ABHD5 regulates midgut-specific lipid homeostasis in Bombyx mori.

ABHD5 Bombyx mori CRISPR/Cas9 lipid metabolism

Journal

Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965

Informations de publication

Date de publication:
06 Jun 2024
Historique:
revised: 27 03 2024
received: 04 02 2024
accepted: 03 05 2024
medline: 6 6 2024
pubmed: 6 6 2024
entrez: 6 6 2024
Statut: aheadofprint

Résumé

Lipids are an important energy source and are utilized as substrates for various physiological processes in insects. Comparative gene identification 58 (CGI-58), also known as α/β hydrolase domain-containing 5 (ABHD5), is a highly conserved and multifunctional gene involved in regulating lipid metabolism and cellular energy balance in many organisms. However, the biological functions of ABHD5 in insects are poorly understood. In the current study, we describe the identification and characterization of the ABHD5 gene in the lepidopteran model insect, Bombyx mori. The tissue expression profile investigated using quantitative reverse transcription polymerase chain reaction (RT-qPCR) reveals that BmABHD5 is widely expressed in all tissues, with particularly high levels found in the midgut and testis. A binary transgenic CRISPR/Cas9 system was employed to conduct a functional analysis of BmABHD5, with the mutation of BmABHD5 leading to the dysregulation of lipid metabolism and excessive lipid accumulation in the larval midgut. Histological and physiological analysis further reveals a significant accumulation of lipid droplets in the midgut of mutant larvae. RNA-seq and RT-qPCR analysis showed that genes related to metabolic pathways were significantly affected by the absence of BmABHD5. Altogether, our data prove that BmABHD5 plays an important role in regulating tissue-specific lipid metabolism in the silkworm midgut.

Identifiants

pubmed: 38841829
doi: 10.1111/1744-7917.13386
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Science Fund for Distinguished Young Scholars of Jiangsu Province
ID : BK20221292
Organisme : National Natural Science Foundation of China
ID : 31925007
Organisme : National Natural Science Foundation of China
ID : 32000333

Informations de copyright

© 2024 Institute of Zoology, Chinese Academy of Sciences.

