A Demonstration of Reduced Life Span via Mitochondrial Mutations, but is it Relevant?

Mitochondria are bacteria-like organelles within cells responsible for, among other things, generating the adenosine triphosphate (ATP) molecules used as a chemical energy stores to power cellular activities. This process produces a varying flux of reactive oxygen species (ROS), molecules that can cause significant damage to molecular machinery when present in large numbers. Large and complex molecules participating in vital cellular processes are fragile things in the face of a horde of small reactive molecules trying to form bonds and bend their partners out of shape. Many aspects of cellular metabolism react to raised levels of ROS, especially those playing a part in housekeeping activities such the prompt removal of damaged proteins and repair of DNA. This dance is a regular part of life: it happens every time you exercise, for example, and is an important part of the way in which exercise produces health benefits. ROS flux in this case is a signal resulting in reactions at the cellular level that lead to improved tissue function at the higher level.

Mitochondria have their own DNA, a legacy of their evolutionary past as symbotic bacteria. It is stuck right next door to the intricate structures that generate both ATP and potentially harmful reactive molecules. Damage to mitochondrial DNA occurs on an ongoing basis, possibly due to the flux of ROS they themselves generate, and possibly during the many, many times mitochondria divide to make up their numbers in a cell. Some of this DNA damage is inconsequential and essentially random: it doesn't spread among mitochondria, and it doesn't appear to cause any great harm. There are mouse lineages artificially weighed down with point mutations in mitochondrial DNA, for example, that seem to suffer no ill effects as a result. However some forms of more drastic mutation, such as deletions, can remove one or more necessary genes from mitochondrial DNA, causing that mitochondrion to fall into a dysfunctional state that can spread. This particular type of dysfunction leads to preferential survival for the malfunctioning mitochondria and they quickly take over the cell, causing it to malfunction also. This is one of the causes of degenerative aging.

Mitochondria within a cell are far from being a static population of structures: mitochondria replicate by division like bacteria, and there are processes watching mitochondria for damage or dysfunction, culling the herd of faulty organelles. Mitochondria are also quite capable of swapping proteins and parts between themselves, or even fusing together. All of this complicates any attempt to watch the progress of damage to mitochondrial DNA in cells: it is evidently rapid, as researchers never find cells in mid-transition between some mitochondria exhibiting harmful DNA damage and all mitochondria in a cell exhibiting that damage.

The way to address this contribution to the aging process is through some form of repair. The Strategies for Engineered Negligible Senescence (SENS) approach is to work around the damage by placing copies of mitochondrial DNA in the cell nucleus. Mitochondrial DNA mutation is only a problem if mitochondria must rely on their DNA to produce needed protein machinery: if there is another source, then the damage is irrelevant. There are numerous other possible approaches, however: repair the DNA directly and periodically, introduce whole new mitochondria into tissues, and so forth. All too few researchers are working on this, however. While it is generally agreed that mitochondria are very important in the aging process, the mainstream position is to work on gathering more data rather than work to fix the damage - though to my eyes this is one of many areas in which it is probably more cost effective to enact a repair therapy and see what happens.

In this research the opposite approach is taken: create damage to mitochondrial DNA and watch the results in mice. This sort of thing is very rarely as educational as we would like it to be, however. It is too easy to break biology in ways that shorten life, and the breaking changes have no necessary connection to aging or ways to lengthen life even when they take place in related areas of molecular biology. Mitochondrial dysfunction of a variety of forms that don't occur in aging cause disease and shorter life spans, and so the details matter greatly, here as everywhere else. Not all mitochondrial DNA mutations are equal, and an experiment of this nature is one where it takes a real specialist in the field to comment on its relevance to aging:

Mom's Mitochondria Affect Pup Longevity

The new study shows that mitochondrial DNA mutations in the mother's eggs can shorten her pups' lives by approximately one third. The mice that inherited mutant mitochondrial DNA showed an average lifespan of 100 weeks compared with 141 weeks for control mice. What is not yet known is how mitochondrial DNA mutations shorten lifespan. Dysfunctional mitochondria could impair cellular metabolism and lead to a variety of problems, such as the accumulation of damaging reactive oxygen species, reduced vitality of stem cells, and reduced DNA repair, leading to the accumulation of damage to the genome in the nucleus. "Aging is a complex process and involves so many different facets, so maybe it's a little bit of everything that together keeps on beating down the organism a little at a time."

