A vertebrate-specific Chp-PAK-PIX pathway maintains E-cadherin at adherens junctions during zebrafish epiboly

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Tay, Hwee Goon ^a   Ng, Yuen Wai ^b   Manser, Ed ^a,b  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PAK INTERACTING EXCHANGE FACTOR; ADAPTOR PROTEIN; BETA CATENIN; F ACTIN; MESSENGER RNA; OLIGONUCLEOTIDE; P21 ACTIVATED KINASE; PHOSPHOTRANSFERASE; PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS;

ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL ADHESION; CELL JUNCTION; CELL MOTION; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GASTRULATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VERTEBRATE; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; METABOLISM; PHYSIOLOGY;

DANIO RERIO; VERTEBRATA;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CELL ADHESION; CELL MOVEMENT; EMBRYO, NONMAMMALIAN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; P21-ACTIVATED KINASES; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; VERTEBRATES; ZEBRAFISH;

EID: 77954633149     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010125     Document Type: Article

References (89)

1. Babb SG, Marrs JA (2004) E-cadherin regulates cell movements and tissue formation in early zebrafish embryos. Dev Dyn 230: 263-277.
2. Montero JA, Carvalho L, Wilsch-Brauninger M, Kilian B, Mustafa C, et al. (2005) Shield formation at the onset of zebrafish gastrulation. Development 132:1187-1198.
3. Ulrich F, Krieg M, Schotz EM, Link V, Castanon I, et al. (2005) Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and Ecadherin. Dev Cell 9: 555-564.
4. Shimizu T, Yabe T, Muraoka O, Yonemura S, Aramaki S, et al. (2005) Ecadherin is required for gastrulation cell movements in zebrafish. Mech Dev 122:747-763.
5. Kane DA, McFarland KN, Warga RM (2005) Mutations in half baked/Ecadherin block cell behaviors that are necessary for teleost epiboly. Development 132: 1105-1116.
6. Buchner DA, Su F, Yamaoka JS, Kamei M, Shavit JA, et al. (2007) pak2a mutations cause cerebral hemorrhage in redhead zebrafish. Proc Natl Acad Sci USA 104: 13996-14001.
7. Liu J, Fraser SD, Faloon PW, Rollins EL, Vom Berg J, et al. (2007) A betaPix Pak2a signaling pathway regulates cerebral vascular stability in zebrafish. Proc Natl Acad Sci USA 104: 13990-13995.
8. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420: 629-635.
9. Raftopoulou M, Hall A (2004) Cell migration: Rho GTPases lead the way. Dev Biol 265: 23-32.
10. Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690-701.
11. Perez-Moreno M, Jamora C, Fuchs E (2003) Sticky business: orchestrating cellular signals at adherens junctions. Cell 112: 535-548.
12. Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6: 622-634.
13. Fukata M, Kaibuchi K (2001) Rho-family GTPases in cadherin-mediated cellcell adhesion. Nat Rev Mol Cell Biol 2: 887-897.
14. Salas-Vidal E, Meijer AH, Cheng X, Spaink HP (2005) Genomic annotation and expression analysis of the zebrafish Rho small GTPase family during development and bacterial infection. Genomics 86: 25-37.
15. Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, et al. (1998) Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17: 3427-3433.
16. Choi SC, Han JK (2002) Xenopus Cdc42 regulates convergent extension movements during gastrulation through Wnt/Ca2+ signaling pathway. Dev Biol 244: 342-357.
17. Habas R, Dawid IB, He X (2003) Coactivation of Rac and Rho by Wnt/ Frizzled signaling is required for vertebrate gastrulation. Genes Dev 17:295-309.
18. Lai SL, Chang CN, Wang PJ, Lee SJ (2005) Rho mediates cytokinesis and epiboly via ROCK in zebrafish. Mol Reprod Dev 71: 186-196.
