Coordinated Lumen Contraction and Expansion during Vulval Tube Morphogenesis in Caenorhabditis elegans

Developmental Cell

Volumn 23, Issue 3, 2012, Pages 494-506

  Farooqui, Sarfarazhussain ^a,b   Pellegrino, Mark W ^a,c   Rimann, Ivo ^a,d   Morf, Matthias K ^a,b   Müller, Louisa ^a   Fröhli, Erika ^a   Hajnal, Alex ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; LET 502 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN ADENOSINE TRIPHOSPHATASE; NOTCH RECEPTOR; RAS PROTEIN; RHO KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LIN 1; UNCLASSIFIED DRUG;

ARTICLE; BRANCHING MORPHOGENESIS; CAENORHABDITIS ELEGANS; CELL FATE; CELL LINEAGE; CONTRACTION STRESS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME REGULATION; HERMAPHRODITIC SPECIES; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VULVA; VULVAL TUBE;

ACTOMYOSIN; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FEMALE; MORPHOGENESIS; MUSCLE CONTRACTION; RECEPTORS, NOTCH; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; VULVA;

CAENORHABDITIS ELEGANS;

EID: 84866007921     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.06.019     Document Type: Article

References (44)

1. Abdus-Saboor I., Mancuso V.P., Murray J.I., Palozola K., Norris C., Hall D.H., Howell K., Huang K., Sundaram M.V. Notch and Ras promote sequential steps of excretory tube development in C. elegans. Development 2011, 138:3545-3555.
2. Andrew D.J., Ewald A.J. Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration. Dev. Biol. 2010, 341:34-55.
3. Beitel G.J., Tuck S., Greenwald I., Horvitz H.R. The Caenorhabditis elegans gene lin-1 encodes an ETS-domain protein and defines a branch of the vulval induction pathway. Genes Dev. 1995, 9:3149-3162.
4. Berset T., Hoier E.F., Battu G., Canevascini S., Hajnal A. Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 2001, 291:1055-1058.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Caussinus E., Colombelli J., Affolter M. Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr. Biol. 2008, 18:1727-1734.
7. Christensen S., Kodoyianni V., Bosenberg M., Friedman L., Kimble J. lag-1, a gene required for lin-12 and glp-1 signaling in Caenorhabditis elegans, is homologous to human CBF1 and Drosophila Su(H). Development 1996, 122:1373-1383.
8. Diogon M., Wissler F., Quintin S., Nagamatsu Y., Sookhareea S., Landmann F., Hutter H., Vitale N., Labouesse M. The RhoGAP RGA-2 and LET-502/ROCK achieve a balance of actomyosin-dependent forces in C. elegans epidermis to control morphogenesis. Development 2007, 134:2469-2479.
9. Estes K.A., Hanna-Rose W. The anchor cell initiates dorsal lumen formation during C. elegans vulval tubulogenesis. Dev. Biol. 2009, 328:297-304.
10. Gally C., Wissler F., Zahreddine H., Quintin S., Landmann F., Labouesse M. Myosin II regulation during C. elegans embryonic elongation: LET-502/ROCK, MRCK-1 and PAK-1, three kinases with different roles. Development 2009, 136:3109-3119.
11. Gov N.S. Collective cell migration patterns: follow the leader. Proc. Natl. Acad. Sci. USA 2007, 104:15970-15971.
12. Greenwald I. LIN-12/Notch signaling in C. elegans. WormBook 2005, 1-16.
13. Herman T., Horvitz H.R. Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway. Proc. Natl. Acad. Sci. USA 1999, 96:974-979.
14. Herman T., Hartwieg E., Horvitz H.R. sqv mutants of Caenorhabditis elegans are defective in vulval epithelial invagination. Proc. Natl. Acad. Sci. USA 1999, 96:968-973.
15. Hwang H.Y., Olson S.K., Esko J.D., Horvitz H.R. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature 2003, 423:439-443.
16. Ihara S., Hagedorn E.J., Morrissey M.A., Chi Q., Motegi F., Kramer J.M., Sherwood D.R. Basement membrane sliding and targeted adhesion remodels tissue boundaries during uterine-vulval attachment in Caenorhabditis elegans. Nat. Cell Biol. 2011, 13:641-651.
17. Jacobs D., Beitel G.J., Clark S.G., Horvitz H.R., Kornfeld K. Gain-of-function mutations in the Caenorhabditis elegans lin-1 ETS gene identify a C-terminal regulatory domain phosphorylated by ERK MAP kinase. Genetics 1998, 149:1809-1822.
18. Kamath R.S., Martinez-Campos M., Zipperlen P., Fraser A.G., Ahringer J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2001, 2. RESEARCH0002.
