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Mitochondria Need Their Sleep: Redox, Bioenergetics, and ...

Mitochondria Need Their Sleep: Redox, Bioenergetics, and .

Mitochondria Need Their Sleep: Redox, Bioenergetics, and Temperature Regulation of Circadian Rhythms and the Role of Cysteine-Mediated Redox Signaling, Uncoupling Proteins, and Substrate Cycles

What are the main findings?

• Hypothesis: Redox, bioenergetic and temperature regulation is critical in maintaining cellular circadian rhythms; wakefulness is mainly “nucleorestorative” and sleep is mainly “mitorestorative”.
• Wakefulness: High metabolic rate induces oxidative stress and redox imbalance.
• Sleep: Fusion remodels mitochondria and the cellular redox balance is restored.
• Sleep: Mitochondria aid activation of rapid immune, inflammatory and heat shock responses.

What is the implication of the main findings?

• Sleep-wake cycling: Provides insights into the role of cysteine-mediated redox signaling, uncoupling and substrate cycles.
• Disorders of human development and aging: Perturbations of circadian tripartite-interactome signaling and mitochondrial-nuclear coregulation are Abstract
• Although circadian biorhythms of mitochondria and cells are highly conserved and crucial for the well-being of complex animals, there is a paucity of studies on the reciprocal interactions between oxidative stress, redox modifications, metabolism, thermoregulation, and other major oscillatory physiological processes. To address this limitation, we hypothesize that circadian/ultradian interaction of the redoxome, bioenergetics, and temperature signaling strongly determine the differential activities of the sleep–wake cycling of mammalians and birds. Posttranslational modifications of proteins by reversible cysteine oxoforms, S-glutathionylation and S-nitrosylation are shown to play a major role in regulating mitochondrial reactive oxygen species production, protein activity, respiration, and metabolomics. 
•  
• Nuclear DNA repair and cellular protein synthesis are maximized during the wake phase, whereas the redoxome is restored and mitochondrial remodeling is maximized during sleep. Hence, our analysis reveals that wakefulness is more protective and restorative to the nucleus (nucleorestorative), whereas sleep is more protective and restorative to mitochondria (mitorestorative). The “redox–bioenergetics–temperature and differential mitochondrial–nuclear regulatory hypothesis” adds to the understanding of mitochondrial respiratory uncoupling, substrate cycling control and hibernation. Similarly, this hypothesis explains how the oscillatory redox–bioenergetics–temperature–regulated sleep–wake states, when perturbed by mitochondrial interactome disturbances, influence the pathogenesis of aging, cancer, spaceflight health effects, sudden infant death syndrome, and diseases of the metabolism and nervous system.
•  

The differential activities of sleep–wake cycling are known to be necessary and important for the well-being of complex animals, such as mammals, birds, and reptiles. Although there are individual reports on the regulation of circadian rhythms by reactive oxygen/nitrogen/sulfur species (ROS/RNS/RSS), the redoxome, metabolomics, bioenergetics, and the thermal state during sleep–wake cycling (or resting–active phases), there is little published on their significant interaction; therefore, a clearer understanding of these reciprocity issues warrants attention, especially the changes wrought by aging and disease. Considering aging alone, the “free radical theory of aging” posits that species of animals with higher metabolic rates produce more oxidative stress, resulting in a shorter life span ; however, this relationship does not hold for all species. Another explanation of longevity is the earlier “rate of living hypothesis” that states that the lower the metabolic rate of a species, the longer its life expectancy. Mitochondria also have a major role in the aging process. They not only affect the metabolic rate but also the production and control of oxidative stress. Therefore, even aging alone is determined not by one but by several interactive physiologic effects.

Free-radical, metabolic, and mitochondrial processes are generally in dynamic equilibrium rather than in a steady state. Therefore, life expectancy hypotheses involving these processes are complicated by diurnal and seasonal variations. Endothermic mammals and birds with smaller mass generally have a longer maximum life span and higher mass-specific metabolic rate, but they also sleep longer. Mice sleep about four times longer than elephants, which sleep for only 3.5 h or less daily. Human resting energy expenditure is highest in the afternoon and evening and reduced by 10–30% at its lowest during sleep. Another circadian parameter, ROS levels, was measured in leukocytes of adults aged 21–25 years old and found to significantly peak at 18:00 and again at 3:00. There is no question that eukaryote cells have extensively evolved with the bioenergetic advantages of atmospheric oxygen and the cytotoxicity of ROS, especially mitochondrial ROS; so much so that ROS and redox-signaling molecules are essential facets of multicellular organisms. Therefore, the diurnal oscillatory nature of ROS is critical when considering redox-controlled biological mechanisms associated with the sleep–wake metabolic states of mammals and birds.

