Trypanosomes Have Six Mitochondrial DNA Helicases with One Controlling Kinetoplast Maxicircle Replication

Molecular Cell

Volumn 35, Issue 4, 2009, Pages 490-501

  Liu, Beiyu ^a   Wang, Jianyang ^a   Yaffe, Nurit ^b   Lindsay, Megan E ^a   Zhao, Zhixing ^a   Zick, Aviad ^b   Shlomai, Joseph ^b   Englund, Paul T ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

DNA; MICROBIO; PROTEINS

Indexed keywords

HELICASE; KINETOPLAST DNA; MITOCHONDRIAL DNA; PROTEINASE;

ARTICLE; GENE CONTROL; GENE OVEREXPRESSION; MITOCHONDRIAL DNA REPLICATION; NONHUMAN; PROTEIN DEGRADATION; RNA INTERFERENCE; SYNTHESIS; TRYPANOSOMA;

ANIMALS; DNA HELICASES; DNA REPLICATION; DNA, KINETOPLAST; DNA, MITOCHONDRIAL; DNA, PROTOZOAN; GENE EXPRESSION REGULATION; MUTATION; PEPTIDE HYDROLASES; PROTOZOAN PROTEINS; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA BRUCEI;

EID: 68949202846     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.07.004     Document Type: Article

References (43)

