Seeing elegance in gene regulatory networks of the worm

Current Opinion in Genetics and Development

Volumn 21, Issue 6, 2011, Pages 776-786

  Van Nostrand, Eric L ^a   Kim, Stuart K ^a  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA; MESSENGER RNA; MICRORNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELT 2; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ALTERNATIVE RNA SPLICING; CAENORHABDITIS ELEGANS; CELL TYPE; DEVELOPMENTAL STAGE; DNA MICROARRAY; DNA SEQUENCE; EMBRYO DEVELOPMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MUTATION; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC RECOMBINATION; GENOME; GENOMICS; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; REGULATORY MECHANISM; REVIEW; RNA INTERFERENCE; RNA TRANSCRIPTION; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENOME, HELMINTH; MICRORNAS; SYSTEMS BIOLOGY; TRANSCRIPTION FACTORS;

CAENORHABDITIS ELEGANS;

EID: 80054751363     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2011.08.007     Document Type: Review

References (71)

1. The C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018.
2. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 1976, 275:327-348.
3. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
4. Kim S.K., Lund J., Kiraly M., Duke K., Jiang M., Stuart J.M., Eizinger A., Wylie B.N., Davidson G.S. A gene expression map for Caenorhabditis elegans. Science 2001, 293:2087-2092.
5. Stuart J.M., Segal E., Koller D., Kim S.K. A gene-coexpression network for global discovery of conserved genetic modules. Science 2003, 302:249-255.
6. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
7. Sulston J.E., Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 1977, 56:110-156.
8. Lamm A.T., Stadler M.R., Zhang H., Gent J.I., Fire A.Z. Multimodal RNA-seq using single-strand, double-strand, and CircLigase-based capture yields a refined and extended description of the C. elegans transcriptome. Genome Res 2011, 21:265-275.
9. Hillier L.W., Reinke V., Green P., Hirst M., Marra M.A., Waterston R.H. Massively parallel sequencing of the polyadenylated transcriptome of C. elegans. Genome Res 2009, 19:657-666.
10. Ramani A.K., Nelson A.C., Kapranov P., Bell I., Gingeras T.R., Fraser A.G. High resolution transcriptome maps for wild-type and nonsense-mediated decay-defective Caenorhabditis elegans. Genome Biol 2009, 10:R101.
11. Shin H., Hirst M., Bainbridge M.N., Magrini V., Mardis E., Moerman D.G., Marra M.A., Baillie D.L., Jones S.J. Transcriptome analysis for Caenorhabditis elegans based on novel expressed sequence tags. BMC Biol 2008, 6:30.
12. Ramani A.K., Calarco J.A., Pan Q., Mavandadi S., Wang Y., Nelson A.C., Lee L.J., Morris Q., Blencowe B.J., Zhen M., et al. Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Res 2011, 21:342-348.
13. Mangone M., Manoharan A.P., Thierry-Mieg D., Thierry-Mieg J., Han T., Mackowiak S.D., Mis E., Zegar C., Gutwein M.R., Khivansara V., et al. The landscape of C. elegans 3' UTRs. Science 2010, 329:432-435.
14. Ambros V., Lee R.C., Lavanway A., Williams P.T., Jewell D. MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol 2003, 13:807-818.
15. Lim L.P., Lau N.C., Weinstein E.G., Abdelhakim A., Yekta S., Rhoades M.W., Burge C.B., Bartel D.P. The microRNAs of Caenorhabditis elegans. Genes Dev 2003, 17:991-1008.
16. Ruby J.G., Jan C., Player C., Axtell M.J., Lee W., Nusbaum C., Ge H., Bartel D.P. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 2006, 127:1193-1207.
