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Proteomic analysis reveals perturbed energy metabolism and elevated oxidative stress in hearts of rats with inborn low aerobic capacity
dc.contributor.authorBurniston, Jatin G.en_US
dc.contributor.authorKenyani, Jennaen_US
dc.contributor.authorWastling, Jonathan M.en_US
dc.contributor.authorBurant, Charles F.en_US
dc.contributor.authorQi, Nathan R.en_US
dc.contributor.authorKoch, Lauren G.en_US
dc.contributor.authorBritton, Steven L.en_US
dc.date.accessioned2011-11-10T15:33:50Z
dc.date.available2012-10-01T18:34:26Zen_US
dc.date.issued2011-08en_US
dc.identifier.citationBurniston, Jatin G.; Kenyani, Jenna; Wastling, Jonathan M.; Burant, Charles F.; Qi, Nathan R.; Koch, Lauren G.; Britton, Steven L. (2011). "Proteomic analysis reveals perturbed energy metabolism and elevated oxidative stress in hearts of rats with inborn low aerobic capacity." PROTEOMICS 11(16): 3369-3379. <http://hdl.handle.net/2027.42/86916>en_US
dc.identifier.issn1615-9853en_US
dc.identifier.issn1615-9861en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/86916
dc.description.abstractSelection on running capacity has created rat phenotypes of high‐capacity runners (HCRs) that have enhanced cardiac function and low‐capacity runners (LCRs) that exhibit risk factors of metabolic syndrome. We analysed hearts of HCRs and LCRs from generation 22 of selection using DIGE and identified proteins from MS database searches. The running capacity of HCRs was six‐fold greater than LCRs. DIGE resolved 957 spots and proteins were unambiguously identified in 369 spots. Protein expression profiling detected 67 statistically significant ( p <0.05; false discovery rate <10%, calculated using q ‐values) differences between HCRs and LCRs. Hearts of HCR rats exhibited robust increases in the abundance of each enzyme of the β‐oxidation pathway. In contrast, LCR hearts were characterised by the modulation of enzymes associated with ketone body or amino acid metabolism. LCRs also exhibited enhanced expression of antioxidant enzymes such as catalase and greater phosphorylation of α B‐crystallin at serine 59, which is a common point of convergence in cardiac stress signalling. Thus, proteomic analysis revealed selection on low running capacity is associated with perturbations in cardiac energy metabolism and provided the first evidence that the LCR cardiac proteome is exposed to greater oxidative stress.en_US
dc.publisherWILEY‐VCH Verlagen_US
dc.subject.other2‐DEen_US
dc.subject.otherAnimal Proteomicsen_US
dc.subject.otherAnimal Selection Modelen_US
dc.subject.otherMSen_US
dc.titleProteomic analysis reveals perturbed energy metabolism and elevated oxidative stress in hearts of rats with inborn low aerobic capacityen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelBiological Chemistryen_US
dc.subject.hlbsecondlevelChemical Engineeringen_US
dc.subject.hlbsecondlevelChemistryen_US
dc.subject.hlbsecondlevelMaterials Science and Engineeringen_US
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biologyen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.subject.hlbtoplevelScienceen_US
dc.subject.hlbtoplevelEngineeringen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Internal Medicine, University of Michigan, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumDepartment of Anesthesiology, University of Michigan, Ann Arbor, MI, USAen_US
dc.contributor.affiliationotherResearch Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, UKen_US
dc.contributor.affiliationotherInstitute for Health Research, Liverpool John Moores University, Liverpool, UKen_US
dc.contributor.affiliationotherInstitute of Infection and Global Health, University of Liverpool, Liverpool, UKen_US
dc.contributor.affiliationotherMuscle Physiology and Proteomics Laboratory, Research Institute for Sport and Exercise Sciences, Tom Reilly Building, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK Fax: +44‐151‐904‐6284en_US
dc.identifier.pmid21751351en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/86916/1/3369_ftp.pdf
dc.identifier.doi10.1002/pmic.201000593en_US
dc.identifier.sourcePROTEOMICSen_US
dc.identifier.citedreferenceKoch, L. G., Britton, S. L., Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol. Genomics 2001, 5, 45 – 52.en_US
dc.identifier.citedreferenceCarlborg, O., Jacobsson, L., Ahgren, P., Siegel, P., Andersson, L., Epistasis and the release of genetic variation during long‐term selection. Nat. Genet. 2006, 38, 418 – 420.en_US
