The LIN-15A and LIN-56 transcriptional regulators interact to negatively regulate EGF/Ras signaling in Caenorhabditis elegans vulval cell-fate determination

Genetics

Volumn 187, Issue 3, 2011, Pages 803-815

  Davison, Ewa M ^a   Saffer, Adam M ^a   Huang, Linda S ^b,c   DeModena, John ^b   Sternberg, Paul W ^b   Horvitz, H Robert ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; PROTEIN MYB; RAS PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LIN 15A; TRANSCRIPTION FACTOR LIN 56; TRANSCRIPTION FACTOR LIN 8; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL FATE; CHROMATIN ASSEMBLY AND DISASSEMBLY; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EPIDERMAL GROWTH FACTOR; FEMALE; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; MOLECULAR SEQUENCE DATA; RAS PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VULVA;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 79953216029     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.124487     Document Type: Article

References (85)

1. ANDERSEN, E. C., and H. R. HORVITZ, 2007 Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development. Development 134: 2991-2999.
2. ANDERSEN, E. C., A. M. SAFFER and H. R. HORVITZ, 2008 Multiple levels of redundant processes inhibit Caenorhabditis elegans vulval cell fates. Genetics 179: 2001-2012.
3. AROIAN, R. V.,M.KOGA, J. E. MENDEL, Y. OHSHIMA andP. W. STERNBERG, 1990 The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily. Nature 348: 693-699.
4. BEITEL, G. J., S. G. CLARK and H. R. HORVITZ, 1990 Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction. Nature 348: 503-509.
5. BEITEL, G. J., E. J. LAMBIE and H. R. HORVITZ, 2000 The C. elegans gene lin-9, which acts in an Rb-related pathway, is required for gonadal sheath cell development and encodes a novel protein. Gene 254: 253-263.
6. BELFIORE, M., L. D. MATHIES, P. PUGNALE, G.MOULDER, R. BARSTEAD et al., 2002 The MEP-1 zinc-finger protein acts withMOGDEAH box proteins to control gene expression via the fem-3 3′ untranslated region in Caenorhabditis elegans. RNA 8: 725-739.
7. BLUMENTHAL, T., D. EVANS, C.D. LINK, A. GUFFANTI, D.LAWSON et al., 2002 A global analysis of Caenorhabditis elegans operons. Nature 417: 851-854.
8. BOXEM, M., and S. VAN DEN HEUVEL, 2002 C. elegans class B synthetic multivulva genes act in G(1) regulation. Curr. Biol. 12: 906-911.
9. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
10. CAYROL, C., C. LACROIX, C. MATHE, V. ECOCHARD, M.CERIBELLI et al., 2007 The THAP-zinc finger protein THAP1 regulates endothelial cell proliferation through modulation of pRB/E2F cell-cycle target genes. Blood 109: 584-594.
11. CEOL, C. J., and H. R. HORVITZ, 2001 dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol. Cell 7: 461-473.
12. CEOL, C. J., and H. R. HORVITZ, 2004 A new class of C. elegans syn-Muv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling. Dev. Cell 6: 563-576.
13. CHEN, F., B. M. HERSH, B. CONRADT, Z. ZHOU, D. RIEMER et al., 2000 Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death. Science 287: 1485-1489.
14. CLARK, S. G., X. LU and H. R. HORVITZ, 1994 The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137: 987-997.
15. CLASSON, M., and E. HARLOW, 2002 The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2: 910-917.
16. CLOUAIRE, T., M. ROUSSIGNE, V. ECOCHARD, C. MATHE, F. AMALRIC et al., 2005 The THAP domain of THAP1 is a large C2CH module with zinc-dependent sequence-specific DNA-binding activity. Proc. Natl. Acad. Sci. USA 102: 6907-6912.
17. COUTEAU, F., F. GUERRY, F. MULLER and F. PALLADINO, 2002 A heterochromatin protein 1 homologue in Caenorhabditis elegans acts in germline and vulval development. EMBO Rep. 3: 235-241.
