Evolution of human longevity uncoupled from caloric restriction mechanisms

PLoS One. 2014 Jan 6;9(1):e84117. doi: 10.1371/journal.pone.0084117. eCollection 2014.

Abstract

Caloric restriction (CR) and chemical agents, such as resveratrol and rapamycin that partially mimic the CR effect, can delay morbidity and mortality across a broad range of species. In humans, however, the effects of CR or other life-extending agents have not yet been investigated systematically. Human maximal lifespan is already substantially greater compared to that of closely related primate species. It is therefore possible that humans have acquired genetic mutations that mimic the CR effect. Here, we tested this notion by comparing transcriptome differences between humans and other primates, with the transcriptome changes observed in mice subjected to CR. We show that the human transcriptome state, relative to other primate transcriptomes, does not match that of the CR mice or mice treated with resveratrol, but resembles the transcriptome state of ad libitum fed mice. At the same time, the transcriptome changes induced by CR in mice are enriched among genes showing age-related changes in primates, concentrated in specific expression patterns, and can be linked with specific functional pathways, including insulin signalling, cancer, and the immune response. These findings indicate that the evolution of human longevity was likely independent of CR-induced lifespan extension mechanisms. Consequently, application of CR or CR-mimicking agents may yet offer a promising direction for the extension of healthy human lifespan.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aging / physiology
  • Animals
  • Brain / drug effects
  • Brain / metabolism
  • Caloric Restriction*
  • Cluster Analysis
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects
  • Humans
  • Longevity / physiology*
  • Macaca mulatta
  • Male
  • Mice
  • Pan troglodytes
  • Resveratrol
  • Signal Transduction
  • Sirolimus / metabolism
  • Stilbenes / pharmacology
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Stilbenes
  • TOR Serine-Threonine Kinases
  • Resveratrol
  • Sirolimus

Grants and funding

This work was supported by the Ministry of Science and Technology of the People's Republic of China (grant no. 2012DFG31940), National Natural Science Fund of China (grants no. 31171232 and 31050110128), the Max Planck-Society, and the Bundesministerum fuer Bildung und Forschung for financial support. PK was supported by 1000 Plan for Foreign Experts; MS was supported by fellowships from the Chinese Academy of Sciences (2009Y2BS12) and the European Molecular Biology Organization (EMBO ALTF 1475–2010). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.