Inhibition of prolyl hydroxylases by dimethyloxaloylglycine after stroke reduces ischemic brain injury and requires hypoxia inducible factor-1α

Neurobiology of Disease

Volumn 45, Issue 2, 2012, Pages 733-742

  Ogle, Molly E ^a   Gu, Xiaohuan ^a   Espinera, Alyssa R ^a   Wei, Ling ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dimethyloxaloylglycine; Focal cerebral ischemia; Hypoxia inducible factor; Postconditioning; Preconditioning; Prolyl hydroxylase

Indexed keywords

ACRIFLAVINE; CASPASE 3; DIGOXIN; DIMETHYLOXALOYLGLYCINE; ENDOTHELIAL CELL GROWTH FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENZYME INHIBITOR; ERYTHROPOIETIN; GLYCINE DERIVATIVE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PYRUVATE DEHYDROGENASE KINASE; PYRUVATE DEHYDROGENASE KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN BLOOD FLOW; BRAIN CELL; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DOSE RESPONSE; DRUG TARGETING; ENOS GENE; ENZYME ACTIVATION; ENZYME INHIBITION; EPO GENE; GENE; GENE CONTROL; HIF 1ALPHA GENE; IN VITRO STUDY; IN VIVO STUDY; MARKER GENE; MIDDLE CEREBRAL ARTERY; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXYGEN SENSING; PDK 1 GENE; PDK 4 GENE; PRIORITY JOURNAL; RISK REDUCTION; STROKE; TRANSCRIPTION INITIATION; VEGF GENE;

AMINO ACIDS, DICARBOXYLIC; ANIMALS; BLOTTING, WESTERN; BRAIN; BRAIN ISCHEMIA; CELLS, CULTURED; CEREBROVASCULAR CIRCULATION; ENZYME INHIBITORS; GENE EXPRESSION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; LASER-DOPPLER FLOWMETRY; MICE; NEURONS; PROCOLLAGEN-PROLINE DIOXYGENASE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84855786346     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.10.020     Document Type: Article

References (60)

