Estrogen inhibits starvation-induced apoptosis in osteocytes by a redox-independent process involving association of JNK and glutathione S-transferase P1-1

FEBS Open Bio. 2017 Apr 5;7(5):705-718. doi: 10.1002/2211-5463.12216. eCollection 2017 May.

Abstract

Estrogen deficiency causes bone loss as a result of microdamage, oxidative stress, and osteocyte apoptosis. A relationship between oxidative stress-induced apoptosis, c-Jun N-terminal kinase (JNK) activation, and expression of factors involved in bone remodeling has been demonstrated in osteocytes. However, the molecular regulation of these events in osteocytes treated with 17β-estradiol (17β-E2) remains unexplored. The MLO-Y4 murine osteocyte-like cell line was used as a model to study starvation-induced apoptosis and ROS production during 17β-E2 treatment. Expression of glutathione S-transferase P1-1 (GSTP1-1), receptor activator kB ligand (RANKL), osteoprotegerin (OPG), sclerostin, and kinases activation were measured by western blot. In addition, the GSTP1-1/JNK association was assessed by immunoprecipitation, and GSTP1-1 involvement in the osteocyte response to 17β-E2 was detected by specific siRNA transfection. 17β-E2 prevents starvation-induced apoptosis (DNA fragmentation and caspase activation), the increase in sclerostin expression and the RANKL/OPG ratio, which are all related to JNK activation due to oxidative stress in osteocytes. This occurs through GSTP1-1 overexpression, which can inhibit JNK activation by formation of a GSTP1-1/JNK complex. No early antioxidant action of 17β-E2 has been found but the estrogen effect is similar to N-acetylcysteine which, by increasing the intracellular redox state, maintains JNK bound to GSTP1-1. Thus, the antiapoptotic and osteogenic effect of 17β-E2 in MLO-Y4 occurs by a redox-independent process involving GSTP1-1/JNK association. This study clarifies at molecular level the effect of 17β-E2 on osteocyte activity and identifies a possible role of GSTP1-1 and JNK activity in bone remodeling and repair mechanisms.

Keywords: GSTP1‐1 expression; JNK activity; RANKL/OPG ratio; estrogen; osteocyte apoptosis.