Advertisement

The Molecular Genetic Basis of Positional Information in Insect Segments

Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 18)

Abstract

Pattern formation is the process by which a group of initially unspecified cells organizes itself to generate a precise array of structures. Pattern forming systems as diverse as the vertebrate limb, the insect segment, and the hydra body column, are remarkably resistant to environmental effects and to malicious manipulations perpetrated by researchers. Large variations in the overall size of the organism, the number of cells, and the growth conditions can be tolerated. Injuries result in attempts by the surviving cells to regenerate the pattern. For example, if part of an insect segment is damaged or surgically removed then some or all of the missing structures will be regenerated during subsequent molts. Such regenerative responses to injury are termed “pattern regulation”. Pattern regulation almost certainly reflects the same mechanisms that accommodate variations in cell number and arrangement during normal development. Thus, studies of pattern regulation in response to injury should reveal the processes that form pattern de novo during development.

Keywords

Positional Information Imaginal Disc Homeotic Gene Drosophila Embryo Segment Polarity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abbott LC, Karpen GH, Schubiger G (1981) Compartmental restrictions and blastema formation during pattern regulation in Drosophila imaginal leg discs. Dev Biol 87: 64–75PubMedGoogle Scholar
  2. Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101: 1–22PubMedGoogle Scholar
  3. Anderson K (1987) Dorsal-ventral embryonic pattern genes of Drosophila. Trends Genet 3: 91–97Google Scholar
  4. Artavanis-Tsakonas S (1988) The molecular biology of the Notch locus and the fine tuning of differentiation in Drosophila. Trends Genet 4: 95–100PubMedGoogle Scholar
  5. Baker NE (1987) Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos. EMBO J 6: 1765–1773PubMedGoogle Scholar
  6. Baker NE (1988a) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol 125: 96–108PubMedGoogle Scholar
  7. Baker NE (1988b) Localization of transcripts from the wingless gene in whole Drosophila embryos. Development 103: 289–98PubMedGoogle Scholar
  8. Baker NE (1988c) Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wingless mutation. Development 102: 489–97PubMedGoogle Scholar
  9. Bate M, Martinez Arias A (1991) The embryonic origin of imaginal discs in Drosophila. Development 112: 755–761PubMedGoogle Scholar
  10. Baumgartner S, Bopp D, Burri M, Noll M (1987) Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev 1: 1247–1267PubMedGoogle Scholar
  11. Baumgartner S, Noll M (1991) Network of interactions among pair-rule genes regulating paired expression during primordial segmentation of Drosophila. Mech Dev 33: 1–18Google Scholar
  12. Bejsovec A, Martinez-Arias A (1991) Roles of wingless in patterning the larval epidermis of Drosophila. Development 113: 471–485PubMedGoogle Scholar
  13. Bopp D, Burri M, Baumgartner S, Frigerio G, Noll M (1986) Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell 47: 1033–1040PubMedGoogle Scholar
  14. Bourouis M, Heitzler P, El Messal M, Simpson P (1989) Mutant Drosophila embryos in which all cells adopt a neural fate. Nature (Lond) 341: 442–444Google Scholar
  15. Bourouis M, Moore P, Ruel L, Grau Y, Heitzler P, Simpson P (1990) An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2+ subfamily. EMBO J 9: 2877–2884PubMedGoogle Scholar
  16. Bryant PJ (1975) Pattern formation in the imaginal wing disc of Drosophila melanogaster: fate map, regeneration and duplication. J Exp Zool 193: 49–77PubMedGoogle Scholar
  17. Bryant PJ (1987) Experimental and genetic analysis of growth and cell proliferation in Drosophila imaginal discs. In: Genetic regulation of development. Alan R Liss, New YorkGoogle Scholar
  18. Bryant PJ, Fraser SE (1988) Wound healing, cell communication, and DNA synthesis during imaginal disc regeneration in Drosophila. Dev Biol 127: 197–208PubMedGoogle Scholar
  19. Bryant SV, French V, Bryant PJ (1981) Distal regeneration and symmetry. Science 212: 993–1002PubMedGoogle Scholar
  20. Busson D, Limbourg-Bouchon B, Mariol M-C, Préat T, Lamour-Isnard C (1988) Genetic analysis of viable and lethal fused mutants of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 197: 221–230Google Scholar
