Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
GoGreen Membership

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 6 June 2003:
Vol. 300. no. 5625, pp. 1581 - 1584
DOI: 10.1126/science.1084737

Reports

Programmed DNA Deletion As an RNA-Guided System of Genome Defense

Meng-Chao Yao,* Patrick Fuller, Xiaohui Xi

Genomewide DNA rearrangements occur in many eukaryotes during development, but their functions and mechanisms are poorly understood. Previous studies have implicated a sequence-recognition mechanism based on RNA-mediated interactions between nuclei in ciliated protozoa. In this study, we found that the process recognized and deleted a foreign gene integrated in a Tetrahymena chromosome, suggesting an unusual mechanism of genome surveillance. We further found that injection of double-stranded RNA into the cell at specific developmental stages triggers efficient deletion of the targeted genomic regions. Together the results indicate an RNA-based mechanism that directs genomewide DNA rearrangements and serves to disable invading genetic agents.

Division of Basic Sciences, Fred Hutchinson Cancer ResearchCenter, 1100 Fairview Avenue North, Post Office Box 19024, Seattle, WA 98109, USA.

* To whom correspondence should be addressed. E-mail: mcyao{at}fhcrc.org

Read the Full Text



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena.
L. Aronica, J. Bednenko, T. Noto, L. V. DeSouza, K.W. M. Siu, J. Loidl, R. E. Pearlman, M. A. Gorovsky, and K. Mochizuki (2008)
Genes & Dev. 22, 2228-2241
   Abstract »    Full Text »    PDF »
Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia.
G. Lepere, M. Betermier, E. Meyer, and S. Duharcourt (2008)
Genes & Dev. 22, 1501-1512
   Abstract »    Full Text »    PDF »
Non-Mendelian Inheritance of Paralogs of 2 Cytoskeletal Genes in the Ciliate Chilodonella uncinata.
T. Robinson and L. A. Katz (2007)
Mol. Biol. Evol. 24, 2495-2503
   Abstract »    Full Text »    PDF »
Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components.
M. El-Shami, D. Pontier, S. Lahmy, L. Braun, C. Picart, D. Vega, M.-A. Hakimi, S. E. Jacobsen, R. Cooke, and T. Lagrange (2007)
Genes & Dev. 21, 2539-2544
   Abstract »    Full Text »    PDF »
Tudor Nuclease Genes and Programmed DNA Rearrangements in Tetrahymena thermophila.
R. A. Howard-Till and M.-C. Yao (2007)
Eukaryot. Cell 6, 1795-1804
   Abstract »    Full Text »    PDF »
Identification of novel chromatin-associated proteins involved in programmed genome rearrangements in Tetrahymena.
M.-C. Yao, C.-H. Yao, L. M. Halasz, P. Fuller, C. H. Rexer, S. H. Wang, R. Jain, R. S. Coyne, and D. L. Chalker (2007)
J. Cell Sci. 120, 1978-1989
   Abstract »    Full Text »    PDF »
Bexarotene (LGD1069, Targretin), a Selective Retinoid X Receptor Agonist, Prevents and Reverses Gemcitabine Resistance in NSCLC Cells by Modulating Gene Amplification.
P. Tooker, W.-C. Yen, S.-C. Ng, A. Negro-Vilar, and T. W. Hermann (2007)
Cancer Res. 67, 4425-4433
   Abstract »    Full Text »    PDF »
Induction of Gene Silencing by Hairpin RNA Expression in Tetrahymena thermophila Reveals a Second Small RNA Pathway.
R. A. Howard-Till and M.-C. Yao (2006)
Mol. Cell. Biol. 26, 8731-8742
   Abstract »    Full Text »    PDF »
The germ line limited M element of Tetrahymena is targeted for elimination from the somatic genome by a homology-dependent mechanism.
C. A. Kowalczyk, A. M. Anderson, M. Arce-Larreta, and D. L. Chalker (2006)
Nucleic Acids Res. 34, 5778-5789
   Abstract »    Full Text »    PDF »
Genome Architecture Drives Protein Evolution in Ciliates.
R. A. Zufall, C. L. McGrath, S. V. Muse, and L. A. Katz (2006)
Mol. Biol. Evol. 23, 1681-1687
   Abstract »    Full Text »    PDF »
The Condensin Complex Is Essential for Amitotic Segregation of Bulk Chromosomes, but Not Nucleoli, in the Ciliate Tetrahymena thermophila.
M. D. Cervantes, R. S. Coyne, X. Xi, and M.-C. Yao (2006)
Mol. Cell. Biol. 26, 4690-4700
   Abstract »    Full Text »    PDF »
The SUMO Pathway Is Developmentally Regulated and Required for Programmed DNA Elimination in Paramecium tetraurelia.
A. Matsuda and J. D. Forney (2006)
Eukaryot. Cell 5, 806-815
   Abstract »    Full Text »    PDF »
Evolution of Programmed DNA Rearrangements in a Scrambled Gene.
L. C. Wong and L. F. Landweber (2006)
Mol. Biol. Evol. 23, 756-763
   Abstract »    Full Text »    PDF »
Two classes of endogenous small RNAs in Tetrahymena thermophila.
S. R. Lee and K. Collins (2006)
Genes & Dev. 20, 28-33
   Abstract »    Full Text »    PDF »
