Non-coding stem-bulge RNAs are required for cell proliferation and embryonic development in C. elegans

Journal of Cell Science

Volumn 128, Issue 11, 2015, Pages 2118-2129

  Kowalski, Madzia P ^a   Baylis, Howard A ^a   Krude, Torsten ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cell proliferation; DNA replication; Non coding RNA

Indexed keywords

MORPHOLINO OLIGONUCLEOTIDE; UNTRANSLATED RNA;

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; CHROMOSOME; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; EMBRYO DEVELOPMENT; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VERTEBRATE; ANIMAL; GENETICS;

CAENORHABDITIS ELEGANS; NEMATODA; VERTEBRATA;

ANIMALS; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; DNA REPLICATION; EMBRYONIC DEVELOPMENT; RNA, UNTRANSLATED;

EID: 84930788049     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.166744     Document Type: Article

References (50)

1. Aftab, M. N., He, H., Skogerbø, G. and Chen, R. (2008). Microarray analysis of ncRNA expression patterns in Caenorhabditis elegans after RNAi against snoRNA associated proteins. BMC Genomics 9, 278.
2. Baugh, L. R., Hill, A. A., Slonim, D. K., Brown, E. L. and Hunter, C. P. (2003). Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development 130, 889-900.
3. Benkemoun, L., Descoteaux, C., Chartier, N. T., Pintard, L. and Labbé, J. C. (2014). PAR-4/LKB1 regulates DNA replication during asynchronous division of the early C. elegans embryo. J. Cell Biol. 205, 447-455.
4. Boria, I., Gruber, A. R., Tanzer, A., Bernhart, S. H., Lorenz, R., Mueller, M. M., Hofacker, I. L. and Stadler, P. F. (2010). Nematode sbRNAs: homologs of vertebrate Y RNAs. J. Mol. Evol. 70, 346-358.
5. Brauchle, M., Baumer, K. and Gönczy, P. (2003). Differential activation of the DNA replication checkpoint contributes to asynchrony of cell division in C. elegans embryos. Curr. Biol. 13, 819-827.
6. Brown, D. D. and Littna, E. (1964). RNA synthesis during the development of Xenopus laevis, the South African clawed toad. J. Mol. Biol. 8, 669-687.
7. Chen, X. and Wolin, S. L. (2004). The Ro 60 kDa autoantigen: insights into cellular function and role in autoimmunity. J. Mol. Med. 82, 232-239.
8. Chowdhury, D., Choi, Y. E. and Brault, M. E. (2013). Charity begins at home: non-coding RNA functions in DNA repair. Nat. Rev. Mol. Cell Biol. 14, 181-189.
9. Christov, C. P., Gardiner, T. J., Szüts, D. and Krude, T. (2006). Functional requirement of noncoding Y RNAs for human chromosomal DNA replication. Mol. Cel. Biol. 26, 6993-7004.
10. Christov, C. P., Trivier, E. and Krude, T. (2008). Noncoding human Y RNAs are overexpressed in tumours and required for cell proliferation. Br. J. Cancer 98, 981-988.
11. Collart, C., Christov, C. P., Smith, J. C. and Krude, T. (2011). The midblastula transition defines the onset of Y RNA-dependent DNA replication in Xenopus laevis. Mol. Cell. Biol. 31, 3857-3870.
12. Crooks, G. E., Hon, G., Chandonia, J. M. and Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190.
13. Deng, W., Zhu, X., Skogerbø, G., Zhao, Y., Fu, Z., Wang, Y., He, H., Cai, L., Sun, H., Liu, C. et al. (2006). Organization of the Caenorhabditis elegans small non-coding transcriptome: genomic features, biogenesis, and expression. Genome Res. 16, 20-29.
14. Edgar, L. G. (1995). Blastomere culture and analysis. Methods Cell Biol. 48, 303-321.
15. Edgar, L. G. and McGhee, J. D. (1988). DNA synthesis and the control of embryonic gene expression in C. elegans. Cell 53, 589-599.
16. Eisen, J. S. and Smith, J. C. (2008). Controlling morpholino experiments: don't stop making antisense. Development 135, 1735-1743.
17. Encalada, S. E., Martin, P. R., Phillips, J. B., Lyczak, R., Hamill, D. R., Swan, K. A. and Bowerman, B. (2000). DNA replication defects delay cell division and disrupt cell polarity in early Caenorhabditis elegans embryos. Dev. Biol. 228, 225-238.
18. Gaggioli, V., Zeiser, E., Rivers, D., Bradshaw, C. R., Ahringer, J. and Zegerman, P. (2014). CDK phosphorylation of SLD-2 is required for replication initiation and germline development in C. elegans. J. Cell Biol. 204, 507-522.
19. Gardiner, T. J., Christov, C. P., Langley, A. R. and Krude, T. (2009). A conserved motif of vertebrate Y RNAs essential for chromosomal DNA replication. RNA 15, 1375-1385.
20. Hall, A. E., Turnbull, C. and Dalmay, T. (2013). Y RNAs: recent developments. BioMolecular Concepts 4, 103-110.
21. Hendrick, J. P., Wolin, S. L., Rinke, J., Lerner, M. R. and Steitz, J. A. (1981). Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells. Mol. Cell. Biol. 1, 1138-1149.