17. Kato M., de Lencastre A., Pincus Z., Slack F.J. Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 2009, 10:R54.
18. He H., Wang J., Liu T., Liu X.S., Li T., Wang Y., Qian Z., Zheng H., Zhu X., Wu T. Mapping the C. elegans noncoding transcriptome with a whole-genome tiling microarray. Genome Res 2007, 17:1471-1477.
19. Spencer W.C., Zeller G., Watson J.D., Henz S.R., Watkins K.L., McWhirter R.D., Petersen S., Sreedharan V.T., Widmer C., Jo J., et al. A spatial and temporal map of C. elegans gene expression. Genome Res 2011, 21:325-341.
20. Lu Z.J., Yip K.Y., Wang G., Shou C., Hillier L.W., Khurana E., Agarwal A., Auerbach R., Rozowsky J., Cheng C., et al. Prediction and characterization of noncoding RNAs in C. elegans by integrating conservation, secondary structure, and high-throughput sequencing and array data. Genome Res 2011, 21:276-285.
21. Reece-Hoyes J.S., Shingles J., Dupuy D., Grove C.A., Walhout A.J., Vidal M., Hope I.A. Insight into transcription factor gene duplication from Caenorhabditis elegans Promoterome-driven expression patterns. BMC Genomics 2007, 8:27.
22. Hunt-Newbury R., Viveiros R., Johnsen R., Mah A., Anastas D., Fang L., Halfnight E., Lee D., Lin J., Lorch A., et al. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 2007, 5:e237.
23. Dupuy D., Bertin N., Hidalgo C.A., Venkatesan K., Tu D., Lee D., Rosenberg J., Svrzikapa N., Blanc A., Carnec A., et al. Genome-scale analysis of in vivo spatiotemporal promoter activity in Caenorhabditis elegans. Nat Biotechnol 2007, 25:663-668.
24. Reinke V., Smith H.E., Nance J., Wang J., Van Doren C., Begley R., Jones S.J., Davis E.B., Scherer S., Ward S., et al. A global profile of germline gene expression in C. elegans. Mol Cell 2000, 6:605-616.
25. Gaudet J., Mango S.E. Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 2002, 295:821-825.
26. Wang X., Zhao Y., Wong K., Ehlers P., Kohara Y., Jones S.J., Marra M.A., Holt R.A., Moerman D.G., Hansen D. Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics 2009, 10:213.
27. McGhee J.D., Sleumer M.C., Bilenky M., Wong K., McKay S.J., Goszczynski B., Tian H., Krich N.D., Khattra J., Holt R.A., et al. The ELT-2 GATA-factor and the global regulation of transcription in the C. elegans intestine. Dev Biol 2007, 302:627-645.
28. Von Stetina S.E., Watson J.D., Fox R.M., Olszewski K.L., Spencer W.C., Roy P.J., Miller D.M. Cell-specific microarray profiling experiments reveal a comprehensive picture of gene expression in the C. elegans nervous system. Genome Biol 2007, 8:R135.
29. Zhang Y., Ma C., Delohery T., Nasipak B., Foat B.C., Bounoutas A., Bussemaker H.J., Kim S.K., Chalfie M. Identification of genes expressed in C. elegans touch receptor neurons. Nature 2002, 418:331-335.
30. Fox R.M., Von Stetina S.E., Barlow S.J., Shaffer C., Olszewski K.L., Moore J.H., Dupuy D., Vidal M., Miller D.M. A gene expression fingerprint of C. elegans embryonic motor neurons. BMC Genomics 2005, 6:42.
31. Colosimo M.E., Brown A., Mukhopadhyay S., Gabel C., Lanjuin A.E., Samuel A.D., Sengupta P. Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr Biol 2004, 14:2245-2251.
32. Meissner B., Warner A., Wong K., Dube N., Lorch A., McKay S.J., Khattra J., Rogalski T., Somasiri A., Chaudhry I., et al. An integrated strategy to study muscle development and myofilament structure in Caenorhabditis elegans. PLoS Genet 2009, 5:e1000537.
33. McGhee J.D., Fukushige T., Krause M.W., Minnema S.E., Goszczynski B., Gaudet J., Kohara Y., Bossinger O., Zhao Y., Khattra J., et al. ELT-2 is the predominant transcription factor controlling differentiation and function of the C. elegans intestine, from embryo to adult. Dev Biol 2009, 327:551-565.
