Threonine deprivation rapidly activates the system A amino acid transporter in primary cultures of rat neurons from the essential amino acid sensor in the anterior piriform cortex

Journal of Nutrition

Volumn 133, Issue 7, 2003, Pages 2156-2164

  Blais, Anne ^a   Huneau, Jean François ^a   Magrum, Linda J ^b   Koehnle, Thomas J ^b   Sharp, James W ^b   Tomé, Daniel ^a   Gietzen, Dorothy W ^b  

^a AGROPARISTECH   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amino acid; Brain; Deficiency; Neuron culture; Nutrient sensor

Indexed keywords

AMINO ACID TRANSPORTER; COTRANSPORTER; ESSENTIAL AMINO ACID; ISOBUTYRIC ACID DERIVATIVE; METHYLAMINOISOBUTYRIC ACID; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID DEFICIENCY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TRANSPORT; CEREBELLUM; CHEMORECEPTOR REFLEX; CHEMOSENSITIVITY; CONTROLLED STUDY; EUKARYOTE; GLIA; HIPPOCAMPUS; MALE; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; PROTEIN PHOSPHORYLATION; PYRIFORM CORTEX; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALIA; AVES; EUKARYOTA;

EID: 0038606360     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/133.7.2156     Document Type: Article

References (63)

