PPARγ stimulation promotes mitochondrial biogenesis and prevents glucose deprivation-induced neuronal cell loss

Neurochemistry International

Volumn 55, Issue 7, 2009, Pages 496-504

  Miglio, Gianluca ^a   Rosa, Arianna C ^a   Rattazzi, Lorenza ^a   Collino, Massimo ^a   Lombardi, Grazia ^b   Fantozzi, Roberto ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Mitochondrial biogenesis; Peroxisome proliferator activated receptor gamma; PGC 1 ; Pioglitazone; Rosiglitazone; SH SY5Y neuroblastoma cells

Indexed keywords

CYTOCHROME C OXIDASE; GLUCOSE; MALONIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PIOGLITAZONE; PYRUVIC ACID; ROSIGLITAZONE; SUCCINATE DEHYDROGENASE (UBIQUINONE); TRANSCRIPTION FACTOR NRF1; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; MALONIC ACID DERIVATIVE; MITOCHONDRIAL DNA; NEUROPROTECTIVE AGENT;

ARTICLE; BIOGENESIS; CELL LOSS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DATA ANALYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NERVE CELL; NEUROLOGIC DISEASE; NEUROPROTECTION; PRIORITY JOURNAL; UPREGULATION; BIOSYNTHESIS; CELL DEATH; CELL MEMBRANE POTENTIAL; DRUG EFFECT; DRUG POTENTIATION; GENETICS; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STIMULATION; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL DEATH; CELL LINE, TUMOR; DNA, MITOCHONDRIAL; GLUCOSE; HUMANS; HYPOGLYCEMIC AGENTS; MALONATES; MEMBRANE POTENTIALS; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; PPAR GAMMA; PYRUVIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STIMULATION, CHEMICAL; THIAZOLIDINEDIONES;

EID: 69349091599     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2009.05.001     Document Type: Article

References (51)

