Design and constraints of the Drosophila segment polarity module: Robust spatial patterning emerges from intertwined cell state switches

Journal of Experimental Zoology

Volumn 294, Issue 3, 2002, Pages 179-215

  Von Dassow, George ^a,b   Odell, Garrett M ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CI PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; ENGRAIL PROTEIN, DROSOPHILA; HOMEODOMAIN PROTEIN; MEMBRANE PROTEIN; ONCOPROTEIN; PTC PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR; WINGLESS PROTEIN, DROSOPHILA;

ANIMAL; ANIMAL EMBRYO; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; DROSOPHILA MELANOGASTER; FEEDBACK SYSTEM; GENE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; COMPUTER SIMULATION; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEEDBACK, BIOCHEMICAL; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; HOMEODOMAIN PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0037108607     PISSN: 0022104X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jez.10144     Document Type: Article

References (116)

1. Akimaru H, Chen Y, Dai P, Hou DX, Nonaka M, Smolik SM, Armstrong S, Goodman RH, Ishii S. 1997. Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 386:735-738.
2. Alcedo J, Noll M. 1997. Hedgehog and its patched-smoothened receptor complex: a novel signalling mechanism at the cell surface. Biol Chem 378:583-590.
3. Alcedo J, Ayzenzon M, Von Ohlen T, Noll M, Hooper JE. 1996. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86:221-232.
4. Alexandre C, Jacinto A, Ingham PW. 1996. Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev 10:2003-2013.
5. Alves G, Limbourg-Bouchon B, Tricoire H, Brissard-Zahraoui J, Lamour-Isnard C, Busson D. 1998. Modulation of Hedgehog target gene expression by the Fused serine-threonine kinase in wing imaginal discs. Mech Dev 78:17-31.
6. Ancel LW, Fontana W. 2000. Plasticity, evolvability, and modularity in RNA. J Exp Zool (Mol Dev Evol) 288:242-283.
7. Anderson DT. 1973. Embryology and phylogeny in annelids and arthropods. New York: Pergamon Press. xiv, 495 pp.
8. Aza-Blanc P, Ramirez-Weber FA, Laget MP, Schwartz C, Kornberg TB. 1997. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89:1043-1053.
9. Bellaiche Y, The I, Perrimon N. 1998. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 394:85-88.
10. Bhanot P, Brink M, Samos CH, Hsieh JC, Wang Y, Macke JP, Andrew D, Nathans J, Nusse R. 1996. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382:225-230.
11. Bhanot P, Fish M, Jemison JA, Nusse R, Nathans J, Cadigan KM. 1999. Frizzled and DFrizzled-2 function as redundant receptors for Wingless during Drosophila embryonic development. Development 126:4175-4186.
12. Bhat KM. 1996. The patched signaling pathway mediates repression of gooseberry allowing neuroblast specification by wingless during Drosophila neurogenesis. Development 122:2921-2932.
13. Bhat KM. 1998. frizzled and frizzled 2 playa partially redundant role in wingless signaling and have similar requirements to wingless in neurogenesis. Cell 95:1027-1036.
14. Bhat KM, van Beers EH, Bhat P. 2000. Sloppy paired acts as the downstream target of wingless in the Drosophila CNS and interaction between sloppy paired and gooseberry inhibits sloppy paired during neurogenesis. Development 127:655-665.
15. Blair SS, Ralston A. 1997. Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development 124:4053-4063.
16. Brown SJ, Hilgenfeld RB, Denell RE. 1994. The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc Natl Acad Sci U S A 91:12922-12926.
17. Brown SJ, Parrish JK, Beeman RW, Denell RE. 1997. Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum. Mech Dev 61:165-173.
18. Brunner E, Peter O, Schweizer L, Basler K. 1997. pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 385:829-833.
19. Burke R, Nellen D, Bellotto M, Hafen E, Senti KA, Dickson BJ, Basler K. 1999. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 99:803-815.
20. Cadigan KM, Nusse R. 1997. Wnt signaling: a common theme in animal development. Genes Dev 11:3286-3305.
21. Cadigan KM, Grossniklaus U, Gehring WJ. 1994a. Functional redundancy: the respective roles of the two sloppy paired genes in Drosophila segmentation. Proc Natl Acad Sci U S A 91:6324-6328.
22. Cadigan KM, Grossniklaus U, Gehring WJ. 1994b. Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev 8:899-913.
23. Cadigan KM, Fish MP, Rulifson EJ, Nusse R. 1998. Wingless repression of Drosophila frizzled 2 expression shapes the Wingless morphogen gradient in the wing. Cell 93:767-777.
24. Carroll SB. 1990. Zebra patterns in fly embryos: activation of stripes or repression of interstripes? Cell 60:9-16.
25. Cavallo RA, Cox RT, Moline MM, Roose J, Polevoy GA, Clevers H, Peifer M, Bejsovec A. 1998. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395:604-608.