In general, metabolic rate scales with body size and temperature. The resting metabolic rate per gram of body weight of a mouse is about sevenfold greater than in humans. One estimate of the total energy expenditure of a sedentary man suggests that a 10th is accounted for by physical activity, a 10th is adaptive, facultative thermogenesis (due to the cold or dietary intake), and eight 10ths are due to the basal/resting metabolic rate. About two-thirds of the resting metabolic rate is dedicated to homeothermy, that is, to maintaining a stable core temperature. Therefore, homeothermy accounts for about 50% of the total energy expenditure in humans and a similar percentage in mice. Thermoregulation in mammals and birds keeps their internal temperature steady, within a few degrees Celsius. This internal temperature, generally higher than that of their surroundings, requires both physiologic and behavioral mechanisms to keep the temperature within a narrow range. It has been estimated from patients with fever that the metabolic rate increases by 13%/°C. The reason for this elevated and finely tuned body temperature in endothermic/homoeothermic species is unknown. The core and brain temperatures of humans (children and adults) drop during sleep by about 1 °C, lowest 3 h before wakening, and rise during the day to a peak in the evening. A crucial aspect of the redox–bioenergetics–temperature and differential mitochondrial–nuclear regulatory hypothesis we develop is that the lowering of core temperature during sleep increases oxidative stress in mitochondria, necessitating uncoupling proteins (UCPs) to lower ROS levels and raise heat production.

It is recognized that the circadian rhythms of physiological processes at all organizational levels in the body are controlled by central and peripheral “clocks,” with the “redox clock” being one of the latter. Four-fifths of protein-coding genes, in at least one of 64 tissues and brain regions from baboons, exhibited 24 h rhythms in gene expression. In mammals, the central circadian clock is the suprachiasmatic nucleus (SCN) of the hypothalamus that genetically oscillates and is primarily influenced by light. The mammalian target of rapamycin (mTOR) has a key role in the entrainment of the SCN. Downstream targets of mTOR complex 1 (mTORC1) promote the synthesis of both protein and glutathione. The SCN also entrains slave oscillators in extra-SCN brain regions and peripheral tissues. However, every cell in the body has its own reciprocal circadian rhythm–redox state timekeeping and even the SCN can be modulated by the redox state downstream of the free radical, nitric oxide (•NO).

Oxidative stress arises from redox imbalance or bias between antioxidants and pro-oxidants. Over 90% of mammalian oxygen consumption is by mitochondria, which are also the major cellular source of ROS, such as superoxide radicals O2•−, hydroxyl radicals •OH, hydrogen peroxide H2O2 and the peroxide functional group ROOR. RNS include •NO and the powerful oxidant peroxynitrite ONOO−. Oxygen is normally reduced via the mitochondrial electron transport chain (ETC) by four electrons to water when they arrive at cytochrome C oxidase, the terminal ETC complex, also known as complex IV (CIV). Alternatively, oxygen is terminally reduced by one, two, or three electrons, respectively, via mitochondrial redox carriers CI, CII, and CIII yielding ROS: O2•−, H2O2, or •OH, respectively. These mitochondrial ROS are generated by <2% of ETC electrons that leak from the ETC, mostly via CI, and interact with oxygen not consumed by mitochondrial respiration.

