Advertisement
JOURNAL ARTICLES
A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans
J.N. Maloof, J. Whangbo, J.M. Harris, G.D. Jongeward, C. Kenyon
Development 1999 126: 37-49;

Summary

The specification of body pattern along the anteroposterior (A/P) body axis is achieved largely by the actions of conserved clusters of Hox genes. Limiting expression of these genes to localized regional domains and controlling the precise patterns of expression within those domains is critically important for normal patterning. Here we report that egl-20, a C. elegans gene required to activate expression of the Hox gene mab-5 in the migratory neuroblast QL, encodes a member of the Wnt family of secreted glycoproteins. We have found that a second Wnt pathway gene, bar-1, which encodes a beta-catenin/Armadillo-like protein, is also required for activation of mab-5 expression in QL. In addition, we describe the gene pry-1, which is required to limit expression of the Hox genes lin-39, mab-5 and egl-5 to their correct local domains. We find that egl-20, pry-1 and bar-1 all function in a linear genetic pathway with conserved Wnt signaling components, suggesting that a conserved Wnt pathway activates expression of mab-5 in the migratory neuroblast QL. Moreover, we find that members of this Wnt signaling system play a major role in both the general and fine-scale control of Hox gene expression in other cell types along the A/P axis.

Reference

    1. Adler P. N.
    (1992) The genetic control of tissue polarity in Drosophila. BioEssays 14, 735–741
    OpenUrlCrossRefPubMedWeb of Science
    1. Bhanot P.,
    2. Brink M.,
    3. Samos C. H.,
    4. Hsieh J.,
    5. Wang Y.,
    6. Macke J. P.,
    7. Andrew D.,
    8. Nathans J.,
    9. Nusse R.
    (1996) A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382, 225–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Brannon M.,
    2. Gomperts M.,
    3. Sumoy L.,
    4. Moon R. T.,
    5. Kimelman D.
    (1997) A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev 11, 2359–2370
    OpenUrlAbstract/FREE Full Text
    1. Brenner S.
    (1974) The genetics of C. elegans. Genetics 77, 71–94
    OpenUrlAbstract/FREE Full Text
    1. Cadigan K. M.,
    2. Nusse R.
    (1997) Wnt signaling: a common theme in animal development. Genes Dev 11, 3286–3305
    OpenUrlFREE Full Text
    1. Castelli-Gair J.,
    2. Akam M.
    (1995) How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metameres. Development 121, 2973–2982
    OpenUrlAbstract
    1. Chisholm A.
    (1991) Control of cell fate in the tail region of C. elegans by the gene egl-5. Development 111, 921–932
    OpenUrlAbstract/FREE Full Text
    1. Clark S. G.,
    2. Chisholm A. D.,
    3. Horvitz H. R.
    (1993) Control of cellfates in the central body region of C. elegans by the homeobox gene lin-39. Cell 74, 43–55
    OpenUrlCrossRefPubMedWeb of Science
    1. Costa M.,
    2. Weir M.,
    3. Coulson A.,
    4. Sulston J.,
    5. Kenyon C.
    (1988) Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox. Cell 55, 747–756
    OpenUrlCrossRefPubMedWeb of Science
    1. Cowing D. W.,
    2. Kenyon C.
    (1992) Expression of the homeotic gene mab-5 during Caenorhabditis elegans embryogenesis. Development 116, 481–490
    OpenUrlAbstract/FREE Full Text
    1. Desai C.,
    2. Garriga G.,
    3. McIntire S. L.,
    4. Horvitz H. R.
    (1988) A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638–646
    OpenUrlCrossRefPubMedWeb of Science
    1. Eisenmann D. M.,
    2. Maloof J. N.,
    3. Simske J. S.,
    4. Kenyon C.,
    5. Kim S. K.
    (1998) The-catenin homolog BAR-1 and LET-60 Rascoordinately regulate the Hox gene lin-39 during C. elegans vulval development. Development 125, 3667–3680
