View Item 

Show simple item record

Brain diabetic neurodegeneration segregates with low intrinsic aerobic capacity
dc.contributor.authorChoi, Joungilen_US
dc.contributor.authorChandrasekaran, Krishen_US
dc.contributor.authorDemarest, Tyler G.en_US
dc.contributor.authorKristian, Tiboren_US
dc.contributor.authorXu, Suen_US
dc.contributor.authorVijaykumar, Kadambarien_US
dc.contributor.authorDsouza, Kevin Geoffreyen_US
dc.contributor.authorQi, Nathan R.en_US
dc.contributor.authorYarowsky, Paul J.en_US
dc.contributor.authorGallipoli, Raoen_US
dc.contributor.authorKoch, Lauren G.en_US
dc.contributor.authorFiskum, Gary M.en_US
dc.contributor.authorBritton, Steven L.en_US
dc.contributor.authorRussell, James W.en_US
dc.date.accessioned2014-09-03T16:51:41Z
dc.date.availableWITHHELD_12_MONTHSen_US
dc.date.available2014-09-03T16:51:41Z
dc.date.issued2014-08en_US
dc.identifier.citationChoi, Joungil; Chandrasekaran, Krish; Demarest, Tyler G.; Kristian, Tibor; Xu, Su; Vijaykumar, Kadambari; Dsouza, Kevin Geoffrey; Qi, Nathan R.; Yarowsky, Paul J.; Gallipoli, Rao; Koch, Lauren G.; Fiskum, Gary M.; Britton, Steven L.; Russell, James W. (2014). "Brain diabetic neurodegeneration segregates with low intrinsic aerobic capacity." Annals of Clinical and Translational Neurology 1(8): 589-604.en_US
dc.identifier.issn2328-9503en_US
dc.identifier.issn2328-9503en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/108300
dc.description.abstractObjectives Diabetes leads to cognitive impairment and is associated with age‐related neurodegenerative diseases including Alzheimer's disease ( AD ). Thus, understanding diabetes‐induced alterations in brain function is important for developing early interventions for neurodegeneration. Low‐capacity runner ( LCR ) rats are obese and manifest metabolic risk factors resembling human “impaired glucose tolerance” or metabolic syndrome. We examined hippocampal function in aged LCR rats compared to their high‐capacity runner ( HCR ) rat counterparts. Methods Hippocampal function was examined using proton magnetic resonance spectroscopy and imaging, unbiased stereology analysis, and a Y maze. Changes in the mitochondrial respiratory chain function and levels of hyperphosphorylated tau and mitochondrial transcriptional regulators were examined. Results The levels of glutamate, myo ‐inositol, taurine, and choline‐containing compounds were significantly increased in the aged LCR rats. We observed a significant loss of hippocampal neurons and impaired cognitive function in aged LCR rats. Respiratory chain function and activity were significantly decreased in the aged LCR rats. Hyperphosphorylated tau was accumulated within mitochondria and peroxisome proliferator‐activated receptor‐gamma coactivator 1 α , the NAD + ‐dependent protein deacetylase sirtuin 1, and mitochondrial transcription factor A were downregulated in the aged LCR rat hippocampus. Interpretation These data provide evidence of a neurodegenerative process in the hippocampus of aged LCR rats, consistent with those seen in aged‐related dementing illnesses such as AD in humans. The metabolic and mitochondrial abnormalities observed in LCR rat hippocampus are similar to well‐described mechanisms that lead to diabetic neuropathy and may provide an important link between cognitive and metabolic dysfunction.en_US
dc.publisherWiley Periodicals, Inc.en_US
dc.publisherAcademic Pressen_US
dc.titleBrain diabetic neurodegeneration segregates with low intrinsic aerobic capacityen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelNeurology and Neurosciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/108300/1/acn386.pdf
