PGC-1α regulation of mitochondrial degeneration in experimental diabetic neuropathy

Neurobiology of Disease

Volumn 64, Issue , 2014, Pages 118-130

  Choi, Joungil ^a,b   Chandrasekaran, Krish ^a,b   Inoue, Tatsuya ^a,b   Muragundla, Anjaneyulu ^a,b   Russell, James W ^a,b  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetes; Mitochondria; Neuropathy; Oxidative stress

Indexed keywords

CHOLESTEROL; GLUCOSE; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; STREPTOZOCIN; TRANSCRIPTION FACTOR NRF1; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CELL VACUOLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CRANIOMETRY; DIABETOGENESIS; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA CONTENT; DOWN REGULATION; EXPERIMENTAL DIABETIC NEUROPATHY; GENE OVEREXPRESSION; GLUCOSE BLOOD LEVEL; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION DEGENERATION; MOUSE; NERVE CONDUCTION; NONHUMAN; NRF1 GENE; OXIDATIVE STRESS; PERIPHERAL NEUROPATHY; PGC 1ALPHA GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN OXIDATION; SPINAL GANGLION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TFAM GENE;

DIABETES; MITOCHONDRIA; NEUROPATHY; OXIDATIVE STRESS;

ANIMALS; CELLS, CULTURED; CHOLESTEROL; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; GANGLIA, SPINAL; HIGH MOBILITY GROUP PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; NEURONS; NUCLEAR RESPIRATORY FACTOR 1; OXIDATION-REDUCTION; OXIDATIVE STRESS; TRANSCRIPTION FACTORS; TRIGLYCERIDES; VACUOLES;

EID: 84893085007     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.01.001     Document Type: Article

References (67)

