Transcription Termination Factor reb1p Causes Two Replication Fork Barriers at Its Cognate Sites in Fission Yeast Ribosomal DNA in Vivo

Molecular and Cellular Biology

Volumn 24, Issue 1, 2004, Pages 398-406

  Sánchez Gorostiaga, Alicia ^a   López Estraño, Carlos ^a,b   Krimer, Dora B ^a   Schvartzman, Jorge B ^a   Hernández, Pablo ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; RIBOSOME DNA; RIBOSOME RNA; TRANS ACTING FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION TERMINATION FACTOR REB1P; UNCLASSIFIED DRUG;

ARTICLE; CELL BUDDING; DNA BINDING; DNA REPLICATION; EUKARYOTE; GENE DELETION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

DNA REPLICATION; DNA, RIBOSOMAL; DNA-BINDING PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION FACTORS;

EUKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 17944401516     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.1.398-406.2004     Document Type: Article

References (44)

1. Bähler, J., J. Q. Wu, M. S. Longtine, N. G. Shah, A. McKenzie III, A. B. Steever, A. Wach, P. Philippsen, and J. R. Pringle. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943-951.
2. Benguría, A., P. Hernández, D. B. Krimer, and J. B. Schvartzman. 2003. Sir2p suppresses recombination of replication forks stalled at the replication fork barrier of ribosomal DNA in Saccharomyces cerevisiae. Nucleic Acids Res. 31:893-898.
3. Brewer, B. J., and W. L. Fangman. 1988. A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell 55:637-643.
4. Brewer, B. J., D. Lockshon, and W. L. Fangman. 1992. The arrest of replication forks in the rDNA of yeast occurs independently of transcription. Cell 71:267-276.
5. Caddle, M. S., and M. P. Calos. 1994. Specific initiation at an origin of replication from Schizosaccharomycespombe. Mol. Cell. Biol. 14:1796-1805.
6. Dalgaard, J. Z., and A. J. S. Klar. 2000. swi1 and swi3 perform imprinting, pausing, and termination of DNA replication in S. pombe. Cell 102:745-751.
7. Dalgaard, J. Z., and A. J. S. Klar. 2001. A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mat1 in S. pombe. Genes Dev. 15:2060-2068.
8. Fourel, G., E. Revardel, C. E. Koering, and E. Gilson. 1999. Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J. 18:2522-2537.
9. Friedman, K. L., and B. J. Brewer. 1994. The analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol. 262:613-627.
10. Gerber, J.-K., E. Göegel, C. Berger, M. Wallisch, F. Müller, I. Grummt, and F. Grummt. 1997. Termination of mammalian rDNA replication: polar arrest of replication fork movement by transcription termination factor TTF-I. Cell 90:559-567.
11. Gomez, M., and F. Antequera. 1999. Organization of DNA replication origins in the fission yeast genome. EMBO J. 18:5683-5690.
12. Grummt, I., U. Maier, A. Ohrlein, N. Hassouna, and J. P. Bachellerie. 1985. Transcription of mouse rDNA terminates downstream of the 3′ end of 28S RNA and involves interaction of factors with repeated sequences in the 3′ spacer. Cell 43:801-810.
13. Hernández, P., L. Martín-Parras, M. L. Martí nez-Robles, and J. B. Schvartzman. 1993. Conserved features in the mode of replication of eukaryotic ribosomal RNA genes. EMBO J. 12:1475-1485.
14. Hindley, J., G. Phear, M. Stein, and D. Beach. 1987. Sucllencodes a predicted 13-kilodalton protein that is essential for cell viability and is directly involved in the division cycle of Schizosaccharomyces pombe. Mol. Cell. Biol. 7:504-511.
15. Huberman, J. A., L. D. Spotila, K. A. Nawotka, S. M. El-Assouli, and L. R. Davis. 1987. The in vivo replication origin of the yeast 2 microns plasmid. Cell 51:473-481.
16. Ju, Q. D., B. E. Morrow, and J. R. Warner. 1990. REB1, a yeast DNA-binding protein with many targets, is essential for growth and bears some resemblance to the oncogene myb. Mol. Cell. Biol. 10:5226-5234.
17. Kaeberlein, M., M. McVey, and L. Guarente. 1999. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 13:2570-2580.
18. Kobayashi, T., D. J. Heck, M. Nomura, and T. Horiuchi. 1998. Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev. 12:3821-3830.
19. Kobayashi, T., and T. Horiuchi. 1996. A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1:465-474.
20. Kobayashi, T., M. Nomura, and T. Horiuchi. 2001. Identification of DNA cis elements essential for expansion of ribosomal DNA repeats in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:136-147.
