Abstract
Genome sequence analysis of Entamoeba species revealed various classes of transposable elements. While E. histolytica and E. dispar are rich in non-long terminal repeat (LTR) retrotransposons, E. invadens contains predominantly DNA transposons. Non-LTR retrotransposons of E. histolytica constitute three families of long interspersed nuclear elements (LINEs), and their short, nonautonomous partners, SINEs. They occupy ~ 11% of the genome. The EhLINE1/EhSINE1 family is the most abundant and best studied. EhLINE1 is 4.8 kb, with two ORFs that encode functions needed for retrotransposition. ORF1 codes for the nucleic acid-binding protein, and ORF2 has domains for reverse transcriptase (RT) and endonuclease (EN). Most copies of EhLINEs lack complete ORFs. ORF1p is expressed constitutively, but ORF2p is not detected. Retrotransposition could be demonstrated upon ectopic over expression of ORF2p, showing that retrotransposition machinery is functional. The newly retrotransposed sequences showed a high degree of recombination. In transcriptomic analysis, RNA-Seq reads were mapped to individual EhLINE1 copies. Although full-length copies were transcribed, no full-length 4.8 kb transcripts were seen. Rather, sense transcripts mapped to ORF1, RT and EN domains. Intriguingly, there was strong antisense transcription almost exclusively from the RT domain. These unique features of EhLINE1 could serve to attenuate retrotransposition in E. histolytica.
This is a preview of subscription content, log in via an institution to check access.
Adapted from Lorenzi et al. (2008)
(adapted from Yadav et al. 2012)
(adapted from Kaur et al. 2021)
Similar content being viewed by others
References
Agrahari M, Gaurav AK, Bhattacharya A, Bhattacharya S (2017) Cytosine DNA methylation at promoter of non LTR retrotransposon and heat shock protein gene (HSP70) of Entamoeba histolytica and lack of correlation with transcription status. Mol Biochem Parasitol. https://doi.org/10.1016/j.molbiopara.2017.01.001
Aksoy S, Williams S, Chang S, Richards FF (1990) SLACS retrotransposon from Trypanosoma brucei gambiense is similar to mammalian LINEs. Nucleic Acids Res. https://doi.org/10.1093/nar/18.4.785
Alexandrova EA, Olovnikov IA, Malakhova GV, Zabolotneva AA, Suntsova MV, Dmitriev SE, Buzdin AA (2012) Sense transcripts originated from an internal part of the human retrotransposon LINE-1 5′ UTR. Gene. https://doi.org/10.1016/j.gene.2012.09.026
Alisch RS, Garcia-Perez JL, Muotri AR, Gage FH, Moran JV (2006) Unconventional translation of mammalian LINE-1 retrotransposons. Genes Dev. https://doi.org/10.1101/gad.1380406
Arkhipova IR, Morrison HG (2001) Three retrotransposon families in the genome of Giardia lamblia: two telomeric, one dead. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.231494798
Bagchi A, Bhattacharya A, Bhattacharya S (1999) Lack of a chromosomal copy of the circular rDNA plasmid of Entamoeba histolytica. Int J Parasitol 29(11):1775–1783. https://doi.org/10.1016/s0020-7519(99)00125-3
Bagchi A (2001) Studies on structure and organization of chromosomes in Entamoeba histolytica. Ph.D. thesis, Jawaharlal Nehru University, New Delhi, India
Bakre AA, Rawal K, Ramaswamy R, Bhattacharya A, Bhattacharya S (2005) The LINEs and SINEs of Entamoeba histolytica: comparative analysis and genomic distribution. Exp Parasitol. https://doi.org/10.1016/j.exppara.2005.02.009
Bhattacharya S, Bakre A, Bhattacharya A (2002) Mobile genetic elements in protozoan parasites. J Genet. https://doi.org/10.1007/BF02715903
Bibiłło A, Eickbush TH (2002) The reverse transcriptase of the R2 non-LTR retrotransposon: continuous synthesis of cDNA on non-continuous RNA templates. J Mol Biol. https://doi.org/10.1006/jmbi.2001.5369