dc.identifier.doi10.1002/acn3.86en_US
dc.identifier.sourceAnnals of Clinical and Translational Neurologyen_US
dc.identifier.citedreferenceChoi J, Batchu VV, Schubert M, et al. A novel PGC‐1alpha isoform in brain localizes to mitochondria and associates with PINK1 and VDAC. Biochem Biophys Res Commun 2013; 435: 671 – 677.en_US
dc.identifier.citedreferenceStrachan MW, Price JF, Frier BM. Diabetes, cognitive impairment, and dementia. BMJ 2008; 336: 6.en_US
dc.identifier.citedreferenceCole AR, Astell A, Green C, et al. Molecular connexions between dementia and diabetes. Neurosci Biobehav Rev 2007; 31: 1046 – 1063.en_US
dc.identifier.citedreferenceGrunblatt E, Bartl J, Riederer P. The link between iron, metabolic syndrome, and Alzheimer's disease. J Neural Transm 2011; 118: 371 – 379.en_US
dc.identifier.citedreferenceOtt A, Stolk RP, van Harskamp F, et al. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 1999; 53: 1937 – 1942.en_US
dc.identifier.citedreferenceCrane PK, Walker R, Hubbard RA, et al. Glucose levels and risk of dementia. N Engl J Med 2013; 369: 540 – 548.en_US
dc.identifier.citedreferenceKoch LG, Britton SL. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genomics 2001; 5: 45 – 52.en_US
dc.identifier.citedreferenceWisloff U, Najjar SM, Ellingsen O, et al. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 2005; 307: 418 – 420.en_US
dc.identifier.citedreferenceKoch LG, Britton SL, Wisloff U. A rat model system to study complex disease risks, fitness, aging, and longevity. Trends Cardiovasc Med 2013; 22: 29 – 34.en_US
dc.identifier.citedreferenceValla J, Schneider L, Niedzielko T, et al. Impaired platelet mitochondrial activity in Alzheimer's disease and mild cognitive impairment. Mitochondrion 2006; 6: 323 – 330.en_US
dc.identifier.citedreferenceMoreira PI, Santos MS, Seica R, et al. Brain mitochondrial dysfunction as a link between Alzheimer's disease and diabetes. J Neurol Sci 2007; 257: 206 – 214.en_US
dc.identifier.citedreferenceJohnson GV, Stoothoff WH. Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 2004; 117: 5721 – 5729.en_US
dc.identifier.citedreferenceLi L, Holscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev 2007; 56: 384 – 402.en_US
dc.identifier.citedreferenceMiklossy J, Qing H, Radenovic A, et al. Beta amyloid and hyperphosphorylated tau deposits in the pancreas in type 2 diabetes. Neurobiol Aging 2010; 31: 1503 – 1515.en_US
dc.identifier.citedreferenceSivitz WI, Yorek MA. Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal 2010; 12: 537 – 577.en_US
dc.identifier.citedreferenceGibson GE, Starkov A, Blass JP, et al. Cause and consequence: mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age‐associated neurodegenerative diseases. Biochim Biophys Acta 2010; 1802: 122 – 134.en_US
dc.identifier.citedreferenceHinder LM, Vivekanandan‐Giri A, McLean LL, et al. Decreased glycolytic and tricarboxylic acid cycle intermediates coincide with peripheral nervous system oxidative stress in a murine model of type 2 diabetes. J Endocrinol 2013; 216: 1 – 11.en_US
dc.identifier.citedreferenceBosetti F, Brizzi F, Barogi S, et al. Cytochrome c oxidase and mitochondrial F1F0‐ATPase (ATP synthase) activities in platelets and brain from patients with Alzheimer's disease. Neurobiol Aging 2002; 23: 371 – 376.en_US
dc.identifier.citedreferenceOlsson AH, Yang BT, Hall E, et al. Decreased expression of genes involved in oxidative phosphorylation in human pancreatic islets from patients with type 2 diabetes. Eur J Endocrinol 2011; 165: 589 – 595.en_US
