Knockdown of the Drosophila GTPase nucleostemin 1 impairs large ribosomal subunit biogenesis, cell growth, and midgut precursor cell maintenance

Molecular Biology of the Cell

Volumn 20, Issue 20, 2009, Pages 4424-4434

  Rosby, Raphyel ^a   Zhengfang, Cui ^a   Rogers, Emily ^a   DeLivron, Megan A ^b   Robinson, Victoria L ^b   DiMario, Patrick J ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN NUCLEOSTEMIN1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIBODY LABELING; ARTICLE; BIOGENESIS; CELL GROWTH; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DROSOPHILA; HUMAN; HUMAN CELL; LARGE RIBOSOMAL SUBUNIT; MIDGUT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; STEM CELL;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CELL NUCLEOLUS; CHROMOSOMES; CONSERVED SEQUENCE; DROSOPHILA PROTEINS; GENE DELETION; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; GTP-BINDING PROTEINS; GUANOSINE TRIPHOSPHATE; INTESTINES; LARVA; LYSOSOMES; MALPIGHIAN TUBULES; MOLECULAR SEQUENCE DATA; NEOPLASMS, EXPERIMENTAL; PHAGOSOMES; PUPA; RIBOSOME SUBUNITS, LARGE; RNA INTERFERENCE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 70350094390     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-06-0592     Document Type: Article

References (61)

