Ammonium alters creatine transport and synthesis in a 3D culture of developing brain cells, resulting in secondary cerebral creatine deficiency

European Journal of Neuroscience

Volumn 27, Issue 7, 2008, Pages 1673-1685

  Braissant, Olivier ^a   Cagnon, Laurène ^a   Monnet Tschudi, Florianne ^b   Speer, Oliver ^c   Wallimann, Theo ^c   Honegger, Paul ^b   Henry, Hugues ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c ETH ZURICH   (Switzerland)

Author keywords

Brain; Creatine; Guanidinoacetate; Hyperammonemia; Rat

Indexed keywords

AMMONIA; CREATININE; GLYCINE AMIDINOTRANSFERASE; GLYCINE TRANSPORTER 1; GUANIDINOACETIC ACID; GUANIDOACETATE METHYLTRANSFERASE; SOLUTE CARRIER FAMILY 6 MEMBER 8; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CELL; BRAIN DEVELOPMENT; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HYPERAMMONEMIA; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; TANDEM MASS SPECTROMETRY;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CREATINE; FEMALE; MEMBRANE TRANSPORT PROTEINS; PREGNANCY; QUATERNARY AMMONIUM COMPOUNDS; RATS;

EID: 41549151211     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06126.x     Document Type: Article

References (61)

