The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation during Gonad Morphogenesis

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Sano, Hiroko ^a,g   Kunwar, Prabhat S ^a,h   Renault, Andrew D ^a,i   Barbosa, Vitor ^a,j   Clark, Ivan B N ^b   Ishihara, Shuji ^c,d   Sugimura, Kaoru ^e,f   Lehmann, Ruth ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Centre for Systems Biology at Edinburgh   (United Kingdom)

^c UNIVERSITY OF TOKYO   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^g KURUME UNIVERSITY   (Japan)

^h CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

ⁱ MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^j INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CADHERIN; ENABLED PROTEIN; GREEN FLUORESCENT PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ORIENTATION; CELL SHAPE; CELLULAR PARAMETERS; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENA GENE; GENE MUTATION; GONAD DEVELOPMENT; NONHUMAN; PRIMORDIAL GERM CELL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIMULATION; SOMATIC GONADAL PRECURSOR; STEM CELL;

ANIMALS; CADHERINS; CELL SHAPE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GERM CELLS; GONADS; MODELS, BIOLOGICAL; MORPHOGENESIS; ORGANOGENESIS; PROTEIN TRANSPORT; STEM CELLS; TIME-LAPSE IMAGING;

ENA;

EID: 84871571667     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052649     Document Type: Article

References (57)

