Loss of survival factors and activation of inflammatory cascades in brain sympathetic centers in type 1 diabetic mice

Am J Physiol Endocrinol Metab. 2015 Apr 15;308(8):E688-98. doi: 10.1152/ajpendo.00504.2014. Epub 2015 Feb 24.

Abstract

Neuroinflammation and neurodegeneration have been observed in the brain in type 1 diabetes (T1D). However, little is known about the mediators of these effects. In T1D mice with 12- and 35-wk duration of diabetes we examined two mechanisms of neurodegeneration, loss of the neuroprotective factors insulin-like growth factor I (IGF-I) and IGF-binding protein-3 (IGFBP-3) and changes in indoleamine 2,3-dioxygenase (IDO) expression in the brain, and compared the response to age-matched controls. Furthermore, levels of matrix metalloproteinase-2 (MMP-2), nucleoside triphosphate diphosphohydrolase-1 (CD39), and ionized calcium-binding adaptor molecule 1 (Iba-1) were utilized to assess inflammatory changes in astrocytes, microglia, and blood vessels. In the diabetic hypothalamus (HYPO), we observed 20% reduction in neuronal soma diameter (P<0.05) and reduced neuronal expression of IGFBP-3 (-32%, P<0.05) and IGF-I (-15%, P<0.05) compared with controls at 35 wk. In diabetic HYPO, MMP-2 expression was increased in astrocytes (46%, P<0.01), and IDO⁺ cell density rose by (62%, P<0.05). CD39 expression dropped by 30% (P<0.05) in microglia and blood vessels. With 10 wk of systemic treatment using minocycline, an anti-inflammatory agent that crosses the blood-brain barrier, MMP-2, IDO, and CD39 levels normalized (P<0.05). Our results suggest that increased IDO and early loss of CD39⁺ protective cells lead to activation of inflammation in sympathetic centers of the CNS. As a downstream effect, the loss of the neuronal survival factors IGFBP-3 and IGF-I and the neurotoxic products of the kynurenine pathway contribute to the loss of neuronal density observed in the HYPO in T1D.

Keywords: brain; diabetes; inflammation; sympathetic nervous system.

Publication types

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

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use
  • Astrocytes / drug effects
  • Astrocytes / immunology
  • Astrocytes / metabolism
  • Astrocytes / pathology
  • Diabetes Mellitus, Type 1 / complications*
  • Diabetes Mellitus, Type 1 / drug therapy
  • Diabetes Mellitus, Type 1 / physiopathology
  • Diabetic Neuropathies / immunology
  • Diabetic Neuropathies / metabolism*
  • Diabetic Neuropathies / pathology
  • Diabetic Neuropathies / prevention & control
  • Disease Progression
  • Down-Regulation* / drug effects
  • Encephalitis / complications*
  • Encephalitis / immunology
  • Encephalitis / metabolism
  • Encephalitis / prevention & control
  • Hypothalamus / drug effects
  • Hypothalamus / immunology
  • Hypothalamus / metabolism*
  • Hypothalamus / pathology
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / metabolism
  • Insulin-Like Growth Factor Binding Protein 3 / metabolism
  • Insulin-Like Growth Factor I / metabolism
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Male
  • Mice, Inbred C57BL
  • Microglia / drug effects
  • Microglia / immunology
  • Microglia / metabolism
  • Microglia / pathology
  • Minocycline / therapeutic use
  • Nerve Tissue Proteins / antagonists & inhibitors
  • Nerve Tissue Proteins / metabolism*
  • Neurons / drug effects
  • Neurons / immunology
  • Neurons / metabolism
  • Neurons / pathology
  • Sympathetic Nervous System / drug effects
  • Sympathetic Nervous System / immunology
  • Sympathetic Nervous System / metabolism*
  • Sympathetic Nervous System / pathology
  • Up-Regulation / drug effects

Substances

  • Anti-Inflammatory Agents, Non-Steroidal
  • IDO1 protein, mouse
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Inflammation Mediators
  • Insulin-Like Growth Factor Binding Protein 3
  • Nerve Tissue Proteins
  • insulin-like growth factor-1, mouse
  • Insulin-Like Growth Factor I
  • Minocycline