26. Chen CM, Struhl G. 1999. Wingless transduction by the Frizzled and Frizzled2 proteins of Drosophila. Development 126:5441-5452.
27. Chen Y, Struhl G. 1996. Dual roles for patched in sequestering and transducing Hedgehog. Cell 87:553-563.
28. Chen Y, Struhl G. 1998. In vivo evidence that Patched and Smoothened constitute distinct binding and transducing components of a Hedgehog receptor complex. Development 125:4943-4948.
29. Chen Y, Gallaher N, Goodman RH, Smolik SM. 1998. Protein kinase A directly regulates the activity and proteolysis of cubitus interruptus. Proc Natl Acad Sci U S A 95:2349-2354.
30. Chen Y, Goodman RH, Smolik SM. 2000. Cubitus interruptus requires Drosophila CREB-binding protein to activate wingless expression in the Drosophila embryo. Mol Cell Biol 20:1616-1625.
31. Dawes R, Dawson I, Falciani F, Tear G, Akam M. 1994. Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120:1561-1572.
32. Dearden PK, Akam M. 2001. Early embryo patterning in the grasshopper, Schistocerca gregaria: wingless, decapentaplegic and caudal expression. Development 128:3435-3444.
33. Dierick HA, Bejsovec A. 1998. Functional analysis of Wingless reveals a link between intercellular ligand transport and dorsal-cell-specific signaling. Development 125:4729-4738.
34. DiNardo S, Heemskerk J, Dougan S, O'Farrell PH. 1994. The making of a maggot: patterning the Drosophila embryonic epidermis. Curr Opin Genet Dev 4:529-534.
35. DiNardo S, Sher E, Heemskerk-Jongens J, Kassis JA, O'Farrell PH. 1988. Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332:604-609.
36. Dominguez M, Brunner M, Hafen E, Basler K. 1996. Sending and receiving the hedgehog signal: control by the Drosophila Gli protein Cubitus interruptus. Science 272:1621-1625.
37. Edgar BA, Odell GM, Schubiger G. 1989. A genetic switch, based on negative regulation, sharpens stripes in Drosophila embryos. Dev Genet 10:124-142.
38. Gallitano-Mendel A, Finkelstein R. 1997. Novel segment polarity gene interactions during embryonic head development in Drosophila. Dev Biol 192:599-613.
39. Gaul U, Jackle H. 1987. Pole region-dependent repression of the Drosophila gap gene Kruppel by maternal gene products. Cell 51:549-555.
40. Gibson G, Wagner G. 2000. Canalization in evolutionary genetics: a stabilizing theory? BioEssays 22:372-380.
41. Gonzalez F, Swales L, Bejsovec A, Skaer H, Martinez Arias A. 1991. Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech Dev 35:43-54.
42. Grbic M, Nagy LM, Strand MR. 1998. Development of polyembryonic insects: a major departure from typical insect embryogenesis. Dev Genes Evol 208:69-81.
43. Grossniklaus U, Pearson RK, Gehring WJ. 1992. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev 6:1030-1051.
44. Hacker U, Lin X, Perrimon N. 1997. The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development 124:3565-3573.
45. Hartwell LH, Hopfield JJ, Leibler S, Murray AW. 1999. From molecular to modular cell biology. Nature 402: C47-52.
46. Heemskerk J, DiNardo S, Kostriken R, O'Farrell PH. 1991. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 352:404-410.
47. Hepker J, Wang QT, Motzny CK, Holmgren R, Orenic TV. 1997. Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development 124:549-558.
48. Hooper JE. 1994. Distinct pathways for autocrine and paracrine Wingless signalling in Drosophila embryos. Nature 372:461-464.
49. Hooper JE, Scott MP. 1989. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59:751-765.
50. Ingham PW, Baker NE, Martinez-Arias A. 1988. Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature 331:73-75.
51. Jiang J, Struhl G. 1998. Regulation of the Hedgehog and Wingless signalling pathways by the F- box/WD40-repeat protein Slimb. Nature 391:493-496.
52. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB. 1999. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532-534.
53. Kobayashi M, Tolkunova EN, Fujioka M, Jaynes JB. 1998. The role of extradenticle and Meis1/Homothorax as a mediator of Engrailed repression activity in embryos. Annu Drosophila Res Conf Abstr, 40th 184C.
54. Kraut R, Levine M. 1991. Mutually repressive interactions between the gap genes giant and Kruppel define middle body regions of the Drosophila embryo. Development 111:611-621.
55. Lawrence PA, Sampedro J. 1993. Drosophila segmentation: after the first three hours. Development 119:971-976.
56. Lawrence PA, Casal J, Struhl G. 1999. hedgehog and engrailed: pattern formation and polarity in the Drosophila abdomen. Development 126:2431-2439.
