Platelets with wings: The maturation of Drosophila integrin biology

Current Opinion in Cell Biology

Volumn 15, Issue 5, 2003, Pages 607-613

  Brower, Danny L ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; INTEGRIN; PROTEIN;

BIOLOGY; CELL ADHESION; DROSOPHILA; EXPERIMENT; GENETIC ANALYSIS; GENETIC SCREENING; MUSCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; THROMBOCYTE;

ANIMALIA; INVERTEBRATA; METAZOA;

EID: 0141756142     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(03)00102-9     Document Type: Review

References (59)

1. Brown N.H., Gregory S.L., Martin-Bermudo M.D. Integrins as mediators of morphogenesis in Drosophila. Dev Biol. 223:2000;1-16.
2. Bökel C., Brown N.H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev Cell. 3:2002;311-321.
3. Wright T.R.F. The phenogenetics of the embryonic mutant, lethal myospheroid, in Drosophila melanogaster. J Exp Zool. 143:1960;77-99.
4. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell. 110:2002;673-687.
5. Hynes R.O., Zhao Q. The evolution of cell adhesion. J Cell Biol. 150:2000;F89-F96.
6. Stark K.A., Yee G.H., Roote C.E., Williams E.L., Zusman S., Hynes R.O. A novel α integrin subunit associates with βPS and functions in tissue morphogenesis and movement during Drosophila development. Development. 124:1997;4583-4594.
7. Schöck F., Perrimon N. Retraction of the Drosophila germ band requires cell-matrix interaction. Genes Dev. 17:2003;597-602.
8. Brabant M.C., Fristrom D., Bunch T.A., Brower D.L. Distinct spatial and temporal functions for PS integrins during Drosophila wing morphogenesis. Development. 122:1996;3307-3317.
9. Martin-Bermudo M.D., Dunin-Borkowski O.M., Brown N.H. Specificity of PS integrin function during embryogenesis resides in the α subunit extracellular domain. EMBO J. 16:1997;4184-4193.
10. Martin-Bermudo M.D., Alvarez-Garcia I., Brown N.H. Migration of the Drosophila primordial midgut cells requires coordination of diverse PS integrin functions. Development. 126:1999;5161-5169.
11. Boube M., Martin-Bermudo M.D., Brown N.H., Casanova J. Specific tracheal migration is mediated by complementary expression of cell surface proteins. Genes Dev. 15:2001;1554-1562 This very nice paper demonstrates requirements for particular integrins in the morphogenesis of the tracheal branches of the fly respiratory system. It provides an excellent example of adhesion molecules mediating specific cell migrations, in a system where the signals that regulate expression of the molecules can also be investigated.
12. Grotewiel M.S., Beck C.D., Wu K.H., Zhu X.R., Davis R.L. Integrin-mediated short-term memory in Drosophila. Nature. 391:1998;455-460.
13. Ayyub C., Rodrigues V., Hasan G., Siddiqi O. Genetic analysis of olfC demonstrates a role for the position-specific integrins in the olfactory system of Drosophila melanogaster. Mol Gen Genet. 263:2000;498-504.
14. Beumer K.J., Rohrbough J., Prokop A., Broadie K. A role for PS integrins in morphological growth and synaptic function at the postembryonic neuromuscular junction of Drosophila. Development. 126:1999;5833-5846.
15. Rohrbough J., Grotewiel M.S., Davis R.L., Broadie K. Integrin-mediated regulation of synaptic morphology, transmission, and plasticity. J Neurosci. 20:2000;6868-6878.
16. Suzuki K., Grinnell A.D., Kidokoro Y. Hypertonicity-induced transmitter release at Drosophila neuromuscular junctions is partly mediated by integrins and cAMP/protein kinase A. J Physiol. 538:2002;103-119.
17. Billuart P., Winter C.G., Maresh A., Zhao X., Luo L. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell. 107:2001;195-207.
18. Beumer K., Matthies H.J., Bradshaw A., Broadie K. Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development. 129:2002;3381-3391.
19. Hoang B., Chiba A. Genetic analysis on the role of integrin during axon guidance in Drosophila. J Neurosci. 18:1998;7847-7855.
20. Stevens A., Jacobs J.R. Integrins regulate responsiveness to Slit repellent signals. J Neurosci. 22:2002;4448-4455 The authors examine axon pathfinding across the midline of the fly central nervous system, and uncover sensitive genetic interactions between integrin genes and the gene encoding the extracellular axon repellent Slit. The dosage-sensitive effects extend to integrin ligand genes, and are quite specific; for example, genetic interactions are not seen between integrins and mutations for the axon attractant, netrin. The authors propose that integrin adhesive strength might help set threshold values for other axon guidance cues.
