Intermittent fasting attenuates lipopolysaccharide-induced neuroinflammation and memory impairment

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Vasconcelos, Andrea R ^a   Yshii, Lidia M ^a   Viel, Tania A ^a   Buck, Hudson S ^b   Mattson, Mark P ^c   Scavone, Cristoforo ^a   Kawamoto, Elisa M ^a,c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Medical School of Santa Casa of Sao Paulo SP   (Brazil)

^c NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Inflammation; Intermittent fasting; Memory; TLR4

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; NITRIC OXIDE SYNTHASE; RANTES; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; TLR4 PROTEIN, RAT; INTERLEUKIN 1ALPHA; MESSENGER RNA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BARNES MAZE TEST; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; GENE SEQUENCE; HIPPOCAMPUS; LOCOMOTION; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; MENTAL TASK; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PASSIVE AVOIDANCE TEST; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION; ANIMAL; AVOIDANCE BEHAVIOR; BRAIN; CHEMICALLY INDUCED; DIET RESTRICTION; DISEASE MODEL; DRUG EFFECTS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; MAZE TEST; MEMORY DISORDERS; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; TOXICITY; WISTAR RAT; ANIMAL TISSUE; BACTERIAL INFECTION; BRAIN TISSUE; COGNITION; COGNITIVE DEFECT; DISSECTION; INTERMITTENT FASTING; RAT MODEL; SEPSIS;

ANIMALS; AVOIDANCE LEARNING; BRAIN; CYTOKINES; DISEASE MODELS, ANIMAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FASTING; GENE EXPRESSION REGULATION; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MAZE LEARNING; MEMORY DISORDERS; MOTOR ACTIVITY; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR; TOLL-LIKE RECEPTOR 4;

EID: 84901942277     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-85     Document Type: Article

References (92)

1. Fitó M, Guxens M, Corella D, Sáez G, Estruch R, de la Torre R, Francés F, Cabezas C, López-Sabater Mdel C, Marrugat J, García-Arellano A, Arós F, Ruiz-Gutierrez V, Ros E, Salas-Salvadó J, Fiol M, Solá R, Covas MI, PREDIMED Study Investigators Effect of a traditional Mediterranean diet on lipoprotein oxidation: a randomized controlled trial. Arch Intern Med 2007, 167:1195-1203. PREDIMED Study Investigators.
2. Ye SM, Johnson RW. Increased interleukin-6 expression by microglia from brain of aged mice. J Neuroimmunol 1999, 93:139-148.
3. Richwine AF, Godbout JP, Berg BM, Chen J, Escobar J, Millard DK, Johnson RW. Improved psychomotor performance in aged mice fed diet high in antioxidants is associated with reduced ex vivo brain interleukin-6 production. Brain Behav Immun 2005, 19:512-520.
4. DeLegge MH, Smoke A. Neurodegeneration and inflammation. Nutr Clin Pract 2008, 23:35-41.
5. Breitner JC, Baker LD, Montine TJ, Meinert CL, Lyketsos CG, Ashe KH, Brandt J, Craft S, Evans DE, Green RC, Ismail MS, Martin BK, Mullan MJ, Sabbagh M, Tariot PN, ADAPT Research Group Extended results of the Alzheimer's disease anti-inflammatory prevention trial. Alzheimers Dement 2011, 7:402-411. ADAPT Research Group.
6. Dodel R, Rominger A, Bartenstein P, Barkhof F, Blennow K, Förster S, Winter Y, Bach JP, Popp J, Alferink J, Wiltfang J, Buerger K, Otto M, Antuono P, Jacoby M, Richter R, Stevens J, Melamed I, Goldstein J, Haag S, Wietek S, Farlow M, Jessen. Intravenous immunoglobulin for treatment of mild-tomoderate Alzheimer's disease: a phase 2, randomised, double-blind, placebo-controlled, dose-finding trial. Lancet Neurol 2013, 12(3):233-243.
7. Stewart WF, Kawas C, Corrada M, Metter EJ. Risk of Alzheimer's disease and duration of NSAID use. Neurology 1997, 48:626-632.