57. Lee HH, Frasch M. 2000. Wingless effects mesoderm patterning and ectoderm segmentation events via induction of its downstream target sloppy paired. Development 127:5497-5508.
58. Li X, Noll M. 1993. Role of the gooseberry gene in Drosophila embryos: maintenance of wingless expression by a wingless-gooseberry autoregulatory loop. EMBO J 12:4499-4509.
59. Li X, Gutjahr T, Noll M. 1993. Separable regulatory elements mediate the establishment and maintenance of cell states by the Drosophila segment-polarity gene gooseberry. EMBO J 12:1427-1436.
60. Lin X, Perrimon N. 1999. Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signalling. Nature 400:281-284.
61. Manoukian AS, Yoffe KB, Wilder EL, Perrimon N. 1995. The porcupine gene is required for wingless autoregulation in Drosophila. Development 121:4037-4044.
62. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ. 1996. Biochemical evidence that patched is the Hedgehog receptor [see Comments]. Nature 384:176-179.
63. Martinez-Arias A. 1993. Development and patterning of the larval epidermis of Drosophila. In: Bate M, Martinez-Arias A, editors. The development of Drosophila melanogaster. Plainview, NY: Cold Spring Harbor Laboratory Press. p 517-608.
64. Martinez Arias A, Baker NE, Ingham PW. 1988. Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103:157-170.
65. Meir E, von Dassow G, Munro E, Odell GM. 2002a. Robustness, flexibility, and the role of lateral inhibition in the neurogenic network. Curr Biol 12:778-786.
66. Meir E, Munro E, Odell GM, von Dassow G. 2002b. Ingeneue: a versatile tool for reconstituting genetic networks, with examples from the segment polarity network. J Exp Zool (Mol Dev Evol) 294:216-251.
67. Moline MM, Southern C, Bejsovec A. 1999. Directionality of wingless protein transport influences epidermal patterning in the Drosophila embryo. Development 126:4375-4384.
68. Monnier V, Dussillol F, Alves G, Lamour-Isnard C, Plessis A. 1998. Suppressor of fused links fused and Cubitus interruptus on the hedgehog signalling pathway. Curr Biol 8:583-586.
69. Nagy LM. 1998. Changing patterns of gene regulation in the evolution of arthropod morphology. Am Zool 38:818-828.
70. Nagy LM, Carroll S. 1994. Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum. Nature 367:460-463.
71. Ohlmeyer JT, Kalderon D. 1998. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 396:749-753.
72. Oppenheimer DI, MacNicol AM, Patel NH. 1999. Functional conservation of the wingless-engrailed interaction as shown by a widely applicable baculovirus misexpression system. Curr Biol 9:1288-1296.
73. Orenic TV, Slusarski DC, Kroll KL, Holmgren RA. 1990. Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. Genes Dev 4:1053-1067.
74. Patel NH. 1994. The evolution of arthropod segmentation: insights from comparisons of gene expression patterns. Development (Suppl):201-207.
75. Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS. 1989. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58:955-968.
76. Patel NH, Ball EE, Goodman CS. 1992. Changing role of evenskipped during the evolution of insect pattern formation. Nature 357:339-342.
77. Patel NH, Hayward DC, Lall S, Pirkl NR, DiPietro D, Ball EE. 2001. Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128:3459-3472.
78. Peterson MD, Popadic A, Kaufman TC. 1998. The expression of two engrailed-related genes in an apterygote insect and a phylogenetic analysis of insect engrailed-related genes. Dev Genes Evol 208:547-557.
79. Pfeiffer S, Vincent JP. 1999. Signalling at a distance: transport of Wingless in the embryonic epidermis of Drosophila. Semin Cell Dev Biol 10:303-309.
80. Porter JA, Ekker SC, Park WJ, von Kessler DP, Young KE, Chen CH, Ma Y, Woods AS, Cotter RJ, Koonin EV, Beachy PA. 1996a. Hedgehog patterning activity: role of a lipophilic modification mediated by the carboxy-terminal autoprocessing domain. Cell 86:21-34.
81. Porter JA, Young KE, Beachy PA. 1996b. Cholesterol modification of hedgehog signaling proteins in animal development. Science 274:255-259.
82. Robbins DJ, Nybakken KE, Kobayashi R, Sisson JC, Bishop JM, Therond PP. 1997. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 90:225-234.
83. Rogers BT, Kaufman TC. 1996. Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 122:3419-3432.
84. Sanicola M, Sekelsky J, Elson S, Gelbart WM. 1995. Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed. Genetics 139:745-756.
85. Sanson B, Alexandre C, Fascetti N, Vincent JP. 1999. Engrailed and hedgehog make the range of Wingless asymmetric in Drosophila embryos. Cell 98:207-216.