1. Abu-Amara M., Yang S.Y., Quaglia A., Rowley P., Fuller B., Seifalian A., Davidson B. Role of endothelial nitric oxide synthase in remote ischemic preconditioning of the mouse liver. Liver Transpl. 2011, 17:610-619.
2. American Heart Association Heart Disease and Stroke Statistics 2008, American Heart Association, Dallas, Texas, USA.
3. Aminova L.R., Chavez J.C., Lee J., Ryu H., Kung A., Lamanna J.C., Ratan R.R. Prosurvival and prodeath effects of hypoxia-inducible factor-1alpha stabilization in a murine hippocampal cell line. J. Biol. Chem. 2005, 280:3996-4003.
4. Aragones J., et al. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat. Genet. 2008, 40:170-180.
5. Baranova O., Miranda L.F., Pichiule P., Dragatsis I., Johnson R.S., Chavez J.C. Neuron-specific inactivation of the hypoxia inducible factor 1 alpha increases brain injury in a mouse model of transient focal cerebral ischemia. J. Neurosci. 2007, 27:6320-6332.
6. Bouet V., Freret T., Toutain J., Divoux D., Boulouard M., Schumann-Bard P. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp. Neurol. 2007, 203:555-567.
7. Bouet V., Boulouard M., Toutain J., Divoux D., Bernaudin M., Schumann-Bard P., Freret T. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat. Protoc. 2009, 4:1560-1564.
8. Broughton B.R., Reutens D.C., Sobey C.G. Apoptotic mechanisms after cerebral ischemia. Stroke 2009, 40:e331-e339.
9. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294:1337-1340.
10. Choi D.W., Maulucci-Gedde M., Kriegstein A.R. Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 1987, 7:357-368.
11. Coulet F., Nadaud S., Agrapart M., Soubrier F. Identification of hypoxia-response element in the human endothelial nitric-oxide synthase gene promoter. J. Biol. Chem. 2003, 278:46230-46240.
12. Cummins E.P., Berra E., Comerford K.M., Ginouves A., Fitzgerald K.T., Seeballuck F., Godson C., Nielsen J.E., Moynagh P., Pouyssegur J., Taylor C.T. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18154-18159.
13. Del Zoppo G.J., Sharp F.R., Heiss W.D., Albers G.W. Heterogeneity in the penumbra. J. Cereb. Blood Flow Metab. 2011, 31:1836-1851.
14. Digicaylioglu M., Lipton S.A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 2001, 412:641-647.
15. Epstein A.C., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54.
16. Fabricius M., Lauritzen M. Laser-Doppler evaluation of rat brain microcirculation: comparison with the [14C]-iodoantipyrine method suggests discordance during cerebral blood flow increases. J. Cereb. Blood Flow Metab. 1996, 16:156-161.
17. Farinelli S.E., Greene L.A., Friedman W.J. Neuroprotective actions of dipyridamole on cultured CNS neurons. J. Neurosci. 1998, 18:5112-5123.
18. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 1996, 16:4604-4613.
19. Freret T., Bouet V., Leconte C., Roussel S., Chazalviel L., Divoux D., Schumann-Bard P., Boulouard M. Behavioral deficits after distal focal cerebral ischemia in mice: usefulness of adhesive removal test. Behav. Neurosci. 2009, 123:224-230.
20. Gidday J.M., Fitzgibbons J.C., Shah A.R., Park T.S. Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci. Lett. 1994, 168:221-224.
21. Helton R., Cui J., Scheel J.R., Ellison J.A., Ames C., Gibson C., Blouw B., Ouyang L., Dragatsis I., Zeitlin S., Johnson R.S., Lipton S.A., Barlow C. Brain-specific knock-out of hypoxia-inducible factor-1alpha reduces rather than increases hypoxic-ischemic damage. J. Neurosci. 2005, 25:4099-4107.
22. Huang Z., Huang P.L., Ma J., Meng W., Ayata C., Fishman M.C., Moskowitz M.A. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J. Cereb. Blood Flow Metab. 1996, 16:981-987.
23. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001, 292:464-468.
24. Iyer N.V., Kotch L.E., Agani F., Leung S.W., Laughner E., Wenger R.H., Gassmann M., Gearhart J.D., Lawler A.M., Yu A.Y., Semenza G.L. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 1998, 12:149-162.
25. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., Kriegsheim A., Hebestreit H.F., Mukherji M., Schofield C.J., Maxwell P.H., Pugh C.W., Ratcliffe P.J. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292:468-472.
26. Jiang B.H., Semenza G.L., Bauer C., Marti H.H. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am. J. Physiol. 1996, 271:C1172-C1180.
27. Jin K.L., Mao X.O., Greenberg D.A. Vascular endothelial growth factor rescues HN33 neural cells from death induced by serum withdrawal. J. Mol. Neurosci. 2000, 14:197-203.
28. Jin K.L., Mao X.O., Greenberg D.A. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:10242-10247.
29. Kasiganesan H., Sridharan V., Wright G. Prolyl hydroxylase inhibitor treatment confers whole-animal hypoxia tolerance. Acta Physiol. 2007, 190:163-169.
30. Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3:177-185.
31. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe M., Handa N., Fukunaga R., Kimura K., Mikoshiba K., et al. 'Ischemic tolerance' phenomenon found in the brain. Brain Res. 1990, 528:21-24.
32. Lee K., Zhang H., Qian D.Z., Rey S., Liu J.O., Semenza G.L. Acriflavine inhibits HIF-1 dimerization, tumor growth, and vascularization. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17910-17915.
