Developmental Biology of Drosophila; Fall 1994

Sylabus

About this course:

I developed this as a graduate reading course, in part for myself to learn about recent issues of animal development. I was working at the time on early olfactory development of both zebrafish and moth, and was particularly interested in genes common to both represented phyla. Text for the course was Peter Lawrence's Making of a Fly. The course focused on fly development up to cellularization, and then focused on genes common to insect and vertebrate. The course met one evening per week with two and sometimes three presentations per night, as indicated. Where appropriate, the first half of each evening focused on fly and the second half vertebrate. About 12 students participated.

While this specific material is clearly dated now, the outline of development is, of course, not. These papers may therefore prove useful as spring boards, as they define the state of knowledge of 1994.

The overall course outline immediately follows. The full reading list is linked from these entries.

Sylabus - click on dated entries for complete reading lists

30 August; Chapters 1 and 2
Organization of course. Participant commitments.(13 weeks, 24 presentations)
Lecture by Vogt: Overview of Insect/Drosophila Development, oogenesis and Initial Coordinate Systems

6 September. Chapter 3(a). Organization in the pre-gastrula I: patterning of the Gap Genes by Maternal Effect Genes
0. Mutant Screens of Nusslein-Volhard and Wieschaus
I. Bicoid. the anterior gradient.
II. Regulation of Hunchback by Bicoid and Nanos; Hunchback gradient is the result of the Anterior-Posterior gradient processes.

13 September. Chapter 3(b). Organization in the pre-gastrula I: patterning of the Pair Rule Genes by the Gap Genes.
Regulation of: Gap Genes by Hunchback, Tailless and Gap genes; Pair Rule Genes by Gap Genes; Second Stripe of Eve
I.a. Distribution of the Gap Genes (Figure 3.4).
I.b. Discussion of Figure 3.5; Regulation of Gap genes by hunchback
II. Regulation of eve second stripe: transcriptional regulation of a pair-rule gene (Figures 3.10 - 3.12).

20 September. Chapter 4(a). Compartments.
what compartments are; specification of parasegments (reg. of en by eve and ftz); introduction of the segment polarity genes (wingless, hedgehog, etc., etc.).
I. Compartments. Clonal Experiments that Define compartments (Figure 4.3).
II. Compartmental expression of the pair rule geneseve and ftz and of the selector gene engrailed (Figures 4.5 & 4.7).

27 September. Chapter 5(a). Selector Genes: the homeodomain, structure and function.
I. The biothorax complex (BX-C) in the spatial regulation: anterior-posterior specification in four layers: ectoderm, somatic and visceral endoderm, and gut.
II. Homologous homeobox patterns in vertebrate and fly.

4 October. Action and evolution of homeobox genes.
I. Action of homeobox genes of vertebrate CNS development.
II. Evolution of homeobox genes.

11 October. No Class; Dick is in France.

18 October. Chapter 4(b): The Segment Polarity Genes: Hedgehog and Sonic Hedgehog

I. Drosophila Hedgehog
II. Vertebrate Sonic Hedgehog

25 October. Cellular Morphogens: Drosophila Wingless and Vertebrate Wnt
I. Cell-cell communication in Drosophila: Wingless (Ubx and dpp: visceral mesoderm
induction of gut) II. Vertebrate wnt (winglesshomologue): early patterning in Xenopus laevis.

1 November. Specification of Pattern: Development of the Larval Nervous System
I. The initial pattern: specification of neuroblasts.
II. Initial development of neural circuits: axonal pathfinding and target recognition.
III. Patterned gene expression within the CNS

8 November, Hierarchical specification of patterned cell identity, the larval PNS.
I. Larval PNS I
II. Larval PNS II, some recent developments.

15 November. Postembryonic Development: Adult Metamorphosis and Imaginal Disc Development.
I. Imaginal Disc Development I
II. Imaginal Disc Development II

22 November. Hormones and hormone action: temporal regulation of development.
0. Hormonal Regulation of Insect Development: Juvenile Hormone and Ecdysone.
I. Mechanisms of steroid action: ecdysone and the ecdysone receptor family.
II. Mechanisms underlying diverse EcR action: heterodimers and spliced variants.

29 November. Development of the adult nervous system.
I. Adult CNS: Neurogenesis; Respecification; Cell Death.
II. Expression of alternative EcR forms correspond with specific cell fates in CNS.

