The impact of chloroquine-induced autophagy inhibition on the metabolic processes of the fat body in Bombyx mori during larval-pupal metamorphosis
Keywords:
Autophagy, Bombyx mori, Chloroquine, Fat bodyAbstract
The fat body of insects is integral to various metabolic processes, including nutrient transformation, energy storage, and the synthesis of hemolymph proteins. This organ also stores carbohydrates primarily in the form of glycogen and mobilizes them as trehalose, while triglycerides serve as a significant energy reserve. Trophocytes, the principal cells of the fat body, are responsible for its metabolic functions and undergo considerable remodeling during the larval-pupal metamorphosis. Autophagy, particularly macroautophagy, is essential for cellular homeostasis, and any disruption in this process can result in metabolic disorders. In insects, especially during metamorphosis, autophagy is critical for the remodeling of the fat body; however, its effects on fat body metabolism have not been thoroughly investigated. This study aimed to explore the role of autophagy in the metabolic functions of the silkworm, Bombyx mori fat body during larval-pupal metamorphosis, using chloroquine as an autophagy inhibitor. Our findings elucidate the impact of chloroquine treatment on key components of the fat body and provide insights into the role of autophagy in regulating fat body metabolism.
References
Arias E, Cuervo AM. Chaperone-mediated autophagy in protein quality control. Curr Opin Cell Biol. 2011;23(2):184-9.
Athenstaedt K, Daum G. The life cycle of neutral lipids: synthesis, storage and degradation. Cell Mol Life Sci. 2006;63(12):1355-69.
Bergmeyer HU, Bernt E. UV-Assay. In Methods of enzymatic analysis. Academic Press. Biochem Pharmacol. 1976;23:2495-2531.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;7(72):248-54.
Butterworth Fm, Bodenstein D, King Rc. Adipose Tissue of Drosophila Melanogaster. I. An Experimental Study of Larval Fat Body. J Exp Zool. 1965;158:141-53.
Chapman RF. The Insects: Structure and function (4th edition) Cambridge, UK: Cambridge University Press, 1998.
Chino H. Lipid Transport: Biochemistry of Hemolymph Lipophorin. In: Kerkut, G.A. and Gilbert, L.I., Eds., Comprehensive Insect Physiology, Biochemistry and Pharmacology, Pergamon Press, New York. 1985;10:115-135.
Cynober L, Aussel C, Vaubourdolle M, Agneray J, Ekindjian OG. Modulation of insulin action on 2-deoxyglucose uptake by chloroquine in chick embryo fibroblasts. Diabetes. 1987;36(1):27-32.
De Priester W, Van Pelt-Verkuil E, De Leeuw G. Demonstration of acid phosphatase activity induced by 20-hydroxyecdysone in the fat body of Calliphora. Cell Tissue Res. 1979;200(3):435-42.
Dean RL, Collins JV, Locke M. Structure of the fat body. In G. A. Kerkut & L. I. Gilbert (Eds.), Comprehensive insect physiology, biochemistry, and pharmacology, 1985, New York, NY: Pergamon Press, 155-210.
Doeppner TR, Coman C, Burdusel D, Ancuta DL, Brockmeier U, Pirici DN, et al. Long-term treatment with chloroquine increases lifespan in middle-aged male mice possibly via autophagy modulation, proteasome inhibition and glycogen metabolism. Aging (Albany NY). 2022;14(10):4195-4210.
Downer RGH. Physiological and environmental considerations in insect bioenergetics, pp. 1-17. In: R.G.H. Downer (ed.), Energy metabolism in insects, 1981.
Downer RGH, Matthews JR. Patterns of lipid distribution and utilization in insects. Am Zool. 1976;16:733-45p.
De Duve C, De Barsy T, Poole B, Trouet A, Tulkens P, Van Hoof F. Commentary. Lysosomotropic agents. Biochem Pharmacol. 1974;23(18):2495-531.
Han C, Chen E, Shen G, Peng Z, Xu Y, Zhang H, et al. Vitellogenin receptor selectively endocytoses female-specific and highly-expressed hemolymph proteins in the silkworm, Bombyx mori. Biochem Cell Biol. 2017;95(4):510-516.
Haunerland NH. Insect storage proteins: gene families and receptors. Insect Biochem Mol Biol. 1996;26(8-9):755-65.
He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67-93.
Hyrsl P, Simek V. An analysis of hemolymph protein profiles during the final instar, prepupa and pupa of the silkworm Bombyx mori (Lepidoptera, Bombycidae). Biologia, Bratislava. 2005;60:207-213.
Izumi S, Fujie J, Yamada S, Tomino S. Molecular Properties and Biosynthesis of Major Plasma Proteins in Bombyx mori. Biochimica et Biophysica Acta-Protein Structure. 1981;670:222-229.
Kaufmann C, Brown MR. Regulation of carbohydrate metabolism and flight performance by a hypertrehalosaemic hormone in the mosquito Anopheles gambiae. J Insect Physiol. 2008;54(2):367-77.
Kawooya JK, Law JH. Purification and properties of microvitellogenin of Manduca sexta role of juvenile hormone in appearance and uptake. Biochem Biophys Res Commun. 1983;117(2):643-50.
Kim EJ, Park HJ, Park TH. Inhibition of apoptosis by recombinant 30K protein originating from silkworm hemolymph. Biochem Biophys Res Commun. 2003;308(3):523-8.
Kim KH, Lee MS. Autophagy-a key player in cellular and body metabolism. Nat Rev Endocrinol. 2014;10(6):322-37.