  21. Cabrera C, Martinez-Arias A, Bate M (1987) The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila. Cell 50: 425–433PubMedGoogle Scholar
  22. Campbell GL, Caveney S (1989) engrailed gene expression in the abdominal segment of Oncopeltus: gradients and cell states in the insect segment. Dev Biol 106: 727–737Google Scholar
  23. Campbell GL, Shelton PMJ (1987) Cell behavior during postembryonic pattern regulation in the insect abdomen (Oncopeltus fasciatus) I. Regeneration of the segment borders. Development 101: 221–235Google Scholar
  24. Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New YorkGoogle Scholar
  25. Carroll SB (1990) Zebra patterns in fly embryos: activation of stripes or repression of interstripes? Cell 60: 9–16PubMedGoogle Scholar
  26. Carroll SB, Scott MP (1986) Zygotically-active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis. Cell 45: 113–126PubMedGoogle Scholar
  27. Carroll SB, Vavra SH (1989) The zygotic control of Drosophila pair-rule gene expression. II. Spatial repression by gap and pair-rule gene products. Dev 107: 673–683Google Scholar
  28. Chasan R, Anderson KV (1989) The role of easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo. Cell 56: 391400Google Scholar
  29. Cohen B, Wimmer EA, Cohen SM (1991) Early development of the leg and wing primordia in the Drosophila embryo. Mech Dev 33: 229–240PubMedGoogle Scholar
  30. Cohen SM, Bronner G, Kuttner F, Jürgens G, Jäckle H (1989) Distal-less encodes a homeodomain protein required for limb development in Drosophila. Nature (Lond) 338: 432–434Google Scholar
  31. Cohen SM (1990) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature (Lond) 343: 173–177Google Scholar
  32. Côté S, Preiss A, Haller J, Schuh R, Kienlin A, Seifert A, Jäckle H (1987) The gooseberry-zipper region of Drosophila: five genes encode spatially restricted transcripts in the embryo. EMBO J 6: 2793–2801PubMedGoogle Scholar
  33. The Molecular Genetic Basis of Positional Information in Insect Segments 41Google Scholar
  34. Crick FH, Lawrence PA (1975) Compartments and polyclones in insect development. Science 189: 340–347PubMedGoogle Scholar
  35. Dale L, Bownes M (1980) Is regeneration in Drosophila the result of epimorphic regulation? Wilhelm Roux’s Arch Dev Biol 189: 91–96Google Scholar
  36. DeLotto R, Spierer P (1986) A gene required for the specification of dorsal-ventral pattern of Drosophila appears to encode a serine protease. Nature (Lond) 323: 688–692Google Scholar
  37. Denell RE, Hummels KR, Wakimoto B, Kaufman TC (1981) A developmental genetic analysis of the lethal syndrome associated with the Antennapedia locus of Drosophila melanogaster. Dev Biol 81: 43–50PubMedGoogle Scholar
  38. Desplan C, Theis J, O’Farrell PH (1985) The Drosophila developmental gene, engrailed, encodes sequence specific DNA binding activity. Nature (Lond) 318: 630–635Google Scholar
  39. DiNardo S, O’Farrell PH (1987) Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes. Genes Dev 1: 1212–1225PubMedGoogle Scholar
  40. DiNardo S, Kuner JM, Theis J, O’Farrell PH (1985) Development of embryonic pattern in Drosophila melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 43: 59–69PubMedGoogle Scholar
  41. DiNardo S, Sher E, Heemskerk-Jorgens J, Kassis J, O’Farrell P (1988) Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature (Lond) 332: 604–609Google Scholar
  42. Doe CQ, Goodman CS (1985) Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev Biol 111: 206–219Google Scholar
  43. Driever W, Nusslein-Volhard C (1989) The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature (Lond) 337: 138–143Google Scholar
  44. Eaton S, Kornberg TB (1990) Repression of ci-D in posterior compartments of Drosophila by engrailed. Genes Dev 4: 1068–1077PubMedGoogle Scholar
  45. Eldon ED, Pirotta V (1991) Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development 111: 367–378PubMedGoogle Scholar
  46. Fausto-Sterling A (1971) On the timing and place of action during embryogenesis of the female-sterile mutants fused and rudimentary Drosophila melanogaster. Dev Biol 26: 452–463PubMedGoogle Scholar
  47. Fausto-Sterling A (1978) Pattern formation in the wing veins of the fused mutant (Drosophila melanogaster). Dev Biol 63: 358–369PubMedGoogle Scholar
  48. Fjose A, McGinnis WJ, Gehring WJ (1985) Isolation of a homeobox-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcript. Nature (Lond) 313: 284–289Google Scholar
