Deletion or inhibition of the oxygen sensor PHD1 protects against ischemic stroke via reprogramming of neuronal metabolism

Cell Metabolism

Volumn 23, Issue 2, 2016, Pages 280-291

  Quaegebeur, Annelies ^a,b   Segura, Inmaculada ^a,b   Schmieder, Roberta ^a,b   Verdegem, Dries ^a,b   Decimo, Ilaria ^a,b   Bifari, Francesco ^a,b   Dresselaers, Tom ^c   Eelen, Guy ^a,b   Ghosh, Debapriva ^d   Davidson, Shawn M ^e   Schoors, Sandra ^a,b   Broekaert, Dorien ^a,b   Cruys, Bert ^a,b   Govaerts, Kristof ^c   De Legher, Carla ^a,b   Bouché, Ann ^a,b   Schoonjans, Luc ^a,b   Ramer, Matt S ^a,b,f   Hung, Gene ^g   Bossaert, Goele ^h   Cleveland, Don W ⁱ   Himmelreich, Uwe ^c   Voets, Thomas ^d   Lemmens, Robin ^a,b,j   Bennett, C Frank ^g   Robberecht, Wim ^a,b,j   De Bock, Katrien ^a,b,k   Dewerchin, Mieke ^a,b   Ghesquière, Bart ^b   Fendt, Sarah Maria ^a,b   Carmeliet, Peter ^a,b   more..

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^d LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g ISIS PHARMACEUTICALS   (United States)

^h Katholieke Universiteit Leuven   (Belgium)

ⁱ LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^j UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^k ETH ZURICH   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; OXYGEN RADICAL; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL HYDROXYLASE DOMAIN PROTEIN; UNCLASSIFIED DRUG; CARBON; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OLIGONUCLEOTIDE; OXYGEN; PHD1 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; SCAVENGER;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; BRAIN NERVE CELL; CARBON METABOLISM; CELL DEATH; CELL METABOLISM; CONTROLLED STUDY; DETOXIFICATION; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE OXIDATION; GLYCOLYSIS; HOMEOSTASIS; IN VITRO STUDY; MITOCHONDRION; MOUSE; NEUROPROTECTION; NONHUMAN; NUCLEAR REPROGRAMMING; OXYGEN CONSUMPTION; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; COMPLICATION; DEFICIENCY; DRUG EFFECTS; GENE DELETION; HYDROXYLATION; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; OXIDATION REDUCTION REACTION; PATHOLOGY; PHENOTYPE; STROKE; VASCULARIZATION;

ANIMALS; BRAIN; BRAIN ISCHEMIA; CARBON; CELLULAR REPROGRAMMING; FREE RADICAL SCAVENGERS; GENE DELETION; HYDROXYLATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INJECTIONS, INTRAVENTRICULAR; MICE, KNOCKOUT; NEURONS; NEUROPROTECTION; OLIGONUCLEOTIDES; OXIDATION-REDUCTION; OXYGEN; PENTOSE PHOSPHATE PATHWAY; PHENOTYPE; PROCOLLAGEN-PROLINE DIOXYGENASE; REACTIVE OXYGEN SPECIES; STROKE;

EID: 84957934688     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.12.007     Document Type: Article

References (41)

