IMR Press / FBL / Volume 25 / Issue 1 / DOI: 10.2741/4799
Drosophila model for studying the link between lipid metabolism and development
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1 Department of Functional Chemistry, Kyoto Institute of Technology, Kyoto, 606-8585, Japan
2 Department of Biology, Cantho University, Cantho City, 900000, Vietnam
Send correspondence to: Kaeko Kamei, Department of Biomolecular Engineering, Kyoto Institute of Technology, Kyoto 606-8585, Japan, Tel: 81-075-724-7553, Fax: 81-075-724-7553, E-mail:
Front. Biosci. (Landmark Ed) 2020, 25(1), 147–158;
Published: 1 January 2020
(This article belongs to the Special Issue Cutting edge of insect biomedical science)

Developmental processes are cascades of biological changes linked with information transfer, growth, and differentiation during the life cycle of an organism. Lipid metabolism plays a vital role in the life cycle of organisms. Drosophila models grant numerous advantages in investigating the underlying mechanisms of each process as well as their connections. In each section of this review, we will discuss multiple studies revealing the function of lipid-related genes in different stages of early development: spermatogenesis, oogenesis, embryogenesis along with late development in life cycle of Drosophila.

Lipid Metabolism

‘Lipid’ is a general term used for substances that are non-polar and insoluble in water. It comprises a wide range of compounds with differing chemical structures. Lipid function varies from storing energy to acting as structural components of cell membranes, to participating in various biological processes. Lipid metabolism is a balance between lipid synthesis and degradation that determines the fat mass (2). The synthesis of lipids in tissues has been considered to be essential for component and energy metabolism during cell transformation. Therefore, lipid metabolism is crucial in the development of organisms. Drosophila melanogaster, the fruit fly, is one of the most commonly used model organisms in biomedical science (3). Most of the metabolism-related genes and gene families are conserved between Drosophila and humans (4). Additionally, many analogous organ systems involved in nutrient uptake, storage and metabolism are common in humans and fruit flies. Moreover, in Drosophila, lipids are stored in the form of triacylglycerol (TAG) in lipid droplets, which are similar to adipocyte cells in mammals. Lipid droplets are omnipresent and dynamically regulated organelles, which are found in various cell types throughout the complex life cycle of the flies (5). These features make Drosophila a versatile model for studying the mechanisms of developmental and processes of lipid metabolism. Previous studies have revealed the function of several lipid-related genes involved in the development, however the overall connection remains to be unveiled. In this article, we selectively review several studies in regard of the link between lipid metabolism and development to generate consistent understanding, as well as encourage further investigations.


Lipid metabolism in Drosophila is divided into two main distinct processes, one is the formation of lipid in the form of TAG called lipogenesis and the other is lipolysis or mobilization of TAG from lipid droplet. The lipogenesis, TAG synthesis follows Kennedy pathway consisting of four enzymatic reactions. Three of four reactions are catalyzed by acyltransferases using fatty acid Coenzyme A (FA-CoA) (6). The initial TAG synthesis step is the acylation of glycerol-3-phosphate (G-3-P) to lysophosphatidic acid (LPA) catalyzed by glycerol-3-phosphate acyltransferase (GPAT) (7). Next, the acylation of LPA to produce phosphatidic acid (PA) catalyzed by 1-acylglycerol-3-phosphate O-acyltransferase (AGPAT) (8). In the third step, the dephosphorylation of PA to diacylglycerol (DAG) at the endoplasmic reticulum (ER) membrane is catalyzed by Mg2+-dependent PA phosphatase, Lipin (9). Lipin is a multi-functional protein that acts as enzyme in TAG synthesis. It is also present in nucleus as a transcriptional co-activator in a complex with peroxisome proliferator-activated receptor gamma coactivator-1alpha (PGC-1alpha) and peroxisome proliferator-activated receptor alpha (PPARalpha), which are master regulators of genes related to mitochondrial biogenesis and fatty acid oxidation (10, 11). The final step from DAG to TAG is catalyzed by diacylglycerol O-acyltransferase (DGAT), encoded by CG1941, CG1942, or CG1943, which remains relatively unexplored (5, 12).