1. Rose, W. C. (1931) Feeding experiments with mixtures of highly purified amino acids I. The inadequacy of diets containing nineteen amino acids. J. Biol. Chem. 94: 155-165.
2. Harper, A. E., Benevenga, N. J. & Wohlhueter, R. M. (1970) Effects of ingestion of disproportionate amounts of amino acids. Physiol. Rev. 50: 428-558.
3. Rogers, Q. R. & Leung, P.M.B. (1973) The influence of amino acids on the neuroregulation of food intake. Fed. Proc. 32: 1709-1719.
4. Rogers, Q. R. & Leung, P.M.B. (1977) The control of food intake: when and how are amino acids involved? In: The Chemical Senses and Nutrition (Kare, M. R. & Maller, O., eds.), pp. 213-249. Academic Press, New York, NY.
5. Gietzen, D. W., Leung, P.M.B., Castonguay, T. W., Hartman, W. J. & Rogers, Q.R. (1986) Time course of food intake and plasma and brain amino acid concentrations in rats fed amino acid-imbalanced or -deficient diets. In: Interaction of the Chemical Senses with Nutrition (Kare, M. R. & Brand, J. G., eds.), pp. 415-456. Academic Press, New York, NY.
6. Gietzen, D. W. (1993) Neural mechanisms in the responses to amino acid deficiency. J. Nutr. 123: 610-625.
7. Koehnle, T. J., Cussell, M. C. & Gietzen, D. W. (2003) Rats rapidly reject diets deficient in essential amino acids. J. Nutr. (in press).
8. Leung, P.M.B. & Rogers, Q. R. (1969) Food intake: regulation by plasma amino acid pattern. Life Sci. 8: 1-9.
9. Leung, P.M.B., Larson, D. M. & Rogers, Q. R. (1972) Food intake and preference of olfactory bulbectomized rats fed amino acid imbalanced or deficient diets. Physiol. Behav. 9: 553-557.
10. Markison, S., Gietzen, D. W. & Spector, A. C. (1999) Essential amino acid deficiency enhances long-term intake but not short-term licking of the required nutrient. J. Nutr. 129: 1604-1612.
11. Leung, P.M.B. & Rogers, Q. R. (1971) Importance of prepyriform cortex in food-intake response of rats to amino acids. Am. J. Physiol. 221: 929-935.
12. Beverly, J. L., Gietzen, D. W. & Rogers, Q. R. (1990) Effect of dietary limiting amino acid in prepyriform cortex on meal patterns. Am. J. Physiol. 259: R716-R723.
13. Monda, M., Sullo, A., De Luca, V., Pellicano, M. P. & Viggiano, A. (1997) L-Threonine injection into PPC modifies food intake, lateral hypothalamic activity, and sympathetic discharge. Am. J. Physiol. 273: R554-R559.
14. Piredda, S. & Gale, K. (1985) A crucial epileptogenic site in the deep prepiriform cortex. Nature (Lond.) 317: 623-625.
15. Ekstrand, J. J., Domroese, M. E., Johnson, D. M., Feig, S. L., Knodel, S. M., Behan, M. & Haberly, L. B. (2001) A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J. Comp. Neurol. 434: 289-307.
16. Haberly, L. B. & Price, J. L. (1978) Association and commissural fiber systems of the olfactory cortex of the rat: I. Systems originating in the piriform cortex and adjacent areas. J. Comp. Neurol. 178: 711-740.
17. Gietzen, D. W., Erecius, L. F. & Rogers, Q. R. (1998) Neurochemical changes after imbalanced diets suggest a brain circuit mediating anorectic responses to amino acid deficiency in rats. J. Nutr. 128: 771-781.
18. Sharp, J. W., Magrum, L. J. & Gietzen, D. W. (2002) Role of MAP kinase in signaling indispensable amino acid deficiency in the brain. Brain Res. Mol. Brain Res. 105: 11-18.
19. Magrum, L. J., Hickman, M. A. & Gietzen, D. W. (1999) Increased intracellular calcium in rat anterior piriform cortex in response to threonine after threonine deprivation. J. Neurophysiol. 81: 1147-1149.
20. Oxender, D. L. & Christensen, H. N. (1963) Distinct mediating systems for the transport of neutral amino acids by the Ehrlich cell. J. Biol. Chem. 238: 3686-3699.
21. Gazzola, G. C., Franchi-Gazzola, R., Ronchi, P. & Guidotti, G. G. (1973) Regulation of amino acid transport in chick embryo heart cells. 3. Formal identification of the A mediation as an adaptive transport system. Biochim. Biophys. Acta 311: 292-301.
22. Christensen, H. N. (1990) Role of amino acid transport and counter-transport in nutrition and metabolism. Physiol. Rev. 70: 43-77.
