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PMID: 17581113 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Novel mechanism of inhibition of rat kidney-type glutaminase by bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide (BPTES).

The Biochemical journal ·Vol. 406 ·No. 3 ·2007-09-15 ·Pages 407-14

Robinson MM, McBryant SJ, Tsukamoto T, Rojas C, Ferraris DV, Hamilton SK, Hansen JC, Curthoys NP

Abstract

The release of GA (mitochondrial glutaminase) from neurons following acute ischaemia or during chronic neurodegenerative diseases may contribute to the propagation of glutamate excitotoxicity. Thus an inhibitor that selectively inactivates the released GA may limit the accumulation of excess glutamate and minimize the loss of neurological function that accompanies brain injury. The present study examines the mechanism of inactivation of rat KGA (kidney GA isoform) by the small-molecule inhibitor BPTES [bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide]. BPTES is a potent inhibitor of KGA, but not of the liver GA isoform, glutamate dehydrogenase or gamma-glutamyl transpeptidase. Kinetic studies indicate that, with respect to glutamine, BPTES has a K(i) of approx. 3 microM. Moreover, these studies suggest that BPTES inhibits the allosteric activation caused by phosphate binding and promotes the formation of an inactive complex. Gel-filtration chromatography and sedimentation-velocity analysis were used to examine the effect of BPTES on the phosphate-dependent oligomerization of KGA. This established that BPTES prevents the formation of large phosphate-induced oligomers and instead promotes the formation of a single oligomeric species with distinct physical properties. Sedimentation-equilibrium studies determined that the oligomer produced by BPTES is a stable tetramer. Taken together, the present work indicates that BPTES is a unique and potent inhibitor of rat KGA and elucidates a novel mechanism of inactivation.

