Increased Indoleamine 2,3-Dioxygenase and Quinolinic Acid Expression in Microglia and Müller Cells of Diabetic Human and Rodent Retina

Invest Ophthalmol Vis Sci. 2017 Oct 1;58(12):5043-5055. doi: 10.1167/iovs.17-21654.

Abstract

Purpose: We investigated the relationship between inflammation, neuronal loss, and expression of indoleamine 2, 3-dioxygenase (IDO) and quinolinic acid (QUIN) in the retina of subjects with type 1 diabetes (T1D) and type 2 diabetes (T2D) and in the retina of rats with T1D.

Methods: Retinas from T1D (n = 7), T2D (n = 13), and 20 age-matched nondiabetic human donors and from T1D (n = 3) and control rats (n = 3) were examined using immunohistochemistry for IDO, QUIN, cluster of differentiation 39 (CD39), ionized calcium-binding adaptor molecule (Iba-1, for macrophages and microglia), Vimentin (VIM; for Müller cells), neuronal nuclei (NeuN; for neurons), and UEA1 lectin (for blood vessels).

Results: Based on morphologic criteria, CD39+/ionized calcium binding adaptor molecule 1(Iba-1+) resident microglia and CD39-/Iba-1+ bone marrow-derived macrophages were present at higher density in T1D (13% increase) and T2D (26% increase) human retinas when compared with controls. The density and brightness of IDO+ microglia were increased in both T1D and T2D human retinas. The intensity of QUIN+ expression on CD39+ microglia and VIM+ Müller cells was greatly increased in both human T1D and T2D retinas. T1D retinas showed a 63% loss of NeuN+ neurons and T2D retinas lost approximately 43% when compared with nondiabetic human retinas. Few QUIN+ microglia-like cells were seen in nondiabetic retinas, but the numbers increased 18-fold in T1D and 7-fold in T2D in the central retina. In T1D rat retinas, the density of IDO+ microglia increased 2.8-fold and brightness increased 2.1-fold when compared with controls.

Conclusions: Our findings suggest that IDO and QUIN expression in the retinas of diabetic rats and humans could contribute to the neuronal degeneration that is characteristic of diabetic retinopathy.

MeSH terms

  • Aged
  • Animals
  • Antigens, CD / metabolism
  • Antigens, Nuclear / metabolism
  • Apyrase / metabolism
  • Biomarkers / metabolism*
  • Calcium-Binding Proteins / metabolism
  • DNA-Binding Proteins / metabolism
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Type 1 / metabolism
  • Diabetes Mellitus, Type 2 / metabolism
  • Diabetic Retinopathy / metabolism*
  • Diabetic Retinopathy / pathology
  • Ependymoglial Cells / metabolism*
  • Ependymoglial Cells / pathology
  • Female
  • Fluorescent Antibody Technique, Indirect
  • Humans
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism*
  • Male
  • Microfilament Proteins / metabolism
  • Microglia / metabolism*
  • Microglia / pathology
  • Microscopy, Confocal
  • Middle Aged
  • Nerve Tissue Proteins / metabolism
  • Quinolinic Acid / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Retina / metabolism*
  • Retina / pathology
  • Vimentin / metabolism

Substances

  • AIF1 protein, human
  • Aif1 protein, rat
  • Antigens, CD
  • Antigens, Nuclear
  • Biomarkers
  • Calcium-Binding Proteins
  • DNA-Binding Proteins
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Microfilament Proteins
  • Nerve Tissue Proteins
  • Rbfox3 protein, rat
  • Vimentin
  • neuronal nuclear antigen NeuN, human
  • Apyrase
  • CD39 antigen
  • Quinolinic Acid