Chronic administration of methylmalonate on young rats alters neuroinflammatory markers and spatial memory

Immunobiology

Volumn 218, Issue 9, 2013, Pages 1175-1183

  Ribeiro, Leandro Rodrigo ^a   Della Pace, Iuri Domingues ^a   de Oliveira Ferreira, Ana Paula ^a   Funck, Vinícius Rafael ^a   Pinton, Simone ^a   Bobinski, Franciane ^b   de Oliveira, Clarissa Vasconcelos ^a   da Silva Fiorin, Fernando ^a   Duarte, Marta Maria Medeiros Frescura ^c   Furian, Ana Flávia ^a   Oliveira, Mauro Schneider ^a   Nogueira, Cristina Wayne ^a   dos Santos, Adair Roberto Soares ^a,b   Royes, Luiz Fernando Freire ^a   Fighera, Michele Rechia ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^c UNIVERSIDADE LUTERANA DO BRASIL   (Brazil)

Author keywords

Cerebral cortex; Memory; Methylmalonate; Neuroinflammation; Rat

Indexed keywords

3 NITROTYROSINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; METHYLMALONIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ACIDEMIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR CHANGE; BRAIN CORTEX; CELL DIFFERENTIATION; CELL TYPE; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE MARKER; EXPLORATORY BEHAVIOR; FEMALE; IMMUNE RESPONSE; MALE; MAZE TEST; MONONUCLEAR CELL; NERVOUS SYSTEM INFLAMMATION; NEUTROPHIL COUNT; NONHUMAN; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL MEMORY; WISTAR RAT;

3-NITROTYROSINE; 3-NT; 5-BROMO-4-CHLORO-3-INDOLYL PHOSPHATE AND P-NITRO BLUE TETRAZOLIUM; BBB; BCIP/NBT; BLOOD-BRAIN BARRIER; BOVINE SERUM ALBUMIN; BSA; CENTRAL NERVOUS SYSTEM; CEREBRAL CORTEX; CNS; COX-2; CYCLOOXYGENASE-2; ELEVATED PLUS MAZE; ELISA; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY/ULTRAVIOLET; HPLC-UV; IEM; IL-1Β; INBORN ERROR OF METABOLISM; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; INTERLEUKIN-1 BETA; MCM; MEMORY; METHYLMALONATE; METHYLMALONIC ACID, METHYLMALONATE; METHYLMALONYL-COA MUTASE; MMA; N-METHYL-D-ASPARTATE; NEUROINFLAMMATION; NFΚB; NMDA; NUCLEAR FACTOR KAPPA B; OBJECTS EXPLORATION TEST; OET; PBS; PHOSPHATE BUFFERED SALINE; R.I.; RAT; RECOGNITION INDEX; S.C.; SDS; SEM; SODIUM DODECYL SULFATE-POLYACRYLAMIDE GELS; STANDARD ERROR OF THE MEAN; SUBCUTANEOUSLY; TBS; TBS-T; TNF-Α; TRIS-BORATE SALINE; TUMOR NECROSIS FACTOR-ALPHA; TWEEN 20 IN TRIS-BORATE SALINE;

AMINO ACID METABOLISM, INBORN ERRORS; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CEREBRAL CORTEX; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; MEMORY DISORDERS; METHYLMALONIC ACID; NEUROIMMUNOMODULATION; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, WISTAR; SPATIAL BEHAVIOR; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE;

EID: 84880037841     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2013.04.008     Document Type: Article

References (81)

1. Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 2004, 75:639.
2. Aronica E., Crino P.B. Inflammation in epilepsy: clinical observations. Epilepsia 2011, 52(Suppl. 3):26.
3. Baumgarter E.R., Viardot C. Long-term follow-up of 77 patients with isolated methylmalonic acidaemia. J. Inherit. Metab. Dis. 1995, 18:138.
4. Belarbi K., Arellano C., Ferguson R., Jopson T., Rosi S. Chronic neuroinflammation impacts the recruitment of adult-born neurons into behaviorally relevant hippocampal networks. Brain Behav. Immun. 2012, 26:18.
5. Bernardino L., Xapelli S., Silva A.P., Jakobsen B., Poulsen F.R., Oliveira C.R., Vezzani A., Malva J.O., Zimmer J. Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci. 2005, 25:6734.
6. Bevins R.A., Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat. Protoc. 2006, 1:1306.
7. Bezzi P., Domercq M., Brambilla L., Galli R., Schols D., De Clercq E., Vescovi A., Bagetta G., Kollias G., Meldolesi J., Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 2001, 4:702.
8. Bins M., Huiges W., Timmers T., Gelsema E.S., Halie M.R. Neutrophil granulation stained with May Grunwald Giemsa or pure Azure B-eosin Y quantified by image analysis. Blut 1989, 58:79.
9. Bossu 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-alpha and IL-18. J. Neuroinflammation 2012, 9:101.
10. Bradford M.M. 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.
11. Brusque A., Rotta L., Pettenuzzo L.F., Junqueira D., Schwarzbold C.V., Wyse A.T., Wannmacher C.M., Dutra-Filho C.S., Wajner M. Chronic postnatal administration of methylmalonic acid provokes a decrease of myelin content and ganglioside N-acetylneuraminic acid concentration in cerebrum of young rats. Braz. J. Med. Biol. Res. 2001, 34:227.
12. Cameron B., Landreth G.E. Inflammation, microglia, and Alzheimer's disease. Neurobiol. Dis. 2010, 37:503.
13. Casu M.A., Sanna A., Spada G.P., Falzoi M., Mongeau R., Pani L. Effects of acute and chronic valproate treatments on p-CREB levels in the rat amygdala and nucleus accumbens. Brain Res. 2007, 1141:15.
14. Chandler R.J., Zerfas P.M., Shanske S., Sloan J., Hoffmann V., DiMauro S., Venditti C.P. Mitochondrial dysfunction in mut methylmalonic acidemia. FASEB J. 2009, 23:1252.
15. Chen J., Marsh T., Zhang J.S., Graham S.H. Expression of cyclo-oxygenase 2 in rat brain following kainate treatment. Neuroreport 1995, 6:245.
16. Chung K.K. Say NO to neurodegeneration: role of S-nitrosylation in neurodegenerative disorders. Neurosignals 2006, 15:307.
17. Chung Y.C., Ko H.W., Bok E., Park E.S., Huh S.H., Nam J.H., Jin B.K. The role of neuroinflammation on the pathogenesis of Parkinson's disease. BMB Rep. 2010, 43:225.
18. Cippitelli A., Zook M., Bell L., Damadzic R., Eskay R.L., Schwandt M., Heilig M. Reversibility of object recognition but not spatial memory impairment following binge-like alcohol exposure in rats. Neurobiol. Learn. Mem. 2010, 94:538.
19. de Mattos-Dutra A., Meirelles R., Bevilaqua da Rocha B., Kommers T., Wofchuk S.T., Wajner M., Pessoa-Pureur R. Methylmalonic and propionic acids increase the in vitro incorporation of 32P into cytoskeletal proteins from cerebral cortex of young rats through NMDA glutamate receptors. Brain Res. 2000, 856:111.
20. de Mello C.F., Begnini J., Jimenez-Bernal R.E., Rubin M.A., de Bastiani J., da Costa E., Wajner M. Intrastriatal methylmalonic acid administration induces rotational behavior and convulsions through glutamatergic mechanisms. Brain Res. 1996, 721:120.
