17
Views
27
CrossRef citations to date
0
Altmetric
Article

A Mitochondrial DNA Primase Is Essential for Cell Growth and Kinetoplast DNA Replication in Trypanosoma brucei

&
Pages 1319-1328 | Received 11 Sep 2009, Accepted 30 Dec 2009, Published online: 20 Mar 2023

REFERENCES

  • Abu-Elneel, K., D. R. Robinson, M. E. Drew, P. T. Englund, and J. Shlomai. 2001. Intramitochondrial localization of universal minicircle sequence-binding protein, a trypanosomatid protein that binds kinetoplast minicircle replication origins. J. Cell Biol. 153:725–734.
  • Avrahami, D., Y. Tzfati, and J. Shlomai. 1995. A single-stranded DNA binding protein binds the origin of replication of the duplex kinetoplast DNA. Proc. Natl. Acad. Sci. U. S. A. 92:10511–10515.
  • Bakshi, R. P., and T. A. Shapiro. 2004. RNA interference of Trypanosoma brucei topoisomerase IB: both subunits are essential. Mol. Biochem. Parasitol. 136:249–255.
  • Birkenmeyer, L., H. Sugisaki, and D. S. Ray. 1987. Structural characterization of site-specific discontinuities associated with replication origins of minicircle DNA from Crithidia fasciculata. J. Biol. Chem. 262:2384–2392.
  • Carpenter, L. R., and P. T. Englund. 1995. Kinetoplast maxicircle DNA replication in Crithidia fasciculata and Trypanosoma brucei. Mol. Cell. Biol. 15:6794–6803.
  • Chandler, J., A. V. Vandoros, B. Mozeleski, and M. M. Klingbeil. 2008. Stem-loop silencing reveals that a third mitochondrial DNA polymerase, POLID, is required for kinetoplast DNA replication in trypanosomes. Eukaryot. Cell 7:2141–2146.
  • Chen, J., C. A. Rauch, J. H. White, P. T. Englund, and N. R. Cozzarelli. 1995. The topology of the kinetoplast DNA network. Cell 80:61–69.
  • Chowdhury, A. R., Z. Zhao, and P. T. Englund. 2008. Effect of hydroxyurea on procyclic Trypanosoma brucei: an unconventional mechanism for achieving synchronous growth. Eukaryot. Cell 7:425–428.
  • Claros, M. G., and P. Vincens. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241:779–786.
  • Conaway, R. C., and I. R. Lehman. 1982. A DNA primase activity associated with DNA polymerase alpha from Drosophila melanogaster embryos. Proc. Natl. Acad. Sci. U. S. A. 79:2523–2527.
  • Cunningham, I. 1977. New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. J. Protozool. 24:325–329.
  • Downey, N., J. C. Hines, K. M. Sinha, and D. S. Ray. 2005. Mitochondrial DNA ligases of Trypanosoma brucei. Eukaryot. Cell 4:765–774.
  • Drew, M. E., and P. T. Englund. 2001. Intramitochondrial location and dynamics of Crithidia fasciculata kinetoplast minicircle replication intermediates. J. Cell Biol. 153:735–744.
  • Engel, M., and D. S. Ray. 1998. A structure-specific DNA endonuclease is enriched in kinetoplasts from Crithidia fasciculata. Nucleic Acids Res. 26:4733–4738.
  • Engel, M. L., J. C. Hines, and D. S. Ray. 2001. The Crithidia fasciculata RNH1 gene encodes both nuclear and mitochondrial isoforms of RNase H. Nucleic Acids Res. 29:725–731.
  • Engel, M. L., and D. S. Ray. 1999. The kinetoplast structure-specific endonuclease I is related to the 5′ exo/endonuclease domain of bacterial DNA polymerase I and colocalizes with the kinetoplast topoisomerase II and DNA polymerase beta during replication. Proc. Natl. Acad. Sci. U. S. A. 96:8455–8460.
  • Englund, P. T. 1979. Free minicircles of kinetoplast DNA networks in Crithidia fasciculata. J. Biol. Chem. 254:4895–4900.
  • Grams, J., J. C. Morris, M. E. Drew, Z. Wang, P. T. Englund, and S. L. Hajduk. 2002. A trypanosome mitochondrial RNA polymerase is required for transcription and replication. J. Biol. Chem. 277:16952–16959.
  • Hines, J. C., M. L. Engel, H. Zhao, and D. S. Ray. 2001. RNA primer removal and gap filling on a model minicircle replication intermediate. Mol. Biochem. Parasitol. 115:63–67.
  • Hines, J. C., and D. S. Ray. 1997. Tandem arrangement of two genes encoding kinetoplast-associated H1 histone-like proteins. Mol. Biochem. Parasitol. 89:41–49.