  49. Foe VE (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107: 1–22PubMedGoogle Scholar
  50. Foe VE, Alberts BM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. Cell Sci J 61: 31–70Google Scholar
  51. French V, Bryant PJ, Bryant SV (1976) Pattern regulation in epimorphic fields. Science 193: 969–981PubMedGoogle Scholar
  52. Frasch M, Levine M (1987) Complementary patterns of even-skipped and fushi tarazu expression involve their differential regulation by a common set of segmentation genes in Drosophila. Genes Dev 1: 981–995PubMedGoogle Scholar
  53. Frigerio G, Burri M, Bopp D, Baumgartner M, Noll M (1986) Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell 47: 735–746PubMedGoogle Scholar
  54. Frischer LE, Hagen FS, Garber RL (1986) An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs. Cell 47: 1017–1023PubMedGoogle Scholar
  55. Garcia-Bellido A (1975) Genetic control of wing disc development in Drosophila. Ciba Found Symp 29: 161–182PubMedGoogle Scholar
  56. Garcia-Bellido A (1977) Homeotic and atavic mutations in insects. Am Zool 17: 613–629Google Scholar
  57. Garcia-Bellido A, Lawrence PA, Morata G (1979) Compartments in animal development. Sci Am 241: 102–110Google Scholar
  58. Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartmentalization of the wing disk of Drosophila. Nature (Lond) New Biol 245: 251253Google Scholar
  59. Gergen JP, Wieschaus EF (1986) Localized requirements for gene activity in segmentation of Drosophila embryos: analysis of armadillo, fused, giant and unpaired mutations in mosaic embryos. Wilhelm Roux’s Arch Dev Biol 195: 49–62Google Scholar
  60. Gergen JP, Coulter D, Wieschaus E (1986) Segmental pattern and blastoderm cell identities. In: Subtelny S (ed) Gametogenesis and the early embryo. Liss Symp Soc Dev Biol, New York, pp 195–220Google Scholar
  61. Gierer A, Meinhardt H (1972) A theory of biological pattern formation. Kybernetik 12: 30–39PubMedGoogle Scholar
  62. Gonzalez F, Swales L, Bejsovec A, Skaer H, Martinez-Arias A (1991) Secretion and movenment of wingless protein in the epidermis of the Drosophila embryo. Mech Dev 35: 43–54PubMedGoogle Scholar
  63. Grau Y, Simpson P (1987) The segment polarity gene costal-2 in Drosophila. I. The organization of both primary and secondary embryonic fields may be affected. Dev Biol 122: 186–200Google Scholar
  64. Harding K, Levine M (1988) Gap genes define the limits of Antennapedia and bithorax gene expression during early development in Drosophila EMBO J 7: 205–214Google Scholar
  65. Harding K, Hoey T, Warrior R, Levine M (1989) Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila. EMBO J 8: 1205–1212PubMedGoogle Scholar
  66. Harding K, Rushlow C, Doyle HJ, Hoey T, Levine L (1986) Cross-regulatory interactions among pair-rule genes in Drosophila. Science 233: 953–959PubMedGoogle Scholar
  67. Hashimoto C, Hudson KL, Anderson KV (1988) The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52: 269–279PubMedGoogle Scholar
  68. Hazelrigg T, Kaufman TC (1983) Revertants of dominant mutations associated with the Antennapedia gene complex of Drosophila melanogaster. Genetics 105: 581— 600Google Scholar
  69. Heemskerk J, DiNardo S, Kostriken R, O’Farrell PH (1991) Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature (Lond) 352: 404–410Google Scholar
  70. Hidalgo A (1991) Interactions between segment polarity genes and the generation of the segmental pattern in Drosophila. Mech Dev 35: 77–87PubMedGoogle Scholar
  71. Hidalgo A, Ingham P (1990) Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development 110: 291–301PubMedGoogle Scholar
  72. Hiromi Y, Gehring WJ (1987) Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50: 963–974PubMedGoogle Scholar
  73. Hooper JE, Scott MP (1989) The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59: 751–765PubMedGoogle Scholar
  74. Hooper KL, Parkhurst SM, Ish-Horowicz D (1989) Spatial control of hairy protein expression during embryogenesis. Development 107: 489–504PubMedGoogle Scholar
  75. Hoch M, Seifert E, Jäckle H (1991) Gene expression mediated by cis-acting sequences of the Krüppel gene in response to the Drosophila morphogens bicoid and hunchback. EMBO J 10: 2267–2278PubMedGoogle Scholar
  76. Howard K, Ingham P (1986) Regulatory interactions between the segmentation genes fushi tarazu, hairy, and engrailed in the Drosophila blastoderm. Cell 44: 949–957PubMedGoogle Scholar
