The transcription factor HLH-2/E/Daughterless regulates anchor cell invasion across basement membrane in C. elegans

Developmental Biology

Volumn 357, Issue 2, 2011, Pages 380-391

  Schindler, Adam J ^a   Sherwood, David R ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Anchor cell; Basement membrane; Cell invasion; HLH 2; Transcriptional regulation

Indexed keywords

CADHERIN; DAUGHTERLESS PROTEIN; DROSOPHILA PROTEIN; E PROTEIN; F ACTIN; PROTEIN FOS; PROTEIN FOS 1A; PROTOCADHERIN; REGULATOR PROTEIN; SCLEROPROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HL 2; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CDH 3 GENE; CELL INVASION; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; GENE; GENETIC ANALYSIS; HEMICENTIN GENE; MIG 6 GENE; NONHUMAN; ORTHOLOGY; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REGULATORY MECHANISM; RNA INTERFERENCE; TRANSCRIPTION REGULATION;

CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 80052152100     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.07.012     Document Type: Article

References (56)

1. Adiseshaiah P., Vaz M., Machireddy N., Kalvakolanu D.V., Reddy S.P. A Fra-1-dependent, matrix metalloproteinase driven EGFR activation promotes human lung epithelial cell motility and invasion. J. Cell. Physiol. 2008, 216:405-412.
2. Arnone M.I., Davidson E.H. The hardwiring of development: organization and function of genomic regulatory systems. Development 1997, 124:1851-1864.
3. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
4. Chesney M.A., Lam N., Morgan D.E., Phillips B.T., Kimble J. C. elegans HLH-2/E/Daughterless controls key regulatory cells during gonadogenesis. Dev. Biol. 2009, 331:14-25.
5. Cram E.J., Shang H., Schwarzbauer J.E. A systematic RNA interference screen reveals a cell migration gene network in C. elegans. J. Cell Sci. 2006, 119:4811-4818.
6. Gertler F., Condeelis J. Metastasis: tumor cells becoming MENAcing. Trends Cell Biol. 2011, 21:81-90.
7. Hagedorn E.J., Yashiro H., Ziel J.W., Ihara S., Wang Z., Sherwood D.R. Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans. Dev. Cell 2009, 17:187-198.
8. Hedgecock E.M., Culotti J.G., Hall D.H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 1990, 4:61-85.
9. Hobert O. PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 2002, 32:728-730.
10. Hwang B.J., Sternberg P.W. A cell-specific enhancer that specifies lin-3 expression in the C. elegans anchor cell for vulval development. Development 2004, 131:143-151.
11. Hwang B.J., Meruelo A.D., Sternberg P.W. C. elegans EVI1 proto-oncogene, EGL-43, is necessary for Notch-mediated cell fate specification and regulates cell invasion. Development 2007, 134:669-679.
12. 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.
13. Inoue T., Wang M., Ririe T.O., Fernandes J.S., Sternberg P.W. Transcriptional network underlying Caenorhabditis elegans vulval development. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:4972-4977.
14. Kao G., Huang C.C., Hedgecock E.M., Hall D.H., Wadsworth W.G. The role of the laminin beta subunit in laminin heterotrimer assembly and basement membrane function and development in C. elegans. Dev. Biol. 2006, 290:211-219.
15. Karp X., Greenwald I. Post-transcriptional regulation of the E/Daughterless ortholog HLH-2, negative feedback, and birth order bias during the AC/VU decision in C. elegans. Genes Dev. 2003, 17:3100-3111.
16. Karp X., Greenwald I. Multiple roles for the E/Daughterless ortholog HLH-2 during C. elegans gonadogenesis. Dev. Biol. 2004, 272:460-469.
17. Kawano T., Zheng H., Merz D.C., Kohara Y., Tamai K.K., Nishiwaki K., Culotti J.G. C. elegans mig-6 encodes papilin isoforms that affect distinct aspects of DTC migration, and interacts genetically with mig-17 and collagen IV. Development 2009, 136:1433-1442.
18. Kee B.L. E and ID proteins branch out. Nat. Rev. Immunol. 2009, 9:175-184.
19. Kirouac M., Sternberg P.W. cis-Regulatory control of three cell fate-specific genes in vulval organogenesis of Caenorhabditis elegans and C. briggsae. Dev. Biol. 2003, 257:85-103.
20. Kustikova O., Kramerov D., Grigorian M., Berezin V., Bock E., Lukanidin E., Tulchinsky E. Fra-1 induces morphological transformation and increases in vitro invasiveness and motility of epithelioid adenocarcinoma cells. Mol. Cell. Biol. 1998, 18:7095-7105.
21. Lam N., Chesney M.A., Kimble J. Wnt signaling and CEH-22/tinman/Nkx2.5 specify a stem cell niche in C. elegans. Curr. Biol. 2006, 16:287-295.
22. Lee M., Cram E.J., Shen B., Schwarzbauer J.E. Roles for beta(pat-3) integrins in development and function of Caenorhabditis elegans muscles and gonads. J. Biol. Chem. 2001, 276:36404-36410.
23. Lifanov A.P., Makeev V.J., Nazina A.G., Papatsenko D.A. Homotypic regulatory clusters in Drosophila. Genome Res. 2003, 13:579-588.
24. Luo Y.P., Zhou H., Krueger J., Kaplan C., Liao D., Markowitz D., Liu C., Chen T., Chuang T.H., Xiang R., Reisfeld R.A. The role of proto-oncogene Fra-1 in remodeling the tumor microenvironment in support of breast tumor cell invasion and progression. Oncogene 2010, 29:662-673.
