PS integrins and laminins: Key regulators of cell migration during drosophila embryogenesis

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Urbano, Jose M ^a,c   Domínguez Giménez, Paloma ^b   Estrada, Beatriz ^a   Martín Bermudo, María D ^a  

^a Departamento de Biología Molecular e Ingeniería Bioquímica   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; LAMININ; LAMININA; LAMININW; PS INTEGRIN; PS1 INTEGRIN; PS2 INTEGRIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; BLOOD CELL; CELL MIGRATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; MESODERM; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; ANIMAL EMBRYO; CELL MOTION; CONFOCAL MICROSCOPY; CYTOLOGY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; PRENATAL DEVELOPMENT; TIME LAPSE IMAGING; TRANSGENIC ANIMAL;

VERTEBRATA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MOVEMENT; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GREEN FLUORESCENT PROTEINS; IN SITU HYBRIDIZATION; INTEGRINS; LAMININ; MESODERM; MICROSCOPY, CONFOCAL; TIME-LAPSE IMAGING;

EID: 80052853791     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023893     Document Type: Article

References (69)

1. Bokel C, Brown NH, (2002) Integrins in Development: moving on, respoding to, and sticking to the extracellular matrix. Developmental Cell 3: 311-321.
2. Roote CE, Zusman S, (1995) Functions for PS integrins in tissue adhesion, migration, and shape changes during early embryonic development in Drosophila. Dev Biol 169: 322-336.
3. Martin-Bermudo MD, Alvarez-Garcia I, Brown NH, (1999) Migration of the drosophila primordial midgut cells requires coordination of diverse PS integrin functions. Development 126: 5161-5169.
4. Boube M, Martin-Bermudo MD, Brown N, Casanova J, (2001) Specific tracheal migration is mediated by complementary expression of cell surface proteins. Genes and development 15: 1554-1562.
5. Devenport D, Brown NH, (2004) Morphogenesis in the absence of integrins:mutation of both Drosophila βsubunits prevents midgut migration. Development 131: 5405-5415.
6. Bradley PL, Myat MM, Comeaux CA, Andrew DJ, (2003) Posterior migration of the salivary gland requires an intact visceral mesoderm and integrin function. Dev Biol 257: 249-262.
7. Reuter R, Grunewald B, Leptin M, (1993) A role for mesoderm in endodermal migration and morphogenesis in Drosophila. Development 119: 1135-1145.
8. Tepass U, Hartenstein V, (1994) Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 120: 579-590.
9. Georgias C, Wasser M, Hinz U, (1997) A basic-helix-loop-helix proetin expressed in precursors of Drosophila longitudinal visceral muscles. Mech Dev 69: 115-124.
10. Kusch T, Reuter R, (1999) Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling. Development 126: 3991-4003.
11. Zaffran S, Kuchler A, Lee HH, Frasch M, (2001) biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila. Genes Dev 15: 2900-2915.
12. Narasimha M, Brown NH, (2005) Integrins and associated proteins in Drosophila development. Integrins and Development Edited by Erik Danen.Eurekah.com.
13. Leptin M, Bogaert T, Lehmann R, Wilcox M, (1989) The function of PS integrins during Drosophila embryogenesis. Cell 56: 401-408.
14. Swan LE, Wichmann C, Prange U, Schmid A, Schmidt M, et al. (2004) A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev 18: 223-237.
15. Hacker U, Kaufmann E, Hartmann C, Jurgens G, Knochel W, et al. (1995) The Drosophila fork head domain protein crocodile is required for the establishment of head structures. EMBO J 14: 5306-5317.
16. Ismat A, Schaub C, Reim I, Kirchner K, Schultheis D, et al. (2010) HLH54F is required for the specification and migration of longitudinal gut muscle founders from the caudal mesoderm of Drosophila. Development 137: 3107-3117.
17. Horwitz A, Duggan K, Buck C, Beckerle MC, Burridge K, (1986) Interaction of plasma mambrane fibronectin receptor with Talin- a transmembrane linkage. Nature 320: 531-533.
