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Hi All,

How long we will live?

Is it described by: 'the most likely sign to hang in any hypothetical ageing

headquarters at the moment would read: " It's the free radicals, stupid! " '?

Or maybe, is it modified from what the Clinton staff had as 'a simple, and now

infamous, sign to remind them to stay on message: " It's the economy, stupid! " ',

to:

" It's the [calorie] economy, stupid! " ?

From Jeanne Calment to yeast and back to Jeanne Calment seems like a long

distance.

Please see the below.

Nemoto S, Finkel T.

Ageing and the mystery at Arles.

Nature. 2004 May 13;429(6988):149-52. No abstract available.

PMID: 15141200

What determines how long we will live? Studies of simple organisms, single cells

and

mammals hint that certain shared principles underlie ageing, and raise the

possibility of devising ways to extend life — if we want to.

" I don't want to achieve immortality through my work. I want to achieve it

through

not dying " — Woody (1935–?)

In August 1997, Jeanne Calment was laid to rest in a simple ceremony in the

south of

France. Those who eulogized her life that day noted that it was unremarkable in

all

but one respect: she had been born on 21 February 1875. Five years before her

birth,

Napoleon III had been overthrown and the French Third Republic was formed. In

her

native Arles, Impressionism would take root and flourish. Years later, she would

often tell visitors of her recollection of the painter Van Gogh, whom

she

regarded as " dirty and badly dressed " . When pressed for the secret of her

longevity,

Madame Calment would stress her consumption of large quantities of olive oil and

port wine, and the fact that she quit smoking, albeit aged 119.

Insurance companies study life expectancy all the time (see Box 1), but science

long

neglected the issue. Although the events that initiate life and the processes

that

determine its end were avidly examined, there was curiously little study of what

determines the speed at which we travel between these two points. Ageing, unlike

other biological processes, was not felt to be a subject that is readily

dissected

into its components. Several laboratories have, however, spent the past decade

chipping away at this notion. Although their collective efforts have not yet

produced a completed work of art, they at least provide the first discernible

outline of the molecular path-ways that regulate lifespan.

Box 1. How long will you live?

The theoretical maximum lifespan in humans is still a subject of considerable

debate. For most of us, however, our life expectancy is determined not by

theoretical limits but by a confluence of factors we can't control (genetic) and

factors we struggle to control (behavioural and environmental). For a hint on

how

long you might live — or at least how long an insurance company thinks you might

live — simply fill out the questionnaire below. (From ref. 36.)

Begin with the number 76 and add or subtract as follows:

If you are age 30–50 (+2), if 51–70 (+4) _____

Male (-3), Female (+4) _____

Live in an urban area of population more than 2 million (-2), or a town under

10,000 (+2) _____

One grandparent lived to age 85 (+2), or all grandparents lived to 80 (+6)

_____

A parent died of cardiovascular disease or a stroke before age 50 (-4) _____

Brother, sister or parent under 50 has cancer or heart disease, or diabetes

since

childhood (-3) _____

Earn the equivalent of over US$50,000 (-2) _____

Finished college (+1), or have a graduate/professional degree (+2) _____

65 or over and still working (+3) _____

Live with a spouse or friend (+5) _____

Live alone (-3) and (-3) for every decade you lived alone since age 25 _____

Work behind a desk (-3), do work requiring strenuous physical labour (-3)

_____

Exercise strenuously for 30 minutes 5 times a week (+4), 2–3 times a week

(+2)____

Sleep more than ten hours a day (-4) _____

Personality is relaxed (+3) or intense (-3), happy (+1) or unhappy (-2) _____

Speeding ticket in the previous year (-1) _____

Drink the equivalent of 1 oz of liquor per day (-1) _____

Smoke more than 2 packs per day (-8), 1–2 packs/day (-6), or 1/2–1 pack/day

(-3)

_____

Overweight by 50 lbs or more (-8), 30–49 lbs (-4), 1–29 lbs (-2) _____

If over age 40, do you have a check-up or (if female) see a gynaecologist

annually? (+2) _____

>>>Calculated life expectancy ______

http://www.nature.com.qe2a-proxy.mun.ca/nature/journal/v429/n6988/box/429149a_bx\

1.html

Simple organisms

Yeast would seem an unlikely model system for learning about human ageing. A

single-celled organism, essential perhaps for our daily bread and our favourite

brew, it seems to lack the complexity that we associate with higher-order

functions

such as ageing. Nonetheless, yeast 'replicative lifespan' — a measure of the

number

of divisions a mother yeast cell can undergo — has become a useful surrogate for

mammalian ageing. Early in life, a mother yeast cell can readily divide,

asymmetrically, to produce a daughter cell. Later on, when the mother cell has

divided many times, it begins to enlarge and its capacity to produce progeny

diminishes. The fact that middle-aged yeast as well as middle-aged humans are

generally slower, fatter and less interested in reproduction provides our first

(albeit broad) clue that certain biological markers of ageing — and so, perhaps,

the

underlying mechanisms — might have been conserved during evolution.

