Growth of the protozoan parasite Entamoeba histolytica in 5-azacytidine has limited effects on parasite gene expression

BMC Genomics

Volumn 8, Issue , 2007, Pages

  Ali, Ibne Kairim M ^a   Ehrenkaufer, Gretchen M ^a   Hackney, Jason A ^a   Singh, Upinder ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; BISULFITE; CYSTEINE PROTEINASE; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE INHIBITOR; GENOMIC DNA; LYSOZYME;

ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DNA METHYLATION; DNA MICROARRAY; DOWN REGULATION; ENTAMOEBA HISTOLYTICA; GENE CONTROL; GENE EXPRESSION; GENE NUMBER; GENE SEQUENCE; GENE SILENCING; GENOME; MICROBIAL GROWTH; NONHUMAN; PARASITE VIRULENCE; PATHOGENESIS; PROTOZOON; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; AZACITIDINE; CHO CELLS; CRICETINAE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENTAMOEBA HISTOLYTICA; GENE EXPRESSION REGULATION; GENE SILENCING; GENES, PROTOZOAN; GENOME, PROTOZOAN; MESOCRICETUS; MICROARRAY ANALYSIS; PROTOZOAN PROTEINS; VIRULENCE;

ENTAMOEBA HISTOLYTICA; EUKARYOTA; PROTOZOA;

EID: 33846820165     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-8-7     Document Type: Article

References (74)

