Heterozygous Meg2 Ablation Causes Intraocular Pressure Elevation and Progressive Glaucomatous Neurodegeneration

Mol Neurobiol. 2019 Jun;56(6):4322-4345. doi: 10.1007/s12035-018-1376-2. Epub 2018 Oct 12.

Abstract

Glaucomatous neurodegeneration represents one of the major causes of irreversible blindness worldwide. Yet, the detailed molecular mechanisms that initiate optic nerve damage and retinal ganglion cell (RGC) loss are not fully understood. Members of the protein tyrosine phosphatase (PTP) superfamily are key players in numerous neurodegenerative diseases. In order to investigate the potential functional relevance of the PTP megakaryocyte 2 (Meg2) in retinal neurodegeneration, we analyzed Meg2 knockout (KO) and heterozygous (HET)-synonym protein-tyrosine phosphatase non-receptor type 9 (Ptpn9)-mice. Interestingly, via global microarray and quantitative real-time PCR (RT-qPCR) analyses of Meg2 KO and HET retinae, we observed a dysregulation of several candidate genes that are highly associated with retinal degeneration and intraocular pressure (IOP) elevation, the main risk factor for glaucoma. Subsequent IOP measurements in Meg2 HET mice verified progressive age-dependent IOP elevation. Ultrastructural analyses and immunohistochemistry showed severe optic nerve degeneration accompanied by a dramatic loss of RGCs. Additionally, HET mice displayed reactive micro-/macrogliosis and early activation of the classical complement cascade with pronounced deposition of the membrane attack complex (MAC) in the retina and optic nerve. When treated with latanoprost, significant IOP lowering prevented RGC loss and microglial invasion in HET mice. Finally, electroretinogram (ERG) recordings revealed reduced a- and b-wave amplitudes, indicating impaired retinal functionality in Meg2 HET mice. Collectively, our findings indicate that the heterozygous loss of Meg2 in mice is sufficient to cause IOP elevation and glaucomatous neurodegeneration. Thus, Meg2 HET mice may serve as a novel animal model to study the pathomechanism involved in the onset and progression of glaucoma.

Keywords: Glaucoma; Intraocular pressure elevation; Mouse model; Neurodegeneration; Protein tyrosine phosphatase Meg2; Retina.

MeSH terms

  • Animals
  • Complement Activation / drug effects
  • Disease Progression*
  • Down-Regulation / genetics
  • Glaucoma / complications*
  • Glaucoma / genetics
  • Glaucoma / pathology
  • Glaucoma / physiopathology*
  • Gliosis / complications
  • Gliosis / pathology
  • Heterozygote
  • Intraocular Pressure* / drug effects
  • Latanoprost / pharmacology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia / drug effects
  • Microglia / metabolism
  • Microglia / pathology
  • Neuroprotective Agents / pharmacology
  • Optic Nerve / drug effects
  • Optic Nerve / pathology
  • Optic Nerve / ultrastructure
  • Protein Tyrosine Phosphatases, Non-Receptor / deficiency*
  • Protein Tyrosine Phosphatases, Non-Receptor / metabolism
  • Retinal Degeneration / complications*
  • Retinal Degeneration / genetics
  • Retinal Degeneration / pathology
  • Retinal Degeneration / physiopathology*
  • Retinal Ganglion Cells / drug effects
  • Retinal Ganglion Cells / pathology
  • Up-Regulation / genetics

Substances

  • Neuroprotective Agents
  • Latanoprost
  • Protein Tyrosine Phosphatases, Non-Receptor
  • Ptpn9 protein, mouse