Bibillo A, Eickbush TH (2004) End-to-end template jumping by the reverse transcriptase encoded by the R2 retrotransposon. J Biol Chem. https://doi.org/10.1074/jbc.M310450200
Boeke JD (1997) Lines and Alus—the polyA connection. Nat Genet. https://doi.org/10.1038/ng0597-6
Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434. https://doi.org/10.1146/annurev.mi.43.100189.002155
Bringaud F, Biteau N, Melville SE, Hez S, El-Sayed NM, Leech V, Berriman M, Hall N, Donelson JE, Baltz T (2002) A new, expressed multigene family containing a hot spot for insertion of retroelements is associated with polymorphic subtelomeric regions of Trypanosoma brucei. Eukaryot Cell. https://doi.org/10.1128/EC.1.1.137-151.2002
Bringaud F, Müller M, Cerqueira GC, Smith M, Rochette A, El-Sayed NMA, Papadopoulou B, Ghedin E (2007) Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog. https://doi.org/10.1371/journal.ppat.0030136
Bringaud F, Ghedin E, El-Sayed NMA, Papadopoulou B (2008) Role of transposable elements in trypanosomatids. Microbes Infect. https://doi.org/10.1016/j.micinf.2008.02.009
Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian HH (2003) Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.0831042100
Burke WD, Malik HS, Rich SM, Eickbush TH (2002) Ancient lineages of non-LTR retrotransposons in the primitive eukaryote, Giardia lamblia. Mol Biol Evol 19(5):619–630. https://doi.org/10.1093/oxfordjournals.molbev.a004121
Callahan KE, Hickman AB, Jones CE, Ghirlando R, Furano AV (2012) Polymerization and nucleic acid-binding properties of human L1 ORF1 protein. Nucleic Acids Res. https://doi.org/10.1093/nar/gkr728
Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, Attreed M, Avner P, Wutz A, Barillot E, Greally JM, Voinnet O, Heard E (2010) LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell. https://doi.org/10.1016/j.cell.2010.04.042
Christensen SM, Eickbush TH (2005) R2 target-primed reverse transcription: ordered cleavage and polymerization steps by protein subunits asymmetrically bound to the target DNA. Mol Cell Biol. https://doi.org/10.1128/mcb.25.15.6617-6628.2005
Christensen SM, Bibillo A, Eickbush TH (2005) Role of the Bombyx mori R2 element N-terminal domain in the target-primed reverse transcription (TPRT) reaction. Nucleic Acids Res. https://doi.org/10.1093/nar/gki957
Cost GJ, Feng Q, Jacquier A, Boeke JD (2002) Human L1 element target-primed reverse transcription in vitro. EMBO J. https://doi.org/10.1093/emboj/cdf592
Craig NL (2002) Mobile DNA: an introduction. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. American Society for Microbiology, Washington, D.C., pp 3–11
Crichton JH, Dunican DS, MacLennan M, Meehan RR, Adams IR (2014) Defending the genome from the enemy within: Mechanisms of retrotransposon suppression in the mouse germline. Cell Mol Life Sci. https://doi.org/10.1007/s00018-013-1468-0
Criscione SW, Theodosakis N, Micevic G, Cornish TC, Burns KH, Neretti N, Rodić N (2016) Genome-wide characterization of human L1 antisense promoter-driven transcripts. BMC Genom. https://doi.org/10.1186/s12864-016-2800-5
Cruz-Reyes J, ur-Rehman T, Spice WM, Ackers JP (1995) A novel transcribed repeat element from Entamoeba histolytica. Gene. https://doi.org/10.1016/0378-1119(95)00549-X
Deininger PL, Batzer MA (1999) Alu repeats and human disease. Mol Genet Metab. https://doi.org/10.1006/mgme.1999.2864
Delviks-Frankenberry K, Galli A, Nikolaitchik O, Mens H, Pathak VK, Hu WS (2011) Mechanisms and factors that influence high frequency retroviral recombination. Viruses. https://doi.org/10.3390/v3091650
