High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat

Nature. 2013 Jul 18;499(7458):346-9. doi: 10.1038/nature12234. Epub 2013 Jun 19.

Abstract

The naked mole rat (Heterocephalus glaber) displays exceptional longevity, with a maximum lifespan exceeding 30 years. This is the longest reported lifespan for a rodent species and is especially striking considering the small body mass of the naked mole rat. In comparison, a similarly sized house mouse has a maximum lifespan of 4 years. In addition to their longevity, naked mole rats show an unusual resistance to cancer. Multi-year observations of large naked mole-rat colonies did not detect a single incidence of cancer. Here we identify a mechanism responsible for the naked mole rat's cancer resistance. We found that naked mole-rat fibroblasts secrete extremely high-molecular-mass hyaluronan (HA), which is over five times larger than human or mouse HA. This high-molecular-mass HA accumulates abundantly in naked mole-rat tissues owing to the decreased activity of HA-degrading enzymes and a unique sequence of hyaluronan synthase 2 (HAS2). Furthermore, the naked mole-rat cells are more sensitive to HA signalling, as they have a higher affinity to HA compared with mouse or human cells. Perturbation of the signalling pathways sufficient for malignant transformation of mouse fibroblasts fails to transform naked mole-rat cells. However, once high-molecular-mass HA is removed by either knocking down HAS2 or overexpressing the HA-degrading enzyme, HYAL2, naked mole-rat cells become susceptible to malignant transformation and readily form tumours in mice. We speculate that naked mole rats have evolved a higher concentration of HA in the skin to provide skin elasticity needed for life in underground tunnels. This trait may have then been co-opted to provide cancer resistance and longevity to this species.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cell Proliferation
  • Cell Transformation, Neoplastic / metabolism*
  • Cells, Cultured
  • Contact Inhibition
  • Disease Resistance
  • Fibroblasts / metabolism
  • Glucuronosyltransferase / chemistry
  • Guinea Pigs
  • Humans
  • Hyaluronan Synthases
  • Hyaluronic Acid / metabolism*
  • Mice
  • Mole Rats
  • Molecular Sequence Data

Substances

  • Hyaluronic Acid
  • Glucuronosyltransferase
  • Hyaluronan Synthases