dc.identifier.citedreferenceSoyal SM, Felder TK, Auer S, et al. Greatly extended PPARGC1A genomic locus encodes several new brain‐specific isoforms and influences Huntington disease age of onset. Hum Mol Genet 2012; 21: 3461 – 3473.en_US
dc.identifier.citedreferenceJohri A, Starkov AA, Chandra A, et al. Truncated peroxisome proliferator‐activated receptor‐gamma coactivator 1alpha splice variant is severely altered in Huntington's disease. Neurodegener Dis 2011; 8: 496 – 503.en_US
dc.identifier.citedreferenceLin J, Wu PH, Tarr PT, et al. Defects in adaptive energy metabolism with CNS‐linked hyperactivity in PGC‐1alpha null mice. Cell 2004; 119: 121 – 135.en_US
dc.identifier.citedreferenceMootha VK, Lindgren CM, Eriksson KF, et al. PGC‐1alpha‐responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34: 267 – 273.en_US
dc.identifier.citedreferenceSt‐Pierre J, Drori S, Uldry M, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC‐1 transcriptional coactivators. Cell 2006; 127: 397 – 408.en_US
dc.identifier.citedreferenceCaballero B. The global epidemic of obesity: an overview. Epidemiol Rev 2007; 29: 1 – 5.en_US
dc.identifier.citedreferenceEkstrand MI, Falkenberg M, Rantanen A, et al. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 2004; 13: 935 – 944.en_US
dc.identifier.citedreferenceSilva JP, Kohler M, Graff C, et al. Impaired insulin secretion and beta‐cell loss in tissue‐specific knockout mice with mitochondrial diabetes. Nat Genet 2000; 26: 336 – 340.en_US
dc.identifier.citedreferenceWang R, Li JJ, Diao S, et al. Metabolic stress modulates Alzheimer's beta‐secretase gene transcription via SIRT1‐PPARgamma‐PGC‐1 in neurons. Cell Metab 2013; 17: 685 – 694.en_US
dc.identifier.citedreferenceKhan RS, Fonseca‐Kelly Z, Callinan C, et al. SIRT1 activating compounds reduce oxidative stress and prevent cell death in neuronal cells. Front Cell Neurosci 2012; 6: 63.en_US
dc.identifier.citedreferenceJiang M, Wang J, Fu J, et al. Neuroprotective role of Sirt1 in mammalian models of Huntington's disease through activation of multiple Sirt1 targets. Nat Med 2011; 18: 153 – 158.en_US
dc.identifier.citedreferenceSeifert EL, Bastianelli M, Aguer C, et al. Intrinsic aerobic capacity correlates with greater inherent mitochondrial oxidative and H 2 O 2 emission capacities without major shifts in myosin heavy chain isoform. J Appl Physiol 1985; 2012: 1624 – 1634.en_US
dc.identifier.citedreferenceThyfault JP, Rector RS, Uptergrove GM, et al. Rats selectively bred for low aerobic capacity have reduced hepatic mitochondrial oxidative capacity and susceptibility to hepatic steatosis and injury. J Physiol 2009; 587: 1805 – 1816.en_US
dc.identifier.citedreferenceSapolsky RM. Cellular defenses against excitotoxic insults. J Neurochem 2001; 76: 1601 – 1611.en_US
dc.identifier.citedreferenceMark LP, Prost RW, Ulmer JL, et al. Pictorial review of glutamate excitotoxicity: fundamental concepts for neuroimaging. Am J Neuroradiol 2001; 22: 1813 – 1824.en_US
dc.identifier.citedreferenceYoshiyama Y, Higuchi M, Zhang B, et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007; 53: 337 – 351.en_US
dc.identifier.citedreferencePaula‐Lima AC, De Felice FG, Brito‐Moreira J, et al. Activation of GABA receptors by taurine and muscimol blocks the neurotoxicity of beta‐amyloid in rat hippocampal and cortical neurons. Neuropharmacology 2005; 49: 1140 – 1148.en_US
dc.identifier.citedreferenceWu H, Jin Y, Wei J, et al. Mode of action of taurine as a neuroprotector. Brain Res 2005; 1038: 123 – 131.en_US
