The transition from vitellogenesis to choriogenesis triggers the downregulation of the UPR sensors IRE1 and PERK and alterations in the ER architecture in the follicle cells of the vector Rhodnius prolixus

Ríos, T.; Bomfim, Larissa; Ramos, Isabela

doi:10.1007/s00441-021-03547-z

Cited by 8 publications

(12 citation statements)

References 51 publications

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“…Within the ovary, all mRNAs tended to be more expressed in the tropharium, suggesting that this site is indeed the main source of maternal mRNA synthesis in the ovary and that cytoplasmic bridges are used to deliver the mRNAs to the transcriptionally inactive developing oocytes (Kunkel, 1991). This pattern, of highest expression levels in the tropharium, has been observed before in R. prolixus for genes of the autophagy pathway (Vieira et al, 2018;Bomfim and Ramos, 2020;Pereira et al, 2020), the ubiquitin-proteasome system (Pereira et al, 2022) and the unfolded protein response (Rios et al, 2022). It is important to notice, however, that although the temperature, humidity, light/dark cycles, and blood feeding intervals for each insect in this study were strictly controlled, it is expected that adult insects develop certain phenotypes during their early life.…”

Section: Discussionsupporting

confidence: 61%

Functional characterization of maternally accumulated hydrolases in the mature oocytes of the vector Rhodnius prolixus reveals a new protein phosphatase essential for the activation of the yolk mobilization and embryo development

Almeida

Dittz²,

Pereira³

et al. 2023

Front. Physiol.

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Yolk biogenesis and consumption have been well conserved in oviparous animals throughout evolution. Most egg-laying animals store yolk proteins within the oocytes’ yolk granules (Ygs). Following fertilization, the Ygs participate in controlled pathways of yolk breakdown to support the developing embryo’s anabolic metabolism. While the unfolding of the yolk degradation program is a crucial process for successful development in many species, the molecular mechanisms responsible for yolk mobilization are still mysterious and have mostly not been explored. Here, we investigate the functional role of the oocyte maternally accumulated mRNAs of a protein phosphatase (PP501) and two aspartic proteases (cathepsin-D 405, CD405 and cathepsin-D 352, CD352) in the yolk degradation and reproduction of the insect vector of Chagas disease Rhodnius prolixus. We found that PP501 and CD352 are highly expressed in the vitellogenic ovary when compared to the other organs of the adult insect. Parental RNAi silencing of PP501 resulted in a drastic reduction in oviposition and increased embryo lethality whereas the silencing of CD352 resulted only in a slight decrease in oviposition and embryo viability. To further investigate the PP501-caused high reproduction impairment, we investigated the Ygs biogenesis during oocyte maturation and the activation of the yolk degradation program at early development. We found that the Ygs biogenesis was deficient during oogenesis, as seen by flow cytometry, and that, although the PP501-silenced unviable eggs were fertilized, the Ygs acidification and acid phosphatase activity were affected, culminating in a full impairment of the yolk proteins degradation at early embryogenesis. Altogether we found that PP501 is required for the oocyte maturation and the activation of the yolk degradation, being, therefore, essential for this vector reproduction.

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Section: Discussionsupporting

confidence: 61%

Functional characterization of maternally accumulated hydrolases in the mature oocytes of the vector Rhodnius prolixus reveals a new protein phosphatase essential for the activation of the yolk mobilization and embryo development

Almeida

Dittz²,

Pereira³

et al. 2023

Front. Physiol.

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“…In addition, because it is known that even slight changes in the levels of the UPS and autophagy can result in disturbed protein homeostasis and triggering of the unfolded protein response (UPR; Hetz, 2012), we asked if the UPR‐responsive ER chaperones immunoglobulin heavy‐chain‐binding protein (Bip; Pobre et al, 2019) and protein disulfide isomerase (PDI; Perri et al, 2016; Wang, 1998; Wang et al, 2015) would be modulated in our silenced samples. A few isoforms of both chaperones have been previously detected in the ovaries of R. prolixus (Rios et al, 2021). Interestingly, E1‐silenced samples presented a tendency in the upregulation of the ER chaperones BiPs, whereas PDI isoforms remained unaltered (Figure 5a).…”

Section: Resultsmentioning

confidence: 96%

“…In R. prolixus , transcriptome analysis showed that the FCs are committed to transcription, translation, and vesicular traffic (Medeiros et al, 2011), and electron microscopy evidenced the FC's typical secretory cell morphology (Bomfim & Ramos, 2020; Rios et al, 2021). Nevertheless, while studies on the programmed gene‐specific transcriptional activation of the chorion genes have been performed in models such as B. mori and D. melanogaster (Papantonis et al, 2015; Velentzas et al, 2018), the machinery and signals encompassing the chorion proteins synthesis, sorting, and secretion by the FCs are still largely unexplored.…”

