biochem Mol Biol. 2010;40(5):363–75. Epub 2010/03/30. S0965-1748(10)00070-6 [pii] doi: 10.1016/j.ibmb.2010.03.003 20347980.

12. Blomquist GJ, Bagneres AG. Insect Hydrocarbons: Biology, Biochemistry, and Chemical Ecology: Cambridge University Press; 2010.

13. Gutierrez E, Wiggins D, Fielding B, Gould AP. Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature. 2007;445(7125):275–80. Epub 2006/12/01. nature05382 [pii] doi: 10.1038/nature05382 17136098.

14. Ferveur JF. The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. Bioessays. 1997;19(4):353–8. Epub 1997/04/01. doi: 10.1002/bies.950190413 9136633.

15. Wicker-Thomas C, Garrido D, Bontonou G, Napal L, Mazuras N, Denis B, et al. Flexible origin of hydrocarbon/pheromone precursors in Drosophila melanogaster. J Lipid Res. 2015;56(11):2094–101. doi: 10.1194/jlr.M060368 26353752; PubMed Central PMCID: PMC4617396.

16. Qiu Y, Tittiger C, Wicker-Thomas C, Le Goff G, Young S, Wajnberg E, et al. An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci U S A. 2012;109(37):14858–63. doi: 10.1073/pnas.1208650109 22927409; PubMed Central PMCID: PMC3443174.

17. Zuber R, Norum M, Wang Y, Oehl K, Gehring N, Accardi D, et al. The ABC transporter Snu and the extracellular protein Snsl cooperate in the formation of the lipid-based inward and outward barrier in the skin of Drosophila. Eur J Cell Biol. 2018;97(2):90–101. doi: 10.1016/j.ejcb.2017.12.003 29306642.

18. Yu Z, Wang Y, Zhao X, Liu X, Ma E, Moussian B, et al. The ABC transporter ABCH-9C is needed for cuticle barrier construction in Locusta migratoria. Insect Biochem Mol Biol. 2017;87:90–9. doi: 10.1016/j.ibmb.2017.06.005 28610908.

19. Broehan G, Kroeger T, Lorenzen M, Merzendorfer H. Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics. 2013;14:6. doi: 10.1186/1471-2164-14-6 23324493; PubMed Central PMCID: PMC3560195.

20. Liu S, Zhou S, Tian L, Guo E, Luan Y, Zhang J, et al. Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori. BMC Genomics. 2011;12:491. doi: 10.1186/1471-2164-12-491 21981826; PubMed Central PMCID: PMC3224256.

21. Bretschneider A, Heckel DG, Vogel H. Know your ABCs: Characterization and gene expression dynamics of ABC transporters in the polyphagous herbivore Helicoverpa armigera. Insect Biochem Mol Biol. 2016;72:1–9. doi: 10.1016/j.ibmb.2016.03.001 26951878.

22. Pignatelli P, Ingham VA, Balabanidou V, Vontas J, Lycett G, Ranson H. The Anopheles gambiae ATP-binding cassette transporter family: phylogenetic analysis and tissue localization provide clues on function and role in insecticide resistance. Insect Mol Biol. 2018;27(1):110–22. doi: 10.1111/imb.12351 29068552.

23. Qi W, Ma X, He W, Chen W, Zou M, Gurr GM, et al. Characterization and expression profiling of ATP-binding cassette transporter genes in the diamondback moth, Plutella xylostella (L.). BMC Genomics. 2016;17(1):760. doi: 10.1186/s12864-016-3096-1 27678067; PubMed Central PMCID: PMC5039799.

24. Dermauw W, Osborne EJ, Clark RM, Grbic M, Tirry L, Van Leeuwen T. A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics. 2013;14:317. doi: 10.1186/1471-2164-14-317 23663308; PubMed Central PMCID: PMC3724490.