86. Sato A, Kojima T, Ui-Tei K, Miyata Y, Salgo K. 1999. Dfrizzled-3, a new Drosophila Wnt receptor, acting as an attenuator of Wingless signaling in wingless hypomorphic mutants. Development 126:4421-4430.
87. Schmidt JE, von Dassow G, Kimelman D. 1996. Regulation of dorsal-ventral patterning: the ventralizing effects of the novel Xenopus homeobox gene Vox. Development 122:1711-1721.
88. Schwartz C, Locke J, Nishida C, Kornberg TB. 1995. Analysis of cubitus interruptus regulation in Drosophila embryos and imaginal disks. Development 121:1625-1635.
89. Sisson JC, Ho KS, Suyama K, Scott MP. 1997. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90:235-245.
90. Sivasankaran R, Calleja M, Morata G, Basler K. 2000. The wingless target gene dfz3 encodes a new member of the Drosophila frizzled family. Mech Dev 91:427-431.
91. Sommer RJ, Tautz D. 1993. Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Triboliurn (Coleoptera). Nature 361:448-450.
92. Strigini M, Cohen SM. 1997. A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124:4697-4705.
93. Strigini M, Cohen SM. 2000. Wingless gradient formation in the Drosophila wing. Curr Biol 10:293-300.
94. Struhl G, Barbash DA, Lawrence PA. 1997. Hedgehog organises the pattern and polarity of epidermal cells in the Drosophila abdomen. Development 124:2143-2154.
95. Tabata T, Eaton S, Kornberg TB. 1992. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 6:2635-2645.
96. Tanaka K, Kitagawa Y, Kadowaki T. 2002. Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J Biol Chem 277:12816-12823.
97. Tautz D, Friedrich M, Schroder R. 1994. Insect embryogenesis-what is ancestral and what is derived? Development (Suppl):193-199.
98. The I, Perrimon N. 2000. Morphogen diffusion: the case of the Wingless protein. Nat Cell Biol 2:E79-E82.
99. Therond PP, Limbourg Bouchon B, Gallet A, Dussilol F, Pietri T, van den Heuvel M, Tricoire H. 1999. Differential requirements of the Fused kinase for Hedgehog signalling in the Drosophila embryo. Development 126:4039-4051.
100. Tsuda M, Kamimura K, Nakato H, Archer M, Staatz W, Fox B, Humphrey M, Olson S, Futch T, Kaluza V, Siegfried E, Stam L, Selleck SB. 1999. The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature 400:276-280.
101. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789-799.
102. van den Heuvel M, Ingham PW. 1996. smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382:547-551.
103. van den Heuvel M, Nusse R, Johnston P, Lawrence PA. 1989. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59:739-749.
104. Vincent JP, Lawrence PA. 1994. Drosophila wingless sustains engrailed expression only in adjoining cells: evidence from mosaic embryos. Cell 77:909-915.
105. Vincent JP, O'Farrell PH. 1992. The state of engrailed expression is not clonally transmitted during early Drosophila development. Cell 68:923-931.
106. Vinson CR, Conover S, Adler PN. 1989. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338:263-264.
107. von Dassow G, Munro E. 1999. Modularity in animal development and evolution: elements of a conceptual framework for EvoDevo. J Exp Zool (Mol Dev Evol) 285:307-325.
108. von Dassow G, Schmidt JE, Kimelman D. 1993. Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeo box gene. Genes Dev 7:355-366.
109. von Dassow G, Meir E, Munro EM, Odell GM. 2000. The segment polarity network is a robust developmental module. Nature 406:188-192.
110. Von Ohlen T, Hooper JE. 1997. Hedgehog signaling regulates transcription through Gli/Ci binding sites in the wingless enhancer. Mech Dev 68:149-156.
111. Von Ohlen T, Lessing D, Nusse R, Hooper JE. 1997. Hedgehog signaling regulates transcription through cubitus interruptus, a sequence-specific DNA binding protein. Proc Natl Acad Sci U S A 94:2404-2409.
112. Wagner GP, Booth G, Bagheri-Chaichian H. 1997. A population genetic theory of canalization. Evolution 51:329-347.
113. Waltzer L, Bienz M. 1998. Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling. Nature 395:521-525.
114. Wang QT, Holmgren RA. 1999. The subcellular localization and activity of Drosophila cubitus interruptus are regulated at multiple levels. Development 126:5097-5106.
115. Wesley CS. 1999. Notch and wingless regulate expression of cuticle patterning genes. Mol Cell Biol 19:5743-5758.
116. Yoffe KB, Manoukian AS, Wilder EL, Brand AH, Perrimon N. 1995. Evidence for engrailed-independent wingless auto-regulation in Drosophila. Dev Biol 170:636-650.