A nucleolar AAA-NTPase is required for parasite division

Molecular Microbiology

Volumn 90, Issue 2, 2013, Pages 338-355

  Suvorova, Elena S ^a   Radke, Joshua B ^a   Ting, Li Min ^c   Vinayak, Sumiti ^b   Alvarez, Carmelo A ^a   Kratzer, Stella ^a   Kim, Kami ^c   Striepen, Boris ^b   White, Michael W ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AAA ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE; CHAPERONE; CYSTEINE; MICROORGANISM PROTEIN; NUCLEOLUS ASSOCIATED PROTEIN 1; PROTEIN R2TP; RNA 28S; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; TYROSINE; UNCLASSIFIED DRUG;

AAA ATPASE GENE; AMINO ACID SUBSTITUTION; ARTICLE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENOME ANALYSIS; GENOMIC INSTABILITY; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOLUS; NUCLEOLUS ASSOCIATED PROTEIN 1 GENE; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA PROCESSING; TEMPERATURE MEASUREMENT; TEMPERATURE SENSITIVITY; TOXOPLASMA GONDII;

APICOMPLEXA; EUKARYOTA;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SUBSTITUTION; CELL CYCLE PROTEINS; CELL DIVISION; CELL NUCLEOLUS; CYSTEINE; EVOLUTION, MOLECULAR; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION TEST; HOT TEMPERATURE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHYLOGENY; PROTOZOAN PROTEINS; RIBOSOMES; RNA, RIBOSOMAL, 28S; TOXOPLASMA; TYROSINE;

EID: 84885383079     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12367     Document Type: Article

References (60)

