Selective Longevity

The duration of life (longevity), the onset of aging, and the rate of mortality significantly differ among animal and plant species. In eukaryotes, the life span varies from a few days' duration in yeast cells (in Saccharomyces, mean chronological life span is 6 to 30-40 days, depending on environment and nutrients) to a duration of 5000 years in the California bristlecone pine (Pinus longaeva). In vertebrates, aging and death, assumed to occur in all species, were originally attributed to species-specific genetic programs. However, the early view of a rigid, genetically preprogrammed life span is gradually being replaced by one of greater plasticity in response to environmental modifications (Chapters 1 and 5). It is now possible to envision that aging may be retarded by a combination of appropriate genetic and environmental modifications. Accordingly, the life spans of sexually reproducing species may be categorized according to rapid, gradual, or negligible rates of senescence (4,5) (Fig. 1).

Rapid senescence is usually observed in organisms that have a short period of optimal function in adult life. In addition to the ones listed in Figure 1, the Pacific salmon (Oncorhynkus) represents a prime example of an organism characteristic of this group. The salmon undergoes severe stress (with high blood cortisol levels, Chapter 9) at the time of spawning and dies shortly thereafter at about one year of age (6). However, if reproduction and the associated stress are blocked, the salmon will continue to live for some (six to seven) years (6). Other species fitting into this category, and listed in Figure 1, include yeast, some nematodes (Caenorhabditis), the housefly (Drosophila), and some longer-lived (10-100 years) species that

FIGURE 1 Comparison of maximum life span in different animal species. Species differ widely in longevity (total life span from zygote to oldest adult in years) and in the rate of senescence in adult (semiquantitative scale ranging from rapid to gradual to negligible senescence). Data on maximum life spans depend on husbandry conditions (temperature, nutrition). Rapid senescence: Yeast (Saccharomyces cerevisae) two to four days during asexual budding; nematode (Caenorhabditis elegans) 30 days; housefly (Drosophila melanogastei) 60 days; Pacific salmon (Onchorynchus) three to six years; male tarantula (Eurypelma californica) 10 years; vascular plants: thick-stemmed bamboo (Phyllostachys bambusoides, P. henonis) 120 years; Puya raimondii (related to the pineapple) 150 years. Gradual senescence. Mouse (Mus musculus) 4.2 years; human (Jeanne Calment) 122.4 years. Negligible senescence. Fish (Pacific perch), rockfish (Sebastes aleutianus) 140 years; orange roughy (Hoplostethus atlanticus) 140 years; warty oreo (Allocyttus verrucosus) >130 years; sturgeon (Acipenser fulvescens) 152 years; tortoise (Geochelone gigantea) 150 years; bivalve mollusc: ocean quahog (Artica islandica) 220 years; Great Basin bristlecone pine (Pinus longaeva) 4862 years. Ring dating often underestimates, and the true ages are probably greater than 5000 years. Inclusion of clonal, asexual, reproducing species, e.g., clones of the crosote bush, an asexually reproducing species, would extend the upper range of postzygotic life spans to >10,000 years. Source: Courtesy of Dr. C. E. Finch. From Refs. 4,5.

Lifespans of Sexually Reproducing Species: Rate of Senescence in Adult:

Rapid

2 Caenorhabditis 7 Man

3 Housefly

4 Tarantula

5 Bamboo

2 Caenorhabditis 7 Man

3 Housefly

4 Tarantula

5 Bamboo

8 Pacific percii

9 Tortoise

10 Quahog

11 Bristlecone pine die after a very short senescence period, such as the tarantula (Eurypelma californica) and some species of bamboo (such as in the genus Phillostachys).

Gradual senescence characterizes the majority of animals and plants with life spans ranging from one year to more than 100 years. Humans (and many animals used in the laboratory for the study of aging) fall into this category. In these animals, midlife is marked by a progressive decline in function and a progressive increase in the number of diseases affecting the same individual simultaneously (see comorbidity below).

Negligible senescence occurs in species that, at older ages, do not show evidence of physiologic dysfunctions, acceleration of mortality, or limit to the life span. Examples of species in this category include some fishes (e.g., rockfish, orange roughy), turtles (e.g., tortoises such as the Testudo sumerii that may live to 150 years), and some trees [e.g., bristlecone pine (7)]. Other life forms—particularly plants and invertebrates—in which aging may not occur at all have been considered immortal. Examples of selective immortality include some protozoa (e.g., Paramecium) and metazoa (e.g., sea anemones such as Cereas pedunculatus in which the individual "jellies" have a fixed life span, but the larval "stub" produces a constant supply of new blanks as old ones are removed, and the specimens remain vigorous indefinitely) (8). The absence of signs of aging may not be equated with immortality. Rather, these organisms may better fit the negligible senescence category in which they die from a cause that might kill them at any age.

The molecular pathways involved in the regulation of chronologic life span appear conserved in yeasts, worms, and flies and, possibly, in rodents and humans (9). Survival would depend on the activity of partially conserving glucose (in yeast) or insulin/insulin-like growth factor-1 (IGF-1) (in worms, flies)

or growth hormone (GH)/IGF-1 (in mice, and perhaps, also in humans) signals. This signaling downregulates antioxidant enzymes, heat shock proteins, and glycogen or fat accumulation while promoting growth, fecundity, and, eventually, mortality (Table 1). When mutations are introduced in the genes that regulate the life span, such as downregulation or inactivation of the receptors for the insulin/IGF-1 ligand or of AKT (protein kinase and transcription factor or kinase B), the life span is significantly prolonged in yeast (10), worms (11), flies (12), and mice (13) (Fig. 2). In some of these mutants, energy metabolism shifts from aerobic to anaerobic, free radical accumulation is reduced, and resistance to stress is increased (Table 2). Increased resistance to stress may be mediated in part by the activation of antioxidant enzymes and heat shock proteins that are synthesized in response to stress. An example of such proteins are the chaperone proteins that help other proteins to fold, thereby avoiding the production of inactive proteins or protein aggregates (14,15). However, the increased longevity is also associated with several unwanted side effects such as reduced growth, delayed maturation, and reduced fecundity. In humans, GH or IGF-1 deficiencies or excesses may cause several diseases (e.g., dwarfism, gigantism, and obesity). The effect of such diseases on the life span is usually negative (16,17). Further discussion of the use of mutants as animal models of aging is presented in Chapters 4 and 5.

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