Références

Arêdes, D.S., Rios, T., Carvalho‐Kelly, L.F., Braz, V., Araripe, L.O., Bruno, R.V. et al. (2024) Deficiency of Brummer lipase disturbs lipid mobilization and locomotion, and impairs reproduction due to defects in the eggshell ultrastructure in the insect vector Rhodnius prolixus. Biochimica et Biophysica Acta ‐ Molecular and Cell Biology of Lipids, 1869, 159442.
Arrese, E.L. and Soulages, J.L. (2010) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology, 55, 207–225.
Attardo, G.M., Benoit, J.B., Michalkova, V., Yang, G., Roller, L., Bohova, J., et al. (2012) Analysis of lipolysis underlying lactation in the tsetse fly, Glossina morsitans. Insect Biochemistry and Molecular Biology, 42, 360–370.
Battaglioni, S., Benjamin, D., Wälchli, M., Maier, T. and Hall, M.N. (2022) mTOR substrate phosphorylation in growth control. Cell, 185, 1814–1836.
Brown, A.L. and Mark Brown, J. (2017) Critical roles for α/β hydrolase domain 5 (ABHD5)/comparative gene identification‐58 (CGI‐58) at the lipid droplet interface and beyond. Biochimica et Biophysica Acta ‐ Molecular and Cell Biology of Lipids, 1862, 1233–1241.
Brown, J.M., Betters, J.L., Lord, C., Ma, Y., Han, X., Yang, K. et al. (2010) CGI‐58 knockdown in mice causes hepatic steatosis but prevents diet‐induced obesity and glucose intolerance. Journal of Lipid Research, 51, 3306–3315.
Chen, K., Yu, Y., Zhang, Z., Hu, B., Liu, X., James, A.A. et al. (2023a) Engineering a complex, multiple enzyme‐mediated synthesis of natural plant pigments in the silkworm, Bombyx mori. Proceedings of the National Academy of Sciences USA, 120, e2306322120.
Chen, K., Yu, Y., Zhang, Z., Hu, B., Liu, X. and Tan, A. (2023b) The morphogen Hedgehog is essential for proper adult morphogenesis in Bombyx mori. Insect Biochemistry and Molecular Biology, 153, 103906.
Elsayed, S.M., Torre, E., Tavian, D., Moro, L., Angelini, C., Abdel Ghaffar, T.Y. et al. (2023) A novel ABHD5 mutation in two Chanarin Dorfman siblings with severe and heterogeneous clinical phenotype. Genes and Diseases, 10, 690–693.
Finck, B.N., Gropler, M.C., Chen, Z., Leone, T.C., Croce, M.A., Harris, T.E. et al. (2006) Lipin1 is an inducible amplifier of the hepatic PGC‐1alpha/PPARalpha regulatory pathway. Cell Metabolism, 4, 199–210.
Ghosh, A.K., Ramakrishnan, G., Chandramohan, C. and Rajasekharan, R. (2008) CGI‐58, the causative gene for Chanarin‐Dorfman syndrome, mediates acylation of lysophosphatidic acid. Journal of Biological Chemistry, 283, 24525–24533.
Grabner, G.F., Xie, H., Schweiger, M. and Zechner, R. (2021) Lipolysis: cellular mechanisms for lipid mobilization from fat stores. Nature Metabolism, 3, 1445–1465.
Granneman, J.G., Moore, H.P., Granneman, R.L., Greenberg, A.S., Obin, M.S. and Zhu, Z. (2007) Analysis of lipolytic protein trafficking and interactions in adipocytes. Journal of Biological Chemistry, 282, 5726–5735.
Granneman, J.G., Moore, H.P., Krishnamoorthy, R. and Rathod, M. (2009) Perilipin controls lipolysis by regulating the interactions of AB‐hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). Journal of Biological Chemistry, 284, 34538–34544.
Gronke, S., Mildner, A., Fellert, S., Tennagels, N., Petry, S., Muller, G. et al. (2005) Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metabolism, 1, 323–330.
Gruber, A., Cornaciu, I., Lass, A., Schweiger, M., Poeschl, M., Eder, C. et al. (2010) The N‐terminal region of comparative gene identification‐58 (CGI‐58) is important for lipid droplet binding and activation of adipose triglyceride lipase. Journal of Biological Chemistry, 285, 12289–12298.
Grumet, L., Eichmann, T.O., Taschler, U., Zierler, K.A., Leopold, C., Moustafa, T. et al. (2016) Lysosomal acid lipase hydrolyzes retinyl ester and affects retinoid turnover. Journal of Biological Chemistry, 291, 17977–17987.
Hehlert, P., Hofferek, V., Heier, C., Eichmann, T.O., Riedel, D., Rosenberg, J. et al. (2019) The α/β‐hydrolase domain‐containing 4‐ and 5‐related phospholipase Pummelig controls energy storage in Drosophila. Journal of Lipid Research, 60, 1365–1378.