25. Madsen C.D., Sahai E. Cancer dissemination-lessons from leukocytes. Dev. Cell 2010, 19:13-26.
26. Matus D.Q., Li X.Y., Durbin S., Agarwal D., Chi Q., Weiss S.J., Sherwood D.R. In vivo identification of regulators of cell invasion across basement membranes. Sci. Signal. 2010, 3:ra35.
27. Naito Y., Yamada T., Matsumiya T., Ui-Tei K., Saigo K., Morishita S. dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference. Nucleic Acids Res. 2005, 33:W589-W591.
28. Oliveri P., Tu Q., Davidson E.H. Global regulatory logic for specification of an embryonic cell lineage. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:5955-5962.
29. Ozanne B.W., Spence H.J., McGarry L.C., Hennigan R.F. Transcription factors control invasion: AP-1 the first among equals. Oncogene 2007, 26:1-10.
30. Perez-Moreno M.A., Locascio A., Rodrigo I., Dhondt G., Portillo F., Nieto M.A., Cano A. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J. Biol. Chem. 2001, 276:27424-27431.
31. Pollheimer J., Knofler M. Signalling pathways regulating the invasive differentiation of human trophoblasts: a review. Placenta 2005, 26(Suppl. A):S21-30.
32. Portman D.S., Emmons S.W. The basic helix-loop-helix transcription factors LIN-32 and HLH-2 function together in multiple steps of a C. elegans neuronal sublineage. Development 2000, 127:5415-5426.
33. Ramaswamy S., Ross K.N., Lander E.S., Golub T.R. A molecular signature of metastasis in primary solid tumors. Nat. Genet. 2003, 33:49-54.
34. Rho H.K., McClay D.R. The control of foxN2/3 expression in sea urchin embryos and its function in the skeletogenic gene regulatory network. Development 2011, 138:937-945.
35. Rimann I., Hajnal A. Regulation of anchor cell invasion and uterine cell fates by the egl-43 Evi-1 proto-oncogene in Caenorhabditis elegans. Dev. Biol. 2007, 308:187-195.
36. Ririe T.O., Fernandes J.S., Sternberg P.W. The Caenorhabditis elegans vulva: a post-embryonic gene regulatory network controlling organogenesis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20095-20099.
37. Rowe R.G., Weiss S.J. Breaching the basement membrane: who, when and how?. Trends Cell Biol. 2008, 18:560-574.
38. Rowe R.G., Weiss S.J. Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Annu. Rev. Cell Dev. Biol. 2009, 25:567-595.
39. Sarin S., Antonio C., Tursun B., Hobert O. The C. elegans tailless/TLX transcription factor nhr-67 controls neuronal identity and left/right asymmetric fate diversification. Development 2009, 136:2933-2944.
40. Sherwood D.R., Sternberg P.W. Anchor cell invasion into the vulval epithelium in C. elegans. Dev. Cell 2003, 5:21-31.
41. Sherwood D.R., Butler J.A., Kramer J.M., Sternberg P.W. FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 2005, 121:951-962.
42. Slattery C., McMorrow T., Ryan M.P. Overexpression of E2A proteins induces epithelial-mesenchymal transition in human renal proximal tubular epithelial cells suggesting a potential role in renal fibrosis. FEBS Lett. 2006, 580:4021-4030.
43. Sobrado V.R., Moreno-Bueno G., Cubillo E., Holt L.J., Nieto M.A., Portillo F., Cano A. The class I bHLH factors E2-2A and E2-2B regulate EMT. J. Cell Sci. 2009, 122:1014-1024.
44. Sternberg P.W. Working in the post-genomic C. elegans world. Cell 2001, 105:173-176.
45. Tabara H., Sarkissian M., Kelly W.G., Fleenor J., Grishok A., Timmons L., Fire A., Mello C.C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 1999, 99:123-132.
46. Tamai K.K., Nishiwaki K. bHLH transcription factors regulate organ morphogenesis via activation of an ADAMTS protease in C. elegans. Dev. Biol. 2007, 308:562-571.
47. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
48. Uhlirova M., Bohmann D. JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J. 2006, 25:5294-5304.
49. van 't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., Peterse H.L., van der Kooy K., Marton M.J., Witteveen A.T., Schreiber G.J., Kerkhoven R.M., Roberts C., Linsley P.S., Bernards R., Friend S.H. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536.
50. Vogel B.E., Hedgecock E.M. Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 2001, 128:883-894.
51. Wang W., Wyckoff J.B., Frohlich V.C., Oleynikov Y., Huttelmaier S., Zavadil J., Cermak L., Bottinger E.P., Singer R.H., White J.G., Segall J.E., Condeelis J.S. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res. 2002, 62:6278-6288.
52. Wang W., Goswami S., Sahai E., Wyckoff J.B., Segall J.E., Condeelis J.S. Tumor cells caught in the act of invading: their strategy for enhanced cell motility. Trends Cell Biol. 2005, 15:138-145.
53. Wilkinson H.A., Fitzgerald K., Greenwald I. Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision. Cell 1994, 79:1187-1198.
54. Wu S.Y., Yang Y.P., McClay D.R. Twist is an essential regulator of the skeletogenic gene regulatory network in the sea urchin embryo. Dev. Biol. 2008, 319:406-415.
55. Yilmaz M., Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009, 28:15-33.
56. 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.