Mammalian HCA66 protein is required for both ribosome synthesis and centriole duplication

Nucleic Acids Research

Volumn 40, Issue 13, 2012, Pages 6270-6289

  Bonnart, Chrystelle ^a,b   Gérus, Marie ^a,b   Hoareau Aveilla, Coralie ^a,b   Kiss, Tamás ^a,b   Caizergues Ferrer, Michèle ^a,b   Henry, Yves ^a,b   Henras, Anthony K ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN HCA66; RIBOSOME RNA; RNA 18S; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVITY; CELL FUNCTION; CELL MATURATION; CELLULAR DISTRIBUTION; CENTRIOLE DUPLICATION; CENTROSOME; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RIBOSOME SUBUNIT; RIBOSOME SYNTHESIS; RNA CLEAVAGE; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; YEAST CELL;

ANTIGENS, NEOPLASM; CARRIER PROTEINS; CELL NUCLEOLUS; CENTRIOLES; CENTROSOME; HELA CELLS; HUMANS; NUCLEAR PROTEINS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RIBOSOMES; RNA PRECURSORS; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 18S; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES;

MAMMALIA;

EID: 84864490082     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks234     Document Type: Article

References (63)

1. Henras, A.K., Soudet, J., Gerus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci., 65, 2334-2359.
2. Kressler, D., Hurt, E. and Bassler, J. (2010) Driving ribosome assembly. Biochim. Biophys. Acta, 1803, 673-683.
3. Panse, V.G. and Johnson, A.W. (2010) Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci., 35, 260-266.
4. Russell, J. and Zomerdijk, J.C. (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem. Sci., 30, 87-96.
5. Clemente-Blanco, A., Mayan-Santos, M., Schneider, D.A., Machn, F., Jarmuz, A., Tschochner, H. and Aragon, L. (2009) Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature, 458, 219-222.
6. 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.
7. Rosado, I.V., Kressler, D. and de la Cruz, J. (2007) Functional analysis of Saccharomyces cerevisiae ribosomal protein Rpl3p in ribosome synthesis. Nucleic Acids Res., 35, 4203-4213.
8. Grimm, T., Holzel, M., Rohrmoser, M., Harasim, T., Malamoussi, A., Gruber-Eber, A., Kremmer, E. and Eick, D. (2006) Dominant-negative Pes1 mutants inhibit ribosomal RNA processing and cell proliferation via incorporation into the PeBoW-complex. Nucleic Acids Res., 34, 3030-3043.
9. Holzel, M., Rohrmoser, M., Schlee, M., Grimm, T., Harasim, T., Malamoussi, A., Gruber-Eber, A., Kremmer, E., Hiddemann, W., Bornkamm, G.W. et al. (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.
10. Iwanami, N., Higuchi, T., Sasano, Y., Fujiwara, T., Hoa, V.Q., Okada, M., Talukder, S.R., Kunimatsu, S., Li, J., Saito, F. et al. (2008) WDR55 is a nucleolar modulator of ribosomal RNA synthesis, cell cycle progression, and teleost organ development. PLoS Genet., 4, e1000171.
11. Lapik, Y.R., Fernandes, C.J., Lau, L.F. and Pestov, D.G. (2004) Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol. Cell, 15, 17-29.
12. 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.
13. Bhat, K.P., Itahana, K., Jin, A. and Zhang, Y. (2004) Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. EMBO J., 23, 2402-2412.
14. Dai, M.S., Zeng, S.X., Jin, Y., Sun, X.X., David, L. and Lu, H. (2004) Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol. Cell. Biol., 24, 7654-7668.
15. Rubbi, C.P. and Milner, J. (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J., 22, 6068-6077.
16. Yuan, X., Zhou, Y., Casanova, E., Chai, M., Kiss, E., Grone, H.J., Schutz, G. and Grummt, I. (2005) Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Mol. Cell, 19, 77-87.
17. Lindstrom, M.S. and Nister, M. (2010) Silencing of ribosomal protein S9 elicits a multitude of cellular responses inhibiting the growth of cancer cells subsequent to p53 activation. PLoS One, 5, e9578.
18. Lindstrom, M.S. and Zhang, Y. (2008) Ribosomal protein S9 is a novel B23/NPM-binding protein required for normal cell proliferation. J. Biol. Chem., 283, 15568-15576.
19. Llanos, S. and Serrano, M. (2010) Depletion of ribosomal protein L37 occurs in response to DNA damage and activates p53 through the L11/MDM2 pathway. Cell Cycle, 9, 4005-4012.
