Proteomic identification of binding partners for the brain metabolite Lanthionine Ketimine (LK) and documentation of LK effects on microglia and motoneuron cell cultures

Journal of Neuroscience

Volumn 30, Issue 8, 2010, Pages 2979-2988

  Hensley, Kenneth ^a   Christov, Alexandar ^a   Kamat, Shekhar ^a   Zhang, X Cai ^b   Jackson, Kenneth W ^b   Snow, Stephen ^d   Post, Jan ^c  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c Oklahoma School of Science and Mathematics   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

5,6 DIHYDRO 2H 1,4 THIAZINE 3,5 DICARBOXYLIC ACID; BETA TUBULIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GLUTATHIONE BINDING PROTEIN LANTHIONINE SYNTHETASE LIKE PROTEIN 1; GLUTATHIONE DERIVATIVE; HYDROGEN PEROXIDE; LANTHIONINE; MUNC18 PROTEIN; MYELIN BASIC PROTEIN; NEUROFIBROMIN; POLYPEPTIDE; SULFIDE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTROPHORESIS; ELECTROSPRAY; EMBRYO; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROGLIA; MOTONEURON; NEURITE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SCHIZOPHRENIA;

AMINO ACIDS, SULFUR; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; BRAIN; CATTLE; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELLS, CULTURED; ESTERS; HYDRO-LYASES; INFLAMMATION MEDIATORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICROGLIA; MOLECULAR STRUCTURE; MOTOR NEURONS; MULTIENZYME COMPLEXES; MUNC18 PROTEINS; MYELIN BASIC PROTEINS; NERVE TISSUE PROTEINS; NEUROCHEMISTRY; NEUROFIBROMIN 1; PROTEOMICS;

EID: 77649092461     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5247-09.2010     Document Type: Article

References (46)