1. Aoun P., Watson D.G., and Simpkins J.W. Neuroprotective effects of PPARgamma agonists against oxidative insults in HT-22 cells. Eur. J. Pharmacol. 472 (2003) 65-71
2. Ballesteros J.R., Mishra O.P., and McGowan J.E. Alterations in cerebral mitochondria during acute hypoglycemia. Biol. Neonat. 84 (2003) 159-163
3. Beal M.F. Energetics in the pathogenesis of neurodegenerative diseases. Trends Neurosci. 23 (2005) 298-304
4. Beal M.F., Brouillet E., Jenkins B., Henshaw R., Rosen B., and Hyman B.T. Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J. Neurochem. 61 (1993) 1147-1150
5. Berger J., and Moller D.E. The mechanisms of action of PPARs. Annu. Rev. Med. 53 (2002) 409-435
6. Breidert T., Callebert J., Heneka M.T., Landreth G., Launay J.M., and Hirsch E.C. Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J. Neurochem. 82 (2002) 615-624
7. Budde K., Neumayer H.H., Fritsche L., Sulowicz W., Stompôr T., and Eckland D. The pharmacokinetics of pioglitazone in patients with impaired renal function. Br. J. Clin. Pharmacol. 55 (2003) 368-374
8. Colca J.R., McDonald W.G., Waldon D.J., Leone J.W., Lull J.M., Bannow C.A., Lund E.T., and Mathews W.R. Identification of a novel mitochondrial protein ("mitoNEET") cross-linked specifically by a thiazolidinedione photoprobe. Am. J. Physiol. Endocrinol. Metab. 286 (2004) E252-E260
9. Culman J., Zhao Y., Gohlke P., and Herdegen T. PPAR-gamma: therapeutic target for ischemic stroke. Trends Pharmacol. Sci. 28 (2007) 244-249
10. de la Monte S.M., and Wands J.R. Molecular indices of oxidative stress and mitochondrial dysfunction occur early and often progress with severity of Alzheimer's disease. J. Alzheimers Dis. 9 (2006) 167-181
11. Dehmer T., Heneka M.T., Sastre M., Dichgans J., and Schulz J.B. Protection by pioglitazone in the MPTP model of Parkinson's disease correlates with I kappa B alpha induction and block of NF kappa B and iNOS activation. J. Neurochem. 88 (2004) 494-501
12. Dello Russo C., Gavrilyuk V., Weinberg G., Almeida A., Bolanos J.P., Palmer J., Pelligrino D., Galea E., and Feinstein D.L. Peroxisome proliferator-activated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. J. Biol. Chem. 278 (2003) 5828-5836
13. Fuenzalida K., Quintanilla R., Ramos P., Piderit D., Fuentealba R.A., Martinez G., Inestrosa N.C., and Bronfman M. Peroxisome proliferator-activated receptor gamma up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J. Biol. Chem. 282 (2007) 37006-37015
14. Fujisawa K., Nishikawa T., Kukidome D., Imoto K., Yamashiro T., Motoshima H., Matsumura T., and Araki E. TZDs reduce mitochondrial ROS production and enhance mitochondrial biogenesis. Biochem. Biophys. Res. Commun. 379 (2009) 43-48
15. Ghosh S., Patel N., Rahn D., McAllister J., Sadeghi S., Horwitz G., Berry D., Wang K.X., and Swerdlow R.H. The thiazolidinedione pioglitazone alters mitochondrial function in human neuron-like cells. Mol. Pharmacol. 71 (2007) 1695-1702
16. Gomez-Lazaro M., Galindo M.F., Melero-Fernandez de Mera R.M., Fernandez-Gómez F.J., Concannon C.G., Segura M.F., Comella J.X., Prehn J.H., and Jordan J. Reactive oxygen species and p38 mitogen-activated protein kinase activate Bax to induce mitochondrial cytochrome c release and apoptosis in response to malonate. Mol. Pharmacol. 71 (2007) 736-743
17. Hondares E., Mora O., Yubero P., Rodriguez de la Concepción M., Iglesias R., Giralt M., and Villarroya F. Thiazolidinediones and rexinoids induce peroxisome proliferator-activated receptor-coactivator (PGC)-1alpha gene transcription: an autoregulatory loop controls PGC-1alpha expression in adipocytes via peroxisome proliferator-activated receptor-gamma coactivation. Endocrinology 147 (2006) 2829-2838
18. Jung T.W., Lee J.Y., Shim W.S., Kang E.S., Kim S.K., Ahn C.W., Lee H.C., and Cha B.S. Rosiglitazone protects human neuroblastoma SH-SY5Y cells against MPP+ induced cytotoxicity via inhibition of mitochondrial dysfunction and ROS production. J. Neurol. Sci. 253 (2007) 53-60
19. Kauppinen R.A., and Nicholls D.G. Synaptosomal bioenergetics. The role of glycolysis, pyruvate oxidation and responses to hypoglycaemia. Eur. J. Biochem. 158 (1986) 159-165
20. Kiaei M., Kipiani K., Chen J., Calingasan N.Y., and Beal M.F. Peroxisome proliferator-activated receptor-gamma agonist extends survival in transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 191 (2005) 331-336
21. Kim E.J., Park K.S., Chung S.Y., Sheen Y.Y., Moon D.C., Song Y.S., Kim K.S., Song S., Yun Y.P., Lee M.K., Oh K.W., Yoon D.Y., and Hong J.T. Peroxisome proliferator-activated receptor-gamma activator 15-deoxy-delta12,14-prostaglandin J2 inhibits neuroblastoma cell growth through induction of apoptosis: association with extracellular signal-regulated kinase signal pathway. J. Pharmacol. Exp. Ther. 307 (2003) 505-517
22. Kobayashi K., Xin Y., Ymer S.I., Werther G.A., and Russo V.C. Subtractive hybridisation screen identifies genes regulated by glucose deprivation in human neuroblastoma cells. Brain Res. 1170 (2007) 129-139
