Effect of the branched-chain α-keto acids accumulating in maple syrup urine disease on S100B release from glial cells

Journal of the Neurological Sciences

Volumn 260, Issue 1-2, 2007, Pages 87-94

  Funchal, Cláudia ^a   Tramontina, Francine ^a   dos Santos, André Quincozes ^a   de Souza, Daniela Fraga ^a   Gonçalves, Carlos Alberto ^a   Pessoa Pureur, Regina ^a   Wajner, Moacir ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Antioxidants; Branched chain keto acids; Creatine; Kinase inhibitors; Maple syrup urine disease; S100B

Indexed keywords

2 OXOACID; 2 OXOISOCAPROIC ACID; 2 OXOISOVALERIC ACID; 3 METHYL 2 OXOVALERIC ACID; ANTIOXIDANT; CALMODULIN; CREATINE; CYCLIC AMP; GLUTATHIONE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PROTEIN KINASE; PROTEIN S100B; TROLOX C; UNCLASSIFIED DRUG; VALERIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GLIA CELL; MAPLE SYRUP URINE DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION;

ANIMALS; BRAIN; CELL DEATH; CELL LINE, TUMOR; CREATINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; ENZYME INHIBITORS; KETO ACIDS; MAPLE SYRUP URINE DISEASE; NERVE DEGENERATION; NERVE GROWTH FACTORS; NEUROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN KINASES; RATS; S100 PROTEINS;

EID: 34547699000     PISSN: 0022510X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jns.2007.04.011     Document Type: Article

References (83)

