Methylene blue-induced neuronal protective mechanism against hypoxia-reoxygenation stress

Neuroscience

Volumn 301, Issue , 2015, Pages 193-203

  Ryou, M G ^a   Choudhury, G R ^a   Li, W ^a   Winters, A ^a   Yuan, F ^b   Liu, R ^a   Yang, S H ^a,b  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Hypoxia inducible factor; Ischemia and reperfusion injury; Methylene blue; Neuroprotection; Oxygen and glucose deprivation

Indexed keywords

2 (N (7 NITROBENZ 2 OXA 1,3 DIAZOL 4 YL)AMINO) 2 DEOXY GLUCOSE; 2 METHOXYESTRADIOL; ADENOSINE TRIPHOSPHATE; DEOXYGLUCOSE; ERYTHROPOIETIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLYCOLYTIC ENZYME; HEXOKINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; METHYLENE BLUE; OXYGENASE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PROLYL HYDROXYLASE 2; PROTEIN KINASE B; UNCLASSIFIED DRUG; GLUCOSE; NEUROPROTECTIVE AGENT; OXYGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN HYPOXIA; CALCEIN-AM ASSAY; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE MICROSCOPY; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; IMMUNOBLOTTING; IN VITRO STUDY; NEUROPROTECTION; NONHUMAN; OXYGEN CONCENTRATION; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; REOXYGENATION; SIGNAL TRANSDUCTION; SPECTROPHOTOMETRY; ANIMAL; C57BL MOUSE; CELL HYPOXIA; CELL LINE; CYTOLOGY; DRUG EFFECTS; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; METABOLISM; PHYSIOLOGICAL STRESS; REPERFUSION INJURY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL HYPOXIA; CELL LINE; GLUCOSE; HIPPOCAMPUS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-ISCHEMIA, BRAIN; METHYLENE BLUE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; OXYGEN; REPERFUSION INJURY; STRESS, PHYSIOLOGICAL;

EID: 84931275214     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.05.064     Document Type: Article

References (59)

