Age-associated decline in mitochondrial respiration and electron transport in <i>Drosophila melanogaster</i>

Ferguson, Melissa; Mockett, Robin J.; Shen, Yi; Orr, William C.; Sohal, Rajindar S.

doi:10.1042/bj20042130

Cited by 185 publications

(214 citation statements)

References 53 publications

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“…This inference is consistent with a previous study, showing age-associated decline in mitochondrial respiration and electron transport in the flight muscle of Drosophila melanogaster (Ferguson et al 2005). The decline in mitochondrial energy utilization in the trophocytes and fat cells of workers most likely reflect the accumulation of oxidative damages.…”

Section: δψMsupporting

confidence: 93%

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Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera)

Chuang

Hsu

2012

AGE

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Trophocytes and fat cells in honeybees (Apis mellifera) have served as targets for cellular senescence studies, but mitochondrial energy utilization with advancing age in workers is unknown. In this study, mitochondrial energy utilization was evaluated in the trophocytes and fat cells of young and old workers reared in a field hive. The results showed that (1) mitochondrial density increased with advancing age; (2) mitochondrial membrane potential (ΔΨm), nicotinamide adenine dinucleotide oxidized form (NAD + ) concentration, adenosine triphosphate (ATP) concentration, and NAD + /nicotinamide adenine dinucleotide reduced form (NADH) ratio decreased with advancing age; and (3) the expression of NADH dehydrogenase 1 (ND1), ATP synthase, and voltage-dependent anion channel 1 (VDAC1) increased with advancing age, whereas ND1 and ATP synthase did not differ with advancing age after normalization to mitochondrial density and VDAC1. These results show that the trophocytes and fat cells of young workers have higher mitochondrial energy utilization efficiency than those of old workers and that aging results in a decline in mitochondrial energy utilization in the trophocytes and fat cells of worker honeybees.

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Section: δψMsupporting

confidence: 93%

“…Likewise, orchid bee foragers also have higher flight metabolic rate in flight muscles (Suarez et al 2005). This higher energy consumption increases oxidative damages (Ferguson et al 2005). …”

Section: δψMmentioning

confidence: 99%

Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera)

Chuang

Hsu

2012

AGE

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“…Insect mitochondria have been shown to be impermeable to many TCA cycle intermediates [62], which led to the use of proline to increase TCA cycle intermediates, also referred to as a 'sparker' metabolite in several studies conducted on insects and viewed mostly as an NAD-linked substrate [7,49,63,64]. Proline is indeed an important metabolite used to replenish TCA cycle intermediates and maintain the potential for pyruvate oxidation ( [7,[39][40][41]65], and possibly [24]).…”

Section: (B) Flight Muscle Metabolic Propertiesmentioning

confidence: 99%

Proline as a fuel for insect flight: enhancing carbohydrate oxidation in hymenopterans

et al. 2016

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Bees are thought to be strict users of carbohydrates as metabolic fuel for flight. Many insects, however, have the ability to oxidize the amino acid proline at a high rate, which is a unique feature of this group of animals. The presence of proline in the haemolymph of bees and in the nectar of plants led to the hypothesis that plants may produce proline as a metabolic reward for pollinators. We investigated flight muscle metabolism of hymenopteran species using high-resolution respirometry performed on permeabilized muscle fibres. The muscle fibres of the honeybee, Apis mellifera, do not have a detectable capacity to oxidize proline, as those from the migratory locust, Locusta migratoria, used here as an outgroup representative. The closely related bumblebee, Bombus impatiens, can oxidize proline alone and more than doubles its respiratory capacity when proline is combined with carbohydrate-derived substrates. A distant wasp species, Vespula vulgaris, exhibits the same metabolic phenotype as the bumblebee, suggesting that proline oxidation is common in hymenopterans. Using a combination of mitochondrial substrates and inhibitors, we further show that in B. impatiens, proline oxidation provides reducing equivalents and electrons directly to the electron transport system. Together, these findings demonstrate that some bee and wasp species can greatly enhance the oxidation of carbohydrates using proline as fuel for flight.

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“…An extensive literature has documented age-specific increases in damage to mitochondrial proteins, membranes, and mtDNA (Sohal and Weindruch 1996;Wallace 1997;Yan et al 1997), age-specific declines in the activity of mitochondrial enzyme complexes (Schwarze et al 1998;Ferguson et al 2005), and the accumulation of mutant mtDNAs within cells (heteroplasmy) (Cortopassi et al 1992;Wallace 1995;Wang et al 2001). But there is little direct experimental evidence that mtDNA mutations play a causal role in whole animal aging.…”

mentioning

confidence: 99%

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

2006

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Under the mitochondrial theory of aging, physiological decline with age results from the accumulated cellular damage produced by reactive oxygen species generated during electron transport in the mitochondrion. A large body of literature has documented age-specific declines in mitochondrial function that are consistent with this theory, but relatively few studies have been able to distinguish cause from consequence in the association between mitochondrial function and aging. Since mitochondrial function is jointly encoded by mitochondrial (mtDNA) and nuclear genes, the mitochondrial genetics of aging should be controlled by variation in (1) mtDNA, (2) nuclear genes, or (3) nuclear-mtDNA interactions. The goal of this study was to assess the relative contributions of these factors in causing variation in Drosophila longevity. We compared strains of flies carrying mtDNAs with varying levels of divergence: two strains from Zimbabwe (,20 bp substitutions between mtDNAs), strains from Crete and the United States (20-40 bp substitutions between mtDNAs), and introgression strains of Drosophila melanogaster carrying mtDNA from Drosophila simulans in a D. melanogaster Oregon-R chromosomal background (.500 silent and 80 amino acid substitutions between these mtDNAs). Longevity was studied in reciprocal cross genotypes between pairs of these strains to test for cytoplasmic (mtDNA) factors affecting aging. The intrapopulation crosses between Zimbabwe strains show no difference in longevity between mtDNAs; the interpopulation crosses between Crete and the United States show subtle but significant differences in longevity; and the interspecific introgression lines showed very significant differences between mtDNAs. However, the genotypes carrying the D. simulans mtDNA were not consistently short-lived, as might be predicted from the disruption of nuclear-mitochondrial coadaptation. Rather, the interspecific mtDNA strains showed a wide range of variation that flanked the longevities seen between intraspecific mtDNAs, resulting in very significant nuclear 3 mtDNA epistatic interaction effects. These results suggest that even ''defective'' mtDNA haplotypes could extend longevity in different nuclear allelic backgrounds, which could account for the variable effects attributable to mtDNA haplogroups in human aging.

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Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster

Cited by 185 publications

References 53 publications

Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera)

Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera)

Proline as a fuel for insect flight: enhancing carbohydrate oxidation in hymenopterans

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

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