1. R.J. Appelhoff, Y.M. Tian, R.R. Raval, H. Turley, A.L. Harris, C.W. Pugh, P.J. Ratcliffe, and J.M. Gleadle Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor J. Biol. Chem. 279 2004 38458 38465
2. J. Aragonés, M. Schneider, K. Van Geyte, P. Fraisl, T. Dresselaers, M. Mazzone, R. Dirkx, S. Zacchigna, H. Lemieux, N.H. Jeoung, and et al. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism Nat. Genet. 40 2008 170 180
3. J. Aragonés, P. Fraisl, M. Baes, and P. Carmeliet Oxygen sensors at the crossroad of metabolism Cell Metab. 9 2009 11 22
4. J.E. Ayala, D.P. Bracy, O.P. McGuinness, and D.H. Wasserman Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse Diabetes 55 2006 390 397
5. J.B. Bederson, L.H. Pitts, S.M. Germano, M.C. Nishimura, R.L. Davis, and H.M. Bartkowski Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats Stroke 17 1986 1304 1308
6. K. Bensaad, A. Tsuruta, M.A. Selak, M.N. Vidal, K. Nakano, R. Bartrons, E. Gottlieb, and K.H. Vousden TIGAR, a p53-inducible regulator of glycolysis and apoptosis Cell 126 2006 107 120
7. V. Bouet, M. Boulouard, J. Toutain, D. Divoux, M. Bernaudin, P. Schumann-Bard, and T. Freret The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice Nat. Protoc. 4 2009 1560 1564
8. J.M. Buescher, M.R. Antoniewicz, L.G. Boros, S.C. Burgess, H. Brunengraber, C.B. Clish, R.J. DeBerardinis, O. Feron, C. Frezza, B. Ghesquiere, and et al. A roadmap for interpreting (13)C metabolite labeling patterns from cells Curr. Opin. Biotechnol. 34 2015 189 201
9. L. Cao, J. Chen, M. Li, Y.Y. Qin, M. Sun, R. Sheng, F. Han, G. Wang, and Z.H. Qin Endogenous level of TIGAR in brain is associated with vulnerability of neurons to ischemic injury Neurosci. Bull. 31 2015 527 540
10. P.H. Chan Reactive oxygen radicals in signaling and damage in the ischemic brain J. Cereb. Blood Flow Metab. 21 2001 2 14
11. R.L. Chen, S. Nagel, M. Papadakis, T. Bishop, P. Pollard, P.J. Ratcliffe, C.W. Pugh, and A.M. Buchan Roles of individual prolyl-4-hydroxylase isoforms in the first 24 hours following transient focal cerebral ischaemia: insights from genetically modified mice J. Physiol. 590 2012 4079 4091
12. G. D'Alessandro, E. Calcagno, S. Tartari, M. Rizzardini, R.W. Invernizzi, and L. Cantoni Glutamate and glutathione interplay in a motor neuronal model of amyotrophic lateral sclerosis reveals altered energy metabolism Neurobiol. Dis. 43 2011 346 355
13. R. Dringen Metabolism and functions of glutathione in brain Prog. Neurobiol. 62 2000 649 671
14. I.L. Ferreira, T. Cunha-Oliveira, M.V. Nascimento, M. Ribeiro, M.T. Proença, C. Januário, C.R. Oliveira, and A.C. Rego Bioenergetic dysfunction in Huntington's disease human cybrids Exp. Neurol. 231 2011 127 134
15. P. Fraisl, J. Aragonés, and P. Carmeliet Inhibition of oxygen sensors as a therapeutic strategy for ischaemic and inflammatory disease Nat. Rev. Drug Discov. 8 2009 139 152
16. A. Herrero-Mendez, A. Almeida, E. Fernández, C. Maestre, S. Moncada, and J.P. Bolaños The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1 Nat. Cell Biol. 11 2009 747 752
17. T. Krucker, A. Lang, and E.P. Meyer New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics Microsc. Res. Tech. 69 2006 138 147
18. M. Kuraoka, T. Furuta, T. Matsuwaki, T. Omatsu, Y. Ishii, S. Kyuwa, and Y. Yoshikawa Direct experimental occlusion of the distal middle cerebral artery induces high reproducibility of brain ischemia in mice Exp. Anim. 58 2009 19 29
19. J. Larson, K.L. Drew, L.P. Folkow, S.L. Milton, and T.J. Park No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates J. Exp. Biol. 217 2014 1024 1039
20. M. Li, M. Sun, L. Cao, J.H. Gu, J. Ge, J. Chen, R. Han, Y.Y. Qin, Z.P. Zhou, Y. Ding, and Z.H. Qin A TIGAR-regulated metabolic pathway is critical for protection of brain ischemia J. Neurosci. 34 2014 7458 7471