So what determines how many times a mother yeast cell can divide? Numerous

environmental and genetic determinants have been identified. Among the

environmental

factors are several non-lethal stresses, for example reducing the glucose levels

in

the growth medium from 2% to 0.5%; such 'caloric restriction' can significantly

increase the replicative lifespan of yeast. This concept of 'less is more' when

it

comes to calories and longevity is a theme that we see again and again, from

yeast

to mice.

In yeast, low-glucose conditions extend lifespan through the action of a gene

termed

SIR2 (ref. 1). Strikingly, a similar lengthening of lifespan ensues when yeast

are

simply manipulated to produce too much of the protein product of this gene2.

This

product, Sir2, was first identified as a protein that modifies the physical

state of

DNA, causing a phenomenon known as genetic silencing ('Sir' stands for 'silent

information regulator'). Most evidence now supports the idea that Sir2 extends

lifespan in yeast by regulating gene expression or suppressing recombination

(the

exchange of chunks of DNA between chromosomes), although the relevant genetic

targets of Sir2 are unknown.

But what is the link between caloric restriction and Sir2? The protein's effects

on

DNA are achieved through its histone deacetylase activity — its ability to

remove

specific acetyl groups from histones and other proteins that wrap up DNA. This

activity of Sir2 in turn depends on the cellular levels of nicotinamide adenine

dinucleotide (NAD)2. NAD and its reduced form, NADH, represent a sort of basic

energy currency in cells. Caloric restriction in yeast might increase Sir2

activity

by altering either the NAD:NADH ratio or the levels of the NAD derivative

nicotinamide. In other simple organisms, such as the fruitfly Drosophila

melanogaster, caloric restriction might not only increase the activity of Sir2,

but

also directly regulate its levels3. Increased Sir2 levels and activity might

then

dampen gene expression and recombination, leading (somehow) to an extension in

lifespan.

Too much Sir2 also extends lifespan in the nematode worm Caenorhabditis

elegans2.

Like yeast, C. elegans has become a useful model in ageing research. Old and

young

worms look and act differently (Fig. 1), and the creature's lifespan is an

experimentally manageable 20–25 days. Moreover, the worm genome has been

completely

sequenced, it is reasonably straightforward to mutate its genes and study the

effects, and the expression of its genes can be easily manipulated using RNA

interference (RNAi) methods — a technique for knocking out the middle step in

the

'DNA to messenger RNA to protein' cascade that constitutes gene expression.

Figure 1 Life and death of a worm.

Over the past decade, studies of worms carrying mutations in one gene or another

have revealed many genes besides SIR2 that can, individually, regulate C.

elegans

lifespan (reviewed in ref. 4). We don't have space to describe them all here,

but

many seem to regulate metabolic parameters. Some of the longer-lived mutant

worms,

for instance, have difficulty eating and thus are caloric-restricted through

genetic

hardwiring. Another long-lived mutant, named clk-1, cannot synthesize coenzyme

Q, a

molecule that is involved in metabolism in mitochondria (the cell's major

energy-generating bodies).

Finally, an interesting cluster of mutations affects the well-characterized

insulin/insulin-like growth factor-1 (IGF-1) pathway. This signalling cascade is

involved in nutritional sensing and metabolic regulation in a wide spectrum of

organisms4. In long-lived animals with mutations in genes encoding components of

this pathway, the activity of the DAF-16 protein (a member of the so-called

Forkhead

family, which regulates gene expression) is modestly increased (see Fig. 2 for

why

this happens). Two research groups5, 6 have begun to track down the

transcriptional

targets of DAF-16. Although their different approaches uncovered non-overlapping

sets of targets, both groups identified genes that apparently regulate

metabolism

and the organism's response to 'oxidative stress' — caused by the imbalance

between

intracellular levels of reactive oxygen species (also termed free radicals or

oxidants), generated in part as a by-product of metabolism, and the cellular

antioxidant system. The mammalian counterparts of DAF-16 activate the

transcription

of similar stress-related genes7, 8.

