Failing Autophagy and Lipofuscin Accumulation in the Aging Brain

It is known that the cellular housekeeping process of autophagy declines with aging, and it is also known that the metabolic waste known as lipofuscin builds up in long-lived cells at the same time. In the SENS view of aging, this lipofuscin accumulation is one of the causes of failing autophagy, as it accumulates in the recycling structures called lysosomes, degrading their function. Definitively proving this direction of causation, versus it being the other way around, is ever a challenge, however. The most effective way to do that is to clear out lipofuscin in old tissues and then observe the results, but at present this can only be achieved for a few of the many constituent compounds that make up this form of waste.

Autophagy is a self-degradative, highly regulated process that involves the non-specific degradation of cytoplasmic macromolecules and organelles via the lysosomal system. There are three different autophagic pathways based on the mechanisms for delivery of cargo to lysosomes: macroautophagy, microautophagy and chaperone-mediated autophagy (CMA). Macroautophagy (herein referred to as autophagy) is the major lysosomal pathway for the turnover of cytoplasmic components. Emerging evidence indicates that autophagy protects cells by removing long-lived proteins, aggregated protein complexes, and excess or damaged organelles. Defects in autophagy, therefore, are associated to various pathological conditions within organisms, including tumorigenesis, defects in developmental programs and the build-up of toxic, protein aggregates involved in neurodegeneration such as Amyloid precursor protein (APP). It has been recently suggested that the progressive age-related decline of autophagic and lysosomal activity may also be responsible for the continuous intraneuronal accumulation of lipofuscin, or "age pigment".

For this study, we aimed to investigate the expression of autophagic markers and the accumulation of pathologic proteins such as APP and lipofuscin in aged bovine brains. Microscopic findings in the brains of our aged bovines are similar to those previously described in old animals of other species as well as in cattle. In this study, the age-dependent intraneuronal accumulation of lipofuscin is one of the most striking features of aged brains. This finding is not actually new, as it has been described for more than 150 years. In the past, lipofuscin was generally thought to be an innocent end product of oxidation which has no significant influence on cellular activities, but in the last decade several authors have investigated about the possible detrimental and pathogenic potential of this material.

The so-called "mitochondrial-lysosomal axis theory of aging" tries to explain the possible relationship between lipofuscin accumulation, decreased autophagy, increased Reactive Oxygen Species (ROS) production, and mitochondrial damage in senescent long-lived postmitotic cells. According to this theory, in senescent cells lysosomal enzymes are directed towards the plentiful lipofuscin-rich lysosomes and, subsequently, they are lost for effective autophagic degradation because lipofuscin remains non-degradable. The consequences are a progressive impairment of autophagy and the gradual accumulation of damaged mitochondria, other organelles and misfolded proteins that lead to neurodegeneration. Unfortunately, our results cannot support a direct association between lipofuscin accumulation and autophagy impairment in aged bovine brains. According to recent scientific literature, we can only hypothesize that progressive and severe lipofuscin accumulation may irreversibly lead to functional decline and death of neurons by diminishing lysosomal degradative capacity and by preventing lysosomal enzymes from targeting to functional autophagosomes.

Further studies are indeed necessary to better understand how lipofuscin accumulation can influence the neuronal autophagic and apoptotic pathways in bovine brains. It would be interesting to perform double-staining techniques in order to show whether lipofuscin is directly related to autophagic and apoptosis markers and/or to pathologic protein deposition. Unfortunately, to our knowledge, a specific antibody for lipofuscin is not available since this complex substance is mainly composed of cross-linked protein and lipid residues. Alternatively, combined histochemical and immunohistochemical staining protocols can be performed to simultaneously localize lipofuscin and the antigen of interest. However, since lipofuscin progressively accumulates throughout the life of neurons, this combined immunohistochemical/histochemical protocol is not perfectly indicated to investigate the mechanism and relative timing of intraneuronal lipofuscin accumulation and the deposition of other proteins. Primary cultured neuronal cells exhibit, in vitro, a variety of features that are frequently observed in physiologically aged neurons in vivo, including lipofuscin accumulation. Thus, long-term aging culture of primary cultured neurons would be a remarkable model to unravel, at least in part, the molecular mechanisms behind lipofuscin accumulation and its pathological effects on neuronal cells.

Link: https://dx.doi.org/10.1186/s12917-017-1028-1

Comments

Why aren't more groups working on lipofuscin removal? Is it a problem similar to glucosepane where there are no decent validated probes (antibodies) to the various components of lipofuscin, and hence you can't even tell if your treatment is actually removing it?

"Unfortunately, to our knowledge, a specific antibody for lipofuscin is not available since this complex substance is mainly composed of cross-linked protein and lipid residues."

Is it even possible to create good probes for lipofuscin?

Posted by: Jim at April 18th, 2017 10:35 AM

> Why aren't more groups working on lipofuscin removal?