19. Kinoshita N, Sasai N, Misaki K, Yonemura S (2008) Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation. Mol Biol Cell 19: 2289-2299.
20. Wherlock M, Mellor H (2002) The Rho GTPase family: a Racs to Wrchs story. J Cell Sci 115: 239-240.
21. Solnica-Krezel L (2006) Gastrulation in zebrafish -- all just about adhesion? Curr Opin Genet Dev 16: 433-441.
22. Montero JA, Heisenberg CP (2004) Gastrulation dynamics: cells move into focus. Trends Cell Biol 14: 620-627.
23. Solnica-Krezel L, Driever W (1994) Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120: 2443-2455.
24. Cheng JC, Miller AL, Webb SE (2004) Organization and function of microfilaments during late epiboly in zebrafish embryos. Dev Dyn 231:313-323.
25. Strahle U, Jesuthasan S (1993) Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119: 909-919.
26. Aronheim A, Broder YC, Cohen A, Fritsch A, Belisle B, et al. (1998) Chp, a homologue of the GTPase Cdc42Hs, activates the JNK pathway and is implicated in reorganizing the actin cytoskeleton. Curr Biol 8: 1125-1128.
27. Weisz Hubsman M, Volinsky N, Manser E, Yablonski D, Aronheim A (2007) Autophosphorylation-dependent degradation of Pak1, triggered by the Rhofamily GTPase, Chp. Biochem J 404: 487-497.
28. Guemar L, de Santa Barbara P, Vignal E, Maurel B, Fort P, et al. (2007) The small GTPase RhoV is an essential regulator of neural crest induction in Xenopus. Dev Biol 310: 113-128.
29. Notarnicola C, Le Guen L, Fort P, Faure S, de Santa Barbara P (2008) Dynamic expression patterns of RhoV/Chp and RhoU/Wrch during chicken embryonic development. Dev Dyn 237: 1165-1171.
30. Chenette EJ, Abo A, Der CJ (2005) Critical and distinct roles of amino- and carboxyl-terminal sequences in regulation of the biological activity of the Chp atypical Rho GTPase. J Biol Chem 280: 13784-13792.
31. Kang R, Wan J, Arstikaitis P, Takahashi H, Huang K, et al. (2008) Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456: 904-909.
32. Zalik SE, Lewandowski E, Kam Z, Geiger B (1999) Cell adhesion and the actin cytoskeleton of the enveloping layer in the zebrafish embryo during epiboly. Biochem Cell Biol 77: 527-542.
33. Hsu HJ, Liang MR, Chen CT, Chung BC (2006) Pregnenolone stabilizes microtubules and promotes zebrafish embryonic cell movement. Nature 439:480-483.
34. Warga RM, Kane DA (2007) A role for N-cadherin in mesodermal morphogenesis during gastrulation. Dev Biol 310: 211-225.
35. Noren NK, Liu BP, Burridge K, Kreft B (2000) p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J Cell Biol 150: 567-580.
36. Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI (2005) Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actinfilament assembly. Cell 123: 903-915.
37. Weis WI, Nelson WJ (2006) Re-solving the cadherin-catenin-actin conundrum. J Biol Chem 281: 35593-35597.
38. Ulrich F, Heisenberg CP (2008) Probing E-cadherin endocytosis by morpholinomediated Rab5 knockdown in zebrafish. Methods Mol Biol 440: 371-387.
39. Shook D, Keller R (2003) Mechanisms, mechanics and function of epithelialmesenchymal transitions in early development. Mech Dev 120: 1351-1383.
40. Kim SH, Li Z, Sacks DB (2000) E-cadherin-mediated cell-cell attachment activates Cdc42. J Biol Chem 275: 36999-37005.
41. Nakagawa M, Fukata M, Yamaga M, Itoh N, Kaibuchi K (2001) Recruitment and activation of Rac1 by the formation of E-cadherin-mediated cell-cell adhesion sites. J Cell Sci 114: 1829-1838.