1. Sonnenblick BP, (1941) Germ Cell Movements and Sex Differentiation of the Gonads in the Drosophila Embryo. Proc Natl Acad Sci U S A 27: 484-489.
2. Clark IB, Jarman AP, Finnegan DJ, (2007) Live imaging of Drosophila gonad formation reveals roles for Six4 in regulating germline and somatic cell migration. BMC Dev Biol 7: 52.
3. Richardson BE, Lehmann R, (2010) Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 11: 37-49.
4. Sano H, Renault AD, Lehmann R, (2005) Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J Cell Biol 171: 675-683.
5. Kunwar PS, Sano H, Renault AD, Barbosa V, Fuse N, et al. (2008) Tre1 GPCR initiates germ cell transepithelial migration by regulating Drosophila melanogaster E-cadherin. J Cell Biol 183: 157-168.
6. Brookman JJ, Toosy AT, Shashidhara LS, White RA, (1992) The 412 retrotransposon and the development of gonadal mesoderm in Drosophila. Development 116: 1185-1192.
7. Warrior R, (1994) Primordial germ cell migration and the assembly of the Drosophila embryonic gonad. Dev Biol 166: 180-194.
8. Boyle M, DiNardo S, (1995) Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121: 1815-1825.
9. Broihier HT, Moore LA, Van Doren M, Newman S, Lehmann R, (1998) zfh-1 is required for germ cell migration and gonadal mesoderm development in Drosophila. Development 125: 655-666.
10. Moore LA, Broihier HT, Van Doren M, Lehmann R, (1998) Gonadal mesoderm and fat body initially follow a common developmental path in Drosophila. Development 125: 837-844.
11. Moore LA, Broihier HT, Van Doren M, Lunsford LB, Lehmann R, (1998) Identification of genes controlling germ cell migration and embryonic gonad formation in Drosophila. Development 125: 667-678.
12. Riechmann V, Rehorn KP, Reuter R, Leptin M, (1998) The genetic control of the distinction between fat body and gonadal mesoderm in Drosophila. Development 125: 713-723.
13. Jenkins AB, McCaffery JM, Van Doren M, (2003) Drosophila E-cadherin is essential for proper germ cell-soma interaction during gonad morphogenesis. Development 130: 4417-4426.
14. Van Doren M, Mathews WR, Samuels M, Moore LA, Broihier HT, et al. (2003) fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development 130: 2355-2364.
15. Mathews WR, Ong D, Milutinovich AB, Van Doren M, (2006) Zinc transport activity of Fear of Intimacy is essential for proper gonad morphogenesis and DE-cadherin expression. Development 133: 1143-1153.
16. Weyers JJ, Milutinovich AB, Takeda Y, Jemc JC, Van Doren M, (2011) A genetic screen for mutations affecting gonad formation in Drosophila reveals a role for the slit/robo pathway. Dev Biol 353: 217-228.
17. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, et al. (2002) Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109: 509-521.
18. Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, et al. (2005) Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J Biol Chem 280: 28653-28662.
19. Bear JE, Loureiro JJ, Libova I, Fassler R, Wehland J, et al. (2000) Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101: 717-728.
20. Wills Z, Bateman J, Korey CA, Comer A, Van Vactor D, (1999) The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22: 301-312.
21. Gates J, Mahaffey JP, Rogers SL, Emerson M, Rogers EM, et al. (2007) Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134: 2027-2039.
22. Homem CC, Peifer M, (2009) Exploring the roles of diaphanous and enabled activity in shaping the balance between filopodia and lamellipodia. Mol Biol Cell 20: 5138-5155.
23. Gates J, Nowotarski SH, Yin H, Mahaffey JP, Bridges T, et al. (2009) Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev Biol 333: 90-107.
24. Tucker PK, Evans IR, Wood W, (2011) Ena drives invasive macrophage migration in Drosophila embryos. Dis Model Mech 4: 126-134.
25. Vasioukhin V, Bauer C, Yin M, Fuchs E, (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100: 209-219.
26. Scott JA, Shewan AM, den Elzen NR, Loureiro JJ, Gertler FB, et al. (2006) Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol Biol Cell 17: 1085-1095.
27. Baum B, Perrimon N, (2001) Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat Cell Biol 3: 883-890.
28. Barbosa V, Kimm N, Lehmann R, (2007) A maternal screen for genes regulating Drosophila oocyte polarity uncovers new steps in meiotic progression. Genetics 176: 1967-1977.
29. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB, (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19: 541-564.
30. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, et al. (2004) Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118: 363-373.
31. Lehmann R, Nusslein-Volhard C, (1986) Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47: 141-152.
32. Comer AR, Ahern-Djamali SM, Juang JL, Jackson PD, Hoffmann FM, (1998) Phosphorylation of Enabled by the Drosophila Abelson tyrosine kinase regulates the in vivo function and protein-protein interactions of Enabled. Mol Cell Biol 18: 152-160.
33. Edwards KA, Demsky M, Montague RA, Weymouth N, Kiehart DP, (1997) GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev Biol 191: 103-117.
34. Clark IB, Boyd J, Hamilton G, Finnegan DJ, Jarman AP, (2006) D-six4 plays a key role in patterning cell identities deriving from the Drosophila mesoderm. Dev Biol 294: 220-231.
35. Kirby RJ, Hamilton GM, Finnegan DJ, Johnson KJ, Jarman AP, (2001) Drosophila homolog of the myotonic dystrophy-associated gene, SIX5, is required for muscle and gonad development. Curr Biol 11: 1044-1049.
36. Lecuit T, Lenne PF, (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8: 633-644.
37. Krieg M, Arboleda-Estudillo Y, Puech PH, Kafer J, Graner F, et al. (2008) Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10: 429-436.
38. Gilboa L, Lehmann R, (2004) How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males. Development 131: 4895-4905.
39. DeFalco T, Le Bras S, Van Doren M, (2004) Abdominal-B is essential for proper sexually dimorphic development of the Drosophila gonad. Mech Dev 121: 1323-1333.
40. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M, (2010) alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12: 533-542.
41. Simpson JH, Kidd T, Bland KS, Goodman CS, (2000) Short-range and long-range guidance by slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance. Neuron 28: 753-766.
42. Hivert B, Liu Z, Chuang CY, Doherty P, Sundaresan V, (2002) Robo1 and Robo2 are homophilic binding molecules that promote axonal growth. Mol Cell Neurosci 21: 534-545.
43. Spitzweck B, Brankatschk M, Dickson BJ, (2010) Distinct protein domains and expression patterns confer divergent axon guidance functions for Drosophila Robo receptors. Cell 140: 409-420.
44. Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS, (2000) Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101: 703-715.
45. Gertler FB, Comer AR, Juang JL, Ahern SM, Clark MJ, et al. (1995) enabled, a dosage-sensitive suppressor of mutations in the Drosophila Abl tyrosine kinase, encodes an Abl substrate with SH3 domain-binding properties. Genes Dev 9: 521-533.
46. Ahern-Djamali SM, Comer AR, Bachmann C, Kastenmeier AS, Reddy SK, et al. (1998) Mutations in Drosophila enabled and rescue by human vasodilator-stimulated phosphoprotein (VASP) indicate important functional roles for Ena/VASP homology domain 1 (EVH1) and EVH2 domains. Mol Biol Cell 9: 2157-2171.
47. Tepass U, Gruszynski-DeFeo E, Haag TA, Omatyar L, Torok T, et al. (1996) shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev 10: 672-685.
48. Fox DT, Homem CC, Myster SH, Wang F, Bain EE, et al. (2005) Rho1 regulates Drosophila adherens junctions independently of p120ctn. Development 132: 4819-4831.
49. Peifer M, Wieschaus E, (1990) The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63: 1167-1176.
50. Zhao DB, Cote S, Jahnig F, Haller J, Jackle H, (1988) Zipper encodes a putative integral membrane protein required for normal axon patterning during Drosophila neurogenesis. EMBO J 7: 1115-1119.
51. Van Doren M, Williamson AL, Lehmann R, (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8: 243-246.
52. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
53. Lehmann R, Tautz D, (1994) In situ hybridization to RNA. Methods Cell Biol 44: 575-598.
54. Glazier JA, Graner F, (1993) Simulation of the differential adhesion driven rearrangement of biological cells. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 47: 2128-2154.
55. Farhadifar R, Roper JC, Aigouy B, Eaton S, Julicher F, (2007) The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17: 2095-2104.
56. Nakajima A, Ishihara S, (2011) Kinetics of the cellular Potts model revisited. New Jour Phys 3: 033035.
57. Ishihara S, Sugimura K, (2012) Bayesian inference of force dynamics during morphogenesis. J Theor Biol 313C: 201-211.