Phosphorylation of RNA polymerase II is independent of P-TEFb in the C. elegans germline

Development (Cambridge)

Volumn 140, Issue 17, 2013, Pages 3703-3713

  Bowman, Elizabeth Anne ^a   Bowman, Christopher Ray ^b   Ahn, Jeong H ^a   Kelly, William G ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C. elegans; CDK 12; CDK 9

Indexed keywords

CYCLIN DEPENDENT KINASE 12; CYCLIN DEPENDENT KINASE 9; CYCLIN T; PROTEIN SERINE THREONINE KINASE; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; DEGRADATION; DEVELOPMENT; ENZYME PHOSPHORYLATION; GAMETOGENESIS; GASTRULATION; NONHUMAN; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROMOTER REGION; SOMATIC CELL; SYNCYTIUM; TRANSCRIPTION ELONGATION; X CHROMOSOME;

C. ELEGANS; CDK-12; CDK-9;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CLUTCH SIZE; CYCLIN-DEPENDENT KINASES; GERM CELLS; MICROSCOPY, FLUORESCENCE; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA POLYMERASE II; SERINE;

EID: 84881601434     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.095778     Document Type: Article

References (62)

1. Adelman, K. and Lis, J. T. (2012). Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 13, 720-731.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Andersen, E. C. and Horvitz, H. R. (2007). Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development. Development 134, 2991-2999.
4. Ashcroft, S. J. H. and Pereira, C. (2003). Practical Statistics for the Biological Sciences: Simple Pathways to Statistical Analyses. Basingstoke, UK; New York, NY: Palgrave Macmillan.
5. Bartkowiak, B. and Greenleaf, A. L. (2011). Phosphorylation of RNAPII: To P-TEFb or not to P-TEFb? Transcription 2, 115-119.
6. Bartkowiak, B., Liu, P., Phatnani, H. P., Fuda, N. J., Cooper, J. J., Price, D. H., Adelman, K., Lis, J. T. and Greenleaf, A. L. (2010). CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev. 24, 2303-2316.
7. Baugh, L. R., Demodena, J. and Sternberg, P. W. (2009). RNA Pol II accumulates at promoters of growth genes during developmental arrest. Science 324, 92-94.
8. Bender, L. B., Suh, J., Carroll, C. R., Fong, Y., Fingerman, I. M., Briggs, S. D., Cao, R., Zhang, Y., Reinke, V. and Strome, S. (2006). MES-4: an autosomeassociated histone methyltransferase that participates in silencing the X chromosomes in the C. elegans germ line. Development 133, 3907-3917.
9. Blazek, D., Kohoutek, J., Bartholomeeusen, K., Johansen, E., Hulinkova, P., Luo, Z., Cimermancic, P., Ule, J. and Peterlin, B. M. (2011). The Cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev. 25, 2158-2172.
10. Buratowski, S. and Kim, T. (2010). The role of cotranscriptional histone methylations. Cold Spring Harb. Symp. Quant. Biol. 75, 95-102.
11. Cecere, G., Hoersch, S., Jensen, M. B., Dixit, S. and Grishok, A. (2013). The ZFP-1(AF10)/DOT-1 complex opposes H2B ubiquitination to reduce Pol II transcription. Mol. Cell 50, 894-907.
12. Chapman, R. D., Heidemann, M., Albert, T. K., Mailhammer, R., Flatley, A., Meisterernst, M., Kremmer, E. and Eick, D. (2007). Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318, 1780-1782.
13. Cho, H., Kim, T. K., Mancebo, H., Lane, W. S., Flores, O. and Reinberg, D. (1999). A protein phosphatase functions to recycle RNA polymerase II. Genes Dev. 13, 1540-1552.
14. Chu, Y., Sutton, A., Sternglanz, R. and Prelich, G. (2006). The BUR1 cyclindependent protein kinase is required for the normal pattern of histone methylation by SET2. Mol. Cell. Biol. 26, 3029-3038.
15. Cole, C., Barber, J. D. and Barton, G. J. (2008). The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201.
16. Curran, S. P., Wu, X., Riedel, C. G. and Ruvkun, G. (2009). A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 459, 1079-1084.
17. Egloff, S. and Murphy, S. (2008). Cracking the RNA polymerase II CTD code. Trends Genet. 24, 280-288.