    OpenUrlAbstract
    1. Ferguson E. L.,
    2. Horvitz H. R.
    (1985) Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110, 17–72
    OpenUrlAbstract/FREE Full Text
    1. Fire A.,
    2. Harrison S. W.,
    3. Dixon D.
    (1990) A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189–198
    OpenUrlCrossRefPubMedWeb of Science
    1. Frohman M. A.
    (1993) Rapid amplification of complementary DNA ends for generation of full-length complementary DNAs: thermal RACE. Meth. Enzymol 218, 340–356
    OpenUrlCrossRefPubMedWeb of Science
    1. Gavin B. J.,
    2. McMahon J. A.,
    3. McMahon A. P.
    (1990) Expression of multiple novel Wnt-1/int-1 -related genes during fetal and adult mouse development. Genes Dev 4, 2319–2332
    OpenUrlAbstract/FREE Full Text
    1. Han M.
    (1997) Gut reaction to Wnt signaling in worms [comment]. Cell 90, 581–584
    OpenUrlCrossRefPubMed
    1. Harris J.,
    2. Honigberg L.,
    3. Robinson N.,
    4. Kenyon C.
    (1996) Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position. Development 122, 3117–3131
    OpenUrlAbstract
    1. Hedgecock E. M.,
    2. Culotti J. G.,
    3. Hall D. H.,
    4. Stern B. D.
    (1987) Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100, 365–382
    OpenUrlAbstract
    1. Herman M. A.,
    2. Vassilieva L. L.,
    3. Horvitz H. R.,
    4. Shaw J. E.,
    5. Herman R. K.
    (1995) The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously. Cell 83, 101–110
    OpenUrlCrossRefPubMedWeb of Science
    1. Kenyon C.
    (1986) A gene involved in the development of the posterior body region of C. elegans. Cell 46, 477–487
    OpenUrlCrossRefPubMedWeb of Science
    1. Maloof J. N.,
    2. Kenyon C.
    (1998) The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development 125, 181–190
    OpenUrlAbstract
    1. Mello C. C.,
    2. Kramer J. M.,
    3. Stinchcomb D.,
    4. Ambros V.
    (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10, 3959–3970
    OpenUrlPubMedWeb of Science
    1. Miller J. R.,
    2. Moon R. T.
    (1996) Signal transduction through beta-catenin and specification of cell fate during embryogenesis. Genes Dev 10, 2527–2539
    OpenUrlFREE Full Text
    1. Munemitsu S.,
    2. Albert I.,
    3. Souza B.,
    4. Rubinfeld B.,
    5. Polakis P.
    (1995) Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. USA 92, 3046–3050
    OpenUrlAbstract/FREE Full Text
    1. Nelson C. E.,
    2. Morgan B. A.,
    3. Burke A. C.,
    4. Laufer E.,
    5. DiMambro E.,
    6. Murtaugh L. C.,
    7. Gonzales E.,
    8. Tessarollo L.,
    9. Parada L. F.,
    10. Tabin C.
    (1996) Analysis of Hox gene expression in the chick limb bud. Development 122, 1449–1466
    OpenUrlAbstract
    1. Nusse R.
    (1997) A versatile transcriptional effector of Wingless signaling. Cell 89, 321–323
    OpenUrlCrossRefPubMedWeb of Science
    1. Orsulic S.,
    2. Peifer M.
    (1996) An in vivo structure-function study of armadillo, the beta-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for wingless signaling. J. Cell Biol 134, 1283–1300
    OpenUrlAbstract/FREE Full Text
    1. Pai L. M.,
    2. Orsulic S.,
    3. Bejsovec A.,
    4. Peifer M.
    (1997) Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124, 2255–2266
    OpenUrlAbstract
    1. Peifer M.,
    2. Sweeton D.,
    3. Casey M.,
    4. Wieschaus E.
    (1994) wingless signal and Zeste-white 3 kinase trigger opposing changes in intracellular distribution of Armadillo. Development 120, 369–380
    OpenUrlAbstract
    1. Pirrotta V.
    (1997) PcG complexes and chromatin silencing. Curr. Opin. Genet. Dev 7, 249–258
    OpenUrlCrossRefPubMedWeb of Science
    1. Polakis P.
    (1997) The adenomatous polyposis coli (APC) tumor suppressor. Biochim. Biophys. Acta 1332, 127–147
