A new nuclear function of the Entamoeba histolytica glycolytic enzyme enolase: The metabolic regulation of cytosine-5 methyltransferase 2 (Dnmt2) activity

PLoS Pathogens

Volumn 6, Issue 2, 2010, Pages

  Tovy, Ayala ^a   Tov, Rama Siman ^a   Gaentzsch, Ricarda ^b   Helm, Mark ^b,c   Ankri, Serge ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 PHOSPHOGLYCERIC ACID; CYTOSINE 5 METHYLTRANSFERASE 2; DNA METHYLTRANSFERASE; EHMET ENZYME; ENOLASE; GLUTATHIONE; GLYCEROL DERIVATIVE; METHYLTRANSFERASE; PHOSPHOENOLPYRUVATE; TRANSFER RNA; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; PROTOZOAL PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; ENTAMOEBA HISTOLYTICA; ENZYME ACTIVITY; ENZYME LOCALIZATION; GLUCOSE METABOLISM; GLYCOLYSIS; IMMUNOPRECIPITATION; MALE; METABOLIC REGULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA METHYLATION; TROPHOZOITE; TWO HYBRID SYSTEM; WESTERN BLOTTING; CELL NUCLEUS; ENZYMOLOGY; MASS SPECTROMETRY; METABOLISM; POLYMERASE CHAIN REACTION;

ENTAMOEBA HISTOLYTICA;

CELL NUCLEUS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; ENTAMOEBA HISTOLYTICA; IMMUNOPRECIPITATION; PHOSPHOPYRUVATE HYDRATASE; POLYMERASE CHAIN REACTION; PROTOZOAN PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 77649263299     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000775     Document Type: Article

References (57)