Lipid droplets are made up of neutral lipid core encapsulated with a lipid monolayer with proteins, the best known of which is a family of protein named, PAT domain proteins. The PAT domain proteins include adipose differentiation-related protein (ADRP) and TIP47, and collectively named Perilipin (PLIN) (13). In Drosophila, there are two types of PLIN, called lipid storage droplet (LSD)-1 and 2. The interaction between LSD-1/2 and lipases in lipid droplet varies in associated with different stages of lipolysis according to the body`s requirement of lipid. In basal lipolysis, LSD-1 prevents the access of lipases to lipids droplets, and suppresses activation of Brummer lipase (Bmm), a homolog of human adipocyte triglyceride lipase. This is done by composing a complex with comparative gene identification-58 (CGI-58) which is an activator of Bmm. In stimulated lipolysis, LSD-1 is phosphorylated by protein kinase A (PKA) in response to hormonal signals, and phosphorylated LSD-1 facilitates maximal lipolysis by recruiting hormone-sensitive lipase (HSL) and allowing Bmm to access the lipid droplet (14, 15), while LSD-2 protect lipid droplet from Bmm and HSL-mediated lipolysis

We are able to establish versatile research models for understanding lipid metabolism. An in vivo high throughput obesity study screening more than 500 candidates identified numerous genes which may cause obesity, most of which are related to lipid metabolism. However, several exceptions were shown, including interferon-responsive genes ARID2; the interleukin binding factor ILF2; some ubiquitin enzymes UBE2N, UBR2, HERC4, and FBWX5; and lastly, eight members of Hedgehog signaling pathway which in turn were revealed to be regulators of brown/white adipose cell fate in mice (16). Quantification of TAG content in individuals is a conventional method to identify obesity in Drosophila. Triacylglycerol can be measured using various techniques such as, thin layer chromatography (17), mass spectrometry (18), colorimetric sulfo-phospho-vanillin (19), or indirectly estimation with enzymatic assay post-lipolysis (20). Obesity can also be characterized at the cellular level via quantification of size and number of lipid droplets in the body (21). Similar to mammals, feeding a high-sugar diet to Drosophila model produces hyperglycemia, insulin resistance, and obesity, which imitate type 2 diabetes. Several transcriptional alterations were found, suggesting that Drosophila fed with high-sugar diet could be a potential model for screening genes and pathways contributing to insulin resistance (22). Likewise, high-fat diet can also produce obesity phenotype and promotes insulin resistance in Drosophila (23), as well as enhances the synthesis of cardiomyocyte-derived apoB-lipoproteins (24). In our recent study, we generated a Drosophila model for screening anti-obesity substances (25). We introduced the fusion gene of bmm promoter and enhanced green fluorescent protein (EGFP) gene with nuclear localization sequence in Drosophila. The GFP intensity in nucleus of salivary gland showed good negative correlation with obesity, suggesting that the transgenic fly is useful for screening anti-obesity candidates. By oral administration of various substances to 3rd-instar larvae, we found that histone deacetylases (HDAC) 8 and 9 inhibitors as well as several natural substances, including mulberry leaf, cabbage, and red paprika have potential anti-obesity. In contrary, flies fed with dried tomato showed a slightly decrease in GFP signal, suggesting an increase in lipid storage (25).


Spermatogenesis in Drosophila is a process to produce mature spermatozoa from germ-line stem cells (GSCs). The GSCs will be divided by mitosis to form spermatocytes, then undergo meiosis and cytokinesis to form spermatids, followed by steps of elongation, individualization and coiling to emerge as mature sperms (26). Since Drosophila testes is an organ rich of lipids, multiple membranes remodeling processes occur there, including cytokinesis and differentiation of sperm. The first evidence of a relation between fatty acid and spermatogenesis dated back to the characterization of scully (scu), a homolog of mammalian mitochondrial type II L-3-hydroxyacyl-CoA dehydrogenase, which is involved in beta-oxidation of short chain fatty acids (27). Scu mutants showed phenotypes with significant reductions in size of testes and degeneration of spermatocytes which was caused by abnormal accumulations of lipids (27). On the other hand, very long chain fatty acids (VLCFAs) with over 20 carbon chain-length are components of cellular lipid and also precursors of lipid regulators (28). Cyst cell-specific RNAi of noa (also known as Baldspot which encodes for ELOVL6, a member of elongases for synthesizing VLCFA) resulted in defects in the individualization process during spermatogenesis. Also, the noa gene activity seems to require the communication between cyst cells and germ cells, indicating that cyst cell-specific NOA plays an important role in germ cells development (29). In germ cells, a study showed the necessity of VLCFAs for successful cleavage-furrow ingression during cell division in spermatocytes, since a loss-of-function mutant in Drosophila bond gene, which encodes another member of ELOVL enzyme family, causes male-sterile phenotype (30). Bond also plays a central role in the production of Drosophila sex pheromone CH503, thus controlling the male fertility and rivalry of fertility (31). Therefore, elongation of VLCFAs on both cyst cell and germ cell are crucial for successful spermatogenesis. Moreover, in mammals, beta-oxidation of VLCFAs is performed in peroxisomes and peroxin (pex), an exclusive protein family in peroxisomes, participates in maintaining Drosophila male fertility. Mutants in pex2, pex10, pex13 show elevated levels of VLCFAs in spermatocytes, which lead to defected cytokinesis and misshapen elongated spermatid (32). Besides, lysophospholipid acyltransferase (LPLAT) also contributes in proper spermatogenesis as three Drosophila homologs of membrane-bound O-acyltransferase domain containing 1 (MBOAT1), Oys, Nes, and Frj were found to have combined effect on male fertility. Males with Oys-nes double mutant and oys-nes-frj triple mutant produce defective spermatid individualization phenotype, which can be explained by an elevated level of the saturated fatty acid content of several phospholipids (33).

