Morphogens, compartments, and pattern: Lessons from Drosophila?

Cell

Volumn 85, Issue 7, 1996, Pages 951-961

  Lawrence, Peter A ^a   Struhl, Gary ^b  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b Columbia Univ Coll of Phys and S ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN;

CELL INTERACTION; DNA REPLICATION; DROSOPHILA; GENE; GERM LAYER; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0030604688     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81297-0     Document Type: Review

References (100)

1. Alkema, M.J., van der Lugt, N.M.T., Bobeldijk, R.C., Berns, A., and van Lohuizen, M. (1995). Transformation of axial skeleton due to overexpression of bmi-1 in transgenic mice. Nature 374, 724-727.
2. Basler, K., and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
3. Bejsovec, A., and Martinez-Arias, A. (1991). Roles of wingless in patterning the larval epidermis of Drosophila. Development 113, 471-485.
4. Bienz, M., and Müller, J. (1995). Transcriptional silencing of homeotic genes in Drosophila. BioEssays 17, 775-784.
5. Blair, S.S. (1993). Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila. Development 119, 339-351.
6. Blair, S.S. (1995). Compartments and appendage development in Drosophila. BioEssays 17, 299-309.
7. Blair, S.S., Brower, D.L., Thomas, J.B., and Zavortink, M. (1994). The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120, 1805-1815.
8. Bohn, H. (1974). Extent and properties of the regeneration field in the larval legs of cockroaches (Leucophaea maderae). III. Origin of the tissues and determination of symmetry properties in the regenerates. J. Embryol. Exp. Morph. 32, 81-98.
9. Bryant, P.J. (1970). Cell lineage relationships in the imaginal wing disc of Drosophila melanogaster. Dev. Biol. 22, 389-411.
10. Capdevila, J., and Guerrero, I. (1994). Targeted expression of the signalling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13, 4459-4468.
11. Capdevila, J., Estrada, M.P., Sénchez-Herrero, E., and Guerrero, I. (1994). The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J., 13, 71-82.
12. Cohen, S.M. (1993). Imaginai disc development. In The Development of Drosophila melanogaster, M. Bate and A. Martinez-Arias, eds. (Plainview, New York: Cold Spring Harbor Laboratory Press), pp. 747-841.
13. de Celis, J.F., Garcia-Bellido, A., and Bray, S.J. (1996). Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122, 359-369.
14. Diaz-Benjumea, F.J., and Cohen, S.M. (1993). Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741-752.
15. Diaz-Benjumea, F.J., and Cohen, S.M. (1995). Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121, 4215-4225.
16. DiNardo, S., Kuner, J.M., Theis, J., and O'Farrell, P.H. (1985). Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 43, 59-69.
17. Doherty, D., Feger, G., Younger-Shepherd, S., Jan, L.Y., and Jan, Y.N. (1996). Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes Dev. 10, 421-434.
18. Dollé, P., Izpisua-Belmonte, J.C., Brown, J.M., Tickle, C., and Duboule, D. (1991). Hox-4 genes and the morphogenesis of mammalian genitalia. Genes Dev. 5, 1767-1776.
19. Dollé, P., Dierich, A., LeMeur, M., Schimmang, T., Schuhbaur, B., Chambon, P., and Duboule, D. (1993). The disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell 75, 431-441.
20. Driever, W., and Nüsslein-Volhard, C. (1988a). The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95-104.
21. Driever, W., and Nüsslein-Volhard, C. (1988b). A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-94.
22. Driever, W., Thoma, G., and Nüsslein-Volhard, C. (1989). Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340, 363-367.
23. Duncan, I.M. (1982). Polycomblike: a gene that appears to be required for normal expression of the Bithorax and Antennapedia gene complexes of Drosophila melanogaster. Genetics 102, 49-70.
24. Fjose, A., McGinnis, W.J., and Gehring, W.J. (1985). Isolation of a homoeobox-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcripts. Nature 313, 284-289.
25. Garcia-Bellido, A. (1975). Genetic control of wing disc development in Drosophila. CIBA Foundation Symp. 29, 161-183.
26. Garcia-Bellido, A., and de Celis, J.F. (1992). Developmental genetics of the venation pattern of Drosophila. Annu. Rev. Genet. 26, 277-304.
27. Garcia-Bellido, A., Morata, G., and Ripoll, P. (1973). Developmental compartmentalization of the wing disk of Drosophila. Nature New Biol. 245, 251-253.
28. Garcia-Bellido, A., Lawrence, P.A., and Morata, G. (1979). Compartments in animal development. Sci. Am. 241, 102-110.
29. Goodrich, L.V., Johnson, R.L., Milenkovic, L., McMahon, J.A., and Scott, M.P. (1996). Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 10, 301-312.