  77. Howard K, Ingham P, Rushlow C (1988) Region-specific alleles of the Drosophila segmentation gene hairy. Genes Dev 2: 1037–1046PubMedGoogle Scholar
  78. Hülskamp M, Pfeifle C, 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 (Lond) 346: 646–648Google Scholar
  79. Immerglück K, Lawrence PA, Bienz M (1990) Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62: 261–268PubMedGoogle Scholar
  80. Ingham PW (1988) The molecular genetics of embryonic pattern formation in Drosophila. Nature (Lond) 335: 25–34Google Scholar
  81. Ingham P, Martinez-Arias A, Lawrence PA, Howard K (1985) Expression of engrailed in the parasegment of Drosophila. Nature (Lond) 317: 634–636Google Scholar
  82. Ingham PW, Martinez-Arias A (1986) The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature (Lond) 324: 592–597Google Scholar
  83. Ingham PW, Baker NE, Martinez-Arias A (1988) Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature (Lond) 331: 73–75Google Scholar
  84. Ingham PW, Taylor AM, Nakano Y (1991) Role of the Drosophila patched gene in positional signalling. Nature (Lond) 353: 184–187Google Scholar
  85. Irish VF, Martinez-Arias A, Akam M (1989) Spatial regulation of the Antennapedia and Ultrabithorax genes during Drosophila early development. EMBO J 8: 1527–1537PubMedGoogle Scholar
  86. Jaynes JB, O’Farrell PH (1988) Activation and repression of transcription by homeodomain-containing proteins that bind a common site. Nature (Lond) 336: 744–749Google Scholar
  87. Jiang J, Hoey T, Levine M (1991) Autoregulation of a segmentation gene in Drosophila: Combinatorial interactions of the even-skipped homeo box protein with a distal enhancer element. Genes Dev 5: 265–277PubMedGoogle Scholar
  88. St Johnston DR, Gelbart WM (1987) Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 6: 2785–2791Google Scholar
  89. Joyner AL, Herrup BA, Auerbach CA, Rossant DJ (1991) Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Science 251: 1239–1243PubMedGoogle Scholar
  90. Joyner AL, Kornberg T, Coleman KG, Cox RD, Martin GR (1985) Expression during embryogenesis of a mouse gene with sequence homology to the Drosophila engrailed gene. Cell 43: 29–37PubMedGoogle Scholar
  91. Jürgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Wilhelm Roux’s Arch Dev Biol 196: 141–157Google Scholar
  92. Kaufman TC, Lewis R, Wakimoto B (1980) Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homeotic gene complex in polytene chromosomal interval 84A, B. Genetics 94: 115–133PubMedGoogle Scholar
  93. Klingensmith J, Noll E, Perrimon N (1989) The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death. Dev Biol 134: 130–145PubMedGoogle Scholar
  94. Kornberg T (1981) engrailed: a gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci USA 78:1095–1099Google Scholar
  95. Kornberg T, Siden I, O’Farrell P, Simon M (1985) The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40: 45–53PubMedGoogle Scholar
  96. Krasnow MA, Saffman EE, Kornfeld K, Hogness DS (1989) Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell 57: 1031–1043PubMedGoogle Scholar
  97. Kraut R, Levine M (1991) Spatial regulation of the gap gene giant during Drosophila development. Development 111: 601–609PubMedGoogle Scholar
  98. Kuner JM, Nakanishi M, Ali Z, Drees B, Gustayson E, Theis J, Kauvar L, Kornberg T, O’Farrell PH (1985) Molecular cloning of engrailed: a gene involved in the development of pattern in Drosophila melanogaster. Cell 42: 309–316PubMedGoogle Scholar
  99. Laughon A, Scott MP (1984) Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature (Lond) 310: 25–31Google Scholar
  100. Lawrence PA (1966) Gradients in the insect segment: the orientation of hairs in the milkweed bug Oncopeltus fasciatus. J Exp Biol 44: 607–620Google Scholar
  101. Lawrence PA (1981) The cellular basis of segmentation in insects. Cell 26: 3–10PubMedGoogle Scholar
  102. Lawrence PA (1982) Cell lineage of the thoracic muscles of Drosophila. Cell 29: 493–503PubMedGoogle Scholar
  103. Lawrence PA (1989) Cell lineage and cell states in the Drosophila embryo. In: Evered D, Marsh J (eds) Cellular basis of morphogenesis, 144. John Wiley, New York, pp 131–149Google Scholar
  104. Lawrence PA, Johnston P (1984) On the role of the engrailed + gene in the internal organs of Drosophila. EMBO J 3: 2839–2844PubMedGoogle Scholar
  105. Lawrence PA, Morata G (1976) Compartments in the wing of Drosophila: a study of the engrailed gene. Dev Biol 50: 321–337PubMedGoogle Scholar