23. Guidotti, G. G. & Gazzola, G. C. (1992) Amino acid transporters: systematic approach and principles of control. In: Mammalian Amino Acid Transport Mechanisms and Control (Kilberg, M. S. & Häussinger, D., eds.), pp. 3-29. Plenum Press, New York, NY.
24. Armano, S., Coco, S., Bacci, A., Pravettoni, E., Schenk, U., Verderio, C., Varoqui, H., Erickson, J. D. & Matteoli, M. (2002) Localization and functional relevance of system a neutral amino acid transporters in cultured hippocampal neurons. J. Biol. Chem. 277: 10467-10473.
25. Brewer, G. J. (1997) Isolation and culture of adult rat hippocampal neurons. J. Neurosci. Methods 71: 143-155.
26. Gietzen, D. W., Leung, P. M. B. & Rogers, Q. R. (1986) Norepinephrine and amino acids in prepyriform cortex of rats fed imbalanced amino acid diets. Physiol. Behav. 36: 1071-1080.
27. Brewer, G. J., Torricelli, J. R., Evege, E. K. & Price, P. J. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35: 567-576.
28. Brewer, G. J. (1995) Serum-free B27/Neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, and dentate gyrus. J. Neurosci. Res. 42: 674-683.
29. Evans, M. S., Collings, M. A. & Brewer, G. J. (1998) Electrophysiology of embryonic, adult, and aged rat hippocampal neurons in serum-free culture. J. Neurosci. Methods 79: 37-46.
30. Blais, A., Bissonnette, P. & Berteloot, A. (1987) Common characteristics for Na+-dependent sugar transport in Caco-2 cells and human fetal colon. J. Membr. Biol. 99: 113-125.
31. Kilberg, M. S. & Häussinger, D. (1992) Mammalian Amino Acid Transport Mechanisms and Control. Plenum Press, New York, NY.
32. Franchi-Gazzola, R., Visigalli, R., Bussolati, O., Dall'Asta, V. & Gazzola, G. C. (1999) Adaptive increase of amino acid transport system A requires ERK1/2 activation. J. Biol. Chem. 274: 28922-28928.
33. Iiboshi, Y., Papst, P. J., Kawasome, H., Hosoi, H., Abraham, R. T., Houghton, P. J. & Terada, N. (1999) Amino acid-dependent control of p70(s6k). Involvement of tRNA aminoacylation in the regulation. J. Biol. Chem. 274: 1092-1099.
34. Peyrollier, K., Hajduch, E., Blair, A. S., Hyde, R. & Hundal, H. S. (2000). L-Leucine availability regulates phosphatidylinositol 3-kinase, p70 S6 kinase and glycogen synthase kinase-3 activity in L6 muscle cells: evidence for the involvement of the mammalian target of rapamycin (mTOR) pathway in the L-leucine-induced up-regulation of system A amino acid transport. Biochem. J. 350: 361-368.
35. Molero, J. C., Whitehead, J. P., Meerloo, T. & James, D. E. (2001) Nocodazole inhibits insulin-stimulated glucose transport in 3T3-L1 adipocytes via a microtubule-independent mechanism. J. Biol. Chem. 276: 43829-43835.
36. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
37. Bode, B. P. (2001) Recent molecular advances in mammalian glutamine transport. J. Nutr. 131: 2475S-2485S.
38. Albers, A., Broer, A., Wagner, C. A., Setiawan, I., Lang, P. A., Kranz, E. U., Lang, F. & Broer, S. (2001) Na+ transport by the neural glutamine transporter ATA1. Pflugers Arch. 443: 92-101.
39. Palacin, M., Estevez, R., Bertran, J. & Zorzano, A. (1998) Molecular biology of mammalian plasma membrane amino acid transporters. Physiol. Rev. 78: 969-1054.
40. Lion, T. (2001) Current recommendations for positive controls in RTPCR assays. Leukemia 15: 1033-1037.
41. Ling, R., Bridges, C. C., Sugawara, M., Fujita, T., Leibach, F. H., Prasad, P. D. & Ganapathy, V. (2001) Involvement of transporter recruitment as well as gene expression in the substrate-induced adaptive regulation of amino acid transport system A. Biochim. Biophys. Acta 1512: 15-21.
42. Bain, P. J., LeBlanc-Chaffin, R., Chen, H., Palii, S. S., Leach, K. M. & Kilberg, M. S. (2002) The mechanism for transcriptional activation of the human ATA2 transporter gene by amino acid deprivation is different than that for asparagine synthetase. J. Nutr. 132: 3023-3029.
43. Gazzola, R. F., Sala, R., Bussolati, O., Visigalli, R., Dall'Asta, V., Ganapathy, V. & Gazzola, G. C. (2001) The adaptive regulation of amino acid transport system A is associated to changes in ATA2 expression. FEBS Lett. 490: 11-14.
