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Amebiasis pp 393-408 | Cite as

Archetypical and Specialized DNA Replication Proteins in Entamoeba histolytica

  • Guillermo Pastor-Palacios
  • Varinia López-Ramírez
  • Cesar S. Cardona-Félix
  • Elisa Azuara Liceaga
  • Samuel Lara-Gonzalez
  • Luis G. Brieba
Chapter

Abstract

Accurate DNA replication and repair are essential tasks for survival. In eukaryotes, DNA polymerases replicate genomes that can be composed of billions of base pairs. These genomes can be chemically damaged or modified, jeopardizing its integrity, and cells have evolved mechanisms to ameliorate the mutagenic effect of DNA damage. DNA replication and DNA lesion bypass in bacteria, yeast, and humans have been widely studied; however, little is known about these processes in other organisms. Entamoeba histolytica is a parasitic protozoan responsible for amebic dysentery and hepatic abscess. Herein, we define the DNA replication apparatus of Entamoeba histolytica and review the biochemical peculiarities of family A and family B2 DNA polymerases involved in DNA lesion bypass. Our data indicate that E. histolytica is a mosaic of archetypical family B DNA polymerases (α, ε, and δ) present at the replication fork and specialized DNA polymerases with novel lesion bypass properties.

Keywords

Proliferate Cellular Nuclear Antigen Entamoeba Histolytica Abasic Site TPR2 Motif Proliferate Cellular Nuclear Antigen 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Research in the LGB laboratory is supported by CONACYT-grant 128647. We thank the Howard Hughes Medical Institute for support.

