A multilocus sequence typing system (MLST) reveals a high level of diversity and a genetic component to Entamoeba histolytica virulence

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Gilchrist, Carol A ^a   Ali, Ibne Karim M ^a   Kabir, Mamun ^b   Alam, Faisal ^c   Scherbakova, Sana ^d   Ferlanti, Eric ^d   Weedall, Gareth D ^e   Hall, Neil ^e   Haque, Rashidul ^b   Petri, William A ^a   Caler, Elisabet ^d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^c RAJSHAHI MEDICAL COLLEGE   (Bangladesh)

^d J CRAIG VENTER INSTITUTE   (United States)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL DNA;

ARTICLE; ENTAMOEBA HISTOLYTICA; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; MULTILOCUS SEQUENCE TYPING SYSTEM; NONHUMAN; PARASITE VIRULENCE; PROTOZOAL GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CHILD; CHILD, PRESCHOOL; CLUSTER ANALYSIS; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; FEMALE; GENETIC VARIATION; HUMANS; INFANT; INFANT, NEWBORN; MALE; MIDDLE AGED; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; VIRULENCE; YOUNG ADULT;

ENTAMOEBA HISTOLYTICA;

EID: 84864201369     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-151     Document Type: Article

References (63)

1. Biodefense Research Agenda for Category B and C Priority Pathogens. NIAID, NIH Publication 2003 03-5315 1 50
2. Entamoeba histolytica infection in children and protection from subsequent amebiasis. Haque R, Mondal D, Duggal P, Kabir M, Roy S, Farr BM, Sack RB, Petri WA, Infect Immun 2006 74 904 909 10.1128/IAI.74.2.904-909.2006 16428733 (Pubitemid 43185523)
3. Influence of human leukocyte antigen class II alleles on susceptibility to Entamoeba histolytica. Duggal P, Haque R, Roy S, Mondal D, Sack RB, Farr BM, Beaty TH, Petri WA, J Infect Dis 2004 189 520 526 10.1086/381272 14745711 (Pubitemid 38213163)
4. A mutation in the leptin receptor is associated with Entamoeba histolytica infection in children. Duggal P, Guo X, Haque R, Peterson KM, Ricklefs S, Mondal D, Alam F, Noor Z, Verkerke HP, Marie C, Leduc CA, Chua SC, Myers MG, Leibel RL, Houpt E, Gilchrist CA, Sher A, Porcella SF, Petri WA, J Clin Invest 2011 121 1191 1198 10.1172/JCI45294 21393862
5. Prospective case-control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Haque R, Mondal D, Karim A, Molla IH, Rahim A, Faruque ASG, Ahmad N, Kirkpatrick BD, Houpt E, Snider C, Petri WA, Clin Infect Dis 2009 48 1191 1197 10.1086/597580 19323634
6. Diagnosis of amebic liver abscess and amebic colitis by detection of Entamoeba histolytica DNA in blood, urine, and saliva by a real-time PCR assay. Haque R, Kabir M, Noor Z, Rahman SMM, Mondal D, Alam F, Rahman I, Al Mahmood A, Ahmed N, Petri WA, J Clin Microbiol 2010 48 2798 2801 10.1128/JCM.00152-10 20534800
7. Crosstalk at the initial encounter: interplay between host defense and ameba survival strategies. Guo X, Houpt E, Petri WA, Curr Opin Immunol 2007 19 376 384 10.1016/j.coi.2007.07.005 17702556 (Pubitemid 47284863)
8. Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Gilchrist CA HE, Trapaidze N, Fei Z, Crasta O, Asgharpour A, Evans C, Martino-Catt S, Baba DJ, Stroup S, Hamano S, Ehrenkaufer G, Okada M, Singh U, Nozaki T, Mann BJ, Petri WA, Mol Biochem Parasitol 2006 147 163 76 10.1016/j.molbiopara.2006.02.007 16569449
9. Regulation of Virulence of Entamoeba histolytica by the URE3-BP Transcription Factor. Gilchrist CA, Moore ES, Zhang Y, Bousquet CB, Lannigan JA, Mann BJ, Petri WA, mBio 2010 1 00057 10 20689746
10. Using differential gene expression to study Entamoeba histolytica pathogenesis. Gilchrist CA, Petri WA, Trends Parasitol 2009 25 124 131 10.1016/j.pt.2008.12.007 19217826
11. Structure and content of the Entamoeba histolytica genome. Clark CG, Alsmark UCM, Tazreiter M, Saito-Nakano Y, Ali V, Marion S, Weber C, Mukherjee C, Bruchhaus I, Tannich E, Leippe M, Sicheritz-Ponten T, Foster PG, Samuelson J, Nol CJ, Hirt RP, Embley TM, Gilchrist CA, Mann BJ, Singh U, Ackers JP, Bhattacharya S, Bhattacharya A, Lohia A, Guillén N, Duchêne M, Nozaki T, Hall N, Adv Parasitol 2007 65 51 190 18063096 (Pubitemid 350183945)