There's one over here, but it's only a small project:

https://fit.uni-tuebingen.de/Project/Details?id=4435

> Is it even possible to create good probes for lipofuscin?

Lipofuscin in the eye or skin is fluorescent and can be seen with an ultra-violet lamp.
Your ophtalmologist probably checked that already, so ask him.

Posted by: Matthias F at April 18th, 2017 10:48 AM

Note that the stuff in your eye that is commonly called "lipofuscin" is actually A2E, not the "lipofuscin" found in the brain and heart. The predominant fluorescent material in the skin isn't lipofuscin either (and despite the persistent prolongevist urban myth, liver spots are NOT lipofuscin!): it's not even intracellular, but is some kind of glycoxidative modification to skin collagen. (I doubt that it's very persistent: it corresponds to medium-term glycemic exposure, like HbA1C, and you can boost levels via short-term feeding of a high-glycotoxin meal and lower it in diabetics with better glycemic control).

Posted by: Michael at April 18th, 2017 1:53 PM

Thanks Michael for straightening that one out. I actually have a list of who's working on what in cleaning out the lysosome, but don't have any idea how reliable that is. Maybe you would like to comment on that one, too. Some components:

7-keto-cholesterol: SENS had a project there that went to Human Rejuvenation Technologies in 2013 and seems to work under the hood since then. Status unclear.

A2E: Ichor Therapeutics is a SENS spin-off that works towards clinical trials. Katairo GmbH is a spin-off from Tübingen University that lacks financing but has received orphan medicinal product designation.

Misfolded proteins beta and tau: Let the brain cells die (WTF) and remove the garbage with antibodies. Biogen is doing clinical trials on that.

Posted by: Matthias F at April 18th, 2017 6:18 PM

@Jim: I don't think anyone has a robust strategy for lipofuscin removal yet. One part of Jason Gaspar's SENS Research Foundation-funded work at Rice University has been on a way to slow its accumulation, which suggests something about the way it's formed, and might point the way toward a removal strategy, but much more direct evidence on the mechanism would be needed, along with evidence of a net reduction over time.

One question is whether lipofuscin only builds up after the lysosome fails for other reasons, such that clearing out the intralysosomal gak might in turn allow lipofuscin or its precursors (mitochondria, primarily) to be degraded again. This might open up a similar "bank shot" to the one being investigated by Julie Andersen as part of the Buck Institute's collaboration with SENS Research Foundation.

@Matthias: You've really misunderstood the plan on Abeta and tau! The whole idea is to remove Abeta and tau aggregates before frank neuronal loss sets in, likely delaying the onset and rate of neuronal loss. I'm not sure where you're getting the reverse idea: none of the sundry Abeta or tau (or alpha-synuclein) immunotherapies' postulated mechanisms of action involve that. Some of them remove different species of extracellular Abeta and tau aggregates; in the case of Abeta, there's evidence that some of them also cross the (living!) cell membrane and drag intraneuronal Abeta into the lysosome for degradation. This could also conceivably occur with some vaccines against tau aggregates, although no one has shown that in any particular case yet and it's been shown not to happen in mice in a couple of specific cases.

Ccertainly NFT in particular are left over extracellularly after their host neurons die, and thus might be captured by antibodies that target extracellular tau aggregates, but no one is just going after these "ghost tangles."

In addition, it's possible that in going after extracellular tau and alpha-synuclein aggregates, it might prevent or help reverse their intracellular accumulation, if there is some kind of "osmotic effect."

Absent a more direct strategy, then, one or more of the several immunotherapies in clinical trials or preclinical development, or work on other intralysosomal aggregates, might lead to clearance intraneuronal tau and alpha-synuclein aggregates.

Posted by: Michael at April 19th, 2017 2:27 PM

> You've really misunderstood the plan on Abeta and tau!

Actually I was too sloppy in my formulation, because it was 1:18 AM after I accidentally pressed BS in the preview and Explorer ate my first post. I wrote it down and completely missed that it sounds more like a plan than a description of the nasty state of the art.

What's more I even skipped a presentation by John Furber from Legendary Pharmaceuticals given at the SENS6 conference. He successfully testet clearing out the lysosome completely through exocytosis on neurons in vitro. Had some autofluorescent pictures of them, too.

> In addition, it's possible that in going after extracellular tau and alpha-synuclein aggregates, it might prevent or help reverse their intracellular accumulation, if there is some kind of "osmotic effect."

So does that "crossing the cell membrane" go both ways or is the cell actively dragging that stuff into the lysosome?

Posted by: Matthias F at April 19th, 2017 5:18 PM

Hi Matthias,

You asked,

> So does that "crossing the cell membrane" go both ways or is the
> cell actively dragging that stuff into the lysosome?

Sorry: what "crossing the cell membrane"? Are you asking about antibodies crossing the cell membrane carrying beta-amyloid, or tau and alpha-synuclein aggregates being transferred from cell to cell at the synapse?

Posted by: Michael at April 29th, 2017 1:37 PM
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