18. Freter, R., Osawa, M. and Nishikawa, S. (2010). Adult stem cells exhibit global suppression of RNA polymerase II serine-2 phosphorylation. Stem Cells 28, 1571-1580.
19. Frøkjær-Jensen, C., Davis, M. W., Hopkins, C. E., Newman, B. J., Thummel, J. M., Olesen, S. P., Grunnet, M. and Jorgensen, E. M. (2008). Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375-1383.
20. Fuda, N. J., Buckley, M. S., Wei, W., Core, L. J., Waters, C. T., Reinberg, D. and Lis, J. T. (2012). Fcp1 dephosphorylation of the RNA polymerase II C-terminal domain is required for efficient transcription of heat shock genes. Mol. Cell. Biol. 32, 3428-3437.
21. Furuhashi, H., Takasaki, T., Rechtsteiner, A., Li, T., Kimura, H., Checchi, P. M., Strome, S. and Kelly, W. G. (2010). Trans-generational epigenetic regulation of C. elegans primordial germ cells. Epigenetics Chromatin 3, 15.
22. Garvin, C., Holdeman, R. and Strome, S. (1998). The phenotype of mes-2, mes-3, mes-4 and mes-6, maternal-effect genes required for survival of the germline in Caenorhabditis elegans, is sensitive to chromosome dosage. Genetics 148, 167-185.
23. Gassmann, R., Rechtsteiner, A., Yuen, K. W., Muroyama, A., Egelhofer, T., Gaydos, L., Barron, F., Maddox, P., Essex, A., Monen, J. et al. (2012). An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 484, 534-537.
24. Gaydos, L. J., Rechtsteiner, A., Egelhofer, T. A., Carroll, C. R. and Strome, S. (2012). Antagonism between MES-4 and Polycomb repressive complex 2 promotes appropriate gene expression in C. elegans germ cells. Cell Rep. 2, 1169-1177.
25. Ghosh, D. and Seydoux, G. (2008). Inhibition of transcription by the Caenorhabditis elegans germline protein PIE-1: genetic evidence for distinct mechanisms targeting initiation and elongation. Genetics 178, 235-243.
26. Glover-Cutter, K., Larochelle, S., Erickson, B., Zhang, C., Shokat, K., Fisher, R. P. and Bentley, D. L. (2009). TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Mol. Cell. Biol. 29, 5455-5464.
27. Kawasaki, I., Shim, Y. H., Kirchner, J., Kaminker, J., Wood, W. B. and Strome, S. (1998). PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94, 635-645.
28. Kelly, W. G., Schaner, C. E., Dernburg, A. F., Lee, M. H., Kim, S. K., Villeneuve, A. M. and Reinke, V. (2002). X-chromosome silencing in the germline of C. elegans. Development 129, 479-492.
29. Kimura, H., Hayashi-Takanaka, Y., Goto, Y., Takizawa, N. and Nozaki, N. (2008). The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct. Funct. 33, 61-73.
30. Kizer, K. O., Phatnani, H. P., Shibata, Y., Hall, H., Greenleaf, A. L. and Strahl, B. D. (2005). A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol. Cell. Biol. 25, 3305-3316.
31. Kohoutek, J. and Blazek, D. (2012). Cyclin K goes with Cdk12 and Cdk13. Cell Div. 7, 12.
32. Kruesi, W. S., Core, L. J., Waters, C. T., Lis, J. T. and Meyer, B. J. (2013). Condensin controls recruitment of RNA polymerase II to achieve nematode Xchromosome dosage compensation. eLife 2, e00808.
33. Kumsta, C. and Hansen, M. (2012). C. elegans rrf-1 mutations maintain RNAi efficiency in the soma in addition to the germline. PLoS ONE 7, e35428.
34. Lee, J. M. and Greenleaf, A. L. (1991). CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr. 1, 149-167.
35. Liu, J. and Kipreos, E. T. (2000). Evolution of cyclin-dependent kinases (CDKs) and CDK-activating kinases (CAKs): differential conservation of CAKs in yeast and metazoa. Mol. Biol. Evol. 17, 1061-1074.
36. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R. et al. (2011). CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229.
37. Meinhart, A., Kamenski, T., Hoeppner, S., Baumli, S. and Cramer, P. (2005). A structural perspective of CTD function. Genes Dev. 19, 1401-1415.
38. Merritt, C. and Seydoux, G. (2010). The Puf RNA-binding proteins FBF-1 and FBF-2 inhibit the expression of synaptonemal complex proteins in germline stem cells. Development 137, 1787-1798.
