Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster

Saari, Sina; Andjelković, Ana; Garcia, Geovana S.; Jacobs, Howard T.; Oliveira, Marcos T.

doi:10.1186/s12861-017-0151-3

Cited by 18 publications

(15 citation statements)

References 42 publications

(58 reference statements)

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“…However, it is unclear how the AOX-mediated changes in the QH 2 /Q ratio can impact metabolism and subsequently, ROS production at other mitochondrial sites. Recently, AOX expression was shown to decrease male fertility in Drosophila melanogaster [67]. While the role of ROS in mediating fertility is unclear, it demonstrates that AOX can influence physiologic processes.…”

Section: Detecting and Modulating Ret Ros Generationmentioning

confidence: 99%

Physiologic Implications of Reactive Oxygen Species Production by Mitochondrial Complex I Reverse Electron Transport

2019

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Mitochondrial reactive oxygen species (ROS) can be either detrimental or beneficial depending on the amount, duration, and location of their production. Mitochondrial complex I is a component of the electron transport chain and transfers electrons from NADH to ubiquinone. Complex I is also a source of ROS production. Under certain thermodynamic conditions, electron transfer can reverse direction and reduce oxygen at complex I to generate ROS. Conditions that favor this reverse electron transport (RET) include highly reduced ubiquinone pools, high mitochondrial membrane potential, and accumulated metabolic substrates. Historically, complex I RET was associated with pathological conditions, causing oxidative stress. However, recent evidence suggests that ROS generation by complex I RET contributes to signaling events in cells and organisms. Collectively, these studies demonstrate that the impact of complex I RET, either beneficial or detrimental, can be determined by the timing and quantity of ROS production. In this article we review the role of site-specific ROS production at complex I in the contexts of pathology and physiologic signaling.

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Section: Detecting and Modulating Ret Ros Generationmentioning

confidence: 99%

Physiologic Implications of Reactive Oxygen Species Production by Mitochondrial Complex I Reverse Electron Transport

2019

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“…Sperm expressing AOX, which bypasses a major site of mtROS formation in the electron transport chain, complex III [28], would therefore be expected to show lower ROS production. Given our results, it seems likely that, while AOX is expressed in the testes and seminal vesicles of AOX males [29], it is not expressed in the germline itself. Although the daGal4 driver is supposedly ubiquitously expressed, it is not unusual for "ubiquitous" drivers to show no expression in germ cells [30].…”

Section: Discussionmentioning

confidence: 66%

Somatic production of reactive oxygen species does not predict its production in sperm cells across Drosophila melanogaster lines

et al. 2021

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Objective Sperm ageing has major evolutionary implications but has received comparatively little attention. Ageing in sperm and other cells is driven largely by oxidative damage from reactive oxygen species (ROS) generated by the mitochondria. Rates of organismal ageing differ across species and are theorized to be linked to somatic ROS levels. However, it is unknown whether sperm ageing rates are correlated with organismal ageing rates. Here, we investigate this question by comparing sperm ROS production in four lines of Drosophila melanogaster that have previously been shown to differ in somatic mitochondrial ROS production, including two commonly used wild-type lines and two lines with genetic modifications standardly used in ageing research. Results Somatic ROS production was previously shown to be lower in wild-type Oregon-R than in wild-type Dahomey flies; decreased by the expression of alternative oxidase (AOX), a protein that shortens the electron transport chain; and increased by a loss-of-function mutation in dj-1β, a gene involved in ROS scavenging. Contrary to predictions, we found no differences among these four lines in the rate of sperm ROS production. We discuss the implications of our results, the limitations of our study, and possible directions for future research.

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“…Considering that the genes encoding any alternative enzyme have been lost independently from the evolutionary lines that led to the arthropods and vertebrates, it is plausible that these enzymes might also impact these animals’ fitness negatively. We have recently investigated male reproductive success in AOX‐expressing flies as an important component of fitness, and showed that AOX can cause a significant decrease in mature sperm production, due to an abnormal accumulation of these cells in the testes (Saari et al, ). These males reproduce normally under non‐competitive conditions, but are ultimately unable to succeed in sperm competition assays against wild‐type males, the most likely reproductive condition present in nature for Drosophila .…”

Section: Potential Negative Impacts For Animal Physiology and Reprodumentioning

confidence: 99%

Xenotopic expression of alternative electron transport enzymes in animal mitochondria and their impact in health and disease

Camargo

Chioda

Rodrigues

et al. 2018

Cell Biology International

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The mitochondrial respiratory chain in vertebrates and arthropods is different from that of most other eukaryotes because they lack alternative enzymes that provide electron transfer pathways additional to the oxidative phosphorylation (OXPHOS) system. However, the use of diverse experimental models, such as human cells in culture, Drosophila melanogaster and the mouse, has demonstrated that the transgenic expression of these alternative enzymes can impact positively many phenotypes associated with human mitochondrial and other cellular dysfunction, including those typically presented in complex IV deficiencies, Parkinson's, and Alzheimer's. In addition, these enzymes have recently provided extremely valuable data on how, when, and where reactive oxygen species, considered by many as “by‐products” of OXPHOS, can contribute to animal longevity. It has also been shown that the expression of the alternative enzymes is thermogenic in cultured cells, causes reproductive defects in flies, and enhances the deleterious phenotype of some mitochondrial disease models. Therefore, all the reported beneficial effects must be considered with caution, as these enzymes have been proposed to be deployed in putative gene therapies to treat human diseases. Here, we present a brief review of the scientific data accumulated over the past decade that show the benefits and the risks of introducing alternative branches of the electron transport into mammalian and insect mitochondria, and we provide a perspective on the future of this research field.

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Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster

Cited by 18 publications

References 42 publications

Physiologic Implications of Reactive Oxygen Species Production by Mitochondrial Complex I Reverse Electron Transport

Physiologic Implications of Reactive Oxygen Species Production by Mitochondrial Complex I Reverse Electron Transport

Somatic production of reactive oxygen species does not predict its production in sperm cells across Drosophila melanogaster lines

Xenotopic expression of alternative electron transport enzymes in animal mitochondria and their impact in health and disease

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