Abstract
Cell fusion is fundamental for reproduction and organ formation. Fusion between most C. elegans epithelial cells is mediated by the EFF-1 fusogen. However, fusion between the anchor cell and the utse syncytium that establishes a continuous uterine-vulval tube proceeds normally in eff-1 mutants. By isolating mutants where the anchor-cell fails to fuse, we identified aff-1. AFF-1 ectopic expression results in fusion of cells that normally do not fuse in C. elegans. The fusogen activity of AFF-1 was further confirmed by its ability to fuse heterologous cells. AFF-1 and EFF-1 differ in their fusogenic activity and expression patterns but share eight conserved predicted disulfide bonds in their ectodomains, including a putative TGF-beta-type-I-Receptor domain. We found that FOS-1, the Fos transcription factor ortholog that controls anchor-cell invasion during nematode development, is a specific activator of aff-1-mediated anchor-cell fusion. Thus, FOS-1 links cell invasion and fusion in a developmental cascade.
MeSH Terms
Amino Acid Sequence
Animals
Caenorhabditis elegans/cytology,embryology,metabolism
Caenorhabditis elegans Proteins/chemistry,metabolism
Cell Fusion
Cytoplasm/metabolism
Embryo, Nonmammalian/cytology
Epithelial Cells/cytology
Female
Insecta/cytology
Models, Biological
Molecular Sequence Data
Mutation/genetics
Phenotype
Proto-Oncogene Proteins c-fos/chemistry,metabolism
Transcription Factors/chemistry,metabolism
Vulva/cytology,growth & development
Chemicals
AFF-1 protein, C elegans
Caenorhabditis elegans Proteins
FOS-1 protein, C elegans
Proto-Oncogene Proteins c-fos
Transcription Factors
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Sapir Amir
Department of Biology, Technion-Israel Institute of Technology, Haifa 32000, Israel.
Choi Jaebok
Leikina Evgenia
Avinoam Ori
Valansi Clari
Chernomordik Leonid V
Newman Anna P
Podbilewicz Benjamin
References (31)
31 references, click to expand
-
Anchor cell invasion into the vulval epithelium in C. elegans.
Dev Cell. 2003 Jul;5(1):21-31
PMID: 12852849
-
The EGL-13 SOX domain transcription factor affects the uterine pi cell lineages in Caenorhabditis elegans.
Genetics. 2003 Nov;165(3):1623-8
PMID: 14668410
-
The Jalview Java alignment editor.
Bioinformatics. 2004 Feb 12;20(3):426-7
PMID: 14960472
-
EFF-1 is sufficient to initiate and execute tissue-specific cell fusion in C. elegans.
Curr Biol. 2004 Sep 7;14(17):1587-91
PMID: 15341747
-
The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans.
Genes Dev. 2004 Oct 1;18(19):2380-91
PMID: 15466489
-
The genetics of Caenorhabditis elegans.
Genetics. 1974 May;77(1):71-94
PMID: 4366476
-
cis-Regulatory control of three cell fate-specific genes in vulval organogenesis of Caenorhabditis elegans and C. briggsae.
Dev Biol. 2003 May 1;257(1):85-103
PMID: 12710959
-
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
-
The type I membrane protein EFF-1 is essential for developmental cell fusion.
Dev Cell. 2002 Mar;2(3):355-62
PMID: 11879640
-
Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans.
Gene. 2001 Jan 24;263(1-2):103-12
PMID: 11223248
-
The Caenorhabditis elegans heterochronic gene lin-29 coordinates the vulval-uterine-epidermal connections.
Curr Biol. 2000 Nov 30;10(23):1479-88
PMID: 11114514
-
The lin-11 LIM domain transcription factor is necessary for morphogenesis of C. elegans uterine cells.
Development. 1999 Dec;126(23):5319-26
PMID: 10556057
-
Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegans.
Dev Biol. 1981 Oct 30;87(2):286-300
PMID: 7286433
-
Pattern formation during vulval development in C. elegans.
Cell. 1986 Mar 14;44(5):761-72
PMID: 3753901
-
Cell autonomy of lin-12 function in a cell fate decision in C. elegans.
Cell. 1989 Jun 30;57(7):1237-45
PMID: 2736627
-
A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion.
Cell. 1993 Nov 5;75(3):409-18
PMID: 8221884
-
Cell fusions in the developing epithelial of C. elegans.
Dev Biol. 1994 Feb;161(2):408-24
PMID: 8313992
-
Implantation and the placenta: key pieces of the development puzzle.
Science. 1994 Dec 2;266(5190):1508-18
PMID: 7985020
-
The Caenorhabditis elegans lin-12 gene mediates induction of ventral uterine specialization by the anchor cell.
Development. 1995 Feb;121(2):263-71
PMID: 7768171
-
cdh-3, a gene encoding a member of the cadherin superfamily, functions in epithelial cell morphogenesis in Caenorhabditis elegans.
Development. 1996 Dec;122(12):4149-57
PMID: 9012534
-
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
PMID: 9254694
-
Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis.
Curr Biol. 1998 Sep 24;8(19):1087-90
PMID: 9768364
-
COG-2, a sox domain protein necessary for establishing a functional vulval-uterine connection in Caenorhabditis elegans.
Development. 1999 Jan;126(1):169-79
PMID: 9834196
-
Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis.
Development. 1999 Feb;126(4):691-9
PMID: 9895317
-
Fusogenic activity of EFF-1 is regulated via dynamic localization in fusing somatic cells of C. elegans.
Curr Biol. 2005 Mar 8;15(5):413-23
PMID: 15753035
-
FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans.
Cell. 2005 Jun 17;121(6):951-62
PMID: 15960981
-
A molecular recognition paradigm: promiscuity associated with the ligand-receptor interactions of the activin members of the TGF-beta superfamily.
J Mol Recognit. 2005 Sep-Oct;18(5):385-403
PMID: 15948132
-
N-ethylmaleimide sensitive factor is required for fusion of the C. elegans uterine anchor cell.
Dev Biol. 2006 Sep 1;297(1):87-102
PMID: 16769048
-
The C. elegans developmental fusogen EFF-1 mediates homotypic fusion in heterologous cells and in vivo.
Dev Cell. 2006 Oct;11(4):471-81
PMID: 17011487
-
Proliferation and cell-cell fusion of endometrial carcinoma are induced by the human endogenous retroviral Syncytin-1 and regulated by TGF-beta.
J Mol Med (Berl). 2007 Jan;85(1):23-38
PMID: 17066266
-
Cell fusion.
WormBook. 2006;:1-32
PMID: 18050486