Neurometabolic mechanisms for memory enhancement and neuroprotection of methylene blue

Progress in Neurobiology

Volumn 96, Issue 1, 2012, Pages 32-45

  Rojas, Julio C ^a   Bruchey, Aleksandra K ^a   Gonzalez Lima, F ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cytochrome oxidase; Memory; Methylene blue; Methylthioninium chloride; Mitochondria; Neuroprotection

Indexed keywords

METHYLENE BLUE; ROTENONE; SCOPOLAMINE;

BRAIN DAMAGE; BRAIN DISEASE; CELL RESPIRATION; DOSE RESPONSE; DRUG MECHANISM; DRUG RESPONSE; DRUG STRUCTURE; ENZYME ACTIVITY; HUMAN; IN VIVO STUDY; LOW DRUG DOSE; MEMORY; METABOLIC CAPACITY; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OPTIC NERVE DISEASE; PRIORITY JOURNAL; REVIEW; SPATIAL MEMORY; STRIATAL NEURODEGENERATION;

ANIMALS; ANTIOXIDANTS; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MEMORY; METHYLENE BLUE; MOLECULAR STRUCTURE; NEUROPROTECTIVE AGENTS; NOOTROPIC AGENTS; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 82655179828     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2011.10.007     Document Type: Review

References (124)

1. Allexsaht W.J. The use of methylene blue in the treatment of catatonic dementia praecox patients. Psychiat. Quart. 1938, 12:245-252.
2. Andresen M., Dougnac A., Diaz O., Hernandez G., Castillo L., Bugedo G., et al. Use of methylene blue in patients with refractory septic shock: impact on hemodynamics and gas exchange. J. Crit. Care 1998, 13:164-168.
3. Arieff A.J., Pyzik S.W. Quadriplegia after intrathecal injection of methylene blue. J. Am. Med. Assoc. 1960, 173:794-796.
4. Artuch R., Aracil A., Mas A., Monros E., Vilaseca M.A., Pineda M. Cerebrospinal fluid concentrations of idebenone in Friedreich ataxia patients. Neuropediatrics 2004, 35:95-98.
5. Atamna H. Amino acids variations in amyloid-beta peptides, mitochondrial dysfunction, and new therapies for Alzheimer's disease. J. Bioenerg. Biomembr. 2009, 41:457-464.
6. Atamna H., Nguyen A., Schultz C., Boyle K., Newberry J., Kato H., et al. Methylene blue delays cellular senescence and enhances key mitochondrial biochemical pathways. FASEB J. 2008, 22:703-712.
7. Atlante A., Amadoro G., Bobba A., de Bari L., Corsetti V., Pappalardo G., et al. A peptide containing residues 26-44 of tau protein impairs mitochondrial oxidative phosphorylation acting at the level of the adenine nucleotide translocator. Biochim. Biophys. Acta 2008, 1777:1289-1300.
8. Auerbach S.S., Bristol D.W., Peckham J.C., Travlos G.S., Hebert C.D., Chhabra R.S. Toxicity and carcinogenicity studies of methylene blue trihydrate in F344N rats and B6C3F1 mice. Food Chem. Toxicol. 2010, 48:169-177.
9. Barrett D., Shumake J., Jones D., Gonzalez-Lima F. Metabolic mapping of mouse brain activity after extinction of a conditioned emotional response. J. Neurosci. 2003, 23:5740-5749.
10. Bennett M.C., Diamond D.M., Stryker S.L., Parks J.K., Parker W.D. Cytochrome oxidase inhibition: a novel animal model of Alzheimer's disease. J. Geriatr. Psychiatry Neurol. 1992, 5:93-101.
11. Bennett, M.C., Rose, G.M., 1998. Behavioral, electrophysiological and biochemical consequences of chronic cytochrome oxidase inhibition in rats. In: Gonzalez-Lima, F. (Ed.), Cytochrome oxidase in neuronal metabolism and Alzheimer's disease. Plenum Press, New York, pp. 217-232.
12. Berndt J.D., Callaway N.L., Gonzalez-Lima F. Effects of chronic sodium azide on brain and muscle cytochrome oxidase activity: a potential model to investigate environmental contributions to neurodegenerative diseases. J. Toxicol. Environ. Health A 2001, 63:67-77.
13. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 2000, 3:1301-1306.
14. Blass N., Fung D. Dyed but not dead-methylene blue overdose. Anesthesiology 1976, 45:458-459.
15. Bruchey A.K., Gonzalez-Lima F. Behavioral, physiological and biochemical hormetic responses to the autoxidizable dye methylene blue. Am. J. Pharm. Toxicol. 2008, 3:72-79.
16. Brusque A.M., Borba Rosa R., Schuck P.F., Dalcin K.B., Ribeiro C.A., Silva C.G., et al. Inhibition of the mitochondrial respiratory chain complex activities in rat cerebral cortex by methylmalonic acid. Neurochem. Int. 2002, 40:593-601.
17. Buchholz K., Schirmer R.H., Eubel J.K., Akoachere M.B., Dandekar T., Becker K., et al. Interactions of methylene blue with human disulfide reductases and their orthologues from Plasmodium falciparum. Antimicrob. Agents Chemother. 2008, 52:183-191.
18. Calabrese E.J., Bachmann K.A., Bailer A.J., Bolger P.M., Borak J., Cai L., et al. Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Toxicol. Appl. Pharmacol. 2007, 222:122-128.
19. Calabrese E.J., Hoffmann G.R., Stanek E.J., Nascarella M.A. Hormesis in high-throughput screening of antibacterial compounds in E coli. Hum. Exp. Toxicol. 2010, 29:667-677.
20. Calabrese E.J., Mattson M.P., Calabrese V. Resveratrol commonly displays hormesis: occurrence and biomedical significance. Hum. Exp. Toxicol. 2010, 29:980-1015.
21. Callaway N.L., Riha P.D., Bruchey A.K., Munshi Z., Gonzalez-Lima F. Methylene blue improves brain oxidative metabolism and memory retention in rats. Pharmacol. Biochem. Behav. 2004, 77:175-181.
22. Callaway N.L., Riha P.D., Wrubel K.M., McCollum D., Gonzalez-Lima F. Methylene blue restores spatial memory retention impaired by an inhibitor of cytochrome oxidase in rats. Neurosci. Lett. 2002, 332:83-86.
23. Cleeter M.W., Cooper J.M., Darley-Usmar V.M., Moncada S., Schapira A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide, Implications for neurodegenerative diseases. FEBS Lett. 1994, 345:50-54.
24. Clifton J., Leikin J.B. Methylene blue. Am. J. Ther. 2003, 10:289-291.
25. Cohen N., Robinson D., Ben-Ezzer J., Hemo Y., Hasharoni A., Wolmann Y., et al. Reduced NO accumulation in arthrotic cartilage by exposure to methylene blue. Acta Orthop. Scand. 2000, 71:630-636.
26. Cooper C.E. Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector?. Trends Biochem. Sci. 2002, 27:33-39.
27. Daemen-Gubbels C.R., Groeneveld P.H., Groeneveld A.B., van Kamp G.J., Bronsveld W., Thijs L.G. Methylene blue increases myocardial function in septic shock. Crit. Care Med. 1995, 23:1363-1370.
28. Deiana S., Harrington C.R., Wischik C.M., Riedel G. Methylthioninium chloride reverses cognitive deficits induced by scopolamine: comparison with rivastigmine. Psychopharmacology (Berl) 2009, 202:53-65.
29. Deutsch S.I., Rosse R.B., Schwartz B.L., Fay-McCarthy M., Rosenberg P.B., Fearing K. Methylene blue adjuvant therapy of schizophrenia. Clin. Neuropharmacol. 1997, 20:357-363.
30. Dhar S.S., Liang H.L., Wong-Riley M.T. Nuclear respiratory factor 1 co-regulates AMPA glutamate receptor subunit 2 and cytochrome c oxidase: tight coupling of glutamatergic transmission and energy metabolism in neurons. J. Neurochem. 2009, 108:1595-1606.
31. Dhar S.S., Liang H.L., Wong-Riley M.T. Transcriptional coupling of synaptic transmission and energy metabolism: role of nuclear respiratory factor 1 in co-regulating neuronal nitric oxide synthase and cytochrome c oxidase genes in neurons. Biochim. Biophys. Acta 2009, 1793:1604-1613.