1. Abu-Elneel K., Robinson D.R., Drew M.E., Englund P.T., and Shlomai J. Intramitochondrial localization of universal minicircle sequence-binding protein, a trypanosomatid protein that binds kinetoplast minicircle replication origins. J. Cell Biol. 153 (2001) 725-734
2. Bessler J.B., Torredagger J.Z., and Zakian V.A. The Pif1p subfamily of helicases: region-specific DNA helicases?. Trends Cell Biol. 11 (2001) 60-65
3. Boulé J.B., and Zakian V.A. Roles of Pif1-like helicases in the maintenance of genomic stability. Nucleic Acids Res. 34 (2006) 4147-4153
4. Boulé J.B., Vega L.R., and Zakian V.A. The yeast Pif1p helicase removes telomerase from telomeric DNA. Nature 438 (2005) 57-61
5. Budd M.E., Reis C.C., Smith S., Myung K., and Campbell J.L. Evidence suggesting that Pif1 helicase functions in DNA replication with the Dna2 helicase/nuclease and DNA polymerase delta. Mol. Cell. Biol. 26 (2006) 2490-2500
6. Carpenter L.R., and Englund P.T. Kinetoplast maxicircle DNA replication in Crithidia fasciculata and Trypanosoma brucei. Mol. Cell. Biol. 15 (1995) 6794-6803
7. Chen J., Englund P.T., and Cozzarelli N.R. Changes in network topology during the replication of kinetoplast DNA. EMBO J. 14 (1995) 6339-6347
8. Downey N., Hines J.C., Sinha K.M., and Ray D.S. Mitochondrial DNA Ligases of Trypanosoma brucei. Eukaryot. Cell 4 (2005) 765-774
9. Drew M.E., and Englund P.T. Intramitochondrial location and dynamics of Crithidia fasciculata kinetoplast minicircle replication intermediates. J. Cell Biol. 153 (2001) 735-744
10. Engel M.L., and Ray D.S. A structure-specific DNA endonuclease is enriched in kinetoplasts purified from Crithidia fasciculata. Nucleic Acids Res. 26 (1998) 4733-4738
11. Ferguson M., Torri A.F., Ward D.C., and Englund P.T. In situ hybridization to the Crithidia fasciculata kinetoplast reveals two antipodal sites involved in kinetoplast DNA replication. Cell 70 (1992) 621-629
12. Foury F., and Kolodynski J. pif mutation blocks recombination between mitochondrial rho+ and rho- genomes having tandemly arrayed repeat units in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 80 (1983) 5345-5349
13. Grams J., Morris J.C., Drew M.E., Wang Z., Englund P.T., and Hajduk S.L. A trypanosome mitochondrial RNA polymerase is required for transcription and replication. J. Biol. Chem. 277 (2002) 16952-16959
14. Hajduk S.L., Klein V.A., and Englund P.T. Replication of kinetoplast DNA maxicircles. Cell 36 (1984) 483-492
15. Hall M.C., and Matson S.W. Helicase motifs: the engine that powers DNA unwinding. Mol. Microbiol. 34 (1999) 867-877
16. Hoeijmakers J.H.J., and Weijers P.J. The segregation of kinetoplast DNA networks in Trypanosoma brucei. Plasmid 4 (1980) 97-116
17. Ivessa A.S., Zhou J.Q., and Zakian V.A. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100 (2000) 479-489
18. Jensen B.C., Kifer C.T., Brekken D.L., Randall A.C., Wang Q., Drees B.L., and Parsons M. Characterization of protein kinase CK2 from Trypanosoma brucei. Mol. Biochem. Parasitol. 151 (2007) 28-40
19. Kaguni L.S. DNA polymerase gamma, the mitochondrial replicase. Annu. Rev. Biochem. 73 (2004) 293-320
20. Klingbeil M.M., Motyka S.A., and Englund P.T. Multiple mitochondrial DNA polymerases in Trypanosoma brucei. Mol. Cell 10 (2002) 175-186
21. Lahaye A., Stahl H., Thines-Sempoux D., and Foury F. PIF1: a DNA helicase in yeast mitochondria. EMBO J. 10 (1991) 997-1007
22. Lai D.H., Hashimi H., Lun Z.R., Ayala F.J., and Lukes J. Adaptations of Trypanosoma brucei to gradual loss of kinetoplast DNA: Trypanosoma equiperdum and Trypanosoma evansi are petite mutants of T. brucei. Proc. Natl. Acad. Sci. USA 105 (2008) 1999-2004
23. Li C., and Englund P.T. A mitochondrial DNA primase from the trypanosomatid Crithidia fasciculata. J. Biol. Chem. 272 (1997) 20787-20792
24. Li Z., Lindsay M.E., Motyka S.A., Englund P.T., and Wang C.C. Identification of a bacterial-like HslVU protease in the mitochondria of Trypanosoma brucei and its role in mitochondrial DNA replication. PLoS Pathog. 4 (2008) e1000048
25. Liu B., Liu Y., Motyka S.A., Agbo E.E., and Englund P.T. Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol. 21 (2005) 363-369
26. Liu B., Molina H., Kalume D., Pandey A., Griffith J.D., and Englund P.T. Role of p38 in replication of Trypanosoma brucei kinetoplast DNA. Mol. Cell. Biol. 26 (2006) 5382-5393
27. Liu Y., Motyka S.A., and Englund P.T. Effects of RNA interference of Trypanosoma brucei structure-specific endonuclease-I on kinetoplast DNA replication. J. Biol. Chem. 280 (2005) 35513-35520
28. McCaffery J.M., and Gillin F.D. Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp. Parasitol. 79 (1994) 220-235
29. Melendy T., Sheline C., and Ray D.S. Localization of a type II DNA topoisomerase to two sites at the periphery of the kinetoplast DNA of Crithidia fasciculata. Cell 55 (1988) 1083-1088
30. Myler P.J., Glick D., Feagin J.E., Morales T.H., and Stuart K.D. Structural organization of the maxicircle variable region of Trypanosoma brucei: identification of potential replication origins and topoisomerase II binding sites. Nucleic Acids Res. 21 (1993) 687-694
31. Ogbadoyi E.O., Robinson D.R., and Gull K. A high-order trans-membrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol. Biol. Cell 14 (2003) 1769-1779
32. Pérez-Morga D.L., and Englund P.T. Microtechnique for electron microscopy of DNA. Nucleic Acids Res. 21 (1993) 1328-1329
33. Saxowsky T.T., Choudhary G., Klingbeil M.M., and Englund P.T. Trypanosoma brucei has two distinct mitochondrial DNA polymerase beta enzymes. J. Biol. Chem. 278 (2003) 49095-49101
34. Scocca J.R., and Shapiro T.A. A mitochondrial topoisomerase IA essential for late theta structure resolution in African trypanosomes. Mol. Microbiol. 67 (2008) 820-829
35. Shapiro T.A. Kinetoplast DNA maxicircles: Networks within networks. Proc. Natl. Acad. Sci. USA 90 (1993) 7809-7813
36. Shlomai J. The structure and replication of kinetoplast DNA. Curr. Mol. Med. 4 (2004) 623-647
37. Simpson L., Sbicego S., and Aphasizhev R. Uridine insertion/deletion RNA editing in trypanosome mitochondria: a complex business. RNA 9 (2003) 265-276
38. Stuart K.D., Schnaufer A., Ernst N.L., and Panigrahi A.K. Complex management: RNA editing in trypanosomes. Trends Biochem. Sci. 30 (2005) 97-105
39. Torri A.F., and Englund P.T. Purification of a mitochondrial DNA polymerase from Crithidia fasciculata. J. Biol. Chem. 267 (1992) 4786-4792
40. Wang Z., and Englund P.T. RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J. 20 (2001) 4674-4683
41. Wang Z., Morris J.C., Drew M.E., and Englund P.T. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275 (2000) 40174-40179
42. Woodward R., and Gull K. Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J. Cell Sci. 95 (1990) 49-57
43. Zhou J., Monson E.K., Teng S.C., Schulz V.P., and Zakian V.A. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 289 (2000) 771-774