Denli AM, Narvaiza I, Kerman BE, Pena M, Benner C, Marchetto MCN, Diedrich JK, Aslanian A, Ma J, Moresco JJ, Moore L, Hunter T, Saghatelian A, Gage FH (2015) Primate-specific ORF0 contributes to retrotransposon-mediated diversity. Cell. https://doi.org/10.1016/j.cell.2015.09.025
Derr LK, Strathern JN (1993) A role for reverse transcripts in gene conversion. Nature. https://doi.org/10.1038/361170a0
Dewannieux M, Esnault C, Heidmann T (2003) LINE-mediated retrotransposition of marked Alu sequences. Nature Genet. https://doi.org/10.1038/ng1223
Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, Kopera HC, Athanikar JN, Hasnaoui M, Bucheton A, Moran JV, Gilbert N (2010) Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet. https://doi.org/10.1371/journal.pgen.1001150
Eickbush TH, Malik HS (2014) Origins and evolution of retrotransposons. Mobile DNA II. https://doi.org/10.1128/9781555817954.ch49
Elbarbary RA, Lucas BA, Maquat LE (2016) Retrotransposons as regulators of gene expression. Science. https://doi.org/10.1126/science.aac7247
Faulkner GJ, Carninci P (2009) Altruistic functions for selfish DNA. Cell Cycle. https://doi.org/10.4161/cc.8.18.9536
Feng Q, Moran JV, Kazazian HH, Boeke JD (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell. https://doi.org/10.1016/S0092-8674(00)81997-2
Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet. https://doi.org/10.1016/0168-9525(89)90039-5
Finnegan DJ (1997) Transposable elements: how non-LTR retrotransposons do it. Curr Biol. https://doi.org/10.1016/s0960-9822(06)00112-6
Fisher O, Siman-Tov R, Ankri S (2006) Pleiotropic phenotype in Entamoeba histolytica overexpressing DNA methyltransferase (Ehmeth). Mol Biochem Parasitol. https://doi.org/10.1016/j.molbiopara.2006.01.007
Fraga MF, Esteller M (2002) DNA methylation: a profile of methods and applications. Biotechniques. https://doi.org/10.2144/02333rv01
Garcia-Perez JL, Doucet AJ, Bucheton A, Moran JV, Gilbert N (2007) Distinct mechanisms for trans-mediated mobilization of cellular RNAs by the LINE-1 reverse transcriptase. Genome Res. https://doi.org/10.1101/gr.5870107
Gaurav AK, Kumar J, Agrahari M, Bhattacharya A, Yadav VP, Bhattacharya S (2017) Functionally conserved RNA-binding and protein-protein interaction properties of LINE-ORF1p in an ancient clade of non-LTR retrotransposons of Entamoeba histolytica. Mol Biochem Parasitol. https://doi.org/10.1016/j.molbiopara.2016.11.004
Gogvadze E, Barbisan C, Lebrun MH, Buzdin A (2007) Tripartite chimeric pseudogene from the genome of rice blast fungus Magnaporthe grisea suggests double template jumps during long interspersed nuclear element (LINE) reverse transcription. BMC Genom. https://doi.org/10.1186/1471-2164-8-360
Hackett JA, Reddington JP, Nestor CE, Dunican DS, Branco MR, Reichmann J, Reik W, Surani MA, Adams IR, Meehan RR (2012) Promoter DNA methylation couples genome-defence mechanisms to epigenetic reprogramming in the mouse germline. Development (cambridge). https://doi.org/10.1242/dev.081661
Hancks DC, Kazazian HH (2012) Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22(3):191–203. https://doi.org/10.1016/j.gde.2012.02.006
Hancks DC, Goodier JL, Mandal PK, Cheung LE, Kazazian HH (2011) Retrotransposition of marked SVA elements by human L1s in cultured cells. Hum Mol Genet. https://doi.org/10.1093/hmg/ddr245
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(1):55–63. https://doi.org/10.1016/j.molbiopara.2006.02.005
Heras SR, López MC, Olivares M, Thomas MC (2007) The L1Tc non-LTR retrotransposon of Trypanosoma cruzi contains an internal RNA-pol II-dependent promoter that strongly activates gene transcription and generates unspliced transcripts. Nucleic Acids Res. https://doi.org/10.1093/nar/gkl1137