Phosphatidylinositol (PI) metabolism pathway has been well characterized in Drosophila, which is a cycle between PI, PI-4-phosphate (PI4P), PI-4, 5-bisphosphate (PIP2), and PI 3, 4, 5-triphosphate (PIP3) under the regulation of multiple kinases and phosphatases. By regulating the level of these components, the PI pathway-related genes show their function in controlling sperm development. Reduced level of PIP2 by low-level expression of SigD or null mutation of Sktl (PI 5-kinase, PI5K) results in formation of abnormal bipolar spermatid cysts (34). Contrastingly, overexpression of SigD in testes leads to decrease in number of elongated spermatids, interfering with the ability of docking the basal body to the nuclear envelope, as well as disrupting normal development of flagellar axoneme (35). Notably, co-expression of Sktl, which promotes PIP2 production, suppress the phenotype of SigD overexpression (35). Besides PIP2-related gene, other genes like four wheel drive (fwd) (encodes for kinase PI4Kbeta) or giotto (also called vibrator) also cause cytokinesis defects in spermatids meiosis due to furrow instability (36–38). Further study showed that rab11, a small GTPase, is the link that mediated by both, Fwd and Giotto in the same cytokinetic pathway, responsible for proper cytokinesis (39).

Two cholesterol trafficking proteins, Niemann-Pick type C (NPC) and Oxysterol binding protein (OSBP), have been well studied for their link to Drosophila spermatogenesis. The npc1 (one of two genes encoding NPC) null mutants are male sterile due to the dysfunction in spermatids individualization (40). This study also found the phenotypes are independent of ecdysone, which suggests the requirement of cholesterol transport into testes by NPC to perform individualization (40). In vivo loss-of-function mutants of osbp exhibits spermatids individualization defective phenotype, cooperated by FAN (a member of testes-specific vesicle-associated membrane protein-associated protein, VAP protein). Furthermore, the sterility phenotype of osbp mutant can be rescued by feeding cholesterol, confirming the relation between cholesterol and spermatogenesis (41). Taken together, fatty acid, PI and cholesterol plays essential roles in multiple biological processes of Drosophila spermatogenesis. The fact that the level of these lipids needs to be adequately regulated in spermatocytes for right functions strengthen the contribution of lipid metabolism-related genes for spermatogenesis.


Early studies had revealed the crucial roles of lipid droplet in Drosophila embryo development by investigating its impact and kinetics of embryo vesicle transport (42) or analyzing its associated proteins (43). One of the first lipid metabolism-related genes which had been characterized in embryo development was midway (mdy) gene. The mdy encodes for Drosophila homolog of diglyceride O-acyltransferase (DGAT), which converts DAG into TAG. Mutants of mdy showed the diminished accumulation of neutral lipid, and subsequently induced apoptosis of egg chamber during mid-oogenesis (44). Wun and wun-2 act as lipid phosphate phosphatases and are necessary for germline development in Drosophila embryo. Wun/wun-2 mutations affect the polarity of primordial germ cells (PGCs) as well as prevent them from migrating laterally to the middle of the embryo. The PGCs that fails to relocate would undergo Wun/Wun-2-dependent manner cell death pathway (45). Furthermore, it is suggested that Wun and Wun-2 may participate in the same process with Oys and Nes functions of which were mentioned in spermatogenesis. In female oys and nes double mutant, migration of embryo germ cells is disrupted. These two genes seem to work together since the phenotype is not observed in single mutant of oys, nes or frj. Surprisingly, triple mutants of these genes produce no stronger phenotypes indicating that Frj may not need for this process (33). The effect of Nes expression, however, can be significantly increased by zygotic expression of Wun-2 (33).

