Therapeutic modulation of cerebral l-lysine metabolism in a mouse model for glutaric aciduria type I

Brain

Volumn 134, Issue 1, 2011, Pages 157-170

  Sauer, Sven W ^a   Opp, Silvana ^a   Hoffmann, Georg F ^a   Koeller, David M ^b   Okun, Jürgen G ^a   Kölker, Stefan ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

basic amino acid transporter; dicarboxylic acids; lysine metabolism; pipecolic acid; saccharopine

Indexed keywords

2 AMINOADIPATE AMINOTRANSAMINASE; 2 AMINOADIPATE AMINOTRANSFERASE; 2 AMINOADIPATE SEMIALDEHYDE DEHYDROGENASE; 2 AMINOADIPATE SEMIALDEHYDE SYNTHASE; AMINO ACID TRANSPORTER; ARGININE; CARBON 14; CARNITINE; CATALASE; CLOFIBRATE; DICARBOXYLIC ACID; GLUTARIC ACID; GLUTARYLCARNITINE; LYSINE; MITOCHONDRIAL 2 AMINOADIPATE SEMIALDEHYDE SYNTHASE; ORNITHINE; OXIDOREDUCTASE; OXOGLUTARATE DEHYDROGENASE; PIPECOLATE OXIDASE; PIPECOLIC ACID; PIPECOLIC ACID OXIDASE; SACCHAROPINE DEHYDROGENASE; UNCLASSIFIED DRUG;

ADD ON THERAPY; AMINO ACID ANALYSIS; AMINO ACID BLOOD LEVEL; AMINO ACID BRAIN LEVEL; AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DAMAGE; BRAIN METABOLISM; BRAIN TISSUE; CATABOLISM; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME DEFICIENCY; FATTY ACID OXIDATION; FEMALE; GLUTARYL COENZYME A DEHYDROGENASE DEFICIENCY; LIVER LEVEL; MALE; MITOCHONDRION; MOUSE; NEUROMODULATION; NEUROTOXICITY; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; TISSUE HOMOGENATE; TISSUE SPECIFICITY;

2-AMINOADIPATE TRANSAMINASE; 2-AMINOADIPIC ACID; AMINO ACID METABOLISM, INBORN ERRORS; ANALYSIS OF VARIANCE; ANIMALS; ARGININE; BRAIN; BRAIN DISEASES, METABOLIC; CARNITINE; CATALASE; GLUTARYL-COA DEHYDROGENASE; KETOGLUTARIC ACIDS; LYSINE; MICE;

EID: 78650692977     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq269     Document Type: Article

References (80)