References

  1. 1.
    Garcia-Diaz M, Bebenek K (2007) Multiple functions of DNA polymerases. CRC Crit Rev Plant Sci 26:105–122PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Bebenek K, Kunkel TA (2004) Functions of DNA polymerases. Adv Protein Chem 69:137–165PubMedCrossRefGoogle Scholar
  3. 3.
    Shcherbakova PV, Bebenek K, Kunkel TA (2003) Functions of eukaryotic DNA polymerases. Sci Aging Knowledge Environ 2003:RE3PubMedCrossRefGoogle Scholar
  4. 4.
    Kornberger A, Baker T (1992) DNA replication. Freeman, New YorkGoogle Scholar
  5. 5.
    Doublie S, Tabor S, Long AM, Richardson CC, Ellenberger T (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Ǻ resolution. Nature (Lond) 391:251–258CrossRefGoogle Scholar
  6. 6.
    Beese LS, Derbyshire V, Steitz TA (1993) Structure of DNA polymerase I Klenow fragment bound to duplex DNA. Science 260:352–355PubMedCrossRefGoogle Scholar
  7. 7.
    Berman AJ, Kamtekar S, Goodman JL, Lazaro JM, de Vega M et al (2007) Structures of phi29 DNA polymerase complexed with substrate: the mechanism of translocation in B-family polymerases. EMBO J 26:3494–3505PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Yamtich J, Sweasy JB (2010) DNA polymerase family X: function, structure, and cellular roles. Biochim Biophys Acta 1804:1136–1150PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Bhattacharya S, Som I, Bhattacharya A (1998) The ribosomal DNA plasmids of Entamoeba. Parasitol Today 14:181–185PubMedCrossRefGoogle Scholar
  10. 10.
    Panigrahi SK, Jhingan GD, Som I, Bhattacharya A, Petri WA Jr et al (2009) Promoter analysis of palindromic transcription units in the ribosomal DNA circle of Entamoeba histolytica. Eukaryot Cell 8:69–76PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Ghosh S, Satish S, Tyagi S, Bhattacharya A, Bhattacharya S (2003) Differential use of multiple replication origins in the ribosomal DNA episome of the protozoan parasite Entamoeba histolytica. Nucleic Acids Res 31:2035–2044PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Burch DJ, Li E, Reed S, Jackson TF, Stanley SL Jr (1991) Isolation of a strain-specific Entamoeba histolytica cDNA clone. J Clin Microbiol 29:696–701PubMedCentralPubMedGoogle Scholar
  13. 13.
    Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J et al (2005) The genome of the protist parasite Entamoeba histolytica. Nature (Lond) 433:865–868CrossRefGoogle Scholar
  14. 14.
    Makioka A, Ohtomo H, Kobayashi S, Takeuchi T (1998) Effects of aphidicolin on Entamoeba histolytica growth and DNA synthesis. Tokai J Exp Clin Med 23:417–422PubMedGoogle Scholar
  15. 15.
    Tolstrup J, Krause E, Tannich E, Bruchhaus I (2007) Proteomic analysis of Entamoeba histolytica. Parasitology 134:289–298PubMedCrossRefGoogle Scholar
  16. 16.
    Biswas SB, Khopde SM, Zhu Fx F, Biswas EE (2003) Subunit interactions in the assembly of Saccharomyces cerevisiae DNA polymerase alpha. Nucleic Acids Res 31:2056–2065PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Dehde S, Rohaly G, Schub O, Nasheuer HP, Bohn W et al (2001) Two immunologically distinct human DNA polymerase alpha-primase subpopulations are involved in cellular DNA replication. Mol Cell Biol 21:2581–2593PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Pellegrini L (2012) The Pol alpha-primase complex. Subcell Biochem 62:157–169PubMedCrossRefGoogle Scholar
  19. 19.
    Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PM, Kunkel TA (2008) Division of labor at the eukaryotic replication fork. Mol Cell 30:137–144PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Nishimura K, Ishiai M, Horikawa K, Fukagawa T, Takata M et al (2012) Mcm8 and Mcm9 form a complex that functions in homologous recombination repair induced by DNA interstrand crosslinks. Mol Cell 47:511–522PubMedCrossRefGoogle Scholar
  21. 21.
    Fan J, Pavletich NP (2012) Structure and conformational change of a replication protein A heterotrimer bound to ssDNA. Genes Dev 26:2337–2347PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Gerik KJ, Li X, Pautz A, Burgers PM (1998) Characterization of the two small subunits of Saccharomyces cerevisiae DNA polymerase delta. J Biol Chem 273:19747–19755PubMedCrossRefGoogle Scholar
  23. 23.
    Zhang P, Mo JY, Perez A, Leon A, Liu L et al (1999) Direct interaction of proliferating cell nuclear antigen with the p125 catalytic subunit of mammalian DNA polymerase delta. J Biol Chem 274:26647–26653PubMedCrossRefGoogle Scholar
  24. 24.
    Reynolds N, Warbrick E, Fantes PA, MacNeill SA (2000) Essential interaction between the fission yeast DNA polymerase delta subunit Cdc27 and Pcn1 (PCNA) mediated through a C-terminal p21(Cip1)-like PCNA binding motif. EMBO J 19:1108–1118PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Lorenzi HA, Puiu D, Miller JR, Brinkac LM, Amedeo P et al (2010) New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. PLoS Negl Trop Dis 4:e716PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Lohia A, Mukherjee C, Majumder S, Dastidar PG (2007) Genome re-duplication and irregular segregation occur during the cell cycle of Entamoeba histolytica. Biosci Rep 27:373–384PubMedCrossRefGoogle Scholar
  27. 27.
    Pastor-Palacios G, Azuara-Liceaga E, Brieba LG (2010) A nuclear family A DNA polymerase from Entamoeba histolytica bypasses thymine glycol. PLoS Negl Trop Dis 4:e786PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Jessberger R, Podust V, Hubscher U, Berg P (1993) A mammalian protein complex that repairs double-strand breaks and deletions by recombination. J Biol Chem 268:15070–15079PubMedGoogle Scholar