Enzymatic antioxidants are a principal means of counteracting this oxidative stress. These enzymes include catalase, glutathione peroxidase (GPX), peroxiredoxin (PRX), superoxide dismutase (SOD), and thioredoxin (TRX). Oxidative stress is also lessened by nonenzymatic antioxidants of glutathione (GSH, γ-glutamyl-cysteinyl-glycine), melatonin, uric acid, vitamins C, and vitamin E. Enzymatic antioxidants in humans usually peak during the light phase (e.g., catalase, GPX, PRX, and SOD), whereas most nonenzymatic antioxidants peak during the dark phase (melatonin, vitamins C and E, GSH, but not uric acid). The understanding of human circadian trends of enzymatic and nonenzymatic antioxidants is augmented by rodent and other animal studies, taking account of species differences and that animals such as rodents have a nocturnal wake state, in contrast to the diurnal activity of humans.

Two important redox processes that are protective to mitochondria (i.e., mitoprotective) are anion carriers and posttranslational modifications of protein thiols. The mitochondrial anion carrier protein family, located in the mitochondrial inner membrane, includes the subfamilies of the UCPs and adenine nucleotide translocase (ANT). The latter catalyzes the exchange of the adenosine diphosphate (ADP) anion for adenosine triphosphate (ATP). Anionic fatty acids, superoxide, and peroxidation products transfer across the mitochondrial inner membrane via UCPs and ANT activating the inducible proton leak. The mitochondrial coupling efficiency, calculated as the ATP generated by oxidative phosphorylation per molecule of oxygen consumed, is reduced by proton leakage, and some of the proton motive force (membrane potential and proton gradient) is converted to heat. Mitochondrial proton leaks and uncoupling of mitochondrial electron transport from phosphorylation are the principal means of counteracting oxidative stress by reducing the mitochondrial inner membrane potential that lessens the electron leakage along with ROS generation. Thiol-based and non-thiol protein posttranslational modifiers are involved in circadian regulation. Some of these modifications are reversible, including phosphorylation, glycosylation, ubiquitination, methylation, and acetylation. Our focus is on the reversible cysteine oxoforms—S-glutathionylation (-S-SG-) and S-nitrosation (also referred to as S-nitrosylation (-S-NO))—that provide proteins with redox respiratory protective measures to minimize oxidative and nitrosative stress.

On examination of the redoxome, bioenergetics, and thermal regulatory processes in humans, we hypothesize that the interactome, metabolic, and physiological circadian oscillations are strongly regulated by cellular cysteine-mediated posttranslational modifications of proteins, mitochondrial respiratory uncoupling, and temperature (Figure 1). The case is made that these spatiotemporal cycles of the redoxome, bioenergetics and temperature promote a wake phase that is more protective and restorative to the nucleus, which we term “nucleorestorative,” whereas sleep is more protective and restorative to mitochondria, hence “mitorestorative.” Following the introductory first section, the second section describes circadian posttranslational modifications and redox couples comprising electron donor and electron acceptor molecules. The third section focuses on the primary processes controlling mitochondrial bioenergetics, such as anion carriers (including UCPs), anion carrier mediators (such as thyroid hormones and melatonin), and the temporal separation of substrate or futile cycles. The fourth section describes how core temperature and other stressors affect mitochondrial heat shock response, oxidative stress, and temperature-dependent rhythms. The fifth section gives the implications of the redox–bioenergetics–temperature and differential mitochondrial–nuclear regulatory hypothesis in terms of uncoupling theories, childhood development, aging and related-diseases, hibernation in animals, and the effects of space radiation. In the sixth section, the implications of the hypothesis are given in view of sleep theories, followed by the concluding final section.

 

Oxidative stress arises from redox imbalance or bias between antioxidants and pro-oxidants. Over 90% of mammalian oxygen consumption is by mitochondria, which are also the major cellular source of ROS, such as superoxide radicals O2•−, hydroxyl radicals •OH, hydrogen peroxide H2O2 and the peroxide functional group ROOR [20,21]. RNS include •NO and the powerful oxidant peroxynitrite ONOO−. Oxygen is normally reduced via the mitochondrial electron transport chain (ETC) by four electrons to water when they arrive at cytochrome C oxidase, the terminal ETC complex, also known as complex IV (CIV). Alternatively, oxygen is terminally reduced by one, two, or three electrons, respectively, via mitochondrial redox carriers CI, CII, and CIII yielding ROS: O2•−, H2O2, or •OH, respectively. These mitochondrial ROS are generated by <2% of ETC electrons that leak from the ETC, mostly via CI, and interact with oxygen not consumed by mitochondrial respiration.

