Ketamine treatment partly reverses alterations in brain derived-neurotrophic factor, oxidative stress and energy metabolism parameters induced by an animal model of depression

Current Neurovascular Research

Volumn 12, Issue 1, 2015, Pages 73-84

  Réus, Gislaine Z ^a,b   Nacif, Marcos Paulo ^a   Abelaira, Helena M ^a   Tomaz, Débora B ^a   Dos Santos, Maria Augusta B ^a   Carlessi, Anelise S ^a   Matias, Beatriz I ^a   Da Luz, Jaine R ^a   Steckert, Amanda V ^a   Jeremias, Gabriela C ^a   Scaini, Giselli ^a   Morais, Meline O S ^a   Streck, Emilio L ^a   Quevedo, João ^a,b  

^a UNIVERSITY OF SOUTHERN SANTA CATARINA   (Brazil)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

BDNF; Depression; Energy metabolism; Ketamine; NMDA receptor; Oxidative stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CARBONYL DERIVATIVE; CREATINE KINASE; KETAMINE; MALONALDEHYDE; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE; AMINO ACID RECEPTOR BLOCKING AGENT; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEPRESSION; DRUG MECHANISM; ENERGY METABOLISM; FEMALE; HIPPOCAMPUS; NEUROANATOMY; NONHUMAN; NUCLEUS ACCUMBENS; OXIDATIVE STRESS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; ANALYSIS OF VARIANCE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; MALE; MATERNAL DEPRIVATION; METABOLISM; NEWBORN; PATHOLOGY; PREGNANCY; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CREATINE KINASE; DEPRESSION; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; KETAMINE; MALE; MATERNAL DEPRIVATION; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, WISTAR; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84926328298     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/1567202612666150122122924     Document Type: Article

References (76)