1. Chuang D.T., and Shih V.E. Maple syrup urine disease (branched-chain ketoaciduria). In: Scriver C.R., Beaudet A.L., Sly W.L., and Valle D. (Eds). The metabolic and molecular bases of inherited disease. 8th ed. (2001), McGraw-Hill, New York 1971-2005
2. Ogier de Baulny H., and Saudubray J.M. Branched-chain organic acidurias. Semin Neonatol 7 (2002) 65-74
3. Nyhan W.L. Maple syrup urine disease: branched-chain ketoaciduria. In: Nyhan W.L. (Ed). Abnormalities in amino acid metabolism in clinical medicine (1984), Appleton-Century-Crofts, Norwalk 21-35
4. Treacy E., Clow C.L., Reade T.R., Chitayat D., Mamer O.A., and Scriver C.R. Maple syrup urine disease: interrelationship between branched chain amino-, oxo-, and hydroxyacids; implications for treatment; association with CNS dysmelination. J Inherit Metab Dis 15 (1992) 121-135
5. Schadewaldt P., and Wendel U. Metabolism of branched-chain amino acids in maple syrup urine disease. Eur J Pediatr 156 (1997) 62-66
6. Snyderman S.E., Norton P.M., and Roitman E. Maple syrup urine disease with particular reference to diet therapy. Pediatrics 34 (1964) 454-472
7. Howell R.K., and Lee M. Influence of alpha-ketoacids on the respiration of brain in vitro. Proc Soc Exp Biol Med 113 (1963) 660-663
8. Halestrap A., Brand M.D., and Denton R.M. Inhibition of mitochondrial pyruvate transport by phenylpyruvate and α-ketoisocaproate. Biochim Biophys Acta 367 (1974) 102-108
9. Land J.M., Mowbray J., and Clark J.B. Control of pyruvate and β-hydroxy-butyrate utilization in rat brain mitochondria and its relevance to phenylketonuria and maple syrup urine disease. J Neurochem 26 (1976) 823-830
10. Danner D.J., and Elsas J.L. Disorders of branched chain amino acid and keto acid metabolism. In: Scriver C.R., Beaudet A.L., Sly W.S., and Valle D. (Eds). The metabolic basis of inherited disease (1989), Mc Graw Hill, New York 671-692
11. Yudkoff M., Daikhin Y., Lin Z.P., Nissin I., Stern J., Pleasure D., et al. Interrelationships of leucine and glutamate metabolism in cultured astrocytes. J Neurochem 62 (1994) 1192-11202
12. Zielke H.R., Zielke C.L., Baab P.J., and Collins R.M. Large neutral amino acids auto exchange when infused by microdialysis into the rat brain: implications for maple syrup urine disease and phenylketonuria. Neurochem Int 40 (2002) 347-354
13. Pilla C., Cardozo R.F., Dutra-Filho C.S., Wyse A.T., Wajner M., and Wannmacher C.M. Creatine kinase activity from rat brain is inhibited by branched-chain amino acids in vitro. Neurochem Res 28 (2003) 675-679
14. Sgaravati A.M., Rosa R.B., Schuck P.F., Ribeiro C.A.J., Wannmacher C.M.D., Wyse A.T.S., et al. Inhibition of brain energy metabolism by the α-keto acids accumulating in maple syrup urine disease. Biochim Biophys Acta 1639 (2003) 232-238
15. Funchal C., Schuck P.F., Santos A.Q., Jacques-Silva M.C., Gottfried C., Pessoa-Pureur R., et al. Creatine and antioxidant treatment prevent the inhibition of creatine kinase activity and the morphological alterations of C6 glioma cells induced by the branched-chain alfa-keto acids accumulating in maple syrup urine disease. Cell Mol Neurobiol 26 (2006) 67-79
16. Tashian R. Inhibition of brain glutamic acid descarboxylase by phenylalanine, leucine and valine derivates: a suggestion concerning the neurological defect in phenylketonuria and branched-chain keto aciduria. Metabolism 10 (1961) 393-400
17. Appel S.H. Inhibition of brain protein synthesis: an approach to a biochemical basis of neurological dysfunction in the amino-acidurias. Trans N Y Acad Sci 29 (1966) 63-70
18. Taketomi T., Kunishita T., Hara A., and Mizushima S. Abnormal protein and lipidic composition of the cerebral myelin of a patient with maple syrup urine disease. Jpn J Exp Med 53 (1983) 109-116
19. Tribble D., and Shapira R. Myelin proteins: degradation in rat brain initiated by metabolites causative of maple syrup urine disease. Biochem Biophys Res Commun 114 (1983) 440-446