The components of the PI pathway also contribute in keeping embryogenesis intact. The PI 4-kinase alpha (PI4KIIIa) is required for enrichment of PI4P and PIP2, which is essential for actin formation, membrane trafficking, and cell polarity. Null mutant of PI4KIIIa, exhibits the effects on egg chamber formation that differ from those of null mutants of fwd (encodes PI4Kβ) and PI4KII (also encodes synthesis enzymes of PI4P and PIP2) (37). Further investigation suggested that the phenotype of PI4KIIIa mutants are more likely to affect Golgi rather than the plasma membrane (46). In contrary, PI4KIIIa gives a similar effect with Sktl (PIP5K), another PIP2-regulating enzyme, in the process of maintaining egg chamber polarity (46, 47). On a side note, another member of PI kinases family, PI3K has been shown to be involved in regulating cell migration, which is crucial for embryonic development, in many different cell types via directly binding their kinase products to proteins (48, 49). Akt, a downstream kinase of PI3K, is similarly, required for normal embryo development, as reduced levels of Akt leads to incomplete centrosome migration, corrupted mitotic spindles, and loss of nuclei trafficking into the embryos (50).

Clearance of histones is necessary in most cells of Drosophila since free histones are toxic, yet in Drosophila embryo, high level of extranuclear histones are accumulated, suggesting its necessity in early development. In this stage, histones are bounded to lipid droplets for its safe storage and delivery, thus, indicating another role of lipid in embryogenesis (43). Jabba is a lipid droplet protein that required for docking of histones to the adipocyte-like organelles. In jabba mutants’ embryos, histones levels of H2A, H2B, and H2Av reduces significantly, despite the mutants develops normally due to the immediate biosynthesis of new histones to compensate for the lacking (51). However, further investigation pointed that jabba mutants’ embryos under conditions of increased temperature induced to hasten the development (from 21°C to 25°C) cannot recruit new histones fast enough to deal with this challenge. This leads to nuclear falling and reduced hatching of eggs (52). Recently, Jabba was characterized as a substrate of casein kinase 2 (CK2) and essential component for an earlier developmental process, oogenesis, as shRNA targeting jabba in female exhibits reduced egg production (53). In addition to roles of lipids in oogenesis, two lipid-related genes, fatty acid synthases named, Bad egg and a homolog of PGC-1 called, Spargel which regulates the formation of eggshells in Drosophila ovary were identified in a screening study of patterning-defect lines. Mutants of bad egg exhibited thin shell phenotype while mutants of spargel caused long pair of dorsal appendages, which act as a respiratory organelle of Drosophila egg (54). It is worth to mention that lipid-related genes can affect early development in yet another manner; two enzymes, Minotaur and Zucchini, which conventionally act in the biosynthesis pathway of phosphatidic acid (PA), also revealed to have critical roles in piRNA biosynthesis (55, 56). piRNA, in turn, guides Piwi proteins to form a molecular code that separates transposons from endogenous genes and prevents germ cell genomes against the activity of those genetic elements (56). All those evidences collectively exhibit that lipid metabolism – related genes regulate oogenesis and embryogenesis in various manners.


Lipid droplets function through all development stages of Drosophila. They are not only detected in adipose tissue but also present in other tissues such as imaginal discs, which give rise to adult body structures like eyes, legs, wing after metamorphosis, salivary glands, gut, the Malpighian tubules, etc. (5). In the fat body of Drosophila, ectopically expressed GFP-tagged lipid storage droplet 1 or 2 (LSD-1 or LSD-2) reside in the lipid droplets (57). Interestingly, our studies showed that the expression of LSD-1 and LSD-2 is not only essential for lipid metabolism but also plays a crucial function in development. The dysfunction of Lsd-1, a Drosophila homolog of perilipin 1 (PLIN1), on the wing disc by genetic knockdown leads to disruption of normal wing development. Further investigation suggested that the loss of LSD-1 function release distress signals in mitochondria, which decrease ATP production while increasing ROS generation and eventually result in cell death (58). On the other hand, while LSD-2 does not show any noticeable effects in eye, hemocytes, nervous system, or thorax; we found that genetic knockdown of lsd-2 also interrupts Drosophila wing formation via inducing cell death. However, unlike LSD-1, we did not find an increase in ROS generation in LSD-2 knockdown flies, but instead, the expression of a highly anticipated transcription factors participating in development, dFoxO and its target in caspase-dependent apoptotic pathway Reaper (Rpr) are significantly up-regulated. Moreover, loss-of-function dFoxO in LSD-2 knockdown flies can rescue the curly wing phenotype and suppress the cell death signal, while overexpression of dFoxO worsens the outcomes (59). Additionally, several studies in other models showed the role of PLIN1in inflammatory responses in lean adipose tissue through lipid dysregulation (60), and that PLIN2 associates with the progression of the age-related disease, such as fatty liver, type 2 diabetes, sarcopenia, and cancer (61).