32. Dhar S.S., Wong-Riley M.T. Coupling of energy metabolism and synaptic transmission at the transcriptional level: role of nuclear respiratory factor 1 in regulating both cytochrome c oxidase and NMDA glutamate receptor subunit genes. J. Neurosci. 2009, 29:483-492.
33. Du H., Guo L., Yan S., Sosunov A.A., McKhann G.M., Yan S.S. Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:18670-18675.
34. Dufour C., Grill J., Sabouraud P., Behar C., Munzer M., Motte J., et al. Ifosfamide induced encephalopathy: 15 observations. Arch. Pediatr. 2006, 13:140-145.
35. Furian A.F., Fighera M.R., Oliveira M.S., Ferreira A.P., Fiorenza N.G., de Carvalho Myskiw J., et al. Methylene blue prevents methylmalonate-induced seizures and oxidative damage in rat striatum. Neurochem. Int. 2007, 50:164-171.
36. Gabrielli D., Belisle E., Severino D., Kowaltowski A.J., Baptista M.S. Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions. Photochem. Photobiol. 2004, 79:227-232.
37. Gillman P.K. Methylene blue is a potent monoamine oxidase inhibitor. Can. J. Anaesth. 2008, 55:311-312.
38. Gonzalez-Lima F. Brain imaging of auditory learning functions in rats: Studies with fluorodeoxyglucose autoradiography and cytochrome oxidase histochemistry. Advances in Metabolic Mapping Techniques for Brain Imaging of Behavioral and Learning Functions 1992, 39-109. Kluwer Academic Publishers, Dordrecht/Boston/London. F. Gonzalez-Lima, T. Finkenstädt, H. Scheich (Eds.).
39. Gonzalez-Lima F., Bruchey A.K. Extinction memory improvement by the metabolic enhancer methylene blue. Learn. Mem. 2004, 11:633-640.
40. Gonzalez-Lima F., Cada A. Quantitative histochemistry of cytochrome oxidase activity: Theory, methods and regional vulnerability. Cytochrome Oxidase in Neuronal Metabolism and Alzheimer's Disease 1998, Plenum Press, New York. F. Gonzalez-Lima (Ed.).
41. Gonzalez-Lima F., Valla J., Cada A. Brain cytochrome oxidase activity and how it relates to the pathophysiology of memory and Alzheimer's disease. Free Radicals, Oxidative Stress and Antioxidants: Pathological and Physiological Significance 1998, 205-227. Plenum Press, New York. T. Ozben (Ed.).
42. Gonzalez-Lima F., Valla J., Lorandby L. Cytochrome oxidase inhibition in Alzheimer's disease. Cytochrome Oxidase in Neuronal Metabolism and Alzheimer's Disease 1998, 171-202. Plenum Press, New York. F. Gonzalez-Lima (Ed.).
43. Gonzalez-Lima F., Valla J., Matos-Collazo S. Quantitative cytochemistry of cytochrome oxidase and cellular morphometry of the human inferior colliculus in control and Alzheimer's patients. Brain Res. 1997, 752:117-126.
44. Govindaiah, Shankaranarayana Rao B.S., Ramamohan Y., Singh Y.K., Dhingra N.K., Raju T.R. Cytochrome oxidase activity in rat retinal ganglion cells during postnatal development. Brain Res. Dev. Brain Res. 2000, 124:117-120.
45. Guzman-Barron E.S., Hoffmann L.A. The catalytic effect of dyes on the oxygen consumption of living cells. J. Gen. Physiol. 1930, 13:483-494.
46. Harvey B.H., Duvenhage I., Viljoen F., Scheepers N., Malan S.F., Wegener G., et al. Role of monoamine oxidase, nitric oxide synthase and regional brain monoamines in the antidepressant-like effects of methylene blue and selected structural analogues. Biochem. Pharmacol. 2010, 80:1580-1591.
47. Heidenreich R., Natowicz M., Hainline B.E., Berman P., Kelley R.I., Hillman R.E., et al. Acute extrapyramidal syndrome in methylmalonic acidemia: metabolic stroke involving the globus pallidus. J. Pediatr. 1988, 113:1022-1027.