  29. 29.
    Moldovan GL, Pfander B, Jentsch S (2007) PCNA, the maestro of the replication fork. Cell 129:665–679PubMedCrossRefGoogle Scholar
  30. 30.
    Cardona-Felix CS, Lara-Gonzalez S, Brieba LG (2011) Structure and biochemical characterization of proliferating cellular nuclear antigen from a parasitic protozoon. Acta Crystallogr D Biol Crystallogr 67:497–505PubMedCrossRefGoogle Scholar
  31. 31.
    Yao NY, O’Donnell M (2012) The RFC clamp loader: structure and function. Subcell Biochem 62:259–279PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Maiorano D, Lutzmann M, Mechali M (2006) MCM proteins and DNA replication. Curr Opin Cell Biol 18:130–136PubMedCrossRefGoogle Scholar
  33. 33.
    Liu Y, Richards TA, Aves SJ (2009) Ancient diversification of eukaryotic MCM DNA replication proteins. BMC Evol Biol 9:60PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Das S, Lohia A (2000) MCM proteins of Entamoeba histolytica. Arch Med Res 31:S269–S270PubMedCrossRefGoogle Scholar
  35. 35.
    Das S, Mukherjee C, Sinha P, Lohia A (2005) Constitutive association of Mcm2-3-5 proteins with chromatin in Entamoeba histolytica. Cell Microbiol 7:259–267PubMedCrossRefGoogle Scholar
  36. 36.
    Blanton HL, Radford SJ, McMahan S, Kearney HM, Ibrahim JG et al (2005) REC, Drosophila MCM8, drives formation of meiotic crossovers. PLoS Genet 1:e40PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Oakley GG, Patrick SM (2010) Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci 15:883–900CrossRefGoogle Scholar
  38. 38.
    Cardona-Felix CS, Pastor-Palacios G, Cardenas H, Azuara-Liceaga E, Brieba LG (2010) Biochemical characterization of the DNA ligase I from Entamoeba histolytica. Mol Biochem Parasitol 174:26–35PubMedCrossRefGoogle Scholar
  39. 39.
    Bambara RA, Murante RS, Henricksen LA (1997) Enzymes and reactions at the eukaryotic DNA replication fork. J Biol Chem 272:4647–4650PubMedCrossRefGoogle Scholar
  40. 40.
    Seow F, Sato S, Janssen CS, Riehle MO, Mukhopadhyay A et al (2005) The plastidic DNA replication enzyme complex of Plasmodium falciparum. Mol Biochem Parasitol 141:145–153PubMedCrossRefGoogle Scholar
  41. 41.
    Kennedy SR, Chen CY, Schmitt MW, Bower CN, Loeb LA (2011) The biochemistry and fidelity of synthesis by the apicoplast genome replication DNA polymerase Pfprex from the malaria parasite Plasmodium falciparum. J Mol Biol 410:27–38PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Klingbeil MM, Motyka SA, Englund PT (2002) Multiple mitochondrial DNA polymerases in Trypanosoma brucei. Mol Cell 10:175–186PubMedCrossRefGoogle Scholar
  43. 43.
    Bruhn DF, Sammartino MP, Klingbeil MM (2011) Three mitochondrial DNA polymerases are essential for kinetoplast DNA replication and survival of bloodstream from Trypanosoma brucei. Eukaryot Cell 10:734–743PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6:525–530PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Mi-ichi F, Abu Yousuf M, Nakada-Tsukui K, Nozaki T (2009) Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc Natl Acad Sci USA 106:21731–21736PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Kapitonov VV, Jurka J (2006) Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci USA 103:4540–4545PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Yonath A, Bashan A (2004) Ribosomal crystallography: initiation, peptide bond formation, and amino acid polymerization are hampered by antibiotics. Annu Rev Microbiol 58:233–251PubMedCrossRefGoogle Scholar
  48. 48.
    Ho MX, Hudson BP, Das K, Arnold E, Ebright RH (2009) Structures of RNA polymerase–antibiotic complexes. Curr Opin Struct Biol 19:715–723PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Bhattacharya S, Bakre A, Bhattacharya A (2002) Mobile genetic elements in protozoan parasites. J Genet 81:73–86PubMedCrossRefGoogle Scholar
  50. 50.
    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 110:207–213PubMedCrossRefGoogle Scholar
  51. 51.
    Pastor-Palacios G, Lopez-Ramirez V, Cardona-Felix CS, Brieba LG (2012) A transposon-derived DNA polymerase from Entamoeba histolytica displays intrinsic strand displacement, processivity and lesion bypass. PLoS One 7:e49964PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Marceau AH, Bernstein DA, Walsh BW, Shapiro W, Simmons LA et al (2013) Protein interactions in genome maintenance as novel antibacterial targets. PLoS One 8:e58765PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Robinson A, Causer RJ, Dixon NE (2012) Architecture and conservation of the bacterial DNA replication machinery, an underexploited drug target. Curr Drug Targets 13:352–372PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Sanyal G, Doig P (2012) Bacterial DNA replication enzymes as targets for antibacterial drug discovery. Expert Opin Drug Discov 7:327–339PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  • Guillermo Pastor-Palacios
    • 1
  • Varinia López-Ramírez
    • 1
  • Cesar S. Cardona-Félix
    • 1
  • Elisa Azuara Liceaga
    • 2
  • Samuel Lara-Gonzalez
    • 3
  • Luis G. Brieba
    • 1
  1. 1.Laboratorio Nacional de Genómica para la BiodiversidadCentro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalIrapuatoMexico
  2. 2.Universidad Autónoma de la Ciudad de México, Posgrado en Ciencias GenómicasMéxico DFMexico
  3. 3.División de Biología MolecularIPICYT, Camino a la PresaSan Luis PotosíMexico

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