AGO CLIP Reveals an Activated Network for Acute Regulation of Brain Glutamate Homeostasis in Ischemic Stroke

Cell Rep. 2019 Jul 23;28(4):979-991.e6. doi: 10.1016/j.celrep.2019.06.075.

Abstract

Post-transcriptional regulation by microRNAs (miRNAs) is essential for complex molecular responses to physiological insult and disease. Although many disease-associated miRNAs are known, their global targets and culminating network effects on pathophysiology remain poorly understood. We applied Argonaute (AGO) crosslinking immunoprecipitation (CLIP) to systematically elucidate altered miRNA-target interactions in brain following ischemia and reperfusion (I/R) injury. Among 1,190 interactions identified, the most prominent was the cumulative loss of target regulation by miR-29 family members. Integration of translational and time-course RNA profiles revealed a dynamic mode of miR-29 target de-regulation, led by acute translational activation and a later increase in RNA levels, allowing rapid proteomic changes to take effect. These functional regulatory events rely on canonical and non-canonical miR-29 binding and engage glutamate reuptake signals, such as glial glutamate transporter (GLT-1), to control local glutamate levels. These results uncover a miRNA target network that acts acutely to maintain brain homeostasis after ischemic stroke.

Keywords: AGO CLIP; GLT-1; brain homeostasis; glia; glutamate; ischemia and reperfusion injury; miR-29; miRNA targets; post-transcriptional regulation; stroke.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Argonaute Proteins / metabolism*
  • Base Sequence
  • Brain / metabolism*
  • Brain Ischemia / complications
  • Brain Ischemia / genetics
  • Brain Ischemia / metabolism*
  • Cross-Linking Reagents / chemistry*
  • Down-Regulation / genetics
  • Gene Regulatory Networks
  • Glucose / deficiency
  • Glutamic Acid / metabolism*
  • Homeostasis*
  • Humans
  • Immunoprecipitation
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Models, Biological
  • Neuroglia / metabolism
  • Oxygen
  • Polymorphism, Genetic
  • Signal Transduction
  • Stroke / complications
  • Stroke / genetics
  • Stroke / metabolism*
  • Time Factors

Substances

  • Argonaute Proteins
  • Cross-Linking Reagents
  • MIRN29a microRNA, human
  • MicroRNAs
  • Glutamic Acid
  • Glucose
  • Oxygen