Kitada M, Koya D. Autophagy in metabolic disease and ageing. Nature reviews. Endocrinology, 2021;17(11):647–661.
Korolenko TA, Rukavishnikova EV, Safina AF, Dushkin MI, Mynkina GI. Endocytosis by Liver Cells During Suppression of Intralysosomal Proteolysis" Biological Chemistry. 1992;373(2):573-580.
Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970;227(5259):680–685.
Larsen WL. Cell remodeling in the fat body of an insect, Tissue and Cell. 1976;8(1):73-92.
Lenz AG, Holzer H. Effect of chloroquine on proteolytic processes and energy metabolism in yeast. Arch Microbiol. 1984;137:104–108.
Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6:463–477.
Li S, Yu X, Feng Q. Fat body biology in the last decade. Annual Review of Entomology. 2019;64:315–333.
Nagata M, Kobayashi J. Effects of nutrition on storage protein concentrations in the larval hemolymph of the silkworm Bombyx mori. Journal of Sericultural Science of Japan, 1990;59(6):469-474.
Pant R, Morris ID. Variation in glycogen, total free sugars, protein, alkaline and acid phosphatases, citrate and inorganic phosphorus level in fat body of Philosamia ricini (eri-silkworm) during development. J Biochem. 1972;71(1):1-8.
Park MS, Park P, Takeda A. Roles of fat body trophocytes, mycetocytes and urocytes in the American cockroach, Periplaneta americana under starvation conditions: An ultrastructural study, Arthropod Structure & Development. 2013;42(4):287-295.
Poiani SB, Da Cruz-Landim C. Storaged products and presence of acid phosphatase in fat body cells at pre-pupal worker stage of Apis mellifera Linnaeus, 1758 (Hymenoptera, Apidae). Micron. 2012;43(2-3):475-8.
Roma G, Bueno O, Camargo‐Mathias M. Morpho‐physiological analysis of the insect fat body: A review. Micron. 2010;41(5):395-401.
Ryoo HD, Baehrecke EH. Distinct death mechanisms in Drosophila development. Curr Opin Cell Biol. 2010;22:889-95.
Saghir SA, Ansari RA. Metabolism (biotransformation). Faculty Books and Book Chapters 2. Amsterdam, Netherlands: Elsevier, 2014, 1-34.
Schulze RJ, Sathyanarayan A, Mashek DG. Breaking fat: The regulation and mechanisms of lipophagy. Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2017;1862:1178–1187.
Singh R, Xiang Y, Wang Y, Baikati K, Cuervo AM, Luu YK, et al. Autophagy regulates adipose mass and differentiation in mice. J Clin Invest. 2009;119:3329–3339.
Telfer WH, Kunkel JG. The function and evolution of insect storage hexamers. Annu. Rev. Entomol. 1991;36:205-228.
Thompson SN. Trehalose: the insect ‘blood’ sugar. Adv Insect Physiol. 2003:31:205–85.
Tian L, Ma L, Guo E, Deng X, Ma S, Xia Q, et al. 20-Hydroxyecdysone upregulates Atg genes to induce autophagy in the Bombyx fat body. Autophagy. 2013;9(8):1172-87.
Tsuchida K, Wells MA. Digestion, absorption, transport and storage of fat during the last larval stadium of Manduca sexta. Changes in the role of lipophorin in the delivery of dietary lipid to the fat body. Insect biochemistry. 1988;18(3):263-268.
Ujita M, Katsuno Y, Kawachi I, Ueno Y, Banno Y, Fujii H, et al. Glucan-binding activity of silkworm 30-kDa apolipoprotein and its involvement in defense against fungal infection. Biosci Biotechnol Biochem. 2005;69(6):1178-85.
Uranli R, Göncü E, Parlak O. Investigation of the influence of the juvenile hormone analogue fenoxycarb on major hemolymph proteins of the silkworm Bombyx mori during the last larval instar, Turkish Journal of Zoology. 2011;35(2):223-236.
Van Handel E. Rapid determination of glycogen and sugars in mosquitoes. J Am Mosq Control Assoc. 1985a;1(3):299-301.
Van Handel E. Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc. 1985b;1(3):302-4.
Van Handel E, Day JF. Assay of lipids, glycogen and sugars in individual mosquitoes: correlations with wing length in field-collected Aedes vexans. J Am Mosq Control Assoc. 1988;4(4):549-50.
Weidberg H, Shvets E, Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem. 2011;80:125-56.
Xu F, Tautenhahn HM, Dirsch O, Dahmen U. Blocking autophagy with chloroquine aggravates lipid accumulation and reduces intracellular energy synthesis in hepatocellular carcinoma cells, both contributing to its anti-proliferative effect. J Cancer Res Clin Oncol. 2022;148(12):3243-3256.
Yamada T, Habara O, Kubo H, Nishimura T. Fat body glycogen serves as a metabolic safeguard for the maintenance of sugar levels in Drosophila. Development. 2018;14:145(6).
Zheng H, Yang X, Xi Y. Fat body remodeling and homeostasis control in Drosophila. Life Sci. 2016;167:22-31.
Zhong BX, Li JK, Lin JR, Liang JS, Su SK, Xu HS, et al. Possible effect of 30K proteins in embryonic development of silkworm Bombyx mori. Acta Biochim Biophys Sin (Shanghai). 2005;37(5):355-61.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Ebru Goncu, Seçkin Şenkaya, Esen Poyraz Tinartaş, Tugce Ordu
This work is licensed under a Creative Commons Attribution 4.0 International License.