dc.identifier.citedreferenceSanta‐Maria I, Hernandez F, Moreno FJ, et al. Taurine, an inducer for tau polymerization and a weak inhibitor for amyloid‐beta‐peptide aggregation. Neurosci Lett 2007; 429: 91 – 94.en_US
dc.identifier.citedreferenceThurston JH, Sherman WR, Hauhart RE, et al. Myo‐inositol: a newly identified nonnitrogenous osmoregulatory molecule in mammalian brain. Pediatr Res 1989; 26: 482 – 485.en_US
dc.identifier.citedreferenceRipps H, Shen W. Review: taurine: a “very essential” amino acid. Mol Vis 2012; 18: 2673 – 2686.en_US
dc.identifier.citedreferenceDu AT, Schuff N, Amend D, et al. Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease. J Neurol Neurosurg Psychiatry 2001; 71: 441 – 447.en_US
dc.identifier.citedreferenceWalter A, Korth U, Hilgert M, et al. Glycerophosphocholine is elevated in cerebrospinal fluid of Alzheimer patients. Neurobiol Aging 2004; 25: 1299 – 1303.en_US
dc.identifier.citedreferenceFarber SA, Slack BE, Blusztajn JK. Acceleration of phosphatidylcholine synthesis and breakdown by inhibitors of mitochondrial function in neuronal cells: a model of the membrane defect of Alzheimer's disease. FASEB J 2000; 14: 2198 – 2206.en_US
dc.identifier.citedreferenceKerchner GA, Hess CP, Hammond‐Rosenbluth KE, et al. Hippocampal CA1 apical neuropil atrophy in mild Alzheimer disease visualized with 7‐T MRI. Neurology 2010; 75: 1381 – 1387.en_US
dc.identifier.citedreferenceHoxworth JM, Xu K, Zhou Y, et al. Cerebral metabolic profile, selective neuron loss, and survival of acute and chronic hyperglycemic rats following cardiac arrest and resuscitation. Brain Res 1999; 821: 467 – 479.en_US
dc.identifier.citedreferenceChurchwell JC, Morris AM, Musso ND, et al. Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory. Neurobiol Learn Mem 2010; 93: 415 – 421.en_US
dc.identifier.citedreferenceWikgren J, Mertikas GG, Raussi P, et al. Selective breeding for endurance running capacity affects cognitive but not motor learning in rats. Physiol Behav 2012; 106: 95 – 100.en_US
dc.identifier.citedreferenceTweedie C, Romestaing C, Burelle Y, et al. Lower oxidative DNA damage despite greater ROS production in muscles from rats selectively bred for high running capacity. Am J Physiol Regul Integr Comp Physiol 2011; 300: R544 – R553.en_US
dc.identifier.citedreferenceAquilano K, Baldell S, Pagliei B, et al. Extranuclear localization of SIRT1 and PGC‐1alpha: an insight into possible roles in diseases associated with mitochondrial dysfunction. Curr Mol Med 2013; 13: 140 – 154.en_US
dc.identifier.citedreferenceAquilano K, Vigilanza P, Baldelli S, et al. Peroxisome proliferator‐activated receptor gamma co‐activator 1 alpha (PGC‐1alpha) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J Biol Chem 2010; 285: 21590 – 21599.en_US
dc.identifier.citedreferenceChen J, Zhou Y, Mueller‐Steiner S, et al. SIRT1 protects against microglia‐dependent amyloid‐beta toxicity through inhibiting NF‐kappaB signaling. J Biol Chem 2005; 280: 40364 – 40374.en_US
dc.identifier.citedreferenceRamadori G, Lee CE, Bookout AL, et al. Brain SIRT1: anatomical distribution and regulation by energy availability. J Neurosci 2005; 28: 9989 – 9996.en_US
dc.identifier.citedreferenceBiason‐Lauber A, Boni‐Schnetzler M, Hubbard BP, et al. Identification of a SIRT1 mutation in a family with type 1 diabetes. Cell Metab 2013; 17: 448 – 455.en_US
dc.identifier.citedreferenceKilbride SM, Gluchowska SA, Telford JE, et al. High‐level inhibition of mitochondrial complexes III and IV is required to increase glutamate release from the nerve terminal. Mol Neurodegener 2011; 6: 53.en_US