22. Hyrien, O., Maric, C. and Méchali, M. (1995). Transition in specification of embryonic metazoan DNA replication origins. Science 270, 994-997.
23. Krude, T. (2000). Initiation of human DNA replication in vitro using nuclei from cells arrested at an initiation-competent state. J. Biol. Chem. 275, 13699-13707.
24. Krude, T., Christov, C. P., Hyrien, O. and Marheineke, K. (2009). Y RNA functions at the initiation step of mammalian chromosomal DNA replication. J. Cell Sci. 122, 2836-2845.
25. Labbé, J. C., Hekimi, S. and Rokeach, L. A. (1999). The levels of the RoRNP-associated Y RNA are dependent upon the presence of ROP-1, the Caenorhabditis elegans Ro60 protein. Genetics 151, 143-150.
26. Labbé, J. C., Burgess, J., Rokeach, L. A. and Hekimi, S. (2000). ROP-1, an RNA quality-control pathway component, affects Caenorhabditis elegans dauer formation. Proc. Natl. Acad. Sci. USA 97, 13233-13238.
27. Langley, A. R., Chambers, H., Christov, C. P. and Krude, T. (2010). Ribonucleoprotein particles containing non-coding Y RNAs, Ro60, La and nucleolin are not required for Y RNA function in DNA replication. PLoS ONE 5, e13673.
28. Langley, A. R., Smith, J. C., Stemple, D. L. and Harvey, S. A. (2014). New insights into the maternal to zygotic transition. Development 141, 3834-3841.
29. Lerner, M. R., Boyle, J. A., Hardin, J. A. and Steitz, J. A. (1981). Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus. Science 211, 400-402.
30. Lewis, J. A. and Fleming, J. T. (1995). Basic culture methods. Methods Cell Biol. 48, 3-29.
31. Louvet-Vallée, S., Kolotuev, I., Podbilewicz, B. and Félix, M. A. (2003). Control of vulval competence and centering in the nematode Oscheius sp. 1 CEW1. Genetics 163, 133-146.
32. Mathews, D. H., Sabina, J., Zuker, M. and Turner, D. H. (1999). Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288, 911-940.
33. Mello, C. and Fire, A. (1995). DNA transformation. Methods Cell Biol. 48, 451-482.
34. Mohammad, M. M., Donti, T. R., Sebastian Yakisich, J., Smith, A. G. and Kapler, G. M. (2007). Tetrahymena ORC contains a ribosomal RNA fragment that participates in rDNA origin recognition. EMBO J. 26, 5048-5060.
35. Morris, K. V. and Mattick, J. S. (2014). The rise of regulatory RNA. Nat. Rev. Genet. 15, 423-437.
36. Newport, J. and Kirschner, M. (1982a). A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30, 675-686.
37. Newport, J. and Kirschner, M. (1982b). A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30, 687-696.
38. Norseen, J., Thomae, A., Sridharan, V., Aiyar, A., Schepers, A. and Lieberman, P. M. (2008). RNA-dependent recruitment of the origin recognition complex. EMBO J. 27, 3024-3035.
39. Sharma, V. and Misteli, T. (2013). Non-coding RNAs in DNA damage and repair. FEBS Lett. 587, 1832-1839.
40. Sonneville, R., Querenet, M., Craig, A., Gartner, A. and Blow, J. J. (2012). The dynamics of replication licensing in live Caenorhabditis elegans embryos. J. Cell Biol. 196, 233-246.
41. Sulston, J. E., Schierenberg, E., White, J. G. and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
42. van den Heuvel, S. (2005). Cell-cycle regulation. InWormBook (ed. The C. elegans Research Community). Pasadena, CA: Wormbook.
43. Van Horn, D. J., Eisenberg, D., O'Brien, C. A. and Wolin, S. L. (1995). Caenorhabditis elegans embryos contain only one major species of Ro RNP. RNA 1, 293-303.
44. Walston, T. and Hardin, J. (2010). An agar mount for observation of Caenorhabditis elegans embryos. Cold Spring Harb. Protoc. 2010, pdb prot5540.
45. Wang, I., Kowalski, M. P., Langley, A. R., Rodriguez, R., Balasubramanian, S., Hsu, S. T. and Krude, T. (2014). Nucleotide contributions to the structural integrity and DNA replication initiation activity of noncoding Y RNA. Biochemistry 53, 5848-5863.
46. Will, S., Reiche, K., Hofacker, I. L., Stadler, P. F. and Backofen, R. (2007). Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering. PLOS Comput. Biol. 3, e65.
47. Wolin, S. L. and Cedervall, T. (2002). The La protein. Annu. Rev. Biochem. 71, 375-403.
48. Zhang, A. T., Langley, A. R., Christov, C. P., Kheir, E., Shafee, T., Gardiner, T. J. and Krude, T. (2011). Dynamic interaction of Y RNAs with chromatin and initiation proteins during human DNA replication. J. Cell Sci. 124, 2058-2069.
49. Zheng, M., Messerschmidt, D., Jungblut, B. and Sommer, R. J. (2005). Conservation and diversification of Wnt signaling function during the evolution of nematode vulva development. Nat. Genet. 37, 300-304.
50. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415.