20. Sun, X.X., Wang, Y.G., Xirodimas, D.P. and Dai, M.S. (2010) Perturbation of 60 S ribosomal biogenesis results in ribosomal protein L5-and L11-dependent p53 activation. J. Biol. Chem., 285, 25812-25821.
21. Castle, C.D., Cassimere, E.K., Lee, J. and Denicourt, C. (2010) Las1L is a nucleolar protein required for cell proliferation and ribosome biogenesis. Mol. Cell. Biol., 30, 4404-4414.
22. 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.
23. Holzel, M., Orban, M., Hochstatter, J., Rohrmoser, M., Harasim, T., Malamoussi, A., Kremmer, E., Langst, G. and Eick, D. (2010) Defects in 18 S or 28 S rRNA processing activate the p53 pathway. J. Biol. Chem., 285, 6364-6370.
24. 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.
25. McMahon, M., Ayllon, V., Panov, K.I. and O'Connor, R. (2010) Ribosomal 18 S RNA processing by the IGF-I-responsive WDR3 protein is integrated with p53 function in cancer cell proliferation. J. Biol. Chem., 285, 18309-18318.
26. Peng, Q., Wu, J., Zhang, Y., Liu, Y., Kong, R., Hu, L., Du, X. and Ke, Y. (2010) 1A6/DRIM, a novel T-UTP, activates RNA polymerase I transcription and promotes cell proliferation. PLoS One, 5, e14244.
27. Wang, Y., Liu, J., Zhao, H., Lu, W., Zhao, J., Yang, L., Li, N., Du, X. and Ke, Y. (2007) Human 1A6/DRIM, the homolog of yeast Utp20, functions in the 18S rRNA processing. Biochim. Biophys. Acta, 1773, 863-868.
28. Yu, W., Qiu, Z., Gao, N., Wang, L., Cui, H., Qian, Y., Jiang, L., Luo, J., Yi, Z., Lu, H. et al. (2010) PAK1IP1, a ribosomal stress-induced nucleolar protein, regulates cell proliferation via the p53-MDM2 loop. Nucleic Acids Res., 39, 2234-2248.
29. Deisenroth, C. and Zhang, Y. (2010) Ribosome biogenesis surveillance: probing the ribosomal protein-MDM2-p53 pathway. Oncogene, 29, 4253-4260.
30. Ionescu, C.N., Origanti, S. and McAlear, M.A. (2004) The yeast rRNA biosynthesis factor Ebp2p is also required for efficient nuclear division. Yeast, 21, 1219-1232.
31. Killian, A., Le Meur, N., Sesboue, R., Bourguignon, J., Bougeard, G., Gautherot, J., Bastard, C., Frebourg, T. and Flaman, J.M. (2004) Inactivation of the RRB1-Pescadillo pathway involved in ribosome biogenesis induces chromosomal instability. Oncogene, 23, 8597-8602.
32. Oeffinger, M., Fatica, A., Rout, M.P. and Tollervey, D. (2007) Yeast Rrp14p is required for ribosomal subunit synthesis and for correct positioning of the mitotic spindle during mitosis. Nucleic Acids Res., 35, 1354-1366.
33. Oeffinger, M. and Tollervey, D. (2003) Yeast Nop15p is an RNA-binding protein required for pre-rRNA processing and cytokinesis. EMBO J., 22, 6573-6583.
34. Cai, T., Aulds, J., Gill, T., Cerio, M. and Schmitt, M.E. (2002) The Saccharomyces cerevisiae RNAse mitochondrial RNA processing is critical for cell cycle progression at the end of mitosis. Genetics, 161, 1029-1042.
35. Gill, T., Aulds, J. and Schmitt, M.E. (2006) A specialized processing body that is temporally and asymmetrically regulated during the cell cycle in Saccharomyces cerevisiae. J. Cell Biol., 173, 35-45.
36. Gill, T., Cai, T., Aulds, J., Wierzbicki, S. and Schmitt, M.E. (2004) RNAse MRP cleaves the CLB2 mRNA to promote cell cycle progression: novel method of mRNA degradation. Mol. Cell. Biol., 24, 945-953.
37. Okuda, M., Horn, H.F., Tarapore, P., Tokuyama, Y., Smulian, A.G., Chan, P.K., Knudsen, E.S., Hofmann, I.A., Snyder, J.D., Bove, K.E. et al. (2000) Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell, 103, 127-140.
38. Ugrinova, I., Monier, K., Ivaldi, C., Thiry, M., Storck, S., Mongelard, F. and Bouvet, P. (2007) Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication. BMC Mol. Biol., 8, 66.
39. Piddubnyak, V., Rigou, P., Michel, L., Rain, J.C., Geneste, O., Wolkenstein, P., Vidaud, D., Hickman, J.A., Mauviel, A. and Poyet, J.L. (2007) Positive regulation of apoptosis by HCA66, a new Apaf-1 interacting protein, and its putative role in the physiopathology of NF1 microdeletion syndrome patients. Cell Death Differ., 14, 1222-1233.
40. Fant, X., Gnadt, N., Haren, L. and Merdes, A. (2009) Stability of the small gamma-tubulin complex requires HCA66, a protein of the centrosome and the nucleolus. J. Cell Sci., 122, 1134-1144.