8. In Veld B, Ruitenberg A, Hofman A, Launer L, van Duijn C, Stijnen T, Breteler M, Stricker B. Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med 2001, 345:1515-1521.
9. Vlad SC, Miller DR, Kowall NW, Felson DT. Protective effects of NSAIDs on the development of Alzheimer disease. Neurology 2008, 70:1672-1677.
10. Imbimbo BP, Solfrizzi V, Panza F. Are NSAIDs useful to treat Alzheimer's disease or mild cognitive impairment?. Front Aging Neurosci 2010, 2.
11. Hoffmann A, Baltimore D. Circuitry of nuclear factor kappaB signaling. Immunol Rev 2006, 210:171-186.
12. Mattson MP, Meffert MK. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 2006, 13:852-860.
13. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998, 16:225-260.
14. Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002, 109:S81-S96.
15. Kaltschmidt C, Kaltschmidt B, Neumann H, Wekerle H, Baeuerle PA. Constitutive NF-kappa B activity in neurons. Mol Cell Biol 1994, 14:3981-3992.
16. Camandola S, Mattson MP. NF-kappa B as a therapeutic target in neurodegenerative diseases. Expert Opin Ther Targets 2007, 11:123-132.
17. Weberpals M, Hermes M, Hermann S, Kummer M, Terwel D, Semmler A, Berger M, Schäfers M, Heneka M. NOS2 gene deficiency protects from sepsis-induced long-term cognitive deficits. J Neurosci 2009, 29:14177-14184.
18. Okun E, Barak B, Saada-Madar R, Rothman S, Griffioen K, Roberts N, Castro K, Mughal M, Pita M, Stranahan A, Thiruma A, Mark M. Evidence for a developmental role for TLR4 in learning and memory. PLoS One 2012, 7:e47522.
19. Walter S, Letiembre M, Liu Y, Heine H, Penke B, Hao W, Bode B, Manietta N, Walter J, Schulz-Schuffer W, Fassbender K. Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell Physiol Biochem 2007, 20(6):947-956.
20. Tang S, Lathia J, Selvaraj P, Jo D, Mughal M, Cheng A, Siler D, Markesbery W, Arumugam T, Mattson M. Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid beta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp Neurol 2008, 213:114-121.
21. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, Mattson MP. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci U S A 2007, 104:13798-13803.
22. Schnydrig S, Korner L, Landweer S, Ernst B, Walker G, Otten U, Kunz D. Peripheral lipopolysaccharide administration transiently affects expression of brain-derived neurotrophic factor, corticotropin and proopiomelanocortin in mouse brain. Neurosci Lett 2007, 429:69-73.
23. Belarbi K, Jopson T, Tweedie D, Arellano C, Luo W, Greig N, Rosi S. TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflammation 2012, 25:23.
24. Bossù P, Cutuli D, Palladino I, Caporali P, Angelucci F, Laricchiuta D, Gelfo F, De Bartolo P, Caltagirone C, Petrosini L. A single intraperitoneal injection of endotoxin in rats induces long-lasting modifications in behavior and brain protein levels of TNF-α and IL-18. J Neuroinflammation 2012, 9:101.
25. Semmler A, Frisch C, Debeir T, Ramanathan M, Okulla T, Klockgether T, Heneka M. Long-term cognitive impairment, neuronal loss and reduced cortical cholinergic innervation after recovery from sepsis in a rodent model. Exp Neurol 2007, 204:733-740.
26. Rosi S, Vazdarjanova A, Ramirez-Amaya V, Worley PF, Barnes CA, Wenk GL. Memantine protects against LPS-induced neuroinflammation, restores behaviorally-induced gene expression and spatial learning in the rat. Neuroscience 2006, 142:1303-1315.
27. Liu X, Wu Z, Hayashi Y, Nakanishi H. Age-dependent neuroinflammatory responses and deficits in long-term potentiation in the hippocampus during systemic inflammation. Neuroscience 2012, 216:133-142.