1. Aberg, N.D., Brywe, K.G. Isgaard, J. (2006) Aspects of growth hormone and insulin-like growth factor-I related to neuroprotection, regeneration, and functional plasticity in the adult brain. Sci. World J., 6, 53 80.
2. Bachmann, C., Braissant, O., Villard, A.M., Boulat, O. Henry, H. (2004) Ammonia toxicity to the brain and creatine. Mol. Genet. Metab., 81 (Suppl. 1 S52 S57.
3. Basu-Modak, S., Braissant, O., Escher, P., Desvergne, B., Honegger, P. Wahli, W. (1999) Peroxisome proliferator-activated receptor beta regulates acyl-CoA synthetase 2 in reaggregated rat brain cell cultures. J. Biol. Chem., 274, 35881 35888.
4. Baumgartner, M.R., Hu, C.A., Almashanu, S., Steel, G., Obie, C., Aral, B., Rabier, D., Kamoun, P., Saudubray, J.M. Valle, D. (2000) Hyperammonemia with reduced ornithine, citrulline, arginine and proline: a new inborn error caused by a mutation in the gene encoding delta (1) -pyrroline-5-carboxylate synthase. Hum. Mol. Genet., 9, 2853 2858.
5. Bélanger, M., Asashima, T., Ohtsuki, S., Yamaguchi, H., Ito, S. Terasaki, T. (2007) Hyperammonemia induces transport of taurine and creatine and suppresses claudin-12 gene expression in brain capillary endothelial cells in vitro. Neurochem. Int., 50, 95 101.
6. Braissant, O. (2004) Measurement of nitric oxide-related enzymes in the brain by in situ hybridization. Methods Mol. Biol., 279, 113 124.
7. Braissant, O. (2006) Neurofilament proteins in brain diseases. In : Arlen, R.K. (Ed.), New Research on Neurofilament Proteins. Nova Science Publishers Inc., New York, pp. 25 51.
8. Braissant, O. (2007) Pathways depending on urea cycle intermediates. In : Bachmann, C., Häberle, J., Koch, H.G. Leonard, J. (Eds), Pathophysiology and Management of Hyperammonemia. SPS Publications, Heilbronn, pp. 25 41.
9. Braissant, O., Bachmann, C. Henry, H. (2007) Expression and function of AGAT, GAMT and CT1 in the mammalian brain. Subcell. Biochem., 46, 67 81.
10. Braissant, O., Gotoh, T., Loup, M., Mori, M. Bachmann, C. (2001a) Differential expression of the cationic amino acid transporter 2 (B) in the adult rat brain. Mol. Brain Res., 91, 189 195.
11. Braissant, O. Henry, H. (2008) AGAT, GAMT and SLC6A8 distribution in the central nervous system, in relation to creatine deficiency syndromes: a review. J. Inher. Metab. Dis., in press doi : Bachmann, C. (2001b) Endogenous synthesis and transport of creatine in the rat brain: an in situ hybridization study. Mol. Brain Res., 86, 193 201.
12. Braissant, O., Henry, H., Villard, A.M., Speer, O., Wallimann, T. Bachmann, C. (2005) Creatine synthesis and transport during rat embryogenesis: Spatiotemporal expression of AGAT, GAMT and CT1. BMC Dev. Biol., 5, 9.
13. Braissant, O., Henry, H., Villard, A.M., Zurich, M.G., Loup, M., Eilers, B., Parlascino, G., Matter, E., Boulat, O., Honegger, P. Bachmann, C. (2002) Ammonium-induced impairment of axonal growth is prevented through glial creatine. J. Neurosci., 22, 9810 9820.
14. Braissant, O., Honegger, P., Loup, M., Iwase, K., Takiguchi, M. Bachmann, C. (1999) Hyperammonemia: regulation of argininosuccinate synthetase and argininosuccinate lyase genes in aggregating cell cultures of fetal rat brain. Neurosci. Lett., 266, 89 92.
15. Braissant, O. Wahli, W. (1998) A simplified in situ hybridization protocol using non-radioactively labelled probes to detect abundant and rare mRNAs on tissue sections. Biochemica, 1, 10 16.
16. Butterworth, R.F. (1998) Effects of hyperammonaemia on brain function. J. Inher. Metab. Dis., 21 (Suppl. 1 6 20.
17. Cagnon, L. Braissant, O. (2007) Hyperammonemia-induced toxicity for the developing central nervous system. Brain Res. Rev., 56, 183 197.
18. Carlson, M. Van Pilsum, J.F. (1973) S-adenosylmethionine: guanidinoacetate N-methyltransferase activities in livers from rats with hormonal deficiencies or excesses. Proc. Soc. Exp. Biol. Med., 143, 1256 1259.
19. Cleary, M.A., Dorland, L., de Koning, T.J., Poll-The, B.T., Duran, M., Mandell, R., Shih, V.E., Berger, R., Olpin, S.E. Besley, G.T. (2005) Ornithine aminotransferase deficiency: diagnostic difficulties in neonatal presentation. J. Inherit. Metab. Dis., 28, 673 679.
20. Dionisi-Vici, C., Bachmann, C., Gambarara, M., Colombo, J.P. Sabetta, G. (1987) Hyperornithinemia-hyperammonemia-homocitrullinuria syndrome: low creatine excretion and effect of citrulline, arginine, or ornithine supplement. Pediatr. Res., 22, 364 367.
