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PMID: 17434473 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

The SynMuv genes of Caenorhabditis elegans in vulval development and beyond.

Developmental biology ·Vol. 306 ·No. 1 ·2007-06-01 ·Pages 1-9

Fay DS, Yochem J

Abstract

For a nonessential diminutive organ comprised of only 22 nuclei, the Caenorhabditis elegans vulva has done very well for itself. The status of the vulva as an overachiever is in part due to its inherent structural simplicity as well as to the intricate regulation of its induction and development. Studies over the past twenty years have shown the vulva to be a microcosm for organogenesis and a model for the integration of complex signaling pathways. Furthermore, many of these signaling molecules are themselves associated with cancer in mammals. This review focuses on what is perhaps the most intriguing and complex story to emerge from these studies thus far, the role of the Synthetic Multivulval (SynMuv) genes in controlling vulval cell-fate adoption. Recent advances have led to a greater mechanistic understanding of how these genes function during vulval development and have also identified roles for these genes in diverse developmental processes.

MeSH Terms
Animals Caenorhabditis elegans/anatomy & histology,genetics,growth & development Female Gene Expression Regulation, Developmental Genes, Helminth/genetics,physiology Organogenesis/genetics Ovum Transcription, Genetic Vulva/anatomy & histology,growth & development
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Fay David S
University of Wyoming, College of Agriculture, Department of Molecular Biology, Dept 3944, 1000 E. University Avenue, Laramie, WY 82071, USA. davidfay@uwyo.edu <davidfay@uwyo.edu>
Yochem John
References (75)
75 references, click to expand
  1. The Rb/E2F pathway: expanding roles and emerging paradigms.
    Genes Dev. 2000 Oct 1;14(19):2393-409 PMID: 11018009
  2. The C. elegans Mi-2 chromatin-remodelling proteins function in vulval cell fate determination.
    Development. 2000 Dec;127(24):5277-84 PMID: 11076750
  3. Transcription of meiotic cell cycle and terminal differentiation genes depends on a conserved chromatin associated protein, whose nuclear localisation is regulated.
    Development. 2000 Dec;127(24):5463-73 PMID: 11076766
  4. The C. elegans E2F- and DP-related proteins are required for embryonic asymmetry and negatively regulate Ras/MAPK signaling.
    Mol Cell. 2001 Mar;7(3):451-60 PMID: 11463371
  5. Abnormal cell lineages in mutants of the nematode Caenorhabditis elegans.
    Dev Biol. 1981 Feb;82(1):41-55 PMID: 7014288
  6. Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans.
    Genetics. 1980 Oct;96(2):435-54 PMID: 7262539
  7. SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans.
    Dev Cell. 2006 May;10(5):667-72 PMID: 16678779
  8. Cellular functions of TIP60.
    Int J Biochem Cell Biol. 2006;38(9):1496-509 PMID: 16698308
  9. Diverse chromatin remodeling genes antagonize the Rb-involved SynMuv pathways in C. elegans.
    PLoS Genet. 2006 May;2(5):e74 PMID: 16710447
  10. Identification and classification of genes that act antagonistically to let-60 Ras signaling in Caenorhabditis elegans vulval development.
    Genetics. 2006 Jun;173(2):709-26 PMID: 16624904
  11. C. elegans ISWI and NURF301 antagonize an Rb-like pathway in the determination of multiple cell fates.
    Development. 2006 Jul;133(14):2695-704 PMID: 16774993
  12. A mutant allele of BARA/LIN-9 rescues the cdk4-/- phenotype by releasing the repression on E2F-regulated genes.
    Exp Cell Res. 2006 Aug 1;312(13):2465-75 PMID: 16730350
  13. RB and cell cycle progression.
    Oncogene. 2006 Aug 28;25(38):5220-7 PMID: 16936740
  14. Rb family proteins as modulators of gene expression and new aspects regarding the interaction with chromatin remodeling enzymes.
    Oncogene. 2006 Aug 28;25(38):5263-7 PMID: 16936746
  15. The C. elegans HP1 homologue HPL-2 and the LIN-13 zinc finger protein form a complex implicated in vulval development.
    Dev Biol. 2006 Sep 15;297(2):308-22 PMID: 16890929
  16. dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development.
