Role of CYP311A1 in wing development of Drosophila melanogaster.
Cyp311a1
apoptosis
cell cortex
cell proliferation
lipid
wing
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
06 Mar 2024
06 Mar 2024
Historique:
revised:
11
01
2024
received:
31
10
2023
accepted:
17
01
2024
medline:
6
3
2024
pubmed:
6
3
2024
entrez:
6
3
2024
Statut:
aheadofprint
Résumé
Lipid homeostasis is crucial for growth and development of organisms. Several cytochrome P450 monooxygenases (CYPs) are involved in lipid metabolism. The function of Cyp311a1 in the anterior midgut as a regulator of phosphatidylethanolamine (PE) metabolism in Drosophila melanogaster has been demonstrated, as depletion of Cyp311a1 caused larval growth arrest that was partially rescued by supplying PE. In this study, we investigated the role of CYP311A1 in wing morphogenesis in Drosophila. Using the GAL4-UAS system, Cyp311a1 was selectively knocked down in the wing disc. A deformed wing phenotype was observed in flies with reduced Cyp311a1 transcripts. BODIPY and oil red O staining revealed a reduction of neutral lipids in the wing disc after the depletion of Cyp311a1. In addition, we observed an enhanced sensitivity to Eosin Y penetration in the wings of Cyp311a1 knocked-down flies. Moreover, the reduction of CYP311A1 function in developing wings does not affect cell proliferation and apoptosis, but entails disordered Phalloidin or Cadherin distribution, suggesting an abnormal cell morphology and cell cortex structure in wing epithelial cells. Taken together, our results suggest that Cyp311a1 is needed for wing morphogenesis by participating in lipid assembly and cell homeostasis.
Identifiants
pubmed: 38445520
doi: 10.1111/1744-7917.13342
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 32170505
Organisme : National Natural Science Foundation of China
ID : 32170526
Organisme : Natural Science Foundation of Shanxi Province
ID : 20210302123473
Informations de copyright
© 2024 Institute of Zoology, Chinese Academy of Sciences.
Références
Adler, P.N., Sobala, L.F., Thom, D. and Nagaraj, R. (2013) dusky-like is required to maintain the integrity and planar cell polarity of hairs during the development of the Drosophila wing. Developmental Biology, 379, 76-91.
Balabanidou, V., Kampouraki, A., Maclean, M., Blomquist, G.J., Tittiger, C., Juárez, M.P. et al. (2016) Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae. Proceedings of the National Academy of Sciences USA, 113, 9268-9273.
Binh, T.D., Pham, T.L.A., Men, T.T., Dang, T.T.P. and Kamei, K. (2019) LSD-2 dysfunction induces dFoxO-dependent cell death in the wing of Drosophila melanogaster. Biochemical and Biophysical Research Communications, 509, 491-497.
Chen, N., Fan, Y.L., Bai, Y., Li, X.D., Zhang, Z.F. and Liu, T.-X. (2016) Cytochrome P450 gene, CYP4G51, modulates hydrocarbon production in the pea aphid Acyrthosiphon pisum. Insect Biochemistry and Molecular Biology, 76, 84-94.
Chung, H., Sztal, T., Pasricha, S., Sridhar, M., Batterham, P. and Daborn, P.J. (2009) Characterization of Drosophila melanogaster cytochrome P450 genes. Proceedings of the National Academy of Sciences USA, 106, 5731-5736.
Dermauw, W., Van Leeuwen, T. and Feyereisen, R. (2020) Diversity and evolution of the P450 family in arthropods. Insect Biochemistry and Molecular Biology, 127, 103490.
Dong, W., Zhang, X., Kong, Y., Zhao, Z., Mahmoud, A., Wu, L. et al. (2022) CYP311A1 in the anterior midgut is involved in lipid distribution and microvillus integrity in Drosophila melanogaster. Cellular and Molecular Life Sciences, 79, 261.
Fauny, J.D., Silber, J. and Zider, A. (2005) Drosophila Lipid Storage Droplet 2 gene (Lsd-2) is expressed and controls lipid storage in wing imaginal discs. Developmental Dynamics, 232, 725-732.
Feyereisen, R. (2012) Insect CYP genes and P450 enzymes. Insect Molecular Biology and Biochemistry, 236-316.
Fristrom, D., Wilcox, M. and Fristrom, J. (1993) The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development (Cambridge, England), 117, 509-523.
Giraudo, M., Hilliou, F., Fricaux, T., Audant, P., Feyereisen, R. and Le Goff, G. (2015) Cytochrome P450s from the fall armyworm (Spodoptera frugiperda): responses to plant allelochemicals and pesticides. Insect Molecular Biology, 24, 115-128.
Guittard, E., Blais, C., Maria, A., Parvy, J.P., Pasricha, S., Lumb, C. et al. (2011) CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Developmental Biology, 349, 35-45.
Guo, L., Zhang, Z., Xu, W., Ma, J., Liang, N., Li, C. et al. (2023) Expression profile of CYP402C1 and its role in resistance to imidacloprid in the whitefly Bemisia tabaci. Insect Science, 30, 146-160.
Guo, Y., Zhang, X., Wu, H., Yu, R., Zhang, J., Zhu, K.Y. et al. (2015) Identification and functional analysis of a cytochrome P450 gene CYP9AQ2 involved in deltamethrin detoxification from Locusta migratoria. Pesticide Biochemistry and Physiology, 122, 1-7.