1. Agrawal, S., van Dooren, G.G., Beatty, W.L., and Striepen, B. (2009) Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins. J Biol Chem 284: 33683-33691.
2. Bahler, J. (2005) Cell-cycle control of gene expression in budding and fission yeast. Annu Rev Genet 39: 69-94.
3. Behnke, M.S., Wootton, J.C., Lehmann, M.M., Radke, J.B., Lucas, O., Nawas, J., etal. (2010) Coordinated progression through two subtranscriptomes underlies the tachyzoite cycle of Toxoplasma gondii. PLoS ONE 5: e12354.
4. Bernstein, K.A., Bleichert, F., Bean, J.M., Cross, F.R., and Baserga, S.J. (2007) Ribosome biogenesis is sensed at the Start cell cycle checkpoint. Mol Biol Cell 18: 953-964.
5. Boisvert, F.M., van Koningsbruggen, S., Navascues, J., and Lamond, A.I. (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8: 574-585.
6. Boulon, S., Marmier-Gourrier, N., Pradet-Balade, B., Wurth, L., Verheggen, C., Jady, B.E., etal. (2008) The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 180: 579-595.
7. Bozdech, Z., Llinas, M., Pulliam, B.L., Wong, E.D., Zhu, J., and DeRisi, J.L. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5.
8. Briggs, L.C., Baldwin, G.S., Miyata, N., Kondo, H., Zhang, X., and Freemont, P.S. (2008) Analysis of nucleotide binding to P97 reveals the properties of a tandem AAA hexameric ATPase. J Biol Chem 283: 13745-13752.
9. Conde de Felipe, M.M., Lehmann, M.M., Jerome, M.E., and White, M.W. (2008) Inhibition of Toxoplasma gondii growth by pyrrolidine dithiocarbamate is cell cycle specific and leads to population synchronization. Mol Biochem Parasitol 157: 22-31.
10. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., etal. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
11. Dereeper, A., Audic, S., Claverie, J.M., and Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10: 8.
12. Duderstadt, K.E., and Berger, J.M. (2008) AAA+ ATPases in the initiation of DNA replication. Crit Rev Biochem Mol Biol 43: 163-187.
13. Fujiwara, Y., Fujiwara, K., Goda, N., Iwaya, N., Tenno, T., Shirakawa, M., and Hiroaki, H. (2011) Structure and function of the N-terminal nucleolin binding domain of nuclear valosin-containing protein-like 2 (NVL2) harboring a nucleolar localization signal. J Biol Chem 286: 21732-21741.
14. Gadal, O., Strauss, D., Braspenning, J., Hoepfner, D., Petfalski, E., Philippsen, P., etal. (2001) A nuclear AAA-type ATPase (Rix7p) is required for biogenesis and nuclear export of 60S ribosomal subunits. EMBO J 20: 3695-3704.
15. Gagnon, K.T., Zhang, X., Qu, G., Biswas, S., Suryadi, J., Brown, B.A., 2nd, and Maxwell, E.S. (2010) Signature amino acids enable the archaeal L7Ae box C/D RNP core protein to recognize and bind the K-loop RNA motif. RNA 16: 79-90.
16. Gaji, R.Y., Behnke, M.S., Lehmann, M.M., White, M.W., and Carruthers, V.B. (2011) Cell cycle-dependent, intercellular transmission of Toxoplasma gondii is accompanied by marked changes in parasite gene expression. Mol Microbiol 79: 192-204.
17. Gubbels, M.J., Vaishnava, S., Boot, N., Dubremetz, J.F., and Striepen, B. (2006) A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J Cell Sci 119: 2236-2245.
18. Gubbels, M.J., Lehmann, M., Muthalagi, M., Jerome, M.E., Brooks, C.F., Szatanek, T., etal. (2008a) Forward genetic analysis of the apicomplexan cell division cycle in Toxoplasma gondii. PLoS Pathog 4: e36.
19. Gubbels, M.J., White, M., and Szatanek, T. (2008b) The cell cycle and Toxoplasma gondii cell division: tightly knit or loosely stitched? Int J Parasitol 38: 1343-1358.
20. Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K., and Elledge, S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816.
21. Her, J., and Chung, I.K. (2012) The AAA-ATPase NVL2 is a telomerase component essential for holoenzyme assembly. Biochem Biophys Res Commun 417: 1086-1092.
22. Hernandez-Verdun, D. (2011) Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2: 189-194.
23. Holzel, M., Rohrmoser, M., Schlee, M., Grimm, T., Harasim, T., Malamoussi, A., etal. (2005) Mammalian WDR12 is a novel member of the Pes1-Bop1 complex and is required for ribosome biogenesis and cell proliferation. J Cell Biol 170: 367-378.
24. Holzel, M., Burger, K., Muhl, B., Orban, M., Kellner, M., and Eick, D. (2010) The tumor suppressor p53 connects ribosome biogenesis to cell cycle control: a double-edged sword. Oncotarget 1: 43-47.
25. Huen, J., Kakihara, Y., Ugwu, F., Cheung, K.L., Ortega, J., and Houry, W.A. (2010) Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes. Biochem Cell Biol 88: 29-40.
26. Hutson, S.L., Mui, E., Kinsley, K., Witola, W.H., Behnke, M.S., El Bissati, K., etal. (2010) T. gondii RP promoters & knockdown reveal molecular pathways associated with proliferation and cell-cycle arrest. PLoS ONE 5: e14057.
27. Huynh, M.H., and Carruthers, V.B. (2009) Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell 8: 530-539.
28. Kakihara, Y., and Houry, W.A. (2012) The R2TP complex: discovery and functions. Biochim Biophys Acta 1823: 101-107.
29. Kimura, M., Stone, R.C., Hunt, S.C., Skurnick, J., Lu, X., Cao, X., etal. (2010) Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat Protoc 5: 1596-1607.
30. Krastev, D.B., and Buchholz, F. (2011) Ribosome biogenesis and p53: who is regulating whom? Cell Cycle 10: 3417-3418.
31. Kressler, D., Roser, D., Pertschy, B., and Hurt, E. (2008) The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J Cell Biol 181: 935-944.