Hon CC, Weber C, Sismeiro O, Proux C, Koutero M, Deloger M, Das S, Agrahari M, Dillies MA, Jagla B, Coppee JY, Bhattacharya A, Guillen N (2013) Quantification of stochastic noise of splicing and polyadenylation in Entamoeba histolytica. Nucleic Acids Res. https://doi.org/10.1093/nar/gks1271
Huntley DM, Pandis I, Butcher SA, Ackers JP (2010) Bioinformatic analysis of Entamoeba histolytica SINE1 elements. BMC Genom. https://doi.org/10.1186/1471-2164-11-321
Iwasaki YW, Siomi MC, Siomi H (2015) PIWI-interacting RNA: Its biogenesis and functions. Annu Rev Biochem. https://doi.org/10.1146/annurev-biochem-060614-034258
Jamburuthugoda VK, Eickbush TH (2014) Identification of RNA binding motifs in the R2 retrotransposon-encoded reverse transcriptase. Nucleic Acids Res. https://doi.org/10.1093/nar/gku514
Kajikawa M, Okada N (2002) LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell. https://doi.org/10.1016/S0092-8674(02)01041-3
Kaur D, Agrahari M, Singh SS, Mandal PK, Bhattacharya A, Bhattacharya S (2021) Transcriptomic analysis of Entamoeba histolytica reveals domain-specific sense strand expression of LINE-encoded ORFs with massive antisense expression of RT domain. Plasmid. https://doi.org/10.1016/j.plasmid.2021.102560
Kazazian HH Jr (1998) Mobile elements and disease. Curr Opin Genet Dev 8(3):343–350. https://doi.org/10.1016/s0959-437x(98)80092-0
Kazazian HH Jr (2000) Genetics L1. retrotransposons shape the mammalian genome. Science (new York, NY) 289(5482):1152–1153. https://doi.org/10.1126/science.289.5482.1152
Khadgi BB, Govindaraju A, Christensen SM (2019) Completion of LINE integration involves an open ‘4-way’ branched DNA intermediate. Nucleic Acids Res. https://doi.org/10.1093/nar/gkz673
Khazina E, Weichenrieder O (2009) Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.0809964106
Kimmel BE, ole-MoiYoi OK, Young JR (1987) Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol Cell Biol. https://doi.org/10.1128/MCB.7.4.1465
Kolosha VO, Martin SL (1997) In vitro properties of the first ORF protein from mouse LINE-1 support its role in ribonucleoprotein particle formation during retrotransposition. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.94.19.10155
Kolosha VO, Martin SL (2003) High-affinity, non-sequence-specific RNA binding by the open reading frame 1 (ORF1) protein from long interspersed nuclear element 1 (LINE-1). J Biol Chem. https://doi.org/10.1074/jbc.M210487200
Kuduvalli PN, Rao JE, Craig NL (2001) Target DNA structure plays a critical role in Tn7 transposition. EMBO J. https://doi.org/10.1093/emboj/20.4.924
Kulpa DA, Moran JV (2006) Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat Struct Mol Biol. https://doi.org/10.1038/nsmb1107
Kumari V, Sharma R, Yadav VP, Gupta AK, Bhattacharya A, Bhattacharya S (2011) Differential distribution of a SINE element in the Entamoeba histolytica and Entamoeba dispar genomes: role of the LINE-encoded endonuclease. BMC Genom. https://doi.org/10.1186/1471-2164-12-267
Kumari V, Iyer LR, Roy R, Bhargava V, Panda S, Paul J, Verweij JJ, Clark CG, Bhattacharya A, Bhattacharya S (2013) Genomic distribution of SINEs in Entamoeba histolytica strains: implication for genotyping. BMC Genom. https://doi.org/10.1186/1471-2164-14-432
Lev-Maor G, Sorek R, Shomron N, Ast G (2003) The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons. Science. https://doi.org/10.1126/science.1082588
Liao G-C (2000) Insertion site preferences of the P transposable element in Drosophila melanogaster. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.050017397