28. Thomson L, Sutherland R. Systemic administration of lipopolysaccharide and interleukin-1beta have different effects on memory consolidation. Brain Res Bull 2005, 67:24-29.
29. Kim JJ, Diamond DM. The stressed hippocampus, synaptic plasticity and lost memories. Nature Rev Neurosci 2002, 3:453-462.
30. Seguin JA, Brennan J, Mangano E, Hayley S. Proinflammatory cytokines differentially influence adult hippocampal cell proliferation depending upon the route and chronicity of administration. Neuropsychiatr Dis Treat 2009, 5:5-14.
31. Bruce-Keller AJ, Umberger G, McFall R, Mattson MP. Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann Neurol 1999, 45:8-15.
32. Halagappa VK, Guo Z, Pearson M, Matsuoka Y, Cutler RG, Laferla FM, Mattson MP. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease. Neurobiol Dis 2007, 26:212-220.
33. Singh R, Lakhanpal D, Kumar S, Sharma S, Kataria H, Kaur M, Kaur G. Late-onset intermittent fasting dietary restriction as a potential intervention to retard age-associated brain function impairments in male rats. Age (Dordr) 2012, 34:917-933.
34. Arumugam T, Phillips T, Cheng A, Morrell C, Mattson M. R W: Age and energy intake interact to modify multiple cellular stress response pathways involved in ischemic stroke outcome. Ann Neurol 2010, 67:41-52.
35. Glezer I, Munhoz CD, Kawamoto EM, Marcourakis T, Avellar MC, Scavone C. MK-801 and 7-Ni attenuate the activation of brain NF-kappa B induced by LPS. Neuropharmacology 2003, 45:1120-1129.
36. Baraldi T, Schöwe N, Balthazar J, Monteiro-Silva K, Albuquerque M, Buck H, Viel T. Cognitive stimulation during lifetime and in the aged phase improved spatial memory, and altered neuroplasticity and cholinergic markers of mice. Exp Gerontol 2013, 48:831-838.
37. Rong Y, Baudry M. Seizure activity results in a rapid induction of nuclear factor-kappa B in adult but not juvenile rat limbic structures. J Neurochem 1996, 67:662-668.
38. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
39. Salinovich O, Montelaro RC. Reversible staining and peptide mapping of proteins transferred to nitrocellulose after separation by sodium dodecylsulfate-polyacrylamide gel electrophoresis. Anal Biochem 1986, 156:341-347.
40. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
41. Qin L, Wu X, Block M, Liu Y, Breese G, Hong J, Knapp D, Crews F. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
42. Contestabile A, Monti B, Ciani E. Brain nitric oxide and its dual role in neurodegeneration/neuroprotection: understanding molecular mechanisms to devise drug approaches. Curr Med Chem 2003, 10:2147-2174.
43. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 2007, 8:766-775.
44. Ownby RL. Neuroinflammation and cognitive aging. Curr Psychiat Rep 2010, 12:39-45.
45. Ren L, Lubrich B, Biber K, Gebicke-Haerter PJ. Differential expression of inflammatory mediators in rat microglia cultured from different brain regions. Brain Res Mol Brain Res 1999, 65:198-205.
46. McGeer PL, McGeer EG. Inflammation and the degenerative diseases of aging. Ann N Y Acad Sci 2004, 1035:104-116.
47. Mattson MP. Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann N Y Acad Sci 2008, 1144:97-112.
48. Mattson MP, Wan R. Beneficial effects of intermittent fasting and caloric restriction on the cardiovascular and cerebrovascular systems. J Nutr Biochem 2005, 16:129-137.
49. Semmler A, Widmann C, Okulla T, Urbach H, Kaiser M, Widman G, Mormann F, Weide J, Fliessbach K, Hoeft A, Andreas H, Jessen F, Putensen C, Heneka M. Persistent cognitive impairment, hippocampal atrophy and EEG changes in sepsis survivors. J Neurol Neurosurg Psychiatry 2013, 84:62-69.
50. Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 1979, 93:74-104.