12. Recent insights into Entamoeba development: identification of transcriptional networks associated with stage conversion. Singh U, Ehrenkaufer GM, Int J Parasitol 2009 39 41 47 10.1016/j.ijpara.2008.09.004 18938171
13. Genomic DNA microarrays for Entamoeba histolytica: applications for use in expression profiling and strain genotyping. MacFarlane R, Bhattacharya D, Singh U, Exp Parasitol 2005 110 196 202 10.1016/j.exppara.2005.03.006 15955312 (Pubitemid 40813358)
14. Short hairpin RNA-mediated knockdown of protein expression in Entamoeba histolytica. Linford AS, Moreno H, Good KR, Zhang H, Singh U, Petri WA, BMC Microbiol 2009 9 38 10.1186/1471-2180-9-38 19222852
15. Transcriptional silencing of multiple genes in trophozoites of Entamoeba histolytica. Bracha R, Nuchamowitz Y, Anbar M, Mirelman D, PLoS Pathogens 2006 2 48 10.1371/journal.ppat.0020048 16733544 (Pubitemid 43794310)
16. Nuclear localized antisense small RNAs with 5-polyphosphate termini regulate long-term transcriptional gene silencing in Entamoeba histolytica G3 strain. Zhang H, Alramini H, Tran V, Singh U, J Biol Chem 2011 286 44467 44479 10.1074/jbc.M111.278184 22049083
17. Development of a negative selectable marker for Entamoeba histolytica. Abhyankar MM, Haviland SM, Gilchrist CA, Petri WA, J Visualized Exp 2010 46 2410 10.3791/2410
18. Geographic diversity among genotypes of Entamoeba histolytica field isolates. Haghighi A, Kobayashi S, Takeuchi T, Thammapalerd N, Nozaki T, J Clin Microbiol 2003 41 3748 3756 10.1128/JCM.41.8.3748-3756.2003 12904386 (Pubitemid 36994712)
19. Entamoeba histolytica: genetic diversity of African strains based on the polymorphism of the serine-rich protein gene. Samie A, Obi CL, Bessong PO, Houpt E, Stroup S, Njayou M, Sabeta C, Mduluza T, Guerrant RL, Exp Parasitol 2008 118 354 361 10.1016/j.exppara.2007.09.008 18028911 (Pubitemid 351181431)
20. Entamoeba histolytica: the serine-rich gene polymorphism-based genetic variability of clinical isolates from Georgia. Simonishvili S, Tsanava S, Sanadze K, Chlikadze R, Miskalishvili A, Lomkatsi N, Imnadze P, Petri WA, Trapaidze N, Exp Parasitol 2005 110 313 317 10.1016/j.exppara.2005.02.015 15955330 (Pubitemid 40813378)
21. Remarkable genetic polymorphism among Entamoeba histolytica isolates from a limited geographic area. Haghighi A, Kobayashi S, Takeuchi T, Masuda G, Nozaki T, J Clin Microbiol 2002 40 4081 4090 10.1128/JCM.40.11.4081-4090.2002 12409379 (Pubitemid 35285794)
22. Molecular epidemiology of Entamoeba spp.: evidence of a bottleneck (Demographic sweep) and transcontinental spread of diploid parasites. Ghosh S, Frisardi M, Ramirez-Avila L, Descoteaux S, Sturm-Ramirez K, Newton-Sanchez OA, Santos-Preciado JI, Ganguly C, Lohia A, Reed S, Samuelson J, J Clin Microbiol 2000 38 3815 3821 11015408
23. Use of PCR amplification of tRNA gene-linked short tandem repeats for genotyping Entamoeba histolytica. Ali IKM, Zaki M, Clark CG, J Clin Microbiol 2005 43 5842 5847 10.1128/JCM.43.12.5842-5847.2005 16333065 (Pubitemid 43100627)
24. Evidence for a link between parasite genotype and outcome of infection with Entamoeba histolytica. Ali IKM, Mondal U, Roy S, Haque R, Petri WA, Clark CG, J Clin Microbiol 2007 45 285 289 10.1128/JCM.01335-06 17122021
25. Longitudinal study of intestinal Entamoeba histolytica infections in asymptomatic adult carriers. Blessmann J, Ali IKM, Nu PAT, Dinh BT, Viet TQN, Van AL, Clark CG, Tannich E, J Clin Microbiol 2003 41 4745 4750 10.1128/JCM.41.10.4745-4750.2003 14532214 (Pubitemid 37259788)
26. Evidence for a link between locus R-R sequence type and outcome of infection with Entamoeba histolytica. Ali IKM, Haque R, Alam F, Kabir M, Siddique A, Petri WA, Clin Microbiol Infect 2012 18 235 7 10.1111/j.1469-0691. 2012.03826.x 22448930
