Opposing activities of LIT-1/NLK and DAF-6/patched-related direct sensory compartment morphogenesis in C. elegans

PLoS Biology

Volumn 9, Issue 8, 2011, Pages

  Oikonomou, Grigorios ^a   Perens, Elliot A ^a   Lu, Yun ^a   Watanabe, Shigeki ^b   Jorgensen, Erik M ^b   Shaham, Shai ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXY TERMINAL TELOPEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE; NEMO LIKE KINASE; PHOSPHOTRANSFERASE; PROTEIN MOM 4; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; WNT PROTEIN; ACTIN; CAENORHABDITIS ELEGANS PROTEIN; DAF 6 PROTEIN, C ELEGANS; DAF-6 PROTEIN, C ELEGANS; LIT 1 PROTEIN, C ELEGANS; LIT-1 PROTEIN, C ELEGANS; MEMBRANE PROTEIN; MOM 4 PROTEIN, C ELEGANS; MOM-4 PROTEIN, C ELEGANS; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CYTOGENETICS; DAF 6 GENE; ENZYME ACTIVITY; ENZYME REPRESSION; GENE; GENE EXPRESSION; GENE FUNCTION; GENE MAPPING; GENE MUTATION; GLIA CELL; LIT 1 GENE; MORPHOGENESIS; NONHUMAN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; CHEMISTRY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOPRECIPITATION; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN BINDING; TWO HYBRID SYSTEM;

CAENORHABDITIS ELEGANS;

ACTINS; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EMBRYO, NONMAMMALIAN; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MORPHOGENESIS; MUTATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; TWO-HYBRID SYSTEM TECHNIQUES; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 80052332002     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001121     Document Type: Article

References (55)

