Dysfunctional Mitophagy in the Aging Brain

Every cell in the body contains hundreds of mitochondria, the evolved descendants of ancient symbiotic bacteria. Their primary purpose is to produce adenosine triphosphate (ATP), an energy store molecule used to power cellular operations. They are also involved in a great many other aspects of cell function, however. Mitochondria are dynamic organelles, capable of fusing together, passing component parts between one another, and replicating like bacteria. A cell regulates mitochondrial function in part through mitophagy, an autophagy process that breaks down and recycles mitochondria when they become worn and damaged.

Mitochondrial function is understandably vital to cell function. With age, however, mitochondria change and falter. Their dynamics alter, making it harder for mitophagy to function correctly, and components of the broader autophagic process themselves exhibit dysfunction. The result is an accumulation of broken, malfunctioning mitochondria. An alternative, less common path is the generation of mutations in mitochondrial DNA that both cause dysfunction and protect the broken mitochondria from mitophagy, allowing them to take over a cell via replication.

Cells containing dysfunctional mitochondria behave poorly. Organ function suffers as a consequence. This is one of the noteworthy contributing causes of degenerative aging, though it is likely that most mitochondrial dysfunction is downstream of underlying issues that cause alterations in the expression of proteins necessary to mitophagy or mitochondrial dynamics. The brain is an interesting mix of mitochondrial issues, as it is both energy-hungry, and thus sensitive to disruption of mitochondrial function, and contains a great many long-lived cells, in which the progressive age-related failure of mitophagy likely has a different balance of causes in comparison to to those of short-lived cells.

What can an individual do about the challenge of mitochondrial dysfunction in aging? Presently not a great deal. The only available approaches to improved mitophagy, such as NAD upregulation, tend to replicate a thin slice of the benefits produced by exercise. Calorie restriction slows the progression of all aspects of aging, mitochondrial function included, but only to a modest degree in humans. More promising classes of therapy that may be capable of producing meaningful degrees of rejuvenation, such as gene therapies to copy mitochondrial genes into the cell nucleus, or transplantation of functional mitochondria in large numbers, are being worked on, but clinical availability remains years in the future.

Impaired Mitophagy in Neurons and Glial Cells during Aging and Age-Related Disorders

Aging is accompanied by a decline in cognitive function in a significant part of the population and is a major risk factor for the development of most neurodegenerative diseases, including Alzheimer's disease (AD) and Parkinson's disease (PD). Mechanisms of brain aging remain poorly understood, and studies aimed at the development of targeted therapy for neurodegenerative diseases are an important task for modern medicine.

Over the past few decades, it has been shown that aging processes in the brain are closely associated with mitochondrial dysfunction, resulting in oxidative stress and bioenergetic deficiency in various cells of the nervous tissue, which are extremely sensitive to energy deprivation. Mitochondrial dysfunction is also a key pathological marker for neurodegenerative diseases. For example, it is a central player in sporadic and familial forms of PD, since dopaminergic neurons of the substantia nigra are especially vulnerable to energy deficiency due to their ability for autonomous activity, constant recirculation of synaptic vesicles, and developed axonal network. Therefore, maintaining adequate energy levels through a functional pool of mitochondria is critical for neuron survival and function.

The main mechanism that prevents the development of mitochondrial dysfunction is mitophagy. Mitophagy is a complex multicomponent process that ensures control of the quality and quantity of mitochondria by eliminating damaged forms of these organelles via autophagy. The importance of mitophagy for neurons may be explained by the significant role of the cytoplasmic renewal system for postmitotic cell populations. Maintaining the basal level of mitophagy is critical for ensuring the correct functioning of neurites since the bulk of mitochondria are localized in the distal parts of neuronal processes. Mitophagy restricts the production of reactive oxygen species, prevents the accumulation of mitochondrial DNA (mtDNA) mutations and the decrease in ATP production, and blocks apoptotic signaling and the activation of inflammasomes. It is the progressive decline in this type of selective macroautophagy throughout life that appears to lead to mitochondrial dysfunction and aging.

Many neurodegenerative diseases are characterized by the accumulation of neurotoxic protein aggregates resulting from mutations in the genes encoding for proteins that trigger mitophagy: PTEN-induced kinase 1 (PINK1), parkin, and protein deglycase DJ-1, among others. Therefore, determination of the relationships between mitophagy markers and various parameters of neurodegenerative processes in PD, AD, and other age-related disorders seems to be highly promising from both a clinical and fundamental point of view.