1. Bahr O, Mader I, Zschocke J, Dichgans J, Schulz JB. Adult onset glutaric aciduria type I presenting with a leukoencephalopathy. Neurology 2002; 59: 1802-4.
2. Baric I, Wagner L, Feyh P, Liesert M, Buckel W, Hoffmann GF. Sensitivity and specificity of free and total glutaric acid and 3-hydroxyglutaric acid measurements by stable-isotope dilution assays for the diagnosis of glutaric aciduria type I. J Inherit Metab Dis 1999; 22: 867-82.
3. Benevenga NJ, Blemings KP. Unique aspects of lysine nutrition and metabolism. J Nutr 2007; 137: 1610-5.
4. Bennett JP, Logan WJ, Snyder SH. Amino acids as central nervous transmitters: the influence of ions, amino acid analogues and ontogeny on transport systems for L-glutamic and L-aspartic acids and glycine into central nervous synaptosomes of the rat. J Neurochem 1973; 21: 1533-50.
5. Bennett MJ, Marlow N, Pollitt RJ, Wales JK. Glutaric aciduria type 1:biochemical investigations and postmortem findings. Eur J Pediatr1986; 145: 403-5.
6. Bijarnia S, Wiley V, Carpenter K, Christodoulou J, Ellaway CJ, Wilcken B.Glutaric aciduria type I: outcome following detection by newbornscreening. J Inherit Metab Dis 2008; 31: 503-7.
7. Bjugstad KB, Goodman SI, Freed CR. Age at symptom onset predictsseverity of motor impairment and clinical outcome of glutaric acidemiatype 1. J Pediatr 2000; 137: 681-6.
8. Blemings KP, Crenshaw TD, Benevenga NJ. Mitochondrial lysine uptakelimits hepatic lysine oxidation in rats fed diets containing 5, 20 or 60%casein. J Nutr 1998; 128: 2427-34.
9. Blemings KP, Crenshaw TD, Swick RW, Benevenga NJ.Lysine-alpha- ketoglutarateReductase and SaccharopineDehydrogenase Are Located Only in the Mitochondrial Matrix in RatLiver. J Nutr 1994; 124: 1215-21.
10. Bunik VI, Pavlova OG. Inactivation of alpha-ketoglutarate dehydrogenaseduring its enzymatic reaction. Biochemistry (Mosc) 1997; 62: 973-82.
11. Chang YF. Pipecolic acid pathway: the major lysine metabolic route in therat brain. Biochem Biophys Res Commun 1976; 69: 174-80.
12. Chang YF. Lysine metabolism in the rat brain: blood-brain barriertransport, formation of pipecolic acid and human hyperpipecolatemia.J Neurochem 1978; 30: 355-60.
13. Chang YF, Ghosh P, Rao VV. L-pipecolic acid metabolism in human liver:L-alpha-aminoadipate delta-semialdehyde oxidoreductase. BiochimBiophys Acta 1990; 1038: 300-5.
14. Christensen E, Ribes A, Merinero B, Zschocke J. Correlation of genotypeand phenotype in glutaryl-CoA dehydrogenase deficiency. J InheritMetab Dis 2004; 27: 861-8.
15. Coman D, Yaplito-Lee J, Boneh A. New indications and controversies inarginine therapy. Clin Nutr 2008; 27: 489-96.
16. Dancis J, Hutzler J. The significance of hyperpipecolatemia in Zellwegersyndrome. Am J Hum Genet 1986; 38: 707-11.
17. Djouadi F, Bastin J. PPARs as therapeutic targets for correction of inbornmitochondrial fatty acid oxidation disorders. J Inherit Metab Dis 2008;31: 217-25.
18. Dwyer TM, Rao KS, Goodman SI, Frerman FE. Proton AbstractionReaction, Steady-State Kinetics, and Oxidation Reduction Potentialof Human Glutaryl-CoA Dehydrogenase. Biochemistry 2000; 39:11488-99.
19. Fiermonte G, Dolce V, David L, Santorelli FM, Dionisi-Vici C, Palmieri F,et al. The mitochondrial ornithine transporter bacterial expression, renconstitution, functional characterization and tissue distribution oftwo human isoforms. J Biol Chem 2003; 278: 32778-83.
20. Funk CB, Prasad AN, Frosk P, Sauer S, Kolker S, Greenberg CR, et al.Neuropathological, biochemical and molecular findings in a glutaricacidemia type 1 cohort. Brain 2005; 128: 711-22.
21. Giacobini E, Nomura Y, Schmidt-Glenewinkel T. Pipecolic acid: origin,biosynthesis and metabolism in the brain. Cell Mol Biol Incl CytoEnzymol 1980; 26: 135-46.
22. Goodman SI, Markey SP, Moe PG, Miles BS, Teng CC. Glutaric aciduria;a "new" disorder of amino acid metabolism. Biochem Med 1975; 12:12-21.