51. Harrison FE, Hosseini AH, McDonald MP. Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav Brain Res 2009, 198:247-251.
52. Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 1995, 81:905-915.
53. Dawood MY, Lumley LA, Robison CL, Saviolakis GA, Meyerhoff JL. Accelerated Barnes maze test in mice for assessment of stress effects on memory. Ann N Y Acad Sci 2004, 1032:304-307.
54. Izquierdo I, Medina JH, Vianna MR, Izquierdo LA, Barros DM. Separate mechanisms for short- and long-term memory. Behav Brain Res 1999, 103:1-11.
55. Jarvik ME, Kopp R. An improved one-trial passive avoidance learning situation. Psychol Rep 1967, 21:221-224.
56. Munhoz CD, Lepsch LB, Kawamoto EM, Malta MB, de Sá Lima L, Avellar MCW, Sapolsky RM, Scavone C. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-κB in the frontal cortex and hippocampus via glucocorticoid secretion. J Neurosci 2006, 26:3813-3820.
57. Frank M, Baratta M, Sprunger D, Watkins L, Maier S. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 2007, 21:47-59.
58. Mattson MP. Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab 2012, 16(6):706-722. doi:10.1016/j.cmet.2012.08.012. Epub 2012 Nov 15.
59. Okun E, Griffioen K, Barak B, Roberts NJ, Castro K, Pita MA, Cheng A, Mughal MR, Wan R, Ashery U, Mattson MP. Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis. Proc Natl Acad Sci U S A 2010, 107:15625-15630.
60. Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 2007, 9:1081-1088.
61. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010, 11:373-384.
62. Moncada S, Bolanos JP. Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 2006, 97:1676-1689.
63. Zanelli SA, Trimmer PA, Solenski NJ. Nitric oxide impairs mitochondrial movement in cortical neurons during hypoxia. J Neurochem 2006, 97:724-736.
64. Guix FX, Uribesalgo I, Coma M, Munoz FJ. The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 2005, 76:126-152.
65. Ksontini R, MacKay SL, Moldawer LL. Revisiting the role of tumor necrosis factor alpha and the response to surgical injury and inflammation. Arch Surg 1998, 133:558-567.
66. Moore KW, de Waal MR, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001, 19:683-765.
67. Strle K, Zhou JH, Shen WH, Broussard SR, Johnson RW, Freund GG, Dantzer R, Kelley KW. Interleukin-10 in the brain. Crit Rev Immunol 2001, 21:427-449.
68. Schottelius AJ, Mayo MW, Sartor RB, Baldwin AS. Interleukin-10 signaling blocks inhibitor of kappaB kinase activity and nuclear factor kappaB DNA binding. J Biol Chem 1999, 274:31868-31874.
69. Casadesus G, Smith MA, Basu S, Hua J, Capobianco DE, Siedlak SL, Zhu X, Perry G. Increased isoprostane and prostaglandin are prominent in neurons in Alzheimer disease. Mol Neurodegener 2007, 2:2.
70. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, White CL, Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci U S A 1989, 86:7611-7615.
71. Montine TJ, Sidell KR, Crews BC, Markesbery WR, Marnett LJ, Roberts LJ, Morrow JD. Elevated CSF prostaglandin E2 levels in patients with probable AD. Neurology 1999, 53:1495-1498.
72. Ben Menachem-Zidon O, Goshen I, Kreisel T, Ben Menahem Y, Reinhartz E, Ben Hur T, Yirmiya R. Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 receptor antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology 2008, 33:2251-2262.
73. Richwine AF, Sparkman NL, Dilger RN, Buchanan JB, Johnson RW. Cognitive deficits in interleukin-10-deficient mice after peripheral injection of lipopolysaccharide. Brain Behav Immun 2009, 23:794-802.
74. Hein AM, Stasko MR, Matousek SB, Scott-McKean JJ, Maier SF, Olschowka JA, Costa AC, O'Banion MK. Sustained hippocampal IL-1beta overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav Immun 2010, 24:243-253.
75. Shaftel SS, Kyrkanides S, Olschowka JA, Miller JN, Johnson RE, O'Banion MK. Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J Clin Invest 2007, 117:1595-1604.