27. Unique organisation of tRNA genes in Entamoeba histolytica. Clark CG, Ali IKM, Zaki M, Loftus BJ, Hall N, Mol Biochem Parasitol 2006 146 24 29 10.1016/j.molbiopara.2005.10.013 16307803 (Pubitemid 43132799)
28. Tissue invasion by Entamoeba histolytica: evidence of genetic selection and/or DNA reorganization events in organ tropism. Ali IKM, Solaymani-Mohammadi S, Akhter J, Roy S, Gorrini C, Calderaro A, Parker SK, Haque R, Petri WA, Clark CG, PLoS Negl Trop Dis 2008 2 219 10.1371/journal.pntd.0000219 18398490 (Pubitemid 352002925)
29. Identification of an avirulent Entamoeba histolytica strain with unique tRNA-linked short tandem repeat markers. Escueta-de Cadiz A, Kobayashi S, Takeuchi T, Tachibana H, Nozaki T, Parasitol Int 2010 59 75 81 10.1016/j.parint.2009.10.010 19895903
30. Amebiasis in HIV-1-infected Japanese men: clinical features and response to therapy. Watanabe K, Gatanaga H, Escueta-de Cadiz A, Tanuma J, Nozaki T, Oka S, PLoS Negl Trop Dis 2011 5 1318 10.1371/journal.pntd.0001318 21931875
31. A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Tibayrenc M, Kjellberg F, Ayala FJ, Proc Natl Acad Sci U S A 1990 87 2414 2418 10.1073/pnas.87.7.2414 2320563
32. Advances in mechanisms of genetic instability related to hereditary neurological diseases. Wells RD, Dere R, Hebert ML, Napierala M, Son LS, Nucleic Acids Res 2005 33 3785 3798 10.1093/nar/gki697 16006624 (Pubitemid 41418548)
33. New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. Lorenzi HA, Puiu D, Miller JR, Brinkac LM, Amedeo P, Hall N, Caler EV, PLoS Negl Trop Dis 2010 4 716 10.1371/journal.pntd.0000716 20559563
34. The genome of the protist parasite Entamoeba histolytica. Loftus B, Anderson I, Davies R, Alsmark UCM, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillén N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El-Sayed NM, Petri WA, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N, Nature 2005 433 865 868 10.1038/nature03291 15729342 (Pubitemid 40314894)
35. Genomic diversity of the human intestinal parasite Entamoeba histolytica. Weedall GD, Clark CG, Koldkjær P, Kay S, Bruchhaus I, Paterson S, Hall N, Genome Biol 13 5 38 [Epub ahead of print]
36. Coding and noncoding genomic regions of Entamoeba histolytica have significantly different rates of sequence polymorphisms: implications for epidemiological studies. Bhattacharya D, Haque R, Singh U, J Clin Microbiol 2005 43 4815 9 10.1128/JCM.43.9.4815-4819.2005 16145147 (Pubitemid 41298283)
37. Host-Parasite interactions in Entamoeba histolytica and Entamoeba dispar: what have we learned from their genomes? Wilson IW, Weedall GD, Hall N, Parasite Immunology 34 90 99
38. Entamoeba shows reversible variation in ploidy under different growth conditions and between life cycle phases. Mukherjee C, Clark CG, Lohia A, PLoS Negl Trop Dis 2008 2 281 10.1371/journal.pntd.0000281 18714361
39. Use of a monoclonal antibody in an enzyme immunoassay for the detection of Entamoeba histolytica in fecal specimens. Ungar BL, Yolken RH, Quinn TC, AmJTrop Med Hyg 1985 34 465 472 (Pubitemid 15041369)
40. A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. Diamond LS, Clark CG, J Eukaryot Microbiol 40 340 344
41. Involvement of p21racA, phosphoinositide 3-kinase, and vacuolar ATPase in phagocytosis of bacteria and erythrocytes by Entamoeba histolytica: suggestive evidence for coincidental evolution of amebic invasiveness. Ghosh SK, Samuelson J, Infect Immun 1997 65 4243 4249 9317033 (Pubitemid 27422084)
42. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739 10.1093/molbev/msr121 21546353
43. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. Blom N, Gammeltoft S, Brunak S, J Mol Biol 1999 294 1351 1362 10.1006/jmbi.1999.3310 10600390 (Pubitemid 30008805)