Furthermore, there are plenty of evidences suggesting the expression of lipid-related proteins in non-adipocyte tissues may link to development. The enzyme of lipogenesis processes, Drosophila 1-acyl-sn-glycerol-3-phosphate acyltransferase 1/2 (dAGPAT1/2, CG3812) expresses exclusively in the nervous system, testes, and ovaries (62). One of the phosphatidate phosphatases, dLipin, is considered as a strong link in development. The decreased expression of this gene not only affect the healthy development of fat body, but also involves in that down-regulation of the insulin-receptor-controlled PI3K-Akt pathway and increased hemolymph sugar levels (63). Schmitt et al. indicated that insulin signaling pathways and a well-known development pathway, target of rapamycin complex 1 (TORC-1), independently regulates the nuclear translocation function of dLipin (63). In mammals, blocking of TORC1 dephosphorylates Lipin 1, leads to its translocation from cytoplasm into the nucleus, where it affects nuclear protein levels, but not mRNA levels, of the transcription factor sterol regulatory element-binding protein 1 (SREBP1). The SREBP1 controls the production of cholesterol, fatty acid, TAG and phospholipid (64). DGAT1 encoded by mdy expresses during all stages of Drosophila development in widely specific tissues such as fat body, ovaries, embryonic, salivary gland, etc. (44). Last but not least, the expression of crucial lipase, Bmm was observed in the multiple post-embryonic organs or tissues including midgut, hindgut, heart, fat body, and salivary gland (62). These findings, taken together, motivate us to investigate the function of lipid metabolism-related genes on the development of specific tissues in Drosophila.


Drosophila has always been considered as a powerful model not only for study in development, but also in lipid metabolism, because of their high resemblance to human genome. It thus provides us with homogenous mechanisms in related disorders. In this review, our goal was to gather the connection between those two aspects: lipid metabolism and development. Various lipid-related genes act together to regulate specific lipid levels which is required to perform crucial biological processes in the membrane during spermatogenesis, or forming eggshells during oogenesis, as well as guiding cell migration during embryogenesis. Beyond that, in recent studies, lipid-related genes prove themselves as participants in multiple developmental processes suggesting their deeper involvement regardless of energy supply. Collectively, these findings not only provide a better understanding of the link between lipid metabolism and development, but also reassure the efficiency of Drosophila model in tackling this matter (Figure 1). In the future, more comprehensive studies on the role of lipid regulation in development and related phenotypes using Drosophila models will be necessary to identify the principle of various associated disorders.

Figure 1

Lipid metabolism relates to different stages of development in Drosophila. There are lipid-related genes function in early development: spermatogenesis, oogenesis, embryogenesis along with late development in life cycle of Drosophila. Genes described in this review are shown.


This work was partially supported by Grants-in-Aid from JSPS Core-to-Core program, B. Asia-Africa Science Platforms.

