L-homocysteine sulfinic acid and other acidic homocysteine derivatives are potent and selective metabotropic glutamate receptor agonists

Journal of Pharmacology and Experimental Therapeutics

Volumn 305, Issue 1, 2003, Pages 131-142

  Shi, Qi ^a   Savage, Jason E ^a   Hufeisen, Sandra J ^a   Rauser, Laura ^a   Grajkowska, Ewa ^b   Ernsberger, Paul ^a   Wroblewski, Jarda T ^b   Nadeau, Joseph H ^a   Roth, Bryan L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYSTEIC ACID; CYSTINE; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; GLUTAMIC ACID; HOMOCYSTEIC ACID; HOMOCYSTEINE; HOMOCYSTEINE DERIVATIVE; HOMOCYSTEINE SULFINIC ACID; HOMOCYSTEINE THIOLACTONE; METHIONINE; NEUROTRANSMITTER RECEPTOR; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG POTENCY; DRUG RECEPTOR BINDING; HUMAN; HUMAN CELL; HYDROLYSIS; HYPERHOMOCYSTEINEMIA; MOLECULAR CLONING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT;

ANIMALS; BINDING SITES; CYCLIC AMP; HOMOCYSTEINE; HUMANS; HYDROLYSIS; PHOSPHATIDYLINOSITOLS; RADIOLIGAND ASSAY; RATS; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 0037381014     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.102.047092     Document Type: Article

References (73)

1. Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, and Tonegawa S (1994) Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGluR1 mutant mice. Cell 79:365-375.
2. Allen JW, Eldadah BA, and Faden AI (1999) Beta-amyloid-induced apoptosis of cerebellar granule cells and cortical neurons: exacerbation by selective inhibition of group I metabotropic glutamate receptors. Neuropharmacology 38:1243-1252.
3. Atlante A, Calissano P, Bobba A, Giannattasio S, Marra E, and Passarella S (2001) Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett 497:1-5.
4. Aubard Y, Darodes N, and Cantaloube M (2000) Hyperhomocysteinemia and pregnancy-review of our present understanding and therapeutic implications. Eur J Obstet Gynecol Reprod Biol 93:157-165.
5. Beckett S and Marsden CA (1997) The effect of central and systemic injection of the 5-HT1A receptor agonist 8-OHDPAT and the 5-HT1A receptor antagonist WAY100635 on periaqueductal grey-induced defence behaviour. J Psychopharmacol 11:35-40.
6. Bennett MR and Balcar VJ (1999) Forty years of amino acid transmission in the brain. Neurochem Int 35:269-280.
7. Brattstrom L and Wilcken DE (2000) Homocysteine and cardiovascular disease: cause or effect? Am J Clin Nutr 72:315-323.
8. Bruno V, Ksiazek I, Battaglia G, Lukic S, Leonhardt T, Sauer D, Gasparini F, Kuhn R, Nicoletti F, and Flor PJ (2000) Selective blockade of metabotropic glutamate receptor subtype 5 is neuroprotective. Neuropharmacology 39:2223-2230.
9. Collard CD, Park KA, Montalto MC, Alapati S, Buras JA, Stahl GL, and Colgan SP (2002) Neutrophil-derived glutamate regulates vascular endothelial barrier function. J Biol Chem 277:14801-14811.
10. Collingridge GL and Lester RA (1989) Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol Rev 41:143-210.
11. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F et al. (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature (Lond) 372:237-243.
12. Curtis DR and Watkins JC (1960) The excitation and depression of spinal neurons by structurally related amino acids. J Neurochem 6:117-141.
13. Daggett LP, Sacaan AI, Akong M, Rao SP, Hess SD, Liaw C, Urrutia A, Jachec C, Ellis SB, Dreessen J, et al. (1995) Molecular and functional characterization of recombinant human metabotropic glutamate receptor subtype 5. Neuropharmacology 34:871-886.
14. De Blasi A, Conn PJ, Pin J, and Nicoletti F (2001) Molecular determinants of metabotropic glutamate receptor signaling. Trends Pharmacol Sci 22:114-120.