1. Auchter A., Williams J., Barksdale B., Monfils M.H., Gonzalez-Lima F. Therapeutic benefits of methylene blue on cognitive impairment during chronic cerebral hypoperfusion. J Alzheimer Dis 2014, 42:S525-535.
2. Audet J.N., Soucy G., Julien J.P. Methylene blue administration fails to confer neuroprotection in two amyotrophic lateral sclerosis mouse models. Neuroscience 2012, 209:136-143.
3. Bergmeyer H.-U. Methods of enzymatic analysis 1983, Academic Press, New York.
4. Boylston M., Beer D. Methemoglobinemia: a case study. Crit Care Nurse 2002, 22:50-55.
5. Chen R.L., et al. HIF prolyl hydroxylase inhibition prior to transient focal cerebral ischaemia is neuroprotective in mice. J Neurochem 2014.
6. Cheng G., Kong R.H., Zhang L.M., Zhang J.N. Mitochondria in traumatic brain injury and mitochondrial-targeted multipotential therapeutic strategies. Br J Pharmacol 2012, 167:699-719.
7. Curtis V.F., et al. Stabilization of HIF through inhibition of Cullin-2 neddylation is protective in mucosal inflammatory responses. FASEB J 2014.
8. Demidenko Z.N., Blagosklonny M.V. The purpose of the HIF-1/PHD feedback loop: to limit mTOR-induced HIF-1alpha. Cell Cycle (Georgetown, Tex.) 2011, 10:1557-1562.
9. Dioum E.M., Clarke S.L., Ding K., Repa J.J., Garcia J.A. HIF-2alpha-haploinsufficient mice have blunted retinal neovascularization due to impaired expression of a proangiogenic gene battery. Invest Ophthalmol Vis Sci 2008, 49:2714-2720.
10. Dioum E.M., et al. Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science 2009, 324:1289-1293.
11. Elias-Miro M., Jimenez-Castro M.B., Rodes J., Peralta C. Current knowledge on oxidative stress in hepatic ischemia/reperfusion. Free Radical Res 2013, 47:555-568.
12. Fang M.C., Perraillon M.C., Ghosh K., Cutler D.M., Rosen A.B. Trends in stroke rates, risk, and outcomes in the United States, 1988-2008. Am J Med 2014.
13. Forsythe J.A., et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996, 16:4604-4613.
14. Funaki M., DiFransico L., Janmey P.A. PI 4,5-P2 stimulates glucose transport activity of GLUT4 in the plasma membrane of 3T3-L1 adipocytes. Biochim Biophys Acta 2006, 1763:889-899.
15. Garcia-Martinez J.M., et al. Ku-0063794 is a specific inhibitor of the mammalian target of rapamycin (mTOR). Biochem J 2009, 421:29-42.
16. Green A.R. Pharmacological approaches to acute ischaemic stroke: reperfusion certainly, neuroprotection possibly. Br J Pharmacol 2008, 153(Suppl. 1):S325-338.
17. Guzy R.D., et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 2005, 1:401-408.
18. Hacke W., et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008, 359:1317-1329.
19. Halstead J.R., et al. A role for PtdIns(4,5)P2 and PIP5Kalpha in regulating stress-induced apoptosis. Curr Biol 2006, 16:1850-1856.
20. Harada H., et al. The Akt/mTOR pathway assures the synthesis of HIF-1alpha protein in a glucose- and reoxygenation-dependent manner in irradiated tumors. J Biol Chem 2009, 284:5332-5342.
21. Hudson C.C., et al. Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol 2002, 22:7004-7014.
22. Kleikers P.W., et al. NADPH oxidases as a source of oxidative stress and molecular target in ischemia/reperfusion injury. J Mol Med (Berlin, Germany) 2012, 90:1391-1406.
23. Kwok E.S., Howes D. Use of methylene blue in sepsis: a systematic review. J Intensive Care Med 2006, 21:359-363.
24. Leontieva O.V., Blagosklonny M.V. M(o)TOR of pseudo-hypoxic state in aging: rapamycin to the rescue. Cell Cycle (Georgetown, Tex.) 2014, 13:509-515.
25. Lin A.L., et al. Methylene blue as a cerebral metabolic and hemodynamic enhancer. PLoS ONE 2012, 7:e46585.
26. Lu H., Forbes R.A., Verma A. Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem 2002, 277:23111-23115.
27. Lu H., et al. Reversible inactivation of HIF-1 prolyl hydroxylases allows cell metabolism to control basal HIF-1. J Biol Chem 2005, 280:41928-41939.
28. Mabjeesh N.J., et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003, 3:363-375.
29. Majmundar A.J., Wong W.J., Simon M.C. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 2010, 40:294-309.
30. Mansfield K.D., et al. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 2005, 1:393-399.