dc.identifier.citedreferenceWisloff, U., Najjar, S. M., Ellingsen, O., Haram, P. M. et al., Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 2005, 307, 418 – 420.en_US
dc.identifier.citedreferenceLujan, H. L., Britton, S. L., Koch, L. G., DiCarlo, S. E., Reduced susceptibility to ventricular tachyarrhythmias in rats selectively bred for high aerobic capacity. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, H2933 – H2941.en_US
dc.identifier.citedreferenceNoland, R. C., Thyfault, J. P., Henes, S. T., Whitfield, B. R. et al., Artificial selection for high‐capacity endurance running is protective against high‐fat diet‐induced insulin resistance. Am. J. Physiol. Endocrinol. Metab. 2007, 293, E31 – E41.en_US
dc.identifier.citedreferencePalpant, N. J., Szatkowski, M. L., Wang, W., Townsend, D. et al., Artificial selection for whole animal low intrinsic aerobic capacity co‐segregates with hypoxia‐induced cardiac pump failure. PLoS One 2009, 4, e6117.en_US
dc.identifier.citedreferenceBye, A., Langaas, M., Hoydal, M. A., Kemi, O. J. et al., Aerobic capacity‐dependent differences in cardiac gene expression. Physiol. Genomics 2008, 33, 100 – 109.en_US
dc.identifier.citedreferenceBiesiadecki, B. J., Brand, P. H., Koch, L. G., Britton, S. L., A gravimetric method for the measurement of total spontaneous activity in rats. Proc. Soc. Exp. Biol. Med. 1999, 222, 65 – 69.en_US
dc.identifier.citedreferenceNelson, M. M., Jones, A. R., Carmen, J. C., Sinai, A. P. et al., Modulation of the host cell proteome by the intracellular apicomplexan parasite Toxoplasma gondii. Infect. Immun. 2008, 76, 828 – 844.en_US
dc.identifier.citedreferenceBurniston, J. G., Adaptation of the rat cardiac proteome in response to intensity‐controlled endurance exercise. Proteomics 2009, 9, 106 – 115.en_US
dc.identifier.citedreferenceHolloway, K. V., O'Gorman, M., Woods, P., Morton, J. P. et al., Proteomic investigation of changes in human vastus lateralis muscle in response to interval‐exercise training. Proteomics 2009, 9, 5155 – 5174.en_US
dc.identifier.citedreferenceLynen, F., Wieland, O., [beta]‐Ketoreductase. In: Methods Enzymol. Academic Press, New York, 1955, 566 – 573.en_US
dc.identifier.citedreferenceBurniston, J. G., Changes in the rat skeletal muscle proteome induced by moderate‐intensity endurance exercise. Biochim. Biophys. Acta 2008, 1784, 1077 – 1086.en_US
dc.identifier.citedreferenceLiang, X., Le, W., Zhang, D., Schulz, H., Impact of the intramitochondrial enzyme organization on fatty acid oxidation. Biochem. Soc. Trans. 2001, 29, 279 – 282.en_US
dc.identifier.citedreferenceMayr, M., Chung, Y. L., Mayr, U., McGregor, E. et al., Loss of PKC‐delta alters cardiac metabolism. Am. J. Physiol. Heart Circ. Physiol. 2004, 287, H937 – H945.en_US
dc.identifier.citedreferenceChu, G., Kerr, J. P., Mitton, B., Egnaczyk, G. F. et al., Proteomic analysis of hyperdynamic mouse hearts with enhanced sarcoplasmic reticulum calcium cycling. Faseb J. 2004, 18, 1725 – 1727.en_US
dc.identifier.citedreferenceSun, B., Wang, J. H., Lv, Y. Y., Zhu, S. S. et al., Proteomic adaptation to chronic high intensity swimming training in the rat heart. Comp. Biochem. Physiol. Part D Genomics Proteomics 2008, 3, 108 – 117.en_US
dc.identifier.citedreferenceGerber, L. K., Aronow, B. J., Matlib, M. A., Activation of a novel long‐chain free fatty acid generation and export system in mitochondria of diabetic rat hearts. Am. J. Physiol. Cell Physiol. 2006, 291, C1198 – C1207.en_US
dc.identifier.citedreferenceGoni, F. M., Requero, M. A., Alonso, A., Palmitoylcarnitine, a surface‐active metabolite. FEBS Lett. 1996, 390, 1 – 5.en_US
dc.identifier.citedreferenceFinck, B. N., The PPAR regulatory system in cardiac physiology and disease. Cardiovasc. Res. 2007, 73, 269 – 277.en_US
dc.identifier.citedreferenceMakowski, L., Noland, R. C., Koves, T. R., Xing, W. et al., Metabolic profiling of PPARalpha − / − mice reveals defects in carnitine and amino acid homeostasis that are partially reversed by oral carnitine supplementation. Faseb J. 2009, 23, 586 – 604.en_US
dc.identifier.citedreferenceChen, C. H., Budas, G. R., Churchill, E. N., Disatnik, M. H. et al., Activation of aldehyde dehydrogenase‐2 reduces ischemic damage to the heart. Science 2008, 321, 1493 – 1495.en_US