    Mol Cell. 2001 Mar;7(3):461-73 PMID: 11463372
  17. lin-35 Rb and cki-1 Cip/Kip cooperate in developmental regulation of G1 progression in C. elegans.
    Development. 2001 Nov;128(21):4349-59 PMID: 11684669
  18. As good as they get: cells in nematode vulva development and evolution.
    Curr Opin Cell Biol. 2001 Dec;13(6):715-20 PMID: 11698187
  19. Role of C. elegans lin-40 MTA in vulval fate specification and morphogenesis.
    Development. 2001 Dec;128(23):4911-21 PMID: 11731470
  20. Egg-laying defective mutants of the nematode Caenorhabditis elegans.
    Genetics. 1983 Aug;104(4):619-47 PMID: 11813735
  21. fzr-1 and lin-35/Rb function redundantly to control cell proliferation in C. elegans as revealed by a nonbiased synthetic screen.
    Genes Dev. 2002 Feb 15;16(4):503-17 PMID: 11850412
  22. A heterochromatin protein 1 homologue in Caenorhabditis elegans acts in germline and vulval development.
    EMBO Rep. 2002 Mar;3(3):235-41 PMID: 11850401
  23. C. elegans class B synthetic multivulva genes act in G(1) regulation.
    Curr Biol. 2002 Jun 4;12(11):906-11 PMID: 12062054
  24. The RB and p53 pathways in cancer.
    Cancer Cell. 2002 Aug;2(2):103-12 PMID: 12204530
  25. LIN-39/Hox triggers cell division and represses EFF-1/fusogen-dependent vulval cell fusion.
    Genes Dev. 2002 Dec 15;16(24):3136-41 PMID: 12502736
  26. MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans.
    Cell. 2002 Dec 27;111(7):991-1002 PMID: 12507426
  27. New genes that interact with lin-35 Rb to negatively regulate the let-60 ras pathway in Caenorhabditis elegans.
    Genetics. 2003 May;164(1):135-51 PMID: 12750327
  28. lin-35/Rb and ubc-18, an E2 ubiquitin-conjugating enzyme, function redundantly to control pharyngeal morphogenesis in C. elegans.
    Development. 2003 Jul;130(14):3319-30 PMID: 12783801
  29. A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling.
    Dev Cell. 2004 Apr;6(4):563-76 PMID: 15068795
  30. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression.
    J Cell Sci. 2004 May 1;117(Pt 11):2173-81 PMID: 15126619
  31. The coordinate regulation of pharyngeal development in C. elegans by lin-35/Rb, pha-1, and ubc-18.
    Dev Biol. 2004 Jul 1;271(1):11-25 PMID: 15196946
  32. lin-35/Rb cooperates with the SWI/SNF complex to control Caenorhabditis elegans larval development.
    Genetics. 2004 Jul;167(3):1177-85 PMID: 15280233
  33. lin-35/Rb and xnp-1/ATR-X function redundantly to control somatic gonad development in C. elegans.
    Dev Biol. 2004 Sep 15;273(2):335-49 PMID: 15328017
  34. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms?
    Genes Dev. 2004 Sep 1;18(17):2046-59 PMID: 15342487
  35. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes.
    Cell. 2004 Oct 15;119(2):181-93 PMID: 15479636
  36. Alterations in ribosome biogenesis cause specific defects in C. elegans hermaphrodite gonadogenesis.
    Dev Biol. 2006 Oct 1;298(1):45-58 PMID: 16876152
  37. The PLZF-like protein TRA-4 cooperates with the Gli-like transcription factor TRA-1 to promote female development in C. elegans.
    Dev Cell. 2006 Oct;11(4):561-73 PMID: 17011494
  38. 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 U S A. 2006 Nov 7;103(45):16782-7 PMID: 17075059
  39. The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis.
    EMBO J. 2007 Jan 10;26(1):144-57 PMID: 17159899
  40. lin-35/Rb and the CoREST ortholog spr-1 coordinately regulate vulval morphogenesis and gonad development in C. elegans.
    Dev Biol. 2007 Feb 15;302(2):448-62 PMID: 17070797
  41. Vulval development.
    WormBook. 2005;:1-28 PMID: 18050418
  42. A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans.
    Nature. 1987 Mar 19-25;326(6110):259-67 PMID: 2881214
  43. Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans.
    Genetics. 1985 May;110(1):17-72 PMID: 3996896
  44. Pattern formation during vulval development in C. elegans.
    Cell. 1986 Mar 14;44(5):761-72 PMID: 3753901
  45. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways.
    Genetics. 1989 Sep;123(1):109-21 PMID: 2806880
  46. Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis.
    Nature. 1990 Nov 8;348(6297):169-71 PMID: 2234080