  106. Lawrence PA, Morata G (1983) The elements of the bithorax complex. Cell 35: 595–601PubMedGoogle Scholar
  107. Lawrence PA, Johnston P, Macdonald P, Struhl G (1987) Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes. Nature (Lond) 328: 440–442Google Scholar
  108. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature (Lond) 276: 565–570Google Scholar
  109. Limbourg-Bouchon B, Busson D, Lamour-Isnard C (1991) Interactions between fused, a segment polarity gene in Drosophila, and other segmentation genes. Development 112: 417–429PubMedGoogle Scholar
  110. Lindsley DL, Grell HE (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst WashingtonGoogle Scholar
  111. Locke M (1959) The cuticular pattern in an insect, Rhodnius prolixus, stai. J Exp Biol 36: 459–477Google Scholar
  112. Locke, M (1966) The cuticular pattern in an insect: the behavior of grafts in segmented appendages. J Insect Physiol 12: 397–402Google Scholar
  113. Locke M, Huie P (1981) Epidermal feet in insect morphogenesis. Nature (Lond) 293: 733–735Google Scholar
  114. Lohs-Schardin M, Sander K, Cremer C, Cremer T, Zorn C (1979) Localized ultraviolet laser microbeam irradiation of early Drosophila embryos: fate maps based on location and frequency of adult defects. Dev Biol 68: 533–545PubMedGoogle Scholar
  115. Macdonald PM, Ingham P, Struhl G (1986) Isolation, structure and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeobox. Cell 47: 721–734PubMedGoogle Scholar
  116. Mahaffey JW, Kaufman TC (1988) The homeotic genes of the Antennapedia complex and the bithorax complex of Drosophila. In: Malacinski GM (ed) Developmental genetics of higher organisms: a primer in developmental biology. Macmillan, New York, pp 329–360Google Scholar
  117. Marcus W (1962) Untersuchiungen über die Polarität der Rumpfhaut von Schmetterlingen. Wilhelm Roux’s Arch Entwicklungsmech Org 154: 56–102Google Scholar
  118. Mariol M-C, Préat T, Limbourg-Bouchon B (1987) Molecular cloning of fused, a gene required for normal segmentation in the Drosophila melanogaster embryo. Mol Cell Biol 7: 3244–3251PubMedGoogle Scholar
  119. Martinez-Arias A (1985) The development of fused-embryos of Drosophila melanogaster. J Embryol Exp Morphol 87: 99–114PubMedGoogle Scholar
  120. Martinez-Arias A (1989) A cellular basis for pattern formation in the insect epidermis. TIG 5: 262–267PubMedGoogle Scholar
  121. Martinez-Arias A, Ingham PW (1985) The origin of pattern duplications in segment polarity mutants of Drosophila melanogaster. J Embryol Exp Morphol 87: 129–135PubMedGoogle Scholar
  122. Martinez-Arias A, Lawrence PA (1985) Parasegments and compartments in the Drosophila embryo. Nature (Lond) 313: 639–642Google Scholar
  123. Martinez-Arias A, White RAH (1988) Ultrabithorax and engrailed expression in Drosophila embryos mutant for segmentation genes of the pair-rule class. Development 102: 325–338Google Scholar
  124. 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: 157–170Google Scholar
  125. Meinhardt H (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev Biol 96: 375–385PubMedGoogle Scholar
  126. Meinhardt H (1986) Hierarchical inductions of cell states: a model for segmentation in Drosophila. J Cell Sci (Suppl) 4: 357–381Google Scholar
  127. Meinhardt H, Gierer A (1980) Generation and regeneration of sequences of structures during morphogenesis. J Theor Biol 85: 429–450PubMedGoogle Scholar
  128. Mittenthal JE (1981) The rule of normal neighbors: a hypothesis for morphogenetic pattern regulation. Dev Biol 88: 15–26PubMedGoogle Scholar
  129. Mohler J (1988) Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. Genetics 120: 1061–1072PubMedGoogle Scholar
  130. Mohler J, Eldon ED, Pirotta V (1989) A novel spatial transcription pattern associated with the segmentation gene giant of Drosophila. EMBO J 8: 1539–1548PubMedGoogle Scholar
  131. Mohler J, Vani K (1992) Molecular organization and embryonic expression of the hedgehog gene in cell-cell communication in segmental patterning of Drosophila. Development, in the pressGoogle Scholar
  132. Morata G, Lawrence PA (1975) Control of compartment development by the engrailed gene in Drosophila. Nature (Lond) 255: 614–617Google Scholar
  133. Morata G, Lawrence PA (1977a) The development of wingless, a homeotic mutation of Drosophila. Dev Biol 56: 227–240PubMedGoogle Scholar
  134. Morata G, Lawrence PA (1977b) Homoeotic genes, compartments and cell determination in Drosophila. Nature (Lond) 265: 211–216Google Scholar