1. Spada F, Rothbauer U, Zolghadr K, Schermelleh L, Leonhardt H (2006) Regulation of DNA methyltransferase 1. Adv Enzyme Regul 46: 224-234.
2. Jeltsch A (2006) Molecular enzymology of mammalian DNA methyltransferases. Curr Top Microbiol Immunol 301: 203-225.
3. Dong A, Yoder JA, Zhang X, Zhou L, Bestor TH, et al. (2001) Structure of human DNMT2, an enigmatic DNA methyltransferase homolog that displays denaturant-resistant binding to DNA. Nucleic Acids Res 29: 439-448.
4. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, et al. (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311: 395-398.
5. Hengesbach M, Meusburger M, Lyko F, Helm M Use of DNAzymes for sitespecific analysis of ribonucleotide modifications. RNA 14(1): 180-187.
6. Jurkowski T, Meusburger M, Phalke S, Helm M, Nellen W, et al. (2008) Human DNMT2 methylates tRNA(Asp) molecules using a DNA methyltransferase-like catalytic mechanism. RNA 14(8): 1663-1670.
7. Okano M, Xie S, Li E (1998) Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res 26: 2536-2540.
8. Kunert N, Marhold J, Stanke J, Stach D, Lyko F (2003) A Dnmt2-like protein mediates DNA methylation in Drosophila. Development 130: 5083-5090.
9. Phalke S, Nickel O, Walluscheck D, Hortig F, Onorati MC, et al. (2009) Retrotransposon silencing and telomere integrity in somatic cells of Drosophila depends on the cytosine-5 methyltransferase DNMT2. Nat Genet 41: 696-702.
10. Katoh M, Curk T, Xu Q, Zupan B, Kuspa A, et al. (2006) Developmentally regulated DNA methylation in Dictyostelium discoideum. Eukaryot Cell 5: 18-25.
11. Kuhlmann M, Borisova BE, Kaller M, Larsson P, Stach D, et al. (2005) Silencing of retrotransposons in Dictyostelium by DNA methylation and RNAi. Nucleic Acids Res 33: 6405-6417.
12. Fisher O, Siman-Tov R, Ankri S (2004) Characterization of cytosine methylated regions and 5-cytosine DNA methyltransferase (Ehmeth) in the protozoan parasite Entamoeba histolytica. Nucleic Acids Res 32: 287-297.
13. Jeltsch A, Nellen W, Lyko F (2006) Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem Sci 31: 306-308.
14. Mund C, Musch T, Strodicke M, Assmann B, Li E, et al. (2004) Comparative analysis of DNA methylation patterns in transgenic Drosophila overexpressing mouse DNA methyltransferases. Biochem J 378: 763-768.
15. Pinarbasi E, Elliott J, Hornby DP (1996) Activation of a yeast pseudo DNA methyltransferase by deletion of a single amino acid. J Mol Biol 257: 804-813.
16. Rountree MR, Bachman KE, Baylin SB (2000) DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25: 269-277.
17. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T (2001) Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. Embo J 20: 2536-2544.
18. Turek-Plewa J, Jagodzinski PP The role of mammalian DNA methyltransferases in the regulation of gene expression. Cell Mol Biol Lett 10(4): 631-647.
19. Banerjee S, Fisher O, Lohia A, Ankri S (2005) Entamoeba histolytica DNA methyltransferase (Ehmeth) is a nuclear matrix protein that binds EhMRS2, a DNA that includes a scaffold/matrix attachment region (S/MAR). Mol Biochem Parasitol 139: 91-97.
20. Harony H, Bernes S, Siman-Tov R, Ankri S (2006) DNA methylation and targeting of LINE retrotransposons in Entamoeba histolytica and Entamoeba invadens. Mol Biochem Parasitol 147: 55-63.
21. Holt A, Wold F (1961) The isolation and characterization of rabbit muscle enolase. J Biol Chem 236: 3227-3231.
22. Saavedra E, Encalada R, Pineda E, Jasso-Chavez R, Moreno-Sanchez R (2005) Glycolysis in Entamoeba histolytica. Biochemical characterization of recombinant glycolytic enzymes and flux control analysis. FEBS J 272: 1767-1783.
23. Riahi Y, Siman-Tov R, Ankri S (2004) Molecular cloning, expression and characterization of a serine proteinase inhibitor gene from Entamoeba histolytica. Mol Biochem Parasitol 133: 153-162.
24. Lavi T, Isakov E, Harony H, Fisher O, Siman-Tov R, et al. (2006) Sensing DNA methylation in the protozoan parasite Entamoeba histolytica. Mol Microbiol 62: 1373-1386.
25. Arhets P, Gounon P, Sansonetti P, N aG (1995) Myosin II is involved in capping and uroid formation in the human pathogen Entamoeba histolytica. Infection and Immunity 63: 4358-4367.
26. Dastidar PG, Majumder S, A L (2007) Eh Klp5 is a divergent member of the kinesin 5 family that regulates genome content and microtubular assembly in Entamoeba histolytica. Cell Microbiol 9: 316-328.
27. Hermann A, Schmitt S, Jeltsch A (2003) The human Dnmt2 has residual DNA-(cytosine-C5) methyltransferase activity. J Biol Chem 278: 31717-31721.