76. Fiore M, Angelucci F, Alleva E, Branchi I, Probert L, Aloe L. Learning performances, brain NGF distribution and NPY levels in transgenic mice expressing TNF-alpha. Behav Brain Res 2000, 112:165-175.
77. Heyser CJ, Masliah E, Samimi A, Campbell IL, Gold LH. Progressive decline in avoidance learning paralleled by inflammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc Natl Acad Sci U S A 1997, 94:1500-1505.
78. Hein AM, Stutzman DL, Bland ST, Barrientos RM, Watkins LR, Rudy JW, Maier SF. Prostaglandins are necessary and sufficient to induce contextual fear learning impairments after interleukin-1 beta injections into the dorsal hippocampus. Neuroscience 2007, 150:754-763.
79. Oitzl MS, van Oers H, Schobitz B, de Kloet ER. Interleukin-1 beta, but not interleukin-6, impairs spatial navigation learning. Brain Res 1993, 613:160-163.
80. Gibertini M, Newton C, Friedman H, Klein TW. Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1-beta. Brain Behav Immun 1995, 9:113-128.
81. Pugh CR, Kumagawa K, Fleshner M, Watkins LR, Maier SF, Rudy JW. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav Immun 1998, 12:212-229.
82. Rachal Pugh C, Fleshner M, Watkins LR, Maier SF, Rudy JW. The immune system and memory consolidation: a role for the cytokine IL-1beta. Neurosci Biobehav Rev 2001, 25:29-41.
83. Esposito K, Pontillo A, Di Palo C, Giugliano G, Masella M, Marfella R, Giugliano D. Effect of weight loss and lifestyle changes on vascular inflammatory markers in obese women: a randomized trial. JAMA 2003, 289:1799-1804.
84. Sharman MJ, Volek JS. Weight loss leads to reductions in inflammatory biomarkers after a very-low-carbohydrate diet and a low-fat diet in overweight men. Clin Sci (Lond) 2004, 107:365-369.
85. Ugochukwu NH, Figgers CL. Caloric restriction inhibits up-regulation of inflammatory cytokines and TNF-alpha, and activates IL-10 and haptoglobin in the plasma of streptozotocin-induced diabetic rats. J Nutr Biochem 2007, 18:120-126.
86. Thackray AM, McKenzie AN, Klein MA, Lauder A, Bujdoso R. Accelerated prion disease in the absence of interleukin-10. J Virol 2004, 78:13697-13707.
87. Nadel L, Hardt O. Update on memory systems and processes. Neuropsychopharmacology 2011, 36:251-273.
88. Lapchak PA, Araujo DM, Hefti F. Systemic interleukin-1 beta decreases brain-derived neurotrophic factor messenger RNA expression in the rat hippocampal formation. Neuroscience 1993, 53:297-301.
89. Lipsky RH, Xu K, Zhu D, Kelly C, Terhakopian A, Novelli A, Marini AM. Nuclear factor kappaB is a critical determinant in N-methyl-D-aspartate receptor-mediated neuroprotection. J Neurochem 2001, 78:254-264.
90. Jiang X, Tian F, Mearow K, Okagaki P, Lipsky RH, Marini AM. The excitoprotective effect of N-methyl-D-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J Neurochem 2005, 94:713-722.
91. Lepsch LB, Munhoz CD, Kawamoto EM, Yshii LM, Lima LS, Curi-Boaventura MF, Salgado TM, Curi R, Planeta CS, Scavone C. Cocaine induces cell death and activates the transcription nuclear factor kappa-B in PC12 cells. Mol Brain 2009, 2:3.
92. Kawamoto EM, Lepsch LB, Boaventura MF, Munhoz CD, Lima LS, Yshii LM, Avellar MC, Curi R, Mattson MP, Scavone C. Amyloid beta-peptide activates nuclear factor-kappaB through an N-methyl-D-aspartate signaling pathway in cultured cerebellar cells. J Neurosci Res 2008, 86:845-860.