15. Do KQ, Benz B, Sorg O, Pellerin L, and Magistretti PJ (1997) beta-Adrenergic stimulation promotes homocysteic acid release from astrocyte cultures: evidence for a role of astrocytes in the modulation of synaptic transmission. J Neurochem 68:2386-2394.
16. Durand P, Prost M, Loreau N, Lussier-Cacan S, and Blache D (2001) Impaired homocysteine metabolism and atherothrombotic disease. Lab Investig 81:645-672.
17. Ferraguti F, Pietra C, Valerio E, Corti C, Chiamulera C, and Conquet F (1997) Evidence against a permissive role of the metabotropic glutamate receptor 1 in acute excitotoxicity. Neuroscience 79:1-5.
18. Gill SS, Pulido OM, Mueller RW, and McGuire PF (1999) Immunochemical localization of metabotropic glutamate receptors in the rat heart. Brain Res Bull 48:143-146.
19. Gomeza J, Mary S, Brabet I, Parmentier ML, Restituito S, Bockaert J, and Pin JP (1996) Coupling of metabotropic glutamate receptors 2 and 4 to G alpha 15, G alpha 16 and chimeric G alpha q/i proteins: characterization of new antagonists. Mol Pharmacol 50:923-930.
20. Grieve A and Griffiths R (1992) Simultaneous measurement by HPLC of the excitatory amino acid transmitter candidates homocysteate and homocysteine sulphinate supports a predominant astrocytic localisation. Neurosci Lett 145:1-5.
21. Hankey GJ and Eikelboom JW (2001) Homocysteine and stroke. Curr Opin Neurol 14:95-102.
22. Hu D, Cao K, Peterson-Wakeman R, and Wang R (2002) Altered profile of gene expression in rat hearts induced by chronic nicotine consumption. Biochem Biophys Res Commun 297:729-736.
23. Jakubowski H, Zhang L, Bardeguez A, and Aviv A (2000) Homocysteine thiolactone and protein homocysteinylation in human endothelial cells: implications for atherosclerosis. Circ Res 87:45-51.
24. Kalkman HO (2002) Antischizophrenic activity independent of dopamine D2 blockade. Expert Opin Ther Target 6:571-582.
25. Kanfer JN, Sorrentino G, and Sitar DS (1998) Phospholipases as mediators of amyloid beta peptide neurotoxicity: an early event contributing to neurodegeneration characteristic of Alzheimer's disease. Neurosci Lett 257:93-96.
26. Kang SS, Wong PW, and Malinow MR (1992) Hyperhomocyst(e)inemia as a risk factor for occlusive vascular disease. Annu Rev Nutr 12:279-298.
27. Kingston AE, Lowndes J, Evans N, Clark B, Tomlinson R, Burnett JP, Mayne NG, Cockerham SL, and Lodge D (1998) Sulphur-containing amino acids are agonists for group 1 metabotropic receptors expressed in clonal RGT cell lines. Neuropharmacology 37:277-287.
28. Kinzie JM, Saugstad JA, Westbrook GL, and Segerson TP (1995) Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neuroscience 69:167-176.
29. Kokame K, Kato H, and Miyata T (1996) Homocysteine-respondent genes in vascular endothelial cells identified by differential display analysis. GRP78/BiP and novel genes. J Biol Chem 271:29659-29665.
30. Kozikowski AP, Steensma D, Araldi GL, Tuckmantel W, Wang S, Pshenichkin S, Surina E, and Wroblewski JT (1998) Synthesis and biology of the conformationally restricted ACPD analogue, 2-aminobicyclo[2.1.1]hexane-2,5-dicarboxylic acid-I, a potent mGluR agonist. J Med Chem 41:1641-1650.
31. Lang D, Kredan MB, Moat SJ, Hussain SA, Powell CA, Bellamy MF, Powers HJ, and Lewis MJ (2000) Homocysteine-induced inhibition of endothelium-dependent relaxation in rabbit aorta: role for superoxide anions. Arterioscler Thromb Vasc Biol 20:422-427.
32. Levine J, Stahl Z, Sela BA, Gavendo S, Ruderman V, and Belmaker RH (2002) Elevated homocysteine levels in young male patients with schizophrenia. Am J Psychiatry 159:1790-1792.