1. Razin A Cedar H DNA methylation and gene expression Microbiol Rev 1991 55 3 451-458 372829 1943996
2. Katoh M Curk T Xu Q Zupan B Kuspa A Shaulsky G Developmentally regulated DNA methylation in Dictyostelium discoideum Eukaryot Cell 2006 5 1 18 25 1360260 16400165 10.1128/EC.5.1.18-25.2006
3. Yoder JA Walsh CP Bestor TH Cytosine methylation and the ecology of intragenomic parasites Trends Genet 1997 13 8 335-340 10.1016/ S0168-9525(97)01181-5 9260521
4. Robertson KD DNA methylation and chromatin - unraveling the tangled web Oncogene 2002 21 35 5361-5379 10.1038/sj.onc.1205609 12154399
5. Goto T Monk M Regulation of X-chromosome inactivation in development in mice and humans Microbiol Mol Biol Rev 1998 62 2 362-378 98919 9618446
6. Dodge JE Ramsahoye BH Wo ZG Okano M Li E De novo methylation of MMLV provirus in embryonic stem cells: CpG versus non-CpG methylation Gene 2002 289 1-2 41-48 10.1016/S0378-1119(02)00469-9 12036582
7. Comb M Goodman HM CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2 Nucleic Acids Res 1990 18 13 3975 3982 331101 1695733 10.1093/nar/18.13.3975
8. Inamdar NM Ehrlich KC Ehrlich M CpG methylation inhibits binding of several sequence-specific DNA-binding proteins from pea, wheat, soybean and cauliflower Plant Mol Biol 1991 17 1 111-123 10.1007/BF00036811 1831056
9. Jones PL Veenstra GJ Wade PA Vermaak D Kass SU Landsberger N Strouboulis J Wolffe AP Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription Nat Genet 1998 19 2 187-191 10.1038/561 9620779
10. Nan X Ng HH Johnson CA Laherty CD Turner BM Eisenman RN Bird A Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex Nature 1998 393 6683 386-389 10.1038/30764 9620804
11. Esteller M Fraga MF Guo M Garcia-Foncillas J Hedenfalk I Godwin AK Trojan J Vaurs-Barriere C Bignon YJ Ramus S DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis Hum Mol Genet 2001 10 26 3001-3007 10.1093/hmg/10.26.3001 11751682
12. Sharma RP Schizophrenia, epigenetics and ligand-activated nuclear receptors: A framework for chromatin therapeutics Schizophr Res 2005 72 2-3 79-90 10.1016/j.schres.2004.03.001 15560954
13. Liu L Wylie RC Andrews LG Tollefsbol TO Aging, cancer and nutrition: The DNA methylation connection Mech Ageing Dev 2003 124 10-12 989 998 10.1016/j.mad.2003.08.001 14659588
14. WHO/PAHO/UNESCO report. A consultation with experts on amoebiasis. Mexico City, Mexico 28-29 January, 1997 Epidemiol Bull 1997 18 1 13-4
15. Fisher O Siman-Tov R Ankri S Characterization of cytosine methylated regions and 5-cytosine DNA methyltransferase (Ehmeth) in the protozoan parasitec Entamoeba histolytica Nucleic Acids Res 2004 32 1 287-297 373271 14715927 10.1093/nar/gkh161
16. Bernes S Siman-Tov R Ankri S Epigenetic and classical activation of Entamoeba histolytica heat shock protein 100 (EHsp100) expression FEBS Lett 2005 579 28 6395-6402 10.1016/j.febslet.2005.09.101 16263115
17. Lavi T Isakov E Harony H Fisher O Siman-Tov R Ankri S Sensing DNA methylation in the protozoan parasite Entamoeba histolytica Mol Microbiol 2006 17059565
18. Fisher O Siman-Tov R Ankri S Pleiotropic phenotype in Entamoeba histolytica overexpressing DNA methyltransferase (Ehmeth) Mol Biochem Parasitol 2006 147 1 48-54 16497397
19. Rojas MV Galanti N Relationship between DNA methylation and cell proliferation in Trypanosoma cruzi FEBS Lett 1991 295 1-3 31-34 10.1016/ 0014-5793(91)81377-K 1722465
20. Juranek S Wieden HJ Lipps HJ De novo cytosine methylation in the differentiating macronucleus of the stichotrichous ciliate Stylonychia lemnae Nucleic Acids Res 2003 31 5 1387-1391 149826 12595545 10.1093/nar/ gkg233
21. Palacios G Martin-Gonzalez A Gutierrez JC Macronuclear DNA demethylation is involved in the encystment process of the ciliate Colpoda inflata Cell Biol Int 1994 18 4 223-228 10.1006/cbir.1994.1067 7519095
22. Yamashita S Tsujino Y Moriguchi K Tatematsu M Ushijima T Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2′-deoxycytidine treatment and oligonucleotide microarray Cancer Sci 2006 97 1 64-71 10.1111/j.1349-7006.2006.00136.x 16367923
23. Suzuki H Gabrielson E Chen W Anbazhagan R van Engeland M Weijenberg MP Herman JG Baylin SB A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer Nat Genet 2002 31 2 141-149 10.1038/ng892 11992124
24. Yamashita K Upadhyay S Osada M Hoque MO Xiao Y Mori M Sato F Meltzer SJ Sidransky D Pharmacologic unmasking of epigenetically silenced tumor suppressor genes in esophageal squamous cell carcinoma Cancer Cell 2002 2 6 485-495 10.1016/S1535-6108(02)00215-5 12498717