  • Hines, J. C., and D. S. Ray. 1998. The Crithidia fasciculata KAP1 gene encodes a highly basic protein associated with kinetoplast DNA. Mol. Biochem. Parasitol. 94:41–52.
  • Iyer, L. M., E. V. Koonin, and D. D. Leipe. 2005. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res. 33:3875–3896.
  • Klingbeil, M. M., S. A. Motyka, and P. T. Englund. 2002. Multiple mitochondrial DNA polymerases in Trypanosoma brucei. Mol. Cell 10:175–186.
  • Kornberg, A. 1988. DNA replication. J. Biol. Chem. 263:1–4.
  • Li, C. J., and P. T. Englund. 1997. A mitochondrial DNA primase from the trypanosomatid Crithidia fasciculata. J. Biol. Chem. 272:20787–20792.
  • Li, Y., Y. Sun, J. C. Hines, and D. S. Ray. 2007. Identification of new kinetoplast DNA replication proteins in trypanosomatids based on predicted S-phase expression and mitochondrial targeting. Eukaryot. Cell 6:2303–2310.
  • Liu, B., Y. Liu, S. A. Motyka, E. E. Agbo, and P. T. Englund. 2005. Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol. 21:363–369.
  • Liu, B., H. Molina, D. Kalume, A. Pandey, J. D. Griffith, and P. T. Englund. 2006. The role of p38 in replication of Trypanosoma brucei kinetoplast DNA. Mol. Cell. Biol. 26:5382–5393.
  • Liu, B., J. Wang, N. Yaffe, M. E. Lindsay, Z. Zhao, A. Zick, J. Shlomai, and P. T. Englund. 2009. Trypanosomes have six mitochondrial DNA helicases with one controlling kinetoplast maxicircle DNA replication. Mol. Cell 35:490–501.
  • Lukes, J., D. L. Guilbride, J. Votypka, A. Zikova, R. Benne, and P. T. Englund. 2002. Kinetoplast DNA network: evolution of an improbable structure. Eukaryot. Cell 1:495–502.
  • Lukes, J., H. Hashimi, and A. Zikova. 2005. Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr. Genet 48:277–299.
  • Lukes, J., J. C. Hines, C. J. Evans, N. K. Avliyakulov, V. P. Prabhu, J. Chen, and D. S. Ray. 2001. Disruption of the Crithidia fasciculata KAP1 gene results in structural rearrangement of the kinetoplast disc. Mol. Biochem. Parasitol. 117:179–186.
  • Mahmood, R., J. C. Hines, and D. S. Ray. 1999. Identification of cis and trans elements involved in the cell cycle regulation of multiple genes in Crithidia fasciculata. Mol. Cell. Biol. 19:6174–6182.
  • Mahmood, R., B. Mittra, J. C. Hines, and D. S. Ray. 2001. Characterization of the Crithidia fasciculata mRNA cycling sequence binding proteins. Mol. Cell. Biol. 21:4453–4459.
  • Melendy, T., C. Sheline, and D. S. Ray. 1988. Localization of a type II DNA topoisomerase to two sites at the periphery of the kinetoplast DNA of Crithidia fasciculata. Cell 55:1083–1088.
  • Mittra, B., and D. S. Ray. 2004. Presence of a poly(A) binding protein and two proteins with cell cycle-dependent phosphorylation in Crithidia fasciculata mRNA cycling sequence binding protein II. Eukaryot. Cell 3:1185–1197.
  • Mittra, B., K. M. Sinha, J. C. Hines, and D. S. Ray. 2003. Presence of multiple mRNA cycling sequence element-binding proteins in Crithidia fasciculata. J. Biol. Chem. 278:26564–26571.
  • Ntambi, J. M., and P. T. Englund. 1985. A gap at a unique location in newly replicated kinetoplast DNA minicircles from Trypanosoma equiperdum. J. Biol. Chem. 260:5574–5579.
  • Ntambi, J. M., T. A. Shapiro, K. A. Ryan, and P. T. Englund. 1986. Ribonucleotides associated with a gap in newly replicated kinetoplast DNA minicircles from Trypanosoma equiperdum. J. Biol. Chem. 261:11890–11895.
  • Onn, I., I. Kapeller, K. Abu-Elneel, and J. Shlomai. 2006. Binding of the universal minicircle sequence binding protein at the kinetoplast DNA replication origin. J. Biol. Chem. 281:37468–37476.
  • Onn, I., N. Milman-Shtepel, and J. Shlomai. 2004. Redox potential regulates binding of universal minicircle sequence binding protein at the kinetoplast DNA replication origin. Eukaryot. Cell 3:277–287.
