Human skin long noncoding RNA WAKMAR1 regulates wound healing by enhancing keratinocyte migration

Proc Natl Acad Sci U S A. 2019 May 7;116(19):9443-9452. doi: 10.1073/pnas.1814097116. Epub 2019 Apr 24.

Abstract

An increasing number of studies reveal the importance of long noncoding RNAs (lncRNAs) in gene expression control underlying many physiological and pathological processes. However, their role in skin wound healing remains poorly understood. Our study focused on a skin-specific lncRNA, LOC105372576, whose expression was increased during physiological wound healing. In human nonhealing wounds, however, its level was significantly lower compared with normal wounds under reepithelialization. We characterized LOC105372576 as a nuclear-localized, RNAPII-transcribed, and polyadenylated lncRNA. In keratinocytes, its expression was induced by TGF-β signaling. Knockdown of LOC105372576 and activation of its endogenous transcription, respectively, reduced and increased the motility of keratinocytes and reepithelialization of human ex vivo skin wounds. Therefore, LOC105372576 was termed "wound and keratinocyte migration-associated lncRNA 1" (WAKMAR1). Further study revealed that WAKMAR1 regulated a network of protein-coding genes important for cell migration, most of which were under the control of transcription factor E2F1. Mechanistically, WAKMAR1 enhanced E2F1 expression by interfering with E2F1 promoter methylation through the sequestration of DNA methyltransferases. Collectively, we have identified a lncRNA important for keratinocyte migration, whose deficiency may be involved in the pathogenesis of chronic wounds.

Keywords: keratinocyte migration; long noncoding RNA; wound healing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Movement*
  • Chronic Disease
  • E2F1 Transcription Factor / metabolism
  • Gene Expression Regulation
  • Humans
  • Keratinocytes / metabolism*
  • Keratinocytes / pathology
  • RNA, Long Noncoding / biosynthesis*
  • Signal Transduction*
  • Skin / metabolism*
  • Skin / pathology
  • Transforming Growth Factor beta / metabolism
  • Wound Healing*
  • Wounds and Injuries / metabolism*
  • Wounds and Injuries / pathology

Substances

  • E2F1 Transcription Factor
  • E2F1 protein, human
  • RNA, Long Noncoding
  • Transforming Growth Factor beta