dc.identifier.citedreferenceZhou, S. G., Wang, P., Pi, R. B., Gao, J. et al., Reduced expression of GSTM2 and increased oxidative stress in spontaneously hypertensive rat. Mol. Cell. Biochem. 2008, 309, 99 – 107.en_US
dc.identifier.citedreferenceThyfault, J. P., Rector, R. S., Uptergrove, G. M., Borengasser, S. J. 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.citedreferenceTweedie, C., Romestaing, C., Burelle, Y., Safdar, A. 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. 2010, 300, R544 – R553.en_US
dc.identifier.citedreferenceAggeli, I. K., Beis, I., Gaitanaki, C., Oxidative stress and calpain inhibition induce alpha B‐crystallin phosphorylation via p38‐MAPK and calcium signalling pathways in H9c2 cells. Cell Signal. 2008, 20, 1292 – 1302.en_US
dc.identifier.citedreferenceWhittaker, R., Glassy, M. S., Gude, N., Sussman, M. A. et al., Kinetics of the translocation and phosphorylation of alphaB‐crystallin in mouse heart mitochondria during ex vivo ischemia. Am. J. Physiol. Heart Circ. Physiol. 2009, 296, H1633 – H1642.en_US
dc.identifier.citedreferenceLaunay, N., Goudeau, B., Kato, K., Vicart, P., Lilienbaum, A., Cell signaling pathways to alphaB‐crystallin following stresses of the cytoskeleton. Exp. Cell. Res. 2006, 312, 3570 – 3584.en_US
dc.identifier.citedreferencePawlak, A., Gil, R. J., Walczak, E., Seweryniak, P., Desmin expression in human cardiomyocytes and selected clinical and echocardiographic parameters in patients with chronic heart failure. Kardiol. Pol. 2009, 67, 955 – 961.en_US
dc.identifier.citedreferenceCooper, G., Cytoskeletal networks and the regulation of cardiac contractility: microtubules, hypertrophy, and cardiac dysfunction. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, H1003 – H1014.en_US
dc.identifier.citedreferenceBluhm, W. F., Martin, J. L., Mestril, R., Dillmann, W. H., Specific heat shock proteins protect microtubules during simulated ischemia in cardiac myocytes. Am. J. Physiol. 1998, 275, H2243 – H2249.en_US
dc.identifier.citedreferenceRybakin, V., Clemen, C. S., Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. Bioessays 2005, 27, 625 – 632.en_US
dc.identifier.citedreferenceSarkar, S., Leaman, D. W., Gupta, S., Sil, P. et al., Cardiac overexpression of myotrophin triggers myocardial hypertrophy and heart failure in transgenic mice. J. Biol. Chem. 2004, 279, 20422 – 20434.en_US
dc.identifier.citedreferenceDevillard, L., Vandroux, D., Tissier, C., Brochot, A. et al., Tubulin ligands suggest a microtubule‐NADPH oxidase relationship in postischemic cardiomyocytes. Eur. J. Pharmacol. 2006, 548, 64 – 73.en_US
dc.identifier.citedreferenceDong, X., Liu, J., Zheng, H., Glasford, J. W. et al., In situ dynamically monitoring the proteolytic function of the ubiquitin‐proteasome system in cultured cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 2004, 287, H1417 – H1425.en_US
dc.identifier.citedreferenceBulteau, A. L., Lundberg, K. C., Humphries, K. M., Sadek, H. A. et al., Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J. Biol. Chem. 2001, 276, 30057 – 30063.en_US
dc.identifier.citedreferencePowell, S. R., Samuel, S. M., Wang, P., Divald, A. et al., Upregulation of myocardial 11S‐activated proteasome in experimental hyperglycemia. J. Mol. Cell. Cardiol. 2008, 44, 618 – 621.en_US
dc.identifier.citedreferenceBurniston, J. G., Hoffman, E. P., Proteomic responses of skeletal and cardiac muscle to exercise. Exp. Rev. Proteomics 2011, 8, 361 – 377.en_US
dc.identifier.citedreferenceTurko, I. V., Murad, F., Quantitative protein profiling in heart mitochondria from diabetic rats. J. Biol. Chem. 2003, 278, 35844 – 35849.en_US
dc.identifier.citedreferenceFaber, M. J., Dalinghaus, M., Lankhuizen, I. M., Bezstarosti, K. et al., Proteomic changes in the pressure overloaded right ventricle after 6 weeks in young rats: correlations with the degree of hypertrophy. Proteomics 2005, 5, 2519 – 2530.en_US
dc.identifier.citedreferenceBugger, H., Schwarzer, M., Chen, D., Schrepper, A. et al., Proteomic remodelling of mitochondrial oxidative pathways in pressure overload‐induced heart failure. Cardiovasc. Res. 2010, 85, 376 – 384.en_US
dc.identifier.citedreferenceMeng, C., Jin, X., Xia, L., Shen, S. M. et al., Alterations of mitochondrial enzymes contribute to cardiac hypertrophy before hypertension development in spontaneously hypertensive rats. J. Proteome Res. 2009, 8, 2463 – 2475.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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