23. Kögel D., Svensson B., Copanaki E., Anguissola S., Bonner C., Thurow N., Gudorf D., Hetschko H., Müller T., Peters M., König H.G., and Prehn J.H. Induction of transcription factor CEBP homology protein mediates hypoglycaemia-induced necrotic cell death in human neuroblastoma cells. J. Neurochem. 99 (2006) 952-964
24. Maeshiba Y., Kiyota Y., Yamashita K., Yoshimura Y., Motohashi M., and Tanayama S. Disposition of the new antidiabetic agent pioglitazone in rats, dogs, and monkeys. Arzneimittelforschung 47 (1997) 29-35
25. Moreno S., Farioli-Vecchioli S., and Cerù M.P. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience 123 (2004) 131-145
26. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
27. Nicholls D.G., and Budd S.L. Mitochondria and neuronal survival. Physiol. Rev. 80 (2000) 315-360
28. Niemi M., Backman J.T., and Neuvonen P.J. Effects of trimethoprim and rifampin on the pharmacokinetics of the cytochrome P450 2C8 substrate rosiglitazone. Clin. Pharmacol. Ther. 76 (2004) 239-249
29. Nisoli E., Clementi E., Paolucci C., Cozzi V., Tonello C., Sciorati C., Bracale R., Valerio A., Francolini M., Moncada S., and Carruba M.O. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299 (2003) 896-899
30. Paddock M.L., Wiley S.E., Axelrod H.L., Cohen A.E., Roy M., Abresch E.C., Capraro D., Murphy A.N., Nechushtai R., Dixon J.E., and Jennings P.A. MitoNEET is a uniquely folded 2Fe2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 14342-21437
31. Pagel-Langenickel I., Bao J., Joseph J.J., Schwartz D.R., Mantell B.S., Xu X., Raghavachari N., and Sack M.N. PGC-1α integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J. Biol. Chem. 283 (2008) 22464-22472
32. Puigserver P., and Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 4 (2003) 78-90
33. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., and Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 (1998) 829-839
34. Rao K.V., and Norenberg M.D. Manganese induces the mitochondrial permeability transition in cultured astrocytes. J. Biol. Chem. 279 (2004) 32333-32338
35. Rong J.X., Qiu Y., Hansen M.K., Zhu L., Zhang V., Xie M., Okamoto Y., Mattie M.D., Higashiyama H., Asano S., Strum J.C., and Ryan T.E. Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone. Diabetes 56 (2007) 1751-1760
36. Russo V.C., Kobayashi K., Najdovska S., Baker N.L., and Werther G.A. Neuronal protection from glucose deprivation via modulation of glucose transport and inhibition of apoptosis: a role for the insulin-like growth factor system. Brain Res. 1009 (2004) 40-53
37. Sakamoto J., Kimura H., Moriyama S., Odaka H., Momose Y., Sugiyama Y., and Sawada H. Activation of human peroxisome proliferator-activated receptor (PPAR) subtypes by pioglitazone. Biochem. Biophys. Res. Commun. 278 (2000) 704-711
38. Schütz B., Reimann J., Dumitrescu-Ozimek L., Kappes-Horn K., Landreth G.E., Schürmann B., Zimmer A., and Heneka M.T. The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosis-like symptoms in superoxide dismutase-G93A transgenic mice. J. Neurosci. 25 (2005) 7805-7812
39. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jäger S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., and Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127 (2006) 397-408
40. Strum J.C., Shehee R., Virley D., Richardson J., Mattie M., Selley P., Ghosh S., Nock C., Saunders A., and Roses A. Rosiglitazone induces mitochondrial biogenesis in mouse brain. J. Alzheimers Dis. 11 (2007) 45-51
41. Suh S.W., Gum E.T., Hamby A.M., Chan P.H., and Swanson R.A. Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J. Clin. Invest. 117 (2007) 910-918
42. Suh S.W., Hamby A.M., and Swanson R.A. Hypoglycemia, brain energetics, and hypoglycemic neuronal death. Glia 55 (2007) 1280-1286
43. Valentiner U., Carlsson M., Erttmann R., Hildebrandt H., and Schumacher U. Ligands for the peroxisome proliferator-activated receptor-gamma have inhibitory effects on growth of human neuroblastoma cells in vitro. Toxicology 213 (2005) 157-168
44. White R.J., and Reynolds I.J. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16 (1996) 5688-5697
45. Willson T.M., Cobb J.E., Cowan D.J., Wiethe R.W., Correa I.D., Prakash S.R., Beck K.D., Moore L.B., Kliewer S.A., and Lehmann J.M. The structure-activity relationship between peroxisome proliferator-activated receptor gamma agonism and the antihyperglycemic activity of thiazolidinediones. J. Med. Chem. 39 (1996) 665-668
46. Wilson-Fritch L., Nicoloro S., Chouinard M., Lazar M.A., Chui P.C., Leszyk J., Straubhaar J., Czech M.P., and Corvera S. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114 (2004) 1281-1289
47. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., and Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98 (1999) 115-124
48. + levels dictate cell survival. Cell 130 (2007) 1095-1107
49. Yki-Järvinen H. Thiazolidinediones. N. Engl. J. Med. 351 (2004) 1106-1118
50. Zhao Y., Patzer A., Herdegen T., Gohlke P., and Culman J. Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats. FASEB J. 20 (2006) 1162-1175
51. Zimmermann M., Gardoni F., Marcello E., Colciaghi F., Borroni B., Padovani A., Cattabeni F., and Di Luca M. Acetylcholinesterase inhibitors increase ADAM10 activity by promoting its trafficking in neuroblastoma cell lines. J. Neurochem. 90 (2004) 1489-1499