21. Kuhn, A., I. Bartsch, and I. Grummt. 1990. Specific interaction of the murine transcription termination factor TTF I with class-1 RNA polymerases. Nature 344:559-562.
22. Lang, W. H., and R. H. Reeder. 1993. The REB1 site is an essential component of a terminator for RNA polymerase I in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:649-658.
23. Lapeyre, B., B. Michot, J. Feliu, and J. P. Bachellerie. 1993. Nucleotide sequence of the Schizosaccharomyces pombe 25S ribosomal RNA and its phylogenetic implications. Nucleic Acids Res. 21:3322.
24. Linskens, M. H. K., and J. A. Huberman. 1988. Organization of replication of ribosomal DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:4927-4935.
25. Little, R. D., T. H. K. Platt, and C. L. Schildkraut. 1993. Initiation and termination of DNA replication in human rRNA genes. Mol. Cell. Biol. 13:6600-6613.
26. López-Estraño, C., J. B. Schvartzman, and P. Hernández. 1997. The replication of ribosomal RNA genes in eukaryotes. Chromosomes Today 12:149-169.
27. López-Estraño, C., J. B. Schvartzman, D. B. Krimer, and P. Hernández. 1998. Co-localization of polar replication fork barriers and rRNA transcription terminators in mouse rDNA. J. Mol. Biol. 277:249-256.
28. López-Estraño, C., J. B. Schvartzman, D. B. Krimer, and P. Hernández. 1999. Characterization of the pea rDNA replication fork barrier: putative cis-acting and trans-acting factors. Plant Mol. Biol. 40:99-110.
29. Maleszka, R., and G. D. Clark-Walker. 1993. Yeasts have a four-fold variation in ribosomal DNA copy number. Yeast 9:53-58.
30. Melekhovets, Y. F., P. S. Shwed, and R. N. Nazar. 1997. In vivo analyses of RNA polymerase I termination in Schizosaccharomyces pombe. Nucleic Acids Res. 25:5103-5109.
31. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823.
32. Olavarrieta, L., P. Hernández, D. B. Krimer, and J. B. Schvartzman. 2002. DNA knotting caused by head-on collision of transcription and replication. J. Mol. Biol. 322:1-6.
33. Pasero, P., and M. Marilley. 1993. Size variation of rDNA clusters in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol. Gen. Genet. 236:448-452.
34. Prentice, H. L. 1992. High efficiency transformation of Schizosaccharomyces pombe by electroporation. Nucleic Acids Res. 20:621.
35. Pütter, V., and F. Grummt. 2002. Transcription termination factor TTF-I exhibits contrahelicase activity during DNA replication. EMBO Rep. 3:147-152.
36. Reeder, R. H., P. Guevara, and J. G. Roan. 1999. Saccharomyces cerevisiae RNA polymerase I terminates transcription at the Reb1 terminator in vivo. Mol. Cell. Biol. 19:7369-7376.
37. Sanchez, J. A., S. M. Kim, and J. A. Huberman. 1998. Ribosomal DNA replication in the fission yeast, Schizosaccharomyces pombe. Exp. Cell Res. 238:220-230.
38. Shwed, P. S., and R. N. Nazar. 1999. Terminator element mutations affect both the efficiency and position of RNA polymerase I termination in Schizosaccharomyces pombe. Nucleic Acids Res. 27:2883-2888.
39. Wai, H., K. Johzuka, L. Vu, K. Eliason, T. Kobayashi, T. Horiuchi, and M. Nomura. 2001. Yeast RNA polymerase I enhancer is dispensable for transcription of the chromosomal rRNA gene and cell growth, and its apparent transcription enhancement from ectopic promoters requires Fob1 protein. Mol. Cell. Biol. 21:5541-5553.
40. Wang, K. L., and J. R. Warner. 1998. Positive and negative autoregulation of REB1 transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:4368-4376.
41. Ward, T. R., M. L. Hoang, R. Prusty, C. K. Lau, R. L. Keil, W. L. Fangman, and B. J. Brewer. 2000. Ribosomal DNA replication fork barrier and HOT1 recombination hot spot: shared sequences but independent activities. Mol. Cell. Biol. 20:4948-4957.
42. Wiesendanger, B., R. Lucchini, T. Koller, and J. M. Sogo. 1994. Replication fork barriers in the Xenopus rDNA. Nucleic Acids Res. 22:5038-5046.
43. Zhang, Z., D. M. Macalpine, and G. M. Kapler. 1997. Developmental regulation of DNA replication: replication fork barriers and programmed gene amplification in Tetrahymena thermophila. Mol. Cell. Biol. 17:6147-6156.
44. Zhao, A., A. Guo, Z. Liu, and L. Pape. 1997. Molecular cloning and analysis of Schizosaccharomyces pombe Reb1p: sequence-specific recognition of two sites in the far upstream rDNA intergenic spacer. Nucleic Acids Res. 25:904-910.