23. Goodman SI, Norenberg MD, Shikes RH, Breslich DJ, Moe PG. Glutaricaciduria: biochemical and morphologic considerations. J Pediatr 1977;90: 746-50.
24. Goodman SI, de Stein X, Schlesinger S, Christensen E, Schwartz M,Greenberg CR, et al. Glutaryl-CoA dehydrogenase mutations in gluta-ric acidemia (type I): review and report of thirty novel mutations. HumMutat 1998; 12: 141-4.
25. Greenberg CR, Duncan AM, Gregory CA, Singal R, Goodman SI. BriefReport: assignment of Human Glutaryl-CoA Dehydrogenase Gene(GCDH) to the Short Arm of Chromosome 19 (19p13. 2) by in SituHybridization and Somatic Cell Hybrid Analysis. Genomics 1994; 21:289-90.
26. Harting I, Neumaier-Probst E, Seitz A, Maier EM, Assmann B, Baric I,et al. Dynamic changes of striatal and extrastriatal abnormalities inglutaric aciduria type I. Brain 2009; 132: 1764-82.
27. Hawkins RA, O'Kane RL, Simpson LA, Viña JR. Structure of the blood-brain barrier and its role in the transport of amino acids. J Nutr 2006; 136: 218-26.
28. Helenius A, Simons K. The binding of detergents to lipophilic and hydro-philic proteins. J Biol Chem 1972; 247: 3656-61.
29. Heringer J, Boy SPN, Ensenauer R, Assmann B, Zschocke J, Harting I, et al. Use of guidelines improves the neurological outcome in glutaric aciduria type I. Ann Neurol 2010;
30. in press.Hirashima M, Hayakawa T, Koike M. Mammalian alpha-Keto Acid Dehydrogenase Complexes. II. An improved procedure for the preparation 2-oxoglutarate dehydrogenase complex from pig heart muscle. J Biol Chem 1967; 242: 902-7.
31. Hoffmann GF, Athanassopoulos S, Burlina AB, Duran M, de Klerk JB, Lehnert W, et al. Clinical course, early diagnosis, treatment, and prevention of disease in glutaryl-CoA dehydrogenase deficiency. Neuropediatrics 1996; 27: 115-23.
32. Hu CA, Donald SP, Yu J, Lin WW, Liu Z, Steel G, et al. Overexpression of proline oxidase induces proline-dependent and mitochondria-mediated apoptosis. Mol Cell Biochem 2007; 295: 85-92.
33. Ijlst L, de Kromme I, Oostheim W, Wanders RJ. Molecular cloning and expression of human L-pipecolate oxidase. Biochem Biophys Res Commun 2000; 270: 1101-5.
34. Koeller DM, Woontner M, Crnic LS, Kleinschmidt-DeMasters B, Stephens J, Hunt EL, et al. Biochemical, pathologic and behavioral analysis of a mouse model of glutaric acidemia type I. Hum Mol Genet 2002; 11: 347-57.
35. Kö lker S, Koeller DM, Okun JG, Hoffmann GF. Pathomechanisms of neurodegeneration in glutaryl-CoA dehydrogenase deficiency. Ann Neurol 2004; 55: 7-12. (Pubitemid 38067355)
36. Kö lker S, Garbade SF, Greenberg CR, Leonard JV, Saudubray JM, Ribes A, et al Natural History, Outcome, and Treatment Efficacy in Children and Adults with Glutaryl-CoA Dehydrogenase Deficiency. Pediatr Res 2006a 59 840-7.
37. Kö lker S, Sauer SW, Surtees RA, Leonard JV. The aetiology of neurological complications of organic acidaemiasa role for the blood-brain barrier. J Inherit Metab Dis 2006b; 29: 701-4.
38. Kö lker S, Christensen E, Leonard JV, Greenberg CR, Burlina AB, Burlina AP, et al Guideline for the diagnosis and management of glutaryl-CoA dehydrogenase deficiency (glutaric aciduria type I). J Inherit Metab Dis 2007a. 30 5-22.
39. Kö lker S, Garbade SF, Boy N, Maier EM, Meissner T, Mü hlhausen C, et al Decline of acute encephalopathic crises in children with glutaryl-CoA dehydrogenase deficiency identified by newborn screening in Germany. Pediatr Res 2007b 62 357-63.
40. Kü lkens S, Harting I, Sauer S, Zschocke J, Hoffmann GF, Gruber S, et al Late-onset neurologic disease in glutaryl-CoA dehydrogenase deficiency. Neurology 2005 64 2142-4.
41. Kyllerman M, Skjeldal O, Christensen E, Hagberg G, Holme E, Lö nnquist T, et al. Long-term follow-up, neurological outcome and survival rate in 28 Nordic patients with glutaric aciduria type 1. Eur J Paediatr Neurol 2004; 8: 121-9.