  • Pasion, S. G., J. C. Hines, X. Ou, R. Mahmood, and D. S. Ray. 1996. Sequences within the 5′ untranslated region regulate the levels of a kinetoplast DNA topoisomerase mRNA during the cell cycle. Mol. Cell. Biol. 16:6724–6735.
  • Ray, D. S. 1989. Conserved sequence blocks in kinetoplast minicircles from diverse species of trypanosomes. Mol. Cell. Biol. 9:1365–1367.
  • Ryan, K. A., and P. T. Englund. 1989. Replication of kinetoplast DNA in Trypanosoma equiperdum. Minicircle H strand fragments which map at specific locations. J. Biol. Chem. 264:823–830.
  • Ryan, K. A., and P. T. Englund. 1989. Synthesis and processing of kinetoplast DNA minicircles in Trypanosoma equiperdum. Mol. Cell. Biol. 9:3212–3217.
  • Saxowsky, T. T., G. Choudhary, M. M. Klingbeil, and P. T. Englund. 2003. Trypanosoma brucei has two distinct mitochondrial DNA polymerase beta enzymes. J. Biol. Chem. 278:49095–49101.
  • Schimanski, B., T. N. Nguyen, and A. Gunzl. 2005. Highly efficient tandem affinity purification of trypanosome protein complexes based on a novel epitope combination. Eukaryot. Cell 4:1942–1950.
  • Scocca, J. R., and T. A. Shapiro. 2008. A mitochondrial topoisomerase IA essential for late theta structure resolution in African trypanosomes. Mol. Microbiol. 67:820–829.
  • Sheline, C., and D. S. Ray. 1989. Specific discontinuities in Leishmania tarentolae minicircles map within universally conserved sequence blocks. Mol. Biochem. Parasitol. 37:151–157.
  • Shlomai, J. 2002. Specific recognition of the replication origins of the kinetoplast DNA. Acta Microbiol. Immunol. Hung. 49:455–467.
  • Shlomai, J. 2004. The structure and replication of kinetoplast DNA. Curr. Mol. Med. 4:623–647.
  • Sinha, K. M., J. C. Hines, N. Downey, and D. S. Ray. 2004. Mitochondrial DNA ligase in Crithidia fasciculata. Proc. Natl. Acad. Sci. U. S. A. 101:4361–4366.
  • Sinha, K. M., J. C. Hines, and D. S. Ray. 2006. Cell cycle-dependent localization and properties of a second mitochondrial DNA ligase in Crithidia fasciculata. Eukaryot. Cell 5:54–61.
  • Sogin, M. L., and J. D. Silberman. 1998. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int. J. Parasitol. 28:11–20.
  • Stuart, K. D., A. Schnaufer, N. L. Ernst, and A. K. Panigrahi. 2005. Complex management: RNA editing in trypanosomes. Trends Biochem. Sci. 30:97–105.
  • Tsurumi, T., and I. R. Lehman. 1990. Release of RNA polymerase from Vero cell mitochondria after herpes simplex virus type 1 infection. J. Virol. 64:450–452.
  • Wang, C. C. 1995. Molecular mechanisms and therapeutic approaches to the treatment of African trypanosomiasis. Annu. Rev. Pharmacol. Toxicol. 35:93–127.
  • Wang, Z., and P. T. Englund. 2001. RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J. 20:4674–4683.
  • Wang, Z., J. C. Morris, M. E. Drew, and P. T. Englund. 2000. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275:40174–40179.
  • Wanrooij, S., J. M. Fuste, G. Farge, Y. Shi, C. M. Gustafsson, and M. Falkenberg. 2008. Human mitochondrial RNA polymerase primes lagging-strand DNA synthesis in vitro. Proc. Natl. Acad. Sci. U. S. A. 105:11122–11127.
  • Wirtz, E., S. Leal, C. Ochatt, and G. A. Cross. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89–101.
  • Xu, C. W., J. C. Hines, M. L. Engel, D. G. Russell, and D. S. Ray. 1996. Nucleus-encoded histone H1-like proteins are associated with kinetoplast DNA in the trypanosomatid Crithidia fasciculata. Mol. Cell. Biol. 16:564–576.
  • Zhao, Z., M. E. Lindsay, A. Roy Chowdhury, D. R. Robinson, and P. T. Englund. 2008. p166, a link between the trypanosome mitochondrial DNA and flagellum, mediates genome segregation. EMBO J. 27:143–154.
  • Zick, A., I. Onn, R. Bezalel, H. Margalit, and J. Shlomai. 2005. Assigning functions to genes: identification of S-phase expressed genes in Leishmania major based on post-transcriptional control elements. Nucleic Acids Res. 33:4235–4242.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.