Figure 2 The DAF-16 signalling pathway and lifespan. The lifespan of the worm is

regulated in part by a detailed biochemical pathway (simplified here) that

influences the activity of the gene-transcription factor DAF-16. The binding of

insulin-like molecules to their receptor (DAF-2) on the cell membrane activates

a

series of protein kinase enzymes: AAP-1–AGE-1 adds phosphate groups (P) to

phosphatidylinositol-4,5-bisphosphate (PIP2), which activates AKT-1–AKT-2. This

enzyme then phosphorylates DAF-16, keeping it in the cytoplasm. Some mutations

that

extend lifespan appear to modestly increase the nuclear localization and hence

activity of DAF-16 in adult worms. The targets of DAF-16 include genes involved

in

overall metabolism or adaptation to stress. A related pathway exists in

fruitflies.

The closest mammalian counterparts of the key proteins are shown in parentheses.

Studies of mutations in single genes are an effective but narrowly focused way

of

investigating the genetic basis of ageing. In the hope of defining the full

spectrum

of genes that regulate ageing, one group9 has turned to RNAi — a

higher-throughput

approach — to selectively inactivate more than 5,000 worm genes in turn. A

familiar

theme emerged: the most frequent category of gene product that appeared to

extend

lifespan when knocked out comprised regulators of mitochondrial function9. RNAi

that

was directed towards several different elements of mitochondrial electron

transport,

a crucial step in metabolism, also increased lifespan10 (although, curiously,

only

when mitochondrial function was inhibited in young worms).

From these studies, preliminary estimates suggest that, on average, inactivation

of

1 out of every 50 random genes results in a reproducible lifespan extension9. In

other words, these genes usually decrease lifespan. But why do worms — and

presumably other species — hang on to so many life-reducing genes? One answer

may be

that, as our genes are (or so it is presumed) selected for only on the basis of

their ability to promote reproduction and hence the continuance of the species,

life-shortening genes must provide certain reproductive advantages to a young

animal. In other words, as Darwin proposed, and as those of us with

teenage

children can readily verify, post-reproductive adults are of little to no

utility.

Single cells

Researchers have also been studying ageing by looking at mammalian cells in

culture

dishes. Like yeast, normal, non-reproductive mammalian cells generally lose

their

ability to proliferate after a fixed number of doublings — a phenomenon termed

the

Hayflick limit. With each ensuing division, a greater proportion of the cells

enter

a state called senescence, characterized by a permanent withdrawal from the

cell-division cycle.

So what determines the Hayflick limit? One explanation for human cells is that

every

population doubling results in a shortening of the ends of each chromosome —

protective caps called telomeres. Reduction of telomere length below a critical

threshold can trigger senescence. Notably, normal non-reproductive cells can be

'immortalized' — meaning that they multiply indefinitely — when engineered to

express telomerase, an enzyme that restores eroded telomeric DNA11. The immortal

nature of cancer cells, and of normal stem cells in embryos and adults, might

relate

to their continuous telomerase activity. Given these observations, some have

argued

that the forced expression of telomerase could potentially reverse or delay the

ravages of ageing. Sceptics have warned, however, that this strategy might lead

to

unacceptable levels of malignancies — a case of the ends, telomeric or

otherwise,

not justifying the means.

Other manipulations of cells in culture influence lifespan, too. For instance,

reduced levels of ambient oxygen delay senescence. The RAS gene, which regulates

yeast replicative lifespan, can also contribute to mammalian cell senescence.

Mutant

Ras proteins are closely linked to the transformation of immortalized cells into

tumour cells, but, paradoxically, the effect of Ras in a normal cell background

is

to block cell division irreversibly12. This has strengthened the concept that

senescence, like apoptosis (programmed cell death), is a protective mechanism.

Interestingly, in both yeast and mammalian cells, RAS induces the production of

a

high level of mitochondrial oxidants, and in human cells these oxidants are

required

to induce senescence13, 14.

Mammals

Although the progress made in simple organisms and single cells has been

remarkable,

much less is known about mammalian ageing. But numerous parallels are emerging.

For

instance, several genetically different strains of long-lived mice have been

described that are characterized by a deficiency in secreted hormones such as

growth

hormone and IGF-1 (ref. 15). These mice are at least vaguely reminiscent of

those

long-lived worms that show reduced IGF-1 signalling. Strikingly, mice in which

the

insulin receptor is inactivated only in adipose (fat) cells also show a 20%

increase

in their lifespan16, as do mice in which the IGF-1 receptor is only partially

inactivated17. The tissue-specific inactivation of the insulin receptor is

reminiscent of studies in worms in which increased DAF-16 activity in just a few

tissues increased the organism's lifespan18.