1. Akude E., Zherebitskaya E., Roy Chowdhury S.K., Girling K., Fernyhough P. 4-Hydroxy-2-nonenal induces mitochondrial dysfunction and aberrant axonal outgrowth in adult sensory neurons that mimics features of diabetic neuropathy. Neurotox. Res. 2009, 17:28-38.
2. Andreasson H., Gyllensten U., Allen M. Real-time DNA quantification of nuclear and mitochondrial DNA in forensic analysis. Biotechniques 2002, 33:402-411.
3. Andrulionyte L., Kuulasmaa T., Chiasson J.L., Laakso M. Single nucleotide polymorphisms of the peroxisome proliferator-activated receptor-alpha gene (PPARA) influence the conversion from impaired glucose tolerance to type 2 diabetes: the STOP-NIDDM trial. Diabetes 2007, 56:1181-1186.
4. Anjaneyulu M., Berent-Spillson A., Inoue T., Choi J., Cherian K., Russell J.W. Transforming growth factor-beta induces cellular injury in experimental diabetic neuropathy. Exp. Neurol. 2008, 211:469-479.
5. Aquilano K., Baldelli S., Pagliei B., Ciriolo M.R. 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.
6. Baar K., Wende A.R., Jones T.E., Marison M., Nolte L.A., Chen M., et al. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 2002, 16:1879-1886.
7. Berent-Spillson A., Russell J.W. Metabotropic glutamate receptor 3 protects neurons from glucose-induced oxidative injury by increasing intracellular glutathione concentration. J. Neurochem. 2007, 101:342-354.
8. Bogacka I., Xie H., Bray G.A., Smith S.R. Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 2005, 54:1392-1399.
9. Brand M.D., Nicholls D.G. Assessing mitochondrial dysfunction in cells. Biochem. J. 2011, 435:297-312.
10. Brownlee M. Negative consequences of glycation. Metabolism 2000, 49:9-13.
11. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
12. Callaghan B.C., Cheng H.T., Stables C.L., Smith A.L., Feldman E.L. Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol. 2012, 11:521-534.
13. Canto C., Auwerx J. Calorie restriction: is AMPK a key sensor and effector?. Physiol. (Bethesda) 2011, 26:214-224.
14. Choi J., Malakowsky C.A., Talent J.M., Conrad C.C., Gracy R.W. Identification of oxidized plasma proteins in Alzheimer's disease. Biochem. Biophys. Res. Commun. 2002, 293:1566-1570.
15. Choi J., Batchu V.V., Schubert M., Castellani R.J., Russell J.W. A novel PGC-1alpha isoform in brain localizes to mitochondria and associates with PINK1 and VDAC. Biochem. Biophys. Res. Commun. 2013, 435:671-677.
16. Chowdhury S.K., Smith D.R., Fernyhough P. The role of aberrant mitochondrial bioenergetics in diabetic neuropathy. Neurobiol. Dis. 2013, 56-65.
17. Christianson J.A., Riekhof J.T., Wright D.E. Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice. Exp. Neurol. 2003, 179:188-199.
18. Coppey L.J., Davidson E.P., Rinehart T.W., Gellett J.S., Oltman C.L., Lund D.D., et al. ACE inhibitor or angiotensin II receptor antagonist attenuates diabetic neuropathy in streptozotocin-induced diabetic rats. Diabetes 2006, 55:341-348.
19. Cowell R.M., Blake K.R., Russell J.W. Localization of the transcriptional coactivator PGC-1alpha to GABAergic neurons during maturation of the rat brain. J. Comp. Neurol. 2007, 502:1-18.
20. Cowell R.M., Talati P., Blake K.R., Meador-Woodruff J.H., Russell J.W. Identification of novel targets for PGC-1alpha and histone deacetylase inhibitors in neuroblastoma cells. Biochem. Biophys. Res. Commun. 2009, 379:578-582.
21. Esterbauer H., Oberkofler H., Krempler F., Patsch W. Human peroxisome proliferator activated receptor gamma coactivator 1 (PPARGC1) gene: cDNA sequence, genomic organization, chromosomal localization, and tissue expression. Genomics 1999, 62:98-102.
22. Finkel T. Cell biology: a clean energy programme. Nature 2006, 444:151-152.
23. He L., Chinnery P.F., Durham S.E., Blakely E.L., Wardell T.M., Borthwick G.M., et al. Detection and quantification of mitochondrial DNA deletions in individual cells by real-time PCR. Nucleic Acids Res. 2002, 30:e68.
24. Heilbronn L.K., Gregersen S., Shirkhedkar D., Hu D., Campbell L.V. Impaired fat oxidation after a single high-fat meal in insulin-sensitive nondiabetic individuals with a family history of type 2 diabetes. Diabetes 2007, 56:2046-2053.
25. Ho E.C., Lam K.S., Chen Y.S., Yip J.C., Arvindakshan M., Yamagishi S., et al. Aldose reductase-deficient mice are protected from delayed motor nerve conduction velocity, increased c-Jun NH2-terminal kinase activation, depletion of reduced glutathione, increased superoxide accumulation, and DNA damage. Diabetes 2006, 55:1946-1953.
26. Huang T.J., Price S.A., Chilton L., Calcutt N.A., Tomlinson D.R., Verkhratsky A., et al. Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes 2003, 52:2129-2136.
27. Johri A., Calingasan N.Y., Hennessey T.M., Sharma A., Yang L., Wille E., et al. Pharmacologic activation of mitochondrial biogenesis exerts widespread beneficial effects in a transgenic mouse model of Huntington's disease. Hum. Mol. Genet. 2012, 21:1124-1137.
28. Kelly D.P., Scarpulla R.C. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004, 18:357-368.
29. Kishi M., Tanabe J., Schmelzer J.D., Low P.A. Morphometry of dorsal root ganglion in chronic experimental diabetic neuropathy. Diabetes 2002, 51:819-824.
30. Kleiner S., Mepani R.J., Laznik D., Ye L., Jurczak M.J., Jornayvaz F.R., et al. Development of insulin resistance in mice lacking PGC-1alpha in adipose tissues. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:9635-9640.
31. Lauria G., Cornblath D.R., Johansson O., McArthur J.C., Mellgren S.I., Nolano M., et al. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur. J. Neurol. 2005, 12:747-758.
32. Lauria G., Lombardi R., Borgna M., Penza P., Bianchi R., Savino C., et al. Intraepidermal nerve fiber density in rat foot pad: neuropathologic-neurophysiologic correlation. J. Peripher. Nerv. Syst. 2005, 10:202-208.
33. Lehman J.J., Barger P.M., Kovacs A., Saffitz J.E., Medeiros D.M., Kelly D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 2000, 106:847-856.