21. de Mello C.F., Rubin M.A., Coelho J., Wajner M., Souza D.O. Effects of methylmalonate and propionate on [3H]glutamate binding, adenylate cyclase activity and lipid synthesis in rat cerebral cortex. Biochem. Mol. Biol. Int. 1997, 42:1143.
22. Dutra J.C., Wajner M., Wannmacher C.M., Wannmacher L.E., Pires R.F., Rosa-Junior A. Effect of postnatal methylmalonate administration on adult rat behavior. Braz. J. Med. Biol. Res. 1991, 24:595.
23. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13632.
24. Erdal N., Gurgul S., Tamer L., Ayaz L. Effects of long-term exposure of extremely low frequency magnetic field on oxidative/nitrosative stress in rat liver. J. Radiat. Res. (Tokyo) 2008, 49:181.
25. Fernandes C.G., Borges C.G., Seminotti B., Amaral A.U., Knebel L.A., Eichler P., de Oliveira A.B., Leipnitz G., Wajner M. Experimental evidence that methylmalonic acid provokes oxidative damage and compromises antioxidant defenses in nerve terminal and striatum of young rats. Cell. Mol. Neurobiol. 2011, 31:775.
26. File S.E., Gonzalez L.E. Anxiolytic effects in the plus-maze of 5-HT1A-receptor ligands in dorsal raphe and ventral hippocampus. Pharmacol. Biochem. Behav. 1996, 54:123.
27. File S.E., Mahal A., Mangiarini L., Bates G.P. Striking changes in anxiety in Huntington's disease transgenic mice. Brain Res. 1998, 805:234.
28. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918.
29. Goyenechea E., Andrade F., de Las Heras J., Lage S., Prieto J.A., Ruiz N., Aldamiz-Echevarria L. Expression of proinflammatory factors in renal cortex induced by methylmalonic acid. Ren. Fail. 2012, 34:885.
30. Guerra-Moreno J., Barrios N., Santiago-Borrero P.J. Severe neutropenia in an infant with methylmalonic acidemia. Bol. Asoc. Med. P.R. 2003, 95:17.
31. Hein A.M., O'Banion M.K. Neuroinflammation and memory: the role of prostaglandins. Mol. Neurobiol. 2009, 40:15.
32. Hein A.M., O'Banion M.K. Neuroinflammation and cognitive dysfunction in chronic disease and aging. J. Neuroimmune Pharmacol. 2012, 7:3.
33. Hemmens B., Mayer B. Enzymology of nitric oxide synthases. Methods Mol. Biol. 1998, 100:1.
34. Horster F., Hoffmann G.F. Pathophysiology, diagnosis, and treatment of methylmalonic aciduria-recent advances and new challenges. Pediatr. Nephrol. 2004, 19:1071.
35. Horster F., Baumgartner M.R., Viardot C., Suormala T., Burgard P., Fowler B., Hoffmann G.F., Garbade S.F., Kolker S., Baumgartner E.R. Long-term outcome in methylmalonic acidurias is influenced by the underlying defect (mut0, mut-, cblA, cblB). Pediatr. Res. 2007, 62:225.
36. Hu S., Sheng W.S., Ehrlich L.C., Peterson P.K., Chao C.C. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation 2000, 7:153.
37. Hutchinson R.J., Bunnell K., Thoene J.G. Suppression of granulopoietic progenitor cell proliferation by metabolites of the branched-chain amino acids. J. Pediatr. 1985, 106:62.
38. Ischiropoulos H., Beckman J.S. Oxidative stress and nitration in neurodegeneration: cause, effect, or association?. J. Clin. Invest. 2003, 111:163.
39. Izquierdo I., Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 1997, 68:285.
40. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Medina J.H., Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 2006, 29:496.
41. Kobayashi S.D., DeLeo F.R. Role of neutrophils in innate immunity: a systems biology-level approach. Wiley Interdiscip. Rev. Syst. Biol. Med. 2009, 1:309.
42. Kolker S., Ahlemeyer B., Krieglstein J., Hoffmann G.F. Methylmalonic acid induces excitotoxic neuronal damage in vitro. J. Inherit. Metab. Dis. 2000, 23:355.
43. Lee J.K., Tran T., Tansey M.G. Neuroinflammation in Parkinson's disease. J. Neuroimmune Pharmacol. 2009, 4:419.