34. Roy P.J., Stuart J.M., Lund J., Kim S.K. Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Nature 2002, 418:975-979.
35. Kunitomo H., Uesugi H., Kohara Y., Iino Y. Identification of ciliated sensory neuron-expressed genes in Caenorhabditis elegans using targeted pull-down of poly(A) tails. Genome Biol 2005, 6:R17.
36. Pauli F., Liu Y., Kim Y.A., Chen P.J., Kim S.K. Chromosomal clustering and GATA transcriptional regulation of intestine-expressed genes in C. elegans. Development 2006, 133:287-295.
37. Gaudet J., Muttumu S., Horner M., Mango S.E. Whole-genome analysis of temporal gene expression during foregut development. PLoS Biol 2004, 2:e352.
38. Gerstein M.B., Lu Z.J., Van Nostrand E.L., Cheng C., Arshinoff B.I., Liu T., Yip K.Y., Robilotto R., Rechtsteiner A., Ikegami K., et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 2010, 330:1775-1787.
39. Long F., Peng H., Liu X., Kim S.K., Myers E. A 3D digital atlas of C. elegans and its application to single-cell analyses. Nat Methods 2009, 6:667-672.
40. Bao Z., Murray J.I., Boyle T., Ooi S.L., Sandel M.J., Waterston R.H. Automated cell lineage tracing in Caenorhabditis elegans. Proc Natl Acad Sci USA 2006, 103:2707-2712.
41. Liu X., Long F., Peng H., Aerni S.J., Jiang M., Sanchez-Blanco A., Murray J.I., Preston E., Mericle B., Batzoglou S., et al. Analysis of cell fate from single-cell gene expression profiles in C. elegans. Cell 2009, 139:623-633.
42. Murray J.I., Bao Z., Boyle T.J., Boeck M.E., Mericle B.L., Nicholas T.J., Zhao Z., Sandel M.J., Waterston R.H. Automated analysis of embryonic gene expression with cellular resolution in C. elegans. Nat Methods 2008, 5:703-709.
43. Murray J.I., Bao Z., Boyle T.J., Waterston R.H. The lineaging of fluorescently-labeled Caenorhabditis elegans embryos with StarryNite and AceTree. Nat Protoc 2006, 1:1468-1476.
44. Kornberg R.D., Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 1999, 98:285-294.
45. Valouev A., Ichikawa J., Tonthat T., Stuart J., Ranade S., Peckham H., Zeng K., Malek J.A., Costa G., McKernan K., et al. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res 2008, 18:1051-1063.
46. Kaplan N., Moore I.K., Fondufe-Mittendorf Y., Gossett A.J., Tillo D., Field Y., LeProust E.M., Hughes T.R., Lieb J.D., Widom J., et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458:362-366.
47. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
48. Kolasinska-Zwierz P., Down T., Latorre I., Liu T., Liu X.S., Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 2009, 41:376-381.
49. Ooi S.L., Priess J.R., Henikoff S. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet 2006, 2:e97.
50. Gu S.G., Fire A. Partitioning the C. elegans genome by nucleosome modification, occupancy, and positioning. Chromosoma 2010, 119:73-87.
51. Whittle C.M., McClinic K.N., Ercan S., Zhang X., Green R.D., Kelly W.G., Lieb J.D. The genomic distribution and function of histone variant HTZ-1 during C. elegans embryogenesis. PLoS Genet 2008, 4:e1000187.
52. Liu T., Rechtsteiner A., Egelhofer T.A., Vielle A., Latorre I., Cheung M.S., Ercan S., Ikegami K., Jensen M., Kolasinska-Zwierz P., et al. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 2011, 21:227-236.
53. Barrasa M.I., Vaglio P., Cavasino F., Jacotot L., Walhout A.J. EDGEdb: a transcription factor-DNA interaction database for the analysis of C. elegans differential gene expression. BMC Genomics 2007, 8:21.