21. M.G. Martin, S. Perga, L. Trovò, A. Rasola, P. Holm, T. Rantamäki, T. Harkany, E. Castrén, F. Chiara, and C.G. Dotti Cholesterol loss enhances TrkB signaling in hippocampal neurons aging in vitro Mol. Biol. Cell 19 2008 2101 2112
22. C. Mauro, S.C. Leow, E. Anso, S. Rocha, A.K. Thotakura, L. Tornatore, M. Moretti, E. De Smaele, A.A. Beg, V. Tergaonkar, and et al. NF-κB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration Nat. Cell Biol. 13 2011 1272 1279
23. M. Mazzone, D. Dettori, R. Leite de Oliveira, S. Loges, T. Schmidt, B. Jonckx, Y.M. Tian, A.A. Lanahan, P. Pollard, C. Ruiz de Almodovar, and et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization Cell 136 2009 839 851
24. L.A. McNeill, K.S. Hewitson, J.M. Gleadle, L.E. Horsfall, N.J. Oldham, P.H. Maxwell, C.W. Pugh, P.J. Ratcliffe, and C.J. Schofield The use of dioxygen by HIF prolyl hydroxylase (PHD1) Bioorg. Med. Chem. Lett. 12 2002 1547 1550
25. B.P. Meloni, A.J. Meade, D. Kitikomolsuk, and N.W. Knuckey Characterisation of neuronal cell death in acute and delayed in vitro ischemia (oxygen-glucose deprivation) models J. Neurosci. Methods 195 2011 67 74
26. P. Mergenthaler, U. Lindauer, G.A. Dienel, and A. Meisel Sugar for the brain: the role of glucose in physiological and pathological brain function Trends Neurosci. 36 2013 587 597
27. M.A. Moskowitz, E.H. Lo, and C. Iadecola The science of stroke: mechanisms in search of treatments Neuron 67 2010 181 198
28. J. Myllyharju Prolyl 4-hydroxylases, master regulators of the hypoxia response Acta Physiol. (Oxf.) 208 2013 148 165
29. A. Oruganty-Das, T. Ng, T. Udagawa, E.L. Goh, and J.D. Richter Translational control of mitochondrial energy production mediates neuron morphogenesis Cell Metab. 16 2012 789 800
30. A. Quaegebeur, and P. Carmeliet Oxygen sensing: a common crossroad in cancer and neurodegeneration Curr. Top. Microbiol. Immunol. 345 2010 71 103
31. P. Rodriguez-Rodriguez, E. Fernandez, A. Almeida, and J.P. Bolaños Excitotoxic stimulus stabilizes PFKFB3 causing pentose-phosphate pathway to glycolysis switch and neurodegeneration Cell Death Differ. 19 2012 1582 1589
32. M. Schneider, K. van Geyte, P. Fraisl, J. Kiss, J. Aragones, M. Mazzone, H. Mairbaurl, K. Debock, N. Ho Jeoung, M. Mollenhauer, and et al. Loss or silencing of the PHD1 prolyl hydroxylase protects livers of mice against ischemia/referpusion injury Gastroenterology 138 2009 1143 1154
33. C.C. Scholz, and C.T. Taylor Hydroxylase-dependent regulation of the NF-κB pathway Biol. Chem. 394 2013 479 493
34. S. Schoors, U. Bruning, R. Missiaen, K.C. Queiroz, G. Borgers, I. Elia, A. Zecchin, A.R. Cantelmo, S. Christen, J. Goveia, and et al. Fatty acid carbon is essential for dNTP synthesis in endothelial cells Nature 520 2015 192 197
35. R.C. Stanton Glucose-6-phosphate dehydrogenase, NADPH, and cell survival IUBMB Life 64 2012 362 369
36. S.W. Suh, B.S. Shin, H. Ma, M. Van Hoecke, A.M. Brennan, M.A. Yenari, and R.A. Swanson Glucose and NADPH oxidase drive neuronal superoxide formation in stroke Ann. Neurol. 64 2008 654 663
37. A. Thathiah, K. Spittaels, M. Hoffmann, M. Staes, A. Cohen, K. Horré, M. Vanbrabant, F. Coun, V. Baekelandt, A. Delacourte, and et al. The orphan G protein-coupled receptor 3 modulates amyloid-beta peptide generation in neurons Science 323 2009 946 951
38. F. Tronche, C. Kellendonk, O. Kretz, P. Gass, K. Anlag, P.C. Orban, R. Bock, R. Klein, and G. Schütz Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety Nat. Genet. 23 1999 99 103
39. B.W. Wong, A. Kuchnio, U. Bruning, and P. Carmeliet Emerging novel functions of the oxygen-sensing prolyl hydroxylase domain enzymes Trends Biochem. Sci. 38 2013 3 11
40. J. Yao, R.W. Irwin, L. Zhao, J. Nilsen, R.T. Hamilton, and R.D. Brinton Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease Proc. Natl. Acad. Sci. USA 106 2009 14670 14675
41. G. Zhao, Y. Zhao, X. Wang, and Y. Xu Knockdown of glucose-6-phosphate dehydrogenase (G6PD) following cerebral ischemic reperfusion: the pros and cons Neurochem. Int. 61 2012 146 155