30. Graham, A., and Lumsden, A. (1996). Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain. Development 122, 473-480.
31. Green, J.B.A., and Smith, J.C. (1990). Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391-394.
32. Green, J.B.A., New, H.V., and Smith, J.C. (1992). Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell 71, 731-739.
33. Guillén, I., Mullor, J.L., Capdevila, J., Sénchez-Herrero, E., Morata, G., and Guerrero, I. (1995). The function of engrailed and the specificiation of Drosophila wing pattern. Development 121, 3447-3456.
34. Gurdon, J.B., Harger, P., Mitchell, A., and Lemaire, P. (1994). Activin signalling and response to a morphogen gradient. Nature 371, 487-492.
35. Gurdon, J.B., Mitchell, A., and Mahony, D. (1995). Direct and continuous assessment by cells of their position in a morphogen gradient. Nature 376, 520-521.
36. Heemskirk, J., and Dinardo, S. (1994). Drosophila hedgehog acts as a morphogen in cellular patterning. Cell 76, 449-460.
37. Hidalgo, A. (1994). Three distinct roles for the engrailed gene in Drosophila wing development. Curr. Biol. 4, 1087-1098.
38. Hoppler, S., and Bienz, M. (1994). Specification of a single cell type by a Drosophila homeotic gene. Cell 76, 689-702.
39. Hülskamp, M., Pfeifle, C., and Tautz, D. (1990). A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature 346, 577-580.
40. Ingham, P.W. (1993). Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. Nature 366, 560-562.
41. Irvine, K.D., and Wieschaus, E. (1994). fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79, 595-606.
42. Jiang, J., and Levine, M. (1993). Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72, 741-752.
43. Kim, J., Irvine, K.D., and Carroll, S.B. (1995). Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82, 795-802.
44. Kornberg, T., Siden, I., O'Farrell, P.H., and Simon, M. (1985). The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40, 45-53.
45. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
46. Lawrence, P.A. (1966). Gradients in the insect segment: the orientation of hairs in the milkweed bug. J. Exp. Biol. 44, 607-620.
47. Lawrence, P.A. (1973). A clonal analysis of segment development in Oncopeltus [Hemiptera]. J. Embryol. Exp. Morph. 30, 681-699.
48. Lawrence, P.A. (1992). The Making of a Fly: The Genetics of Animal Design (Oxford: Blackwell Scientific Publications).
49. Lawrence, P.A., and Struhl, G. (1982). Further studies of the engrailed phenotype in Drosophila. EMBO J. 1, 827-833.
50. Lawrence, P.A., Crick, F.H.C., and Munro, M. (1972). A gradient of positional information in an insect, Rhodnius. J. Cell Sci. 11, 815-853.
51. Lee, J.J., von Kessler, D.P., Parks, S., and Beachy, P.A. (1992). Secretion and localized transcription suggests a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33-50.
52. Lewis, E.B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.
53. Locke, M. (1959). The cuticular pattern in an insect, Rhodnius prolixus, Stl. J. Exp. Biol. 36, 459-477.
54. Lumsden, A. (1990). The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 13, 329-355.
55. Ma, X., Dong, Y., Diepold, K., Scarborough, T., and Ma, J. (1996). The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 122, 1195-1206.
56. Martinez-Arias, A., and Lawrence, P.A. (1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639-642.
57. Meinhardt, H. (1983). Cell determination boundaries as organizing regions for secondary embryonic fields. Dev. Biol. 96, 375-385.
58. Mohler, J. (1988). Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. Genetics 120, 1061-1072.
59. Mohler, J., and Vani, K. (1992). Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development 115, 957-971.
60. Morata, G., and Lawrence, P.A. (1975). Control of compartment development by the engrailed gene in Drosophila. Nature 255, 614-617.
61. Müller, J., Gaunt, S., and Lawrence, P.A. (1995). Function of the Polycomb protein is conserved in mice and flies. Development 121, 2847-2852.
62. Nellen, D., Burke, R., Struhl, G., and Basler, K. (1996). Direct and long-range action of a DPP morphogen gradient. Cell 85, 357-368.
63. Nüsslein-Volhard, C., and Frohnhofer, H.G. (1986). Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324, 120-125.
64. Nüsslein-Volhard, C., and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
65. Padgett, R.W., St Johnston, D., and Gelbart, W.M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature 325, 81-84.
66. Paro, R. (1990). Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 6, 416-421.
67. Porter, J.A., Von Kessler, D., Ekker, S.C., Young, K.E., Lee, J.J., Moses, K., and Beachy, P.A. (1995). The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374, 363-366.