32. Kressler, D., Hurt, E., Bergler, H., and Bassler, J. (2012) The power of AAA-ATPases on the road of pre-60S ribosome maturation - molecular machines that strip pre-ribosomal particles. Biochim Biophys Acta 1823: 92-100.
33. Liu, C., Schroeder, A.A., Kapur, V., and Abrahamsen, M.S. (1998) Telomeric sequences of Cryptosporidium parvum. Mol Biochem Parasitol 94: 291-296.
34. McKeegan, K.S., Debieux, C.M., and Watkins, N.J. (2009) Evidence that the AAA+ proteins TIP48 and TIP49 bridge interactions between 15.5K and the related NOP56 and NOP58 proteins during box C/D snoRNP biogenesis. Mol Cell Biol 29: 4971-4981.
35. Nagahama, M., Hara, Y., Seki, A., Yamazoe, T., Kawate, Y., Shinohara, T., etal. (2004) NVL2 is a nucleolar AAA-ATPase that interacts with ribosomal protein L5 through its nucleolar localization sequence. Mol Biol Cell 15: 5712-5723.
36. Nagahama, M., Yamazoe, T., Hara, Y., Tani, K., Tsuji, A., and Tagaya, M. (2006) The AAA-ATPase NVL2 is a component of pre-ribosomal particles that interacts with the DExD/H-box RNA helicase DOB1. Biochem Biophys Res Commun 346: 1075-1082.
37. Nasmyth, K. (2001) A prize for proliferation. Cell 107: 689-701.
38. Niwa, H., Ewens, C.A., Tsang, C., Yeung, H.O., Zhang, X., and Freemont, P.S. (2012) The role of the N-domain in the ATPase activity of the mammalian AAA ATPase p97/VCP. J Biol Chem 287: 8561-8570.
39. Olguin-Lamas, A., Madec, E., Hovasse, A., Werkmeister, E., Callebaut, I., Slomianny, C., etal. (2011) A novel Toxoplasma gondii nuclear factor TgNF3 is a dynamic chromatin-associated component, modulator of nucleolar architecture and parasite virulence. PLoS Pathog 7: e1001328.
40. Pestov, D.G., Strezoska, Z., and Lau, L.F. (2001) Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: effects of nucleolar protein Bop1 on G(1)/S transition. Mol Cell Biol 21: 4246-4255.
41. Petter, M., Lee, C.C., Byrne, T.J., Boysen, K.E., Volz, J., Ralph, S.A., etal. (2011) Expression of P. falciparum var genes involves exchange of the histone variant H2A.Z at the promoter. PLoS Pathog 7: e1001292.
42. Qu, Z., Weiss, J.N., and MacLellan, W.R. (2003) Regulation of the mammalian cell cycle: a model of the G1-to-S transition. Am J Physiol Cell Physiol 284: C349-C364.
43. Radke, J.R., Striepen, B., Guerini, M.N., Jerome, M.E., Roos, D.S., and White, M.W. (2001) Defining the cell cycle for the tachyzoite stage of Toxoplasma gondii. Mol Biochem Parasitol 115: 165-175.
44. Reilly Ayala, H.B., Wacker, M.A., Siwo, G., and Ferdig, M.T. (2010) Quantitative trait loci mapping reveals candidate pathways regulating cell cycle duration in Plasmodium falciparum. BMC Genomics 11: 577.
45. Reimer, G., Pollard, K.M., Penning, C.A., Ochs, R.L., Lischwe, M.A., Busch, H., and Tan, E.M. (1987) Monoclonal autoantibody from a (New Zealand black x New Zealand white)F1 mouse and some human scleroderma sera target an Mr 34, 000 nucleolar protein of the U3 RNP particle. Arthritis Rheum 30: 793-800.
46. Roos, D.S., Donald, R.G., Morrissette, N.S., and Moulton, A.L. (1994) Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45: 27-63.
47. Rouiller, I., DeLaBarre, B., May, A.P., Weis, W.I., Brunger, A.T., Milligan, R.A., and Wilson-Kubalek, E.M. (2002) Conformational changes of the multifunction p97 AAA ATPase during its ATPase cycle. Nat Struct Biol 9: 950-957.
48. Sanz, E., Yang, L., Su, T., Morris, D.R., McKnight, G.S., and Amieux, P.S. (2009) Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci USA 106: 13939-13944.
49. Striepen, B., Jordan, C.N., Reiff, S., and van Dooren, G.G. (2007) Building the perfect parasite: cell division in apicomplexa. PLoS Pathog 3: e78.
50. Sugimoto, M., Kuo, M.L., Roussel, M.F., and Sherr, C.J. (2003) Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol Cell 11: 415-424.
51. Suvorova, E.S., Lehmann, M.M., Kratzer, S., and White, M.W. (2012) Nuclear actin-related protein is required for chromosome segregation in Toxoplasma gondii. Mol Biochem Parasitol 181: 7-16.
52. Suvorova, E.S., Croken, M., Kratzer, S., Ting, L.M., de Felipe, M.C., Balu, B., etal. (2013) Discovery of a splicing regulator required for cell cycle progression. PLoS Genet 9: e1003305.
53. Svotelis, A., Gevry, N., and Gaudreau, L. (2009) Regulation of gene expression and cellular proliferation by histone H2A.Z. Biochem Cell Biol 87: 179-188.
54. Teuscher, F., Chen, N., Kyle, D.E., Gatton, M.L., and Cheng, Q. (2012) Phenotypic changes in artemisinin-resistant Plasmodium falciparum lines in vitro: evidence for decreased sensitivity to dormancy and growth inhibition. Antimicrob Agents Chemother 56: 428-431.
55. Thiry, M., and Lafontaine, D.L. (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol 15: 194-199.
56. Tucker, M.S., Mutka, T., Sparks, K., Patel, J., and Kyle, D.E. (2012) Phenotypic and genotypic analysis of in vitro-selected artemisinin-resistant progeny of Plasmodium falciparum. Antimicrob Agents Chemother 56: 302-314.
57. Volarevic, S., Stewart, M.J., Ledermann, B., Zilberman, F., Terracciano, L., Montini, E., etal. (2000) Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 288: 2045-2047.
58. Warner, J.R. (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-440.
59. White, M.W., Kameji, T., Pegg, A.E., and Morris, D.R. (1987) Increased efficiency of translation of ornithine decarboxylase mRNA in mitogen-activated lymphocytes. Eur J Biochem 170: 87-92.
60. White, S.R., and Lauring, B. (2007) AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8: 1657-1667.