42. Motley A, Bright NA, Seaman MN, Robinson MS (2003) Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162: 909-918.
43. Manser E, Leung T, Salihuddin H, Zhao ZS, Lim L (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367: 40-46.
44. Manser E, Loo TH, Koh CG, Zhao ZS, Chen XQ, et al. (1998) PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol Cell 1:183-192.
45. Koh CG, Manser E, Zhao ZS, Ng CP, Lim L (2001) Beta1PIX, the PAKinteracting exchange factor, requires localization via a coiled-coil region to promote microvillus-like structures and membrane ruffles. J Cell Sci 114:4239-4251.
46. Loo TH, Ng YW, Lim L, Manser E (2004) GIT1 activates p21-activated kinase through a mechanism independent of p21 binding. Mol Cell Biol 24: 3849-3859.
47. Shin EY, Lee CS, Cho TG, Kim YG, Song S, et al. (2006) betaPak-interacting exchange factor-mediated Rac1 activation requires smgGDS guanine nucleotide exchange factor in basic fibroblast growth factor-induced neurite outgrowth. J Biol Chem 281: 35954-35964.
48. Zhao ZS, Lim JP, Ng YW, Lim L, Manser E (2005) The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A. Mol Cell 20: 237-249.
49. Chong C, Tan L, Lim L, Manser E (2001) The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J Biol Chem 276: 17347-17353.
50. Lozano E, Frasa MA, Smolarczyk K, Knaus UG, Braga VM (2008) PAK is required for the disruption of E-cadherin adhesion by the small GTPase Rac. J Cell Sci 121: 933-938.
51. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, et al. (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81.
52. Ulrich F, Concha ML, Heid PJ, Voss E, Witzel S, et al. (2003) Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation. Development 130: 5375-5384.
53. Nandadasa S, Tao Q, Menon NR, Heasman J, Wylie C (2009) N- and Ecadherins in Xenopus are specifically required in the neural and non-neural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development 136: 1327-1338.
54. Christofori G, Semb H (1999) The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci 24: 73-76.
55. Thiery JP (2003) Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 15: 740-746.
56. Akhtar N, Hotchin NA (2001) RAC1 regulates adherens junctions through endocytosis of E-cadherin. Mol Biol Cell 12: 847-862.
57. Keely PJ, Westwick JK, Whitehead IP, Der CJ, Parise LV (1997) Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature 390: 632-636.
58. Yagi R, Waguri S, Sumikawa Y, Nada S, Oneyama C, et al. (2007) C-terminal Src kinase controls development and maintenance of mouse squamous epithelia. EMBO J 26: 1234-1244.
59. Braga VM, Betson M, Li X, Lamarche-Vane N (2000) Activation of the small GTPase Rac is sufficient to disrupt cadherin-dependent cell-cell adhesion in normal human keratinocytes. Mol Biol Cell 11: 3703-3721.
60. Stappenbeck TS, Gordon JI (2000) Rac1 mutations produce aberrant epithelial differentiation in the developing and adult mouse small intestine. Development 127: 2629-2642.
61. Pirraglia C, Jattani R, Myat MM (2006) Rac function in epithelial tube morphogenesis. Dev Biol 290: 435-446.
62. Chihara T, Kato K, Taniguchi M, Ng J, Hayashi S (2003) Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 130: 1419-1428.
63. Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, et al. (2008) Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134: 135-147.
64. Leskow FC, Holloway BA, Wang H, Mullins MC, Kazanietz MG (2006) The zebrafish homologue of mammalian chimerin Rac-GAPs is implicated in epiboly progression during development. Proc Natl Acad Sci USA 103: 5373-5378.
65. Palacios F, Tushir JS, Fujita Y, D'Souza-Schorey C (2005) Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol 25: 389-402.
