SAX-7/L1CAM and HMR-1/cadherin function redundantly in blastomere compaction and non-muscle myosin accumulation during Caenorhabditis elegans gastrulation

Developmental Biology

Volumn 344, Issue 2, 2010, Pages 731-744

  Grana, Theresa M ^a   Cox, Elisabeth A ^b   Lynch, Allison M ^c   Hardin, Jeff ^c  

^a UNIVERSITY OF MARY WASHINGTON   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

C. elegans; Cadherin; Gastrulation; L1CAM; Non muscle myosin

Indexed keywords

CADHERIN; CELL PROTEIN; CLASSICAL CADHERIN COMPLEX; MYOSIN; PROTEIN HMR1; PROTEIN SAX 7; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOMERE; CAENORHABDITIS ELEGANS; CELL ADHESION; CELL CONTACT; CELL DIVISION; CELL POLARITY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE LOSS; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

EID: 77955277118     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.05.507     Document Type: Article

References (85)

1. Axang C., Rauthan M., Hall D.H., Pilon M. The twisted pharynx phenotype in C. elegans. BMC Dev. Biol. 2007, 7:61.
2. Babb S.G., Barnett J., Doedens A.L., Cobb N., Liu Q., Sorkin B.C., Yelick P.C., Raymond P.A., Marrs J.A. Zebrafish E-cadherin: expression during early embryogenesis and regulation during brain development. Dev. Dyn. 2001, 221:231-237.
3. Berkowitz L.A., Strome S. MES-1, a protein required for unequal divisions of the germline in early C. elegans embryos, resembles receptor tyrosine kinases and is localized to the boundary between the germline and gut cells. Development 2000, 127:4419-4431.
4. Blackmore M., Letourneau P.C. L1, beta1 integrin, and cadherins mediate axonal regeneration in the embryonic spinal cord. J. Neurobiol. 2006, 66:1564-1583.
5. Boo Y.J., Park J.M., Kim J., Chae Y.S., Min B.W., Um J.W., Moon H.Y. L1 expression as a marker for poor prognosis, tumor progression, and short survival in patients with colorectal cancer. Ann. Surg. Oncol. 2007, 14:1703-1711.
6. Braga V.M., Yap A.S. The challenges of abundance: epithelial junctions and small GTPase signalling. Curr. Opin. Cell Biol. 2005, 17:466-474.
7. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
8. Chen L., Ong B., Bennett V. LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling. J. Cell Biol. 2001, 154:841-855.
9. Chisholm A.D. Gastrulation: Wnts signal constriction. Curr. Biol. 2006, 16:R874-R876.
10. Chisholm A.D., Hardin J. Epidermal morphogenesis. WormBook 2005, 1-22.
11. Costa M., Raich W., Agbunag C., Leung B., Hardin J., Priess J.R. A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 1998, 141:297-308.
12. Cox E.A., Tuskey C., Hardin J. Cell adhesion receptors in C. elegans. J. Cell Sci. 2004, 117:1867-1870.
13. De Vries W.N., Evsikov A.V., Haac B.E., Fancher K.S., Holbrook A.E., Kemler R., Solter D., Knowles B.B. Maternal beta-catenin and E-cadherin in mouse development. Development 2004, 131:4435-4445.
14. Dickson T.C., Mintz C.D., Benson D.L., Salton S.R. Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J. Cell Biol. 2002, 157:1105-1112.
15. Edgar L.G. Blastomere culture and analysis. Meth. Cell Biol. 1995, 48:303-321.
16. Fang X., Ji H., Kim S.W., Park J.I., Vaught T.G., Anastasiadis P.Z., Ciesiolka M., McCrea P.D. Vertebrate development requires ARVCF and p120 catenins and their interplay with RhoA and Rac. J. Cell Biol. 2004, 165:87-98.
17. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000, 408:325-330.
18. 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.
19. Gates J., Peifer M. Can 1000 reviews be wrong? Actin, alpha-Catenin, and adherens junctions. Cell 2005, 123:769-772.
20. Gavert N., Conacci-Sorrell M., Gast D., Schneider A., Altevogt P., Brabletz T., Ben-Ze'ev A. L1, a novel target of beta-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J. Cell Biol. 2005, 168:633-642.
21. Geisbrecht E.R., Montell D.J. Myosin VI is required for E-cadherin-mediated border cell migration. Nat. Cell Biol. 2002, 4:616-620.
22. Ghenea S., Boudreau J.R., Lague N.P., Chin-Sang I.D. The VAB-1 Eph receptor tyrosine kinase and SAX-3/Robo neuronal receptors function together during C. elegans embryonic morphogenesis. Development 2005, 132:3679-3690.
23. Gobel V., Barrett P.L., Hall D.H., Fleming J.T. Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 2004, 6:865-873.
24. Goldstein B., Takeshita H., Mizumoto K., Sawa H. Wnt signals can function as positional cues in establishing cell polarity. Dev. Cell 2006, 10:391-396.
