Distinct metabolic profiles in Drosophila sperm and somatic tissues revealed by two-photon NAD(P)H and FAD autofluorescence lifetime imaging

Wetzker, Cornelia; Reinhardt, Klaus

doi:10.1038/s41598-019-56067-w

Cited by 19 publications

(24 citation statements)

References 57 publications

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“…Increased ROS production may have been caused by a malfunctioning electron transfer chain, which can indeed be related to the possibility that less fluid mitochondrial membranes allow more proton leakage and hence more ROS. However, currently it is unknown to what extent Drosophila sperm metabolize by oxidative phosphorylation (which produces ROS)—a recent study (Wetzker & Reinhardt, ) found Drosophila sperm to be highly glycolytic (which does not lead to ROS production).…”

Section: Discussionmentioning

confidence: 99%

Dietary polyunsaturated fatty acids affect volume and metabolism of Drosophila melanogaster sperm

Guo

Reinhardt

2020

J of Evolutionary Biology

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Dietary fatty acids can accumulate in sperm and affect their function in vertebrates. As Drosophila melanogaster shares several pathways of lipid metabolism and shows similar lipid‐dependent phenotypes but lacks some hormones that in vertebrates regulate lipid metabolism, there is currently no clear prediction as to how dietary fatty acids affect the sperm of D. melanogaster. We manipulated the amount and identity of dietary polyunsaturated fatty acids (PUFA) in the food of D. melanogaster males (a treatment known to affect membrane fluidity) and measured changes in sperm parameters. We found that (a) males reared on food containing PUFA‐rich, plant‐derived lipids showed a slower increase in sperm volume over male age compared to males reared on yeast‐derived lipid food which is richer in saturated fatty acids. (b) The resistance of sperm membrane integrity to osmotic stress was not altered by dietary lipid treatment, but (c) food containing yeast‐derived lipids induced a 46% higher in situ rate of production of reactive oxygen species in sperm cells. These findings show that dietary lipids have similar effects on sperm parameters in Drosophila as in vertebrates, affect some, but not all, sperm parameters and modulate male reproductive ageing. In concert with recent findings of sex‐specific seasonal variation of diet choice in the wild, our results suggest a substantial dietary impact on the dynamics of male reproduction in the wild.

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Section: Discussionmentioning

confidence: 99%

Dietary polyunsaturated fatty acids affect volume and metabolism of Drosophila melanogaster sperm

Guo

Reinhardt

2020

J of Evolutionary Biology

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“…In our study, we focused on free sperm but it is important to note that FLIM allows the measurement of sperm metabolism in intact organs (Wetzker & Reinhardt, 2019). An ambitious, though probably distant, vision is to use FLIM to monitor sperm metabolic health in vivo in humans.…”

Section: Methodological Resultsmentioning

confidence: 99%

“…The measurements were executed using a multiphoton, pulsed titanium: sapphire femtosecond laser (Chameleon Ultra II, Coherent, Santa Clara, CA) and the microscopic setup described earlier (Wetzker & Reinhardt, 2019). In brief, the average laser power on the sample was around 12 mW.…”

Section: Nad(p)h and Fad Autofluorescencementioning

confidence: 99%

Seminal fluid and sperm diluent affect sperm metabolism in an insect: Evidence from NAD(P)H and flavin adenine dinucleotide autofluorescence lifetime imaging

Massino

Wetzker

Balvín

et al. 2021

Microscopy Res & Technique

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Sperm metabolism is fundamental to sperm motility and male fertility. Its measurement is still in its infancy, and recommendations do not exist as to whether or how to standardize laboratory procedures. Here, using the sperm of an insect, the common bedbug, Cimex lectularius, we demonstrate that standardization of sperm metabolism is required with respect to the artificial sperm storage medium and a natural medium, the seminal fluid. We used fluorescence lifetime imaging microscopy (FLIM) in combination with time-correlated single-photon counting (TCSPC) to quantify sperm metabolism based on the fluorescent properties of autofluorescent coenzymes, NAD(P)H and flavin adenine dinucleotide. Autofluorescence lifetimes (decay times) differ for the free and protein-bound state of the co-enzymes, and their relative contributions to the lifetime signal serve to characterize the metabolic state of cells. We found that artificial storage medium and seminal fluid separately, and additively, affected sperm metabolism. In a medium containing sugars and amino acids (Grace's Insect medium), sperm showed increased glycolysis compared with a commonly used storage medium, phosphate-buffered saline (PBS). Adding seminal fluid to the sperm additionally increased oxidative phosphorylation, likely reflecting increased energy production of sperm during activation. Our study provides a protocol to measure sperm metabolism independently from motility, stresses that protocol standardizations for sperm measurements should be implemented and, for the first time, demonstrates that seminal fluid alters sperm metabolism. Equivalent protocol standardizations should be imposed on metabolic investigations of human sperm samples.

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“…Post-meiotic D. melanogaster sperm have been shown to undergo oxidative phosphorylation [14,26], generating mtROS in the process [14,27]. 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.…”

Section: Discussionmentioning

confidence: 99%

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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Distinct metabolic profiles in Drosophila sperm and somatic tissues revealed by two-photon NAD(P)H and FAD autofluorescence lifetime imaging

Cited by 19 publications

References 57 publications

Dietary polyunsaturated fatty acids affect volume and metabolism of Drosophila melanogaster sperm

Dietary polyunsaturated fatty acids affect volume and metabolism of Drosophila melanogaster sperm

Seminal fluid and sperm diluent affect sperm metabolism in an insect: Evidence from NAD(P)H and flavin adenine dinucleotide autofluorescence lifetime imaging

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

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