Impaired adenosine monophosphate-activated protein kinase signalling in dorsal root ganglia neurons is linked to mitochondrial dysfunction and peripheral neuropathy in diabetes.

Mitochondrial dysfunction occurs in sensory neurons and may contribute to distal axonopathy in animal models of diabetic neuropathy. The adenosine monophosphate-activated protein kinase and peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) signalling axis senses the metabolic dema...

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Publicado en:Brain: A Journal of Neurology Vol. 135; no. 6; pp. 1751 - 1767
Autores principales: Roy Chowdhury SK, Smith DR, Saleh A, Schapansky J, Marquez A, Gomes S, Akude E, Morrow D, Calcutt NA, Fernyhough P, Roy Chowdhury, Subir K, Smith, Darrell R, Saleh, Ali, Schapansky, Jason, Marquez, Alexandra, Gomes, Suzanne, Akude, Eli, Morrow, Dwane, Calcutt, Nigel A, Fernyhough, Paul
Formato: research Journal Article
Publicado: Oxford University Press / USA Jun2012
Acceso en línea:Ver este registro en EBSCOhost
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      dt: Jun2012
      vid: 135
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      pub: Oxford University Press / USA
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        NLM22561641
        2011562058
        10.1093/brain/aws097
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        atl: Impaired adenosine monophosphate-activated protein kinase signalling in dorsal root ganglia neurons is linked to mitochondrial dysfunction and peripheral neuropathy in diabetes.
      aug:
        au:
          Roy Chowdhury SK
          Smith DR
          Saleh A
          Schapansky J
          Marquez A
          Gomes S
          Akude E
          Morrow D
          Calcutt NA
          Fernyhough P
          Roy Chowdhury, Subir K
          Smith, Darrell R
          Saleh, Ali
          Schapansky, Jason
          Marquez, Alexandra
          Gomes, Suzanne
          Akude, Eli
          Morrow, Dwane
          Calcutt, Nigel A
          Fernyhough, Paul
        affil: Division of Neurodegenerative Disorders, St. Boniface Hospital Research Centre, R4023-1 - 351 Tache Avenue, Winnipeg, MB R2H 2A6, Canada
      sug:
        subj:
          Ganglia, Sensory Pathology
          Mitochondrial Diseases Pathology
          Peripheral Nervous System Diseases Pathology
          Phosphotransferases Metabolism
          Sensory Receptor Cells
          Signal Transduction Physiology
          Adenosine Triphosphate Pharmacodynamics
          Analysis of Variance
          Animal Studies
          Antiinflammatory Agents, Non-Steroidal Therapeutic Use
          Blood Glucose Drug Effects
          Body Weight Drug Effects
          Cell Membrane Drug Effects
          Cells
          Cytological Techniques
          Diabetes Mellitus Complications
          Dose-Response Relationship, Drug
          Genes Drug Effects
          Genetics
          Hyperalgesia Physiopathology
          Male
          Membrane Potentials
          Mice
          Mitochondrial Diseases Drug Therapy
          Mitochondrial Diseases Etiology
          Models, Biological
          Mutation
          Nerve Fibers Pathology
          Neurons Pathology
          Oxygen Consumption Drug Effects
          Peripheral Nervous System Diseases Drug Therapy
          Peripheral Nervous System Diseases Etiology
          Physical Stimulation Adverse Effects
          Proteins
          Proteins Metabolism
          Rats
          Reaction Time
          Reaction Time Drug Effects
          Sensory Receptor Cells Drug Effects
          Sensory Receptor Cells Pathology
          Signal Transduction Drug Effects
          Stilbenes Therapeutic Use
          Male
      ab: Mitochondrial dysfunction occurs in sensory neurons and may contribute to distal axonopathy in animal models of diabetic neuropathy. The adenosine monophosphate-activated protein kinase and peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) signalling axis senses the metabolic demands of cells and regulates mitochondrial function. Studies in muscle, liver and cardiac tissues have shown that the activity of adenosine monophosphate-activated protein kinase and PGC-1α is decreased under hyperglycaemia. In this study, we tested the hypothesis that deficits in adenosine monophosphate-activated protein kinase/PGC-1α signalling in sensory neurons underlie impaired axonal plasticity, suboptimal mitochondrial function and development of neuropathy in rodent models of type 1 and type 2 diabetes. Phosphorylation and expression of adenosine monophosphate-activated protein kinase/PGC-1α and mitochondrial respiratory chain complex proteins were downregulated in dorsal root ganglia of both streptozotocin-diabetic rats and db/db mice. Adenoviral-mediated manipulation of endogenous adenosine monophosphate-activated protein kinase activity using mutant proteins modulated neurotrophin-directed neurite outgrowth in cultures of sensory neurons derived from adult rats. Addition of resveratrol to cultures of sensory neurons derived from rats after 3-5 months of streptozotocin-induced diabetes, significantly elevated adenosine monophosphate-activated protein kinase levels, enhanced neurite outgrowth and normalized mitochondrial inner membrane polarization in axons. The bioenergetics profile (maximal oxygen consumption rate, coupling efficiency, respiratory control ratio and spare respiratory capacity) was aberrant in cultured sensory neurons from streptozotocin-diabetic rats and was corrected by resveratrol treatment. Finally, resveratrol treatment for the last 2 months of a 5-month period of diabetes reversed thermal hypoalgesia and attenuated foot skin intraepidermal nerve fibre loss and reduced myelinated fibre mean axonal calibre in streptozotocin-diabetic rats. These data suggest that the development of distal axonopathy in diabetic neuropathy is linked to nutrient excess and mitochondrial dysfunction via defective signalling of the adenosine monophosphate-activated protein kinase/PGC-1α pathway.
      pubtype: Academic Journal
      doctype:
        research
        Journal Article
      ougenre: Article
    language: English
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