Another regulator of mammalian lifespan is the p66shc protein; deletion of this

signal-transduction intermediate in mice results in a roughly 30% increase in

lifespan19. Like many of the long-lived mutant worms, these mice can survive

oxidative stress better than their normal litter-mates. Moreover, cells from

these

animals have lower levels of oxidants7, 20. Notably, p66shc seems to regulate

the

activity of the mammalian Forkhead-family member that is a counterpart of C.

elegans

DAF-16 (ref. 7). Earlier this year, it was shown that mammalian Forkhead

proteins

also interact, physically and functionally, with NAD-dependent deacetylases from

the

Sir2 family21, 22. For all their evolutionary distance, mammals and nematodes

seem

to have kept the same bag of tricks.

Microarray analyses of the genes that are expressed in young and old tissues

provide

another means of trying to understand ageing in mammals. These analyses look at

the

messenger RNAs (mRNAs) that are expressed, and initial studies revealed that, in

this respect, young and old tissues are remarkably similar23, 24. Indeed,

comparative analysis of the brain and skeletal muscle from old and young mice

showed

that only some 1–2% of all mRNAs differ by more than twofold in their expression

levels. Those of us who wish to resist a mandatory retirement could argue that,

at

the cellular level, we are at roughly 98% of our youthful effectiveness.

Nonetheless, although only a handful of genes may differ, those genes are

clustered

into functional classes that regulate the response to oxidative stress,

inflammation

and overall metabolism. Strikingly, these age-related changes in gene expression

did

not occur when the animals' calorie intake was restricted23, 24.

Whether or not human ageing and longevity could be influenced by caloric

restriction

is unknown, and understandably there are few people willing to participate in

the

lifelong experiment that would be necessary to find out. But further insight

into

human ageing has come from the study of the rare accelerated-ageing syndromes

called

progerias. The most widely known of these inherited disorders is Werner's

syndrome,

which is characterized by the early appearance of grey and thinning hair,

osteoporosis, atherosclerosis and cancer25. The gene that is altered in Werner's

syndrome encodes a DNA helicase; other members of this enzyme family have been

implicated in inherited predispositions to cancer. Such enzymes seem to be

involved

in normal DNA replication, repair and recombination.

These accelerated-ageing syndromes re- mind us of an important distinction

between

our understanding of ageing in people and that in lower organisms. For the most

part, we die from specific diseases and events; the cause of death in lower

organisms is less well understood. Can our understanding of the pathways that

regulate ageing teach us anything about the mechanisms that underlie age-related

diseases? If, for instance, we had a magic potion that slowed human ageing,

would we

also decrease the incidence of diseases such as atherosclerosis and cancer,

which

rises so dramatically as we get older? For the case of malignancies, some

insight

may come from a study in yeast showing that daughters derived from older mother

yeast cells had a roughly 100-fold greater genetic instability than cells from

younger mothers26. If the same occurs in human cells, then cancer and ageing

mechanisms may be inextricably intertwined.

In another example, circulating endothelial progenitor cells — which repair

damaged

blood vessels — decline as a function of human age27. Similarly, in mice, the

ability of resident skeletal-muscle progenitor cells to proliferate and hence

repair

damage appears to decline markedly as a function of age28. These results hint

that

different tissues age at different rates, and that the exhaustion, depletion or

senescence of progenitor cells (including stem cells) might contribute to

overall

ageing as well as age-related diseases. In this context, atherosclerosis,

neurodegeneration and other specific disease states could be viewed as a form of

tissue-specific progeria.

A unified theory?

During the 1992 US presidential campaign between Bill Clinton and Bush

Sr,

out of a whole array of issues it was the economy that most exercised the

electorate. In their campaign room the Clinton staff had a simple, and now

infamous,

sign to remind them to stay on message: " It's the economy, stupid! " In our view,

the

most likely sign to hang in any hypothetical ageing headquarters at the moment

would

read: " It's the free radicals, stupid! "

Indeed, the cellular effects of free radicals represent the most likely

contender to

explain the ageing process across a wide range of species. In a nutshell, the

idea

is that when mitochondrial metabolism — fuelled by food and oxygen — increases,

more

reactive oxygen species are produced as a by-product, with greater adverse

effects

on cells.