44. Leonard J.V. The management and outcome of propionic and methylmalonic acidaemia. J. Inherit. Metab. Dis. 1995, 18:430.
45. Lu J.Q., Joseph J.T., Nash R.A., Storek J., Stevens A.M., Metz L.M., Clark A.W., Johnson E.S., Yong V.W. Neuroinflammation and demyelination in multiple sclerosis after allogeneic hematopoietic stem cell transplantation. Arch. Neurol. 2010, 67:716.
46. Lucas S.M., Rothwell N.J., Gibson R.M. The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 2006, 147(Suppl. 1):S232.
47. +-ATPase activity in the rat striatum and cerebral cortex. Epilepsia 2003, 44:761.
48. Manoli, I., Venditti, C.P., 1993. Methylmalonic Acidemia. Seattle (WA).
49. Mayo L., Quintana F.J., Weiner H.L. The innate immune system in demyelinating disease. Immunol. Rev. 2012, 248:170.
50. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287:248.
51. Medeiros R., Prediger R.D., Passos G.F., Pandolfo P., Duarte F.S., Franco J.L., Dafre A.L., Di Giunta G., Figueiredo C.P., Takahashi R.N., Campos M.M., Calixto J.B. Connecting TNF-alpha signaling pathways to iNOS expression in a mouse model of Alzheimer's disease: relevance for the behavioral and synaptic deficits induced by amyloid beta protein. J. Neurosci. 2007, 27:5394.
52. Melo D.R., Kowaltowski A.J., Wajner M., Castilho R.F. Mitochondrial energy metabolism in neurodegeneration associated with methylmalonic acidemia. J. Bioenerg. Biomembr. 2011, 43:39.
53. Merrill J.E. Tumor necrosis factor alpha, interleukin 1 and related cytokines in brain development: normal and pathological. Dev. Neurosci. 1992, 14:1.
54. Mirandola S.R., Melo D.R., Schuck P.F., Ferreira G.C., Wajner M., Castilho R.F. Methylmalonate inhibits succinate-supported oxygen consumption by interfering with mitochondrial succinate uptake. J. Inherit. Metab. Dis. 2008, 31:44.
55. Moller T. Neuroinflammation in Huntington's disease. J. Neural Transm. 2010, 117:1001.
56. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760.
57. Nathan C., Xie Q.W. Nitric oxide synthases: roles, tolls, and controls. Cell 1994, 78:915.
58. Oberholzer V.G., Levin B., Burgess E.A., Young W.F. Methylmalonic aciduria. An inborn error of metabolism leading to chronic metabolic acidosis. Arch. Dis. Child. 1967, 42:492.
59. Pettenuzzo L.F., Wyse A.T., Wannmacher C.M., Dutra-Filho C.S., Netto C.A., Wajner M. Evaluation of the effect of chronic administration of drugs on rat behavior in the water maze task. Brain Res. Brain Res. Protoc. 2003, 12:109.
60. Pettenuzzo L.F., Schuck P.F., Wyse A.T., Wannmacher C.M., Dutra-Filho C.S., Netto C.A., Wajner M. Ascorbic acid prevents water maze behavioral deficits caused by early postnatal methylmalonic acid administration in the rat. Brain Res. 2003, 976:234.
61. Pinton S., da Rocha J.T., Gai B.M., Nogueira C.W. Sporadic dementia of Alzheimer's type induced by streptozotocin promotes anxiogenic behavior in mice. Behav. Brain Res. 2011, 223:1.
62. Radmanesh A., Zaman T., Ghanaati H., Molaei S., Robertson R.L., Zamani A.A. Methylmalonic acidemia: brain imaging findings in 52 children and a review of the literature. Pediatr. Radiol. 2008, 38:1054.
63. Ransohoff R.M., Brown M.A. Innate immunity in the central nervous system. J. Clin. Invest. 2012, 122:1164.
64. Ribeiro L.R., Fighera M.R., Oliveira M.S., Furian A.F., Rambo L.M., Ferreira A.P., Saraiva A.L., Souza M.A., Lima F.D., Magni D.V., Dezengrini R., Flores E.F., Butterfield D.A., Ferreira J., dos Santos A.R., Mello C.F., Royes L.F. Methylmalonate-induced seizures are attenuated in inducible nitric oxide synthase knockout mice. Int. J. Dev. Neurosci. 2009, 27:157.