1. Bassler, J., Grandi, P., Gadal, O., Leßmann, T., Petfalski, E., Tollervey, D., Lechner, J., and Hurt, E. (2001). Identification of a pre-ribosomal 60S particle that is closely linked to nuclear export. Mol. Cell 8, 517-529. (Pubitemid 32946930)
2. Bassler, J., Kallas, M., and Hurt, E. (2006). The Nug1 GTPase reveals an N-terminal RNA binding domain that is essential for association with 60S pre-ribosomal particles. J. Biol. Chem. 281, 24737-24744.
3. Beekman, C., Nichane, M., De Clercq, S., Maetens, M., Floss, T., Wurst, W., Bellefroid, E., and Marine, J.-C. (2006). Evolutionarily conserved role of nucleostemin: controlling proliferation of stem/progenitor cells during early vertebrate development. Mol. Cell. Biol. 26, 9291-9301.
4. Bodenstein, D. (1950). The postembryonic development of Drosophila. In: Biology of Drosophila, ed. M. Demerec, John Wiley & Sons, New York, 275-367.
5. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering fates and generating phenotypes. Development 118, 401-415. (Pubitemid 23214028)
6. Brodsky, M. H., Weinert, B. T., Tsang, G., Rong, Y. S., McGinnis, N. M., Golic, K. G., Rio, D. C., and Rubin, G. M. (2004). Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol. Cell Biol. 24, 1219-1231.
7. Campbell, T. L., Daigle, D. M., and Brown, E. D. (2005). Characterization of the Bacillus subtilis GTPase YloQ and its role in ribosome function. Biochem. J. 389, 843-852.
8. Campbell, T. L., and Brown, E. D. (2008). Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. J. Bacteriol. 190, 2537-2545.
9. Cerdido, A., and Medina, F. J. (1995). Subnuclear location of fibrillarin and variation in its levels during the cell cycle and during differentiation of plant cells. Chromosoma 103, 625-634.
10. Cui, Z., and DiMario, P. J. (2007). RNAi knockdown of Nopp140 induces Minute-like phenotypes in Drosophila. Mol. Biol. Cell 18, 2179-2191. (Pubitemid 46911369)
11. Curtiss, J., and Heilig, J. S. (1995). Establishment of Drosophila imaginal precursor cells is controlled by the Arrowhead gene. Development 121, 3819-3825.
12. Dai, M.-S., Sun, X.-X., and Lu, H. (2008). Aberrant expression of nucleostemin activates p53 and induces cell cycle arrest via inhibition of MDM2. Mol. Cell Biol. 28, 4365-4376.
13. Daigle, D. M., Rossi, L., Berghuis, A. M., Aravind, L., Koonin, E. V., and Brown, E. D. (2002). YjeQ, an essential, conserved, uncharacterized protein from Escherichia coli, is an unusual GTPase with circularly permuted G-motifs and marked burst kinetics. Biochemistry 41, 11109-11117.
14. Daigle, D. M., and Brown, E. D. (2004). Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J. Bacteriol. 186, 1381-1387. (Pubitemid 38248728)
15. de Cuevas, M., Lee, J. K., and Spradling, A. C. (1996). α-Spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122, 3959-3968. (Pubitemid 27033890)
16. DiMario, P. J., Rosby, R., and Cui, Z. (2006). Direct visualization of GFP-fusion proteins on polytene chromosomes. Dros. Infor. Serv. 89, 115-118.
17. Du, X., Subba Rao, M.R.K., Chen, X.-Q., Wu, W., Mahalingam, S., and Balasundaran, D. (2006). The homologous putative GTPases Grn1p from fission yeast and the human GNL3L are required for growth and play a role in processing of nucleolar pre-rRNA. Mol. Biol. Cell 17, 460-474.
18. Duffy, J. B. (2002). GAL4 system in Drosophila: a geneticist's Swiss army knife. Genesis 34, 1-15.
19. Grisendi, S., Mecucci, C., Falini, B., and Pandolfi, P. P. (2006). Nucleophosmin and cancer. Nat. Rev. Cancer 6, 493-505.
20. Hartenstein, V., and Jan, Y. N. (1992). Studying Drosophila embryogenesis with PlacZ enhancer trap lines. Roux's Arch. Dev. Biol. 201, 194-220.
21. Hedges, J., West, M., and Johnson, A. W. (2005). Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J. 24, 567-579. (Pubitemid 40343258)
22. Himeno, H., et al. (2004). A novel GTPase activated by the small subunit of ribosome. Nucleic Acids Res. 32, 5303-5309. (Pubitemid 39445517)
23. Honma, Y., Kitamura, A., Shioda, R., Maruyama, H., Ozaki, K., Oda, Y., Mini, T., Jenö , P., Maki, Y., Yonezawa, K., Hurt, E., Ueno, M., Uritani, M., Hall, M. N., and Ushimaru, T. (2006). TOR regulates late steps of ribosome maturation in the nucleoplasm via Nog1 in response to nutrients. EMBO J. 25, 3832-3842. (Pubitemid 44300269)
24. Johnson, A. W. (2003). Nuclear export of ribosomal subunits. In: The Nucleolus, ed. M.O.J. Olson, New York: Kluwer Academic/Plenum Publishers, 286-301.
25. Kallstrom, G., Hedges, J., and Johnson, A. (2003). The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol. Cell. Biol. 23, 4344-4355.
26. Kaplan, D. D., Zimmermann, G., Suyama, K., Meyer, T., and Scott, M. P. (2008). A nucleostemin family GTPase, NS3, acts in serotonergic neurons to regulate insulin signaling and control body size. Genes Dev. 22, 1877-1893. (Pubitemid 352008637)
27. Kiehart, D. P., Crawford, J. M., and Montague, R. A. (2000). Quantitative microinjection of Drosophila embryos. In: Drosophila Protocols, ed. W. Sullivan, M. Ashburner, and R. S. Hawley, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 345-359.
28. Kudron, M. M., and Reinke, V. (2008). C. elegans nucleostemin is required for larval growth and germline stem cell division. PLoS Genet. 4, e1000181. doi: 10.1371/journal.pgen. 1000181.
29. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
30. Lanzetta, P. A., Alvarez, L. J., Reinarch, P. S., and Candia, O. A. (1979). An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100, 95-97.
31. Leipe, D. D., Wolf, Y. I., Koonin, E. V., and Aravind, L. (2002). Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317, 41-72.
32. Li, T.-R., and White, K. P. (2003). Tissue-specific gene expression and ecdysone- regulated genomic networks in Drosophila. Dev. Cell 5, 59-72. (Pubitemid 36827342)
33. Ma, H., and Pederson, T. (2007). Depletion of the nucleolar protein nucleostemin causes G1 cell cycle arrest via the p53 pathway. Mol. Biol. Cell 18, 2630-2635.
34. Ma, H., and Pederson, T. (2008a). Nucleostemin is a binding partner of nucleophosmin in human osteosarcoma cells. Mol. Biol. Cell 19, 2870-2875.
35. Ma, H., and Pederson, T. (2008b). Nucleostemin: a multiplex regulator of cell-cycle progression. Trends Cell Biol. 18, 575-579.
36. Matsuo, Y., Morimoto, T., Kuwano, M., Loh, P. C., Oshima, T., and Ogasawara, N. (2006). The GTP-binding protein YlqF participates in the late step of 50S ribosomal subunit assembly in Bacillus subtilis. J. Biol. Chem. 281, 8110-8117. (Pubitemid 43847429)
37. McPhee, C. K., and Baehrecke, E. H. (2009). Autophagy in Drosophila melanogaster. Biochim. Biophys. Acta 1793, 1452-1460.
38. Meng, L., Yasumoto, H., and Tsai, R.Y.L. (2006). Multiple controls regulate nucleostemin portioning between nucleolus and nucleoplasm. J. Cell Sci. 119, 5124-5136. (Pubitemid 46085191)
39. Meng, L., Zhu, Q., and Tsai, R.Y.L. (2007). Nucleolar trafficking of nucleostemin family proteins: common versus protein-specific mechanisms. Mol. Cell Biol. 27, 8670-8682.
40. Misteli, T. (2005). Going in GTP cycles in the nucleolus. J. Cell Biol. 168, 177-178.
41. Normile, D. (2002). Common control for cancer, stem cells. Science 298, 1869.
42. Politz, J.C.R., Polena, I., Trask, I., Bazett-Jones, D. P., and Pederson, T. (2005). A nonribosomal landscape in the nucleolus revealed by the stem cell protein nucleostemin. Mol. Biol. Cell 16, 3401-3410.
43. Reynaud, E. G., Andrade, M. A., Bonneau, F., Bach, T., Ly, N., Knop, M., Scheffzek, K., and Pepperkok, R. (2005). Human Lsg1 defines a family of essential GTPases that correlates with the evolution of compartmentalization. BMC Biol. 3, 21. (Pubitemid 41554952)
44. Romanova, L., Grand, A., Zhang, L., Rayner, S., Katoku-Kikyo, N., Kellner, S., and Kikyo, N. (2009). Critical role of nucleostemin in pre-rRNA processing. J. Biol. Chem. 284, 4968-4977.
45. Rorth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
46. Saveanu, C., Bienvenu, D., Namane, A., Gleizes, P-E., Gas, N., Jacquier, A., and Fromont-Racine, M. (2001). Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J. 20, 6475-6484. (Pubitemid 33078720)
47. Schneider, I. (1972). Cell lines derived from late embryonic stages of Drosophila melanogaster. J. Embryol. Exp. Morphol. 27, 353-365.
48. Skaer, H. (1993). The alimentary canal. In: The Development of Drosophila melanogaster, ed. M. Bate and A. Martinez-Arias, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 941-1012.
49. Sogame, N., Kim, M., and Abrams, J. M. (2003). Drosophila p53 preserves genomic stability by regulating cell death. Proc. Natl. Acad. Sci. USA 100, 4696-4701.
50. Sonnenblick, B. P. (1950). The early embryology of Drosophila melanogaster In: Biology of Drosophila, ed. M. Demerec, New York: John Wiley & Sons, 62-167.
51. Sparrow, J. C. (1971). Melanotic "tumours." In: The Genetics and Biology of Drosophila, Vol.2b, ed. M. Ashburner and T.R.F. Wright, New York: Academic Press, 277-313.
52. Spradling, A. C. (1986). P element-mediated transformation. In: Drosophila: A Practical Approach, ed. D. B. Roberts, Oxford, United Kingdom: IRL Press, 175-197.
53. Steller, H. (2000). Drosophila p53, meeting the grim reaper. Nat. Cell Biol. 2, E100-E102.
54. Szebeni, A., Hingorani, K., Negi, S., and Olson, M.O.J. (2003). Role of protein kinase CK2 phosphorylation in the molecular chaperone activity of nucleolar protein B23. J. Biol. Chem. 278, 9107-9115.
55. Tabor, S., and Richardson, C. C. (1985). A bacteriophage T7 RNA polymerase/ promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82, 1074-1078.
56. Tepass, U., and Hartenstein, V. (1995). Neurogenic and proneural genes control cell fate specification in the Drosophila endoderm. Development 121, 393-405.
57. Tollervey, D., Lehtonen, H., Jansen, R., Kern, H., and Hurt, E. (1993). Temperature- sensitive mutations demonstrate roles for yeast fibrillarin in prerRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 72, 443-457. (Pubitemid 23059413)
58. Tsai, R.Y.L., and McKay, R. D. (2002). A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev. 16, 2991-3003. (Pubitemid 35424188)
59. Tsai, R.Y.L., and McKay, R. D. (2005). A multistep, GTP-driven mechanism controlling the dynamic cycling of nucleostemin. J. Cell Biol. 168, 179-184.
60. Wullschleger, S., Loewith, R., and Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell 124, 471-484.
61. Zhu, X., and Stein, D. (2004). RNAi-mediated inhibition of gene function in the follicle cell layer of the Drosophila ovary. Genesis 40, 101-108. (Pubitemid 39488506)