Enzymatic antioxidants are a principal means of counteracting this oxidative stress. These enzymes include catalase, glutathione peroxidase (GPX), peroxiredoxin (PRX), superoxide dismutase (SOD), and thioredoxin (TRX). Oxidative stress is also lessened by nonenzymatic antioxidants of glutathione (GSH, γ-glutamyl-cysteinyl-glycine), melatonin, uric acid, vitamins C, and vitamin E. Enzymatic antioxidants in humans usually peak during the light phase (e.g., catalase, GPX, PRX, and SOD), whereas most nonenzymatic antioxidants peak during the dark phase (melatonin, vitamins C and E, GSH, but not uric acid). The understanding of human circadian trends of enzymatic and nonenzymatic antioxidants is augmented by rodent and other animal studies, taking account of species differences and that animals such as rodents have a nocturnal wake state, in contrast to the diurnal activity of humans.

Two important redox processes that are protective to mitochondria (i.e., mitoprotective) are anion carriers and posttranslational modifications of protein thiols. The mitochondrial anion carrier protein family, located in the mitochondrial inner membrane, includes the subfamilies of the UCPs and adenine nucleotide translocase (ANT). The latter catalyzes the exchange of the adenosine diphosphate (ADP) anion for adenosine triphosphate (ATP). Anionic fatty acids, superoxide, and peroxidation products transfer across the mitochondrial inner membrane via UCPs and ANT activating the inducible proton leak. The mitochondrial coupling efficiency, calculated as the ATP generated by oxidative phosphorylation per molecule of oxygen consumed, is reduced by proton leakage, and some of the proton motive force (membrane potential and proton gradient) is converted to heat. Mitochondrial proton leaks and uncoupling of mitochondrial electron transport from phosphorylation are the principal means of counteracting oxidative stress by reducing the mitochondrial inner membrane potential that lessens the electron leakage along with ROS generation. Thiol-based and non-thiol protein posttranslational modifiers are involved in circadian regulation. Some of these modifications are reversible, including phosphorylation, glycosylation, ubiquitination, methylation, and acetylation. Our focus is on the reversible cysteine oxoforms—S-glutathionylation (-S-SG-) and S-nitrosation (also referred to as S-nitrosylation (-S-NO))—that provide proteins with redox respiratory protective measures to minimize oxidative and nitrosative stress.

On examination of the redoxome, bioenergetics, and thermal regulatory processes in humans, we hypothesize that the interactome, metabolic, and physiological circadian oscillations are strongly regulated by cellular cysteine-mediated posttranslational modifications of proteins, mitochondrial respiratory uncoupling, and temperature (Figure 1). The case is made that these spatiotemporal cycles of the redoxome, bioenergetics and temperature promote a wake phase that is more protective and restorative to the nucleus, which we term “nucleorestorative,” whereas sleep is more protective and restorative to mitochondria, hence “mitorestorative.” Following the introductory first section, the second section describes circadian posttranslational modifications and redox couples comprising electron donor and electron acceptor molecules. The third section focuses on the primary processes controlling mitochondrial bioenergetics, such as anion carriers (including UCPs), anion carrier mediators (such as thyroid hormones and melatonin), and the temporal separation of substrate or futile cycles. The fourth section describes how core temperature and other stressors affect mitochondrial heat shock response, oxidative stress, and temperature-dependent rhythms. The fifth section gives the implications of the redox–bioenergetics–temperature and differential mitochondrial–nuclear regulatory hypothesis in terms of uncoupling theories, childhood development, aging and related-diseases, hibernation in animals, and the effects of space radiation. In the sixth section, the implications of the hypothesis are given in view of sleep theories, followed by the concluding final section.

Figure 1

Interconnectedness of redoxome, bioenergetics and thermal regulation. The various cellular and mitochondrial (Mt) activities associated with the tripartite-interactome components, such as complexes I and II (CI/CII), fatty-acid oxidation (FAO), fatty-acid synthesis (FAS), and reactive oxygen/nitrogen/sulfur species (ROS/RNS/RSS), are also listed.

Richard B. Richardson and Ryan J. Mailloux     

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10045244/

Published online 2023 Mar 9   

 

James Eckburg

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