48. Henriquez H., el Din A., Ozand P.T., Subramanyam S.B., al Gain S.I. Emergency presentations of patients with methylmalonic acidemia, propionic acidemia and branched chain amino acidemia (MSUD). Brain Dev. 1994, 16(Suppl):86-93.
49. Hevner R.F., Liu S., Wong-Riley M.T. An optimized method for determining cytochrome oxidase activity in brain tissue homogenates. J. Neurosci. Methods 1993, 50:309-319.
50. Ishiwata A., Sakayori O., Minoshima S., Mizumura S., Kitamura S., Katayama Y. Preclinical evidence of Alzheimer changes in progressive mild cognitive impairment: a qualitative and quantitative SPECT study. Acta Neurol. Scand. 2006, 114:91-96.
51. Juffermans N.P., Vervloet M.G., Daemen-Gubbels C.R., Binnekade J.M., de Jong M., Groeneveld A.B. A dose-finding study of methylene blue to inhibit nitric oxide actions in the hemodynamics of human septic shock. Nitric Oxide 2010, 22:275-280.
52. Kelner M.J., Bagnell R., Hale B., Alexander N.M. Methylene blue competes with paraquat for reduction by flavo-enzymes resulting in decreased superoxide production in the presence of heme proteins. Arch. Biochem. Biophys. 1988, 262:422-426.
53. Kelner M.J., Bagnell R., Hale B., Alexander N.M. Potential of methylene blue to block oxygen radical generation in reperfusion injury. Basic Life Sci. 1988, 49:895-898.
54. Klatt P., Heinzel B., John M., Kastner M., Bohme E., Mayer B. Ca2+/calmodulin-dependent cytochrome c reductase activity of brain nitric oxide synthase. J. Biol. Chem. 1992, 267:11374-11378.
55. Kupfer A., Aeschlimann C., Cerny T. Methylene blue and the neurotoxic mechanisms of ifosfamide encephalopathy. Eur. J. Clin. Pharmacol. 1996, 50:249-252.
56. Kupfer A., Aeschlimann C., Wermuth B., Cerny T. Prophylaxis and reversal of ifosfamide encephalopathy with methylene-blue. Lancet 1994, 343:763-764.
57. Larsson N.G., Andersen O., Holme E., Oldfors A., Wahlstrom J. Leber's hereditary optic neuropathy and complex I deficiency in muscle. Ann. Neurol. 1991, 30:701-708.
58. Lee R.B., Urban J.P. Functional replacement of oxygen by other oxidants in articular cartilage. Arthritis Rheum. 2002, 46:3190-3200.
59. Lensman M., Korzhevskii D.E., Mourovets V.O., Kostkin V.B., Izvarina N., Perasso L., et al. Intracerebroventricular administration of creatine protects against damage by global cerebral ischemia in rat. Brain Res. 2006, 1114(18):187-194.
60. Liang W.S., Reiman E.M., Valla J., Dunckley T., Beach T.G., Grover A., et al. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:4441-4446.
61. Lindahl P.E., Oberg K.E. The effect of rotenone on respiration and its point of attack. Exp. Cell Res. 1961, 23:228-237.
62. Lupien S.J., Buss C., Schramek T.E., Maheu F., Pruessner J. Hormetic influence of glucocorticoids on human memory. Nonlinearity Biol. Toxicol. Med. 2005, 3:23-56.
63. Martijn C., Wiklund L. Effect of methylene blue on the genomic response to reperfusion injury induced by cardiac arrest and cardiopulmonary resuscitation in porcine brain. BMC Med. Genomics 2010, 3:27.
64. Martindale S.J., Stedeford J.C. Neurological sequelae following methylene blue injection for parathyroidectomy. Anaesthesia 2003, 58:1041-1042.
65. Martinez J., Jensen R.A., Vasquez B., McGuiness T., McGaugh J.L. Methylene blue alters retention of inhibitory avoidance responses. Physiol. Psychol. 1978, 6:387-390.
