A global analysis of genetic interactions in Caenorhabditis elegans

Journal of Biology

Volumn 6, Issue 3, 2007, Pages

  Byrne, Alexandra B ^a,b   Weirauch, Matthew T ^c   Wong, Victoria ^a   Koeva, Martina ^c   Dixon, Scott J ^a,b   Stuart, Joshua M ^c   Roy, Peter J ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c University of California Santa Cruz   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CAENORHABDITIS ELEGANS PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; GENE EXPRESSION; GENE IDENTIFICATION; GENE INTERACTION; GENE TARGETING; GENETIC ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; GENETICS; METABOLISM;

CAENORHABDITIS ELEGANS; METAZOA; PROTOZOA; SACCHAROMYCES CEREVISIAE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; MODELS, GENETIC; RNA INTERFERENCE;

EID: 34848834757     PISSN: 14785854     EISSN: 14754924     Source Type: Journal    
DOI: 10.1186/jbiol58     Document Type: Article

References (86)

1. Functional profiling of the Saccharomyces cerevisiae genome. G Giaever AM Chu L Ni C Connelly L Riles S Veronneau S Dow A Lucau-Danila K Anderson B Andre, Nature 2002 418 387 391 10.1038/nature00935 12140549
2. What does a worm want with 20,000 genes? J Hodgkin, Genome Biol 2001 2 comment2008.1 2008.4 10.1186/gb-2001-2-11-comment2008
3. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. RS Kamath AG Fraser Y Dong G Poulin R Durbin M Gotta A Kanapin N Le Bot S Moreno M Sohrmann, Nature 2003 421 231 237 10.1038/nature01278 12529635
4. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. F Simmer C Moorman AM van der Linden E Kuijk PV van den Berghe RS Kamath AG Fraser J Ahringer RH Plasterk, PLoS Biol 2003 1 e12 14551910 10.1371/journal.pbio.0000012
5. Synthetic enhancement in gene interaction: a genetic tool come of age. L Guarente, Trends Genet 1993 9 362 366 10.1016/0168-9525(93)90042-G 8273152
6. Mechanisms of suppression. PE Hartman JR Roth, Adv Genet 1973 17 1 105 4585532
7. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. EL Ferguson HR Horvitz, Genetics 1989 123 109 121 2806880
8. Caenorhabditis elegans SUR-5, a novel but conserved protein, negatively regulates LET-60 Ras activity during vulval induction. T Gu S Orita M Han, Mol Cell Biol 1998 18 4556 4564 9671465
9. Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. A Colavita JG Culotti, Dev Biol 1998 194 72 85 10.1006/dbio.1997.8790 9473333
10. Functional overlap between the mec-8 gene and five sym genes in Caenorhabditis elegans. AG Davies CA Spike JE Shaw RK Herman, Genetics 1999 153 117 134 10471705
11. Systematic genetic analysis with ordered arrays of yeast deletion mutants. AH Tong M Evangelista AB Parsons H Xu GD Bader N Page M Robinson S Raghibizadeh CW Hogue H Bussey, Science 2001 294 2364 2368 10.1126/science. 1065810 11743205
12. Global mapping of the yeast genetic interaction network. AH Tong G Lesage GD Bader H Ding H Xu X Xin J Young GF Berriz RL Brost M Chang, Science 2004 303 808 813 10.1126/science.1091317 14764870
13. The synthetic genetic interaction spectrum of essential genes. AP Davierwala J Haynes Z Li RL Brost MD Robinson L Yu S Mnaimneh H Ding H Zhu Y Chen, Nature genetics 2005 37 1147 1152 10.1038/ng1640 16155567
14. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. M Schuldiner SR Collins NJ Thompson V Denic A Bhamidipati T Punna J Ihmels B Andrews C Boone JF Greenblatt, Cell 2005 123 507 519 10.1016/j.cell.2005.08.031 16269340
15. A robust toolkit for functional profiling of the yeast genome. X Pan DS Yuan D Xiang X Wang S Sookhai-Mahadeo JS Bader P Hieter F Spencer JD Boeke, Mol Cell 2004 16 487 496 10.1016/j.molcel.2004.09.035 15525520
16. Systematic interpretation of genetic interactions using protein networks. R Kelley T Ideker, Nat Biotechnol 2005 23 561 566 10.1038/nbt1096 15877074
17. The cell as a collection of protein machines: preparing the next generation of molecular biologists. B Alberts, Cell 1998 92 291 294 10.1016/S0092-8674(00)80922-8 9476889