33. Loscalzo J (1996) The oxidant stress of hyperhomocyst(e)inemia. J Clin Investig 98:5-7.
34. Lu ZL, Saldanha JW, and Hulme EC (2002) Seven-transmembrane receptors: crystals clarify. Trends Pharmacol Sci 23:140-146.
35. Ma B, Shatsky M, Wolfson HJ, and Nussinov R (2002) Multiple diverse ligands binding at a single protein site: a matter of pre-existing populations. Protein Sci 11:184-197.
36. Makris M (2000) Hyperhomocysteinemia and thrombosis. Clin Lab Haematol 22:133-143.
37. Malinow MR, Bostom AG, and Krauss RM (1999) Homocyst(e)ine, diet and cardiovascular diseases: a statement for healthcare professionals from the Nutrition Committee, American Heart Association. Circulation 99:178-182.
38. Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M, Fukuda Y, Sasaki H, Hiroi K, Nakamura Y, Shigemoto R, et al. (1995) Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80:757-765.
39. McCully KS (1969) Vascular pathology of homocysteinemia: implications for the pathogenesis of arteriosclerosis. Am J Pathol 56:111-128.
40. McCully KS (1996) Homocysteine and vascular disease. Nat Med 2:386-389.
41. Miller JW (2000) Homocysteine, Alzheimer's disease and cognitive function. Nutrition 16:675-677.
42. Morris MS, Jacques PF, Rosenberg IH, and Selhub J (2001) Hyperhomocysteinemia associated with poor recall in the third National Health and Nutrition Examination Survey. Am J Clin Nutr 73:927-933.
43. Mukhin AG, Ivanova SA, and Faden AI (1997) mGluR modulation of post-traumatic neuronal death: role of NMDA receptors. Neuroreport 8:2561-2566.
44. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, and Nakanishi S (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268:11868-11873.
45. Ohishi H, Shigemoto R, Nakanishi S, and Mizuno N (1993) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J Comp Neurol 335:252-266.
46. Olney JW, Price MT, Salles KS, Labruyere J, Ryerson R, Mahan K, Frierdich G, and Samson L (1987) L-Homocysteic acid: an endogenous excitotoxic ligand of the NMDA receptor. Brain Res Bull 19:597-602.
47. Outinen PA, Sood SK, Pfeifer SI, Pamidi S, Podor TJ, Li J, Weitz JI, and Austin RC (1999) Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells. Blood 94:959-967.
48. Pekhletski R, Gerlai R, Overstreet LS, Huang XP, Agopyan N, Slater NT, Abramow-Newerly W, Roder JC, and Hampson DR (1996) Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J Neurosci 16:6364-6373.
49. Quinn CT, Griener JC, Bottiglieri T, Hyland K, Farrow A, and Kamen BA (1997) Elevation of homocysteine and excitatory amino acid neurotransmitters in the CSF of children who receive methotrexate for the treatment of cancer. J Clin Oncol 15:2800-2806.
50. Raulli R, Danysz W, and Wroblewski JT (1991) Pretreatment of cerebellar granule cells with concanavalin A potentiates quisqualate-stimulated phosphoinositide hydrolysis. J Neurochem 56:2116-2124.
51. Romano C, Smout S, Miller JK, and O'Malley KL (2002) Developmental regulation of metabotropic glutamate receptor 5b protein in rodent brain. Neuroscience 111:693-698.
52. Roth BL, Baner K, Westkaemper R, Siebert D, Rice KR, Steinberg SA, Ernsberger P, and Rothman RB (2002) Salvinorin A: a potent naturally occurring nonnitrogenous k opioid selective agonist. Proc Natl Acad Sci USA 99:11934-11939.
53. Roth BL, Ernsberger P, Steinberg SA, Rao S, Rauser L, Savage J, Hufeisen S, Berridge MS, and Muzic RF Jr (2001) The in vitro pharmacology of the beta-adrenergic receptor pet ligand (s)-fluorocarazolol reveals high affinity for cloned beta-adrenergic receptors and moderate affinity for the human 5-HT1A receptor. Psychopharmacology (Berl) 157:111-114.
54. Roth BL, Hamblin MW, and Ciaranello RD (1991) Developmental regulation of 5-HT2 and 5-HT1c mRNA and receptor levels. Brain Res Dev Brain Res 58:51-58.