66. Mayer B., Brunner F., Schmidt K. Inhibition of nitric oxide synthesis by methylene blue. Biochem. Pharmacol. 1993, 45:367-374.
67. Medina D.X., Caccamo A., Oddo S. Methylene blue reduces abeta levels and rescues early cognitive deficit by increasing proteasome activity. Brain Pathol. 2011, 21:140-149.
68. Miclescu A., Basu S., Wiklund L. Methylene blue added to a hypertonic-hyperoncotic solution increases short-term survival in experimental cardiac arrest. Crit. Care Med. 2006, 34:2806-2813.
69. Miclescu A., Basu S., Wiklund L. Cardio-cerebral and metabolic effects of methylene blue in hypertonic sodium lactate during experimental cardiopulmonary resuscitation. Resuscitation 2007, 75:88-97.
70. Michel H., Behr J., Harrenga A., Kannt A. Cytochrome c oxidase: structure and spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 1998, 27:329-356.
71. Minoshima S., Giordani B., Berent S., Frey K.A., Foster N.L., Kuhl D.E. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann. Neurol. 1997, 42:85-94.
72. Moosmann B., Skutella T., Beyer K., Behl C. Protective activity of aromatic amines and imines against oxidative nerve cell death. Biol. Chem. 2001, 382:1601-1612.
73. Morrow G., Mahoney M.J., Mathews C., Lebowitz J. Studies of methylmalonyl coenzyme A carbonylmutase activity in methylmalonic acidemia. I. Correlation of clinical, hepatic, and fibroblast data. Pediatr. Res. 1975, 9:641-644.
74. Nascarella M.A., Stanek E.J., Hoffmann G.R., Calabrese E.J. Quantification of hormesis in anticancer-agent dose-responses. Dose Resp. 2009, 7:160-171.
75. Naylor G.J., Martin B., Hopwood S.E., Watson Y. A two-year double-blind crossover trial of the prophylactic effect of methylene blue in manic-depressive psychosis. Biol. Psychiatry 1986, 21:915-920.
76. Necula M., Breydo L., Milton S., Kayed R., van der Veer W.E., Tone P., et al. Methylene blue inhibits amyloid Abeta oligomerization by promoting fibrillization. Biochemistry 2007, 46:8850-8860.
77. O'Leary J.C., Li Q., Marinec P., Blair L.J., Congdon E.E., Johnson A.G., et al. Phenothiazine-mediated rescue of cognition in tau transgenic mice requires neuroprotection and reduced soluble tau burden. Mol. Neurodegener. 2010, 5:45.
78. Ohlow M.J., Moosmann B. Phenothiazine: the seven lives of pharmacology's first lead structure. Drug Discov. Today 2011, 16:119-131.
79. Okun J.G., Horster F., Farkas L.M., Feyh P., Hinz A., Sauer S., et al. Neurodegeneration in methylmalonic aciduria involves inhibition of complex II and the tricarboxylic acid cycle, and synergistically acting excitotoxicity. J. Biol. Chem. 2002, 277:14674-14680.
80. Oz M., Lorke D.E., Hasan M., Petroianu G.A. Cellular and molecular actions of Methylene Blue in the nervous system. Med. Res. Rev. 2011, 31:93-117.
81. Oz M., Lorke D.E., Petroianu G.A. Methylene blue and Alzheimer's disease. Biochem. Pharmacol. 2009, 78:927-932.
82. Pelgrims J., De Vos F., Van den Brande J., Schrijvers D., Prove A., Vermorken J.B. Methylene blue in the treatment and prevention of ifosfamide-induced encephalopathy: report of 12 cases and a review of the literature. Br. J. Cancer 2000, 82:291-294.
83. Peter C., Hongwan D., Kupfer A., Lauterburg B.H. Pharmacokinetics and organ distribution of intravenous and oral methylene blue. Eur. J. Clin. Pharmacol. 2000, 56:247-250.
84. Pfaffendorf M., Bruning T.A., Batnik H.D., van Zwieten P.A. The interaction between methylene blue and the cholinergic system. Br. J. Pharmacol. 1997, 122:95-98.
85. Poirier G.L., Amin E., Good M.A., Aggleton J.P. Early-onset dysfunction of retrosplenial cortex precedes overt amyloid plaque formation in Tg2576 mice. Neuroscience 2011, 174:71-83.
