Tissue-specific direct targets of Caenorhabditis elegans Rb/E2F dictate distinct somatic and germline programs

Genome Biology

Volumn 14, Issue 1, 2013, Pages

  Kudron, Michelle ^a   Niu, Wei ^a   Lu, Zhi ^b,c   Wang, Guilin ^a   Gerstein, Mark ^c   Snyder, Michael ^d   Reinke, Valerie ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TSINGHUA UNIVERSITY   (China)

^c YALE UNIVERSITY   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN HP1; HETEROCHROMATIN PROTEIN HPL 2; HISTONE H3; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CHROMATIN; CSR-1 PROTEIN, C ELEGANS; HISTONE; HPL-2 PROTEIN, C ELEGANS; LIN-35 PROTEIN, C ELEGANS; MES-4 PROTEIN, C ELEGANS; NONHISTONE PROTEIN; REPRESSOR PROTEIN;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; BINDING SITE; CAENORHABDITIS ELEGANS; CELL FATE; CELLS BY BODY ANATOMY; CHROMATIN; CONTROLLED STUDY; CRS 1 GENE; DNA BINDING; DPL 1 GENE; E2F GENE; EFL 1 GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCUS; GENE TARGETING; GENETIC ASSOCIATION; GENETIC TRANSFORMATION; GERMLINE MUTATION; HETEROCHROMATIN; HISTONE METHYLATION; HPL 2 GENE; IN VIVO STUDY; INTESTINE; LIN 35 GENE; MES 4 GENE; MUTANT; NONHUMAN; PHENOTYPE; PIE 1 GENE; RB GENE; SOMATIC MUTATION; TISSUE SPECIFICITY; TRANSGENE; ANIMAL; ANTIBODY SPECIFICITY; GENETIC TRANSCRIPTION; GENETICS; GERM CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; E2F TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; HISTONES; INTESTINES; ORGAN SPECIFICITY; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84872686356     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-1-r5     Document Type: Article

References (45)

1. Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
2. Chen HZ, Tsai SY, Leone G: Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 2009, 9:785-797.
3. Xu X, Bieda M, Jin VX, Rabinovich A, Oberley MJ, Green R, Farnham PJ: A comprehensive ChIP chip analysis of E2F1, E2F4, and E2F6 in normal and tumor cells reveals interchangeable roles of E2F family members. Genome Res 2007, 17:1550-1561.
4. Lee BK, Bhinge AA, Iyer VR: Wide-ranging functions of E2F4 in transcriptional activation and repression revealed by genome-wide analysis. Nucleic Acids Res 2011, 39:3558-3573.
5. Ceol CJ, Horvitz HR: dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol Cell 2001, 7:461-473.
6. Page BD, Guedes S, Waring D, Priess JR: The C. elegans E2F-and DP-related proteins are required for embryonic asymmetry and negatively regulate Ras/MAPK signaling. Mol Cell 2001, 7:451-460.
7. Fay DS, Yochem J: The SynMuv genes of Caenorhabditis elegans in vulval development and beyond. Dev Biol 2007, 306:1-9.
8. Wu X, Shi Z, Cui M, Han M, Ruvkun G: Repression of germline RNAi pathways in somatic cells by retinoblastoma pathway chromatin complexes. PLoS Genet 2012, 8:e1002542.
9. Wang D, Kennedy S, Conte D, Kim JK, Gabel HW, Kamath RS, Mello CC, Ruvkun G: Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants. Nature 2005, 436:593-597.
10. Petrella LN, Wang W, Spike CA, Rechtsteiner A, Reinke V, Strome S: synMuv B proteins antagonize germline fate in the intestine and ensure C. elegans survival. Development 2011, 138:1069-1079.
11. Chi W, Reinke V: Promotion of oogenesis and embryogenesis in the C. elegans gonad by EFL-1/DPL-1 (E2F) does not require LIN-35 (pRB). Development 2006, 133:3147-3157.
12. Zhong M, Niu W, Lu ZJ, Sarov M, Murray JI, Janette J, Raha D, Sheaffer KL, Lam HYK, Preston E, Slightham C, Hillier LW, Brock T, Agarwal A, Auerbach R, Hyman AA, Gerstein M, Mango SE, Kim SK, Waterston RH, Reinke V, Snyder M: Genome-wide identification of binding sites defines distinct functions for Caenorhabditis elegans PHA-4/FOXA in development and environmental response. PLoS Genet 2010, 6:e1000848.
13. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, Alves P, Chateigner A, Perry M, Morris M, Auerbach RK, Feng X, Leng J, Vielle A, Niu W, Rhrissorrakrai K, Agarwal A, Alexander RP, Barber G, Brdlik CM, Brennan J, Brouillet JJ, Carr A, Cheung M-S, Clawson H, Contrino S, et al: Integrative analysis of the Caenorhabditis elegans genome by the modENCODE Project. Science 2010, 330:1775-1787.
14. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, Janette J, Chen C, Alves P, Preston E, Slightham C, Jiang L, Hyman AA, Kim SK, Waterston RH, Gerstein M, Snyder M, Reinke V: Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res 2011, 21:245-254.
15. Tabuchi TM, Deplancke B, Osato N, Zhu LJ, Barrasa MI, Harrison MM, Horvitz HR, Walhout AJM, Hagstrom KA: Chromosome-Biased Binding and Gene Regulation by the Caenorhabditis elegans DRM Complex. PLoS Genet 2011, 7:e1002074.
16. Ouellet J, Roy R: The lin-35/Rb and RNAi pathways cooperate to regulate a key cell cycle transition in C. elegans. BMC Dev Biol 2007, 7:38.
17. Byerly L, Cassada RC, Russell RL: The life cycle of the nematode Caenorhabditis elegans*1:: I. Wild-type growth and reproduction. Dev Biol 1976, 51:23-33.
18. Sulston JE, Schierenberg E, White JG, Thomson JN: The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983, 100:64-119.
19. Rozowsky J, Euskirchen G, Auerbach RK, Zhang ZD, Gibson T, Bjornson R, Carriero N, Snyder M, Gerstein MB: PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol 2009, 27:66-75.
20. Kirienko NV, Fay DS: Transcriptome profiling of the C. elegans Rb ortholog reveals diverse developmental roles. Dev Biol 2007, 305:674-684.
21. Reinke V, Gil IS, Ward S, Kazmer K: Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 2004, 131:311.
22. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJ, Davis EB, Scherer S, Ward S, Kim SK: A global profile of germline gene expression in C. elegans. Mol Cell 2000, 6:605-616.
23. Kelly WG, Schaner CE, Dernburg AF, Lee MH, Kim SK, Villeneuve AM, Reinke V: X-chromosome silencing in the germline of C. elegans. Development 2002, 129:479.
24. Chi W, Reinke V: DPL-1 (DP) acts in the germ line to coordinate ovulation and fertilization in C. elegans. Mech Dev 2009, 126:406-416.
25. Dimova DK, Dyson NJ: The E2F transcriptional network: old acquaintances with new faces. Oncogene 2005, 24:2810-2826.
26. Lin B, Reinke V: The candidate MAP kinase phosphorylation substrate DPL-1 (DP) promotes expression of the MAP kinase phosphatase LIP-1 in C. elegans germ cells. Dev Biol 2008, 316:50-61.
27. Farnham PJ: Insights from genomic profiling of transcription factors. Nat Rev Genet 2009, 10:605-616.
28. Polley SRG, Fay DS: A network of genes antagonistic to the LIN-35 retinoblastoma protein of Caenorhabditis elegans. Genetics 2012, 191:1367-1380.
29. Rechtsteiner A, Ercan S, Takasaki T, Phippen TM, Egelhofer TA, Wang W, Kimura H, Lieb JD, Strome S: The histone H3K36 methyltransferase MES-4 acts epigenetically to transmit the memory of germline gene expression to progeny. PLoS Genet 2010, 6:ii, e1001091.
30. Grishok A, Hoersch S, Sharp PA: RNA interference and retinoblastomarelated genes are required for repression of endogenous siRNA targets in Caenorhabditis elegans. Proc Natl Acad Sci USA 2008, 105:20386-20391.
31. She X, Xu X, Fedotov A, Kelly WG, Maine EM: Regulation of heterochromatin assembly on unpaired chromosomes during Caenorhabditis elegans meiosis by components of a small RNA-mediated pathway. PLoS Genet 2009, 5:e1000624.
32. Claycomb JM, Batista PJ, Pang KM, Gu W, Vasale JJ, Van Wolfswinkel JC, Chaves DA, Shirayama M, Mitani S, Ketting RF, Conte D Jr, Mello CC: The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 2009, 139:123-134.
33. Gu W, Shirayama M, Conte D Jr, Vasale J, Batista PJ, Claycomb JM, Moresco JJ, Youngman EM, Keys J, Stoltz MJ, Chen C-CG, Chaves DA, Duan S, Kasschau KD, Fahlgren N, Yates JR, Mitani S, Carrington JC, Mello CC: Distinct Argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 2009, 36:231-244.
34. Rizzolio F, Esposito L, Muresu D, Fratamico R, Jaraha R, Caprioli GV, Giordano A: RB gene family: Genome-wide ChIP approaches could open undiscovered roads. J Cell Biochem 2009, 109:839-843.
35. Stengel KR, Thangavel C, Solomon DA, Angus SP, Zheng Y, Knudsen ES: Retinoblastoma/p107/p130 pocket proteins: protein dynamics and interactions with target gene promoters. J Biol Chem 2009, 284:19265-19271.
36. Schertel C, Conradt B: C. elegans orthologs of components of the RB tumor suppressor complex have distinct pro-apoptotic functions. Development 2007, 134:3691-3701.
37. Cui M, Chen J, Myers TR, Hwang BJ, Sternberg PW, Greenwald I, Han M: SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans. Dev Cell 2006, 10:667-672.
38. Brenner S: The Genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
39. Praitis V, Casey E, Collar D, Austin J: Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 2001, 157:1217-1226.
40. Lefrançois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T, Yellman CM, Gerstein M, Snyder M: Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC genomics 2009, 10:37.
41. DAVID. [http://david.abcc.ncifcrf.gov/].
42. Statistical significance of the overlap between two groups of genes. [http://nemates.org/MA/progs/overlap_stats.html].
43. Jones AR, Francis R, Schedl T: GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage-and sex-specific expression during Caenorhabditis elegans germline development. Dev Biol 1996, 180:165-183.
44. Leacock SW, Reinke V: Expression profiling of MAP kinase-mediated meiotic progression in Caenorhabditis elegans. PLoS Genet 2006, 2:e174.
45. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J: Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000, 408:325-330.