Needleman D The Material Basis of Life. Trends Cell Biol 2015 25 713 716 DOI: 10.1016/j.tcb.2015.08.011
Vairappan B Chapter 15 - Cholesterol Regulation by Leptin in Alcoholic Liver Disease. In: VBBT-MA of A and N Patel, ed., Academic Press, San Diego 2016 DOI: 10.1016/B978-0-12-800773-0.00015-X
Tolwinski NS Introduction: Drosophila-A Model System for Developmental Biology. J Dev Biol 2017 5 9 DOI: 10.3390/jdb5030009
Reiter LT Potocki L Chien S Gribskov M Bier E A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 2001 11 1114 1125 DOI: 10.1101/gr.169101
Kühnlein RP Thematic review series: Lipid droplet synthesis and metabolism: from yeast to man. Lipid droplet-based storage fat metabolism in Drosophila. J Lipid Res 2012 53 1430 1436 DOI: 10.1194/jlr. R024299
Heier C Kühnlein RP Triacylglycerol Metabolism in Drosophila melanogaster Genetics 210, 1163 LP- 2018 1184 DOI: 10.1534/genetics.118.301583
Wendel AA Lewin TM Coleman RA Glycerol-3-phosphate acyltransferases: rate limiting enzymes of triacylglycerol biosynthesis. Biochim Biophys Acta 2009 1791 501 506 DOI: 10.1016/j.bbalip.2008.10.010
Takeuchi K Reue K Biochemistry, physiology, and genetics of GPAT, AGPAT, and lipin enzymes in triglyceride synthesis. Am J Physiol Endocrinol Metab 2009 296 E1195 209 DOI: 10.1152/ajpendo.90958.2008
Harris TE Finck BN Dual function lipin proteins and glycerolipid metabolism. Trends Endocrinol Metab 2011 22 226 233 DOI: 10.1016/j.tem.2011.02.006
Santos-Rosa H Leung J Grimsey N Peak-Chew S Siniossoglou S The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J 2005 24 1931 1941 DOI: 10.1038/sj.emboj.7600672
Lin J Handschin C Spiegelman BM Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005 1 361 370 DOI: 10.1016/j.cmet.2005.05.004
Yen C-LE Stone SJ Koliwad S Harris C Farese RVJ Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J Lipid Res 2008 49 2283 2301 DOI: 10.1194/jlr. R800018-JLR200
Kimmel AR Brasaemle DL McAndrews-Hill M Sztalryd C Londos C Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J Lipid Res 2010 51 468 471 DOI: 10.1194/jlr. R000034
Yamaguchi T Omatsu N Matsushita S Osumi T CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome. J Biol Chem 2004 279 30490 30497 DOI: 10.1074/jbc. M403920200
Subramanian V Rothenberg A Gomez C Cohen AW Garcia A Bhattacharyya S Shapiro L Dolios G Wang R Lisanti MP Brasaemle DL Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes. J Biol Chem 2004 279 42062 42071 DOI: 10.1074/jbc. M407462200
Pospisilik JA Schramek D Schnidar H Cronin SJF Nehme NT Zhang X Knauf C Cani PD Aumayr K Todoric J Bayer M Haschemi A Puviindran V Tar K Orthofer M Neely GG Dietzl G Manoukian A Funovics M Prager G Wagner O Ferrandon D Aberger F Hui C Esterbauer H Penninger JM Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 2010 140 148 60 DOI: 10.1016/j.cell.2009.12.027
Al-Anzi B Sapin V Waters C Zinn K Wyman RJ Benzer S Obesity-blocking neurons in Drosophila. Neuron 2009 63 329 41 DOI: 10.1016/j.neuron.2009.07.021
Carvalho M Sampaio JL Palm W Brankatschk M Eaton S Shevchenko A Effects of diet and development on the Drosophila lipidome. Mol Syst Biol 2012 8 600 DOI: 10.1038/msb.2012.29
Men TT Thanh DN Van Yamaguchi M Suzuki T Hattori G Arii M Huy NT Kamei K A Drosophila Model for Screening Antiobesity Agents. Biomed Res Int 2016 2016 6293163 DOI: 10.1155/2016/6293163
Hildebrandt A Bickmeyer I Kühnlein RP Reliable Drosophila body fat quantification by a coupled colorimetric assay. PLoS One 2011 6 e23796 DOI: 10.1371/journal.pone.0023796
Grönke S Mildner A Fellert S Tennagels N Petry S Müller G Jäckle H Kühnlein RP Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab 2005 1 323 330 DOI: 10.1016/j.cmet.2005.04.003
Musselman LP Fink JL Narzinski K Ramachandran PV Hathiramani SS Cagan RL Baranski TJ A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis Model Mech 2011 4 842 9 DOI: 10.1242/dmm.007948
Hong S-H Kang M Lee K-S Yu K High fat diet-induced TGF-β/Gbb signaling provokes insulin resistance through the tribbles expression. Sci Rep 2016 6 30265 DOI: 10.1038/srep30265