Hofer, P., Boeszoermenyi, A., Jaeger, D., Feiler, U., Arthanari, H., Mayer, N. et al. (2015) Fatty acid‐binding proteins interact with comparative gene identification‐58 linking lipolysis with lipid ligand shuttling. Journal of Biological Chemistry, 290, 18438–18453.
Igal, R.A., Rhoads, J.M. and Coleman, R.A. (1997) Neutral lipid storage disease with fatty liver and cholestasis. Journal of Pediatric Gastroenterology and Nutrition, 25, 541–547.
Kamal, M., Tokmakjian, L., Knox, J., Han, D., Moshiri, H., Magomedova, L. et al. (2023) PGP‐14 establishes a polar lipid permeability barrier within the C. elegans pharyngeal cuticle. PLoS Genetics, 19, e1011008.
Lass, A., Zimmermann, R., Haemmerle, G., Riederer, M., Schoiswohl, G., Schweiger, M. et al. (2006) Adipose triglyceride lipase‐mediated lipolysis of cellular fat stores is activated by CGI‐58 and defective in Chanarin‐Dorfman syndrome. Cell Metabolism, 3, 309–319.
Lee, J.H., Kong, J., Jang, J.Y., Han, J.S., Ji, Y., Lee, J. et al. (2014) Lipid droplet protein LID‐1 mediates ATGL‐1‐dependent lipolysis during fasting in Caenorhabditis elegans. Molecular and Cellular Biology, 34, 4165–4176.
Lefevre, C., Jobard, F., Caux, F., Bouadjar, B., Karaduman, A., Heilig, R. et al. (2001) Mutations in CGI‐58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin‐Dorfman syndrome. The American Journal of Human Genetics, 69, 1002–1012.
Lehmann, P., Pruisscher, P., Posledovich, D., Carlsson, M., Kakela, R., Tang, P. et al. (2016) Energy and lipid metabolism during direct and diapause development in a pierid butterfly. Journal of Experimental Biology, 219, 3049–3060.
Lord, C.C., Ferguson, D., Thomas, G., Brown, A.L., Schugar, R.C., Burrows, A. et al. (2016) Regulation of hepatic triacylglycerol metabolism by CGI‐58 does not require ATGL co‐activation. Cell Reports, 16, 939–949.
Lu, K., Zhou, J., Chen, X., Li, W., Li, Y., Cheng, Y. et al. (2018) Deficiency of brummer impaires lipid mobilization and JH‐mediated vitellogenesis in the brown planthopper, Nilaparvata lugens. Frontiers in Physiology, 9, 1535.
Mahadevan, S. and Tappel, A.L. (1968) Lysosomal lipases of rat liver and kidney. Journal of Biological Chemistry, 243, 2849–2854.
Matsumoto, Y. and Sekimizu, K. (2016) Evaluation of anti‐diabetic drugs by using silkworm, Bombyx mori. Drug Discoveries and Therapeutics, 10, 19–23.
Montero‐Moran, G., Caviglia, J.M., Mcmahon, D., Rothenberg, A., Subramanian, V., Xu, Z. et al. (2010) CGI‐58/ABHD5 is a coenzyme A‐dependent lysophosphatidic acid acyltransferase. Journal of Lipid Research, 51, 709–719.
Purkrtová, Z., Chardot, T. and Froissard, M. (2015) N‐terminus of seed caleosins is essential for lipid droplet sorting but not for lipid accumulation. Archives of Biochemistry and Biophysics, 579, 47–54.
Sahu‐Osen, A., Montero‐Moran, G., Schittmayer, M., Fritz, K., Dinh, A., Chang, Y.F. et al. (2015) CGI‐58/ABHD5 is phosphorylated on Ser239 by protein kinase A: control of subcellular localization. Journal of Lipid Research, 56, 109–121.
Sanders, M.A., Madoux, F., Mladenovic, L., Zhang, H., Ye, X., Angrish, M. et al. (2015) Endogenous and synthetic ABHD5 ligands regulate ABHD5‐perilipin interactions and lipolysis in fat and muscle. Cell Metabolism, 22, 851–860.
Schmitt, S., Ugrankar, R., Greene, S.E., Prajapati, M. and Lehmann, M. (2015) Drosophila Lipin interacts with insulin and TOR signaling pathways in the control of growth and lipid metabolism. Journal of Cell Science, 128, 4395–4406.
Schweiger, M., Lass, A., Zimmermann, R., Eichmann, T.O. and Zechner, R. (2009) Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI‐58/ABHD5. American Journal of Physiology. Endocrinology and Metabolism, 297, E289–E296.
Sheriff, S., Du, H. and Grabowski, G.A. (1995) Characterization of lysosomal acid lipase by site‐directed mutagenesis and heterologous expression. Journal of Biological Chemistry, 270, 27766–27772.
Srebrnik, A., Brenner, S., Ilie, B. and Messer, G. (1998) Dorfman‐Chanarin syndrome: morphologic studies and presentation of new cases. The American Journal of Dermatopathology, 20, 79–85.
Subramanian, V., Rothenberg, A., Gomez, C., Cohen, A.W., Garcia, A., Bhattacharyya, S. et al. (2004) Perilipin A mediates the reversible binding of CGI‐58 to lipid droplets in 3T3‐L1 adipocytes. Journal of Biological Chemistry, 279, 42062–42071.