44. Sugawara, M., Nakanishi, T., Fei, Y. J., Huang, W., Ganapathy, M. E., Leibach, F. H. & Ganapathy, V. (2000) Cloning of an amino acid transporter with functional characteristics and tissue expression pattern identical to that of system A. J. Biol. Chem. 275: 16473-16477.
45. Tamarappoo, B. K., McDonald, K. K. & Kilberg, M. S. (1996) Expressed human hippocampal ASCT1 amino acid transporter exhibits a pH-dependent change in substrate specificity. Biochim. Biophys. Acta 1279: 131-136.
46. Leung, P.M.B. & Rogers, Q. R. (1987) The effect of amino acids and protein on dietary choice. In: Umami: A Basic Taste (Kawamura, Y. & Kare, M. R., eds.), pp. 565-610. Marcel Dekker, New York, NY.
47. Guidotti, G. G., Gazzola, G. C., Borghetti, A. F. & Franchi-Gazzola, R. (1975) Adaptive regulation of amino acid transport across the cell membrane in avian and mammalian tissues. Biochim. Biophys. Acta 406: 264-279.
48. Matthews, J. C. & Anderson, K. J. (2002) Recent advances in amino acid transporters and excitatory amino acid receptors. Curr. Opin. Clin. Nutr. Metab. Care 5: 77-84.
49. Varoqui, H., Zhu, H., Yao, D., Ming, H. & Erickson, J. D. (2000) Cloning and functional identification of a neuronal glutamine transporter. J. Biol. Chem. 275: 4049-4054.
50. Haberly, L. B. (1990) Olfactory cortex. In: The Synaptic Organization of the Brain (Shepherd, G. M., ed.), pp. 317-345. Oxford University Press, New York, NY.
51. Sharp, J. W., Magrum, L. J. & Gietzen, D. W. (2000) Immediate-early gene, c-Fos, induction by threonine devoid (THR DEV) medium in vitro in anterior piriform cortex brain slices. FASEB J. 14: A261 (abs.).
52. Wang, Y., Cummings, S. L. & Gietzen, D. W. (1996) Temporal-spatial pattern of c-Fos expression in the rat brain in response to indispensable amino acid deficiency I. The initial recognition phase. Mol. Brain Res. 40: 27-34.
53. Collarini, E. J. & Oxender, D. L. (1987) Mechanisms of transport of amino acids across membranes. Annu. Rev. Nutr. 7: 75-90.
54. Tews, J. K., Good, S. S. & Harper, A. E. (1978) Transport of threonine and tryptophan by rat brain slices: relation to other amino acids at concentrations found in plasma. J. Neurochem. 31: 581-589.
55. Anthony, J. C., Anthony, T. G., Kimball, S. R. & Jefferson, L. S. (2001) Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131: 856S-860S.
56. Lynch, C. J. (2001) Role of leucine in the regulation of MTOR by amino acids: revelations from structure-activity studies. J. Nutr. 131: 861S-865S.
57. Blakely, R. D. & Bauman, A. L. (2000) Biogenic amine transporters: regulation in flux. Curr. Opin. Neurobiol. 10: 328-336.
58. Kilberg, M. S., Hutson, R. G. & Laine, R. O. (1994) Amino acid-regulated gene expression in eukaryotic cells. FASEB J. 8: 13-19.
59. Felipe, A., Soler, C. & McGivan, J. D. (1992) Amino acid deprivation leads to the emergence of System A activity and the synthesis of a specific membrane glycoprotein in the bovine renal epithelial cell line NBL-1. Biochem. J. 284: 577-582.
60. Barbosa-Tessmann, I. P., Chen, C., Zhong, C., Schuster, S. M., Nick, H. S. & Kilberg, M. S. (1999) Activation of the unfolded protein response pathway induces human asparagine synthetase gene expression. J. Biol. Chem. 274: 31139-31144.
61. Jousse, C., Bruhat, A., Ferrara, M. & Fafournoux, P. (2000) Evidence for multiple signaling pathways in the regulation of gene expression by amino acids in human cell lines. J. Nutr. 130: 1555-1560.
62. Fernandez, J., Yaman, I., Merrick, W. C., Koromilas, A., Wek, R. C., Sood, R., Hensold, J. & Hatzoglou, M. (2002) Regulation of internal ribosome entry site-mediated translation by eukaryotic initiation factor-2α phosphorylation and translation of a small upstream open reading frame. J. Biol. Chem. 277: 2050-2058.
63. Gietzen, D. W. & Magrum, L. J. (2001) Molecular mechanisms in the brain involved in the anorexia of branched-chain amino acid deficiency. J. Nutr. 131: 851S-855S.