20. Wajner M., and Vargas C.R. Reduction of plasma concentrations of large neutral amino acids in patients with maple urine disease during crises. Arch Dis Child 80 (1999) 579
21. Wajner M., Coelho D.M., Barschak A.G., Araújo P.R., Pires R.F., Lulhier F.L.G., et al. Reduction of large neutral amino acid concentration in plasma and CSF of patients with maple syrup urine disease during crises. J Inherit Metab Dis 23 (2000) 505-512
22. Fontella F.U., Gassen E., Pulrolnik V., Wannmacher C.M.D., Klein A.B., Wajner M., et al. Stimulation of lipid peroxidation in vitro in rat brain by the metabolites accumulating in maple syrup urine disease. Metab Brain Dis 17 (2002) 47-54
23. Bridi R., Araldi J., Sgarbi M.B., Testa C.G., Durigon K., Wajner M., et al. Induction of oxidative stress in rat brain by the metabolites accumulating in maple syrup urine disease. Int J Dev Neurosci 21 (2003) 327-332
24. Bridi R., Braun C.A., Zorzi G.K., Wannmacher C.M., Wajner M., Lissi E.G., et al. Alpha-keto acids accumulating in maple syrup urine disease stimulate lipid peroxidation and reduce antioxidant defences in cerebral cortex from young rats. Metab Brain Dis 20 (2005) 155-167
25. Bridi R., Latini A., Braum C.A., Zorzi G.K., Wajner M., Lissi E., et al. Evaluation of the mechanisms involved in leucine-induced oxidative damage in cerebral cortex of young rats. Free Radic Res 39 (2005) 71-79
26. Araújo P., Wassermann G.F., Tallini K., Furlanetto V., Vargas C.R., Wannmacher C.M., et al. Reduction of large neutral amino acid level in plasma and brain of hyperleucinemic rats. Neurochem Int 38 (2001) 529-537
27. 2+ homeostasis and cell death. J Neurochem 70 (1998) 958-970
28. Takuma K., Baba A., and Matsuda T. Astrocyte apoptosis: implications for neuroprotection. Prog Neurobiol 72 (2004) 111-127
29. Kobayashi K., Hayashi M., Nakano H., Fukutani Y., Sasaki K., Shimazaki M., et al. Apoptosis of astrocytes with enhanced lysosomal activity and oligodendrocytes in white matter lesions in Alzheimer's disease. Neuropathol Appl Neurobiol 28 (2002) 238-251
30. Vernadakis A., Kentroti S., Brodie C., Mangoura D., and Sakellaridis N. C6 glioma cells of early passage have progenitor properties in culture. Adv Exp Med Biol 296 (1991) 181-195
31. Vernadakis A., Lee K., Kentroti S., and Brodie C. Role of astrocytes in aging: late passage primary mouse brain astrocytes and C6 glial cells as models. Prog Brain Res 94 (1992) 391-409
32. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33 (2001) 637-668
33. Ivanekov V.V., Jamieson G.A., Dimlich R.V., and Gruenstein R.V. Characterization of S-100B binding epitopes. Identification of a novel target, the actin capping protein, CapZ. J Biol Chem 270 (1995) 14651-14658
34. Donato R. Calcium-sensitivity of brain microtubule proteins in the presence of S-100 proteins. Cell Calcium 6 (1985) 343-361
35. Sorci G., Agneletti A.L., Bianchi R., and Donato R. Association of S100B with intermediate filaments and microtubules in glial cells. Biochim Biophys Acta 1448 (1998) 277-289
36. Sorci G., Agneletti A.L., and Donato R. Effects of S100A1 and S100B on microtubule stability. An in vitro study using triton-cytoskeletons from astrocyte and myoblast cell lines. Neuroscience 99 (2000) 773-783
37. 2+-dependent manner. J Biol Chem 268 (1993) 12669-12674
38. Van Eldik L.J., and Wainwright M.S. The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci 21 (2003) 97-108
39. Gonçalves D., Karl J., Leite M., Rotta L., Salbego C., Rocha E., et al. High glutamate decreases S100B secretion stimulated by serum deprivation in astrocytes. NeuroReport 13 (2002) 1533-1535
40. Büyuküysal R.L. Protein S100B release from rat brain slices during and after ischemia: comparison with lactate dehydrogenase leakage. Neurochem Int 47 (2005) 580-588
41. Tramontina F., Leite M.C., Goncalves D., Tramontina A.C., Souza D.F., Frizzo J.K., et al. High glutamate decreases S100B secretion by a mechanism dependent on the glutamate transporter. Neurochem Res 31 (2006) 815-820