19. Köppen M., Simske J.S., Sims P.A., Firestein B.L., Hall D.H., Radice A.D., Rongo C., Hardin J.D. Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 2001, 3:983-991.
20. Lackner M.R., Kim S.K. Genetic analysis of the Caenorhabditis elegans MAP kinase gene mpk-1. Genetics 1998, 150:103-117.
21. Lints, R., and Hall, D.H. (2009). Reproductive system, egglaying apparatus In WormAtlas. doi:10.3908/wormatlas,1.24.
22. Lundquist E.A., Reddien P.W., Hartwieg E., Horvitz H.R., Bargmann C.I. Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 2001, 128:4475-4488.
23. Mello C.C., Kramer J.M., Stinchcomb D., Ambros V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991, 10:3959-3970.
24. Miller D.M., Shakes D.C. Immunofluorescence microscopy. Methods Cell Biol. 1995, 48:365-394.
25. Miller L.M., Gallegos M.E., Morisseau B.A., Kim S.K. lin-31, a Caenorhabditis elegans HNF-3/fork head transcription factor homolog, specifies three alternative cell fates in vulval development. Genes Dev. 1993, 7:933-947.
26. Mukhopadhyay A., Deplancke B., Walhout A.J., Tissenbaum H.A. Chromatin immunoprecipitation (ChIP) coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans. Nat. Protoc. 2008, 3:698-709.
27. Omelchenko T., Vasiliev J.M., Gelfand I.M., Feder H.H., Bonder E.M. Rho-dependent formation of epithelial "leader" cells during wound healing. Proc. Natl. Acad. Sci. USA 2003, 100:10788-10793.
28. Pellegrino M.W., Farooqui S., Fröhli E., Rehrauer H., Kaeser-Pebernard S., Müller F., Gasser R.B., Hajnal A. LIN-39 and the EGFR/RAS/MAPK pathway regulate C. elegans vulval morphogenesis via the VAB-23 zinc finger protein. Development 2011, 138:4649-4660.
29. Piekny A.J., Johnson J.L., Cham G.D., Mains P.E. The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis. Development 2003, 130:5695-5704.
30. Pohl C., Bao Z. Chiral forces organize left-right patterning in C. elegans by uncoupling midline and anteroposterior axis. Dev. Cell 2010, 19:402-412.
31. Poujade M., Grasland-Mongrain E., Hertzog A., Jouanneau J., Chavrier P., Ladoux B., Buguin A., Silberzan P. Collective migration of an epithelial monolayer in response to a model wound. Proc. Natl. Acad. Sci. USA 2007, 104:15988-15993.
32. Rodríguez-Fraticelli A.E., Gálvez-Santisteban M., Martín-Belmonte F. Divide and polarize: recent advances in the molecular mechanism regulating epithelial tubulogenesis. Curr. Opin. Cell Biol. 2011, 23:638-646.
33. Sapir A., Choi J., Leikina E., Avinoam O., Valansi C., Chernomordik L.V., Newman A.P., Podbilewicz B. AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 2007, 12:683-698.
34. Schottenfeld J., Song Y., Ghabrial A.S. Tube continued: morphogenesis of the Drosophila tracheal system. Curr. Opin. Cell Biol. 2010, 22:633-639.
35. Sementchenko V.I., Watson D.K. Ets target genes: past, present and future. Oncogene 2000, 19:6533-6548.
36. Sharma-Kishore R., White J.G., Southgate E., Podbilewicz B. Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis. Development 1999, 126:691-699.
37. Sternberg P.W. Vulval development. WormBook 2005, 1-28.
38. Tan P.B., Lackner M.R., Kim S.K. MAP kinase signaling specificity mediated by the LIN-1 Ets/LIN-31 WH transcription factor complex during C. elegans vulval induction. Cell 1998, 93:569-580.
39. Vaughan R.B., Trinkaus J.P. Movements of epithelial cell sheets in vitro. J. Cell Sci. 1966, 1:407-413.
40. Wissmann A., Ingles J., McGhee J.D., Mains P.E. Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape. Genes Dev. 1997, 11:409-422.
41. Wissmann A., Ingles J., Mains P.E. The Caenorhabditis elegans mel-11 myosin phosphatase regulatory subunit affects tissue contraction in the somatic gonad and the embryonic epidermis and genetically interacts with the Rac signaling pathway. Dev. Biol. 1999, 209:111-127.
42. Xavier Trepat M.R.W., Angelini T.E., Millet E., Weitz D.A., Butler J.P., Fredberg J.J. Physical forces during collective cell migration. Nat. Phys. 2009, 5:426-430.
43. Zhang X., Greenwald I. Spatial regulation of lag-2 transcription during vulval precursor cell fate patterning in Caenorhabditis elegans. Genetics 2011, 188:847-858.
44. Ziel J.W., Hagedorn E.J., Audhya A., Sherwood D.R. UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat. Cell Biol. 2009, 11:183-189.