25. Pompeia C Hodge DR Plass C Wu YZ Marquez VE Kelley JA Farrar WL Microarray analysis of epigenetic silencing of gene expression in the KAS-6/1 multiple myeloma cell line Cancer Res 2004 64 10 3465-3473 10.1158/0008-5472.CAN-03-3970 15150099
26. Chang S Pikaard CS Transcript profiling in Arabidopsis reveals complex responses to global inhibition of DNA methylation and histone deacetylation J Biol Chem 2005 280 1 796-804 15516340
27. Gilchrist CA Houpt E Trapaidze N Fei Z Crasta O Asgharpour A Evans C Martino-Catt S Baba DJ Stroup S Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome Mol Biochem Parasitol 2006 147 2 163-176 10.1016/j.molbiopara.2006.02.007 16569449
28. Orozco E Martinez-Palomo A Lopez-Revilla R [An in vitro model for the quantitative study of E. histolytica virulence] Arch Invest Med (Mex) 1978 9 Suppl 1 257-260 211959
29. Ghadirian E Meerovitch E Pathogenicity of axenically cultivated Entamoeba histolytica, strain 200:NIH, in the hamster J Parasitol 1979 65 5 768-771 10.2307/3280359 229205
30. Shah PH MacFarlane RC Bhattacharya D Matese JC Demeter J Stroup SE Singh U Comparative genomic hybridizations of Entamoeba strains reveal unique genetic fingerprints that correlate with virulence Eukaryot Cell 2005 4 3 504-515 1087797 15755913 10.1128/EC.4.3.504-515.2005
31. MacFarlane RC Singh U Identification of differentially expressed genes in virulent and nonvirulent Entamoeba species: Potential implications for amebic pathogenesis Infect Immun 2006 74 1 340-351 1346599 16368989 10.1128/IAI.74.1.340-351.2006
32. Anbar M Bracha R Nuchamowitz Y Li Y Florentin A Mirelman D Involvement of a short interspersed element in epigenetic transcriptional silencing of the amoebapore gene in Entamoeba histolytica Eukaryot Cell 2005 4 11 1775-1784 1287852 16278444 10.1128/EC.4.11.1775-1784.2005
33. Li M Ou X Lee TD Zeng Y Mato JM Lu SC Silencing of human methionine adenosyltransferase 1A expression by methylation of the coding region J Biol Chem 2004
34. Banerjee S Fisher O Lohia A Ankri S 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 2005 139 1 91-97 10.1016/j.molbiopara.2004.10.003 15610823
35. Entamoeba histolytica Genome Project http://www.tigr.org/tdb/e2k1/eha1/
36. Bracha R Nuchamowitz Y Anbar M Mirelman D Transcriptional silencing of multiple genes in trophozoites of Entamoeba histolytica PLoS Pathog 2006 2 5 e48 1464398 16733544 10.1371/journal.ppat.0020048
37. Platt GM Price C Isolation of a Schizosaccharomyces pombe gene which in high copy confers resistance to the nucleoside analogue 5-azacytidine Yeast 1997 13 5 463-474 10.1002/ (SICI)1097-0061(199704)13:5<463::AID-YEA89>3.0.CO;2-B 9153756
38. Mathieu O Bender J RNA-directed DNA methylation J Cell Sci 2004 117 Pt 21 4881-4888 10.1242/jcs.01479 15456843
39. Hubacek J Biological function of DNA methylation Folia Microbiol (Praha) 1992 37 5 323-329 1337330
40. Doskocil J Sormo'Va Z The Occurrence Of 5-Methylcytosine In Bacterial Deoxyribonucleic Acids Biochim Biophys Acta 1965 95 513-515 14342545
41. Dunn DB Smith JD The occurrence of 6-methylaminopurine in deoxyribonucleic acids Biochem J 1958 68 4 627-636 1200409 13522672
42. Ehrlich M Gama-Sosa MA Carreira LH Ljungdahl LG Kuo KC Gehrke CW DNA methylation in thermophilic bacteria: N4-methylcytosine, 5-methylcytosine, and N6-methyladenine Nucleic Acids Res 1985 13 4 1399-1412 341080 4000939 10.1093/nar/13.4.1399
43. Clark SJ Warnecke PM DNA methylation analysis in mammalian cells Methods 2002 27 2 99-100 10.1016/S1046-2023(02)00059-2 12095265
44. Lorincz MC Dickerson DR Schmitt M Groudine M Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells Nat Struct Mol Biol 2004 11 11 1068-1075 10.1038/nsmb840 15467727
45. Borsatti F Casarini L Mandrioli M Analysis of the expression pattern of the defensin gene in the lepidopteran Mamestra brassicae Invert Surv J 2004 1 34-37 http://www.isj.unimo.it/vol1issue1.htm
46. Hick CA Field LM Devonshire AL Changes in the methylation of amplified esterase DNA during loss and reselection of insecticide resistance in peach-potato aphids, Myzus persicae Insect Biochem Mol Biol 1996 26 1 41-47 10.1016/0965-1748(95)00059-3 8673078
47. Field LM Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer) Biochem J 2000 349 Pt 3 863-868 1221215 10903149
48. Bongiorni S Cintio O Prantera G The relationship between DNA methylation and chromosome imprinting in the coccid Planococcus citri Genetics 1999 151 4 1471-1478 1460555 10101170