6 December. Zebrafish: Drosophila reiterated. Synthesis.

Syllabus (Long): Developmental Biology of Drosophila; Fall 1994, with Reading List

Organization of course.
• Participant committments.(13 weeks, 24 presentations)
  
Lecture by Vogt:
• Overview of Insect/Drospohila Development
  
• Oogenesis
  
• The Maternal Effect Genes: the molecular sources of the gradients that contribute to the initial coordinate system (bicoid, hunchback, nanos, torso, Toll & dorsal).
  

Review Articles:
Developmental genetics of oogenesis. (1993) Spradling AC. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.1-70. Cold Spring Harbor Laboratory Press.

Mitotis and morphogenesis in the Drosophila embryo: point and counterpoint. (1993) Foe VE, GM Odell, BA Edgar. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.149-300. Cold Spring Harbor Laboratory Press.

Maternal control of anterior development in the Drosophila embryo. (1993) Driever W. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.301-324.. Cold Spring Harbor Laboratory Press.

The terminal system of axis determination in the Drosophila embryo. (1993) Sprenger F, C Nusslein-Volhard. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.365-386. Cold Spring Harbor Laboratory Press.

Maternal control of dorsal-ventral polarity and pattern in the embryo. (1993) Chasan R, KV Anderson. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.387-424. Cold Spring Harbor Laboratory Press.

Some recent papers:
Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. (1994) Wang S, T Hazelrigg. Nature 369, 400-403.

Regulation of cell number in Drosophila (1994) Busturia A, PA Lawrence Nature 370, 561-563. Great images of bicoid, ev, en.

Translational regulation of i>nanos by RNA localization. (1994) Gavis ER, R Lehmann. Nature 369, 315-318.

Terminal pattern elements in Drosophilaembryo induced by the torso-like protein. (1994) Martin J-R, A Raibaud, R Ollo. Nature 367, 741-745.

0. Mutant Screens of Nusslein-Volhard and Wieschaus

Mutations affecting the patern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. (1984) Nusslein-Volhard C, E Wieschaus, H Kluding Wilhelm Roux's Arch. Dev. Biol. 193, 267-282.

Mutations affecting the patern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. (1984) Jurgens G, E Wieschaus, C Nusslein-Volhard, H Kluding Wilhelm Roux's Arch. Dev. Biol. 193, 283-295.

Mutations affecting the patern of the larval cuticle in Drosophila melanogaster. III. Zygotic loci on the X chromosome and the fourth chromosome. (1984) Wieschaus E, C Nusslein-Volhard, H Kluding Wilhelm Roux's Arch. Dev. Biol. 193, 296-307.

Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. (1986) Schupbach T, E Wieschaus Roux's Arch. Dev. Biol. 195, 302-317.

I. Bicoid. the anterior gradient.

Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. (1986) HG Frohnhofer, C Nusslein-Volhard. Nature 324, 120-125.

A gradient of bicoid protein in Drosophila embryos. (1988) W Driever, C Nusslein-Volhard. Cell 54, 83-93.

The bicoid protein determines position in theDrosophila embryo in a concentration-dependent manner. (1988) W Driever, C Nusslein-Volhard. Cell 54, 95-104.

II. Regulation of Hunchback by Bicoid and Nanos; Hunchback gradient is the result of the Anterior-Posterior gradient processes.

The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. (1989) W Driever, C Nusslein-Volhard. Nature 337, 138-143.

The gradient morphogen bicoid is a concentration-dependent transcriptional activator. (1989) G Struhl, K Struhl, PM Macdonald. Cell 57, 1259-1273.

The Drosophila posterior-group gene nanos functions by repressing hunchback activity. (1989) V Irish, R Lehmann, M Akam. Nature 338, 646-648.

Differing stratagies for organizing anterior and posterior body patterns in Drosophila embryos. (1989) G Struhl Nature 338, 741-744.

The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. (1991) R Lehmann, C Nusslein-Volhard Development 112, 679-693.

• Regulation of Gap Genes by Hunchbackand Tailless
  
• Self regulation of Gap genes
  
• Regulation of Pair Rule Genes by Gap Genes: Regulation of the Second Stripe of Eve

  Relationship between Drosophila gap gene tailless and a vertebrate nuclear receptor Tlx. (1994) Yu RT, M McKeown, RM Evans, K Umesono. Nature370, 375-379.

  Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. (1994) Patel NH, BG Condron, K Zinn. Nature 367, 429-434.

  I.a. Distrubution of the Gap Genes (Figure 3.4).

  Analysis of maternal effect mutant combinations elucidates regulation and function of the overlap of hunchback and Kruppel gene expression in the Drosophila blastoderm embryo. (1989) U Gaul, H Jackle Development 107, 651-662.

