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The Caenorhabditis Elegans Gene Lin-1 Encodes an ETS-Domai.N Protein and Defines a Branch of the Vulval Induction Pathway

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The Caenorhabditis Elegans Gene Lin-1 Encodes an ETS-Domai.N Protein and Defines a Branch of the Vulval Induction Pathway Downloaded from genesdev.cshlp.org on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press The Caenorhabditis elegans gene lin-1 encodes an ETS-domai.n protein and defines a branch of the vulval Induction pathway Greg J. Beitel, l'z Simon Tuck, 3'4 Iva Greenwald, 3'5 and H. Robert Horvitz 1'6 ~Howard Hughes Medical Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139 USA; SHoward Hughes Medical Institute, aDepartment of Biochemistry and Molecular Biophysics, Columbia University College of Physicians and Surgeons, New York, New York 10032 USA The Caenorhabditis elegans gene lin-1 appears to act after the Ras-Raf-MEK-MAPK signaling cascade that mediates vulval induction. We show that fin-1 is a negative regulator of vulval cell fates and encodes an ETS-domain putative transcription factor containing potential MAPK phosphorylation sites. In lin-1 null mutants, the vulval precursor cells (VPCs) still respond to signaling from the gonadal anchor cell, indicating that lin-1 defines a branch of the inductive signaling pathway. We also provide evidence that the inductive and lateral signaling pathways are integrated to control the 1 ° and 2 ° vulval cell fates after the point at which lin-1 acts in the inductive pathway and that VPCs can assess the relative rather than absolute levels of inductive and lateral signaling in determining whether to express the 1 ° or 2 ° vulval cell fates. [Key Words: lin-1; ETS; signal transduction; cell fate; C. elegans] Received September 19, 1995; revised version accepted October 30, 1995. Signaling pathways involving receptor tyrosine kinases the LIN-3 protein, a member of the epidermal growth (RTKs) and Ras proteins have major roles in determining factor IEGF) family (Hill and Steinberg 1992), and the cell fates and in oncogenesis (for review, see Egan and apparent receptor for the signal is the LET-23 protein, an Weinberg 1993; Pawson and Hunter 19941. Such signal RTK of the EGF receptor subfamily (Aroian et al. 1990). transduction pathways have been highly conserved dur- LET-23, together with the adapter protein SEM-5 (Clark ing evolution. For example, Caenorhabditis elegans vul- et al. 1992; Lowenstein et al. 19921, activates LET-60 Ras val induction is mediated by the let-23 RTK/let-60 Ras (Beitel et al. 1990; Han and Steinberg 1990) and the ki- signaling pathway (for review, see Horvitz and Sternberg nase cascade LIN-45 Raf (Han et al. 1993), MEK-2 MAP 1991; Eisenmann and Kim 1994; Tuck and Greenwald kinase kinase (MAPKK)(Church et al. 1995; Komfeld et 1994). This pathway acts to specify the fates of a set of al. 1995; Wu et al. 1995), and MPK-1 MAP kinase six multipotent hypodermal blast cells, P3.p-P8.p, {MAPK) (Lackner et al. 1994; Wu and Han 1994). The known as the vulval precursor cells (VPCs). The VPCs ordering of the components of this signaling pathway in are considered to be developmentally equivalent, be- C. elegans by genetic analysis has been concordant with cause they can adopt any one of three fates, each of biochemical studies of similar pathways in other organ- which is characterized by a distinct pattern of cell divi- isms. sions (lineage)(see Fig. 1; Sulston and White 1980; Stern- In wild-type hermaphrodites, the pattern of vulval berg and Horvitz 1986; Thomas et al. 1990). Two of these fates is invariant: P5.p, P6.p, and P7.p adopt the 2 °, 1°, fates, termed 1° and 2 °, are vulval fates, because in wild- and 2 ° fates, respectively (Sulston and Horvitz 1977). type animals the 1° and 2 ° lineages generate descendants Two signals are important for this patterning: the induc- that form the vulva. The third fate, termed 3 °, is a non- tive signal from the AC described above and a lateral vulval fate, because the 3 ° lineage generates descendants signal between VPCs (Sternberg 1988; Koga and Oh- that fuse with the hypodermal syncytium and are not shima 1995; Simske and Kim 1995). The lateral signal part of the vulva. appears to be expressed or activated upon reception of Vulval fates are induced by signaling from the anchor the inductive signal, because mutations that reduce vul- cell (AC) of the gonad. The inductive signal appears to be val induction also reduce lateral signaling (Simske and Kim 1995; Tuck and Greenwald 1995). The identity of lateral signal is as yet unknown, but its receptor appears Present addresses: 2Department of Biochemistry, Stanford University, to be the LIN-12 protein (Greenwald et al. 1983; Stem- School of Medicine, Stanford, California 94305 USA; 4Ume;~ Center for Molecular Pathogenesis, Ume~ University, S-901 87 Ume~, Sweden. berg and Horvitz 1989). How the inductive