Mechanisms underlying aberrant expression of miR-29c in uterine leiomyoma

Fertil Steril. 2016 Jan;105(1):236-45.e1. doi: 10.1016/j.fertnstert.2015.09.020. Epub 2015 Oct 9.

Abstract

Objective: To determine the expression of miR-29c and its target genes in leiomyoma and the role of NF-κB, specific protein 1 (SP1), and DNA methylation in its regulation.

Design: Experimental study.

Setting: Academic research laboratory.

Patient(s): Women undergoing hysterectomy for leiomyoma.

Intervention(s): Over- and underexpression of miR-29c; blockade of transcription factors.

Main outcome measure(s): MiR-29c and its target gene levels in leiomyoma and the effects of blockade of transcription factors on miR-29c expression.

Result(s): Leiomyoma as compared with myometrium expressed significantly lower levels of miR-29c, with an inverse relationship with expression of its targets, COL3A1 and DNMT3A. Gain of function of miR-29c inhibited the expression of COL3A1 and DNMT3A at protein and mRNA levels, secreted COL3A1, and rate of cell proliferation. Loss of function of miR-29c had the opposite effect. E2, P, and their combination inhibited miR-29c in leiomyoma smooth muscle cells (LSMC). Phosphorylated NF-κB (p65) and SP1 protein expression were significantly increased in leiomyoma. SiRNA knockdown of SP1 and DNMT3A or their specific inhibitors significantly increased the expression of miR-29c, accompanied by the inhibition of cellular and secreted COL3A1 in siRNA-treated cells. Knockdown of p65 also induced miR-29c expression but had no effect on COL3A1 expression.

Conclusion(s): MiR-29c expression is suppressed in leiomyoma, resulting in an increase in expression of its targets COL3A1 and DNMT3A. The suppression of miR-29c in LSMC is primarily mediated by SP1, NF-κB signaling, and epigenetic modification. Collectively, these results indicate a significant role for miR-29c in leiomyoma pathogenesis.

Keywords: COL3A1; DNMT3A; Leiomyoma; SP1; miR-29c.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Cell Proliferation
  • Collagen Type III / genetics
  • Collagen Type III / metabolism
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Methylation
  • DNA Methyltransferase 3A
  • Down-Regulation
  • Epigenesis, Genetic
  • Estradiol / pharmacology
  • Female
  • Gene Expression Regulation, Neoplastic* / drug effects
  • Humans
  • Leiomyoma / genetics*
  • Leiomyoma / metabolism
  • Leiomyoma / pathology
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Middle Aged
  • Phosphorylation
  • Progesterone / pharmacology
  • RNA Interference
  • Sp1 Transcription Factor / genetics
  • Sp1 Transcription Factor / metabolism
  • Transcription Factor RelA / metabolism
  • Transcription, Genetic
  • Transfection
  • Tumor Cells, Cultured
  • Uterine Neoplasms / genetics*
  • Uterine Neoplasms / metabolism
  • Uterine Neoplasms / pathology

Substances

  • COL3A1 protein, human
  • Collagen Type III
  • DNMT3A protein, human
  • MIRN29a microRNA, human
  • MicroRNAs
  • RELA protein, human
  • Sp1 Transcription Factor
  • SP1 protein, human
  • Transcription Factor RelA
  • Progesterone
  • Estradiol
  • DNA (Cytosine-5-)-Methyltransferases
  • DNA Methyltransferase 3A