1. Aberg K, Axelsson E, Saetre P, Jiang L, Wetterberg L, Pettersson U, Lindholm E, Jazin E (2008) Support for schizophrenia susceptibility locus on chromosome 2q detected in a Swedish isolate using a dense map of microsatellites and SNPs. Am J Med Genet B Neuropsychiatr Genet 147B:1238 -1244.
2. Arimura N, Inagaki N, Chihara K, Menager C, Nakamura N, Iwamatsu A (2000) Phosphorylation of CRMP-2 by Rho kinase: evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 275: 23,973-23:980.
3. Arimura N, Menager C, Fukata Y, Kaibuchi K (2004) Role of CRMP-2 in neuronal polarity. J Neurobiol 58:34-47.
4. Behan AT, Byrne C, Dunn MJ, Cagney G, Cotter DR (2009) Proteomic analysis of membrane microdomain-associated proteins in the dorsolateral prefrontal cortex in schizophrenia and bipolar disorder reveals alterations in LAMP, STXBP1 and BASP1 protein expression. Mol Psychiatry 14:601-613.
5. Beyreuther BK, Freitag J, Heers C, Krebsfänger N, Scharfenecker U, Stöhr T (2007) Lacosamide: a review of preclinical properties. CNS Drug Rev 13:21-42.
6. Blisnick T, Vincensini L, Barale JC, Namane A, Braun Breton C (2005) LANCL1, an erythrocyte protein recruited to the Maurer's clefts during Plasmodium falciparum development. Mol Biochem Parasitol 141:39-47.
7. Braunstein AE, Goryachenkova EV (1984) The beta-replacementspecific pyridoxal-P-dependent lyases. Adv Enzymol Relat Areas Mol Biol 56:1-89.
8. Broch OJ, Ueland PM (1984) Regional distribution of homocysteine in the mammalian brain. J Neurochem 43:1755-1757.
9. Cavallini D, Ricci G, Federii G (1983) The ketimine derivatives of thialysine, lanthionine, cystathionine, cysteine: preparation and properties. In: Sulfur amino acids: biochemical and clinical aspects, pp 355-364. New York: Liss.
10. Cavallini D, Ricci G, Duprè S, Pecci L, Costa M, Matarese RM, Pensa B, Antonucci A, Solinas SP, Fontana M (1991) Sulfur-containing cyclic ketimines and imino acids. A novel family of endogenous products in search for a role. Eur J Biochem 202:217-223.
11. Charrier E, Reibel S, Rogemond V, Aguera M, Thomasset N, Honnorat J (2003) Collapsin response mediator proteins (CRMPs): involvement in nervous system development and adult neurodegenerative disorders. Mol Neurobiol 28:51-64.
12. Chatterjee C, Paul M, Xie L, van der Donk WA (2005) Biosynthesis and mode of action of lantibiotics. Chem Rev 105:633-684.
13. Chung CH, Kurien BT, Mehta P, Mhatre M, Mou S, Pye QN, Stewart C, West M, Williamson KS, Post J, Liu L, Wang R, Hensley K (2007) Identification of lanthionine synthase C-like protein-1 as a prominent glutathione binding protein expressed in the mammalian central nervous system. Biochemistry 46:3262-3269.
14. Cole AR, Noble W, van Aalten L, Plattner F, Meimaridou R, Hogan D, Taylor M, LaFrancois J, Gunn-Moore F, Verkhratsky A, Oddo S, LaFerla F, Giese KP, Dineley KT, Duff K, Richardson JC, Yan SD, Hanger DP, Allan SM, Sutherland C (2007) Collapsin response mediator protein-2 hyperphosphorylation is an early event in Alzheimer's disease progression. J Neurochem 103:1132-1144.
15. Cooper AJ, Anders MW (1990) Glutamine transaminase K and cysteine conjugate β-lyase. Ann NY Acad Sci 585:118-127.
16. Cooper AJL (2004) The role of glutamine transaminase K (GTK) in sulfur and alpha-keto acid metabolism in the brain, and in the possible bioactivation of neurotoxicants. Neurochem Int 44:557-577.
17. Duprè S (2000) Professor Doriano Cavallini: a life for sulfur biochemistry. Adv Exp Med Biol 483:27-29.
18. Durham HD, Dahrouge S, Cashman NR (1993) Evaluation of the spinal cord X neuroblastoma hybrid cell line NSC-34 as a model for neurotoxicity testing. Neurotoxicology 14:387-395.
19. 35S]Lanthionine ketimine binding to bovine brain membranes. Biochem Biophys Res Commun 171:480-486.
20. Fontana M, Brunori A, Costa M, Antonucci A (1997) Detection of cystathionine ketimine and lanthionine ketimine in human brain. Neurochem Res 22:821-844.
21. Foster AC, Kemp JA, Leeson PD, Grimwood S, Donald AE, Marshall GR, Priestley T, Smith JD, Carling RW (1992) Kynurenic acid analogs with improved affinity and selectivity for the glycine site at the N-methyl-D- aspartate receptor from rat brain. Mol Pharmacol 41:914-922.
22. Gharib A, Sarda N, Chabannes B, Cronenberger L, Pacheco H (1982) The regional concentrations of S-adenosyl-L-methionine, S-adenosyl-Lhomocysteine, and adenosine in rat brain. J Neurochem 38:810-815.
23. Hensley K, Fedynyshyn J, Ferrell S, Floyd RA, Gordon B, Grammas P, Hamdheydari L, Mhatre MC, Mou S, Pye QN, Stewart C, West M, West S, Williamson KS (2003) Message and protein level elevation of tumor necrosis factor alpha (TNFα) and TNFα-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 14:74-80.
24. Hikita T, Taya S, Fujino Y, Taneichi-Kuroda S, Ohta K, Tsuboi D, Shinoda T, Kuroda K, Funahashi Y, Uraguchi-Asaki J, Hashimoto R, Kaibuchi K (2009) Proteomic analysis reveals novel binding partners of dysbindin, a schizophrenia-related protein. J Neurochem 110:1567-1574.