1. Ladd CO, Owens MJ, Nemeroff CB. Persistent changes in corticotrophin releasing factor neuronal systems induced by maternal deprivation. Endocrinology 1996; 137 (4): 1212-1218
2. Van Oers HJ, de Kloet ER, Levins S. Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Brain Res Dev Brain Res 1998; 111 (2): 245-252
3. Vazquez DM, Lopez JF, van Hoers H, Watson SJ, Levin S. Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res 2000; 855 (1): 76-82
4. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 2000; 122: 81-103.
5. Khoury AE, Gruber SHM, Mork A, Mathe AA. Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog Neuropsychopharmacol Biol Psychiatry 2006: 30 (3): 535-540.
6. Naughton M, Clarke G, O'Leary OF, Cryan JF, Dinan TG. A review of ketamine in affective disorders: current evidence of clinical efficacy, limitations of use and pre-clinical evidence on proposed mechanisms of action. J Affect Disord 2014; 156: 24-35.
7. Manji HK, Quiroz JA, Sporn J, et al. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 2003; 53 (8): 707-742.
8. Skolnick P, Layer RT, Popik P, Nowak G, Paul IA, Trullas R. Adaptation of N-methyl-D-aspartate (NMDA) receptors following antidepressant treatment: implications for the pharmacotherapy of depression. Pharmacopsychiatry 1996; 29 (1): 23-26.
9. Sanacora G, Zarate CA, Krystal JH, Manji HK. Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 2008; 7 (5): 426-437
10. Bubeníková-Valesová V, Horácek J, Vrajová M, Höschl C. Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 2008; 32 (5): 1014-1023.
11. Zugno AI, Chipindo HL, Volpato AM, et al. Omega-3 prevents behavior response and brain oxidative damage in the ketamine model of schizophrenia. Neuroscience 2014; 259: 223-231.
12. Machado-Vieira R, Salvadore G, Diazgranados N, Zarate CAJ. Ketamine and the next generation of antidepressants with a rapid onset of action. Pharmacol Ther 2009; 123 (2): 143-150.
13. Gideons ES, Kavalali ET, Monteggia LM. Mechanisms underlying differential effectiveness of memantine and ketamine in rapid antidepressant responses. Proc Natl Acad Sci USA 2014; 111 (23): 8649-8654.
14. Réus GZ, Nacif MP, Abelaira HM, et al. Ketamine ameliorates depressive-like behaviors and immune alterations in adult rats following maternal deprivation. Neurosci Lett 2014; 584C: 83-87.
15. Li Y, Zhu ZR, Ou BC, et al. Dopamine D2/D3 but not dopamine D1 receptors are involved in the rapid antidepressant-like effects of ketamine in the forced swim test. Behav Brain Res 2014; 279C: 100-105.
16. Berman AK, Lott RB, Donaldson ST. Periodic maternal deprivation may modulate offspring anxiety-like behavior through mechanisms involving neuroplasticity in the amygdala. Brain Res Bull 2014; 101: 7-11.
17. Suri D, Veenit V, Sarkar A, et al. Early stress evokes agedependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol Psychiatry 2013; 73 (7): 658-666
18. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 2001; 24: 677-736.
19. Branchi I. The mouse communal nest: investigating the epigenetic influences of the early social environment on brain and behavior development. Neurosci Biobehav Rev 2009; 33 (4): 551-9
20. Cies̈lik K, Sowa-Kućma M, Ossowska G, et al. Chronic unpredictable stress-induced reduction in the hippocampal brainderived neurotrophic factor (BDNF) gene expression is antagonized by zinc treatment. Pharmacol Rep 2011; 63 (2): 537-543.
21. Duman RS, Monteggia LM. A neurotrophic model for stressrelated mood disorders. Biol Psychiatry 2006; 59 (12): 1116-1127.
22. Grande I, Fries GR, Kunz M, Kapczinski F. The role of BDNF as a mediator of neuroplasticity in bipolar disorder. Psychiatry Investig 2010; 7 (4): 243-250.
23. Srinivasan S, Avadhani NG. Cytochrome c oxidase dysfunction in oxidative stress. Free Radic Biol Med 2012; 53 (6): 1252-1263.
24. Brand MD, Affourtit C, Esteves TC, et al. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 2004; 37 (6): 755-767.
25. Shao L, Martin MV, Watson SJ, et al. Mitochondrial involvement in psychiatric disorders. Ann Med 2008; 40 (4): 281-295
26. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417 (1): 1-13.
27. Mello PB, Benetti F, Cammarota M, Izquierdo I. Physical exercise can reverse the deficit in fear memory induced by maternal deprivation. Neurobiol Learn Mem 2009; 92 (3): 364-369.