25. Gonczy P., Echeverri C., Oegema K., Coulson A., Jones S.J., Copley R.R., Duperon J., Oegema J., Brehm M., Cassin E., Hannak E., Kirkham M., Pichler S., Flohrs K., Goessen A., Leidel S., Alleaume A.M., Martin C., Ozlu N., Bork P., Hyman A.A. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 2000, 408:331-336.
26. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
27. Haegel H., Larue L., Ohsugi M., Fedorov L., Herrenknecht K., Kemler R. Lack of beta-catenin affects mouse development at gastrulation. Development 1995, 121:3529-3537.
28. Hardin J. Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev. Biol. 1989, 136:430-445.
29. Hardin J., Lockwood C. Skin tight: cell adhesion in the epidermis of Caenorhabditis elegans. Curr. Opin. Cell Biol. 2004, 16:486-492.
30. Heasman J., Ginsberg D., Geiger B., Goldstone K., Pratt T., Yoshida-Noro C., Wylie C. A functional test for maternally inherited cadherin in Xenopus shows its importance in cell adhesion at the blastula stage. Development 1994, 120:49-57.
31. Islam R., Wei S.Y., Chiu W.H., Hortsch M., Hsu J.C. Neuroglian activates Echinoid to antagonize the Drosophila EGF receptor signaling pathway. Development 2003, 130:2051-2059.
32. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
33. Kane D.A., Hammerschmidt M., Mullins M.C., Maischein H.M., Brand M., van Eeden F.J., Furutani-Seiki M., Granato M., Haffter P., Heisenberg C.P., Jiang Y.J., Kelsh R.N., Odenthal J., Warga R.M., Nusslein-Volhard C. The zebrafish epiboly mutants. Development 1996, 123:47-55.
34. Kane D.A., McFarland K.N., Warga R.M. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 2005, 132:1105-1116.
35. Kennedy S., Wang D., Ruvkun G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 2004, 427:645-649.
36. Knight J.K., Wood W.B. Gastrulation initiation in Caenorhabditis elegans requires the function of gad-1, which encodes a protein with WD repeats. Dev. Biol. 1998, 198:253-265.
37. Landsverk M.L., Epstein H.F. Genetic analysis of myosin II assembly and organization in model organisms. Cell. Mol. Life Sci. 2005, 62:2270-2282.
38. Larue L., Ohsugi M., Hirchenhain J., Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl. Acad. Sci. USA 1994, 91:8263-8267.
39. Laufer J.S., Bazzicalupo P., Wood W.B. Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 1980, 19:569-577.
40. Lee J.Y., Goldstein B. Mechanisms of cell positioning during C. elegans gastrulation. Development 2003, 130:307-320.
41. Lee J.Y., Marston D.J., Walston T., Hardin J., Halberstadt A., Goldstein B. Wnt/Frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility. Curr. Biol. 2006, 16:1986-1997.
42. Maddugoda M.P., Crampton M.S., Shewan A.M., Yap A.S. Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell-cell contacts in mammalian epithelial cells. J. Cell Biol. 2007, 178:529-540.
43. Maduro M.F. Endomesoderm specification in Caenorhabditis elegans and other nematodes. Bioessays 2006, 28:1010-1022.
44. Maduro M.F., Rothman J.H. Making worm guts: the gene regulatory network of the Caenorhabditis elegans endoderm. Dev. Biol. 2002, 246:68-85.
45. Maduro M.F., Hill R.J., Heid P.J., Newman-Smith E.D., Zhu J., Priess J.R., Rothman J.H. Genetic redundancy in endoderm specification within the genus Caenorhabditis. Dev. Biol. 2005, 284:509-522.
46. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 2007, 10:19-26.
47. Miller J.R., McClay D.R. Characterization of the role of cadherin in regulating cell adhesion during sea urchin development. Dev. Biol. 1997, 192:323-339.
48. Morton D.G., Shakes D.C., Nugent S., Dichoso D., Wang W., Golden A., Kemphues K.J. The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Dev. Biol. 2002, 241:47-58.
49. Myster S.H., Cavallo R., Anderson C.T., Fox D.T., Peifer M. Drosophila p120catenin plays a supporting role in cell adhesion but is not an essential adherens junction component. J. Cell Biol. 2003, 160:433-449.
50. Nance J., Priess J.R. Cell polarity and gastrulation in C. elegans. Development 2002, 129:387-397.
51. Nance J., Munro E.M., Priess J.R. C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 2003, 130:5339-5350.
52. Nance J., Lee J.Y., Goldstein B. Gastrulation in C. elegans. WormBook 2005, 1-13.
53. Nelson W.J. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 2008, 36:149-155.
54. Norman K.R., Moerman D.G. Alpha spectrin is essential for morphogenesis and body wall muscle formation in Caenorhabditis elegans. J. Cell Biol. 2002, 157:665-677.
55. Ozawa M., Kemler R. The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity. J. Cell Biol. 1998, 142:1605-1613.
56. Peifer M., Yap A.S. Traffic control: p120-catenin acts as a gatekeeper to control the fate of classical cadherins in mammalian cells. J. Cell Biol. 2003, 163:437-440.