28. Boël G, Pichereau V, Mijakovic I, Mazé A, Poncet S, et al. (2004) Is 2-phosphoglycerate-dependent automodification of bacterial enolases implicated in their export. Journal of molecular biology 2: 485-496.
29. Gerlt JA, Babbitt PC, Rayment I (2005) Divergent evolution in the enolase superfamily: the interplay of mechanism and specificity. Arch Biochem Biophys 433: 59-70.
30. Lavi T, Siman-Tov R, Ankri S (2008) EhMLBP is an essential constituent of the Entamoeba histolytica epigenetic machinery and a potential drug target. Molecular Microbiol 69: 55-66.
31. Kim J, Dang C (2005) Multifaceted roles of glycolytic enzymes. Trends Biochem Sci 30: 142-150.
32. Commichau FM, Rothe FM, Herzberg C, Wagner E, Hellwig D, et al. (2009) Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol Cell Proteomics 8: 1350-1360.
33. Carrero JC, Petrossian P, Acosta E, Sanchez-Zerpa M, Ortiz-Ortiz L, et al. (2000) Cloning and characterization of Entamoeba histolytica antigens recognized by human secretory IgA antibodies. Parasitol Res 86: 330-334.
34. Pancholi V, Fischetti VA (1998) alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem 273: 14503-14515.
35. Pancholi V (2001) Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci 58: 902-920.
36. Gassner C, Schneider-Scherzer E, Lottspeich F, Schweiger M, Schweiger M, et al. (1998) Escherichia coli bacteriophage T1 DNA methyltransferase appears to interact with Escherichia coli enolase. Biol Chem 379: 621-623.
37. Entelis N, Brandina I, Kamenski P, Krasheninnikov I, Martin R, et al. (2006) A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes and Development 5: 1609-1620.
38. Zhang X, Verdine GL (1996) Mammalian DNA cytosine-5 methyltransferase interacts with p23 protein. FEBS Lett 392: 179-183.
39. Esteve P, Chin H, Pradhan S (2005) Human maintenance DNA (cytosine-5)-methyltransferase and p53 modulate expression of p53-repressed promoters. Proc Natl Acad Sci U SA 102: 1000-1005.
40. Kang Ht Fau - Hwang ES, Hwang ES (2006) 2-Deoxyglucose: an anticancer and antiviral therapeutic, but not any more a low glucose mimetic. .
41. Thepsuparungsikul V, Seng L, Bailey GB (1971) Differentiation of Entamoeba: encystation of E. invadens in monoxenic and axenic cultures. J Parasitol 57: 1288-1292.
42. Grummt I, Ladurner AG (2008) A metabolic throttle regulates the epigenetic state of rDNA. Cell 133: 577-580.
43. Ooi SK, Bestor TH (2008) The colorful history of active DNA demethylation. Cell 133: 1145-1148.
44. Gehring M, Reik W, Henikoff S (2009) DNA demethylation by DNA repair. Trends Genet 25: 82-90.
45. Morgan HD, Santos F, Green K, Dean W, Reik W (2005) Epigenetic reprogramming in mammals. Hum Mol Genet 14 Spec No 1: R47-58.
46. Schlegel R, Iversen P, Rechsteiner M (1978) The turnover of tRNAs microinjected into animal cells. Nucleic Acids Res. pp 3715-3729.
47. Mj J, Bystrom AS (2002) Dual function of the tRNA(m(5)U54) methyltransferase in tRNA maturation. RNA 8: 324-335.
48. Studte P, Zink S, Jablonowski D, Bar C, von der Haar T, et al. (2008) tRNA and protein methylase complexes mediate zymocin toxicity in yeast. Mol Microbiol 69: 1266-1277.
49. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, et al. (2007) Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28: 860-870.
50. Jablonowski D, Zink S, Mehlgarten C, Daum G, Schaffrath R (2006) tRNAGlu wobble uridine methylation by Trm9 identifies Elongator's key role for zymocin-induced cell death in yeast. Mol Microbiol 59: 677-688.
51. Lee C, Kramer G, Graham DE, Appling DR (2007) Yeast mitochondrial initiator tRNA is methylated at guanosine 37 by the Trm5-encoded tRNA (guanine-N1-)-methyltransferase. J Biol Chem 282: 27744-27753.
52. Fisher O, Siman-Tov R, Ankri S (2006) Pleiotropic phenotype in Entamoeba histolytica overexpressing DNA methyltransferase (Ehmeth). Mol Biochem Parasitol 147: 48-54.
53. Hamann L, Nickel R, Tannich E (1995) Transfection and continuous expression of heterologous genes in the protozoan parasite Entamoeba histolytica. Proc Natl Acad Sci U SA 92: 8975-8979.
54. Gietz R, Schiestl R (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31-34.
55. Bradford MM (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.
56. Anthon GE, Barrett DM (2003) Modified method for the determination of pyruvic acid with dinitrophenylhydrazine in the assessment of onion pungency. Journal of the Science of Food and Agriculture 83: 1210-1213.
57. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.