18. CUI, M., J. CHEN, T. R. MYERS, B. J. HWANG, P. W. STERNBERG et al., 2006 SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans. Dev. Cell 10: 667-672.
19. DAVISON, E.M.,M.M. HARRISON, A. J. WALHOUT, M. VIDAL and H. R. HORVITZ, 2005 lin-8, which antagonizes Caenorhabditis elegans Ras-mediated vulval induction, encodes a novel nuclear protein that interacts with the LIN-35 Rb protein. Genetics 171: 1017-1031.
20. DOWNWARD, J., 2003 Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3: 11-22.
21. DUFOURCQ, P., M. VICTOR, F. GAY, D. CALVO, J. HODGKIN et al., 2002 Functional requirement for histone deacetylase 1 in Cae-norhabditis elegans gonadogenesis. Mol. Cell. Biol. 22: 3024-3034.
22. FAY, D. S., S. KEENAN and M. HAN, 2002 fzr-1 and lin-35/Rb function redundantly to control cell proliferation in C. elegans as revealed by a nonbiased synthetic screen. Genes Dev. 16: 503-517.
23. FERGUSON, E. L., and H. R. HORVITZ, 1985 Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110: 17-72.
24. FERGUSON, E. L., and H. R. HORVITZ, 1989 The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics 123: 109-121.
25. FERGUSON, E. L., P. W. STERNBERG and H. R. HORVITZ, 1987 A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans. Nature 326: 259-267.
26. FIELDS, S., and O. SONG, 1989 A novel genetic system to detect protein-protein interactions. Nature 340: 245-246.
27. FINNEY, M., and G. RUVKUN, 1990 The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63: 895-905.
28. FIRE, A., S. XU, M. K. MONTGOMERY, S. A. KOSTAS, S. E. DRIVER et al., 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
29. FRANCIS, R., and R. H. WATERSTON, 1991 Muscle cell attachment in Caenorhabditis elegans. J. Cell Biol. 114: 465-479.
30. GRUENBAUM, Y., K. K. LEE, J. LIU, M. COHEN and K. L. WILSON, 2002 The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J. Cell Sci. 115: 923-929.
31. GUENTHER, C., and G. GARRIGA, 1996 Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates. Development 122: 3509-3518.
32. HAN, M., and P. W. STERNBERG, 1990 let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein. Cell 63: 921-931.
33. HARLOW, E., and D. LANE, 1988 Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. HARRISON, M. M., C. J. CEOL, X. LU and H. R. HORVITZ, 2006 Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex. Proc. Natl. Acad. Sci. USA 103: 16782-16787.
35. HARRISON, M. M., X. LU and H. R. HORVITZ, 2007 LIN-61, one of two Caenorhabditis elegans malignant-brain-tumor-repeat-containing proteins, acts with the DRM and NuRD-like protein complexes in vulval development but not in certain other biological processes. Genetics 176: 255-271.
36. HEID, C. A., J. STEVENS, K. J. LIVAK and P. M. WILLIAMS, 1996 Real time quantitative PCR. Genome Res. 6: 986-994.
37. HILL, R. J., and P. W. STERNBERG, 1992 The gene lin-3 encodes an inductive signal for vulval development in C. elegans. Nature 358: 470-476.
38. HORVITZ, H. R., and J. E. SULSTON, 1980 Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics 96: 435-454.
39. HSIEH, J., J. LIU, S. A. KOSTAS, C. CHANG, P. W. STERNBERG et al., 1999 The RING finger/B-box factor TAM-1 and a retinoblastoma-like protein LIN-35 modulate context-dependent gene silencing in Caenorhabditis elegans. Genes Dev. 13: 2958-2970.
40. HUANG, L. S., P. TZOU and P. W. STERNBERG, 1994 The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. Mol. Biol. Cell 5: 395-411.
41. HWANG, H. Y., and H. R. HORVITZ, 2002 The Caenorhabditis elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated. Proc. Natl. Acad. Sci. USA 99: 14224-14229.