44. Targets of the Entamoeba histolytica transcription factor URE3-BP. Gilchrist CA, Baba DJ, Zhang Y, Crasta O, Evans C, Caler E, Sobral BWS, Bousquet CB, Leo M, Hochreiter A, Connell SK, Mann BJ, Petri WA, PLoS Negl Trop Dis 2008 2 282 10.1371/journal.pntd.0000282 18846235
45. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Li L, Stoeckert CJ, Roos DS, Genome Res 2003 13 2178 2189 10.1101/gr.1224503 12952885 (Pubitemid 37161775)
46. Amebic liver abscess. Hughes MA, Petri WA, Infect Dis Clin N Am 2000 14 565 582 viii 10.1016/S0891-5520(05)70121-5
47. Human non-synonymous SNPs: server and survey. Ramensky V, Bork P, Sunyaev S, Nucleic Acids Res 2002 30 3894 3900 10.1093/nar/gkf493 12202775 (Pubitemid 35012462)
48. SIFT: Predicting amino acid changes that affect protein function. Ng PC, Henikoff S, Nucleic Acids Res 2003 31 3812 3814 10.1093/nar/gkg509 12824425 (Pubitemid 37442253)
49. Genome wide survey, discovery and evolution of repetitive elements in three Entamoeba species. Lorenzi H, Thiagarajan M, Haas B, Wortman J, Hall N, Caler E, BMC Genomics 2008 9 595 10.1186/1471-2164-9-595 19077187
50. Intermediate subunit of the Gal/GalNAc lectin of Entamoeba histolytica is a member of a gene family containing multiple CXXC sequence motifs. Cheng XJ, Hughes MA, Huston CD, Loftus B, Gilchrist CA, Lockhart LA, Ghosh S, Miller-Sims V, Mann BJ, Petri WA, Tachibana H, Infect Immun 2001 69 5892 5898 10.1128/IAI.69.9.5892-5898.2001 11500468 (Pubitemid 32786530)
51. The bittersweet interface of parasite and host: lectin-carbohydrate interactions during human invasion by the parasite Entamoeba histolytica. Petri WA, Haque R, Mann BJ, Annu Rev Microbiol 2002 56 39 64 10.1146/annurev.micro.56. 012302.160959 12142490 (Pubitemid 35217447)
52. Genetic diversity of Toxoplasma gondii in animals and humans. Sibley LD, Khan A, Ajioka JW, Rosenthal BM, Philos Trans R Soc Lond 2009 364 2749 2761 10.1098/rstb.2009.0087
53. Laboratory cultivation of some human parasitic amoebae. Robinson GL, J Gen Microbiol 1968 53 69 79 10.1099/00221287-53-1-69 4300396
54. High throughput multiplex PCR and probe-based detection with Luminex beads for seven intestinal parasites. Taniuchi M, Verweij JJ, Noor Z, Sobuz SU, van Lieshout L, Petri WA, Haque R, Houpt ER, AmJTrop Med Hyg 2011 84 332 337
55. Amebiasis. Haque R, Huston CD, Hughes M, Houpt E, Petri WA, N Engl J Med 2003 348 1565 1573 10.1056/NEJMra022710 12700377 (Pubitemid 36437934)
56. Primer3 on the WWW for general users and for biologist programmers. Rozen S, Skaletsky H, Methods in Molecular Biology 2000 132 365 386 10547847
57. AmoebaDB and MicrosporidiaDB: functional genomic resources for Amoebozoa and Microsporidia species. Aurrecoechea C, Barreto A, Brestelli J, Brunk BP, Caler EV, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Iodice J, Kissinger JC, Kraemer ET, Li W, Nayak V, Pennington C, Pinney DF, Pitts B, Roos DS, Srinivasamoorthy G, Stoeckert CJ, Treatman C, Wang H, Nucleic Acids Res 2011 39 612 619 10.1093/nar/gkq1006 20974635
58. dbSNP: the NCBI database of genetic variation. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K, Nucleic Acids Res 2001 29 308 311 10.1093/nar/29.1.308 11125122 (Pubitemid 32054478)
59. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Meyer M, Kircher M, Cold Spring Harbor Protocols 2010 2010 db.prot5448 10.1101/pdb.prot5448 20516186
60. An SNP map of the human genome generated by reduced representation shotgun sequencing. Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES, Nature 2000 407 513 516 10.1038/35035083 11029002
61. Aligning multiple whole genomes with Mercator and MAVID. Dewey CN, Meth Mol Biol 2007 395 221 236 10.1007/978-1-59745-514-5-14
62. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Benjamini Y, Hochberg Y, J Royal Stat Soc. Series B (Methodological) 2010 57 289 300
63. R: A Language for Data Analysis and Graphics. Ihaka R, Gentleman R, J Comput Graph Stat 1996 5 299 314