  Kruppel requirement for knirps enhandement reflects overlapping gap gene activities in the Drosophila embryo. (1989) MJ Pankratz, M Hock, E Seifert, H Jackle. Nature 341, 337-340.

  A morphogenetic gradient of hunchback protein organises the expression of the gap genes Kruppel and knirps in the early Drosophila embryo. (1990) M Hulskamp, C Pfeifle, D Tautz Nature 346, 577-580.

  The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. (1990) F Pignoni, RM Baldarelli, E Steingrimsson, RJ Diaz, A Patapoutlan, JR Merriam, JA Lengyel. Cell 62, 151-163.

  Two gap genes mediate maternal terminal pattern information in Drosophila. (1990) D Weigel, G Jurgens, M Klingler, H Jackle. Science 248, 495-498.

  Mutually repressive interactions between th gap genes giant and Kruppel define middle body regions of the Drosophila embryo. (1991) R Kraut, M Levine. Development 111, 611-621.

  I.b. Discussion of Figure 3.5; Regulation of Gap genes by hunchback
  The hunchback gradient specifies body pattern in the Drosophila embryo. (1992) G. Struhl, P Johnston, PA Lawrence Cell 69, 237-249.

  II. Regulation of eve second stripe: trascriptional regulation of a pair-rule gene (Figures 3.10 - 3.12).
  Gradients of Kruppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the Drosophila embryo. (1990> MJ Pankratz, E Seifert, N Gerwin, B Billi, U Nauber, H Jackle. Cell 61, 309-317.

  Decoding positional information: regulation of the pair-rule gene hairy. (1990) KR Howard, G Struhl. Development 110, 1223-1231.

  Transcriptional regulation of a pair-rule stripe in Drosophila. (1991) S Small, R Kraut, T Hoey, R Warrior, M Levine Genes Dev. 5, 827-839.

• what compartments are
  
• specification of parasegments (reg. of en by eve and ftz)
  
• introduction of the segment polarity genes (wingless, hedgehog, etc., etc.).

  I. Compartments. Clonal Experiments that Define compartments (Figure 4.3).

  Control of compartment development by the engrailed gene in Drosophila. (1975) Morata G, PA Lawrence Nature 255, 614-617.

  Compartments in the wing of Drosophila: A study of the engrailed gene. (1976) Lawrence PA, G Morata Dev. Biol. 50, 321-327.

  Further studies of the engrailed phenotype in Drosophila. (1982) Lawrence PA, G Struhl EMBO J 1, 827-833.

  II. Compartmental expression of the pair rule genes eve and ftz and of the selector gene engrailed (Figures 4.5 & 4.7).
  Localization of the fushi tarazu protein during Drosophila embyrogenesis. (1985) Carroll SB, MP Scott Cell 43, 47-57.

  Regulatory interactions between the segmentation genes fushi tarazu, hairy and engrailed in the Drosophila blastoderm. (1986) Howard K, P Ingham Cell 44, 949-957.

  Complementary patterns of even-skipped and fushi tarazu expression involve their differential regulation of a common set of segmentation genes in Drosophila. (1987) Frasch M, M Levine Genes Dev. 1, 981-995.

  Pattern formation in theDrosophila embryo: allocation of cells to parasegments by even-skipped and fushi tarazu. (1989) Lawrence PA, P Johnston Development 105, 761-768.

  Expression of engrailed proteins in arthropods, annelids and chordates. (1989). Patel NH, E Martin-Blanco, KG Coleman, SJ Poole, MC Ellis, TB Kornberg, CS Goodman Cell 58, 955-968.

  Regulation of cell number in Drosophila (1994) Busturia A, PA Lawrence Nature 370, 561-563. (Great images of bicoid, ev, en. )

I. The biothorax complex (BX-C) in the spatial regulation: anterior-posterior specification in four layers: ectoderm, somatic and visceral endoderm, and gut.
discussion of book chapter

II. Homologous homeobox patterns in vertebrate and fly.
Mice and flies head to head. (1992) Holland P, P Ingham, S Krauss Nature 358, 627-628.

Molecular mechanisms of segmental patterning in the vertebrate hindbrain and neural crest. (1993) Wilkinson DG BioEssays 15(August), 499.

Hox and HOM: homologous gene clusters in insects and vertebrates. (1989) Akam M Cell 57, 347-349.

Deformed autoregulatory element from Drosophila functions in a conserved manner in transgenic mice. (1992) Awgulewitsch A, D Jacobs. Nature 358, 341-344.

A human HOX4B regulatory element provides head-specific expression in Drosophila embryos. (1992) Malicki J, Cianetti LC, Peschle C, McGinnis W. Nature 358, 345-347.