28. Garcia LS, Comim CM, Valvassori SS, et al. Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32 (1): 140-144
29. Garcia LS, Comim CM, Valvassori SS, et al. Chronic administration of ketamine elicits antidepressant-like effects in rats without affecting hippocampal brain-derived neurotrophic factor protein levels. Basic Clin Pharmacol Toxicol 2008; 103 (6): 502-506.
30. Réus GZ, Dos Santos MA, Abelaira HM, et al. Imipramine reverses alterations in cytokines and BDNF levels induced by maternal deprivation in adult rats. Behav Brain Res 2013; 242: 40-46.
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193 (1): 265-75.
32. Cassina A, Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 1996; 328 (2): 309-16.
33. Fischer JC, Ruitenbeek W, Berden JA, et al. Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 1985; 153 (1): 23-36.
34. Rustin P, Munnich A, Rötig A. Succinate dehydrogenase and human diseases: new insights into a well-known enzyme. Eur J Hum Genet 2002; 10 (5): 289-91.
35. Hughes BP. A method for the estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathological sera. Clin Chim Acta 1962; 7: 597-603.
36. Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 1990; 186: 421-431.
37. Levine RL, Williams JA, Stadtman ER, Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 1994; 233: 346-357.
38. Bannister JV, Calabrese L. Assays for superoxide dismutase. Methods Biochem Anal 1987; 32: 279-312.
39. McAllister AK, Katz LC, Lo DC. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 1999; 22: 295-318.
40. Sohrabji F, Lewis DK. Estrogen-BDNF interactions: implications for neurodegenerative diseases. Front Neuroendocrinol 2006; 27 (4): 404-414.
41. Musumeci G, Minichiello L. BDNF-TrkB signalling in fear learning: from genetics to neural networks. Rev Neurosci 2011; 22 (3): 303-315.
42. Pluchino N, Russo M, Santoro AN, Litta P, Cela V, Genazzani AR. Steroid hormones and BDNF. Neuroscience 2013; 239: 271-279.
43. Abelaira HM, Réus GZ, Ribeiro KF, et al. Lamotrigine treatment reverses depressive-like behavior and alters BDNF levels in the brains of maternally deprived adult rats. Pharmacol Biochem Behav 2012; 101 (3): 348-353.
44. Della FP, Abelaira HM, Réus GZ, et al. Treatment with tianeptine induces antidepressive-like effects and alters the neurotrophin levels, mitochondrialrespiratory chain and cycle Krebs enzymes in the brain of maternally deprived adult rats. Metab Brain Dis 2013; 28 (1): 93-105.
45. Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but lessrobustly. Neurosci Res 2005; 53 (2): 129-139.
46. Lotrich FE, Albusaysi S, Ferrell RE. Brain-derived neurotrophic factor serum levels and genotype: association with depression during interferon-α treatment. Neuropsychopharmacology 2013; 38 (6): 985-95.
47. Réus GZ, Stringari RB, Ribeiro KF, et al. Maternal deprivation induces depressive-like behaviour and alters neurotrophin levels in the rat brain. Neurochem Res 2011; 36 (3): 460-6
48. Fraga DB, Réus GZ, Abelaira HM, et al. Ketamine alters behavior and decreases BDNF levels in the rat brain as a function of time after drug administration. Rev Bras Psiquiatr 2013; 35 (3): 262-266.
49. Egan MF, Kojima M, Callicott JH, et al. The BDNF val66met polymorphism affects activity dependent secretion of BDNF and human memory and hippocampal function. Cell 2003; 112 (2): 257-269.
50. Jourdi H, Kabbaj M. Acute BDNF treatment upregulates GluR1-SAP97 and GluR2-GRIP1 interactions: implications for sustained AMPA receptor expression. PLoS One 2013; 8 (2): e57124.
51. Tizabi Y, Bhatti BH, Manaye KF, Das JR, Akinfiresoye L. Antidepressant-like effects of low ketamine dose is associated with increased hippocampal AMPA/NMDA receptor density ratio in female Wistar-Kyoto rats. Neuroscience 2012; 213: 72-80.
52. Leonard B, Maes M. Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci Biobehav Rev 2012; 36 (2): 764-785.
53. Gardner A, Johansson A, Wibom R, et al. Alterations of mitochondrial function and correlations with personality traits in selected major depressive disorder patients. J Affect Disord 2003; 76 (1-3): 55-68.
54. Madrigal JL, Olivenza R, Moro M, Lizasoain I, Lorenzo P, Rodrigo J. Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 2001; 24 (4): 420-429.
55. Rezin GT, Gonçalves CL, Daufenbach JF, et al. Acute administration of ketamine reverses the inhibition of mitochondrial respiratory chain induced by chronic mild stress. Brain Res Bull 2009; 79 (6): 418-421.