21. Flavell, D.M., Wells, T., Wells, S.E., Carmignac, D.F., Thomas, G.B. Robinson, I.C. (1996) Dominant dwarfism in transgenic rats by targeting human growth hormone (GH) expression to hypothalamic GH-releasing factor neurons. EMBO J., 15, 3871 3879.
22. Guerrero-Ontiveros, M.L. Wallimann, T. (1998) Creatine supplementation in health and disease. Effects of chronic creatine ingestion in vivo: down-regulation of the expression of creatine transporter isoforms in skeletal muscle. Mol. Cell. Biochem., 184, 427 437.
23. Guthmiller, P., Van Pilsum, J.F., Boen, J.R. McGuire, D.M. (1994) Cloning and sequencing of rat kidney 1-arginine: glycine amidinotransferase. Studies on the mechanism of regulation by growth hormone and creatine. J. Biol. Chem., 269, 17556 17560.
24. Happe, H.K. Murrin, L.C. (1995) In situ hybridization analysis of CHOT1, a creatine transporter, in the rat central nervous system. J. Comp. Neurol., 351, 94 103.
25. Hemmer, W. Wallimann, T. (1993) Functional aspects of creatine kinase in brain. Dev. Neurosci., 15, 249 260.
26. Honegger, P. Monnet-Tschudi, F. (2001) Aggregating neural cell culture. In : Fedoroff, S. Richardson, A. (Eds), Protocols for Neural Cell Culture. Humana Press Inc., Totowa, NJ, pp. 199 218.
27. +-ATPase isoforms regulate glucose utilization in response to membrane depolarization and elevated extracellular potassium. J. Cereb. Blood Flow Metab., 19, 1051 1059.
28. Klein, A.M. Ferrante, R.J. (2007) The neuroprotective role of creatine. Subcell. Biochem., 46, 205 243.
29. Laursen, H. Diemer, N.H. (1979) Morphometric studies of rat glial cell ultrastructure after urease-induced hyperammonaemia. Neuropathol. Appl. Neurobiol., 5, 345 362.
30. Laursen, H. Diemer, N.H. (1980) Morphometry of astrocyte and oligodendrocyte ultrastructure after portocaval anastomosis in the rat. Acta Neuropathol., 51, 65 70.
31. Lee, H., Ogawa, H., Fujioka, M. Gerton, G.L. (1994) Guanidinoacetate methyltransferase in the mouse: extensive expression in Sertoli cells of testis and in microvilli of caput epididymis. Biol. Reprod., 50, 152 162.
32. Majoie, C.B., Mourmans, J.M., Akkerman, E.M., Duran, M. Poll-The, B.T. (2004) Neonatal citrullinemia: comparison of conventional MR, diffusion-weighted, and diffusion tensor findings. Am. J. Neuroradiol., 25, 32 35.
33. McGuire, D.M., Gross, M.D., Van Pilsum, J.F. Towle, H.C. (1984) Repression of rat kidney l-arginine: glycine amidinotransferase synthesis by creatine at a pretranslational level. J. Biol. Chem., 259, 12034 12038.
34. McGuire, D.M., Tormanen, C.D., Segal, I.S. Van Pilsum, J.F. (1980) The effect of growth hormone and thyroxine on the amount of 1-arginine: glycine amidinotransferase in kidneys of hypophysectomized rats. Purification and some properties of rat kidney transamidinase. J. Biol. Chem., 255, 1152 1159.
35. Mercimek-Mahmutoglu, S., Stöckler-Ipsiroglu, S., Adami, A., Appleton, R., Araújo, H.C., Duran, M., Ensenauer, R., Fernandez-Alvarez, E., Garcia, P., Grolik, C., Item, C.B., Leuzzi, V., Marquardt, I., Mühl, A., Saelke-Kellermann, R.A., Salomons, G.S., Schulze, A., Surtees, R., van der Knaap, M.S., Vasconcelos, R., Verhoeven, N.M., Vilarinho, L., Wilichowski, E. Jakobs, C. (2006) GAMT deficiency: features, treatment, and outcome in an inborn error of creatine synthesis. Neurology, 67, 480 484.
36. Molloy, G.R., Wilson, C.D., Benfield, P., de Vellis, J. Kumar, S. (1992) Rat brain creatine kinase messenger RNA levels are high in primary cultures of brain astrocytes and oligodendrocytes and low in neurons. J. Neurochem., 59, 1925 1932.
37. Näntö-Salonen, K., Komu, M., Lundbom, N., Heinänen, K., Alanen, A., Sipilä, I. Simell, O. (1999) Reduced brain creatine in gyrate atrophy of the choroid and retina with hyperornithinemia. Neurology, 53, 303 307.
38. Nishie, M., Mori, F., Houzen, H., Yamaguchi, J., Jensen, P.H. Wakabayashi, K. (2006) Oligodendrocytes within astrocytes ('emperipolesis') in the cerebral white matter in hepatic and hypoglycemic encephalopathy. Neuropathology., 26, 62 65.
39. Norenberg, M.D., Rao, K.V. Jayakumar, A.R. (2005) Mechanisms of ammonia-induced astrocyte swelling. Metab. Brain Dis., 20, 303 318.
40. Ohtsuki, S., Tachikawa, M., Takanaga, H., Shimizu, H., Watanabe, M., Hosoya, K. Terasaki, T. (2002) The blood-brain barrier creatine transporter is a major pathway for supplying creatine to the brain. J. Cereb. Blood Flow Metab., 22, 1327 1335.
41. Perasso, L., Cupello, A., Lunardi, G.L., Principato, C., Gandolfo, C. Balestrino, M. (2003) Kinetics of creatine in blood and brain after intraperitoneal injection in the rat. Brain Res., 974, 37 42.
