Deficiency in MT5-MMP Supports Branching of Human iPSCs-Derived Neurons and Reduces Expression of GLAST/S100 in iPSCs-Derived Astrocytes

Cells. 2021 Jul 6;10(7):1705. doi: 10.3390/cells10071705.

Abstract

For some time, it has been accepted that the β-site APP cleaving enzyme 1 (BACE1) and the γ-secretase are two main players in the amyloidogenic processing of the β-amyloid precursor protein (APP). Recently, the membrane-type 5 matrix metalloproteinase (MT5-MMP/MMP-24), mainly expressed in the nervous system, has been highlighted as a new key player in APP-processing, able to stimulate amyloidogenesis and also to generate a neurotoxic APP derivative. In addition, the loss of MT5-MMP has been demonstrated to abrogate pathological hallmarks in a mouse model of Alzheimer's disease (AD), thus shedding light on MT5-MMP as an attractive new therapeutic target. However, a more comprehensive analysis of the role of MT5-MMP is necessary to evaluate how its targeting affects neurons and glia in pathological and physiological situations. In this study, leveraging on CRISPR-Cas9 genome editing strategy, we established cultures of human-induced pluripotent stem cells (hiPSC)-derived neurons and astrocytes to investigate the impact of MT5-MMP deficiency on their phenotypes. We found that MT5-MMP-deficient neurons exhibited an increased number of primary and secondary neurites, as compared to isogenic hiPSC-derived neurons. Moreover, MT5-MMP-deficient astrocytes displayed higher surface area and volume compared to control astrocytes. The MT5-MMP-deficient astrocytes also exhibited decreased GLAST and S100β expression. These findings provide novel insights into the physiological role of MT5-MMP in human neurons and astrocytes, suggesting that therapeutic strategies targeting MT5-MMP should be controlled for potential side effects on astrocytic physiology and neuronal morphology.

Keywords: Alzheimer’s disease; disease modeling; hiPSC-derived astrocytes; human-induced pluripotent stem cells; metalloproteinase; morphometry; neuronal differentiation; whole-cell patch-clamp.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Amyloid beta-Protein Precursor / genetics
  • Amyloid beta-Protein Precursor / metabolism
  • Astrocytes / cytology
  • Astrocytes / metabolism*
  • CRISPR-Cas Systems
  • Cell Differentiation
  • Cell Line
  • Excitatory Amino Acid Transporter 1 / genetics*
  • Excitatory Amino Acid Transporter 1 / metabolism
  • Gene Editing
  • Gene Expression Regulation
  • Gene Knockout Techniques
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism*
  • Matrix Metalloproteinases, Membrane-Associated / deficiency
  • Matrix Metalloproteinases, Membrane-Associated / genetics*
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism*
  • Neurons / cytology
  • Neurons / metabolism*
  • Patch-Clamp Techniques
  • S100 Calcium Binding Protein beta Subunit / genetics*
  • S100 Calcium Binding Protein beta Subunit / metabolism
  • Signal Transduction

Substances

  • APP protein, human
  • Amyloid beta-Protein Precursor
  • Excitatory Amino Acid Transporter 1
  • S100 Calcium Binding Protein beta Subunit
  • SLC1A3 protein, human
  • MMP24 protein, human
  • Matrix Metalloproteinases, Membrane-Associated