18. From molecular to modular cell biology. LH Hartwell JJ Hopfield S Leibler AW Murray, Nature 1999 402 C47 C52 10.1038/35011540 10591225
19. Pathway redundancy and protein essentiality revealed in the Saccharomyces cerevisiae interaction networks. I Ulitsky R Shamir, Mol Syst Biol 2007 3 104 17437029 10.1038/msb4100144
20. Specific interference by ingested dsRNA. L Timmons A Fire, Nature 1998 395 854 10.1038/27579 9804418
21. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. A Fire S Xu MK Montgomery SA Kostas SE Driver CC Mello, Nature 1998 391 806 811 10.1038/35888 9486653
22. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. AG Fraser RS Kamath P Zipperlen M Martinez-Campos M Sohrmann J Ahringer, Nature 2000 408 325 330 10.1038/35042517 11099033
23. The taxonomy of developmental control in Caenorhabditis elegans. G Ruvkun O Hobert, Science 1998 282 2033 2041 10.1126/science.282.5396.2033 9851920
24. Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. B Lehner C Crombie J Tischler A Fortunato AG Fraser, Nature Genet 2006 38 896 903 10.1038/ng1844 16845399
25. The yeast proteome database (YPD) and Caenorhabditis elegans proteome database (WormPD): comprehensive resources for the organization and comparison of model organism protein information. MC Costanzo JD Hogan ME Cusick BP Davis AM Fancher PE Hodges P Kondu C Lengieza JE Lew-Smith C Lingner, Nucleic Acids Res 2000 28 73 76 10592185 10.1093/nar/28.1.73
26. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. M Ashburner CA Ball JA Blake D Botstein H Butler JM Cherry AP Davis K Dolinski SS Dwight JT Eppig, Nature Genet 2000 25 25 29 10.1038/75556 10802651
27. Modular epistasis in yeast metabolism. D Segre A Deluna GM Church R Kishony, Nature Genet 2005 37 77 83 15592468
28. Genome-wide RNAi screening in Caenorhabditis elegans. RS Kamath J Ahringer, Methods 2003 30 313 321 10.1016/S1046-2023(03)00050-1 12828945
29. Genetics of RAS signaling in C. elegans. PW Sternberg M Han, Trends Genet 1998 14 466 472 10.1016/S0168-9525(98)01592-3 9825675
30. Mechanisms of TGF-β-mediated apoptosis. N Schuster K Krieglstein, Cell Tissue Res 2002 307 1 14 10.1007/s00441-001-0479-6 11810309
31. Transcriptional cooperation between the transforming growth factor-beta and wnt pathways in mammary and intestinal tumorigenesis. E Labbe L Lock A Letamendia AE Gorska R Gryfe S Gallinger HL Moses L Attisano, Cancer Res 2007 67 75 84 10.1158/0008-5472.CAN-06-2559 17210685
32. Gene function prediction from congruent synthetic lethal interactions in yeast. P Ye BD Peyser X Pan JD Boeke FA Spencer JS Bader, Mol Syst Biol 2005 1 2005 0026 16729061
33. Caenorhabditis elegans SOS-1 is necessary for multiple RAS-mediated developmental signals. C Chang NA Hopper PW Sternberg, EMBO J 2000 19 3283 3294 10880441 10.1093/emboj/19.13.3283
34. The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. DM Eisenmann JN Maloof JS Simske C Kenyon SK Kim, Development 1998 125 3667 3680 9716532
35. LET-60 RAS modulates effects of insulin/IGF-1 signaling on development and aging in Caenorhabditis elegans. M Nanji NA Hopper D Gems, Aging Cell 2005 4 235 245 10.1111/j.1474-9726.2005.00166.x 16164423
36. Fibroblast growth factor signaling in Caenorhabditis elegans. CZ Borland JL Schutzman MJ Stern, BioEssays 2001 23 1120 1130 10.1002/bies.10007 11746231
37. A map of the interactome network of the metazoan C. elegans. S Li CM Armstrong N Bertin H Ge S Milstein M Boxem PO Vidalain JD Han A Chesneau T Hao, Science 2004 303 540 543 14704431 10.1126/science.1091403
38. A gene-coexpression network for global discovery of conserved genetic modules. JM Stuart E Segal D Koller SK Kim, Science 2003 302 249 255 10.1126/science.1087447 12934013
39. Predictive models of molecular machines involved in Caenorhabditis elegans early embryogenesis. KC Gunsalus H Ge AJ Schetter DS Goldberg JD Han T Hao GF Berriz N Bertin J Huang LS Chuang, Nature 2005 436 861 865 10.1038/nature03876 16094371
40. A gene expression map for Caenorhabditis elegans. SK Kim J Lund M Kiraly K Duke M Jiang JM Stuart A Eizinger BN Wylie GS Davidson, Science 2001 293 2087 2092 10.1126/science.1061603 11557892
