The HU protein is important for apicoplast genome maintenance and inheritance in Toxoplasma gondii

Eukaryotic Cell

Volumn 11, Issue 7, 2012, Pages 905-915

  Reiff, Sarah B ^a   Vaishnava, Shipra ^a,b   Striepena, Boris ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; PROTOZOAL PROTEIN;

ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; PARASITOLOGY; PLASTID; PLASTID GENOME; TOXOPLASMA; TOXOPLASMOSIS;

DNA-BINDING PROTEINS; GENOME, PLASTID; HUMANS; PLASTIDS; PROTOZOAN PROTEINS; TOXOPLASMA; TOXOPLASMOSIS;

BACTERIA (MICROORGANISMS); TOXOPLASMA; TOXOPLASMA GONDII;

EID: 84863332365     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00029-12     Document Type: Article

References (55)

1. Agrawal S, van Dooren GG, Beatty WL, Striepen B. 2009. Genetic evidence that an endosymbiont-derived endoplasmic reticulumassociated protein degradation (ERAD) system functions in import of apicoplast proteins. J. Biol. Chem. 284:33683-33691.
2. Axen R, Porath J, Ernback S. 1967. Chemical coupling of peptides and proteins to polysaccharides by means of cyanogen halides. Nature 214: 1302-1304.
3. Bernhardt TG, de Boer PA. 2005. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18:555-564.
4. Bonnefoy E, Almeida A, Rouviere-Yaniv J. 1989. Lon-dependent regulation of the DNA binding protein HU in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 86:7691-7695.
5. Brooks CF, et al. 2010. The toxoplasma apicoplast phosphate translocator links cytosolic and apicoplast metabolism and is essential for parasite survival. Cell Host Microbe 7:62-73.
6. Cai X, Fuller AL, McDougald LR, Zhu G. 2003. Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39-46.
7. Cho H, McManus HR, Dove SL, Bernhardt TG. 2011. Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc. Natl. Acad. Sci. U. S. A. 108:3773-3778.
8. Dar MA, Sharma A, Mondal N, Dhar SK. 2007. Molecular cloning of apicoplast-targeted Plasmodium falciparum DNA gyrase genes: unique intrinsic ATPase activity and ATP-independent dimerization of PfGyrB subunit. Eukaryot. Cell 6:398-412.
9. Debarry JD, Kissinger JC. 2011. Jumbled genomes: missing apicomplexan synteny. Mol. Biol. Evol. 28:2855-2871.
10. Dixon NE, Kornberg A. 1984. Protein HU in the enzymatic replication of the chromosomal origin of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 81:424-428.
11. Ersfeld K, Gull K. 1997. Partitioning of large and minichromosomes in Trypanosoma brucei. Science 276:611-614.
12. Fichera ME, Roos DS. 1997. A plastid organelle as a drug target in apicomplexan parasites. Nature 390:407-409.
13. Fox BA, Ristuccia JG, Gigley JP, Bzik DJ. 2009. Efficient gene replacements in Toxoplasma gondii strains deficient for nonhomologous end joining. Eukaryot. Cell 8:520-529.
14. Funnell BE. 1988. Participation of Escherichia coli integration host factor in the P1 plasmid partition system. Proc. Natl. Acad. Sci. U. S. A. 85:6657-6661.
15. Grossman N, Rosner E, Ron EZ. 1989. Termination of DNA replication is required for cell division in Escherichia coli. J. Bacteriol. 171:74-79.
16. Gubbels MJ, Li C, Striepen B. 2003. High-throughput growth assay for Toxoplasma gondii using yellow fluorescent protein. Antimicrob. Agents Chemother. 47:309-316.
17. Guo F, Adhya S. 2007. Spiral structure of Escherichia coli HUalphabeta provides foundation for DNA supercoiling. Proc. Natl. Acad. Sci. U. S. A. 104:4309-4314.
18. Huisman O, et al. 1989. Multiple defects in Escherichia coli mutants lacking HU protein. J. Bacteriol. 171:3704-3712.
19. Huynh MH, Carruthers VB. 2009. Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot. Cell 8:530-539.
20. Kar S, et al. 2006. Right-handed DNA supercoiling by an octameric form of histone-like protein HU: modulation of cellular transcription. J. Biol. Chem. 281:40144-40153.
21. Kar S, Edgar R, Adhya S. 2005. Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc. Natl. Acad. Sci. U. S. A. 102:16397-16402.
22. Karcher D, Koster D, Schadach A, Klevesath A, Bock R. 2009. The Chlamydomonas chloroplast HLP protein is required for nucleoid organization and genome maintenance. Mol. Plant 2:1223-1232.
23. Kobayashi T, et al. 2002. Detection and localization of a chloroplastencoded HU-like protein that organizes chloroplast nucleoids. Plant Cell 14:1579-1589.
24. Li S, Waters R. 1998. Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination. J. Bacteriol. 180:3750-3756.
25. Lindner SE, Llinas M, Keck JL, Kappe SH. 2011. The primase domain of PfPrex is a proteolytically matured, essential enzyme of the apicoplast. Mol. Biochem. Parasitol. 180:69-75.
26. Lorestani A, et al. 2010. A Toxoplasma MORN1 null mutant undergoes repeated divisions but is defective in basal assembly, apicoplast division and cytokinesis. PLoS One 5:e12302. doi:10.1371/journal.pone.0012302.