49. Bongiorni S Prantera G Imprinted facultative heterochromatization in mealybugs Genetica 2003 117 2-3 271 279 10.1023/A:1022964700446 12723706
50. Klose RJ Bird AP Genomic DNA methylation: The mark and its mediators Trends Biochem Sci 2006 31 2 89-97 10.1016/j.tibs.2005.12.008 16403636
51. Eichinger L Noegel AA Comparative genomics of Dictyostelium discoideum and Entamoeba histolytica Curr Opin Microbiol 2005 8 5 606-611 10.1016/ j.mib.2005.08.009 16125444
52. Harony H Bernes S Siman-Tov R Ankri S DNA methylation and targeting of LINE retrotransposons in Entamoeba histolytica and Entamoeba invadens Mol Biochem Parasitol 2006 147 1 55-63 16530279
53. Thornburg BG Gotea V Makalowski W Transposable elements as a significant source of transcription regulating signals Gene 2006 365 104-110 10.1016/ j.gene.2005.09.036 16376497
54. Park CW Kren BT Largaespada DA Steer CJ DNA methylation of Sleeping Beauty with transposition into the mouse genome Genes Cells 2005 10 8 763-776 10.1111/j.1365-2443.2005.00875.x 16098140
55. Bakre AA Rawal K Ramaswamy R Bhattacharya A Bhattacharya S The LINEs and SINEs of Entamoeba histolytica: Comparative analysis and genomic distribution Exp Parasitol 2005 110 3 207-213 10.1016/ j.exppara.2005.02.009 15955314
56. Que X Reed SL Cysteine proteinases and the pathogenesis of amebiasis Clin Microbiol Rev 2000 13 2 196-206 100150 10755997 10.1128/ CMR.13.2.196-206.2000
57. Ankri S Stolarsky T Mirelman D Antisense inhibition of expression of cysteine proteinases does not affect Entamoeba histolytica cytopathic or haemolytic activity but inhibits phagocytosis Mol Microbiol 1998 28 4 777-785 10.1046/j.1365-2958.1998.00837.x 9643545
58. Ankri S Stolarsky T Bracha R Padilla-Vaca F Mirelman D Antisense inhibition of expression of cysteine proteinases affects Entamoeba histolytica-induced formation of liver abscess in hamsters Infect Immun 1999 67 1 421-422 96327 9864246
59. Jacobs T Leippe M Purification and molecular cloning of a major antibacterial protein of the protozoan parasite Entamoeba histolytica with lysozyme-like properties Eur J Biochem 1995 231 3 831-838 10.1111/ j.1432-1033.1995.0831d.x 7649184
60. Coudrier E Amblard F Zimmer C Roux P Olivo-Marin JC Rigothier MC Guillen N Myosin II and the Gal-GalNAc lectin play a crucial role in tissue invasion by Entamoeba histolytica Cell Microbiol 2005 7 1 19-27 10.1111/ j.1462-5822.2004.00426.x 15617520
61. Meissner M Schluter D Soldati D Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion Science 2002 298 5594 837-840 10.1126/science.1074553 12399593
62. Saito-Nakano Y Loftus BJ Hall N Nozaki T The diversity of Rab GTPases in Entamoeba histolytica Exp Parasitol 2005 110 3 244-252 10.1016/ j.exppara.2005.02.021 15955319
63. Ehrenkaufer G Hauqe R Hackney J Eichinger D Singh U Identification of developmentally regulated genes in Entamoeba histolytica: Insights into mechanisms of stage conversion in a protozoan parasite Cellular Microbiology
64. Gilchrist CA Petri WA Virulence factors of Entamoeba histolytica Curr Opin Microbiol 1999 2 4 433-437 10.1016/S1369-5274(99)80076-9 10458982
65. Goll MG Kirpekar F Maggert KA Yoder JA Hsieh CL Zhang X Golic KG Jacobsen SE Bestor TH Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2 Science 2006 311 5759 395-398 10.1126/ science.1120976 16424344
66. Diamond LS Harlow DR Cunnick CC A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba Trans R Soc Trop Med Hyg 1978 72 4 431-432 10.1016/0035-9203(78)90144-X 212851
67. Clark CG Diamond LS Entamoeba histolytica: A method for isolate identification Exp Parasitol 1993 77 4 450-455 10.1006/expr.1993.1105 8253158
68. Bradford MM A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 1976 72 248-254 10.1016/0003-2697(76)90527-3 942051
69. Bracha R Mirelman D Virulence of Entamoeba histolytica trophozoites. Effects of bacteria, microaerobic conditions, and metronidazole J Exp Med 1984 160 2 353-368 10.1084/jem.160.2.353 6088660
70. Loftus B Anderson I Davies R Alsmark UC Samuelson J Amedeo P Roncaglia P Berriman M Hirt RP Mann BJ The genome of the protist parasite Entamoeba histolytica Nature 2005 433 7028 865-868 10.1038/nature03291 15729342
71. Stanford Protein and Nucleic Acid Biotechnology Facility http:// cmgm.stanford.edu/pan/index.html
72. GeneSpring software http://www.silicongenetics.com
73. Entamoeba histolytica sequence BLAST search http://tigrblast.tigr.org/ er-blast/index.cgi?project=eha1
74. Python http://www.python.org