Maternally transmitted mitochondrial DNA mutations can reduce lifespan

The accumulation of mitochondrial DNA (mtDNA) mutations resulting in mitochondrial dysfunction has been heavily implicated in the aging process as well as various age-related disorders and diseases. Replication of the mitochondrial genome continues in mitotic and meiotic cells, as well as in non-dividing cells, with an ~10-fold higher mutation rate than nuclear DNA. Thus, mutations can occur in the maternal germline and be transmitted to offspring. Despite the presence of protective mechanisms that eliminate deleterious mtDNA mutations, evidence indicates inheritability of low levels of heteroplasmy in humans; however, the influence of such mutations on health and lifespan has been largely unclear.

To determine the extent to which inherited mtDNA mutations may contribute to the rate of aging, we designed a series of mouse mutants and previously demonstrated that germline mtDNA mutations can induce and augment aging phenotypes. We also unexpectedly found that a combination of inherited and somatic mtDNA mutations cause stochastic brain malformations. These results suggest that starting life with healthy mitochondria might be important for the maintenance of health during aging. This suggests that the rate of aging may be set early in life before reproduction ends. We now present evidence to demonstrate that the presence of low levels of germline-transmitted mtDNA mutations during development can have life-long consequences not only by causing premature aging phenotypes, but also by shortening lifespan.

Our previous and present findings allow us to conclude that inherited mtDNA mutations alone or in combination with somatic mtDNA mutations, augments the rate of aging and shortens lifespan. These results also provide additional evidence for the hypothesis that certain determinants of aging are present prior to conception and during development. It would be interesting to understand if the rate of aging, determined early during life, can be altered.

That all individuals start life with an initial damage load is supported by the reliability theory of aging, a model of system failure over time in which an organism is considered as a collection of redundant breakable components. This turns out to be a fairly robust and useful way of thinking about the aging of biological organisms at a high level. It has nothing to say about mechanisms, but it does help to steer thinking as to what the plausible mechanisms of aging might be.

Comments

One glaring difference between the above experiments and normal aging via mitochondrial damage (if that does turn out to be a cause of aging)... is that if the mitochondrial mutations are inherited then every cell in the body will start off with these mutations. In de Grey's and others theories of how such mutations cause aging only a small percentage of cells in the body acquire these mutations, but cause systemic damage through a non regular secretory phenotype of some sort.

Even so it would be interesting to take on of these mice and use gene therapy to express the damaged mitochondrial gene in the nucleus and see what happens to the mouse's lifespan (either germline or adult gene therapy).

Posted by: Jim at October 9th, 2014 7:20 PM

It isn't necessarily the case that any inherited mitochondrial mutations would necessarily be present in every cell in the body: unlike nuclear DNA, each cell contains multiple mitochondria and an even larger mtDNA copy number. So when a fertilized egg with an initially mixed population of healthy and mutant mtDNA divides, the mitochondria have to segregate, and this can lead to cells in which some contain the mutant DNA and others do not, or (more often) where healthy and mutant mtDNA is are present in varying ratios from one cell to the next — and the process then repeats itself with each cell division during embryonic and childhood development, and much more slowly during adult life. While some such mutations are so pathogenic (or are present in such high copy number) that they lead to death of the embryo, it is more common that an inherited mutation only affects those cells where the ratio of mutant genomes exceeds some pathogenic threshold (or only affects it in proportion to that ratio, with some floor or ceiling effects). Indeed, such cell-to-cell variation in mutation ratios and cellular function is common in inherited mitochondrial disease, and shifting the ratio is a hotly-pursued therapy for such diseases.

Happily, where the context is developing therapies to indefinitely postpone the disease and debility of aging, the origin of mitochondrial mutations doesn't matter so much: allotopic expression of the mitochondrially-encoded proteins and related strategies will rescue those cells that are completely overtaken by mitochondria with the kind of clonally-expanded deletion mutations that occur during aging by supplying missing mitochondrial electron transport chain proteins, and will rescue many cells with a pathologically-high burden of inherited mutations by increasing the ratio of healthy to mutant proteins. Additionally, these authors found that part of the age-related harm that these inherited mutations cause is the result of accelerating the rate of formation of deletions with age, which latter allotopic expression obviates.

Under real-world conditions, most such inherited mtDNA mutations evidently have relatively little impact on function during youth (since the people bearing them are functioning ... well, youthfully), so obviating the effects of age-related mutations while improving the function of cells with excessive levels of inherited mutations should actually leave the cell better off than those of young people today,who have the same inherited mutations but no allotopically-expressed "backup copies." And if the inherited mutations do contribute to age-related disease and debility through independent mechanisms (cell loss?) that are not rescued directly by shifting the mtDNA balance of cells toward more healthy genomes, then other rejuvenation biotechnologies can be brought in to remove, repair, replace, or render harmless the accumulating damage linking the mutations to aging phenotypes.

Posted by: Michael at October 10th, 2014 12:47 PM
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