Section: Discussionmentioning

confidence: 99%

“…The primers for R. prolixus autophagy‐related genes ATG1/ULK1, ATG3, ATG6/Beclin1, ATG8/LC3 and sequestosome‐1 (p62/SQSTM1) have been described before (Bomfim & Ramos, 2020; Pereira et al, 2020; Santos & Ramos, 2021; Vieira et al, 2018). The primers for the different isoforms of immunoglobulin heavy‐chain‐binding proteins (BIPs) and protein disulfide isomerases (PDIs) have been described by (Rios et al, 2021). R. prolixus 18s gene amplification was used for normalization as previously described (Majerowicz et al, 2011), and its amplification was constant under our experimental conditions (Supporting Information: Figure ) validating it was an appropriate and sufficient endogenous control for our experiments (Bustin et al, 2009).…”

Section: Methodsmentioning

confidence: 99%

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Knockdown of E1‐ and E2‐ubiquitin enzymes triggers defective chorion biogenesis and modulation of autophagy‐related genes in the follicle cells of the vector Rhodnius prolixus

Pereira

Dias

Ramos

2022

Journal Cellular Physiology

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In insects, the last stage of oogenesis is the process where the chorion layers (eggshell) are synthesized and deposited on the surface of the oocytes by the follicle cells. Protein homeostasis is determined by the fine‐tuning of translation and degradation pathways, and the ubiquitin–proteasome system is one of the major degradative routes in eukaryotic cells. The conjugation of ubiquitin to targeted substrates is mediated by the ordered action of E1‐activating, E2‐conjugating, and E3‐ligase enzymes, which covalently link ubiquitin to degradation‐targeted proteins delivering them to the proteolytic complex proteasome. Here, we found that the mRNAs encoding polyubiquitin (pUbq), E1, and E2 enzymes are highly expressed in the ovaries of the insect vector of Chagas Disease Rhodnius prolixus. RNAi silencing of pUbq was lethal whereas the silencing of E1 and E2 enzymes resulted in drastic decreases in oviposition and embryo viability. Eggs produced by the E1‐ and E2‐silenced insects presented particular phenotypes of altered chorion ultrastructure observed by high‐resolution scanning electron microscopy as well as readings for dityrosine cross‐linking and X‐ray elemental microanalysis, suggesting a disruption in the secretory routes responsible for the chorion biogenesis. In addition, the ovaries from silenced insects presented altered levels of autophagy‐related genes as well as a tendency of upregulation in ER chaperones, indicating a disturbance in the general biosynthetic‐secretory pathway. Altogether, we found that E1 and E2 enzymes are essential for chorion biogenesis and that their silencing triggers the modulation of autophagy genes suggesting a coordinated function of both pathways for the progression of choriogenesis.

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“…Early transcriptome analysis showed that the FCs are committed to transcription, translation, and vesicular traffic [56]. Accordingly, electron microscopy evidenced the FC's typical secretory cell morphology with a high content of vesiculated rough endoplasmic reticulum [57,58]. Systemic RNAi experiments targeting the autophagy-related genes ULK1/ATG1, the autophagy-dedicated E2-conjugating enzyme ATG3 [57,59], and E1-activating and E2-conjugating ubiquitin enzymes [60] generated particular phenotypes of chorion malformations due to alterations in the general protein homeostasis of the FCs during choriogenesis, resulting in extremely lower rates of embryo viability.…”

Section: Choriogenesis As An Emerging Target For Safe Interventionsmentioning

confidence: 99%

Vector Control: Insights Arising from the Post-Genomics Findings on Insects’ Reproductive Biology

Ramos¹,

Gomes²

2023

New Advances in Neglected Tropical Diseases

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The high prevalence of neglected vector-borne diseases, such as Chagas disease and dengue fever, imposes enormous health and financial burdens in developing countries. Historically, and still, to this day, the main effective methods to manage those diseases rely on vector population control. Although early efforts in understanding vector-specific biology resulted in important advancements in the development of strategies for the management of vector-borne diseases, studies regarding the complex physiology of local vector species were weakened by the expanding use of insecticide-based tools, which were, at the time, proven simpler and effective. The rising threat of insecticide resistance and climate change (which can expand endemic areas) has reemphasized the need to rely on thorough species-specific vector biology. One approach to controlling vector populations is to disrupt molecular processes or antagonize the metabolic targets required to produce viable eggs. Here, we discuss new findings arising from post-genomics molecular studies on vector reproductive biology and discuss their potential for the elaboration of new effective vector control interventions.

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The transition from vitellogenesis to choriogenesis triggers the downregulation of the UPR sensors IRE1 and PERK and alterations in the ER architecture in the follicle cells of the vector Rhodnius prolixus

Cited by 8 publications

References 51 publications

Functional characterization of maternally accumulated hydrolases in the mature oocytes of the vector Rhodnius prolixus reveals a new protein phosphatase essential for the activation of the yolk mobilization and embryo development

Functional characterization of maternally accumulated hydrolases in the mature oocytes of the vector Rhodnius prolixus reveals a new protein phosphatase essential for the activation of the yolk mobilization and embryo development

Knockdown of E1‐ and E2‐ubiquitin enzymes triggers defective chorion biogenesis and modulation of autophagy‐related genes in the follicle cells of the vector Rhodnius prolixus

Vector Control: Insights Arising from the Post-Genomics Findings on Insects’ Reproductive Biology

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