86. Poppers P.J., Mastri A.R., Lebeaux M., Covino B.G. The effect of methylene blue on neural tissue. Anesthesiology 1970, 33:335-340.
87. Poremba A., Jones D., Gonzalez-Lima F. Metabolic effects of blocking tone conditioning on the rat auditory system. Neurobiol. Learn. Mem. 1997, 68:154-171.
88. Poremba A., Jones D., Gonzalez-Lima F. Classical conditioning modifies cytochrome oxidase activity in the auditory system. Eur. J. Neurosci. 1998, 10:3035-3043.
89. Quirk G.J., Garcia R., Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol. Psychiatry 2006, 60:337-343.
90. Rainer M., Kraxberger E., Haushofer M., Mucke H.A., Jellinger K.A. No evidence for cognitive improvement from oral nicotinamide adenine dinucleotide (NADH) in dementia. J. Neural Transm. 2000, 107:1475-1481.
91. Ramsay R.R., Dunford C., Gillman P.K. Methylene blue and serotonin toxicity: inhibition of monoamine oxidase A (MAO A) confirms a theoretical prediction. Br. J. Pharmacol. 2007, 152:946-951.
92. Rhein V., Baysang G., Rao S., Meier F., Bonert A., Muller-Spahn F., et al. Amyloid-beta leads to impaired cellular respiration, energy production and mitochondrial electron chain complex activities in human neuroblastoma cells. Cell Mol. Neurobiol. 2009, 29:1063-1071.
93. Riha P.D., Bruchey A.K., Echevarria D.J., Gonzalez-Lima F. Memory facilitation by methylene blue: dose-dependent effect on behavior and brain oxygen consumption. Eur. J. Pharmacol. 2005, 511:151-158.
94. Riha P.D., Rojas J.C., Colorado R.A., Gonzalez-Lima F. Animal model of posterior cingulate cortex hypometabolism implicated in amnestic MCI and AD. Neurobiol. Learn. Mem. 2008, 90:112-124.
95. Riha P.D., Rojas J.C., Gonzalez-Lima F. Beneficial network effects of methylene blue in an amnestic model. Neuroimage 2011, 54:2623-2634.
96. Rojas J.C., Gonzalez-Lima F. Mitochondrial optic neuropathy: In vivo model of neurodegeneration and neuroprotective strategies. Eye Brain 2010, 2:21-37.
97. Rojas J.C., Gonzalez-Lima F. Low-level light therapy of the eye and brain. Eye Brain 2011, 3:49-67.
98. Rojas J.C., John J.M., Lee J., Gonzalez-Lima F. Methylene blue provides behavioral and metabolic neuroprotection against optic neuropathy. Neurotox. Res. 2009, 15:260-273.
99. Rojas J.C., Simola N., Kermath B.A., Kane J.R., Schallert T., Gonzalez-Lima F. Striatal neuroprotection with methylene blue. Neuroscience 2009, 163:877-889.
100. Salaris S.C., Babbs C.F., Voorhees W.D. Methylene blue as an inhibitor of superoxide generation by xanthine oxidase. A potential new drug for the attenuation of ischemia/reperfusion injury. Biochem. Pharmacol. 1991, 42:499-506.
101. Scott A., Hunter F.E. Support of thyroxine-induced swelling of liver mitochondria by generation of high energy intermediates at any one of three sites in electron transport. J. Biol. Chem. 1966, 241:1060-1066.
102. Schneider F., Lutun P., Hasselmann M., Stoclet J.C., Tempe J.D. Methylene blue increases systemic vascular resistance in human septic shock. Preliminary observations. Intensive Care Med. 1992, 18:309-311.
103. Sharma H.S., Miclescu A., Wiklund L. Cardiac arrest-induced regional blood-brain barrier breakdown, edema formation and brain pathology: a light and electron microscopic study on a new model for neurodegeneration and neuroprotection in porcine brain. J. Neural Transm. 2011, 118:87-114.
104. Shumake J., Gonzalez-Lima F. Brain systems underlying susceptibility to helplessness and depression. Behav. Cogn. Neurosci. Rev. 2003, 2:198-221.