41. BioGRID: a general repository for interaction datasets. C Stark BJ Breitkreutz T Reguly L Boucher A Breitkreutz M Tyers, Nucleic Acids Res 2006 34 Database D535 D539 16381927 10.1093/nar/gkj109
42. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. JF Rual J Ceron J Koreth T Hao AS Nicot T Hirozane-Kishikawa J Vandenhaute SH Orkin DE Hill S van den Heuvel, Genome Res 2004 14 2162 2168 15489339 10.1101/gr.2505604
43. WormBase. http://www.wormbase.org release WS170
44. Genome-wide prediction of C. elegans genetic interactions. W Zhong PW Sternberg, Science 2006 311 1481 1484 10.1126/science.1123287 16527984
45. Integrating interactome, phenome, and transcriptome mapping data for the C. elegans germline. AJ Walhout J Reboul O Shtanko N Bertin P Vaglio H Ge H Lee L Doucette-Stamm KC Gunsalus AJ Schetter, Curr Biol 2002 12 1952 1958 10.1016/S0960-9822(02)01279-4 12445390
46. Nile red: a selective fluorescent stain for intracellular lipid droplets. P Greenspan EP Mayer SD Fowler, J Cell Biol 1985 100 965 973 10.1083/jcb.100.3.965 3972906
47. Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. J Austin J Kimble, Cell 1989 58 565 571 10.1016/0092-8674(89)90437-6 2758467
48. glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. J Yochem I Greenwald, Cell 1989 58 553 563 10.1016/0092-8674(89)90436-4 2758466
49. FGF negatively regulates muscle membrane extension in Caenorhabditis elegans. SJ Dixon M Alexander R Fernandes N Ricker PJ Roy, Development 2006 133 1263 1275 10.1242/dev.02300 16495308
50. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. DL DeVore HR Horvitz MJ Stern, Cell 1995 83 611 620 10.1016/0092-8674(95)90101-9 7585964
51. Modeling human peroxisome biogenesis disorders in the nematode Caenorhabditis elegans. H Thieringer B Moellers G Dodt WH Kunau M Driscoll, J Cell Sci 2003 116 1797 1804 10.1242/jcs.00380 12665560
52. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. K Ashrafi FY Chang JL Watts AG Fraser RS Kamath J Ahringer G Ruvkun, Nature 2003 421 268 272 10.1038/nature01279 12529643
53. Specificity of TGFbeta signaling is conferred by distinct type I receptors and their associated SMAD proteins in Caenorhabditis elegans. S Krishna LL Maduzia RW Padgett, Development 1999 126 251 260 9847239
54. Hypodermal expression of Caenorhabditis elegans TGF-beta type I receptor SMA-6 is essential for the growth and maintenance of body length. S Yoshida K Morita M Mochii N Ueno, Dev Biol 2001 240 32 45 10.1006/dbio.2001.0443 11784045
55. Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. P Narbonne R Roy, Development 2006 133 611 619 10.1242/dev.02232 16407400
56. The TGF-beta signaling pathway is essential for Drosophila oogenesis. V Twombly RK Blackman H Jin JM Graff RW Padgett WM Gelbart, Development 1996 122 1555 1565 8625842
57. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. T Xie AC Spradling, Cell 1998 94 251 260 10.1016/S0092-8674(00)81424-5 9695953
58. Modelling genotype-phenotype relationships and human disease with genetic interaction networks. B Lehner, J Exp Biol 2007 210 1559 1566 10.1242/jeb.002311 17449820
59. Genome sequence of the nematode C. elegans: a platform for investigating biology. The C. elegans Sequencing Consortium, Science 1998 282 2012 2018 10.1126/science.282.5396.2012 9851916
60. Annotation transfer between genomes: protein-protein interologs and protein-DNA regulogs. H Yu NM Luscombe HX Lu X Zhu Y Xia JD Han N Bertin S Chung M Vidal M Gerstein, Genome Res 2004 14 1107 1118 15173116 10.1101/gr.1774904
61. Gene regulatory networks and the evolution of animal body plans. EH Davidson DH Erwin, Science 2006 311 796 800 10.1126/science.1113832 16469913
62. Basic culture methods. JA Lewis JT Fleming, Caenorhabditis elegans: Modern Biological Analysis of an Organism New York: Academic Press, Epstein H, Shakes D, 1995 48 25 26