Tabunoki, H., Bono, H., Ito, K. and Yokoyama, T. (2016) Can the silkworm (Bombyx mori) be used as a human disease model? Drug Discoveries and Therapeutics, 10, 3–8.
Tabunoki, H., Ono, H., Ode, H., Ishikawa, K., Kawana, N., Banno, Y. et al. (2013) Identification of key uric acid synthesis pathway in a unique mutant silkworm Bombyx mori model of Parkinson's disease. PLoS ONE, 8, e69130.
Tan, Q.Q., Liu, W., Zhu, F., Lei, C.L., Hahn, D.A. and Wang, X.P. (2017) Describing the diapause‐preparatory proteome of the beetle Colaphellus bowringi and identifying candidates affecting lipid accumulation using isobaric tags for mass spectrometry‐based proteome quantification (iTRAQ). Frontiers in Physiology, 8, 251.
Toprak, U., Hegedus, D., Doğan, C. and Güney, G. (2020) A journey into the world of insect lipid metabolism. Archives of Insect Biochemistry and Physiology, 104, e21682.
Traupe, H., Fischer, J. and Oji, V. (2014) Nonsyndromic types of ichthyoses ‐ an update. Journal deer Deutschen Dermatologischen Gesellschaft, 12, 109–121.
Wang, Y., Li, Z., Xu, J., Zeng, B., Ling, L., You, L. et al. (2013) The CRISPR/Cas system mediates efficient genome engineering in Bombyx mori. Cell Research, 23, 1414–1416.
Wu, L., Sokolova, V., Tan, D. and Airola, M. (2022) Molecular basis for membrane binding and lipolysis activation by ABHD5. The FASEB Journal, 36. https://doi.org/10.1096/fasebj.2022.36.S1.L7703
Xie, M. and Roy, R. (2016) Correction: the causative gene in chanarian dorfman syndrome regulates lipid droplet homeostasis in C. elegans. PLoS Genetics, 12, e1006524.
Yamaguchi, T., Omatsu, N., Matsushita, S. and Osumi, T. (2004) CGI‐58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI‐58 mislocalization in Chanarin‐Dorfman syndrome. Journal of Biological Chemistry, 279, 30490–30497.
Yang, F., Xu, X., Hu, B., Zhang, Z., Chen, K., Yu, Y. et al. (2024) Lipid homeostasis is essential for oogenesis and embryogenesis in the silkworm, Bombyx mori. Cellular and Molecular Life Sciences, 81, 127.
Zechner, R., Zimmermann, R., Eichmann, T.O., Kohlwein, S.D., Haemmerle, G., Lass, A. et al. (2012) FAT SIGNALS ‐ lipases and lipolysis in lipid metabolism and signaling. Cell Metabolism, 15, 279–291.
Zhang, H.H., Souza, S.C., Muliro, K.V., Kraemer, F.B., Obin, M.S. and Greenberg, A.S. (2003) Lipase‐selective functional domains of perilipin A differentially regulate constitutive and protein kinase A‐stimulated lipolysis. Journal of Biological Chemistry, 278, 51535–51542.
Zhang, J., Xu, D., Nie, J., Han, R., Zhai, Y. and Shi, Y. (2014) Comparative gene identification‐58 (CGI‐58) promotes autophagy as a putative lysophosphatidylglycerol acyltransferase. Journal of Biological Chemistry, 289, 33044–33053.
Zhou, J., Chen, X., Yan, J., You, K., Yuan, Z., Zhou, Q. et al. (2018) Brummer‐dependent lipid mobilization regulates starvation resistance in Nilaparvata lugens. Archives of Insect Biochemistry and Physiology, 99, e21481.
Ziegler, R. and Van Antwerpen, R. (2006) Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology, 36, 264–272.
Zuber, R., Norum, M., Wang, Y., Oehl, K., Gehring, N., Accardi, D. et al. (2018) 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. European Journal of Cell Biology, 97, 90–101.

Auteurs

Zhiping Xing (Z)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Yuting Zhang (Y)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Hongxia Kang (H)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Hui Dong (H)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Dalin Zhu (D)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Yutong Liu (Y)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Chenxin Sun (C)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Peilin Guo (P)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Bo Hu (B)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Anjiang Tan (A)

Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, China.
Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture, The Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, China.

Classifications MeSH