66. Palacios F, Price L, Schweitzer J, Collard JG, D'Souza-Schorey C (2001) An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. Embo J 20: 4973-4986.
67. Parnas D, Haghighi AP, Fetter RD, Kim SW, Goodman CS (2001) Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 32: 415-424.
68. Donaldson JG, Jackson CL (2000) Regulators and effectors of the ARF GTPases. Curr Opin Cell Biol 12: 475-482.
69. Georgiou M, Marinari E, Burden J, Baum B (2008) Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18: 1631-1638.
70. Leibfried A, Fricke R, Morgan MJ, Bogdan S, Bellaiche Y (2008) Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr Biol 18: 1639-1648.
71. Noren NK, Niessen CM, Gumbiner BM, Burridge K (2001) Cadherin engagement regulates Rho family GTPases. J Biol Chem 276: 33305-33308.
72. Takaishi K, Sasaki T, Kotani H, Nishioka H, Takai Y (1997) Regulation of cellcell adhesion by rac and rho small G proteins in MDCK cells. J Cell Biol 139:1047-1059.
73. Kuroda S, Fukata M, Fujii K, Nakamura T, Izawa I, et al. (1997) Regulation of cell-cell adhesion of MDCK cells by Cdc42 and Rac1 small GTPases. Biochem Biophys Res Commun 240: 430-435.
74. Braga VM, Machesky LM, Hall A, Hotchin NA (1997) The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J Cell Biol 137: 1421-1431.
75. Kardash E, Reichman-Fried M, Maitre JL, Boldajipour B, Papusheva E, et al. A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat Cell Biol 12: 47-53; suppp 41-11.
76. Harden N, Ricos M, Ong YM, Chia W, Lim L (1999) Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J Cell Sci 112 (Pt3): 273-284.
77. Lin F, Chen S, Sepich DS, Panizzi JR, Clendenon SG, et al. (2009) Galpha12/ 13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J Cell Biol 184: 909-921.
78. Larue L, Ohsugi M, Hirchenhain J, Kemler R (1994) E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA 91: 8263-8267.
79. Missy K, Hu B, Schilling K, Harenberg A, Sakk V, et al. (2008) AlphaPIX Rho GTPase guanine nucleotide exchange factor regulates lymphocyte functions and antigen receptor signaling. Mol Cell Biol 28: 3776-3789.
80. Bahri SM, Choy JM, Manser E, Lim L, Yang X (2009) The Drosophila homologue of Arf-GAP GIT1, dGIT, is required for proper muscle morphogenesis and guidance during embryogenesis. Dev Biol 325: 15-23.
81. Williams MJ, Lowrie MB, Bennett JP, Firth JA, Clark P (2005) Cadherin-10 is a novel blood-brain barrier adhesion molecule in human and mouse. Brain Res 1058: 62-72.
82. Hofmann C, Shepelev M, Chernoff J (2004) The genetics of Pak. J Cell Sci 117: 4343-4354.
83. Hayashi ML, Rao BS, Seo JS, Choi HS, Dolan BM, et al. (2007) Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proc Natl Acad Sci USA 104: 11489-11494.
84. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, et al. (2004) Altered cortical synaptic morphology and impaired memory consolidation in forebrain- specific dominant-negative PAK transgenic mice. Neuron 42: 773-787.
85. Dzamba BJ, Jakab KR, Marsden M, Schwartz MA, DeSimone DW (2009) Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization. Dev Cell 16: 421-432.
86. Djiane A, Riou J, Umbhauer M, Boucaut J, Shi D (2000) Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127: 3091-3100.
87. Munoz-Descalzo S, Gomez-Cabrero A, Mlodzik M, Paricio N (2007) Analysis of the role of the Rac/Cdc42 GTPases during planar cell polarity generation in Drosophila. Int J Dev Biol 51: 379-387.
88. Kim GH, Han JK (2005) JNK and ROKalpha function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. Dev Dyn 232: 958-968.
89. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.