105. Smith R.P., Thron C.D. Hemoglobin, methylene blue and oxygen interactions in human red cells. J. Pharmacol. Exp. Ther. 1972, 183:549-558.
106. Sweet G., Standiford S.B. Methylene-blue-associated encephalopathy. J. Am. Coll. Surg. 2007, 204:454-458.
107. Taniguchi S., Suzuki N., Masuda M., Hisanaga S., Iwatsubo T., Goedert M., et al. Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins. J. Biol. Chem. 2005, 280:7614-7623.
108. Teichert J., Hermann R., Ruus P., Preiss R. Plasma kinetics, metabolism, and urinary excretion of alpha-lipoic acid following oral administration in healthy volunteers. J. Clin. Pharmacol. 2003, 43:1257-1267.
109. Vaiserman A.M. Radiation hormesis: historical perspective and implications for low-dose cancer risk assessment. Dose Resp. 2010, 8:172-191.
110. Valla J., Yaari R., Wolf A.B., Kusne Y., Beach T.G., Roher A.E., et al. Reduced posterior cingulate mitochondrial activity in expired young adult carriers of the APOE epsilon4 allele, the major late-onset Alzheimer's susceptibility gene. J. Alzheimers Dis. 2010, 22:307-313.
111. Visarius T.M., Stucki J.W., Lauterburg B.H. Stimulation of respiration by methylene blue in rat liver mitochondria. FEBS Lett. 1997, 412:157-160.
112. Visarius T.M., Stucki J.W., Lauterburg B.H. Inhibition and stimulation of long-chain fatty acid oxidation by chloroacetaldehyde and methylene blue in rats. J. Pharmacol. Exp. Ther. 1999, 289:820-824.
113. Volke V., Wegener G., Vasar E., Rosenberg R. Methylene blue inhibits hippocampal nitric oxide synthase activity in vivo. Brain Res. 1999, 826:303-305.
114. Vutskits L., Briner A., Klauser P., Gascon E., Dayer A.G., Kiss J.Z., et al. Adverse effects of methylene blue on the central nervous system. Anesthesiology 2008, 108:684-692.
115. Wainwright M., Crossley K.B. Methylene Blue-a therapeutic dye for all seasons?. J. Chemother. 2002, 14:431-443.
116. Wen Y., Li W., Poteet E.C., Xie L., Tan C., Yan L.J., et al. Alternative mitochondrial electron transfer as a novel strategy for neuroprotection. J. Biol. Chem. 2011, 286:15515-16504.
117. Wischik C.M., Edwards P.C., Lai R.Y., Roth M., Harrington C.R. Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:11213-11218.
118. Wong-Riley M., Guo A., Bachman N.J., Lomax M.I. Human COX6A1 gene: promoter analysis, cDNA isolation and expression in the monkey brain. Gene 2000, 247:63-75.
119. Wong-Riley M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 1989, 12:94-101.
120. Wong-Riley M.T., Nie F., Hevner R., Liu S. Brain cytochrome oxidase: functional significance and bigenomic regulation in the CNS. Cytochrome Oxidase in Neuronal Metabolism and Alzheimer's Disease 1998, 1-54. Plenum Press, New York. F. Gonzalez-Lima (Ed.).
121. Wright R.O., Lewander W.J., Woolf A.D. Methemoglobinemia: etiology, pharmacology, and clinical management. Ann. Emerg. Med. 1999, 34:646-656.
122. Wrubel K.M., Barrett D., Shumake J., Johnson S.E., Gonzalez-Lima F. Methylene blue facilitates the extinction of fear in an animal model of susceptibility to learned helplessness. Neurobiol. Learn. Mem. 2007, 87:209-217.
123. Wrubel K.M., Riha P.D., Maldonado M.A., McCollum D., Gonzalez-Lima F. The brain metabolic enhancer methylene blue improves discrimination learning in rats. Pharmacol. Biochem. Behav. 2007, 86:712-717.
124. Zhang X., Rojas J.C., Gonzalez-Lima F. Methylene blue prevents neurodegeneration caused by rotenone in the retina. Neurotox. Res. 2006, 9:47-57.