  135. Moscoso del Prado J, Garcia-Bellido A (1984) Genetic regulation of the Achaetescute complex of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 193: 242–245Google Scholar
  136. Nakano Y, Guerrero I, Hidalgo A, Taylor A, Whittle JRS, Ingham PW (1989) The Drosophila segment polarity gene patched encodes a protein with multiple potential membrane spanning domains. Nature (Lond) 341: 508–513Google Scholar
  137. Nardi JB, Kafatos FC (1976) Polarity and gradients in lepidopteran wing epidermis. J Embryol Exp Morphol 36: 469–487PubMedGoogle Scholar
  138. Nardi JB, Magee-Adams SM (1986) Formation of scale spacing patterns in a moth wing. I. Epithelial feet may mediate cell rearrangement. Dev Biol 116: 278–290Google Scholar
  139. Nauber U, Pankratz MJ, Kienlin A, Seifert E, Klemm U, Jackle H (1988) Abdominal segmentation of the Drosophila embryo requires a hormone receptor-like protein encoded by the gap gene knirps. Nature (Lond) 336: 489–492Google Scholar
  140. Nübler-Jung K (1974) Cell migration during pattern reconstitution by intercalary regeneration and cell sorting in Dysdercus intermedius (Dist.). Nature (Lond) 248: 610–611Google Scholar
  141. Nübler-Jung K (1977) Pattern stability in the insect segment. I. Pattern reconstitution by intercalary regeneration and cell sorting in Dysdercus interemedius Dist. Wilhelm Roux’s Arch Dev Biol 183: 17–40Google Scholar
  142. Nüsslein-Volhard C, Roth S (1989) Axis determination in insect embryos. In: Evered D, Marsh J (eds) Cellular basis of morphogenesis, 144. John Wiley, New York, pp 37–64Google Scholar
  143. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature (Lond) 287: 795–801Google Scholar
  144. Nüsslein-Volhard C, Lohs-Schardin M, Cremer C (1980) A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature (Lond) 238: 474–476Google Scholar
  145. Nüsslein-Volhard C, Wieschaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Wilhelm Roux’s Arch Dev Biol 193: 267–282Google Scholar
  146. Orenic T, Chidsey J, Holmgren R (1987) Cell and cubitus interruptus Dominant; two segment polarity genes on the fourth chromosome in Drosophila. Dev Biol 124: 50–56Google Scholar
  147. Orenic TV, Slusarski C, Kroll KL, Holmgren RA (1990) Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. Genes Dev 4: 1053–1067PubMedGoogle Scholar
  148. Pankratz MJ, Seifert E, Gerwin N, Billi B, Nauber U, Jäckle H (1990) Gradients of Krüppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the Drosophila embryo. Cell 61: 309–317PubMedGoogle Scholar
  149. Patel NH, Kornberg T, Goodman CS (1989a) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107: 201–212PubMedGoogle Scholar
  150. Patel NH, Schafer B, Goodman CS, Holmgren R (1989b) The role of segment polarity genes during Drosophila neurogenesis. Genes Dev 3: 890–904PubMedGoogle Scholar
  151. Peifer M, Wieschaus E (1990) The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homologue of human plakoglobin. Cell 63: 1167–1178PubMedGoogle Scholar
  152. Peifer M, Rauskolb C, Williams M, Riggleman B, Wieschaus E (1991) The segment polarity gene armadillo interacts with the wingless signalling pathway in both embryonic and adult pattern formation. Development 111: 1029–1043PubMedGoogle Scholar
  153. Perrimon N, Mahowald AP (1987) Multiple functions of segment polarity genes in Drosophila. Dev Biol 119: 587–600PubMedGoogle Scholar
  154. Perrimon N, Smouse D (1989) Multiple functions of a Drosophila homeotic gene, zeste-white 3, during segmentation and neurogenesis. Dev Biol 135: 287–305PubMedGoogle Scholar
  155. Perrimon N, Engstrom L, Mahowald AP (1989) Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121: 333–352Google Scholar
  156. Phillips RG, Roberts IJH, Ingham PW, Whittle JRS (1990) The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs. Development 110: 105–114PubMedGoogle Scholar
  157. Piepho H (1955) Uber die Ausrichtung der Schuppenbälge and Schuppen am Schmetterlingsrumpf. 42: 22Google Scholar
  158. Piepho, H. and C. Hintze-Podufal (1971) Zur Polarität des Insektensegments. I. Induktion des Segmenthinterrandes bei Galleria mellonella L. Biol Zentralbl 90: 419–431Google Scholar
  159. Pignoni F, Baldarelli RM, Steingrimsson E, Diaz RJ, Patapoutian A, Merriam JR, Lengyel JL (1990) The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 62: 151–163PubMedGoogle Scholar
  160. Poole SJ, Kauvar LM, Drees B, Kornberg T (1985) The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell 40: 37–43PubMedGoogle Scholar