1. Burkitt G. H, Young B, Heath J. W, (1993) Wheater's functional histology: a text and colour atlas. New York Churchill Livinstone.
2. Ross M. H, Romrell L. J, Kaye G. I, (1995) Histology: a text and atlas. Baltimore Williams & Wilkins.
3. Bell J, Bolanowski S, Holmes M. H, (1994) The structure and function of Pacinian corpuscles: a review. Prog Neurobiol 42: 79-128.
4. Suzuki Y, Takeda M, Farbman A. I, (1996) Supporting cells as phagocytes in the olfactory epithelium after bulbectomy. J Comp Neurol 376: 509-517.
5. Hansel D. E, Eipper B. A, Ronnett G. V, (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410: 940-944.
6. Rio C, Dikkes P, Liberman M. C, Corfas G, (2002) Glial fibrillary acidic protein expression and promoter activity in the inner ear of developing and adult mice. J Comp Neurol 442: 156-162.
7. Young R. W, Bok D, (1969) Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol 42: 392-403.
8. Bacaj T, Tevlin M, Lu Y, Shaham S, (2008) Glia are essential for sensory organ function in C. elegans. Science 322: 744-747.
9. Spacek J, (1985) Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol 171: 245-252.
10. Ventura R, Harris K. M, (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906.
11. Ward S, Thomson N, White J. G, Brenner S, (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160: 313-337.
12. Albert P. S, Brown S. J, Riddle D. L, (1981) Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol 198: 435-451.
13. Perkins L. A, Hedgecock E. M, Thomson J. N, Culotti J. G, (1986) Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456-487.
14. Perens E. A, Shaham S, (2005) C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev Cell 8: 893-906.
15. Herman R. K, (1987) Mosaic analysis of two genes that affect nervous system structure in Caenorhabditis elegans. Genetics 116: 377-388.
16. Michaux G, Gansmuller A, Hindelang C, Labouesse M, (2000) CHE-14, a protein with a sterol-sensing domain, is required for apical sorting in C. elegans ectodermal epithelial cells. Curr Biol 10: 1098-1107.
17. Rocheleau C. E, Yasuda J, Shin T. H, Lin R, Sawa H, et al. (1999) WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell 97: 717-726.
18. Symons M, Derry J. M, Karlak B, Jiang S, Lemahieu V, et al. (1996) Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84: 723-734.
19. Sulston J. E, Schierenberg E, White J. G, Thomson J. N, (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64-119.
20. Heiman M. G, Shaham S, (2009) DEX-1 and DYF-7 establish sensory dendrite length by anchoring dendritic tips during cell migration. Cell 137: 344-355.
21. Cassada R. C, Russell R. L, (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46: 326-342.
22. Riddle D. L, Swanson M. M, Albert P. S, (1981) Interacting genes in nematode dauer larva formation. Nature 290: 668-671.
23. Starich T. A, Herman R. K, Kari C. K, Yeh W. H, Schackwitz W. S, et al. (1995) Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics 139: 171-188.
24. Yoshimura S, Murray J. I, Lu Y, Waterston R. H, Shaham S, (2008) mls-2 and vab-3 Control glia development, hlh-17/Olig expression and glia-dependent neurite extension in C. elegans. Development 135: 2263-2275.
25. Landmann F, Quintin S, Labouesse M, (2004) Multiple regulatory elements with spatially and temporally distinct activities control the expression of the epithelial differentiation gene lin-26 in C. elegans. Dev Biol 265: 478-490.
26. Kaletta T, Schnabel H, Schnabel R, (1997) Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 390: 294-298.
27. Shin T. H, Yasuda J, Rocheleau C. E, Lin R, Soto M, et al. (1999) MOM-4, a MAP kinase kinase kinase-related protein, activates WRM-1/LIT-1 kinase to transduce anterior/posterior polarity signals in C. elegans. Mol Cell 4: 275-280.
28. Mizumoto K, Sawa H, (2007) Two betas or not two betas: regulation of asymmetric division by beta-catenin. Trends Cell Biol 17: 465-473.
29. Phillips B. T, Kimble J, (2009) A new look at TCF and beta-catenin through the lens of a divergent C. elegans Wnt pathway. Dev Cell 17: 27-34.
30. Lo M. C, Gay F, Odom R, Shi Y, Lin R, (2004) Phosphorylation by the beta-catenin/MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal-responsive cells in C. elegans. Cell 117: 95-106.
31. Kidd A. R, Miskowski J. A, Siegfried K. R, Sawa H, Kimble J, (2005) A beta-catenin identified by functional rather than sequence criteria and its role in Wnt/MAPK signaling. Cell 121: 761-772.
32. Wang Y, Apicella A, Lee S. K, Ezcurra M, Slone R. D, et al. (2008) A glial DEG/ENaC channel functions with neuronal channel DEG-1 to mediate specific sensory functions in C. elegans. EMBO J 27: 2388-2399.
33. Takeshita H, Sawa H, (2005) Asymmetric cortical and nuclear localizations of WRM-1/beta-catenin during asymmetric cell division in C. elegans. Genes Dev 19: 1743-1748.
34. Mizumoto K, Sawa H, (2007) Cortical beta-catenin and APC regulate asymmetric nuclear beta-catenin localization during asymmetric cell division in C. elegans. Dev Cell 12: 287-299.
35. Drenckhahn D, Mannherz H. G, (1983) Distribution of actin and the actin-associated proteins myosin, tropomyosin, alpha-actinin, vinculin, and villin in rat and bovine exocrine glands. Eur J Cell Biol 30: 167-176.
36. Lee R. W, Trifaró J. M, (1981) Characterization of anti-actin antibodies and their use in immunocytochemical studies on the localization of actin in adrenal chromaffin cells in culture. Neuroscience 6: 2087-2108.
37. Watanabe S, Punge A, Hollopeter G, Willig K. I, Hobson R. J, et al. (2011) Protein localization in electron micrographs using fluorescence nanoscopy. Nat Methods 8: 80-84.
38. Withee J, Galligan B, Hawkins N, Garriga G, (2004) Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 167: 1165.
39. Brott B. K, Pinsky B. A, Erikson R. L, (1998) Nlk is a murine protein kinase related to Erk/MAP kinases and localized in the nucleus. Proc Natl Acad Sci U S A 95: 963-968.
40. Choi K. W, Benzer S, (1994) Rotation of photoreceptor clusters in the developing Drosophila eye requires the nemo gene. Cell 78: 125-136.
41. Ishitani T, Ninomiya-Tsuji J, Nagai S, Nishita M, Meneghini M, et al. (1999) The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 399: 798-802.
42. Thorpe C. J, Moon R. T, (2004) nemo-like kinase is an essential co-activator of Wnt signaling during early zebrafish development. Development 131: 2899-2909.
43. Ohkawara B, Shirakabe K, Hyodo-Miura J, Matsuo R, Ueno N, et al. (2004) Role of the TAK1-NLK-STAT3 pathway in TGF-beta-mediated mesoderm induction. Genes Dev 18: 381-386.
44. Ishitani T, Hirao T, Suzuki M, Isoda M, Ishitani S, et al. (2010) Nemo-like kinase suppresses Notch signalling by interfering with formation of the Notch active transcriptional complex. Nat Cell Biol 12: 278-285.
45. Kuwabara P. E, Lee M. H, Schedl T, Jefferis G. S, (2000) A C. elegans patched gene, ptc-1, functions in germ-line cytokinesis. Genes Dev 14: 1933-1944.
46. Cory G. O, Cramer R, Blanchoin L, Ridley A. J, (2003) Phosphorylation of the WASP-VCA domain increases its affinity for the Arp2/3 complex and enhances actin polymerization by WASP. Mol Cell 11: 1229-1239.
47. Lanzetti L, (2007) Actin in membrane trafficking. Curr Opin Cell Biol 19: 453-458.
48. Galletta B. J, Mooren O. L, Cooper J. A, (2010) Actin dynamics and endocytosis in yeast and mammals. Curr Opin Biotechnol 21: 604-610.
49. Malacombe M, Bader M. F, Gasman S, (2006) Exocytosis in neuroendocrine cells: new tasks for actin. Biochim Biophys Acta 1763: 1175-1183.
50. Trifaró J. M, Gasman S, Gutiérrez L. M, (2008) Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf) 192: 165-172.
51. Valentijn J. A, Valentijn K, Pastore L. M, Jamieson J. D, (2000) Actin coating of secretory granules during regulated exocytosis correlates with the release of rab3D. Proc Natl Acad Sci U S A 97: 1091-1095.
52. Gasman S, Chasserot-Golaz S, Malacombe M, Way M, Bader M. F, (2004) Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15: 520-531.
53. Kim S, Shilagardi K, Zhang S, Hong S. N, Sens K. L, et al. (2007) A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev Cell 12: 571-586.
54. Eitzen G, Wang L, Thorngren N, Wickner W, (2002) Remodeling of organelle-bound actin is required for yeast vacuole fusion. J Cell Biol 158: 669-679.
55. Matus D. Q, Li X. Y, Durbin S, Agarwal D, Chi Q, et al. (2010) In vivo identification of regulators of cell invasion across basement membranes. Science signaling 3: ra35.