56. Goncalves CL, Rezin GT, Ferreira GK, et al. Differential effects of escitalopram administration on cortical and subcortical brain regions metabolic parameters of Wistar rats. Acta Neuropsychiatr 2012; 24: 147-154.
57. Nicholls DG, Vesce S, Kirk L, Chalmers S. Interactions between mitochondrial bioenergetics and cytoplasmic calcium in cultured cerebellar granule cells. Cell Calcium 2003; 34 (4-5): 407-424.
58. Beretta S, Wood JP, Derham B, et al. Partial mitochondrial complex I inhibition induces oxidative damage and perturbs glutamate transport in primary retinal cultures. Relevance to Leber Hereditary Optic Neuropathy (LHON). Neurobiol Dis 2006; 24 (2): 308-317.
59. Zhang X, Rojas JC, Gonzalez-Lima F. Methylene blue prevents neurodegeneration caused by rotenone in the retina. Neurotox Res 2006; 9 (1): 47-57.
60. Rosenstock TR, Carvalho AC, Jurkiewicz A, Frussa-Filho R, Smaili SS. Mitochondrial calcium, oxidative stress and apoptosis in a neurodegenerative disease model induced by 3-nitropropionic acid. J Neurochem 2004; 88 (5): 1220-1228.
61. Albrecht P, Lewerenz J, Dittmer S, Noack R, Maher P, Methner A. Mechanisms of oxidative glutamate toxicity: the glutamate/cystine antiporter system xc-as a neuroprotective drug target. CNS Neurol Disord Drug Targets 2010; 9 (3): 373-382.
62. Nguyen D, Alavi MV, Kim KY, et al. A new vicious cycle involving glutamate excitotoxicity, oxidative stress and mitochondrial dynamics. Cell Death Dis 2011; 2: 240.
63. Ozyurt B, Ozyurt H, Akpolat N, Erdogan H, Sarsilmaz M. Oxidative stress in prefrontal cortex of rat exposed to MK-801 and protective effects of CAPE. Prog Neuropsychopharmacol Biol Psychiatry 2007; 31 (4): 832-838.
64. de Oliveira L, Spiazzi CM, Bortolin T, et al. Different subanesthetic doses of ketamine increase oxidative stress in the brain of rats. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33 (6): 1003-1008.
65. da Silva FC, do Carmo de Oliveira Cito M, da Silva MI, et al. Behavioral alterations and pro-oxidant effect of a single ketamine administration to mice. Brain Res Bull 2010; 83 (1-2): 9-15.
66. Réus GZ, Stringari RB, de Souza B, et al. Harmine and imipramine promote antioxidant activities in prefrontal cortex and hippocampus. Oxid Med Cell Longev 2010; 3 (5): 325-331.
67. Della FP, Abelaira HM, Réus GZ, et al. Tianeptine exerts neuroprotective effects in the brain tissue of rats exposed to the chronic stress model. Pharmacol Biochem Behav 2012; 103 (2): 395-402.
68. Wang C, McInnis J, West JB, et al. Blockade of phencyclidineinduced cortical apoptosis and deficits in prepulse inhibition by M40403, a superoxide dismutase mimetic. J Pharmacol Exp Ther 2003; 304 (1): 266-271.
69. Scallet AC, Schmued LC, Slikker W Jr, et al. Developmental neurotoxicity of ketamine: morphometric confirmation, exposure parameters, and multiple fluorescent labeling of apoptotic neurons. Toxicol Sci 2004; 81 (2): 364-370.
70. Ortiz R, Niciu MJ, Lukkahati N, et al. Shank3 as a potential biomarker of antidepressant response to ketamine and its neural correlates in bipolar depression. J Affect Disord 2014; 172C: 307-311.
71. Cao G, Cutler RG. Protein oxidation and aging: Difficulties in measuring reactive protein carbonyls in tissues using 2,4-dinitrophenylhydrazine. Arch Biochem Biophys 1995; 320 (1): 106-114.
72. Lucca G, Comim CM, Valvassori SS, et al. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 2009; 54 (5-6): 358-362.
73. Inkielewicz-Stępniak I. Impact of fluoxetine on liver damage in rats. Pharmacol Rep 2011; 63 (2): 441-447.
74. Abelaira HM, Réus GZ, Ribeiro KF, et al. Effects of lamotrigine on behavior, oxidative parameters and signaling cascades in ratsexposed to the chronic mild stress model. Neurosci Res 2013; 75 (4): 324-330.
75. Bilici M, Efe H, Köroʇlu MA, Uydu HA, Bekaroʇlu M, Deʇer O. Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 2001; 64 (1): 43-51.
76. Maes M, Mihaylova I, Kubera M, Uytterhoeven M, Vrydags N, Bosmans E. Coenzyme Q10 deficiency in myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) is related to fatigue, autonomic and neurocognitive symptoms and is another risk factor explaining the early mortality in ME/CFS due to cardiovascular disorder. Neuro Endocrinol Lett 2009; 30 (4): 470-476.