    OpenUrl
    1. Rijsekijk F.,
    2. Schuermann M.,
    3. Wagenaar E.,
    4. Parren P.,
    5. Weigel D.,
    6. Nusse R.
    (1987) The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657
    OpenUrlCrossRefPubMedWeb of Science
    1. Rocheleau C. E.,
    2. Downs W. D.,
    3. Lin R.,
    4. Wittmann C.,
    5. Bei Y.,
    6. Cha Y. H.,
    7. Ali M.,
    8. Priess J. R.,
    9. Mello C. C.
    (1997) Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos [see comments]. Cell 90, 707–716
    OpenUrlCrossRefPubMedWeb of Science
    1. Rubinfeld B.,
    2. Albert I.,
    3. Porfiri E.,
    4. Fiol C.,
    5. Munemitsu S.,
    6. Polakis P.
    (1996) Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly [see comments]. Science 272, 1023–1026
    OpenUrlAbstract
    1. Salser S. J.,
    2. Kenyon C.
    (1992) Activation of a C. elegans Antennapedia homologue in migrating cells controls their direction of migration. Nature 355, 2558–.
    OpenUrl
    1. Salser S. J.,
    2. Kenyon C.
    (1996) A C. elegans Hox gene switches on, off, on and off again to regulate proliferation, differentiation and morphogenesis. Development 122, 1651–1661
    OpenUrlAbstract
    1. Sawa H.,
    2. Lobel L.,
    3. Horvitz H. R.
    (1996) The Caenorhabditis elegans gene lin-17, which is required for certain asymmetric cell divisions, encodes a putative seven-transmembrane protein similar to the Drosophila frizzled protein. Genes Dev 10, 2189–2197
    OpenUrlAbstract/FREE Full Text
    1. Siegfried E.,
    2. Chou T. B.,
    3. Perrimon N.
    (1992) Wingless signaling acts through zeste-white 3, the Drosophila homolog glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167–1179
    OpenUrlCrossRefPubMedWeb of Science
    1. Strome S.,
    2. Garvin C.,
    3. Paulsen J.,
    4. Capowski E.,
    5. Martin P.,
    6. Beanan M.
    (1994) Specification and development of the germline in Caenorhabditis elegans. Ciba Foundation Symp 182, 31–45
    OpenUrlPubMed
    1. Thorpe C. J.,
    2. Schlesinger A.,
    3. Carter J. C.,
    4. Bowerman B.
    (1997) Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm [see Comments]. Cell 90, 695–705
    OpenUrlCrossRefPubMedWeb of Science
    1. Trent C.,
    2. Tsung N.,
    3. Horvitz H.
    (1983) Egg-laying defective mutants of the nematode C. elegans. Genetics 104, 619–647
    OpenUrlAbstract/FREE Full Text
    1. van de Wetering M.,
    2. Cavallo R.,
    3. Dooijes D.,
    4. van Beest M.,
    5. van Es J.,
    6. Loureiro J.,
    7. Ypma A.,
    8. Hursh D.,
    9. Jones T.,
    10. Bejsovec A.,
    11. Peifer M.,
    12. Mortin M.,
    13. Clevers H.
    (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789–799
    OpenUrlCrossRefPubMedWeb of Science
    1. von Heijne
    (1986) Net N-C charge imbalance may be important for signal sequence function in bacteria. J. Mol. Biol 192, 287–290
    OpenUrlCrossRefPubMedWeb of Science
    1. Wang B. B.,
    2. Muller I. M.,
    3. Austin J.,
    4. Robinson N. T.,
    5. Chisholm A.,
    6. Kenyon C.
    (1993) A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74, 29–42
    OpenUrlCrossRefPubMedWeb of Science
    1. Williams B. D.,
    2. Schrank B.,
    3. Huynh C.,
    4. Shownkeen R.,
    5. Waterston R. H.
    (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131, 609–624
    OpenUrlAbstract/FREE Full Text
    1. Wrischnik L. A.,
    2. Kenyon C. J.
    (1997) The role of lin-22, a hairy/enhancer of split homolog, in patterning the peripheral nervous system of C. elegans. Development 124, 2875–2888
    OpenUrlAbstract
    1. Zeng L.,
    2. Fagotto F.,
    3. Zhang T.,
    4. Hsu W.,
    5. Vasicek T. J.,
    6. Perry W. R.,
    7. Lee J. J.,
    8. Tilghman S. M.,
    9. Gumbiner B. M.,
    10. Costantini F.
    (1997) The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90, 181–192
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans
J.N. Maloof, J. Whangbo, J.M. Harris, G.D. Jongeward, C. Kenyon
Development 1999 126: 37-49;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.