25. Dermauw W, Van Leeuwen T. The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol. 2014;45:89–110. doi: 10.1016/j.ibmb.2013.11.001 24291285.

26. Pasello M, Giudice AM, Scotlandi K. The ABC subfamily A transporters: multifaceted players with incipient potentialities in cancer. Semin Cancer Biol. 2019. doi: 10.1016/j.semcancer.2019.10.004 31605751.

27. Wang Y, Carballo RG, Moussian B. Double cuticle barrier in two global pests, the whitefly Trialeurodes vaporariorum and the bedbug Cimex lectularius. J Exp Biol. 2017;220(Pt 8):1396–9. doi: 10.1242/jeb.156679 28167802.

28. Wang Y, Yu Z, Zhang J, Moussian B. Regionalization of surface lipids in insects. Proc Biol Sci. 2016;283(1830). doi: 10.1098/rspb.2015.2994 27170708; PubMed Central PMCID: PMC4874700.

29. Teasdale RD, Jackson MR. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu Rev Cell Dev Biol. 1996;12:27–54. doi: 10.1146/annurev.cellbio.12.1.27 8970721.

30. Piehler A, Kaminski WE, Wenzel JJ, Langmann T, Schmitz G. Molecular structure of a novel cholesterol-responsive A subclass ABC transporter, ABCA9. Biochem Biophys Res Commun. 2002;295(2):408–16. Epub 2002/08/02. doi: 10.1016/s0006-291x(02)00659-9 12150964.

31. Bera TK, Iavarone C, Kumar V, Lee S, Lee B, Pastan I. MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc Natl Acad Sci U S A. 2002;99(10):6997–7002. Epub 2002/05/16. doi: 10.1073/pnas.102187299 12011458; PubMed Central PMCID: PMC124517.

32. Li Q, Frank M, Akiyama M, Shimizu H, Ho SY, Thisse C, et al. Abca12-mediated lipid transport and Snap29-dependent trafficking of lamellar granules are crucial for epidermal morphogenesis in a zebrafish model of ichthyosis. Dis Model Mech. 2011;4(6):777–85. doi: 10.1242/dmm.007146 21816950; PubMed Central PMCID: PMC3209647.

33. Moussian B, Seifarth C, Muller U, Berger J, Schwarz H. Cuticle differentiation during Drosophila embryogenesis. Arthropod Struct Dev. 2006;35(3):137–52. Epub 2007/12/20. S1467-8039(06)00020-X [pii] doi: 10.1016/j.asd.2006.05.003 18089066.

34. Yanagi T, Akiyama M, Nishihara H, Sakai K, Nishie W, Tanaka S, et al. Harlequin ichthyosis model mouse reveals alveolar collapse and severe fetal skin barrier defects. Hum Mol Genet. 2008;17(19):3075–83. doi: 10.1093/hmg/ddn204 18632686.

35. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30(9):e36. Epub 2002/04/25. doi: 10.1093/nar/30.9.e36 11972351; PubMed Central PMCID: PMC113859.

36. Gangishetti U, Breitenbach S, Zander M, Saheb SK, Muller U, Schwarz H, et al. Effects of benzoylphenylurea on chitin synthesis and orientation in the cuticle of the Drosophila larva. Eur J Cell Biol. 2009;88(3):167–80. Epub 2008/11/11. S0171-9335(08)00134-9 [pii] doi: 10.1016/j.ejcb.2008.09.002 18996617.

37. Moussian B, Schwarz H. Preservation of plasma membrane ultrastructure in Drosophila embryos and larvae prepared by high-pressure freezing and freeze-substitution. Drosophila Information Service. 2010;93:215–9.

38. Tajiri R, Ogawa N, Fujiwara H, Kojima T. Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster. PLoS Genet. 2017;13(1):e1006548. doi: 10.1371/journal.pgen.1006548 28076349; PubMed Central PMCID: PMC5226733.

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Genetika Reprodukční medicína

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PLOS Genetics


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