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, Hall N (2005) The genome of the protist parasite Entamoeba histolytica. Nature. https://doi.org/10.1038/nature03291
Lorenzi H, Thiagarajan M, Haas B, Wortman J, Hall N, Caler E (2008) Genome wide survey, discovery and evolution of repetitive elements in three Entamoeba species. BMC Genom. https://doi.org/10.1186/1471-2164-9-595
Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell. https://doi.org/10.1016/0092-8674(93)90078-5
Macías F, López MC, Thomas MC (2016) The Trypanosomatid Pr77-hallmark contains a downstream core promoter element essential for transcription activity of the Trypanosoma cruzi L1Tc retrotransposon. BMC Genom. https://doi.org/10.1186/s12864-016-2427-6
Macías F, Afonso-Lehmann R, López MC, Gómez I, Thomas MC (2018) Biology of Trypanosoma cruzi retrotransposons: from an enzymatic to a structural point of view. Curr Genom 19(2):110–118. https://doi.org/10.2174/1389202918666170815150738
Mandal PK, Bagchi A, Bhattacharya A, Bhattacharya S (2004) An Entamoeba histolytica line/sine pair inserts at common target sites cleaved by the restriction enzyme-like line-encoded endonuclease. Eukaryot Cell. https://doi.org/10.1128/EC.3.1.170-179.2004
Mandal PK, Rawal K, Ramaswamy R, Bhattacharya A, Bhattacharya S (2006) Identification of insertion hot spots for non-LTR retrotransposons: computational and biochemical application to Entamoeba histolytica. Nucleic Acids Res. https://doi.org/10.1093/nar/gkl710
Martin SL, Bushman FD (2001) Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol. https://doi.org/10.1128/mcb.21.2.467-475.2001
Martin F, Marañón C, Olivares M, Alonso C, López MC (1995) Characterization of a non-long terminal repeat retrotransposon cDNA (L1Tc) from Trypanosoma cruzi: homology of the first ORF with the Ape family of DNA repair enzymes. J Mol Biol. https://doi.org/10.1006/jmbi.1994.0121
Martin SL, Cruceanu M, Branciforte D, Li PWL, Kwok SC, Hodges RS, Williams MC (2005) LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein. J Mol Biol. https://doi.org/10.1016/j.jmb.2005.03.003
Martínez-Calvillo S, Nguyen D, Stuart K, Myler PJ (2004) Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot Cell. https://doi.org/10.1128/EC.3.2.506-517.2004
Matsuda E, Garfinkel DJ (2009) Posttranslational interference of Ty1 retrotransposition by antisense RNAs. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.0908305106
Minakami R, Kurose K, Etoh K, Furuhata Y, Hattori M, Sakaki Y (1992) Identification of an internal cis-element essential for the human li transcription and a nuclear factor(s) binding to the element. Nucleic Acids Res. https://doi.org/10.1093/nar/20.12.3139
Mittal V, Bhattacharya A, Bhattacharya S (1994) Isolation and characterization of a species-specific multicopy DNA sequence from Entamoeba histolytica. Parasitology. https://doi.org/10.1017/S0031182000076071
Mizrokhi LJ, Georgieva SG, Ilyin YV (1988) Jockey, a mobile drosophila element similar to mammalian LINEs, is transcribed from the internal promoter by RNA polymerase II. Cell. https://doi.org/10.1016/S0092-8674(88)80013-8
Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87(5):917–927. https://doi.org/10.1016/s0092-8674(00)81998-4
Nakamura M, Okada N, Kajikawa M (2012) Self-interaction, nucleic acid binding, and nucleic acid chaperone activities are unexpectedly retained in the unique ORF1p of zebrafish LINE. Mol Cell Biol. https://doi.org/10.1128/mcb.06162-11
Okada N, Hamada M (1997) The 3′ ends of tRNA-derived SINEs originated from the 3′ ends of LINEs: a new example from the bovine genome. J Mol Evol. https://doi.org/10.1007/PL00000058