42. Pilbeam, C.M., Anderson, R.M. Bhathal, P.S. (1983) The brain in experimental portal-systemic encephalopathy. I. Morphological changes in three animal models. J. Pathol., 140, 331 345.
43. Schmidt, A., Marescau, B., Boehm, E.A., Renema, W.K., Peco, R., Das, A., Steinfeld, R., Chan, S., Wallis, J., Davidoff, M., Ullrich, K., Waldschutz, R., Heerschap, A., De Deyn, P.P., Neubauer, S. Isbrandt, D. (2004) Severely altered guanidino compound levels, disturbed body weight homeostasis and impaired fertility in a mouse model of guanidinoacetate N-methyltransferase (GAMT) deficiency. Hum. Mol. Genet., 13, 905 921.
44. Schulze, A. (2003) Creatine deficiency syndromes. Mol. Cell. Biochem., 244, 143 150.
45. Shih, V.E., Laframboise, R., Mandell, R. Pichette, J. (1992) Neonatal form of the hyperornithinaemia, hyperammonaemia, and homocitrullinuria (HHH) syndrome and prenatal diagnosis. Prenat. Diagn., 12, 717 723.
46. Speer, O., Neukomm, L.J., Murphy, R.M., Zanolla, E., Schlattner, U., Henry, H., Snow, R.J. Wallimann, T. (2004) Creatine transporters: a reappraisal. Mol. Cell. Biochem., 256-257, 407 424.
47. Stöckler, S., Schutz, P.W. Salomons, G.S. (2007) Cerebral creatine deficiency syndromes: Clinical aspects, treatment and pathophysiology. Subcell. Biochem., 46, 149 166.
48. Stromberger, C., Bodamer, O.A. Stöckler-Ipsiroglu, S. (2003) Clinical characteristics and diagnostic clues in inborn errors of creatine metabolism. J. Inherit. Metab. Dis., 26, 299 308.
49. Sun, L.Y., Evans, M.S., Hsieh, J., Panici, J. Bartke, A. (2005) Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology, 146, 1138 1144.
50. Tachikawa, M., Fukaya, M., Terasaki, T., Ohtsuki, S. Watanabe, M. (2004) Distinct cellular expressions of creatine synthetic enzyme GAMT and creatine kinases uCK-Mi and CK-B suggest a novel neuron-glial relationship for brain energy homeostasis. Eur. J. Neurosci., 20, 144 160.
51. Takanashi, J., Barkovich, A.J., Cheng, S.F., Weisiger, K., Zlatunich, C.O., Mudge, C., Rosenthal, P., Tuchman, M. Packman, S. (2003) Brain MR imaging in neonatal hyperammonemic encephalopathy resulting from proximal urea cycle disorders. Am. J. Neuroradiol., 24, 1184 1187.
52. Takeoka, M., Soman, T.B., Shih, V.E., Caviness, V.S. Krishnamoorthy, K.S. (2001) Carbamyl phosphate synthetase 1 deficiency: a destructive encephalopathy. Pediatr. Neurol., 24, 193 199.
53. Tarnopolsky, M., Parise, G., Fu, M.H., Brose, A., Parshad, A., Speer, O. Wallimann, T. (2003) Acute and moderate-term creatine monohydrate supplementation does not affect creatine transporter mRNA or protein content in either young or elderly humans. Mol. Cell. Biochem., 244, 159 166.
54. Tuchman, M., Knopman, D.S. Shih, V.E. (1990) Episodic hyperammonemia in adult siblings with hyperornithinemia, hyperammonemia, and homocitrullinuria syndrome. Arch. Neurol., 47, 1134 1137.
55. Valtonen, M., Näntö-Salonen, K., Jääskeläinen, S., Heinänen, K., Alanen, A., Heinonen, O.J., Lundbom, N., Erkintalo, M. Simell, O. (1999) Central nervous system involvement in gyrate atrophy of the choroid and retina with hyperornithinaemia. J. Inher. Metab. Dis., 22, 855 866.
56. Van Pilsum, J.F., Stephens, G.C. Taylor, D. (1972) Distribution of creatine, guanidinoacetate and enzymes for their biosynthesis in the animal kingdom. Implications for phylogeny. Biochem. J., 126, 325 345.
57. Wakamoto, H., Manabe, K., Kobayashi, H. Hayashi, M. (1999) Subclinical portal-systemic encephalopathy in a child with congenital absence of the portal vein. Brain Dev., 21, 425 428.
58. Walker, J.B. (1979) Creatine: biosynthesis, regulation, and function. Adv. Enzymol., 50, 177 242.
59. Wallimann, T., Tokarska-Schlattner, M., Neumann, D., Epand, R.M., Epand, R.F., Andres, R.H., Widmer, H.R., Hornemann, T., Saks, V.A., Agarkova, I. Schlattner, U. (2007) The phosphocreatine circuit: Molecular and cellular physiology of creatine kinases, sensitivity to free radicals and enhancement of creatine supplementation. In : Saks, V.A. (Ed.), Molecular Systems Bioenergetics: Energy for Life, Basic Principles, Organization and Dynamics of Cellular Energetics. Wiley VCH-Publisher Co, Weinheim, pp. 195 264.
60. Wyss, M. Kaddurah-Daouk, R. (2000) Creatine and creatinine metabolism. Physiol. Rev., 80, 1107 1213.
61. Yamanouchi, H., Yokoo, H., Yuhara, Y., Maruyama, K., Sasaki, A., Hirato, J. Nakazato, Y. (2002) An autopsy case of ornithine transcarbamylase deficiency. Brain Dev., 24, 91 94.