21. Brower D.L., Bunch T.A., Mukai L., Adamson T.E., Wehrli M., Lam S., Friedlander E., Roote C.E., Zusman S. Nonequivalent requirements for PS1 and PS2 integrin at cell attachments in Drosophila: genetic analysis of the αPS1 integrin subunit. Development. 121:1995;1311-1320.
22. Prout M., Damania Z., Soong J., Fristrom D., Fristrom J.W. Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics. 146:1997;275-285 This paper, and that by Walsh and Brown below, describe wing blister mosaic screens to identify genes important for integrin mediated adhesions. These screens have provided important genetic tools for subsequent more detailed studies of specific adhesion components.
23. Walsh E.P., Brown N.H. A screen to identify Drosophila genes required for integrin-mediated adhesion. Genetics. 150:1998;791-805. See Prout et al., above.
24. Baker S.E., Lorenzen J.A., Miller S.W., Bunch T.A., Jannuzi A.L., Ginsberg M.H., Perkins L.A., Brower D.L. Genetic interaction between integrins and moleskin, a gene encoding a Drosophila homolog of importin-7. Genetics. 162:2002;285-296 A screen identifies mutations that reduce the dosage of DIM-7, which imports activated ERK into the nucleus, as suppressors of wing blistering caused by inappropriate integrin function during wing morphogenesis. Although this provides a plausible molecular link between previously seen integrin-mediated adhesion and ERK import, genetic data suggest that the wing blister suppression might depend on other roles for DIM-7.
25. Martin-Bermudo M.D., Brown N.H. Intracellular signals direct integrin localization to sites of function in embryonic muscles. J Cell Biol. 134:1996;217-226.
26. Martin-Bermudo M.D., Dunin-Borkowski O.M., Brown N.H. Modulation of integrin activity is vital for morphogenesis. J Cell Biol. 141:1998;1073-1081.
27. Prokop A., Martin-Bermudo M.D., Bate M., Brown N.H. Absence of PS integrins or laminin A affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embryos. Dev Biol. 196:1998;58-76.
28. -/- flies to viability.
29. Bloor J.W., Kiehart D.P. Zipper nonmuscle myosin-II functions downstream of PS2 integrin in Drosophila myogenesis and is necessary for myofibril formation. Dev Biol. 239:2001;215-228.
30. Brown N.H., Gregory S.L., Rickoll W.L., Fessler L.I., Prout M., White R.A., Fristrom J.W. Talin is essential for integrin function in Drosophila. Dev Cell. 3:2002;569-579 Using mutations derived from the wing blister screens, this paper shows that talin (encoded by the gene rhea) is required for most integrin-mediated adhesions during development. Specifically, the requirements for talin are more general than for other similarly studied linkers, ILK, PINCH and the spectraplakin encoded by short stop.
31. Strumpf D., Volk T. Kakapo, a novel cytoskeletal-associated protein is essential for the restricted localization of the neuregulin-like factor, vein, at the muscle-tendon junction site. J Cell Biol. 143:1998;1259-1270.
32. Gregory S.L., Brown N.H. Kakapo, a gene required for adhesion between and within cell layers in Drosophila, encodes a large cytoskeletal linker protein related to plectin and dystrophin. J Cell Biol. 143:1998;1271-1282.
33. Röper K., Gregory S.L., Brown N.H. The 'Spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J Cell Sci. 115:2002;4215-4225 The authors provide a succinct overview of the complex isoforms of proteins generated by the short stop gene (identified in screens for axon-pathfinding mutants and, as kakapo, in wing blister screens) and its vertebrate homologs. The paper summarizes data from several papers that this spectraplakin family includes diverse proteins that can crosslink different components of the cytoskeleton, as well as the cytoskeleton to plasma membrane proteins, such as integrins.
34. Clark K.A., McGrail M., Beckerle M.C. Analysis of PINCH function in Drosophila demonstrates its requirement in integrin-dependent cellular processes. Development. 130:2003;2611-2621 The results show that PINCH is encoded by the gene steamer duck (stck, also from the wing blister screens), and that stck muscle mutants have phenotypes similar to those of ilk alleles, with detachment of the actin filaments from the still-adherent integrin-extracellular-matrix structure.
35. Martin-Bermudo M.D., Brown N.H. The localized assembly of extracellular matrix integrin ligands requires cell-cell contact. J Cell Sci. 113:2000;3715-3723.
36. Hobert O., Moerman D.G., Clark K.A., Beckerle M.C., Ruvkun G. A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in Caenorhabditis elegans. J Cell Biol. 144:1999;45-57.
