Aldo-keto reductase 1C3 expression in MCF-7 cells reveals roles in steroid hormone and prostaglandin metabolism that may explain its over-expression in breast cancer

J Steroid Biochem Mol Biol. 2010 Feb 15;118(3):177-87. doi: 10.1016/j.jsbmb.2009.12.009. Epub 2009 Dec 28.

Abstract

Aldo-keto reductase (AKR) 1C3 (type 5 17beta-hydroxysteroid dehydrogenase and prostaglandin F synthase), may stimulate proliferation via steroid hormone and prostaglandin (PG) metabolism in the breast. Purified recombinant AKR1C3 reduces PGD(2) to 9alpha,11beta-PGF(2), Delta(4)-androstenedione to testosterone, progesterone to 20alpha-hydroxyprogesterone, and to a lesser extent, estrone to 17beta-estradiol. We established MCF-7 cells that stably express AKR1C3 (MCF-7-AKR1C3 cells) to model its over-expression in breast cancer. AKR1C3 expression increased steroid conversion by MCF-7 cells, leading to a pro-estrogenic state. Unexpectedly, estrone was reduced fastest by MCF-7-AKR1C3 cells when compared to other substrates at 0.1muM. MCF-7-AKR1C3 cells proliferated three times faster than parental cells in response to estrone and 17beta-estradiol. AKR1C3 therefore represents a potential target for attenuating estrogen receptor alpha induced proliferation. MCF-7-AKR1C3 cells also reduced PGD(2), limiting its dehydration to form PGJ(2) products. The AKR1C3 product was confirmed as 9alpha,11beta-PGF(2) and quantified with a stereospecific stable isotope dilution liquid chromatography-mass spectrometry method. This method will allow the examination of the role of AKR1C3 in endogenous prostaglandin formation in response to inflammatory stimuli. Expression of AKR1C3 reduced the anti-proliferative effects of PGD(2) on MCF-7 cells, suggesting that AKR1C3 limits peroxisome proliferator activated receptor gamma (PPARgamma) signaling by reducing formation of 15-deoxy-Delta(12,14)-PGJ(2) (15dPGJ(2)).

Keywords: 17β-Hydroxysteroid dehydrogenase; estrogen receptor; peroxisome proliferator activated receptor γ; prostaglandin D2; prostaglandin F synthase.

MeSH terms

  • 20-alpha-Dihydroprogesterone / metabolism
  • 3-Hydroxysteroid Dehydrogenases / genetics
  • 3-Hydroxysteroid Dehydrogenases / metabolism*
  • 5-alpha-Dihydroprogesterone / metabolism
  • Aldo-Keto Reductase Family 1 Member C3
  • Androstenedione / metabolism
  • Androsterone / metabolism
  • Biocatalysis
  • Breast Neoplasms / enzymology
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Dihydrotestosterone / metabolism
  • Dinoprost / metabolism
  • Dinoprost / pharmacology
  • Estradiol / metabolism
  • Estradiol / pharmacology
  • Estrone / metabolism
  • Estrone / pharmacology
  • Etiocholanolone / analogs & derivatives
  • Etiocholanolone / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Gonadal Steroid Hormones / metabolism*
  • Gonadal Steroid Hormones / pharmacology
  • Humans
  • Hydroxyprostaglandin Dehydrogenases / genetics
  • Hydroxyprostaglandin Dehydrogenases / metabolism*
  • Ketosteroids / metabolism
  • Kinetics
  • Progesterone / analogs & derivatives
  • Progesterone / metabolism
  • Prostaglandin D2 / analogs & derivatives
  • Prostaglandin D2 / metabolism
  • Prostaglandin D2 / pharmacology
  • Prostaglandins / metabolism*
  • Prostaglandins / pharmacology
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Testosterone / metabolism
  • Transfection
  • Up-Regulation*

Substances

  • 15-deoxyprostaglandin J2
  • Gonadal Steroid Hormones
  • Ketosteroids
  • Prostaglandins
  • Recombinant Proteins
  • Dihydrotestosterone
  • 20-alpha-Dihydroprogesterone
  • Estrone
  • Testosterone
  • Androstenedione
  • Progesterone
  • Estradiol
  • androstane-3,17-dione
  • Etiocholanolone
  • 5-alpha-Dihydroprogesterone
  • Dinoprost
  • Androsterone
  • 3-Hydroxysteroid Dehydrogenases
  • Hydroxyprostaglandin Dehydrogenases
  • AKR1C3 protein, human
  • Aldo-Keto Reductase Family 1 Member C3
  • Prostaglandin D2