41. Champion, E.A., Lane, B.H., Jackrel, M.E., Regan, L. and Baserga, S.J. (2008) A direct interaction between the Utp6 half-a-tetratricopeptide repeat domain and a specific peptide in Utp21 is essential for efficient pre-rRNA processing. Mol. Cell. Biol., 28, 6547-6556.
42. Dragon, F., Gallagher, J.E., Compagnone-Post, P.A., Mitchell, B.M., Porwancher, K.A., Wehner, K.A., Wormsley, S., Settlage, R.E., Shabanowitz, J., Osheim, Y. et al. (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature, 417, 967-970.
43. Basi, G., Schmid, E. and Maundrell, K. (1993) TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene, 123, 131-136.
44. Voth, W.P., Jiang, Y.W. and Stillman, D.J. (2003) New 'marker swap' plasmids for converting selectable markers on budding yeast gene disruptions and plasmids. Yeast, 20, 985-993.
45. Longtine, M.S., McKenzie, A. III, Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J.R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast, 14, 953-961.
46. Courtheoux, T., Gay, G., Gachet, Y. and Tournier, S. (2009) Ase1/Prc1-dependent spindle elongation corrects merotely during anaphase in fission yeast. J. Cell Biol., 187, 399-412.
47. Tournier, S., Gachet, Y., Buck, V., Hyams, J.S. and Millar, J.B. (2004) Disruption of astral microtubule contact with the cell cortex activates a Bub1, Bub3, and Mad3-dependent checkpoint in fission yeast. Mol. Biol. Cell, 15, 3345-3356.
48. Gietz, D., St Jean, A., Woods, R.A. and Schiestl, R.H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res., 20, 1425.
49. Gerus, M., Bonnart, C., Caizergues-Ferrer, M., Henry, Y. and Henras, A.K. (2010) Evolutionarily conserved function of RRP36 in early cleavages of the pre-rRNA and production of the 40S ribosomal subunit. Mol. Cell. Biol., 30, 1130-1144.
50. Henras, A., Henry, Y., Bousquet-Antonelli, C., Noaillac-Depeyre, J., Gelugne, J.P. and Caizergues-Ferrer, M. (1998) Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J., 17, 7078-7090.
51. Haren, L., Remy, M.H., Bazin, I., Callebaut, I., Wright, M. and Merdes, A. (2006) NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J. Cell Biol., 172, 505-515.
52. Tollervey, D. (1987) A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J., 6, 4169-4175.
53. Pestov, D.G., Lapik, Y.R. and Lau, L.F. (2008) Assays for ribosomal RNA processing and ribosome assembly. Curr. Protoc. Cell Biol., 39, 22.11.1-22.11.16.
54. O'Donohue, M.F., Choesmel, V., Faubladier, M., Fichant, G. and Gleizes, P.E. (2010) Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J. Cell Biol., 190, 853-866.
55. Gallenberger, M., Meinel, D.M., Kroeber, M., Wegner, M., Milkereit, P., Bosl, M.R. and Tamm, E.R. (2011) Lack of WDR36 leads to preimplantation embryonic lethality in mice and delays the formation of small subunit ribosomal RNA in human cells in vitro. Hum. Mol. Genet., 20, 422-435.
56. Knop, M., Pereira, G., Geissler, S., Grein, K. and Schiebel, E. (1997) The spindle pole body component Spc97p interacts with the gamma-tubulin of Saccharomyces cerevisiae and functions in microtubule organization and spindle pole body duplication. EMBO J., 16, 1550-1564.
57. Raynaud-Messina, B. and Merdes, A. (2007) Gamma-tubulin complexes and microtubule organization. Curr. Opin. Cell Biol., 19, 24-30.
58. Chial, H.J. and Winey, M. (1999) Mechanisms of genetic instability revealed by analysis of yeast spindle pole body duplication. Biol. Cell, 91, 439-450.
59. Jaspersen, S.L. and Winey, M. (2004) The budding yeast spindle pole body: structure, duplication, and function. Annu. Rev. Cell Dev. Biol., 20, 1-28.
60. Champion, E.A., Kundrat, L., Regan, L. and Baserga, S.J. (2009) A structural model for the HAT domain of Utp6 incorporating bioinformatics and genetics. Protein Eng. Des. Sel., 22, 431-439.
61. Preker, P.J. and Keller, W. (1998) The HAT helix, a repetitive motif implicated in RNA processing. Trends Biochem. Sci., 23, 15-16.
62. Savkur, R.S. and Olson, M.O. (1998) Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res., 26, 4508-4515.
63. Hoareau-Aveilla, C., Bonoli, M., Caizergues-Ferrer, M. and Henry, Y. (2006) hNaf1 is required for accumulation of human box H/ACA snoRNPs, scaRNPs, and telomerase. RNA, 12, 832-840.