57. Pettitt J., Cox E.A., Broadbent I.D., Flett A., Hardin J. The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J. Cell Biol. 2003, 162:15-22.
58. Pocock R., Benard C.Y., Shapiro L., Hobert O. Functional dissection of the C. elegans cell adhesion molecule SAX-7, a homologue of human L1. Mol. Cell. Neurosci. 2008, 37:56-68.
59. Raich W.B., Agbunag C., Hardin J. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Curr. Biol. 1999, 9:1139-1146.
60. Reynolds A.B. p120-catenin: past and present. Biochim. Biophys. Acta 2007, 1773:2-7.
61. Riethmacher D., Brinkmann V., Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl. Acad. Sci. USA 1995, 92:855-859.
62. Rocheleau C.E., Yasuda J., Shin T.H., Lin R., Sawa H., Okano H., Priess J.R., Davis R.J., Mello C.C. WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell 1999, 97:717-726.
63. Sasakura H., Inada H., Kuhara A., Fusaoka E., Takemoto D., Takeuchi K., Mori I. Maintenance of neuronal positions in organized ganglia by SAX-7, a Caenorhabditis elegans homologue of L1. EMBO J. 2005, 24:1477-1488.
64. Schierenberg E. Reversal of cellular polarity and early cell-cell interaction in the embryos of Caenorhabditis elegans. Dev. Biol. 1987, 122:452-463.
65. Schierenberg E., Miwa J., von Ehrenstein G. Cell lineages and developmental defects of temperature-sensitive embryonic arrest mutants in Caenorhabditis elegans. Dev. Biol. 1980, 76:141-159.
66. Schlesinger A., Shelton C.A., Maloof J.N., Meneghini M., Bowerman B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 1999, 13:2028-2038.
67. Scotland P., Zhou D., Benveniste H., Bennett V. Nervous system defects of AnkyrinB (-/-) mice suggest functional overlap between the cell adhesion molecule L1 and 440-kD AnkyrinB in premyelinated axons. J. Cell Biol. 1998, 143:1305-1315.
68. Sheffield M., Loveless T., Hardin J., Pettitt J. C. elegans enabled exhibits novel interactions with N-WASP, Abl, and cell-cell junctions. Curr. Biol. 2007, 17:1791-1796.
69. Shewan A.M., Maddugoda M., Kraemer A., Stehbens S.J., Verma S., Kovacs E.M., Yap A.S. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 2005, 16:4531-4542.
70. Shtutman M., Levina E., Ohouo P., Baig M., Roninson I.B. Cell adhesion molecule L1 disrupts E-cadherin-containing adherens junctions and increases scattering and motility of MCF7 breast carcinoma cells. Cancer Res. 2006, 66:11370-11380.
71. Simske J.S., Koppen M., Sims P., Hodgkin J., Yonkof A., Hardin J. The cell junction protein VAB-9 regulates adhesion and epidermal morphology in C. elegans. Nat. Cell Biol. 2003, 5:619-625.
72. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
73. Tepass U., Gruszynski-DeFeo E., Haag T.A., Omatyar L., Torok T., Hartenstein V. shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 1996, 10:672-685.
74. Thorpe C.J., Schlesinger A., Carter J.C., Bowerman B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 1997, 90:695-705.
75. Uemura T., Oda H., Kraut R., Hayashi S., Kotaoka Y., Takeichi M. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 1996, 10:659-671.
76. Van Furden D., Johnson K., Segbert C., Bossinger O. The C. elegans ezrin-radixin-moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine. Dev. Biol. 2004, 272:262-276.
77. Wacker S., Grimm K., Joos T., Winklbauer R. Development and control of tissue separation at gastrulation in Xenopus. Dev. Biol. 2000, 224:428-439.
78. Walston T., Tuskey C., Edgar L., Hawkins N., Ellis G., Bowerman B., Wood W., Hardin J. Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev. Cell 2004, 7:831-841.
79. Wang X., Kweon J., Larson S., Chen L. A role for the C. elegans L1CAM homologue lad-1/sax-7 in maintaining tissue attachment. Dev. Biol. 2005, 284:273-291.
80. Wei S.Y., Escudero L.M., Yu F., Chang L.H., Chen L.Y., Ho Y.H., Lin C.M., Chou C.S., Chia W., Modolell J., Hsu J.C. Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev. Cell 2005, 8:493-504.
81. Yamada S., Nelson W.J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 2007, 178:517-527.
82. Zallen J.A., Kirch S.A., Bargmann C.I. Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 1999, 126:3679-3692.
83. Zar J. Biotsatisical Analysis 2010, Pearson/Prentice-Hall, Upper Saddle River, NJ.
84. Zhou D., Lambert S., Malen P.L., Carpenter S., Boland L.M., Bennett V. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J. Cell Biol. 1998, 143:1295-1304.
85. Zhou S., Opperman K., Wang X., Chen L. unc-44 Ankyrin and stn-2 gamma-syntrophin regulate sax-7 L1CAM function in maintaining neuronal positioning in Caenorhabditis elegans. Genetics 2008, 180:1429-1443.