42. HWANG, B. J., H. M. MULLER and P. W. STERNBERG, 2004 Genome annotation by high-throughput 5′ RNA end determination. Proc. Natl. Acad. Sci. USA 101: 1650-1655.
43. KAMATH, R. S., M.MARTINEZ-CAMPOS, P. ZIPPERLEN, A.G. FRASER and J. AHRINGER, 2001 Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2: RESEARCH0002.
44. KAMATH, R. S., A. G. FRASER, Y. DONG, G. POULIN, R. DURBIN et al., 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
45. KATZ, W. S., G. M. LESA, D. YANNOUKAKOS, T. R. CLANDININ, J. SCHLESSINGER et al., 1996 A point mutation in the extracellular domain activates LET-23, the Caenorhabditis elegans epidermal growth factor receptor homolog. Mol. Cell. Biol. 16: 529-537.
46. KNOEPFLER, P. S., and R. N. EISENMAN, 1999 Sin meets NuRD and other tails of repression. Cell 99: 447-450.
47. KOELLE,M. R., and H. R. HORVITZ, 1996 EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115-125.
48. KORENJAK, M., B. TAYLOR-HARDING, U. K. BINNE, J. S. SATTERLEE, O. STEVAUX et al., 2004 Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119: 181-193.
49. KORNFELD, K., 1997 Vulval development in Caenorhabditis elegans. Trends Genet. 13: 55-61.
50. KORNFELD, K., K. L. GUAN and H. R. HORVITZ, 1995 The Caenorhabditis elegans gene mek-2 is required for vulval induction and encodes a protein similar to the protein kinase MEK. Genes Dev. 9: 756-768.
51. KRISHNA, S. S., I.MAJUMDAR and N. V. GRISHIN, 2003 Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 31: 532-550.
52. LACKNER, M. R., K. KORNFELD, L. M. MILLER, H. R. HORVITZ and S. K. KIM, 1994 A MAP kinase homolog, mpk-1, is involved in ras-mediated induction of vulval cell fates in Caenorhabditis elegans. Genes Dev. 8: 160-173.
53. LAITY, J. H., B. M. LEE and P. E. WRIGHT, 2001 Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11: 39-46.
54. LEWIS, P. W., E. L. BEALL, T. C. FLEISCHER, D. GEORLETTE, A. J. LINK et al., 2004 Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev. 18: 2929-2940.
55. LITOVCHICK, L., S. SADASIVAM, L. FLORENS, X. ZHU, S. K. SWANSON et al., 2007 Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26: 539-551.
56. LIU, J., T. ROLEF BEN-SHAHAR, D. RIEMER, M. TREININ, P. SPANN et al., 2000 Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell 11: 3937-3947.
57. LU, X., and H. R. HORVITZ, 1998 lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell 95: 981-991.
58. MELENDEZ, A., and I. GREENWALD, 2000 Caenorhabditis elegans lin-13, a member of the LIN-35 Rb class of genes involved in vulval development, encodes a protein with zinc fingers and an LXCXE motif. Genetics 155: 1127-1137.
59. MELLO, C. C., J. M. KRAMER, D. STINCHCOMB and V. AMBROS, 1991 Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10: 3959-3970.
60. MOGHAL, N., and P. W. STERNBERG, 2003 The epidermal growth factor system in Caenorhabditis elegans. Exp. Cell Res. 284: 150-159.
61. NEVINS, J. R., 2001 The Rb/E2F pathway and cancer. Hum. Mol. Genet. 10: 699-703.
62. NIELSEN, S. J.,R. SCHNEIDER,U. M. BAUER, A. J. BANNISTER, A.MORRISON et al., 2001 Rb targets histone H3 methylation and HP1 to promoters. Nature 412: 561-565.
63. NORMANNO, N., C. BIANCO, A. DE LUCA and D. S. SALOMON, 2001 The role of EGF-related peptides in tumor growth. Front. Biosci. 6: D685-D707.