33. Li Y., Lu Z., Keogh C.L., Yu S.P., Wei L. Erythropoietin-induced neurovascular protection, angiogenesis, and cerebral blood flow restoration after focal ischemia in mice. J. Cereb. Blood Flow Metab. 2007, 27:1043-1054.
34. Li Y., Lu Z.Y., Ogle M., Wei L. Erythropoietin prevents blood brain barrier damage induced by focal cerebral ischemia in mice. Neurochem. Res. 2007, 32:2132-2141.
35. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 1999, 79:1431-1568.
36. Liu Y., Kato H., Nakata N., Kogure K. Protection of rat hippocampus against ischemic neuronal damage by pretreatment with sublethal ischemia. Brain Res. 1992, 586:121-124.
37. Liu X.B., Wang J.A., Ogle M.E., Wei L. Prolyl hydroxylase inhibitor dimethyloxalylglycine enhances mesenchymal stem cell survival. J. Cell. Biochem. 2009, 106(5):903-911.
38. Lomb D.J., Straub J.A., Freeman R.S. Prolyl hydroxylase inhibitors delay neuronal cell death caused by trophic factor deprivation. J. Neurochem. 2007, 103:1897-1906.
39. Martin E., Rosenthal R.E., Fiskum G. Pyruvate dehydrogenase complex: metabolic link to ischemic brain injury and target of oxidative stress. J. Neurosci. Res. 2005, 79:240-247.
40. Murphy T.H., Corbett D. Plasticity during stroke recovery: from synapse to behaviour. Nat. Rev. Neurosci. 2009, 10:861-872.
41. Paciaroni M., Caso V., Agnelli G. The concept of ischemic penumbra in acute stroke and therapeutic opportunities. Eur. Neurol. 2009, 61:321-330.
42. Palmer L.A., Semenza G.L., Stoler M.H., Johns R.A. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am. J. Physiol. 1998, 274:L212-L219.
43. Papandreou I., Cairns R.A., Fontana L., Lim A.L., Denko N.C. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 2006, 3:187-197.
44. Semenza G.L. Transcriptional regulation of gene expression: mechanisms and pathophysiology. Hum. Mutat. 1994, 3:180-199.
45. Siddiq A., Ayoub I.A., Chavez J.C., Aminova L., Shah S., LaManna J.C., Patton S.M., Connor J.R., Cherny R.A., Volitakis I., Bush A.I., Langsetmo I., Seeley T., Gunzler V., Ratan R.R. Hypoxia-inducible factor prolyl 4-hydroxylase inhibition. A target for neuroprotection in the central nervous system. J. Biol. Chem. 2005, 280:41732-41743.
46. Siddiq A., Aminova L.R., Troy C.M., Suh K., Messer Z., Semenza G.L., Ratan R.R. Selective inhibition of hypoxia-inducible factor (HIF) prolyl-hydroxylase 1 mediates neuroprotection against normoxic oxidative death via HIF- and CREB-independent pathways. J. Neurosci. 2009, 29:8828-8838.
47. Sigler A., Mohajerani M.H., Murphy T.H. Imaging rapid redistribution of sensory-evoked depolarization through existing cortical pathways after targeted stroke in mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11759-11764.
48. Sutter C.H., Laughner E., Semenza G.L. Hypoxia-inducible factor 1alpha protein expression is controlled by oxygen-regulated ubiquitination that is disrupted by deletions and missense mutations. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4748-4753.
49. Talukder M.A., Yang F., Shimokawa H., Zweier J.L. eNOS is required for acute in vivo ischemic preconditioning of the heart: effects of ischemic duration and sex. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H437-H445.
50. Wang G.L., Semenza G.L. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J. Biol. Chem. 1993, 268:21513-21518.
51. Wang G.L., Semenza G.L. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 1993, 82:3610-3615.
52. Wang G.L., Semenza G.L. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:4304-4308.
53. Wang G.L., Semenza G.L. Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 1995, 270:1230-1237.
54. Wei L., Rovainen C.M., Woolsey T.A. Ministrokes in rat barrel cortex. Stroke 1995, 26:1459-1462.
55. Whitaker V.R., Cui L., Miller S., Yu S.P., Wei L. Whisker stimulation enhances angiogenesis in the barrel cortex following focal ischemia in mice. J. Cereb. Blood Flow Metab. 2007, 27:57-68.
56. Wick A., Wick W., Waltenberger J., Weller M., Dichgans J., Schulz J.B. Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J. Neurosci. 2002, 22:6401-6407.
57. Yoshida T., Zhang H., Iwase T., Shen J., Semenza G.L., Campochiaro P.A. Digoxin inhibits retinal ischemia-induced HIF-1alpha expression and ocular neovascularization. FASEB J. 2010, 24:1759-1767.
58. Zaman K., Ryu H., Hall D., O'Donovan K., Lin K.I., Miller M.P., Marquis J.C., Baraban J.M., Semenza G.L., Ratan R.R. Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J. Neurosci. 1999, 19:9821-9830.
59. Zhang S.X., Gozal D., Sachleben L.R., Rane M., Klein J.B., Gozal E. Hypoxia induces an autocrine-paracrine survival pathway via platelet-derived growth factor (PDGF)-B/PDGF-beta receptor/phosphatidylinositol 3-kinase/Akt signaling in RN46A neuronal cells. FASEB J. 2003, 17:1709-1711.
60. Zhang H., Qian D.Z., Tan Y.S., Lee K., Gao P., Ren Y.R., Rey S., Hammers H., Chang D., Pili R., Dang C.V., Liu J.O., Semenza G.L. Digoxin and other cardiac glycosides inhibit HIF-1alpha synthesis and block tumor growth. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19579-19586.