54. Deplancke B., Mukhopadhyay A., Ao W., Elewa A.M., Grove C.A., Martinez N.J., Sequerra R., Doucette-Stamm L., Reece-Hoyes J.S., Hope I.A., et al. A gene-centered C. elegans protein-DNA interaction network. Cell 2006, 125:1193-1205.
55. Mukhopadhyay A., Deplancke B., Walhout A.J., Tissenbaum H.A. Chromatin immunoprecipitation (ChIP) coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans. Nat Protoc 2008, 3:698-709.
56. Zhong M., Niu W., Lu Z.J., Sarov M., Murray J.I., Janette J., Raha D., Sheaffer K.L., Lam H.Y., Preston E., et al. 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.
57. van Steensel B., Henikoff S. Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat Biotechnol 2000, 18:424-428.
58. Schuster E., McElwee J.J., Tullet J.M., Doonan R., Matthijssens F., Reece-Hoyes J.S., Hope I.A., Vanfleteren J.R., Thornton J.M., Gems D. DamID in C. elegans reveals longevity-associated targets of DAF-16/FoxO. Mol Syst Biol 2010, 6:399.
59. Oh S.W., Mukhopadhyay A., Dixit B.L., Raha T., Green M.R., Tissenbaum H.A. Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 2006, 38:251-257.
60. Whittle C.M., Lazakovitch E., Gronostajski R.M., Lieb J.D. DNA-binding specificity and in vivo targets of Caenorhabditis elegans nuclear factor I. Proc Natl Acad Sci USA 2009, 106:12049-12054.
61. Lei H., Fukushige T., Niu W., Sarov M., Reinke V., Krause M. A widespread distribution of genomic CeMyoD binding sites revealed and cross validated by ChIP-Chip and ChIP-Seq techniques. PLoS ONE 2010, 5:e15898.
62. Hochbaum D., Zhang Y., Stuckenholz C., Labhart P., Alexiadis V., Martin R., Knölker H.J., Fisher A.L. DAF-12 regulates a connected network of genes to ensure robust developmental decisions. PLoS Genet 2011, 7:e1002179.
63. Niu W., Lu Z.J., Zhong M., Sarov M., Murray J.I., Brdlik C.M., Janette J., Chen C., Alves P., Preston E., et al. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res 2011, 21:245-254.
64. Fukushige T., Brodigan T.M., Schriefer L.A., Waterston R.H., Krause M. Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: evidence for a unified theory of animal muscle development. Genes Dev 2006, 20:3395-3406.
65. Lall S., Grun D., Krek A., Chen K., Wang Y.L., Dewey C.N., Sood P., Colombo T., Bray N., Macmenamin P., et al. A genome-wide map of conserved microRNA targets in C. elegans. Curr Biol 2006, 16:460-471.
66. Zisoulis D.G., Lovci M.T., Wilbert M.L., Hutt K.R., Liang T.Y., Pasquinelli A.E., Yeo G.W. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat Struct Mol Biol 2010, 17:173-179.
67. Barberan-Soler S., Medina P., Estella J., Williams J., Zahler A.M. Co-regulation of alternative splicing by diverse splicing factors in Caenorhabditis elegans. Nucleic Acids Res 2011, 39:666-674.
68. Simonis N., Rual J.F., Carvunis A.R., Tasan M., Lemmens I., Hirozane-Kishikawa T., Hao T., Sahalie J.M., Venkatesan K., Gebreab F., et al. Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat Methods 2009, 6:47-54.
69. Denver D.R., Morris K., Streelman J.T., Kim S.K., Lynch M., Thomas W.K. The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans. Nat Genet 2005, 37:544-548.
70. Raj A., Rifkin S.A., Andersen E., van Oudenaarden A. Variability in gene expression underlies incomplete penetrance. Nature 2010, 463:913-918.
71. Green R.A., Kao H.L., Audhya A., Arur S., Mayers J.R., Fridolfsson H.N., Schulman M., Schloissnig S., Niessen S., Laband K., et al. A high-resolution C. elegans essential gene network based on phenotypic profiling of a complex tissue. Cell 2011, 145:470-482.