and the lat- 6Corresponding author. eral signaling pathways are integrated to control vulval GENES & DEVELOPMENT 9:3149-3162 ~ 1995 by Cold Spring Harbor Laboratory Press ISSN 0890-9369/95 $5.00 3149 Downloaded from genesdev.cshlp.org on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Beitel et al. cell fate and the relative contributions of each pathway AC to the specification of VPC fate in wild-type hermaphro- dites are still unclear. O The identification of genes that act after MPK-1 MAPK during vulval induction is central to understand- ing how MPK-1 controls vulval induction and how the inductive and lateral signaling pathways are integrated. k .... J--~k .... j4-- L.... ] One candidate is lin-31, which encodes a transcription factor of the HNF-3/fork head family (Miller et al. 1993). Another candidate is lin-25, which encodes a protein s having no significant similarity to other proteins in ss SS LLTN TTTT NTLL SS available data bases (Tuck and Greenwald 1995). Here 3: 3 2 1 ~ 2 c~ 3 ~ we describe genetic and molecular studies of a third can- k. didate, lin-1 (Horvitz and Sulston 1980; Sulston and Hor- vitz 1981; Ferguson and Horvitz 1985; Ferguson et al. Figure 1. Model for signaling in vulval induction. Outlined is 1987). Our analysis supports the idea that lin-1, an ETS- a simplified version of the current model for vulval induction domain putative transcription factor, is a target of the lHorvitz and Sternberg 1991). The six hypodermal blast cells Ras-MAPK cascade. Furthermore, our results indicate P3.p-PS.p are developmentally equivalent and are referred to as that the inductive signaling pathway is branched and VPCs. As described in the text, VPCs adopt one of three cell that lin-1 defines one of the branches. Our results sug- fates in response to signaling between the gonadal AC and the VPCs tflared arrowheadsl, between adjacent induced VPCs {hor- gest that the lin-1 branch of the inductive pathway acti- izontal arrow}, and between the syncytial hypodermis and the vates lateral signaling and that the inductive and lateral VPCs lnot shownl. The characteristic 1% 2 °, and 3 ° lineages signals are integrated after the point at which lin-1 acts Ifatesl that the VPCs express in wild-type animals are diagramed in the inductive pathway. We also present genetic evi- below each cell. The vulval fates are defined after two rounds of dence that VPCs can assess the relative rather than ab- division by two criteria: the axis of the third round of nuclear solute levels of inductive and lateral signaling in deter- divisions liT1 transverse; ill lateral; IN1 no division] and adher- mining which vulval fate to adopt. ence to the ventral cuticle, indicated by boldface Ci.e., L){no- menclature and criteria according to Sternberg and Horvitz 19861. The 3° cell fate is nonvulval and the 3° VPC descendants Results fuse with the hypodermal syncytium [iS1 syncytiall. P3.p joins the hypodermal syncytium without undergoing division in Cloning of lin-1 -50% of wild-type animals, and for P3.p both the S S and S lineages are considered 3 ° . lin-1 had been genetically mapped previously between daf-1 IV and lin-22 IV, which had been positioned on both the C. elegans genetic and physical maps IFerguson common, suggesting that they were transcribed from the and Horvitz 1985; Edgley and Riddle 1990; Georgi et al. same locus. The two longest cDNAs began with the SL1 1990, L. Wrischnik and C. Kenyon, pers. comm.1, daf-1 trans-spliced leader sequence (Krause and Hirsh 1987; and Iin-22 were located on two separate sets of ordered for review, see Blumenthal 19951, indicating that they and overlapping YAC and cosmid clones, referred to as are full-length transcripts. We determined and compared contigs. To define the location of lin-1 with respect to the sequences of the longest cDNA and -7 kb of the these contigs, we identified and genetically mapped 16 EagI-SpeI-rescuing fragment (Fig. 3; data not shown). restriction fragment length polymorphisms using The first 160 bp of the longest cDNA was not contained cosmids and cosmid subclones from the physical map as in the EagI-SpeI fragment or the C37F5 cosmid, despite probes (see Materials and methods). In collaboration the ability of these genomic fragments to at least par- with Alan Coulson (The Sanger Centre, Hinxton, U.K.t, tially rescue the lin-l(e12751 phenotype (Fig. 2C; see Ma- we reorganized the physical map in the lin-I region and terials and methodsl. We used polymerase chain reaction localized lin-1 to an -400-kb interval (Fig. 2A!. We used (PCR1 amplification and Southern blot experiments to cosmids from this interval in germ-line transformation determine that the first 160 bp of the predominant lin-1 experiments and in a search for allele-specific polymor- message is encoded by two exons located 15-20 kb from phisms among the >40 known lin-1 mutants (Horvitz the remaining exons (see Materials and methodsl.
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