Okada N, Hamada M, Ogiwara I, Ohshima K (1997) SINEs and LINEs share common 3′ sequences: a review. Gene. https://doi.org/10.1016/S0378-1119(97)00409-5
Ostertag EM, Kazazian HH Jr (2001) Biology of mammalian L1 retrotransposons. Annu Rev Genet. https://doi.org/10.1146/annurev.genet.35.102401.091032
Perepelitsa-Belancio V, Deininger P (2003) RNA truncation by premature polyadenylation attenuates human mobile element activity. Nat Genet. https://doi.org/10.1038/ng1269
Pritham EJ, Feschotte C, Wessler SR (2005) Unexpected diversity and differential success of DNA transposons in four species of Entamoeba protozoans. Mol Biol Evolut. https://doi.org/10.1093/molbev/msi169
Raiz J, Damert A, Chira S, Held U, Klawitter S, Hamdorf M, Löwer J, Strätling WH, Löwer R, Schumann GG (2012) The non-autonomous retrotransposon SVA is trans-mobilized by the human LINE-1 protein machinery. Nucleic Acids Res 40(4):1666–1683. https://doi.org/10.1093/nar/gkr863
Ralston KS, Petri WA (2011) The ways of a killer: how does Entamoeba histolytica elicit host cell death? Essays Biochem. https://doi.org/10.1042/BSE0510193
Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. https://doi.org/10.1038/nature05918
Richardson SR, Doucet AJ, Kopera HC, Moldovan JB, Garcia-Perez JL, Moran JV (2015) The influence of LINE-1 and SINE retrotransposons on mammalian genomes. Mobile DNA III. https://doi.org/10.1128/9781555819217.ch51
Sharma R, Bagchi A, Bhattacharya A, Bhattacharya S (2001) Characterization of a retrotransposon-like element from Entamoeba histolytica. Mol Biochem Parasitol. https://doi.org/10.1016/S0166-6851(01)00300-0
Sharma S, Banyal N, Singh M, Mandal AK, Bhattacharya S, Paul J (2017) SINE polymorphism reveals distinct strains of Entamoeba histolytica from North India. Exp Parasitol. https://doi.org/10.1016/j.exppara.2017.01.007
Shire AM, Ackers JP (2007) SINE elements of Entamoeba dispar. Mol Biochem Parasitol. https://doi.org/10.1016/j.molbiopara.2006.11.010
Silberman JD, Clark CG, Diamond LS, Sogin ML (1999) Phylogeny of the genera Entamoeba and Endolimax as deduced from small-subunit ribosomal RNA sequences. Mol Biol Evol 16(12):1740–1751. https://doi.org/10.1093/oxfordjournals.molbev.a026086
Soifer HS, Rossi JJ (2006) Small interfering RNAs to the rescue: blocking L1 retrotransposition. Nat Struct Mol Biol. https://doi.org/10.1038/nsmb0906-758
Speek M (2001) Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol. https://doi.org/10.1128/MCB.21.6.1973-1985.2001
Stenglein MD, Harris RS (2006) APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem. https://doi.org/10.1074/jbc.M602367200
Swergold GD (1990) Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol. https://doi.org/10.1128/MCB.10.12.6718.Updated
Thomas MC, Macias F, Alonso C, López MC (2010) The biology and evolution of transposable elements in parasites. Trends Parasitol. https://doi.org/10.1016/j.pt.2010.04.001
van Dellen K, Field J, Wang Z, Loftus B, Samuelson J (2002) LINEs and SINE-like elements of the protist Entamoeba histolytica. Gene. https://doi.org/10.1016/S0378-1119(02)00917-4
Vázquez M, Ben-Dov C, Lorenzi H, Moore T, Schijman A, Levin MJ (2000) The short interspersed repetitive element of Trypanosoma cruzi, SIRE, is part of VIPER, an unusual retroelement related to long terminal repeat retrotransposons. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.050578397
Villanueva MS, Williams SP, Beard CB, Richards FF, Aksoy S (1991) A new member of a family of site-specific retrotransposons is present in the spliced leader RNA genes of Trypanosoma cruzi. Mol Cell Biol. https://doi.org/10.1128/mcb.11.12.6139