42. Yudkoff M., Daikhin Y., Nissim I., Horyn O., Luhovyy B., and Nissim I. Brain amino acid requirements and toxicity: the example of leucine. J Nutr 135 (2005) 158S-1531S
43. Funchal C., Rosa A.M., Wajner M., Wofchuk S., and Pessoa-Pureur R. Reduction of glutamate uptake into cerebral cortex of developing rats by the branched-chain α-keto acids accumulating in maple syrup urine disease. Neurochem Res 29 (2004) 747-753
44. Tramontina F., Karl J., Gottfried C., Mendez A., Gonçalves D., Portela L.V., et al. Digitonin-permeabilization of astrocytes in culture monitored by trypan blue exclusion and loss of S100B by ELISA. Brain Res Protoc 6 (2000) 86-90
45. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-267
46. Mangoura D., Sakellaridis N., Jones J., and Vernadakis A. Early and late passage C6 glial cell growth: similarities with primary glial cells in culture. Neurochem Res 14 (1989) 941-947
47. Goya L., Feng P.T., Aliabadi S., and Timiras P.S. Effect of growth factors on the in vitro growth and differentiation of early and late passages of C6 glioma cells. Int J Dev Neurosci 14 (1996) 409-417
48. Haghighat N., and McCandless D.W. Effect of ammonium chloride on energy metabolism of astrocytes and C6-glioma cells. Metab Brain Dis 12 (1997) 287-298
49. Bonini P., Cicconi S., Cardinale A., Vitale C., Serafino A.L., Ciotti M.T., et al. Oxidative stress induces p53-mediated apoptosis in glia: p53 transcription-independent way to die. J Neurosci Res 75 (2004) 83-95
50. Smale G., Nichols N.R., Brady D.R., Finch C.E., and Horton W.E.J. Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 133 (1995) 225-230
51. Sonnewald U., Qu H., and Aschner M. Pharmacology and toxicology of astrocyte-neuron glutamate transport and cycling. J Pharmacol Exp Ther 301 (2002) 1-6
52. Donato R. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60 (2003) 540-551
53. Schulpis K.H., Kariyannis C., and Papassotiriou I. Serum levels of neural protein S-100B in phenylketonuria. Clin Biochem 37 (2004) 76-79
54. Wiltfang J., Nolte W., Otto M., Wildberg J., Bahn E., Figulla H.R., et al. Elevated serum levels of astroglial S100 beta in patients with liver cirrhosis indicate early and subclinical portal-systemic encephalopathy. Metab Brain Dis 14 (1999) 239-251
55. Leite M.C., Brolese G., Almeida L.M.V., Pinero C.C., Gottfried C., and Gonçalves C.A. Ammonia-induced alteration in S100B secretion in astrocytes is not reversed by creatine addition. Brain Res Bull 70 (2006) 179-185
56. Hutson S.M., Berkich D., Drown P., Xu B., Aschner M., and LaNoue K.F. Role of branched-chain aminotransferase isoenzymes and gabapentin in neurotransmitter metabolism. J Neurochem (1998) 863-874
57. Bixel M., Shimomura Y., Hutson S., and Hamprecht B. Distribution of key enzymes of branched-chain metabolism in glial and neuronal cells in culture. J Histochem Cytochem 49 (2001) 407-418
58. Jouvet P., Rustin P., Taylor D.L., Pocock J.M., Felderhoff-Mueser U., Mazarakis N.D., et al. Branched-chain amino acids induce apoptosis in neural cells without mitochondrial membrane depolarization or cytochrome c release: implications for neurological impairment associated with maple syrup urine disease. Mol Biol Cell 11 (2000) 1919-1932
59. Funchal C., de Lima Pelaez P., Oliveira Loureiro S., Vivian L., Dall Bello Pessutto F., Almeida L.M.V., et al. α-Ketoisocaproic acid regulates phosphorylation of intermediate filaments in postnatal rat cortical slices through ionotropic glutamatergic receptors. Dev Brain Res 139 (2002) 267-276
60. Funchal C., Dall Bello Pessutto F., Almeida L.M.V., de Lima Pelaez P., Oliveira Loureiro S., Vivian L., et al. α-Keto-β-methylvaleric acid increases the in vitro phosphorylation of intermediate filaments in cerebral cortex of young rats though the GABAergic system. J Neurol Sci 217 (2004) 17-24
61. Wilken B., Ramirez J.M., Probst I., Rchter D.W., and Henefeld F. Creatine protects the central respiratory network of mammals under anoxic conditions. Pediatr Res 43 (1998) 8-14