The CNA1 Histone of the Ciliate Tetrahymena thermophila Is Essential for Chromosome Segregation in the Germline Micronucleus.
M. D. Cervantes, X. Xi, D. Vermaak, M.-C. Yao, and H. S. Malik (2006)
Mol. Biol. Cell 17, 485-497
   Abstract »    Full Text »    PDF »
Double-Stranded RNA Induces Sequence-Specific Antiviral Silencing in Addition to Nonspecific Immunity in a Marine Shrimp: Convergence of RNA Interference and Innate Immunity in the Invertebrate Antiviral Response?.
J. Robalino, T. Bartlett, E. Shepard, S. Prior, G. Jaramillo, E. Scura, R. W. Chapman, P. S. Gross, C. L. Browdy, and G. W. Warr (2005)
J. Virol. 79, 13561-13571
   Abstract »    Full Text »    PDF »
The evolutionary origin of a complex scrambled gene.
W.-J. Chang, P. D. Bryson, H. Liang, M. K. Shin, and L. F. Landweber (2005)
PNAS 102, 15149-15154
   Abstract »    Full Text »    PDF »
Germ Line Transcripts Are Processed by a Dicer-Like Protein That Is Essential for Developmentally Programmed Genome Rearrangements of Tetrahymena thermophila.
C. D. Malone, A. M. Anderson, J. A. Motl, C. H. Rexer, and D. L. Chalker (2005)
Mol. Cell. Biol. 25, 9151-9164
   Abstract »    Full Text »    PDF »
Ribo-gnome: The Big World of Small RNAs.
P. D. Zamore and B. Haley (2005)
Science 309, 1519-1524
   Abstract »    Full Text »    PDF »
RNA meets chromatin.
E. Bernstein and C. D. Allis (2005)
Genes & Dev. 19, 1635-1655
   Abstract »    Full Text »    PDF »
Elimination of Foreign DNA during Somatic Differentiation in Tetrahymena thermophila Shows Position Effect and Is Dosage Dependent.
Y. Liu, X. Song, M. A. Gorovsky, and K. M. Karrer (2005)
Eukaryot. Cell 4, 421-431
   Abstract »    Full Text »    PDF »
A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase.
K. Mochizuki and M. A. Gorovsky (2005)
Genes & Dev. 19, 77-89
   Abstract »    Full Text »    PDF »
Non-Mendelian Inheritance Induced by Gene Amplification in the Germ Nucleus of Paramecium tetraurelia.
A. Matsuda and M. Takahashi (2005)
Genetics 169, 137-147
   Abstract »    Full Text »    PDF »
Communication Between Parental and Developing Genomes During Tetrahymena Nuclear Differentiation Is Likely Mediated by Homologous RNAs.
D. L. Chalker, P. Fuller, and M.-C. Yao (2005)
Genetics 169, 149-160
   Abstract »    Full Text »    PDF »
RNA Polymerase II Localizes in Tetrahymena thermophila Meiotic Micronuclei When Micronuclear Transcription Associated with Genome Rearrangement Occurs.
K. Mochizuki and M. A. Gorovsky (2004)
Eukaryot. Cell 3, 1233-1240
   Abstract »    Full Text »    PDF »
Effects of Length and Location on the Cellular Response to Double-Stranded RNA.
Q. Wang and G. G. Carmichael (2004)
Microbiol. Mol. Biol. Rev. 68, 432-452
   Abstract »    Full Text »    PDF »
RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia.
O. Garnier, V. Serrano, S. Duharcourt, and E. Meyer (2004)
Mol. Cell. Biol. 24, 7370-7379
   Abstract »    Full Text »    PDF »
A Large Imprinted microRNA Gene Cluster at the Mouse Dlk1-Gtl2 Domain.
H. Seitz, H. Royo, M.-L. Bortolin, S.-P. Lin, A. C. Ferguson-Smith, and J. Cavaille (2004)
Genome Res. 14, 1741-1748
   Abstract »    Full Text »    PDF »
Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement.
K. Mochizuki and M. A. Gorovsky (2004)
Genes & Dev. 18, 2068-2073
   Abstract »    Full Text »    PDF »
Role of Micronucleus-Limited DNA in Programmed Deletion of mse2.9 during Macronuclear Development of Tetrahymena thermophila.
J. S. Fillingham and R. E. Pearlman (2004)
Eukaryot. Cell 3, 288-301
   Abstract »    Full Text »    PDF »
Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena.
Y. Liu, K. Mochizuki, and M. A. Gorovsky (2004)
PNAS 101, 1679-1684
   Abstract »    Full Text »    PDF »
A Non-Long Terminal Repeat Retrotransposon Family Is Restricted to the Germ Line Micronucleus of the Ciliated Protozoan Tetrahymena thermophila.
J. S. Fillingham, T. A. Thing, N. Vythilingum, A. Keuroghlian, D. Bruno, G. B. Golding, and R. E. Pearlman (2004)
Eukaryot. Cell 3, 157-169
   Abstract »    Full Text »    PDF »
RNA Interference and mRNA Silencing, 2004: How Far Will They Reach?.
T. Pederson (2004)
Mol. Biol. Cell 15, 407-410
   Abstract »    Full Text »    PDF »
RNA Interference: Biology, Mechanism, and Applications.
N. Agrawal, P. V. N. Dasaradhi, A. Mohmmed, P. Malhotra, R. K. Bhatnagar, and S. K. Mukherjee (2003)
Microbiol. Mol. Biol. Rev. 67, 657-685
   Abstract »    Full Text »    PDF »
The small RNA world.
E. J. Finnegan and M. A. Matzke (2003)
J. Cell Sci. 116, 4689-4693
   Full Text »    PDF »



ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)