Although such a theory was proposed close to 50 years ago29, its current

incarnation

has nuances (Fig. 3). For instance, there is a growing appreciation that the

production of reactive oxygen species in cells is intricately regulated, and

that

the effects of these species include both random damage to cellular components

and

the regulation of specific pathways30. Similarly, although metabolic rate and

the

production of reactive oxygen species are generally correlated, this

relationship

can be complex. For instance, a group of mitochondrial proteins known as

uncoupling

proteins is activated by superoxide, one type of reactive oxygen species, and

can

induce a metabolic state in which oxygen consumption increases but overall

levels of

reactive oxygen species decline31. Conversely, expression of an activated RAS

gene

in yeast leads to decreased oxygen consumption but increased levels of reactive

oxygen species13.

Figure 3 A current version of the free-radical theory of ageing. Nutrients

(detected

by sensors such as the insulin receptor at the cell membrane) and oxygen fuel

metabolism in the mitochondria, generating reactive oxygen species (ROS). The

levels

of ROS might determine the rate of ageing by inducing random damage in proteins

and

DNA, and by activating specific pathways that depend on the reduction–oxidation

status of particular proteins. DNA damage or recombination might be decreased by

proteins that influence lifespan, including the Werner helicase or members of

the

Sir2 family. Although ROS levels and oxygen consumption are related, the

relationship is complex; proteins such as uncoupling proteins and Ras may alter

the

levels of ROS produced or released per molecule of oxygen consumed. It also

remains

unclear how the cell partitions substrates to the inefficient but ROS-sparing

non-mitochondrial pathways, or the highly efficient but ROS-generating

mitochondrial

pathways.

Nonetheless, many of the known regulators of longevity can be mapped to a scheme

resembling Fig. 3. For instance, inhibiting mitochondrial function — as many of

the

genes uncovered in the C. elegans RNAi screens9, 10 seem to do — might cause the

organism to rely on alternative, non-mitochondrial pathways for energy

production.

These pathways are inherently less efficient, but produce fewer reactive oxygen

species, perhaps leading to the lifespan extension observed. Mutations that

activate

DAF-16, meanwhile, would induce the expression of genes that encode

antioxidants,

and might also shift the organism to a different overall metabolic state.

Caloric

restriction could lead to many changes, including Sir2 activation and a

consequent

reduction in gene expression and recombination, as well as reduced activation of

the

insulin/IGF-1 pathways. The net effect might be to lower oxidant production and

increase the removal of free radicals.

But although this theory is the best candidate to explain the wealth of

experimental

data, disquieting observations persist. Take two examples. First, if ageing

represents the legacy of the combustible mixture of food and oxygen in our

mitochondria, then oxidant-related damage should be, to some degree, cumulative.

But

when fruitflies were caloric-restricted for just two days, their mortality rate

became equivalent to that of flies that spent their whole life hungry32.

Second, at least in yeast, glucose withdrawal extends life but results in a

tripling

in the rate of oxygen consumption33. Oxygen consumption and the generation of

reactive oxygen species are not necessarily equivalent. Still, one would expect

such

a large change in oxygen consumption to be more likely to increase than decrease

the

levels of such species. So the free-radical theory remains a useful, but still

unproven, framework within which to understand how we age, and questions remain

as

to whether levels of oxygen radicals cause, or are merely correlated with,

ageing34.

Conclusions

The discovery of genes that are associated with the regulation of lifespan in

simple

organisms, the apparent clustering of these genes into a handful of discrete

categories and pathways, and the evolutionary conservation of such genes and

pathways have led to the hope that treatments can be developed to slow ageing

and

increase lifespan — if we want to. The idea has obvious social implications,

with

ageing populations already becoming a problem in many countries. Nonetheless, as

caloric restriction seems to be such a robust way to extend life, there is

considerable enthusiasm for the idea of molecules that mimic its effects. At

least

in yeast, such a strategy may hold water: last year, researchers identified

numerous

structurally related small molecules that increase Sir2 activity and so mimic

the

effects of caloric restriction on lifespan35. For those of us who enjoy life's

desserts, the fact that yeast exposed to these compounds lived longer despite

being

cultured in a food-rich environment provides some cause for optimism.

Other potentially promising compounds could include partial inhibitors of the

insulin/IGF-1 pathways, small molecules that block p66shc, or compounds that

modestly activate the Forkhead-family proteins. Will such approaches be

successful?

Can we produce drugs that preserve the quality of life and yet extend its

length?

Some would argue that the proof that such strategies will work is already

discernible from the menagerie of long-lived worms, fruitflies and mice in

existence. Others would say that for evidence of how much remains a mystery, one

need only visit a small graveyard in Arles and find a stone that bears the

simple

inscription: Jeanne Calment, born 1875, died 1997.

Al Pater, PhD; email: old542000@...

__________________________________

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