39. Merritt, C., Rasoloson, D., Ko, D. and Seydoux, G. (2008). 3' UTRs are the primary regulators of gene expression in the C. elegans germline. Curr. Biol. 18, 1476-1482.
40. Nakamura, A. and Seydoux, G. (2008). Less is more: specification of the germline by transcriptional repression. Development 135, 3817-3827.
41. Narita, T., Yamaguchi, Y., Yano, K., Sugimoto, S., Chanarat, S., Wada, T., Kim, D. K., Hasegawa, J., Omori, M., Inukai, N. et al. (2003). Human transcription elongation factor NELF: identification of novel subunits and reconstitution of the functionally active complex. Mol. Cell. Biol. 23, 1863-1873.
42. Pirngruber, J., Shchebet, A. and Johnsen, S. A. (2009). Insights into the function of the human P-TEFb component CDK9 in the regulation of chromatin modifications and co-transcriptional mRNA processing. Cell Cycle 8, 3636-3642.
43. Powell-Coffman, J. A., Knight, J. and Wood, W. B. (1996). Onset of C. elegans gastrulation is blocked by inhibition of embryonic transcription with an RNA polymerase antisense RNA. Dev. Biol. 178, 472-483.
44. Qiu, H., Hu, C. and Hinnebusch, A. G. (2009). Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell 33, 752-762.
45. Rechtsteiner, A., Ercan, S., Takasaki, T., Phippen, T. M., Egelhofer, T. A., Wang, W., Kimura, H., Lieb, J. D. and Strome, S. (2010). The histone H3K36 methyltransferase MES-4 acts epigenetically to transmit the memory of germline gene expression to progeny. PLoS Genet. 6, e1001091.
46. Schaner, C. E., Deshpande, G., Schedl, P. D. and Kelly, W. G. (2003). A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies. Dev. Cell 5, 747-757.
47. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
48. Seydoux, G. and Dunn, M. A. (1997). Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 124, 2191-2201.
49. Shaye, D. D. and Greenwald, I. (2011). OrthoList: a compendium of C. elegans genes with human orthologs. PLoS ONE 6, e20085.
50. Shim, E. Y., Walker, A. K., Shi, Y. and Blackwell, T. K. (2002). CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16, 2135-2146.
51. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. and Fire, A. (2001). On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465-476.
52. Strome, S. and Wood, W. B. (1983). Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 15-25.
53. 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.
54. Swanson, M. S. and Winston, F. (1992). SPT4, SPT5 and SPT6 interactions: effects on transcription and viability in Saccharomyces cerevisiae. Genetics 132, 325-336.
55. Venkatesh, S., Smolle, M., Li, H., Gogol, M. M., Saint, M., Kumar, S., Natarajan, K. and Workman, J. L. (2012). Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489, 452-455.
56. Walker, A. K., Shi, Y. and Blackwell, T. K. (2004). An extensive requirement for transcription factor IID-specific TAF-1 in Caenorhabditis elegans embryonic transcription. J. Biol. Chem. 279, 15339-15347.
57. Whittle, C. M., McClinic, K. N., Ercan, S., Zhang, X., Green, R. D., Kelly, W. G. and Lieb, J. D. (2008). The genomic distribution and function of histone variant HTZ-1 during C. elegans embryogenesis. PLoS Genet. 4, e1000187.
58. Wood, A. and Shilatifard, A. (2006). Bur1/Bur2 and the Ctk complex in yeast: the split personality of mammalian P-TEFb. Cell Cycle 5, 1066-1068.
59. Yamaguchi, Y., Wada, T., Watanabe, D., Takagi, T., Hasegawa, J. and Handa, H. (1999). Structure and function of the human transcription elongation factor DSIF. J. Biol. Chem. 274, 8085-8092.
60. Yamaguchi, Y., Shibata, H. and Handa, H. (2013). Transcription elongation factors DSIF and NELF: promoter-proximal pausing and beyond. Biochim. Biophys. Acta 1829, 98-104.
61. Zhang, F., Barboric, M., Blackwell, T. K. and Peterlin, B. M. (2003). A model of repression: CTD analogs and PIE-1 inhibit transcriptional elongation by P-TEFb. Genes Dev. 17, 748-758.
62. Zhou, Q., Li, T. and Price, D. H. (2012). RNA polymerase II elongation control. Annu. Rev. Biochem. 81, 119-143.