  161. Postlethwait JH, Schneiderman HA (1969) A clonal analysis of determination in Antennapedia, a homeotic mutant of Drosophila melanogaster. Proc Natl Acad Sci USA 64: 176–183PubMedGoogle Scholar
  162. Préat T, Thérond P, Lamour-Isnard C, Limbourg-Bouchon B, Tricoire H, Erk I, Mariol M-C, Busson D (1990) A putative serine/threonine protein kinase encoded by the segment polarity fused gene of Drosophila. Nature (Lond) 347: 87–89Google Scholar
  163. Price JV, Clifford RJ, Schüpbach T (1989) The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homologue. Cell 56: 1085–1092PubMedGoogle Scholar
  164. Reinitz J, Levine M (1990) Control of the initiation of homeotic gene expression by the gap genes giant and tailless in Drosophila. Dev Biol 140: 57–72PubMedGoogle Scholar
  165. Reuter R, Panganiban GEF, Hoffman FM, Scott MP (1990) Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110: 1031–1040PubMedGoogle Scholar
  166. Riggleman B, Schedi P, Wieschaus E (1990) Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by Wingless. Cell 63: 549–560PubMedGoogle Scholar
  167. Riggleman B, Wieschaus E, Schedl P (1989) Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 3: 96–113PubMedGoogle Scholar
  168. Rijsewijk F, Schuermann M, Wagenaar E, Parren P, Weigel D, Nusse R (1987) The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene Wingless. Cell 50: 649–657PubMedGoogle Scholar
  169. Riley PD, Carroll SB, Scott MP (1987) The expression and regulation of Sex combs reduced protein in Drosophila embryos. Genes Dev 1: 716–730PubMedGoogle Scholar
  170. Rosenberg UB, Schroder C, Preiss A, Kienlin A, Côte S, Riede I, Jäckle H (1986) Structural homology of the product of the Drosophila Krüppel gene with Xenopus transcription factor IIIA. Nature (Lond) 319: 336–339Google Scholar
  171. Rushlow CA, Hogan A, Pinchin SM, Howe KM, Lardelli M, Ish-Horowitz D (1989) The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J 8: 3095–3103PubMedGoogle Scholar
  172. Russell MA (1974) Pattern formation in the imaginal discs of a temperature-sensitive cell-lethal mutant of Drosophila melanogaster. Dev Biol 40: 24–39PubMedGoogle Scholar
  173. Sampedro J, Guerrero I (1991) Unrestricted expression of the Drosophila gene patched allows normal segment polarity. Nature (Lond) 353: 187–190Google Scholar
  174. Samson M-L, Jackson-Grusby L, Brent R (1989) Gene activation and DNA binding by Drosophila Ultrabithorax and abdominal A proteins. Cell 57: 1045–1052PubMedGoogle Scholar
  175. Schneuwly S, Kuroiwa A, Gehring WJ (1987) Molecular analysis of the dominant homeotic Antennapedia phenotype. EMBO J 6: 201–206PubMedGoogle Scholar
  176. Scott MP, Carroll SB (1987) The segmentation and homeotic gene network in early Drosophila development. Cell 51: 689–698PubMedGoogle Scholar
  177. Scott MP, O’Farrell PH (1986) Spatial programming of gene expression in early Drosophila embryogenesis. Annu Rev Cell Biol 2: 49–80PubMedGoogle Scholar
  178. Sharma RP (1973) wingless, a new mutant in Drosophila melanogaster. Drosophila Inf Sery 50:134Google Scholar
  179. Siegfried E, Perkins LA, Capaci TM, Perrimon N (1990) Putative protein kinase product of the Drosophila segment-polarity gene zeste-white3. Nature (Lond) 345: 825–829Google Scholar
  180. Simcox AA, Sang JH (1983) When does determination occur in Drosophila embryos? Dev Biol 97: 212–221PubMedGoogle Scholar
  181. Simcox AA, Roberts IJH, Hersperger E, Gribbin MC, Shearn A, Whittle JRS (1989) Imaginal discs can be recovered from cultured embryos mutant for the segment polarity genes engrailed, naked and patched but not from wingless. Development 107: 715–722Google Scholar
  182. Simpson P (1990) Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system. Development 109: 509–519PubMedGoogle Scholar
  183. Simpson P, Crau Y (1987) The segment polarity gene costal-2 in Drosophila II. The origin of imaginal pattern duplications. Dev Biol 122: 201–209Google Scholar
  184. Simpson P, El Messal M, Moscoso Del Prado J, Ripoll P (1988) Stripes of positional homologies across the wing blade of Drosophila melanogaster. Dev Biol 103: 391–401Google Scholar
  185. Small S, Kraut R, Hoey T, Warrior R, Levine M (1991) Transcriptional regulation of a pair-rule stripe in Drosophila. Genes Dev 5: 827–839PubMedGoogle Scholar
  186. Sokol S, Christian JL, Moon RT, Melton DA (1991) Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67: 741–752PubMedGoogle Scholar
