Skip to main content

Archetypical and Specialized DNA Replication Proteins in Entamoeba histolytica

  • Chapter
  • First Online:
Amebiasis

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Garcia-Diaz M, Bebenek K (2007) Multiple functions of DNA polymerases. CRC Crit Rev Plant Sci 26:105–122

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Bebenek K, Kunkel TA (2004) Functions of DNA polymerases. Adv Protein Chem 69:137–165

    Article  CAS  PubMed  Google Scholar 

  3. Shcherbakova PV, Bebenek K, Kunkel TA (2003) Functions of eukaryotic DNA polymerases. Sci Aging Knowledge Environ 2003:RE3

    Article  PubMed  Google Scholar 

  4. Kornberger A, Baker T (1992) DNA replication. Freeman, New York

    Google Scholar 

  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) 391:251–258

    Article  CAS  Google Scholar 

  6. Beese LS, Derbyshire V, Steitz TA (1993) Structure of DNA polymerase I Klenow fragment bound to duplex DNA. Science 260:352–355

    Article  CAS  PubMed  Google Scholar 

  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 26:3494–3505

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Yamtich J, Sweasy JB (2010) DNA polymerase family X: function, structure, and cellular roles. Biochim Biophys Acta 1804:1136–1150

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Bhattacharya S, Som I, Bhattacharya A (1998) The ribosomal DNA plasmids of Entamoeba. Parasitol Today 14:181–185

    Article  CAS  PubMed  Google Scholar 

  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 8:69–76

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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 31:2035–2044

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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 29:696–701

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J et al (2005) The genome of the protist parasite Entamoeba histolytica. Nature (Lond) 433:865–868

    Article  CAS  Google Scholar 

  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 23:417–422

    CAS  PubMed  Google Scholar 

  15. Tolstrup J, Krause E, Tannich E, Bruchhaus I (2007) Proteomic analysis of Entamoeba histolytica. Parasitology 134:289–298

    Article  CAS  PubMed  Google Scholar 

  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 31:2056–2065

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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 21:2581–2593

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Pellegrini L (2012) The Pol alpha-primase complex. Subcell Biochem 62:157–169

    Article  CAS  PubMed  Google Scholar 

  19. Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PM, Kunkel TA (2008) Division of labor at the eukaryotic replication fork. Mol Cell 30:137–144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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 47:511–522

    Article  CAS  PubMed  Google Scholar 

  21. Fan J, Pavletich NP (2012) Structure and conformational change of a replication protein A heterotrimer bound to ssDNA. Genes Dev 26:2337–2347

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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 273:19747–19755

    Article  CAS  PubMed  Google Scholar 

  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 274:26647–26653

    Article  CAS  PubMed  Google Scholar 

  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 19:1108–1118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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:e716

    Article  PubMed Central  PubMed  Google Scholar 

  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 27:373–384

    Article  CAS  PubMed  Google Scholar 

  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:e786

    Article  PubMed Central  PubMed  Google Scholar 

  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 268:15070–15079

    CAS  PubMed  Google Scholar 

  29. Moldovan GL, Pfander B, Jentsch S (2007) PCNA, the maestro of the replication fork. Cell 129:665–679

    Article  CAS  PubMed  Google Scholar 

  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 67:497–505

    Article  CAS  PubMed  Google Scholar 

  31. Yao NY, O’Donnell M (2012) The RFC clamp loader: structure and function. Subcell Biochem 62:259–279

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Maiorano D, Lutzmann M, Mechali M (2006) MCM proteins and DNA replication. Curr Opin Cell Biol 18:130–136

    Article  CAS  PubMed  Google Scholar 

  33. Liu Y, Richards TA, Aves SJ (2009) Ancient diversification of eukaryotic MCM DNA replication proteins. BMC Evol Biol 9:60

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Das S, Lohia A (2000) MCM proteins of Entamoeba histolytica. Arch Med Res 31:S269–S270

    Article  CAS  PubMed  Google Scholar 

  35. Das S, Mukherjee C, Sinha P, Lohia A (2005) Constitutive association of Mcm2-3-5 proteins with chromatin in Entamoeba histolytica. Cell Microbiol 7:259–267

    Article  CAS  PubMed  Google Scholar 

  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:e40

    Article  PubMed Central  PubMed  Google Scholar 

  37. Oakley GG, Patrick SM (2010) Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci 15:883–900

    Article  CAS  Google Scholar 

  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 174:26–35

    Article  CAS  PubMed  Google Scholar 

  39. Bambara RA, Murante RS, Henricksen LA (1997) Enzymes and reactions at the eukaryotic DNA replication fork. J Biol Chem 272:4647–4650

    Article  CAS  PubMed  Google Scholar 

  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 141:145–153

    Article  CAS  PubMed  Google Scholar 

  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 410:27–38

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Klingbeil MM, Motyka SA, Englund PT (2002) Multiple mitochondrial DNA polymerases in Trypanosoma brucei. Mol Cell 10:175–186

    Article  CAS  PubMed  Google Scholar 

  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 10:734–743

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6:525–530

    Article  PubMed Central  PubMed  Google Scholar 

  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 106:21731–21736

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Kapitonov VV, Jurka J (2006) Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci USA 103:4540–4545

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Yonath A, Bashan A (2004) Ribosomal crystallography: initiation, peptide bond formation, and amino acid polymerization are hampered by antibiotics. Annu Rev Microbiol 58:233–251

    Article  CAS  PubMed  Google Scholar 

  48. Ho MX, Hudson BP, Das K, Arnold E, Ebright RH (2009) Structures of RNA polymerase–antibiotic complexes. Curr Opin Struct Biol 19:715–723

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Bhattacharya S, Bakre A, Bhattacharya A (2002) Mobile genetic elements in protozoan parasites. J Genet 81:73–86

    Article  CAS  PubMed  Google Scholar 

  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 110:207–213

    Article  CAS  PubMed  Google Scholar 

  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:e49964

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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:e58765

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Robinson A, Causer RJ, Dixon NE (2012) Architecture and conservation of the bacterial DNA replication machinery, an underexploited drug target. Curr Drug Targets 13:352–372

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Sanyal G, Doig P (2012) Bacterial DNA replication enzymes as targets for antibacterial drug discovery. Expert Opin Drug Discov 7:327–339

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luis G. Brieba .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Pastor-Palacios, G., López-Ramírez, V., Cardona-Félix, C.S., Liceaga, E.A., Lara-Gonzalez, S., Brieba, L.G. (2015). Archetypical and Specialized DNA Replication Proteins in Entamoeba histolytica . In: Nozaki, T., Bhattacharya, A. (eds) Amebiasis. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55200-0_22

Download citation

Publish with us

Policies and ethics