UV-Protection Timer Controls Linkage between Stress and Pigmentation Skin Protection Systems

Mol Cell. 2018 Nov 1;72(3):444-456.e7. doi: 10.1016/j.molcel.2018.09.022. Epub 2018 Oct 25.

Abstract

Skin sun exposure induces two protection programs: stress responses and pigmentation, the former within minutes and the latter only hours afterward. Although serving the same physiological purpose, it is not known whether and how these programs are coordinated. Here, we report that UVB exposure every other day induces significantly more skin pigmentation than the higher frequency of daily exposure, without an associated increase in stress responses. Using mathematical modeling and empirical studies, we show that the melanocyte master regulator, MITF, serves to synchronize stress responses and pigmentation and, furthermore, functions as a UV-protection timer via damped oscillatory dynamics, thereby conferring a trade-off between the two programs. MITF oscillations are controlled by multiple negative regulatory loops, one at the transcriptional level involving HIF1α and another post-transcriptional loop involving microRNA-148a. These findings support trait linkage between the two skin protection programs, which, we speculate, arose during furless skin evolution to minimize skin damage.

Keywords: MITF dynamics; UVB radiation; skin pigmentation; skin proliferation; trait linkage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology
  • Male
  • Melanocytes / physiology
  • Melanocytes / radiation effects
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / physiology
  • Microphthalmia-Associated Transcription Factor / metabolism*
  • Microphthalmia-Associated Transcription Factor / radiation effects
  • Primary Cell Culture
  • Skin / metabolism*
  • Skin / radiation effects*
  • Skin Pigmentation / radiation effects
  • Ultraviolet Rays / adverse effects

Substances

  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • MIRN148 microRNA, human
  • MicroRNAs
  • Microphthalmia-Associated Transcription Factor