31. Marti H.H. Erythropoietin and the hypoxic brain. J Exp Biol 2004, 207:3233-3242.
32. Maxwell P.H., Ratcliffe P.J. Oxygen sensors and angiogenesis. Semin Cell Dev Biol 2002, 13:29-37.
33. Meissner P.E., et al. Methylene blue for malaria in Africa: results from a dose-finding study in combination with chloroquine. Malar J 2006, 5:84.
34. Mi C., et al. 4',6-dihydroxy-4-methoxyisoaurone inhibits the HIF-1alpha pathway through inhibition of Akt/mTOR/p70S6K/4E-BP1 phosphorylation. J Pharmacol Sci 2014, 125:193-201.
35. Niecknig H., et al. Role of reactive oxygen species in the regulation of HIF-1 by prolyl hydroxylase 2 under mild hypoxia. Free Radical Res 2012, 46:705-717.
36. O'Collins V.E., et al. 1,026 experimental treatments in acute stroke. Ann Neurol 2006, 59:467-477.
37. O'Leary J.L., Petty J., Harris A.B., Inukai J. Supravital staining of mammalian brain with intra-arterial methylene blue followed by pressurized oxygen. Stain Technol 1968, 43:197-201.
38. Olsen J.M., et al. Glucose uptake in brown fat cells is dependent on mTOR complex 2-promoted GLUT1 translocation. J Cell Biol 2014, 207:365-374.
39. Ong S.G., et al. HIF-1 reduces ischaemia-reperfusion injury in the heart by targeting the mitochondrial permeability transition pore. Cardiovasc Res 2014, 104:24-36.
40. Park S.H., et al. GABARBP down-regulates HIF-1alpha expression through the VEGFR-2 and PI3K/mTOR/4E-BP1 pathways. Cell Signal 2014, 26:1506-1513.
41. Pientka F.K., et al. Oxygen sensing by the prolyl-4-hydroxylase PHD2 within the nuclear compartment and the influence of compartmentalisation on HIF-1 signalling. J. Cell Sci. 2012, 125:5168-5176.
42. Poteet E., et al. Neuroprotective actions of methylene blue and its derivatives. PLoS ONE 2012, 7:e48279.
43. Preiser J.C., et al. Methylene blue administration in septic shock: a clinical trial. Crit. Care Med. 1995, 23:259-264.
44. Ryou M.G., et al. Pyruvate-fortified cardioplegia evokes myocardial erythropoietin signaling in swine undergoing cardiopulmonary bypass. Am J Physiol 2009, 297:H1914-1922.
45. Ryou M.G., et al. Pyruvate protects the brain against ischemia-reperfusion injury by activating the erythropoietin signaling pathway. Stroke 2012, 43:1101-1107.
46. Ryou M.G., et al. Pyruvate minimizes rtPA toxicity from in vitro oxygen-glucose deprivation and reoxygenation. Brain Res 2013, 1530:66-75.
47. Schenk P., Madl C., Rezaie-Majd S., Lehr S., Muller C. Methylene blue improves the hepatopulmonary syndrome. Ann Intern Med 2000, 133:701-706.
48. Schirmer R.H., et al. Methylene blue as an antimalarial agent. Redox Rep 2003, 8:272-275.
49. Schofield C.J., Zhang Z. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Curr Opin Struct Biol 1999, 9:722-731.
50. Semenza G.L. Hypoxia-inducible factor 1 (HIF-1) pathway. Science's STKE 2007, 2007:cm8.
51. Semenza G.L., Wang G.L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992, 12:5447-5454.
52. Semenza G.L., Shimoda L.A., Prabhakar N.R. Regulation of gene expression by HIF-1. Novartis Found Symp 2006, 272:2-8. [discussion 8-14, 33-16].
53. Trollmann R., Richter M., Jung S., Walkinshaw G., Brackmann F. Pharmacologic stabilization of hypoxia-inducible transcription factors protects developing mouse brain from hypoxia-induced apoptotic cell death. Neuroscience 2014, 278:327-342.
54. Wang G.L., Jiang B.H., Rue E.A., Semenza G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995, 92:5510-5514.
55. Wen Y., et al. Alternative mitochondrial electron transfer as a novel strategy for neuroprotection. J Biol Chem 2011, 286:16504-16515.
56. Wondrak G.T. NQO1-activated phenothiazinium redox cyclers for the targeted bioreductive induction of cancer cell apoptosis. Free Radical Biol Med 2007, 43:178-190.
57. Zhang J., Ma W.Y. Nerve growth factor regulates the expression of vascular endothelial growth factor in human HaCaT keratinocytes via PI3K/mTOR pathway. Genet Mol Res 2014, 13.
58. Zhang P., et al. Hypoxia-inducible factor 3 is an oxygen-dependent transcription activator and regulates a distinct transcriptional response to hypoxia. Cell Rep 2014, 6:1110-1121.
59. Zhong H., et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 2000, 60:1541-1545.