In conclusion, mitophagy pathways play an important role in maintaining physiological homeostasis, are involved in the mechanisms of aging and neurodegenerative disorders, and represent promising targets for the development of potential therapeutic agents aimed at regulating mitochondria quality control in neurons and glial cells. A significant number of molecules that induce or inhibit mitophagy are currently under consideration, which may be useful for testing hypotheses or developing drugs for the treatment of neurodegenerative diseases. The validation of promising drugs in animal and cell models, including neurons and glial cells derived from human iPSCs as well as the elucidation of mitophagy regulation mechanisms in human samples, requires reliable biomarkers.

Currently, specific biomarkers that reflect the activity of mitophagy include ubiquitin phosphorylated at serine 65, phosphorylated PINK1 and parkin, the expression and phosphorylation of several proteins of the outer mitochondrial membrane, in addition to general biomarkers of oxidative stress and neuroinflammation. At the same time, given the variety of the regulatory pathways of mitophagy, there is no doubt that this list will be expanded, eventually including indicators that reflect the state of mitophagy in certain types of cells of the nervous tissue.

Comments

'... though it is likely that most mitochondrial dysfunction is downstream of underlying issues that cause alterations in the expression of proteins necessary to mitophagy or mitochondrial dynamics.'

TL;DR:
It seems to be a 'feed-forward model of regulation whereby mitochondrial function controls mTORC1 assembly, which in turn regulates mitochondrial function.'
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'... genetic ablation of mTORC1 complexes results in a significantly reduced numbers of mitochondria [36]. Conversely, hyperactivation of mTORC1 induces replication of mitochondrial DNA, a precursor to mitochondrial biogenesis...'
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Source:
Unraveling the Multifaceted Nature of the Nuclear Function of mTOR
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7725927/
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'The ability for the cell to convert energetic precursors into chemical energy such as ATP, and energy stores such as fatty acids, glycogen or other storage macromolecules, is tightly regulated. To maintain this delicate balance, the cell must be able to transduce signals that indicate stress, the presence or deficiency of metabolic precursors, such as glucose and amino acids, as well as reactive molecules such as oxygen that are a limiting factor for energy production. In the interest of minimizing energy loss to unnecessary expression programs, the cell has evolved links between mitochondrial function and mTOR signaling [35]. Studies investigating the relationship between mTOR and the mitochondria have identified various connections linking the two at the level of the cytosol. For example, in animal models, genetic ablation of mTORC1 complexes results in a significantly reduced numbers of mitochondria [36]. Conversely, hyperactivation of mTORC1 induces replication of mitochondrial DNA, a precursor to mitochondrial biogenesis [37]. The mitochondrial protein FKBP38 (which belongs to the same immunophilin family as FKBP12) has been shown to interact with mTOR and Rheb (Ras homolog enriched in the brain) in a nutrient-dependent manner. In the presence of amino acids, active Rheb is able to bind and displace the inhibitory FKBP38 protein from binding mTORC1 allowing it to assume its active state.'
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'The mechanistic Target of Rapamycin (mTOR) is well-known for its ability to receive, integrate, and transduce signals that indicate conditions of nutrient and growth factor availability and stress to the rest of the cell [1]. As a highly conserved major hub for this intracellular communication, mTOR interacts with an array of components that are involved in upstream sensing or downstream signal transduction pathways (Figure 1). mTOR forms two distinct canonical complexes, mTORC1 and mTORC2, by differentially assembling subunits in a process that is not well understood. Each ultrastructure responds to both common and unique upstream stimuli, and mediate their respective downstream effects, while also regulating each other via cross-talk and feedback mechanisms [2].'
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As mentioned previously, mTORC1 assembly has been demonstrated to be sensitive to mitochondrial stress, specifically through its association with ATPase complexes [39]. When treated with the mitochondrial inhibitors of electron transport (inducing an energy deprived state), the triple atpase-RuvB-like protein 1 (TTT-RUVBL1/2) complexes that facilitate the assembly and stability of PIKK family kinases [42] were found in low abundance. This correlated with a decrease in observable mTORC1; a similar phenomenon occurred under conditions of glutamine and glucose deprivation [39]. Further experiments concluded the ATPase activity of the TTT-RUVBL1/2 complex was necessary for mTORC1 assembly. This is a fascinating finding that supports a feed-forward model of regulation whereby mitochondrial function controls mTORC1 assembly, which in turn regulates mitochondrial function.'

Posted by: Jones at October 26th, 2021 2:28 PM

Urolithin A !…..very promising agent to enhance mitophagy.

Posted by: Barry at October 27th, 2021 9:40 AM

How does cellular reprogramming (Yamanaka Factors) affect mitochondria? Could that be a strategy to rejuvenate them?

Posted by: Bill at October 31st, 2021 2:21 PM
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