34. Leone T.C., Lehman J.J., Finck B.N., Schaeffer P.J., Wende A.R., Boudina S., et al. PGC-1α deficient mice exhibit multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control, and hepatic steatosis. PLoS Biol. 2005, e101. ([epub]).
35. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002, 418:797-801.
36. Lin J., Wu P.H., Tarr P.T., Lindenberg K.S., St Pierre J., Zhang C.Y., et al. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 2004, 119:125-135. ([see comment]).
37. Mallon P.W., Unemori P., Sedwell R., Morey A., Rafferty M., Williams K., et al. In vivo, nucleoside reverse-transcriptase inhibitors alter expression of both mitochondrial and lipid metabolism genes in the absence of depletion of mitochondrial DNA. J. Infect. Dis. 2005, 191:1686-1696.
38. Martin-Gallan P., Carrascosa A., Gussinye M., Dominguez C. Biomarkers of diabetes-associated oxidative stress and antioxidant status in young diabetic patients with or without subclinical complications. Free Radic. Biol. Med. 2003, 34:1563-1574.
39. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34(3):267-273. ([see comment]).
40. Nystrom T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 2005, 24:1311-1317.
41. Obrosova I.G. How does glucose generate oxidative stress in peripheral nerve?. Int. Rev. Neurobiol. 2002, 50:3-35.
42. Obrosova I.G., Pacher P., Szabo C., Zsengeller Z., Hirooka H., Stevens M.J., et al. Aldose reductase inhibition counteracts oxidative-nitrosative stress and poly(ADP-ribose) polymerase activation in tissue sites for diabetes complications. Diabetes 2005, 54:234-242.
43. Patti M.E., Butte A.J., Crunkhorn S., Cusi K., Berria R., Kashyap S., et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:8466-8471.
44. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24:78-90.
45. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
46. Roy Chowdhury S.K., Smith D.R., Saleh A., Schapansky J., Marquez A., Gomes S., et al. Impaired adenosine monophosphate-activated protein kinase signalling in dorsal root ganglia neurons is linked to mitochondrial dysfunction and peripheral neuropathy in diabetes. Brain 2012, 135:1751-1766.
47. Russell J.W., Sullivan K.A., Windebank A.J., Herrmann D.N., Feldman E.L. Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol. Dis. 1999, 6:347-363.
48. Russell J.W., Golovoy D., Vincent A.M., Mahendru P., Olzmann J.A., Mentzer A., et al. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB 2002, 16:1738-1748.
49. Russell J.W., Berent-Spillson A., Vincent A.M., Freimann C.L., Sullivan K.A., Feldman E.L. Oxidative injury and neuropathy in diabetes and impaired glucose tolerance. Neurobiol. Dis. 2008, 30:420-429.
50. Sasaki H., Schmelzer J.D., Zollman P.J., Low P.A. Neuropathology and blood flow of nerve, spinal roots and dorsal root ganglia in longstanding diabetic rats. Acta Neuropathol. 1997, 93:118-128.
51. Schuh R.A., Kristian T., Gupta R.K., Flaws J.A., Fiskum G. Methoxychlor inhibits brain mitochondrial respiration and increases hydrogen peroxide production and CREB phosphorylation. Toxicol. Sci. 2005, 88:495-504.
52. Smith A.G., Russell J.W., Feldman E.L., Goldstein J., Peltier A., Smith S., et al. Lifestyle intervention for prediabetic neuropathy. Diabetes Care 2006, 29:1294-1299.
53. Song Z., Fu D.T., Chan Y.S., Leung S., Chung S.S., Chung S.K. Transgenic mice overexpressing aldose reductase in Schwann cells show more severe nerve conduction velocity deficit and oxidative stress under hyperglycemic stress. Mol. Cell. Neurosci. 2003, 23:638-647.
54. Soyal S.M., Felder T.K., Auer S., Hahne P., Oberkofler H., Witting A., et al. A 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.
55. St Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 20(127):397-408.
56. Toth C., Rong L.L., Yang C., Martinez J., Song F., Ramji N., et al. Receptor for advanced glycation end products (RAGEs) and experimental diabetic neuropathy. Diabetes 2007, 57:1002-1017.
57. Turk Z. Glycotoxines, carbonyl stress and relevance to diabetes and its complications. Physiol. Res. 2009, 59:147-156.
58. Vincent A.M., Olzmann J.A., Brownlee M., Sivitz W.I., Russell J.W. Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 2004, 53:726-734.
59. Vincent A.M., Perrone L., Sullivan K.A., Backus C., Sastry A.M., Lastoskie C., et al. RAGE activation injures primary sensory neurons via oxidative stress. Endocrinology 2006, 148:548-558.
60. Vincent A.M., Perrone L., Sullivan K.A., Backus C., Sastry A.M., Lastoskie C., et al. Receptor for advanced glycation end products activation injures primary sensory neurons via oxidative stress. Endocrinology 2007, 148:548-558.
61. Vincent A.M., Russell J.W., Sullivan K.A., Backus C., Hayes J.M., McLean L.L., et al. SOD2 protects neurons from injury in cell culture and animal models of diabetic neuropathy. Exp. Neurol. 2007, 208:216-227.
62. Vincent A.M., Hayes J.M., McLean L.L., Vivekanandan-Giri A., Pennathur S., Feldman E.L. Dyslipidemia-induced neuropathy in mice: the role of oxLDL/LOX-1. Diabetes 2009, 58:2376-2385.
63. Vinik A. The protein kinase C-beta inhibitor, ruboxistaurin, for the treatment of diabetic microvascular complications. Expert Opin. Investig. Drugs 2005, 14:1547-1559.
64. Wiggin T.D., Sullivan K.A., Pop-Busui R., Amato A., Sima A.A., Feldman E.L. Elevated triglycerides correlate with progression of diabetic neuropathy. Diabetes 2009, 58:1634-1640.
65. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
66. Yagihashi S., Yamagishi S.I., Wada R.R., Baba M., Hohman T.C., Yabe-Nishimura C., et al. Neuropathy in diabetic mice overexpressing human aldose reductase and effects of aldose reductase inhibitor. Brain 2001, 124:2448-2458.
67. Yu X., Zhang L., Yang X., Huang H., Huang Z., Shi L., et al. Salvianolic acid A protects the peripheral nerve function in diabetic rats through regulation of the AMPK-PGC1alpha-Sirt3 axis. Molecules 2012, 17:11216-11228.