  187. Spencer FA, Hoffman M, Gelbart WM (1982) Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28: 451–461PubMedGoogle Scholar
  188. Stanojevic D, Hoey T, Levine M (1989) Sequence-specific DNA-binding activities of the gap proteins hunchback, and Krüppel in Drosophila. Nature (Lond) 341: 331–335Google Scholar
  189. Stanojevic D, Small D, Levine M (1991) Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science 254: 1385–1387PubMedGoogle Scholar
  190. Steward R (1987) Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 238: 692–694PubMedGoogle Scholar
  191. Struhl G (1981) A homeotic mutation transforming leg to antenna in Drosophila. Nature (Lond) 292: 635–638Google Scholar
  192. Struhl G, Struhl K, Macdonald PM (1989) The gradient morphogen bicoid is a concentration dependent transcriptional activator. Cell 57: 1259–1273PubMedGoogle Scholar
  193. Stunipf H (1968) Further studies on gradient-dependent diversification in the pupal cuticle of Galleria mellonella. J Exp Biol 49: 49–59Google Scholar
  194. Tautz D, Lehmann R, Schnurch H, Schuh R, Seifert E, Kienlin K, Jäckle H (1987) Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes. Nature (Lond) 327: 383–389Google Scholar
  195. Thali M, Müller M, DeLorenzi M, Matthias P, Bienz M (1988) Drosophila homeotic genes encode transcriptional activators similar to mammalian OTF-2. Nature (Lond) 336: 598–601Google Scholar
  196. Thomas KR, Capecchi MR (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature (Lond) 346: 847–850Google Scholar
  197. Tiong SYK, Nash D (1990) Genetic analysis of the adenosine3 (Gart) region of the second chromosome of Drosophila melanogaster. Genetics 124: 889–897PubMedGoogle Scholar
  198. Treisman J, Desplan C (1989) The products of the Drosophila gap genes hunchback and Krüppel bind to the hunchback promoter. Nature (Lond) 341: 335–337Google Scholar
  199. 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: 739–749PubMedGoogle Scholar
  200. Vincent J-P, O’Farrell PH (1992) The state of engrailed expression is not clonally transmitted during early Drosophila development. Cell 68: 923–931PubMedGoogle Scholar
  201. Warrior R, Levine M (1990) Dose-dependent regulation of pair-rule stripes by gap proteins and the initiation of segment polarity. Development 110: 759–767PubMedGoogle Scholar
  202. Weiss PA (1939) Principles in development. Henry Holt White RA, Lehmann R (1986) A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell 47: 311–321Google Scholar
  203. Whittle JRS (1976) Clonal analysis of a genetically caused duplication of the anterior wing in Drosophila melanogaster. Dev Biol 51: 257–268PubMedGoogle Scholar
  204. Wieschaus E, Noell E (1986) Specificity of embryonic lethal mutations in Drosophila analyzed in germ line clones. Wilhelm Roux’s Arch Dev Biol 195: 63–73Google Scholar
  205. Wieschaus E, Gehring W (1976) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol 50: 249–263PubMedGoogle Scholar
  206. Wieschaus E, Riggleman R (1987) Autonomous requirements for the segment polarity gene armadillo during Drosophila embryogenesis. Cell 49: 177–184PubMedGoogle Scholar
  207. Wieschaus E, Nüsslein-Volhard C, Jürgens G (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the X chromosome and the fourth chromosome. Wilhelm Roux’s Arch Dev Biol 193: 267–282Google Scholar
  208. Wigglesworth VB (1940) Local and general factors in the development of “pattern” in Rhodnius prolixus (Hemiptera). J Exp Biol 36: 180–200Google Scholar
  209. Winslow GM, Hayashi S, Krasnow M, Hogness DS, Scott MP (1989) Transcriptional activation by the Antennapedia and fushi tarazu proteins in cultured Drosophila cells. Cell 57: 1017–1030PubMedGoogle Scholar
  210. Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25: 1–47PubMedGoogle Scholar
  211. Wright D, Lawrence PA (1981) Regeneration of the segment boundary in Oncopeltus. Dev Biol 85: 317–327PubMedGoogle Scholar
  212. Zuo P, Stanojevic D, Colgan J, Han K, Levine M, Manley JL (1991) Activation and repression of transcription by the gap proteins hunchback and Krüppel in cultured Drosophila cells. Genes Dev 5: 254–264PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1992

Authors and Affiliations

  1. 1.Department of Cellular and Structural BiologyUniversity of Colorado Health Sciences CenterDenverUSA
  2. 2.Departments of Developmental Biology and GeneticsStanford University School of MedicineStanfordUSA

Personalised recommendations