dc.identifier.citedreferenceMosconi L. Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. FDG‐PET studies in MCI and AD. Eur J Nucl Med Mol Imaging 2005; 32: 486 – 510.en_US
dc.identifier.citedreferenceRamsden M, Kotilinek L, Forster C, et al. Age‐dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 2005; 25: 10637 – 10647.en_US
dc.identifier.citedreferenceMelov S, Adlard PA, Morten K, et al. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS One 2007; 20: e536.en_US
dc.identifier.citedreferenceSantacruz K, Lewis J, Spires T, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005; 309: 476 – 481.en_US
dc.identifier.citedreferenceVidoni ED, Van Sciver A, Johnson DK, et al. A community‐based approach to trials of aerobic exercise in aging and Alzheimer's disease. Contemp Clin Trials 2012; 33: 1105 – 1116.en_US
dc.identifier.citedreferenceYu F,  Thomas W,  Nelson NW, et al. Impact of 6‐month aerobic exercise on Alzheimer's symptoms. J Appl Gerontol. 201x; xx: 1 – 17.en_US
dc.identifier.citedreferenceFrahm J, Haase A, Matthaei D. Rapid three‐dimensional MR imaging using the FLASH technique. J Comput Assist Tomogr 1986; 10: 363 – 368.en_US
dc.identifier.citedreferenceHaase A, Frahm J, Matthaei D, et al. MR imaging using stimulated echoes (STEAM). Radiology 1986; 160: 787 – 790.en_US
dc.identifier.citedreferenceGruetter R. Automatic, localized in vivo adjustment of all first‐ and second‐order shim coils. Magn Reson Med 1993; 29: 804 – 811.en_US
dc.identifier.citedreferenceHennig J, Nauerth A, Friedburg H. RARE imaging: a fast imaging method for clinical MR. Magn Reson Med 1986; 3: 823 – 833.en_US
dc.identifier.citedreferencePrice WS, Arata Y. The manipulation of water relaxation and water suppression in biological systems using the water‐PRESS pulse sequence. J Magn Reson B 1996; 112: 190 – 192.en_US
dc.identifier.citedreferencePaxinos G, Watson C. The mouse brain in stereotaxic coordinates. 6th ed. New York: Academic Press, 2007.en_US
dc.identifier.citedreferenceWolf OT, Dyakin V, Vadasz C, et al. Volumetric measurement of the hippocampus, the anterior cingulate cortex, and the retrosplenial granular cortex of the rat using structural MRI. Brain research. Brain Res Brain Res Protoc 2002; 10: 41 – 46.en_US
dc.identifier.citedreferenceBogaert YE, Sheu KF, Hof PR, et al. Neuronal subclass‐selective loss of pyruvate dehydrogenase immunoreactivity following canine cardiac arrest and resuscitation. Exp Neurol 2000; 161: 115 – 126.en_US
dc.identifier.citedreferenceWittig I, Karas M, Schagger H. High resolution clear native electrophoresis for in‐gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 2000; 6: 1215 – 1225.en_US
dc.identifier.citedreferenceMarjanska M, Curran GL, Wengenack TM, et al. Monitoring disease progression in transgenic mouse models of Alzheimer's disease with proton magnetic resonance spectroscopy. Proc Natl Acad Sci USA 2005; 102: 11906 – 11910.en_US
dc.identifier.citedreferenceXu S, Zhuo J, Racz J, et al. Early microstructural and metabolic changes following controlled cortical impact injury in rat: a magnetic resonance imaging and spectroscopy study. J Neurotrauma 2011; 28: 2091 – 2102.en_US
dc.identifier.citedreferenceProvencher SW. Automatic quantitation of localized in vivo 1 H spectra with LCModel. NMR Biomed 2001; 14: 260 – 264.en_US
dc.identifier.citedreferenceKe YD, Delerue F, Gladbach A, et al. Experimental diabetes mellitus exacerbates tau pathology in a transgenic mouse model of Alzheimer's disease. PLoS One 2009; 4: e7917.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
acn386.pdf
Size:
530.2KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.