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

Arêdes, Daniela Saar; Rios, Thamara; Carvalho-Kelly, Luiz Fernando; Braz, Valdir; Araripe, Luciana O.; Bruno, Rafaela V.; Meyer-Fernandes, José Roberto; Ramos, Isabela; Gondim, Katia C.

doi:10.1016/j.bbalip.2023.159442

Cited by 4 publications

(2 citation statements)

References 76 publications

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“…Similarly, the gene expression of CPT1, which is involved in the transport of activated fatty acids inside mitochondria ( De Paula et al, 2023 ), also increased. The same result was observed for Bmm gene expression ( Arêdes et al, 2024 ), which could result in an increase in neutral lipolysis. Moreover, the transcript levels of ACC and DGAT2, genes involved in lipid synthesis ( Alves-Bezerra and Gondim, 2012 ; Saraiva et al, 2021 ), were reduced.…”

Section: Discussionsupporting

confidence: 80%

In the fed state, autophagy plays a crucial role in assisting the insect vector Rhodnius prolixus mobilize TAG reserves under forced flight activity

Santos-Araujo,

Gomes,

Carvalho-Kelly

et al. 2024

Front. Physiol.

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Autophagy is a cellular degradation pathway mediated by highly conserved autophagy-related genes (Atgs). In our previous work, we showed that inhibiting autophagy under starvation conditions leads to significant physiological changes in the insect vector of Chagas disease Rhodnius prolixus; these changes include triacylglycerol (TAG) retention in the fat body, reduced survival and impaired locomotion and flight capabilities. Herein, because it is known that autophagy can be modulated in response to various stimuli, we further investigated the role of autophagy in the fed state, following blood feeding. Interestingly, the primary indicator for the presence of autophagosomes, the lipidated form of Atg8 (Atg8-II), displayed 20%–50% higher autophagic activation in the first 2 weeks after feeding compared to the third week when digestion was complete. Despite the elevated detection of autophagosomes, RNAi-mediated suppression of RpAtg6 and RpAtg8 did not cause substantial changes in TAG or protein levels in the fat body or the flight muscle during blood digestion. We also found that knockdown of RpAtg6 and RpAtg8 led to modest modulations in the gene expression of essential enzymes involved in lipid metabolism and did not significantly stimulate the expression of the chaperones BiP and PDI, which are the main effectors of the unfolded protein response. These findings indicate that impaired autophagy leads to slight disturbances in lipid metabolism and general cell proteostasis. However, the ability of insects to fly during forced flight until exhaustion was reduced by 60% after knockdown of RpAtg6 and RpAtg8. This change was accompanied by TAG and protein increases as well as decreased ATP levels in the fat body and flight muscle, indicating that autophagy during digestion, i.e., under fed conditions, is necessary to sustain high-performance activity.

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Section: Discussionsupporting

confidence: 80%

In the fed state, autophagy plays a crucial role in assisting the insect vector Rhodnius prolixus mobilize TAG reserves under forced flight activity

Santos-Araujo,

Gomes,

Carvalho-Kelly

et al. 2024

Front. Physiol.

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“…Plus, functional studies in many other genes, which do not necessarily encode a protein that makes up the chorion, such as the yellow-g, yellow-g2, and laccase2 from A. albopictus (Wu et al, 2013;Noh et al, 2020), NIFoxL2 and NIFcp3C from N. lugens (Ye et al, 2017) and mucin1 protein from Spodoptera exigua (Ahmed et al, 2021), also resulted in chorion malformations. In R. prolixus, ultrastructural changes in the chorion have already been reported by the depletion of genes related to different pathways, such as ATG1 and ATG3 (Bomfim and Ramos, 2020;Santos and Ramos, 2021), the E1-activating and E2-conjugating ubiquitin enzymes as well as the alpha6 subunit of the 20S proteasome (Pereira et al, 2022;Faria-Reis et al, 2023), the UPR sensors IRE1α and PERK (Rios et al, 2022), Bicaudal C, a conserved embryo development regulator (Pascual et al, 2021), the acetyl-CoA carboxylase enzyme and Brummer lipase, related to lipid metabolism (Moraes et al, 2022;Arêdes et al, 2024) and Duox, a NADPH oxidase (Dias et al, 2013). These findings, when combined, indicate that chorion synthesis in insects is a susceptible process, as the silencing of genes linked to various pathways produced similar phenotypes.…”

Section: Discussionmentioning

confidence: 99%

Knockdown of Sec16 causes early lethality and defective deposition of the protein Rp30 in the eggshell of the vector Rhodnius prolixus

Rios,

Bomfim,

Pereira

et al. 2024

Front. Cell Dev. Biol.

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In nearly every species of insect, embryonic development takes place outside of the mother’s body and is entirely dependent on the elements that the mother had previously stored within the eggs. It is well known that the follicle cells (FCs) synthesize the eggshell (chorion) components during the process of choriogenesis, the final step of oogenesis before fertilization. These cells have developed a specialization in the massive production of chorion proteins, which are essential for the protection and survival of the embryo. Here, we investigate the function of Sec16, a protein crucial for the endoplasmic reticulum (ER) to Golgi traffic, in the oocyte development in the insect Rhodnius prolixus. We discovered that Sec16 is strongly expressed in vitellogenic females’ ovaries, particularly in the choriogenic oocyte and it is mainly associated with the FCs. Silencing of Sec16 by RNAi caused a sharp decline in oviposition rates, F1 viability, and longevity in adult females. In the FCs, genes involved in the unfolded protein response (UPR), the ubiquitin-proteasome system (UPS), and autophagy were massively upregulated, whereas the mRNAs of Rp30 and Rp45—which code for the two major chorion proteins - were downregulated as a result of Sec16 silencing, indicating general proteostasis disturbance. As a result, the outer surface ultrastructure of Sec16-silenced chorions was altered, with decreased thickness, dityrosine crosslinking, sulfur signals, and lower amounts of the chorion protein Rp30. These findings collectively demonstrate the critical role Sec16 plays in the proper functioning of the FCs, which impacts the synthesis and deposition of particular components of the chorion as well as the overall reproduction of this vector.

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ABHD5 regulates midgut‐specific lipid homeostasis in Bombyx mori

Xing,

Zhang,

Kang

et al. 2024

Insect Science

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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.

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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

Cited by 4 publications

References 76 publications

In the fed state, autophagy plays a crucial role in assisting the insect vector Rhodnius prolixus mobilize TAG reserves under forced flight activity

In the fed state, autophagy plays a crucial role in assisting the insect vector Rhodnius prolixus mobilize TAG reserves under forced flight activity

Knockdown of Sec16 causes early lethality and defective deposition of the protein Rp30 in the eggshell of the vector Rhodnius prolixus

ABHD5 regulates midgut‐specific lipid homeostasis in Bombyx mori

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