27. Matsuzaki M, Kikuchi T, Kita K, Kojima S, Kuroiwa T. 2001. Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma 218:180-191.
28. Mazumdar J, Wilson EH, Masek K, Hunter CA, Striepen B. 2006. Apicoplast fatty acid synthesis is essential for organelle biogenesis and parasite survival in Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 103:13192-13197.
29. Meissner M, Schluter D, Soldati D. 2002. Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298:837-840.
30. Miyabe I, Zhang QM, Kano Y, Yonei S. 2000. Histone-like protein HU is required for recA gene-dependentDNArepair and SOS induction pathways in UV-irradiated Escherichia coli. Int. J. Radiat Biol. 76:43-49.
31. Miyagishima SY, Kabeya Y. 2010. Chloroplast division: squeezing the photosynthetic captive. Curr. Opin. Microbiol. 13:738-746.
32. Moriyama T, Terasawa K, Fujiwara M, Sato N. 2008. Purification and characterization of organellar DNA polymerases in the red alga Cyanidioschyzon merolae. FEBS J. 275:2899-2918.
33. Mukhopadhyay A, et al. 2009. The Toxoplasma gondii plastid replication and repair enzyme complex, PREX. Parasitology 136:747-755.
34. Nair SC, et al. 2011. Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J. Exp. Med. 208:1547-1559.
35. Pino P, et al. 2007. Dual targeting of antioxidant and metabolic enzymes to the mitochondrion and the apicoplast of Toxoplasma gondii. PLoS Pathog. 3:e115. doi:10.1371/journal.ppat.0030115.
36. Prusty D, et al. 2010. Single-stranded DNA binding protein from human malarial parasite Plasmodium falciparum is encoded in the nucleus and targeted to the apicoplast. Nucleic Acids Res. 38:7037-7053.
37. Raghu Ram EV, et al. 2007. Nuclear gyrB encodes a functional subunit of the Plasmodium falciparum gyrase that is involved in apicoplast DNA replication. Mol. Biochem. Parasitol. 154:30-39.
38. Ram EV, Naik R, Ganguli M, Habib S. 2008. DNA organization by the apicoplast-targeted bacterial histone-like protein of Plasmodium falciparum. Nucleic Acids Res. 36:5061-5073.
39. Ramya TN, Mishra S, Karmodiya K, Surolia N, Surolia A. 2007. Inhibitors of nonhousekeeping functions of the apicoplast defy delayed death in Plasmodium falciparum. Antimicrob. Agents Chemother. 51: 307-316.
40. Roos DS, Donald RG, Morrissette NS, Moulton AL. 1994. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45:27-63.
41. Rouviere-Yaniv J, Yaniv M, Germond JE. 1979. E. coli DNA binding protein HU forms nucleosomelike structure with circular doublestranded DNA. Cell 17:265-274.
42. Ryan VT, Grimwade JE, Nievera CJ, Leonard AC. 2002. IHF and HU stimulate assembly of pre-replication complexes at Escherichia coli oriC by two different mechanisms. Mol. Microbiol. 46:113-124.
43. Seow F, et al. 2005. The plastidic DNA replication enzyme complex of Plasmodium falciparum. Mol. Biochem. Parasitol. 141:145-153.
44. Sheiner L, et al. A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog. 7:e1002392. doi:10.1371/journal.ppat.1002392.
45. Shellman VL, Pettijohn DE. 1991. Introduction of proteins into living bacterial cells: distribution of labeled HU protein in Escherichia coli. J. Bacteriol. 173:3047-3059.
46. Striepen B, et al. 2000. The plastid of Toxoplasma gondii is divided by association with the centrosomes. J. Cell Biol. 151:1423-1434.
47. Striepen B, Soldati D. 2007. Genetic manipulation of Toxoplasma gondii, p 391-415. In Weiss LM, Kim K (ed), Toxoplasma gondii: the model apicomplexan-perspectives and methods. Elsevier, San Diego, CA.
48. Vaishnava S, Striepen B. 2006. The cell biology of secondary endosymbiosis-how parasites build, divide and segregate the apicoplast. Mol. Microbiol. 61:1380-1387.
49. van Dooren GG, et al. 2009. A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii. Curr. Biol. 19:267-276.
50. van Dooren GG, Tomova C, Agrawal S, Humbel BM, Striepen B. 2008. Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc. Natl. Acad. Sci. U. S. A. 105:13574-13579.
51. van Noort J, Verbrugge S, Goosen N, Dekker C, Dame RT. 2004. Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc. Natl. Acad. Sci. U. S. A. 101:6969-6974.
52. Wall MK, Mitchenall LA, Maxwell A. 2004. Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc. Natl. Acad. Sci. U. S. A. 101:7821-7826.
53. Wery M, Woldringh CL, Rouviere-Yaniv J. 2001. HU-GFP and DAPI co-localize on the Escherichia coli nucleoid. Biochimie 83:193-200.
54. Wilson RJ, et al. 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261:155-172.
55. Wu L, Chen SX, Jiang XG, Cao JP. 2009. Toxoplasma gondii: a simple real-time PCR assay to quantify the proliferation of the apicoplast. Exp. Parasitol. 123:384-387.