Lee S Bao H Ishikawa Z Wang W Lim H-Y Cardiomyocyte Regulation of Systemic Lipid Metabolism by the Apolipoprotein B-Containing Lipoproteins in Drosophila. PLOS Genet 2017 13 e1006555 DOI: 10.1371/journal.pgen.1006555
Men TT Binh TD Yamaguchi M Huy NT Kamei K Function of Lipid Storage Droplet 1 (Lsd1) in Wing Development of Drosophila melanogaster. Int J Mol Sci 2016 17 DOI: 10.3390/ijms17050648
Wang C Huang X Lipid metabolism and Drosophila sperm development. Sci China Life Sci 2012 55 35 40 DOI: 10.1007/s11427-012-4274-2
Torroja L Ortuño-Sahagún D Ferrús A Hämmerle B Barbas JA scully, an essential gene of Drosophila, is homologous to mammalian mitochondrial type II L-3-hydroxyacyl-CoA dehydrogenase/amyloid-beta peptide-binding protein. J Cell Biol 1998 141 1009 17 DOI: 10.1083/jcb.141.4.1009
Sassa T Kihara A Metabolism of very long-chain Fatty acids: genes and pathophysiology. Biomol Ther (Seoul) 2014 22 83 92 DOI: 10.4062/biomolther.2014.017
Jung A Hollmann M Schäfer MA The fatty acid elongase NOA is necessary for viability and has a somatic role in Drosophila sperm development. J Cell Sci 2007 120 2924 2934 DOI: 10.1242/jcs.006551
Szafer-Glusman E Giansanti MG Nishihama R Bolival B Pringle J Gatti M Fuller MT A role for very-long-chain fatty acids in furrow ingression during cytokinesis in Drosophila spermatocytes. Curr Biol 2008 18 1426 31 DOI: 10.1016/j.cub.2008.08.061
Ng WC Chin JSR Tan KJ Yew JY The fatty acid elongase Bond is essential for Drosophila sex pheromone synthesis and male fertility. Nat Commun 2015 6 8263 DOI: 10.1038/ncomms9263
Chen H Liu Z Huang X Drosophila models of peroxisomal biogenesis disorder: peroxins are required for spermatogenesis and very-long-chain fatty acid metabolism. Hum Mol Genet 2010 19 494 505 DOI: 10.1093/hmg/ddp518
Steinhauer J Gijón MA Riekhof WR Voelker DR Murphy RC Treisman JE Drosophila lysophospholipid acyltransferases are specifically required for germ cell development. Mol Biol Cell 2009 20 5224 35 DOI: 10.1091/mbc.e09-05-0382
Fabian L Wei H-C Rollins J Noguchi T Blankenship JT Bellamkonda K Polevoy G Gervais L Guichet A Fuller MT Brill JA Phosphatidylinositol 4,5-bisphosphate directs spermatid cell polarity and exocyst localization in Drosophila. Mol Biol Cell 2010 21 1546 55 DOI: 10.1091/mbc.e09-07-0582
Wei H-C Rollins J Fabian L Hayes M Polevoy G Bazinet C Brill JA Depletion of plasma membrane PtdIns(4,5)P2 reveals essential roles for phosphoinositides in flagellar biogenesis. J Cell Sci 2008 121 1076 84 DOI: 10.1242/jcs.024927
Giansanti MG Bonaccorsi S Kurek R Farkas RM Dimitri P Fuller MT Gatti M The Class I PITP Giotto Is Required for Drosophila Cytokinesis. Curr Biol 2006 16 195 201 DOI: 10.1016/j.cub.2005.12.011
Brill JA Hime GR Scharer-Schuksz M Fuller MT A phospholipid kinase regulates actin organization and intercellular bridge formation during germline cytokinesis. Development 2000 127 3855 64
Gatt MK Glover DM The Drosophila phosphatidylinositol transfer protein encoded by vibrator is essential to maintain cleavage-furrow ingression in cytokinesis. J Cell Sci 2006 119 2225 2235 DOI: 10.1242/jcs.02933
Polevoy G Wei H-C Wong R Szentpetery Z Kim YJ Goldbach P Steinbach SK Balla T Brill JA Dual roles for the Drosophila PI 4-kinase Four wheel drive in localizing Rab11 during cytokinesis. J Cell Biol 2009 187 847 858 DOI: 10.1083/jcb.200908107
Wang C Ma Z Scott MP Huang X The cholesterol trafficking protein NPC1 is required for Drosophila spermatogenesis. Dev Biol 2011 351 146 155 DOI: 10.1016/j.ydbio.2010.12.042
Ma Z Liu Z Huang X OSBP- and FAN-mediated sterol requirement for spermatogenesis in Drosophila. Development 2010 137 3775 3784 DOI: 10.1242/dev.049312
Welte MA Gross SP Postner M Block SM Wieschaus EF Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell 1998 92 547 57 DOI: 10.1016/S0092-8674(00)80947-2
Cermelli S Guo Y Gross SP Welte MA The Lipid-Droplet Proteome Reveals that Droplets Are a Protein-Storage Depot. Curr Biol 2006 16 1783 1795 DOI: 10.1016/j.cub.2006.07.062
Buszczak M Lu X Segraves WA Chang TY Cooley L Mutations in the midway Gene Disrupt a Drosophila Acyl Coenzyme A: Diacylglycerol Acyltransferase. Genetics 2002 160 1511 1518