65. Romero-Calvo I., Ocon B., Martinez-Moya P., Suarez M.D., Zarzuelo A., Martinez-Augustin O., de Medina F.S. Reversible Ponceau staining as a loading control alternative to actin in Western blots. Anal. Biochem. 2010, 401:318.
66. Royes L.F., Fighera M.R., Furian A.F., Oliveira M.S., Fiorenza N.G., de Carvalho Myskiw J., Frussa-Filho R., Mello C.F. Involvement of NO in the convulsive behavior and oxidative damage induced by the intrastriatal injection of methylmalonate. Neurosci. Lett. 2005, 376:116.
67. Royes L.F., Fighera M.R., Furian A.F., Oliveira M.S., Myskiw Jde C., Fiorenza N.G., Petry J.C., Coelho R.C., Mello C.F. Effectiveness of creatine monohydrate on seizures and oxidative damage induced by methylmalonate. Pharmacol. Biochem. Behav. 2006, 83:136.
68. Salvadori M.G., Bandero C.R., Jesse A.C., Gomes A.T., Rambo L.M., Bueno L.M., Bortoluzzi V.T., Oliveira M.S., Mello C.F. Prostaglandin E(2) potentiates methylmalonate-induced seizures. Epilepsia 2012, 53:189.
69. Schopfer F.J., Baker P.R., Freeman B.A. NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response?. Trends Biochem. Sci. 2003, 28:646.
70. Shigematsu Y., Hirano S., Hata I., Tanaka Y., Sudo M., Sakura N., Tajima T., Yamaguchi S. Newborn mass screening and selective screening using electrospray tandem mass spectrometry in Japan. J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci. 2002, 776:39.
71. Song H.S., Son M.J., Lee Y.M., Kim W.J., Lee S.W., Kim C.W., Kim K.W. Oxygen tension regulates the maturation of the blood-brain barrier. Biochem. Biophys. Res. Commun. 2002, 290:325.
72. Stolp H.B., Johansson P.A., Habgood M.D., Dziegielewska K.M., Saunders N.R., Ek C.J. Effects of neonatal systemic inflammation on blood-brain barrier permeability and behaviour in juvenile and adult rats. Cardiovasc. Psychiatry Neurol. 2011, 2011:469046.
73. Vargas D.L., Nascimbene C., Krishnan C., Zimmerman A.W., Pardo C.A. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann. Neurol. 2005, 57:67.
74. Vasques V., Brinco F., Viegas C.M., Wajner M. Creatine prevents behavioral alterations caused by methylmalonic acid administration into the hippocampus of rats in the open field task. J. Neurol. Sci. 2006, 244:23.
75. Venneti S., Wiley C.A., Kofler J. Imaging microglial activation during neuroinflammation and Alzheimer's disease. J. Neuroimmune Pharmacol. 2009, 4:227.
76. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F., De Simoni M.G. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J. Neurosci. 1999, 19:5054.
77. Viviani B., Bartesaghi S., Gardoni F., Vezzani A., Behrens M.M., Bartfai T., Binaglia M., Corsini E., Di Luca M., Galli C.L., Marinovich M. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J. Neurosci. 2003, 23:8692.
78. Wajner M., Coelho J.C. Neurological dysfunction in methylmalonic acidaemia is probably related to the inhibitory effect of methylmalonate on brain energy production. J. Inherit. Metab. Dis. 1997, 20:761.
79. Wajner M., Brites E.C., Dutra J.C., Buchalter M.S., Pons A.H., Pires R.F., Wannmacher L.E., Rosa Junior A., Trindade V.M., Wannmacher C.M. Diminished concentrations of ganglioside N-acetylneuraminic acid (G-NeuAc) in cerebellum of young rats receiving chronic administration of methylmalonic acid. J. Neurol. Sci. 1988, 85:233.
80. Watkins D., Rosenblatt D.S. Inborn errors of cobalamin absorption and metabolism. Am. J. Med. Genet. C: Semin. Med. Genet. 2011, 157:33.
81. +-ATPase activity in cerebral cortex of rats. Neuroreport 2000, 11:2331.