18. Brown NH, Gregory SL, Rickoll WL, Fessler LI, Prout M, et al. (2002) Talin is essential for integrin function in Drosophila. Developmental Cell 3: 569-579.
19. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
20. Schock F, Perrimon N, (2003) Retraction of the Drosophila germ band requires cell-matrix interaction. Genes Dev 17: 597-602.
21. Brower DL, Bunch TA, Mukai L, Adamson TE, Wehrli M, et al. (1995) Nonequivalent requirements for PS1 and PS2 integrin at cell attachments in Drosophila: genetic analysis of the αPS1 integrin subunit. Development 121: 1311-1320.
22. Bogaert T, Brown N, Wilcox M, (1987) The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments. Cell 51: 929-940.
23. Stark KA, Yee GH, Roote CE, Williams EL, Zusman S, et al. (1997) A novel α integrin subunit associates with βPS and functions in tissue morphogenesis and movement during Drosophila development. Development 124: 4583-4594.
24. Brown NH, (1994) Null mutations in the αPS2 and βPS integrin subunit genes have distinct phenotypes. Development 120: 1221-1231.
25. Wehrli M, DiAntonio A, Fearnley IM, Smith RJ, Wilcox M, (1993) Cloning and characterization of αPS1, a novel Drosophila melanogaster integrin. Mech Dev 43: 21-36.
26. Martin-Bermudo MD, Dunin-Borkowski OM, Brown NH, (1997) Specificity of PS integrin function during embryogenesis resides in the α subunit extracellular domain. EMBO 16: 4184-4193.
27. Narasimha M, Brown NH, (2004) Novel functions for integrins in epithelial morphogenesis. Current Biology 14: 381-385.
28. Tanentzapf G, Devenport D, Godt D, Brown NH, (2007) Integrin-dependent anchoring of a stem-cell niche. Nat Cell Biol 9: 1413-1418.
29. Martin D, Zusman S, Li X, Williams EL, Khare N, et al. (1999) wing blister, a new drosophila Laminin α chain required for cell adhesion and migration during embryonic and imaginal development. J Cell Biol 145: 191-201.
30. Urbano JM, Torgler CN, Molnar C, Tepass U, Lopez-Varea A, et al. (2009) Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 136: 4165-4176.
31. Fessler LI, Nelson RE, Fessler JH, (1994) Drosophila extracellular matrix. Methods Enzymol 245: 271-294.
32. Tepass U, Fessler LI, Aziz A, Hartenstein V, (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120: 1829-1837.
33. Paladi M, Tepass U, (2004) Function of Rho GTPases in embryonic blood cell migration in Drosophila. J Cell Sci 117: 6313-6326.
34. Rehorn KP, Thelen H, Michelson AM, Reuter R, (1996) A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila. Development 122: 4023-4031.
35. Reuter R, (1994) The gene serpent has homeotic properties and specifies endoderm versus ectoderm within the Drosophila gut. Development 120: 1123-1135.
36. Brabant MC, Fristrom D, Bunch TA, Brower DL, (1996) Distinct spatial and temporal functions for PS integrins during Drosophila wing morphogenesis. Development 122: 3307-3317.
37. Martin-Bermudo MD, Brown NH, (1999) Uncoupling integrin adhesion and signaling: the βPS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo. Genes Dev 13: 729-739.
38. Li WH, Yang J, Gu X, (2005) Expression divergence between duplicate genes. Trends Genet 21: 602-607.
39. Hughes AL, (2001) Evolution of the integrins α and β protein family. J Mol Evol 52: 63-72.
40. Hsia CC, McGinnis W, (2003) Evolution of transcription factor function. Curr Opin Genet Dev 13: 199-206.
41. Delon I, Brown NH, (2009) The integrin adhesion complex changes its composition and function during morphogenesis of an epithelium. J Cell Sci 122: 4363-4374.
42. Chan BM, Kassner PD, Schiro JA, Byers HR, Kupper TS, et al. (1992) Distinct cellular functions mediated by different VLA integrin alpha subunit cytoplasmic domains. Cell 68: 1051-1060.
43. Gotwals PJ, Fessler LI, Wehril M, Hynes RO, (1994) Drosophila PS1 integrin is a laminin receptor and differs in ligand specificity from PS2. Proc Natl Acad Sci 91: 11447-11451.