42. Leibel RL, Shih VE, Goodman SI, Bauman ML, McCabe ER, Zwerdling RG, et al. Glutaric acidemia: a metabolic disorder causing progressive choreoathetosis. Neurology 1980; 30: 1163-8.
43. Lindner M, Kö lker S, Schulze A, Christensen E, Greenberg CR, Hoffmann GF. Neonatal screening for glutaryl-CoA dehydrogenase deficiency. J Inherit Metab Dis 2004; 27: 851-9.
44. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-75.
45. Majamaa K, Turpeenniemi-Hujanen TM, Latipää P, Gü nzler V, Hanauske-Abel HM, Hassinen IE, et al. Differences between collagen hydroxylases and 2-oxoglutarate dehydrogenase in their inhibition by structural analogues of 2-oxoglutarate. Biochem J 1985; 229: 127-33.
46. Mihalik SJ, McGuinness M, Watkins PA. Purification and characterization of peroxisomal L-pipecolic acid oxidase from monkey liver. J Biol Chem 1991; 266: 4822-30.
47. Mihalik SJ, Rhead WJ. L-pipecolic acid oxidation in the rabbit and cynomolgus monkey. Evidence for differing organellar locations and cofactor requirements in each species. J Biol Chem 1989; 264: 2509-17.
48. Mihalik SJ, Rhead WJ. Species variation in organellar location and activity of l-pipecolic acid oxidation in mammals. J Comp Physiol B 1991; 160: 671-5.
49. Murthy SN, Janardanasarma MK. Identification of L-amino acid/L-lysine alpha-amino oxidase in mouse brain. Mol Cell Biochem 1999; 197: 13-23.
50. Naughten ER, Mayne PD, Monavari AA, Goodman SI, Sulaiman G, Croke DT. Glutaric aciduria type I: outcome in the Republic of Ireland. J Inherit Metab Dis 2004; 27: 917-20.
51. O'Kane RL, Vina JR, Simpson I, Zaragoza R, Mokashi A, Hawkins RA. Cationic amino acid transport across the blood-brain barrier is mediated exclusively by system y+. Am J Physiol Endocrinol Metab 2006; 291: 412-9.
52. Okuno E, Tsujimoto M, Nakamura M, Kido R. 2-Aminoadipate-2-oxoglutarate aminotransferase isoenzymes in human liver: a plausible physiological role in lysine and tryptophan metabolism. Enzyme Protein 1993; 47: 136-48.
53. Papes F, Kemper EL, Cord-Neto G, Langone F, Arruda P. Lysine degradation through the saccharopine pathway in mammals: involvement of both bifunctional and monofunctional lysine-degrading enzymes in mouse. Biochem J 1999; 344: 555-63.
54. Porciú ncula LO, Dal-Pizzol A, Coitinho AS, Emanuelli T, Souza DO, Wajner M. Inhibition of synaptosomal (3H) glutamate uptake and (3H) glutamate binding to plasma membranes from brain of young rats by glutaric acid in vitro. J Neurol Sci 2000; 173: 93-6.
55. Rao VV, Chang YF. Assay for L-pipecolate oxidate activity in human liver: detection of enzyme deficiency in hyperpipecolic acidaemia. Biochim Biophys Acta - Molecular Basis of Disease 1992; 1139: 189-95.
56. Rao VV, Tsai MJ, PAN X, Chang YF. L-pipecolic acid oxidation in rat: subcellular localization and developmental study. Biochim Biophys Acta - Protein structure and molecular enzymology 1993; 1164: 29-35.
57. Sacksteder KA, Biery BJ, Morrell JC, Goodman BK, Geisbrecht BV, Cox RP, et al. Identification of the alpha-aminoadipic semialdehyde synthase gene, which is defective in familial hyperlysinemia. Am J Hum Genet 2000; 66: 1736-43.
58. Sacksteder KA, Morrell JC, Wanders RJ, Matalon R, Gould SJ. MCD encodes peroxisomal and cytoplasmic forms of malonyl-CoA decarb-oxylase and is mutated in malonyl-CoA decarboxylase deficiency. J Biol Chem 1999; 274: 24461-8.
59. Sauer SW, Okun JG, Schwab MA, Crnic LR, Hoffmann GF, Goodman SI, et al. Bioenergetics in glutaryl-coenzyme A dehydrogenase deficiency: a role for glutaryl-coenzyme A. J Biol Chem 2005; 280: 21830-6.
60. Sauer SW, Okun JG, Fricker G, Mahringer A, Muller I, Crnic LR, 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 2006; 97: 899-910.
