Prolactin-induced neuroprotection against glutamate excitotoxicity is mediated by the reduction of [Ca2+]i overload and NF-κB activation

PLoS One. 2017 May 5;12(5):e0176910. doi: 10.1371/journal.pone.0176910. eCollection 2017.

Abstract

Prolactin (PRL) is a peptidic hormone that displays pleiotropic functions in the organism including different actions in the brain. PRL exerts a neuroprotective effect against excitotoxicity produced by glutamate (Glu) or kainic acid in both in vitro and in vivo models. It is well known that Glu excitotoxicity causes cell death through apoptotic or necrotic pathways due to intracellular calcium ([Ca2+] i) overload. Therefore, the aim of the present study was to assess the molecular mechanisms by which PRL maintains cellular viability of primary cultures of rat hippocampal neurons exposed to Glu excitotoxicity. We determined cell viability by monitoring mitochondrial activity and using fluorescent markers for viable and dead cells. The intracellular calcium level was determined by a fluorometric assay and proteins involved in the apoptotic pathway were determined by immunoblot. Our results demonstrated that PRL afforded neuroprotection against Glu excitotoxicity, as evidenced by a decrease in propidium iodide staining and by the decrease of the LDH activity. In addition, the MTT assay shows that PRL maintains normal mitochondrial activity even in neurons exposed to Glu. Furthermore, the Glu-induced intracellular [Ca2+]i overload was attenuated by PRL. These data correlate with the reduction found in the level of active caspase-3 and the pro-apoptotic ratio (Bax/Bcl-2). Concomitantly, PRL elicited the nuclear translocation of the transcriptional factor NF-κB, which was detected by immunofluorescence and confocal microscopy. To our knowledge, this is the first report demonstrating that PRL prevents Glu excitotoxicity by a mechanism involving the restoration of the intracellular calcium homeostasis and mitochondrial activity, as well as an anti-apoptotic action possibly mediated by the activity of NF-κB. Overall, the current results suggest that PRL could be of potential therapeutic advantage in the treatment of neurodegenerative diseases.

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Caspase 3 / metabolism
  • Cells, Cultured
  • Female
  • Glutamic Acid / toxicity*
  • Hippocampus / cytology
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • NF-kappa B / metabolism*
  • Neuroprotection / drug effects*
  • Pregnancy
  • Prolactin / pharmacology*
  • Rats
  • Rats, Wistar

Substances

  • NF-kappa B
  • Glutamic Acid
  • Prolactin
  • Caspase 3
  • Calcium

Grants and funding

This worked was supported by PAPIIT-UNAM (IN220315, MC; IN205416, LM; IN201216, EFS), PAIP-UNAM (S000-9108, MC), CONACyT (CB239607, LM), Fundação para a Ciência e Tecnologia (LVL) and Nadia Alejandra Rivero Segura is a doctoral student from Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM) and received fellowship 290096 from CONACYT. This work was submitted in fulfillment of the requirements to obtain a PhD degree at the Programa de Doctorado en Ciencias Biomédicas in the Universidad Nacional Autónoma de México (UNAM). The authors give thanks to Ana Margarida Santos do Nascimento (AMSN) and António Temudo (AT) from the Bioimaging Unit of the Instituto de Medicina Molecular (iMM-Lisboa) and to Teresa Montiel (TM) from the Instituto de Fisiología Celular-División de Neurociencias (UNAM) for technical assistance.