44. Darribere T, Guida K, Lajarva H, Johnson KE, Yamada KM, et al. (1990) In vivo analyses of integrin b1 subunit function in fibronectin matrix assembly. J Cell Biol 110: 1813-1823.
45. Skalski M, Alfandari D, Darribere T, (1998) A key function for alphav containing integrins in mesodermal cell migration during Pleurodeles waltl gastrulation. Dev Biol 195: 158-173.
46. Tzu J, Marinkovich MP, (2008) Bridging structure with function: structural, regulatory, and developmental role of laminins. Int J Biochem Cell Biol 40: 199-214.
47. MacMullin A, Jacobs JR, (2006) Slit coordinates cardiac morphogenesis in Drosophila. Dev Biol 293: 154-164.
48. Stevens A, Jacobs JR, (2002) Integrins regulate responsiveness to slit repellent signals. J Neurosci 22: 4448-4455.
49. Lee HK, Seo IA, Park HK, Park YM, Ahn KJ, et al. (2007) Nidogen is a prosurvival and promigratory factor for adult Schwann cells. J Neurochem 102: 686-698.
50. Yelian FD, Edgeworth NA, Dong LJ, Chung AE, Armant DR, (1993) Recombinant entactin promotes mouse primary trophoblast cell adhesion and migration through the Arg-Gly-Asp (RGD) recognition sequence. J Cell Biol 121: 923-929.
51. Dedhar S, Jewell K, Rojiani M, Gray V, (1992) The receptor for the basement membrane glycoprotein entactin is the integrin alpha 3/beta 1. J Biol Chem 267: 18908-18914.
52. Fessler JH, Fessler LI, (1989) Drosophila extracellular matrix. Annu Rev Cell Biol 5: 309-339.
53. Wood W, Jacinto A, (2007) Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat Rev Mol Cell Biol 8: 542-551.
54. Kusche-Gullberg M, Garrison K, Mackrell AJ, Fessler LI, Fessler JH, (1992) Laminin A chain: expression during Drosophila development and genomic sequence. EMBO J 11: 4519-4527.
55. Frank DE, Carter WG, (2004) Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J Cell Sci 117: 1351-1363.
56. Deng W-M, Schneider M, Frock R, Castillejo-Lopez C, Gaman EA, et al. (2003) Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130: 173-184.
57. Henchcliffe C, Garcia-Alonso L, Tang J, Goodman CS, (1993) Genetic analysis of laminin A reveals diverse functions during morphogenesis in Drosophila. Development 118: 325-337.
58. Bunch TA, Brower DL, (1992) Drosophila PS2 integrin mediates RGD-dependent cell-matrix interactions. Development 116: 239-247.
59. Prout M, Damania Z, Soong J, Fristrom D, Fristrom JW, (1997) Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics 146: 275-285.
60. Voigt A, Pflanz R, Schafer U, Jackle H, (2002) Perlecan participates in proliferation activation of quiescent Drosophila neuroblasts. Dev Dyn 224: 403-412.
61. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
62. Shiga Y, Tanaka-Matakatsu M, Hayashi S, (1996) A nuclear GFP/β-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev Growth Differ 38: 99-106.
63. Dunin-Borkowski OM, Brown NH, (1995) Mammalian CD2 is an effective heterologous marker of the cell surface in Drosophila. Dev Biol 168: 689-693.
64. Martin-Bermudo MD, Dunin-Borkowski OM, Brown NH, (1998) Modulation of integrin activity is vital for morphogenesis. J Cell Biol 141: 1073-1081.
65. Schneider M, Khalil AA, Poulton J, Castillejo-Lopez C, Egger-Adam D, et al. (2006) Perlecan and Dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization. Development 133: 3805-3815.
66. Wolfstetter G, Shirinian M, Stute C, Grabbe C, Hummel T, et al. (2009) Fusion of circular and longitudinal muscles in Drosophila is independent of the endoderm but further visceral muscle differentiation requires a close contact between mesoderm and endoderm. Mech Dev 126: 721-736.
67. Chou TB, Perrimon N, (1992) Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131: 643-653.
68. Sokal RR, Rohlf FJ, (1995) Biometry Freeman and Co 3rd Edition.
69. Campos-Ortega JA, Hartenstein V, (1985) The embryonic development of Drosophila melanogaster Berlin Springer-Verlag.