25. Husi H, Grant SGN (2001) Isolation of 2000-kDa complexes of N-methyl-D-aspartate receptor and postsynaptic density 95 from mouse brain. J Neurochem 77:281-291.
26. Kamath AF, Chauhan AK, Kisucka J, Dole VS, Loscalzo J, Handy DE, Wagner DD (2006) Elevated levels of homocysteine compromise blood brain barrier integrity in mice. Blood 107:591-593.
27. Kim BU, Choi J, Ahn KH, Jeong JK, Ha CM, Jeong CS, Lee CK, Kang SG, Lee BJ (2006) Munc18 plays an important role in the regulation of glutamate release during female puberty onset. Mol Cells 22:30-35.
28. Li X, Higashikubo R, Taylor JS (2008) Use of multiple carboxylates to increase intracellular retention of fluorescent probes following release from cell penetrating fluorogenic conjugates. Bioconjug Chem 19:50-56.
29. Lin YL, Hsueh YP (2008) Neurofibromin interacts with CRMP-2 and CRMP-4 in rat brain. Biochem Biophys Res Commun 369:747-752.
30. Liu J, Lamb D, Chou MM, Liu YJ, Li G (2007) Nerve growth factor-mediated neurite outgrowth via regulation of Rab5. Mol Biol Cell 18:1375-1384.
31. Marzinzig M, Nussler AK, Stadler J, Marzinzig E, Barthlen W, Nussler NC, Beger HG, Morris SM Jr, Brückner UB (1997) Improved methods to measure end products of nitric oxide in biological fluids: nitrite, nitrate and S-nitrosothiols. Nitric Oxide 1:177-189.
32. Moroni F (1999) Tryptophan metabolism and brain function: Focus on kynurenine and other indole metabolites. Eur J Pharmacol 375:87-100.
33. Nakata K, Ujike H, Sakai A, Takaki M, Imamura T, Tanaka Y, Kuroda S (2003) The human dihydropyrimidinase-related protein 2 gene on chromosome 8p21 is associated with paranoid-type schizophrenia. Biol Psychiatry 53:571-576.
34. Owen JB, Di Domenico F, Sultana R, Perluigi M, Cini C, Pierce WM, Butterfield DA (2009) Proteomics-determined differences in the concanavalin-A-fractionated proteome of hippocampus and inferior parietal lobule in subjects with Alzheimer's disease and mild cognitive impairment: implications for progression of AD. J Proteome Res 8:471-482.
35. Quach TT, Duchemin AM, Rogemond V, Aguera M, Honnorat J, Belin MF, Kolattukudy PE (2004) Involvement of collapsing response mediator proteins in the neurite extension induced by neurotrophins in dorsal root ganglion neurons. Mol Cell Neurosci 25:433-443.
36. Reed TT, Pierce WM, Markesbery WR, Butterfield DA (2009) Proteomic identification of HNE-bound proteins in early Alzheimer disease: insights into the role of lipid peroxidation in the progression of AD. Brain Res 1274:66-76.
37. Ricci G, Vesci L, Nardini M, Arduini A, Storto S, Rosato N, Cavallini D (1989) Detection of 2H-1,4-thiazine-5,6-dihydro-3,5-dicarboxylic acid (lanthionine ketimine) in the bovine brain by a fluorometric assay. Biochim Biophys Acta 990:211-215.
38. Scott WK, Hauser ER, Schmechel DE, Welsh-Bohmer KA, Small GW, Roses AD, Saunders AM, Gilbert JR, Vance JM, Haines JL, Pericak-Vance MA (2003) Ordered-subsets linkage analysis detects novel Alzheimer disease loci on chromosomes 2q34 and 15q22. Am J Hum Genet 73:1041-1051.
39. Stamm DS, Siegel DG, Mehltretter L, Connelly JJ, Trott A, Ellis N, Zismann V, Stephan DA, George TM, Vekemans M, Ashley-Koch A, Gilbert JR, Gregory SG, Speer MC, NTD Collaborative Group (2008) Refinement of 2q and 7p loci in a large multiplex NTD family. Birth Defects Res A Clin Mol Teratol 82:441-452.
40. Sturla L, Fresia C, Guida L, Bruzzone S, Scarfì S, Usai C, Fruscione F, Magnone M, Millo E, Basile G, Grozio A, Jacchetti E, Allegretti M, De Flora A, Zocchi E (2009) LanCL2 is necessary for abscisic acid binding and signaling in human granulocytes and in rat insulinoma cells. J Biol Chem 284:28045-28057.
41. Urenjak J, Obrenovitch TP (2000) Neuroprotective potency of kynurenic acid against excitotoxicity. NeuroReport 11:1341-1344.
42. Walker WS, Gatewood J, Olivas E, Askew D, Havenith CEG (1995) Mouse microglial cell lines differing in constitutive and interferon gammainducible antigen-presenting activities for naïve and memory CD4+ and CD8+ T cells. J Neuroimmunol 63:163-174.
43. Wang H, Jiang X, Yang F, Gaubatz JW, Ma L, Magera MJ, Yang X, Berger PB, Durante W, Pownall HJ, Schafer AI (2003) Hyperhomocysteinemia accelerates atherosclerosis in cystathionine beta: synthase and apolipoprotein E double knock-out mice with and without dietary perturbation. Blood 101:3901-3907.
44. Watanabe M, Osada J, Aratani Y, Kluckman K, Reddick R, Malinow MR, Maeda N (1995) Mice deficient in cystathionine beta synthase: animal models for mild and severe homocysteinemia. Proc Natl Acad Sci U S A 92:1585-1589.
45. Willey JM, van der Donk WA (2007) Lanthionines: peptides of diverse structure and function. Annu Rev Microbiol 61:477-501.
46. Zhang W, Wang L, Liu Y, Xu J, Zhu G, Cang H, Li X, Bartlam M, Hensley K, Li G, Rao Z, Zhang XC (2009) Structure of human lanthionine synthetase C-like protein 1 and its interaction with EPS8 and glutathione. Genes Dev 23:1387-1392.