  47. Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction.
    Nature. 1990 Dec 6;348(6301):503-9 PMID: 2123303
  48. let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein.
    Cell. 1990 Nov 30;63(5):921-31 PMID: 2257629
  49. The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily.
    Nature. 1990 Dec 20-27;348(6303):693-9 PMID: 1979659
  50. The gene lin-3 encodes an inductive signal for vulval development in C. elegans.
    Nature. 1992 Aug 6;358(6386):470-6 PMID: 1641037
  51. The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development.
    Mol Biol Cell. 1994 Apr;5(4):395-411 PMID: 8054684
  52. The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins.
    Genetics. 1994 Aug;137(4):987-97 PMID: 7982579
  53. The ncl-1 gene and genetic mosaics of Caenorhabditis elegans.
    Genetics. 1995 Nov;141(3):989-1006 PMID: 8582642
  54. Caenorhabditis elegans HOM-C genes regulate the response of vulval precursor cells to inductive signal.
    Dev Biol. 1997 Feb 1;182(1):150-61 PMID: 9073457
  55. The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling.
    Development. 1998 Jan;125(2):181-90 PMID: 9486792
  56. 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. 1998 Dec 23;95(7):981-91 PMID: 9875852
  57. The C. elegans gene lin-36 acts cell autonomously in the lin-35 Rb pathway.
    Development. 1999 Aug;126(15):3449-59 PMID: 10393123
  58. Inhibition of oncogenic transformation by mammalian Lin-9, a pRB-associated protein.
    EMBO J. 2004 Nov 24;23(23):4627-38 PMID: 15538385
  59. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex.
    Genes Dev. 2004 Dec 1;18(23):2929-40 PMID: 15545624
  60. synMuv verite--Myb comes into focus.
    Genes Dev. 2004 Dec 1;18(23):2837-44 PMID: 15574590
  61. lin-35 Rb acts in the major hypodermis to oppose ras-mediated vulval induction in C. elegans.
    Dev Cell. 2005 Jan;8(1):117-23 PMID: 15621535
  62. XNP-1/ATR-X acts with RB, HP1 and the NuRD complex during larval development in C. elegans.
    Dev Biol. 2005 Feb 1;278(1):49-59 PMID: 15649460
  63. FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans.
    Cell. 2005 Jun 17;121(6):951-62 PMID: 15960981
  64. An inversion in the wiring of an intercellular signal: evolution of Wnt signaling in the nematode vulva.
    Bioessays. 2005 Aug;27(8):765-9 PMID: 16015606
  65. Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans.
    EMBO J. 2005 Jul 20;24(14):2613-23 PMID: 15990876
  66. Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants.
    Nature. 2005 Jul 28;436(7050):593-7 PMID: 16049496
  67. The love-hate relationship between Ras and Notch.
    Genes Dev. 2005 Aug 15;19(16):1825-39 PMID: 16103211
  68. Something about SUMO inhibits transcription.
    Curr Opin Genet Dev. 2005 Oct;15(5):536-41 PMID: 16095902
  69. lin-8, which antagonizes Caenorhabditis elegans Ras-mediated vulval induction, encodes a novel nuclear protein that interacts with the LIN-35 Rb protein.
    Genetics. 2005 Nov;171(3):1017-31 PMID: 16020796
  70. gon-14 functions with class B and class C synthetic multivulva genes to control larval growth in Caenorhabditis elegans.
    Genetics. 2006 Feb;172(2):915-28 PMID: 16322520
  71. Loss of LIN-35, the Caenorhabditis elegans ortholog of the tumor suppressor p105Rb, results in enhanced RNA interference.
    Genome Biol. 2006;7(1):R4 PMID: 16507136
  72. 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. 1999 Nov 15;13(22):2958-70 PMID: 10580003
  73. NURD-complex genes antagonise Ras-induced vulval development in Caenorhabditis elegans.
    Curr Biol. 2000 Feb 24;10(4):223-6 PMID: 10704416
  74. 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. 2000 Jul;155(3):1127-37 PMID: 10880475
  75. 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. 2000 Aug 22;254(1-2):253-63 PMID: 10974557
Article Info
Journal
Developmental biology
Abbr.
Dev Biol
ISSN
0012-1606
Published
2007-06-01
Epub
2007-00-20
Pages
1-9
Language
English
Region
United States
NLM ID
0372762
PMCID
PMC1955466
Subset
IM
Grants
NIGMS NIH HHS · R01 GM066868 · United States
NIGMS NIH HHS · R01 GM066868-03 · United States
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