Willhoeft U, Buß H, Tannich E (1999) Analysis of cDNA expressed sequence tags from Entamoeba histolytica: identification of two highly abundant polyadenylated transcripts with no overt open reading frames. Protist. https://doi.org/10.1016/S1434-4610(99)70009-X
Willhoeft U, Buß H, Tannich E (2002) The abundant polyadenylated transcript 2 DNA sequence of the pathogenic protozoan parasite Entamoeba histolytica represents a nonautonomous non-long-terminal-repeat retrotransposon-like element which is absent in the closely related nonpathogenic species Entamoeba dispar. Infect Immunity. https://doi.org/10.1128/IAI.70.12.6798-6804.2002
Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. https://doi.org/10.1002/j.1460-2075.1990.tb07536.x
Yadav VP, Mandal PK, Rao DN, Bhattacharya S (2009) Characterization of the restriction enzyme-like endonuclease encoded by the Entamoeba histolytica non-long terminal repeat retrotransposon EhLINE1. FEBS J. https://doi.org/10.1111/j.1742-4658.2009.07419.x
Yadav VP, Mandal PK, Bhattacharya A, Bhattacharya S (2012) Recombinant SINEs are formed at high frequency during induced retrotransposition in vivo. Nat Commun. https://doi.org/10.1038/ncomms1855
Yang J, Malik HS, Eickbush TH (1999) Identification of the endonuclease domain encoded by R2 and other site-specific, non-long terminal repeat retrotransposable elements. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.96.14.7847
Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. https://doi.org/10.1016/S0168-9525(97)01181-5
Yu F, Zingler N, Schumann G, Strätling WH (2001) Methyl-CpG-binding protein 2 represses LINE-1 expression and retrotransposition but not Alu transcription. Nucleic Acids Res. https://doi.org/10.1093/nar/29.21.4493
Zhang H, Ehrenkaufer GM, Pompey JM, Hackney JA, Singh U (2008) Small RNAs with 5′-polyphosphate termini associate with a piwi-related protein and regulate gene expression in the single-celled eukaryote Entamoeba histolytica. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000219
Zhang H, Alramini H, Tran V, Singh U (2011) Nucleus-localized antisense small RNAs with 5′-polyphosphate termini regulate long term transcriptional gene silencing in Entamoeba histolytica G3 strain. J Biol Chem. https://doi.org/10.1074/jbc.M111.278184
Zhang H, Tran V, Manna D, Ehrenkaufer G, Singh U (2019) Functional characterization of Entamoeba histolytica argonaute proteins reveals a repetitive DR-rich motif region that controls nuclear localization. Msphere. https://doi.org/10.1128/msphere.00580-19
Zhang H, Ehrenkaufer GM, Hall N, Singh U (2020) Identification of oligo-adenylated small RNAs in the parasite Entamoeba and a potential role for small RNA control. BMC Genom. https://doi.org/10.1186/s12864-020-07275-6
Acknowledgements
SB acknowledges financial support from the Indian National Science Academy. Parts of Fig. 1 were reproduced from Lorenzi et al. (2008), published by Springer Nature, under the terms of the creative commons license https://creativecommons.org/licenses/by/2.0.
Author information
Authors and Affiliations
Contributions
DK, MA and SB were involved in drafting the initial manuscript. All authors contributed to the final manuscript, read, and approved the submitted version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Communicated by Martine Collart.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kaur, D., Agrahari, M., Bhattacharya, A. et al. The non-LTR retrotransposons of Entamoeba histolytica: genomic organization and biology. Mol Genet Genomics 297, 1–18 (2022). https://doi.org/10.1007/s00438-021-01843-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-021-01843-5