Sano H Renault AD Lehmann R Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J Cell Biol 2005 171 675 83 DOI: 10.1083/jcb.200506038
Tan J Oh K Burgess J Hipfner DR Brill JA PI4KIII is required for cortical integrity and cell polarity during Drosophila oogenesis. J Cell Sci 2014 127 954 966 DOI: 10.1242/jcs.129031
Gervais L Claret S Januschke J Roth S Guichet A PIP5K-dependent production of PIP2 sustains microtubule organization to establish polarized transport in the Drosophila oocyte. Development 2008 135 3829 38 DOI: 10.1242/dev.029009
Cain RJ Ridley AJ Phosphoinositide 3-kinases in cell migration. Biol Cell 2009 101 13 29 DOI: 10.1042/BC20080079
Yamaguchi N Mizutani T Kawabata K Haga H Leader cells regulate collective cell migration via Rac activation in the downstream signaling of integrin β1 and PI3K. Sci Rep 2015 5 7656 DOI: 10.1038/srep07656
Buttrick GJ Beaumont LMA Leitch J Yau C Hughes JR Wakefield JG Akt regulates centrosome migration and spindle orientation in the early Drosophila melanogaster embryo. J Cell Biol 2008 180 537 48 DOI: 10.1083/jcb.200705085
Li Z Thiel K Thul PJ Beller M Kühnlein RP Welte MA Lipid Droplets Control the Maternal Histone Supply of Drosophila Embryos. Curr Biol 2012 22 2104 2113 DOI: 10.1016/j.cub.2012.09.018
Li Z Johnson MR Ke Z Chen L Welte MA Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development. Curr Biol 2014 24 1485 91 DOI: 10.1016/j.cub.2014.05.022
McMillan EA Longo SM Smith MD Broskin S Lin B Singh NK Strochlic TI The protein kinase CK2 substrate Jabba modulates lipid metabolism during Drosophila oogenesis. J Biol Chem 2018 293 2990 3002 DOI: 10.1074/jbc. M117.814657
Khokhar A Chen N Yuan J-P Li Y Landis GN Beaulieu G Kaur H Tower J Conditional switches for extracellular matrix patterning in Drosophila melanogaster. Genetics 2008 178 1283 93 DOI: 10.1534/genetics.106.065912
Rogers AK Situ K Perkins EM Toth KF Zucchini-dependent piRNA processing is triggered by recruitment to the cytoplasmic processing machinery. Genes Dev 2017 31 1858 1869 DOI: 10.1101/gad.303214.117
Vagin V V Yu Y Jankowska A Luo Y Wasik KA Malone CD Harrison E Rosebrock A Wakimoto BT Fagegaltier D Muerdter F Hannon GJ Minotaur is critical for primary piRNA biogenesis. RNA 2013 19 1064 DOI: 10.1261/rna.039669.113
Miura S Gan J-W Brzostowski J Parisi MJ Schultz CJ Londos C Oliver B Kimmel AR Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J Biol Chem 2002 277 32253 32257 DOI: 10.1074/jbc. M204410200
Men TT Binh TD Yamaguchi M Huy NT Kamei K Function of Lipid Storage Droplet 1 (Lsd1) in Wing Development of Drosophila melanogaster. Int J Mol Sci 2016 17 DOI: 10.3390/ijms17050648
Binh TD Pham TLA Men TT Dang TTP Kamei K LSD-2 dysfunction induces dFoxO-dependent cell death in the wing of Drosophila melanogaster. Biochem Biophys Res Commun 2019 509 491 497 DOI: 10.1016/j.bbrc.2018.12.132
Sohn JH Lee YK Han JS Jeon YG Kim JI Choe SS Kim SJ Yoo HJ Kim JB Perilipin 1 (Plin1) deficiency promotes inflammatory responses in lean adipose tissue through lipid dysregulation. J Biol Chem 2018 293 13974 13988 DOI: 10.1074/jbc. RA118.003541
Yan Y Wang H Hu M Jiang L Wang Y Liu P Liang X Liu J Li C Lindstrom-Battle A Lam SM Shui G Deng W-M Jiao R HDAC6 Suppresses Age-Dependent Ectopic Fat Accumulation by Maintaining the Proteostasis of PLIN2 in Drosophila. Dev Cell 2017 43 99 111.e5 DOI: 10.1016/j.devcel.2017.09.001
Chintapalli VR Wang J Dow JAT Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 2007 39 715 720 DOI: 10.1038/ng2049
Schmitt S Ugrankar R Greene SE Prajapati M Lehmann M Drosophila Lipin interacts with insulin and TOR signaling pathways in the control of growth and lipid metabolism. J Cell Sci 2015 128 4395 4406 DOI: 10.1242/jcs.173740
Peterson TR Sengupta SS Harris TE Carmack AE Kang SA Balderas E Guertin DA Madden KL Carpenter AE Finck BN Sabatini DM mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011 146 408 420 DOI: 10.1016/j.cell.2011.06.034
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