62. Sullivan P.G., Geiser J.D., Mattson M.P., and Scheff S.W. Dietary supplement creatine protects against traumatic bran injury. Ann Neurol 48 (2000) 723-729
63. Zhang W., Narayanan M., and Friedlander R.M. Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann Neurol 53 (2003) 267-270
64. Scheff S.W., and Dhillon H.S. Creatine-enhanced diet alters levels of lactate and free fatty acids after experimental brain injury. Neurochem Res 29 (2004) 469-479
65. Brustovetsky N., Brustovetsky T., and Dubiski J.M. On the mechanisms of neuroprotection by creatine and phosphocreatine. J Neurochem 76 (2001) 425-434
66. Clarke D.D., and Sokoloff L. Circulation and energy metabolism of the brain. In: Siegel G.J., Agranoff B.W., Wayne Albers R., Fisher S.K., and Uhler M.D. (Eds). Basic neurochemistry (1999), Lippincott Wiliams and Wilkins, Philadelphia (PA) 638-669
67. Wyss M., and Kaddurah-Daouk R. Creatine and creatinine metabolism. Physiol Rev 80 (2000) 1107-1212
68. Lesman M., Korzhevskii D.E., Mourovets V., Kostkin V.B., Izvarina N., Perasso L., et al. Intracerebroventricular administration of creatine protects against damage by global cerebral ischemia in rat. Brain Res 1114 (2006) 187-194
69. Lawler J.M., Barnes W.S., Wu G.Y., Song W., and Demaree S. Direct antioxidant properties of creatine. Biochem Biophys Res Commun 290 (2002) 47-52
70. Almeida L.S., Salomons G.S., Hogenboom F.C., Jakobs C., and Schoffelmeer A.N.M. Exocytotic release of creatine in rat brain. Synapse 60 (2006) 118-123
71. Coitinho A.S., Mello C.F., Lima T.T., Bastiani J., Figuera M.R., and Wajner M. Pharmacological evidence that alpha-ketoisovaleric acid induces convulsions through GABAergic and glutamatergic mechanisms in rats. Brain Res 894 (2001) 68-73
72. Funchal C., Latini A., Jacques-Silva M.C., Santos A.Q., Buzin L., Gottfried C., et al. Branched-chain alpha-ketoacids accumulating in maple syrup urine disease induce morphological alterations and oxidative stress in glial cells. Neurochem Int 49 (2006) 640-650
73. Meister A., and Anderson M.E. Glutathione. Annu Ver Biochem 52 (1983) 711-760
74. Arstall M.A., Bailey C., Gross W.L., Bak M., Balligand J.L., and Kelly R.A. Reversible S-nitrosation of creatine kinase by nitric oxide in adult rat ventricular myocytes. J Mol Cell Cardiol 30 (1998) 979-988
75. Radi R., Cassina A., and Hodara R. Nitric oxide and peroxynitrite interactions with mitochondria. Biol Chem 383 (2002) 401-409
76. Han Z., Chen Y.R., Jones C.I., Meenakshiundaram G., Zweier J.L., and Alevriadou B.R. Shear-induced reactive nitrogen species inhibit mitochondrial respiratory complex activities in cultures vascular endothelial cells. Am J Physiol Cell Physiol 292 (2007) C1103-C1112
77. 2+ levels regulate the alternative cell density-dependent secretion of S100B in human glioblastoma cells. J Biol Chem 276 (2001) 30819-30826
78. 2+ and cAMP. Neurochem Res 30 (2005) 1139-1146
79. Balazs R., Miller S., Chun Y., and Cotman C.W. Receptor-coupled phospholipase C and adenylyl cyclase function with different calcium pools in astrocytes. NeuroReport 11 (1998) 1397-1401
80. Guix F.X., Uribesalgo I., Coma M., and Munoz F.J. The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76 (2005) 126-152
81. Hashimoto A., Miyakoda G., Hirose Y., and Mori T. Activation of endothelial nitric oxide synthase by cilostazol via a cAMP/protein kinase A- and phosphatidylinositol 3-kinase/Akt-dependent mechanism. Atherosclerosis 189 (2006) 350-357
82. Hoffmann G.F., Meier-Augestein W., Srockler S., Surtees R., Rating D., and Nyan W.L. Physiology and pathophysiology of organic acids in cerebrospinal fluid. J Inherit Metab Dis 16 (1993) 646-669
83. Sauer S.W., Okun J.G., Fricker G., Mahringer A., Muller I., Crnic L.R., et al. Intracerebral accumulation of glutaric and 3-hydroxyglutaric acids secondary to limited flux across the blood-brain barrier constitute a biochemical risk factor for neurodegeneration in glutaryl-CoA dehydrogenase deficiency. J Neurochem 97 (2006) 899-910