55. Roth BL, Meltzer HY, and Khan N (1998) Binding of typical and atypical antipsychotic drugs to multiple neurotransmitter receptors. Adv Pharmacol 42:482-485.
56. Rothman RB, Baumann MH, Savage JE, Rauser L, McBride A, Hufeisen SJ, and Roth BL (2000) Evidence for possible involvement of 5-HT(2B) receptors in the cardiac valvulopathy associated with fenfluramine and other serotonergic medications. Circulation 102:2836-2841.
57. Sattler R and Tymianski M (2000) Molecular mechanisms of calcium-dependent excitotoxicity. J Mol Med 78:3-13.
58. Selhub J, Jacques PF, Rosenberg IH, Rogers G, Bowman BA, Gunter EW, Wright JD, and Johnson CL (1999) Serum total homocysteine concentrations in the third National Health and Nutrition Examination Survey (1991-1994): population reference ranges and contribution of vitamin status to high serum concentrations. Ann Intern Med 131:331-339.
59. Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, D'Agostino RB, Wilson PW, and Wolf PA (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N Engl J Med 346:476-483.
60. Shapiro DA, Kristiansen K, Weiner DM, Kroeze WK, and Roth BL (2002) Evidence for a model of agonist-induced activation of 5-hydroxytryptamine 2A serotonin receptors that involves the disruption of a strong ionic interaction between helices 3 and 6. J Biol Chem 277:11441-11449.
61. Shigemoto R, Nakanishi S, and Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121-135.
62. Singh IN, Sorrentino G, and Kanfer JN (1998) Activation of LA-N-2 cell phospholipase D by amyloid beta protein (25-35). Neurochem Res 23:1225-1232.
63. Spence JD, Malinow MR, Barnett PA, Marian AJ, Freeman D, and Hegele RA (1999) Plasma homocyst(e)ine concentration, but not MTHFR genotype, is associated with variation in carotid plaque area. Stroke 30:969-973.
64. Stephenson DT and Clemens JA (1998) Metabotropic glutamate receptor activation in vivo induces intraneuronal amyloid immunoreactivity in guinea pig hippocampus. Neurochem Int 33:83-93.
65. Tanabe Y, Nomura A, Masu M, Shigemoto R, Mizuno N, and Nakanishi S (1993) Signal transduction, pharmacological properties and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 13:1372-1378.
66. Thompson GA and Kilpatrick IC (1996) The neurotransmitter candidature of sulphur-containing excitatory amino acids in the mammalian central nervous system. Pharmacol Ther 72:25-36.
67. Ueland PM, Refsum H, Beresford SA, and Vollset SE (2000) The controversy over homocysteine and cardiovascular risk. Am J Clin Nutr 72:324-332.
68. van der Put NM, van Straaten HW, Trijbels FJ, and Blom HJ (2001) Folate, homocysteine and neural tube defects: an overview. Exp Biol Med (Maywood) 226:243-270.
69. Vollset SE, Refsum H, Tverdal A, Nygard O, Nordrehaug JE, Tell GS, and Ueland PM (2001) Plasma total homocysteine and cardiovascular and noncardiovascular mortality: the Hordaland Homocysteine Study. Am J Clin Nutr 74:130-136.
70. Weiss N, Zhang YY, Heydrick S, Bierl C, and Loscalzo J (2001) Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction. Proc Natl Acad Sci USA 98:12503-12508.
71. White AR, Huang X, Jobling MF, Barrow CJ, Beyreuther K, Masters CL, Bush AI, and Cappai R (2001) Homocysteine potentiates copper- and amyloid beta peptide-mediated toxicity in primary neuronal cultures: possible risk factors in the Alzheimer's-type neurodegenerative pathways. J Neurochem 76:1509-1520.
72. Wroblewska B, Wroblewski JT, Pshenichkin S, Surin A, Sullivan SE, and Neale JH (1997) N-Acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J Neurochem 69:174-181.
73. Yokoi M, Kobayashi K, Manabe T, Takahashi T, Sakaguchi I, Katsuura G, Shigemoto R, Ohishi H, Nomura S, Nakamura K, et al. (1996) Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2. Science (Wash DC) 273:645-647.