Hipfner, D.R. and Cohen, S.M. (2004) Connecting proliferation and apoptosis in development and disease. Nature Reviews Molecular Cell Biology, 5, 805-815.
Hurbain, I., Macé, A.S., Romao, M., Prince, E., Sengmanivong, L., Ruel, L. et al. (2022) Microvilli-derived extracellular vesicles carry Hedgehog morphogenic signals for Drosophila wing imaginal disc development. Current Biology, 32, 361-373.e6.
Jacobson, M.D., Weil, M. and Raff, M.C. (1997) Programmed cell death in animal development. Cell, 88, 347-354.
Mak, H.Y. (2012) Thematic review series: lipid droplet synthesis and metabolism: from yeast to man: lipid droplets as fat storage organelles in Caenorhabditis elegans. Journal of Lipid Research, 53, 28.
Klein, T. (2001) Wing disc development in the fly: the early stages. Current Opinion in Genetics & Development, 11, 470-475.
Men, T.T., Binh, T.D., Yamaguchi, M., Huy, N.T. and Kamei, K. (2016) Function of Lipid Storage Droplet 1 (Lsd1) in wing development of Drosophila melanogaster. International Journal of Molecular Sciences, 17, 648.
Milán, M., Campuzano, S. and García-Bellido, A. (1997) Developmental parameters of cell death in the wing disc of Drosophila. Proceedings of the National Academy of Sciences USA, 94, 5691-5696.
Namiki, T., Niwa, R., Sakudoh, T., Shirai, K.I., Takeuchi, H. and Kataoka, H. (2005) Cytochrome P450 CYP307A1/Spook: a regulator for ecdysone synthesis in insects. Biochemical and Biophysical Research Communications, 337, 367-374.
Palm, W., Sampaio, J.L., Brankatschk, M., Carvalho, M., Mahmoud, A., Shevchenko, A. et al. (2012) Lipoproteins in Drosophila melanogaster: assembly, function, and influence on tissue lipid composition. PLoS Genetics, 8, e1002828.
Palm, W., Swierczynska, M.M., Kumari, V., Ehrhart-Bornstein, M., Bornstein, S.R. and Eaton, S. (2013) Secretion and signaling activities of lipoprotein-associated hedgehog and non-sterol-modified hedgehog in flies and mammals. PLoS Biology, 11, e1001505.
Panáková, D., Sprong, H., Marois, E., Thiele, C. and Eaton, S. (2005) Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature, 435, 58-65.
Pei, X., Bai, T., Luo, Y., Zhang, Z., Li, S., Fan, Y. et al. (2023) Acetyl coenzyme A carboxylase modulates lipogenesis and sugar homeostasis in Blattella germanica. Insect Science, Available from: https://doi.org/10.1111/1744-7917.13245
Qiu, Y., Tittiger, C., Wicker-Thomas, C., Le Goff, G., Young, S., Wajnberg, E. et al. (2012) An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proceedings of the National Academy of Sciences USA, 109, 14858-14863.
Thanh, M.T., Pham, T.L.A., Tran, B.D., Nguyen, Y.D.H. and Kaeko, K. (2020) Drosophila model for studying the link between lipid metabolism and development. Frontiers in Bioscience-Landmark, 25, 147-158.
Umemori, M., Habara, O., Iwata, T., Maeda, K., Nishinoue, K., Okabe, A. et al. (2009) RNAi-mediated knockdown showing impaired cell survival in Drosophila wing imaginal disc. Gene Regulation and Systems Biology, 3, 11-20.
Van Meer, G., Voelker, D.R. and Feigenson, G.W. (2008) Membrane lipids: where they are and how they behave. Nature Reviews Molecular Cell Biology, 9, 112.
Wang, Y., Carballo, R.G. and Moussian, B. (2017) Double cuticle barrier in two global pests, the whitefly Trialeurodes vaporariorum and the bedbug Cimex lectularius. Journal of Experimental Biology, 220, 1396-1399.
Wang, Y.L., Wu, L.X., Li, H.Y., Wen, X.Q., Ma, E.B., Zhu, K.Y. et al. (2021) The microRNA miR-184 regulates the CYP303A1 transcript level to control molting of Locusta migratoria. Insect Science, 28, 941-951.
Wang, Y., Yu, Z., Zhang, J. and Moussian, B. (2016) Regionalization of surface lipids in insects. Proceedings of the Royal Society B: Biological Sciences, 283, 20152994.
Werck-Reichhart, D. and Feyereisen, R. (2000) Cytochromes P450: a success story. Genome Biology, 1, 1-9.
Wu, L., Zhang, Z.F., Yu, Z., Yu, R., Ma, E., Fan, Y. et al. (2020) Both LmCYP4G genes function in decreasing cuticular penetration of insecticides in Locusta migratoria. Pest Management Science, 76, 3541-3550.
Yu, Z., Zhang, X., Wang, Y., Moussian, B., Zhu, K.Y., Li, S. et al. (2016) LmCYP4G102: an oenocyte-specific cytochrome P450 gene required for cuticular waterproofing in the migratory locust Locusta migratoria. Scientific Reports, 6, 29980.