61. Sauer SW, Opp S, Mahringer A, Kamiń ski MM, Thiel C, Okun JG, et al. Glutaric aciduria type I and methylmalonic aciduria: simulation of cerebral import and export of accumulating neurotoxic dicarboxylic acids in in vitro models of the blood-brain barrier and the choroid plexus. Biochim Biophys Acta 2010; 1802: 552-60.
62. Scislowski PW, Foster AR, Fuller MF. Regulation of oxidative degradation of L-lysine in rat liver mitochondria. Biochem J 1994; 300: 887.
63. Seccombe DW, James L, Booth F. L-Carnitine treatment in glutaric acid-uria type I. Neurology 1986; 36: 264-7.
64. Sherman EA, Strauss KA, Tortorelli S, Bennett MJ, Knerr I, Morton DH, et al. Genetic Mapping of Glutaric Aciduria, Type 3, to Chromosome 7 and Identification of Mutations in C7orf10.Am J Hum Genet 2008; 83: 604-9.
65. Singh H, Usher S, Poulos A. Mitochondrial and peroxisomal -oxidation of stearic and lignoceric acids by rat brain. J Neurochem 1989; 53: 1711-8.
66. Sadilkova K, Gospe SM Jr, Hahn SH. Simultaneous determination of alpha-aminoadipic semialdehyde, piperideine-6-carboxylate and pipecolic acid by LC-MS/MS for pyridoxine-dependent seizures and folinic acid-responsive seizures. J Neurosci Methods 2009; 184: 136-41.
67. Smith QR. Transport of glutamate and other amino acids at the blood-brain barrier. J Nutr 2000; 130: 1016-22.
68. Stellmer F, Keyser B, Burckhardt BC, Koepsell H, Streichert T, Glatzel M, et al. 3-Hydroxyglutaric acid is transported via the sodium-dependent dicarboxylate transporter NaDC3. J Mol Med 2007; 85: 763-70.
69. Stokke O, Goodman SI, Moe PG. Inhibition of brain glutamate decarb-oxylase by glutarate, glutaconate, and beta-hydroxyglutarate: explanation of the symptoms in glutaric aciduria? Clin Chim Acta 1976; 66: 411-5.
70. Strauss KA, Lazovic J, Wintermark M, Morton DH. Multimodal imaging of striatal degeneration in Amish patients with glutaryl-CoA dehydro-genase deficiency. Brain 2007; 130: 1905-20.
71. Strauss KA, Puffenberger EG, Robinson DL, Morton DH. Type I glutaric aciduria, part 1: natural history of 77 patients. Am J Med Genet 2003; 15: 38-52.
72. Struys EA, Jakobs C. Metabolism of lysine in alpha-aminoadipic semialdehyde dehydrogenase-deficient fibroblasts: evidence for an alternative pathway of pipecolic acid formation. FEBS Lett 2010; 584: 181-6.
73. van Veldhoven PP, Vanhove G, Assselberghs S, Eyssen HJ, Mannaerts GP. Substrate specificities of rat liver peroxisomalacyl-CoA oxidases: palmitoyl-CoA oxidase (inducible acyl-CoAoxidase), pristanoyl-CoA oxidase (non-inducible acyl-CoA oxidase),and trihydroxycoprostanoyl-CoA oxidase. J Biol Chem 1992; 267:20065-74.
74. Wanders RJ, Denis SW, Dacremont G. Studies on the substrate specificityof the inducible and non-inducible acyl-CoA oxidases from rat kidneyperxiosomes. J Biochem 1993; 113: 577-82.
75. Westin MA, Hunt MC, Alexson SE. The identification of a succinyl-CoAthioesterase suggests a novel pathway for succinate production inperoxisomes. J Biol Chem 2005; 280: 38125-32.
76. Woontner M, Crnic LS, Koeller DM. Analysis of the expression of murineglutaryl-CoA dehydrogenase: in vitro and in vivo studies. Mol GenetMetab 2000; 69: 116-22.
77. Yodoya E, Wada M, Shimada A, Katsukawa H, Okada N, Yamamoto A,et al. Functional and molecular identification of sodium-coupleddicarboxylate transporters in rat primary cultured cerebrocorticalastrocytes and neurons. J Neurochem 2006; 97: 162-73.
78. Zinnanti WJ, Lazovic J, Housman C, LaNoue KO, Callaghan JP,Simpson I, et al. Mechanism of age-dependent susceptibility andnovel treatment strategy in glutaric acidemia type I. J Clin Invest2007; 117: 3258-70.
79. Zinnanti WJ, Lazovic J, Wolpert EB, Antonetti DA, Smith MB, Connor JR,et al. A diet-induced mouse model for glutaric aciduria type I. Brain2006; 129: 899-910.
80. Zschocke J, Quak E, Guldberg P, Hoffmann GF. Mutation analysis inglutaric aciduria type I. Br Med J 2000; 37: 177-81.