MeSH Terms
Animals Chromatography, Gel Enzyme Inhibitors/pharmacology Fractionation, Field Flow Glutaminase/antagonists & inhibitors,metabolism Kidney/enzymology,growth & development Kinetics Rats Rats, Sprague-Dawley Sulfides/pharmacology Thiadiazoles/pharmacology Ultracentrifugation
Chemicals
Enzyme Inhibitors Sulfides Thiadiazoles bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide Glutaminase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Robinson Mary M
Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, CO 80523-1870, USA.
McBryant Steven J
Tsukamoto Takashi
Rojas Camilo
Ferraris Dana V
Hamilton Sean K
Hansen Jeffrey C
Curthoys Norman P
References (30)
30 references, click to expand
  1. Increased production of extracellular glutamate by the mitochondrial glutaminase following neuronal death.
    J Biol Chem. 1997 Apr 25;272(17):11276-82 PMID: 9111031
  2. Identification and interpretation of complexity in sedimentation velocity boundaries.
    Biophys J. 1997 Jan;72(1):397-407 PMID: 8994626
  3. Sedimentation velocity analysis of highly heterogeneous systems.
    Anal Biochem. 2004 Dec 15;335(2):279-88 PMID: 15556567
  4. Mice lacking brain/kidney phosphate-activated glutaminase have impaired glutamatergic synaptic transmission, altered breathing, disorganized goal-directed behavior and die shortly after birth.
    J Neurosci. 2006 Apr 26;26(17):4660-71 PMID: 16641247
  5. Cloning and analysis of unique human glutaminase isoforms generated by tissue-specific alternative splicing.
    Physiol Genomics. 1999 Aug 31;1(2):51-62 PMID: 11015561
  6. Identification of two human glutaminase loci and tissue-specific expression of the two related genes.
    Mamm Genome. 2000 Dec;11(12):1107-10 PMID: 11130979
  7. Mechanisms governing the expression of the enzymes of glutamine metabolism--glutaminase and glutamine synthetase.
    J Nutr. 2001 Sep;131(9 Suppl):2467S-74S; discussion 2486S-7S PMID: 11533295
  8. Hepatic glutamine metabolism.
    Nutrition. 2002 Apr;18(4):301-3 PMID: 11934540
  9. Complexity and species variation of the kidney-type glutaminase gene.
    Physiol Genomics. 2002;9(3):157-66 PMID: 12045296
  10. Bacterial expression, purification, and characterization of rat kidney-type mitochondrial glutaminase.
    Protein Expr Purif. 2003 Sep;31(1):140-8 PMID: 12963351
  11. Regulation of renal ammoniagenesis. Subcellular localization of rat kidney glutaminase isoenzymes.
    J Biol Chem. 1974 May 25;249(10):3261-6 PMID: 4364420
  12. Phosphate-dependent glutaminase from rat kidney. Cause of increased activity in response to acidosis and identity with glutaminase from other tissues.
    Arch Biochem Biophys. 1976 Jan;172(1):162-7 PMID: 1252072
  13. Correlation between activation and dimer formation of rat renal phosphate-dependent glutaminase.
    J Biol Chem. 1977 Mar 25;252(6):1927-31 PMID: 845154
  14. Covalent interaction of L-2-amino-4-oxo-5-chloropentanoic acid with rat renal phosphate-dependent glutaminase. Evidence for a specific glutamate binding site and of subunit heterogeneity.
    J Biol Chem. 1978 Oct 10;253(19):7086-90 PMID: 690141
  15. Inactivation of rat renal phosphate-dependent glutaminase with 6-diazo-5-oxo-L-norleucine. Evidence for interaction at the glutamine binding site.
    J Biol Chem. 1979 Apr 25;254(8):2835-8 PMID: 429321
  16. Comparison of the hydrolytic and transfer activities of rat renal gamma-glutamyltranspeptidase.
    J Biol Chem. 1979 Jul 25;254(14):6499-504 PMID: 36397
  17. Properties of rat renal phosphate-dependent glutaminase coupled to Sepharose. Evidence that dimerization is essential for activation.
    Biochem J. 1981 Mar 1;193(3):709-16 PMID: 7305957
  18. Glutamate and the pathophysiology of hypoxic--ischemic brain damage.
    Ann Neurol. 1986 Feb;19(2):105-11 PMID: 2421636
  19. Phosphate-activated glutaminase in the crude mitochondrial fraction (P2 fraction) from human brain cortex.
    J Neurochem. 1986 Nov;47(5):1351-5 PMID: 3531404
  20. Rat hepatic glutaminase: purification and immunochemical characterization.
    Arch Biochem Biophys. 1988 Feb 1;260(2):740-51 PMID: 3277537
  21. Protective effect of N-methyl-D-aspartate antagonists after focal cerebral ischemia in rabbits.
    Stroke. 1989 Sep;20(9):1247-52 PMID: 2672427
  22. 2,3-Dihydroxy-6-nitro-7-sulfamoyl-benzo(F)quinoxaline: a neuroprotectant for cerebral ischemia.
    Science. 1990 Feb 2;247(4942):571-4 PMID: 2154034
  23. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death.
    Annu Rev Neurosci. 1990;13:171-82 PMID: 1970230
  24. Molecular cloning of a cDNA for rat hepatic glutaminase. Sequence similarity to kidney-type glutaminase.
    J Biol Chem. 1990 Jun 25;265(18):10631-6 PMID: 2191954
  25. The role of glutamate in epilepsy and other CNS disorders.
    Neurology. 1994 Nov;44(11 Suppl 8):S14-23 PMID: 7970002
  26. Clinical experience with excitatory amino acid antagonist drugs.
    Stroke. 1995 Mar;26(3):503-13 PMID: 7886734
  27. Role of vasogenic edema and tissue cavitation in ischemic evolution on diffusion-weighted imaging: comparison with multiparameter MR and immunohistochemistry.
    AJNR Am J Neuroradiol. 1995 May;16(5):1107-15 PMID: 7639135
  28. Secondary elevation of extracellular neurotransmitter amino acids in the reperfusion phase following focal cerebral ischemia.
    J Cereb Blood Flow Metab. 1996 Jan;16(1):114-24 PMID: 8530544
  29. Regulation of glutaminase activity and glutamine metabolism.
    Annu Rev Nutr. 1995;15:133-59 PMID: 8527215
  30. Characterization of mitochondrial glutaminase and amino acids at prolonged times after experimental focal cerebral ischemia.
    Brain Res. 1998 Nov 30;813(1):103-11 PMID: 9824679
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
1470-8728
Published
2007-09-15
Pages
407-14
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC2049044
Subset
IM
Grants
NIDDK NIH HHS · R01 DK037124 · United States
NINDS NIH HHS · R43 NS049669 · United States
NIDDK NIH HHS · DK-37124 · United States
NINDS NIH HHS · R43 NS49669 · United States
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