63. A small-molecule screen in C. elegans yields a new calcium channel antagonist. TC Kwok N Ricker R Fraser AW Chan A Burns EF Stanley P McCourt SR Cutler PJ Roy, Nature 2006 441 91 95 10.1038/nature04657 16672971
64. High-throughput screening of small molecules for bioactivity and target identification in Caenorhabditis elegans. AR Burns TC Kwok A Howard E Houston K Johanson A Chan SR Cutler P McCourt PJ Roy, Nat Protoc 2006 1 1906 1914 10.1038/nprot.2006.283 17487175
65. Cluster analysis and display of genome-wide expression patterns. MB Eisen PT Spellman PO Brown D Botstein, Proc Natl Acad Sci USA 1998 95 14863 14868 9843981 10.1073/pnas.95.25.14863
66. Open source clustering software. MJ de Hoon S Imoto J Nolan S Miyano, Bioinformatics 2004 20 1453 1454 10.1093/bioinformatics/bth078 14871861
67. GO gene association download. http://www.geneontology.org/cgi-bin/GO/ downloadGOGA.pl/gene_association.wb.gz
68. From genomics to chemical genomics: new developments in KEGG. M Kanehisa S Goto M Hattori KF Aoki-Kinoshita M Itoh S Kawashima T Katayama M Araki M Hirakawa, Nucleic Acids Res 2006 34 Database D354 D357 16381885 10.1093/nar/gkj102
69. KEGG pathway data for C. elegans download. ftp://ftp.genome.ad.jp/pub/ kegg/pathway/organisms/cel
70. Munich Information Center for Protein Sequences (MIPS). http://mips.gsf.de
71. BioCarta. http://www.biocarta.com/genes/index.asp
72. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman, Nucleic Acids Res 1997 25 3389 3402 9254694 10.1093/nar/25.17.3389
73. The tYNA platform for comparative interactomics: a web tool for managing, comparing and mining multiple networks. KY Yip H Yu PM Kim M Schultz M Gerstein, Bioinformatics 2006 22 2968 2970 10.1093/bioinformatics/btl488 17021160
74. Mining coherent dense subgraphs across massive biological networks for functional discovery. H Hu X Yan Y Huang J Han XJ Zhou, Bioinformatics 2005 21 Suppl 1 i213 i221 10.1093/bioinformatics/bti1049 15961460
75. Comparative analysis of multiple genome-scale data sets. M Werner-Washburne B Wylie K Boyack E Fuge J Galbraith J Weber G Davidson, Genome Res 2002 12 1564 1573 12368249 10.1101/gr.225402
76. SGI Additional data files. http://sysbio.cse.ucsc.edu/Projects/WormSga/ supplemental.html
77. let-756, a C. elegans fgf essential for worm development. R Roubin K Naert C Popovici G Vatcher F Coulier J Thierry-Mieg P Pontarotti D Birnbaum D Baillie D Thierry-Mieg, Oncogene 1999 18 6741 6747 10.1038/sj.onc.1203074 10597282
78. Alternative splicing affecting a novel domain in the C. elegans EGL-15 FGF receptor confers functional specificity. SJ Goodman CS Branda MK Robinson RD Burdine MJ Stern, Development 2003 130 3757 3766 10.1242/dev.00604 12835392
79. Extracellular domain determinants of LET-23 (EGF) receptor tyrosine kinase activity in Caenorhabditis elegans. N Moghal PW Sternberg, Oncogene 2003 22 5471 5480 10.1038/sj.onc.1206648 12934107
80. Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. HR Horvitz JE Sulston, Genetics 1980 96 435 454 7262539
81. The let-60 locus controls the switch between vulval and nonvulval cell fates in Caenorhabditis elegans. M Han RV Aroian PW Sternberg, Genetics 1990 126 899 913 2076820
82. let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein. M Han PW Sternberg, Cell 1990 63 921 931 10.1016/0092-8674(90)90495-Z 2257629
83. Genetic screen for small body size mutants in C. elegans reveals many TGFbeta pathway components. C Savage-Dunn LL Maduzia CM Zimmerman AF Roberts S Cohen R Tokarz RW Padgett, Genesis 2003 35 239 247 10.1002/gene.10184 12717735
84. MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. S Ahmed J Hodgkin, Nature 2000 403 159 164 10.1038/35003120 10646593
85. Cytoscape: a software environment for integrated models of biomolecular interaction networks. P Shannon A Markiel O Ozier NS Baliga JT Wang D Ramage N Amin B Schwikowski T Ideker, Genome Res 2003 13 2498 2504 14597658 10.1101/gr.1239303
86. Towards zoomable multidimensional maps of the cell. Z Hu J Mellor J Wu M Kanehisa JM Stuart C Delisi, Nat Biotechnol 2007 25 547 554 10.1038/nbt1304 17483841