68. Posakony, L.G., Raftery, L.A., and Gelbart, W.M. (1991). Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary. Mech. Dev. 33, 69-82.
69. Riddle, R.D., Johnson, R.L., Laufer, E., and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
70. Roelink, H. (1996). Tripartite signalling of pattern: interactions between Hedgehogs, BMPs, and Wnts in the control of vertebrate development. Curr. Opin. Neurobiol. 6, 33-40.
71. Roelink, H., Porter, J.A., Chiang, C., Tanabe, Y., Chang, D.T., Beachy, P.A., and Jessell, T.M. (1995). Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of Sonic hedgehog autoproteolysis. Cell 81, 445-455.
72. Sampedro, J., Johnston, P., and Lawrence, P.A. (1993). A role for wingless in the segmental gradient of Drosophila? Development 117, 677-687.
73. Sánchez-Herrero, E., Vérnos, I., Marco, R., and Morata, G. (1985). Genetic organization of Drosophila bithorax complex. Nature 313, 108-113.
74. Sanicola, M., Sekelsky, J.S.E., and Gelbart, W.M. (1995). Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed. Genetics 139, 745-756.
75. Simmonds, A.J., Brook, W.J., Cohen, S.M., and Bell, J.B. (1995). Distinguishable functions for engrailed and invected in anterior-posterior patterning in the Drosophila wing. Nature 376, 424-427.
76. Simpson, P., and Morata, G. (1981). Differential mitotic rates and patterns of growth in compartments in the Drosophila wing. Dev. Biol. 85, 299-308.
77. Simpson-Brose, M., Treisman, J., and Desplan, C. (1994). Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78, 855-865.
78. Small, S., Kraut, R., Hoey, T., Warrior, R., and Levine, M. (1991). Transcriptional regulation of a pair-rule stripe in Drosophila. Genes Dev. 5, 827-839.
79. Spencer, F.A., Hoffman, F.M., and Gelbart, W.M. (1982). Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28, 451-461.
80. St Johnston, R.D., and Nüsslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-219.
81. Struhl, G. (1981). A gene product required for correct initiation of segmental determination in Drosophila. Nature 293, 36-41.
82. Struhl, G. (1984). Splitting the bithorax complex of Drosophila. Nature 308, 454-457.
83. Struhl, G., and Basler, K. (1993). Organizing activity of wingless protein in Drosophila. Cell 72, 527-540.
84. + gene product in the determination of segments in Drosophila. Cell 31, 285-292.
85. Struhl, G., Struhl, K., and Macdonald, P.M. (1989). The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259-1273.
86. Struhl, G., Johnston, P., and Lawrence, P.A. (1992). Control of Drosophila body pattern by the hunchback morphogen gradient. Cell 69, 237-249.
87. Stumpf, H.F. (1966). Mechanisms by which cells measure their position within the body. Nature 212, 430-431.
88. Stumpf, H.F. (1968). Further studies on gradient-dependent diversification in the pupal cuticle of Galleria mellonella. J. Exp. Biol. 49, 49-60.
89. Sturtevant, M.A., and Bier, E. (1995). Analysis of the genetic hierarchy guiding wing vein development in Drosophila. Development 121, 785-801.
90. Tabata, T., and Kornberg, T.B. (1994). Hedgehog is a signaling protein with a key role in patterning Drosophila imaginai discs. Cell 76, 89-102.
91. Tabata, T., Eaton, S., and Kornberg, T.B. (1992). The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev. 6, 2635-2645.
92. Tabata, T., Schwartz, C., Gustavson, E., Ali, Z., and Kornberg, T.B. (1995). Creating a Drosophila wing denovo, the role of engrailed, and the compartment border hypothesis. Development 121, 3359-3369.
93. Tickle, C., Summerbell, D., and Wolpert, L. (1975). Positional signalling and specification of digits in chick limb morphogenesis. Nature 254, 199-202.
94. Tiong, S.Y.K., Nash, D., and Bender, W. (1995). Dorsal wing, a locus that affects dorsoventral wing patterning in Drosophila. Development 121, 1649-1656.
95. Turing, A. (1952). The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. 237, 37-72.
96. van den Heuvel, M., Nusse, R., Johnston, P., and Lawrence, P.A. (1989). Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59, 923-931.
97. Vincent, J.P., and O'Farrell, P.H. (1992). The state of engrailed expression is not clonally transmitted during early Drosophila development. Cell 68, 923-931.
98. Williams, J.A., Paddock, S.W., and Carroll, S.B. (1993). Pattern formation in a secondary field: a hierachy of regulatory genes subdivides the developing Drosophila wing disc into discrete sub-regions. Development 117, 571-584.
99. Wolpert, L. (1969). Postional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47.
100. Zecca, M., Basler, K., and Struhl, G. (1995). Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121, 2265-2278.