64. NORMANNO, N., A. DE LUCA, C.BIANCO, L. STRIZZI, M.MANCINO et al., 2006 Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366: 2-16.
65. PILKINTON, M., R. SANDOVAL and O. R. COLAMONICI, 2007 Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex. Oncogene 26: 7535-7543.
66. POULIN, G., Y. DONG, A. G. FRASER, N. A. HOPPER and J. AHRINGER, 2005 Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans. EMBO J. 24: 2613-2623.
67. REDDY, K. C., and A. M. VILLENEUVE, 2004 C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118: 439-452.
68. RICHARDS, E. J., and S. C. ELGIN, 2002 Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108: 489-500.
69. RIDDLE, D. L., 1997 C. Elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
70. RIDDLE, D. L., T. BLUMENTHAL, B. J. MEYER and J. R. PRIESS, 1997 C. elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
71. ROUSSIGNE, M., S. KOSSIDA, A. C. LAVIGNE, T. CLOUAIRE, V. ECOCHARD et al., 2003 The THAP domain: a novel protein motif with similarity to the DNA-binding domain of P element transposase. Trends Biochem. Sci. 28: 66-69.
72. SABOGAL, A., A. Y. LYUBIMOV, J. E. CORN, J. M. BERGER and D. C. RIO, 2010 THAP proteins target specific DNA sites through bipartite recognition of adjacent major and minor grooves. Nat. Struct. Mol. Biol. 17: 117-123.
73. SAMBROOK, J., E. F. FRITSCH and J. SAMBROOK, 1989 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
74. SCHMIT, F., M. KORENJAK, M. MANNEFELD, K. SCHMITT, C. FRANKE et al., 2007 LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6: 1903-1913.
75. SIGURDSON, D. C.,G. J. SPANIER andR. K. HERMAN, 1984 Caenorhabditis elegans deficiency mapping. Genetics 108: 331-345.
76. SOLARI, F., and J. AHRINGER, 2000 NURD-complex genes antagonise Ras-induced vulval development in Caenorhabditis elegans. Curr. Biol. 10: 223-226.
77. THOMAS, J. H., C. J. CEOL, H. T. SCHWARTZ and H. R. HORVITZ, 2003 New genes that interact with lin-35 Rb to negatively regulate the let-60 ras pathway in Caenorhabditis elegans. Genetics 164: 135-151.
78. TIMMONS, L., D. L. COURT and A. FIRE, 2001 Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.
79. UNHAVAITHAYA, Y., T. H. SHIN, N. MILIARAS, J. LEE, T. OYAMA et al., 2002 MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans. Cell 111: 991-1002.
80. VANDEL, L., E. NICOLAS, O. VAUTE, R. FERREIRA, S. AIT-SI-ALI et al., 2001 Transcriptional repression by the retinoblastoma protein through the recruitment of a histone methyltransferase. Mol. Cell. Biol. 21: 6484-6494.
81. VON ZELEWSKY, T., F. PALLADINO, K. BRUNSCHWIG, H. TOBLER, A. HAJNAL et al., 2000 The C. elegans Mi-2 chromatin-remodelling proteins function in vulval cell fate determination. Development 127: 5277-5284.
82. WALHOUT, A. J., R. SORDELLA, X. LU, J. L. HARTLEY, G. F. TEMPLE et al., 2000a Protein interaction mapping in C. elegans using proteins involved in vulval development. Science 287: 116-122.
83. WALHOUT, A. J., G. F. TEMPLE, M. A. BRASCH, J. L. HARTLEY, M. A. LORSON et al., 2000b GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol. 328: 575-592.
84. WU, Y., M. HAN and K. L. GUAN, 1995 MEK-2, a Caenorhabditis elegans MAP kinase kinase, functions in Ras-mediated vulval induction and other developmental events. Genes Dev. 9: 742-755.
85. ZHANG, H. S., and D. C. DEAN, 2001 Rb-mediated chromatin structure regulation and transcriptional repression. Oncogene 20: 3134-3138.