37. Rogalski T.M., Mullen G.P., Gilbert M.M., Williams B.D., Moerman D.G. The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol. 150:2000;253-264.
38. ••], except that work was carried out in C. elegans. As with Drosophila, the kinase domain is shown to be largely irrelevant for the linker function of ILK.
39. Van Vactor D.V., Sink H., Fambrough D., Tsoo R., Goodman C.S. Genes that control neuromuscular specificity in Drosophila. Cell. 73:1993;1137-1153.
40. Prokop A., Uhler J., Roote J., Bate M. The kakapo mutation affects terminal arborization and central dendritic sprouting of Drosophila motor neurons. J Cell Biol. 143:1998;1283-1294.
41. Gao F.B., Brenman J.E., Jan L.Y., Jan Y.N. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13:1999;2549-2561.
42. Lee S., Harris K.L., Whitington P.M., Kolodziej P.A. Short stop is allelic to kakapo, and encodes rod-like cytoskeletal-associated proteins required for axon extension. J Neurosci. 20:2000;1096-1108.
43. Lee S., Kolodziej P.A. Short stop provides an essential link between F-actin and microtubules during axon extension. Development. 129:2002;1195-1204.
44. Reuter J.E., Nardine T.M., Penton A., Billuart P., Scott E.K., Usui T., Uemura T., Luo L. A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development. 130:2003;1203-1213.
45. Martin-Bermudo M.D., Brown N.H. Uncoupling integrin adhesion and signaling: the βPS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo. Genes Dev. 13:1999;729-739.
46. Martin-Bermudo M.D. Integrins modulate the EGFR signaling pathway to regulate tendon cell differentiation in the Drosophila embryo. Development. 127:2000;2607-2615 Unlike most studies that examine integrins and muscle adhesion, this paper demonstrates integrin requirements for differentiation of epithelial tendon cells at muscle attachments. Interestingly, integrins appear to regulate MAP kinase activity by affecting the extracellular levels of localized EGFR ligand Vein. This work complements nicely earlier studies by Strumpf and Volk [31], who showed that the linker protein Shot (AKA Kakapo) also affects tendon cell differentiation via Vein localization.
47. Brabant M.C., Fristrom D., Bunch T.A., Baker S.E., Brower D.L. The PS integrins are required for a regulatory event during Drosophila wing morphogenesis. Ann N Y Acad Sci. 857:1998;99-109.
48. •].
49. Xiong J.P., Stehle T., Diefenbach B., Zhang R., Dunker R., Scott D.L., Joachimiak A., Goodman S.L., Arnaout M.A. Crystal structure of the extracellular segment of integrin αVβ3. Science. 294:2001;339-345.
50. Grinblat Y., Zusman S., Yee G., Hynes R.O., Kafatos F.C. Functions of the cytoplasmic domain of the βPS integrin subunit during Drosophila development. Development. 120:1994;91-102.
51. Jannuzi A.L., Bunch T.A., Brabant M.C., Miller S.W., Mukai L., Zavortink M., Brower D.L. Disruption of C-terminal cytoplasmic domain of βPS integrin subunit has dominant negative properties in developing Drosophila. Mol Biol Cell. 13:2002;1352-1365.
52. Retta S.F., Balzac F., Ferraris P., Belkin A.M., Fassler R., Humphries M.J., De Leo G., Silengo L., Tarone G. β1-integrin cytoplasmic subdomains involved in dominant negative function. Mol Biol Cell. 9:1998;715-731.
53. Zavortink M., Bunch T.A., Brower D.L. Functional properties of alternatively spliced forms of the Drosophila PS2 integrin α subunit. Cell Adhes Commun. 1:1993;251-264.
54. Graner M.W., Bunch T.A., Baumgartner S., Kerschen A., Brower D.L. Splice variants of the Drosophila PS2 integrins differentially interact with RGD-containing fragments of the extracellular proteins tiggrin, ten-m, and D-laminin α2. J Biol Chem. 273:1998;18235-18241.
55. Zusman S., Grinblat Y., Yee G., Kafatos F.C., Hynes R.O. Analyses of PS integrin functions during Drosophila development. Development. 118:1993;737-750.
56. Roote C.E., Zusman S. Alternatively spliced forms of the Drosophila αPS2 subunit of integrin are sufficient for viability and can replace the function of the αPS1 subunit of integrin in the retina. Development. 122:1996;1985-1994.
57. Bloor J.W., Brown N.H. Genetic analysis of the Drosophila αPS2 integrin subunit reveals discrete adhesive, morphogenetic and sarcomeric functions. Genetics. 148:1998;1127-1142.
58. Brown N.H., King D.L., Wilcox M., Kafatos F.C. Developmentally regulated alternative splicing of Drosophila integrin PS2 alpha transcripts. Cell. 59:1989;185-195.
59. Yee GH: Identification and characterization of integrin receptor subunits in Drosophila melanogaster [PhD Thesis]. Cambridge, MA, USA: Massachusetts Institute of Technology 1993.