Nested expression domains of four homeobox genes in developing rostral brain. (1992) Simeone A, D Acampora, M gulisano, A Stornaiuolo, E Boncinelli Nature 358, 687-690.

A homeo domain protein reveals the metameric nature of the developing chick hindbrain. Sundin O, G Eichele (1990) Genes Dev. 4, 1267-1276.

Miscellaneous other references.
Patterning the vertebrate head: murine Hox-2 genes mark distinct subpopulations of premigratory and migrating neural crest. (1991) Krumlauf R, P Hunt, A Graham, D Wilkinson Development 112, 43-51.

Mouse Hox-1.11: a proposcopedia subfamily member eshibiting an anterior boundary of expression in rhombdomere 2. (1993) Kim H-J, DA Lucas, M Zhang, MT Gendron-Maguire, A Baron, T Gridley, J Grippo. Development (was in press August 1993).

Retinoic acid causes an anteroposterior transformation in the developing central nervous system. (1989) Durston A, J Timmermans, W Hage, H Hendriks, N de Vries, M Heideveld, P Nieuwkoop. Nature 340, 140-144.

Sequential activation of HOX2 homeobox genes by retinoic acid in human embryoonal carcinoma cells. (1990) Simeone A, D Acampora, L Arcioni, PW Andrews, E Boncinelli, F MavilloNature 346, 763-766.

Retinoic acid receptors and cellular retinoid binding proteins II. Their differential pattern of transcription during early morphogenesis in mouse embryos. (1991) Ruberte E, P Dolle, P Chambon, G Morriss-Kay Development 116, 357-368.

Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genesin vivo. (1992) Conlon R, J Rossant Development 116, 357-368.

Developmental expression of a novel murine Homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. (1994) Liu ISC, J-d Chen, L Ploder, D Vidgen, D van der Kooy, VI Kalnins, RR McInnes. Neuron 13, 377-393.

I. Action of homeobox genes of vertebrate CNS development.
Retinoic acid alters the hindbrain Hox code and induces the transformation of rhombomeres 2/3 into a rhombomere 4/5 identity. (1992) Marshall H, S Nonchev, M-H Sham, I Muchamore, A Lumsden, R Krumlauf Nature 360, 737-741.

Reversal of axonal pathways from rhombomere 3 correlates with extra Hox expression domains. (1993) Kessel M. Neuron 10, 379-393. (mouse, retinoic acid anteriorizes hox exp., ; link twixt axonal pathfinding and intrinsic neuronal specificaiton by Hox codes.) interesting paper, would complement Goodman and the patterned exp of fly and mouse homeobox genes in CNS.

Cell adhesion molecules as targets for Hox genes: neural cell adhesion molecule promoter activity is modulated by co-transfection with Hox-2.5 and -2.4. (1992) Jones FS, EA Prediger, DA Bittner, EM De Robertis, GM EdelmanProc. Nat. Acad. Sci. USA89, 2086-2090.

Connectin a target of homeotic gene control in Drosophila. (1992) Gould AP, RAH White Development 116, 1163-1174.

II. Evolution of homeobox genes.
Structure and function of the homeotic gene complex (HOM-C) in the beetle, Tribolium castaneum. (1993) Beeman RW, JJ Stuart, SJ Brown, RE Denell BioEssays 15(July), 439.

Insect Development, Is pairing the rule? (1994) Akam M. (News & Views) Nature 367, 410-411. (eve & en rather than homeobox, but it fits with the paper above)

Return to the amphioxus. (1994) Gee H. (News & Views) Nature 370, 504-505.

Archetypal organization of the amphioxus Hox gene cluster. (1994) Garcia-Fernandez J, PWH Holland Nature 370, 563-566.

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18 October. Chapter 4(b): The Segment Polarity Genes: Hedgehog and Sonic Hedgehog

I. Drosophila Hedgehog
Developmental biology, unanimity waits in the wings. (1994) O'Farrell PH. (News & Views) Nature 368, 188-189.

Segment polarity genes and cell patterning within the Drosophila body segment. (1991) Ingham PW. Curr. Opin. Genet. Dev. 1 261-267.

Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. (1993) Ingham PW Nature 366, 208-214.

Drosophila hedgehog acts as a morphogen in cellular patterning (1994) Heemskerk J, S Dinardo Cell 76, 449-460.

Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. (1994) Basler K, G Struhl Nature 368, 208-214.

II. Vertebrate Sonic Hedgehog
More to patterning than sonic hedgehog. (1994) ME Pownall BioEssays 16(June), 381-383.

Sonic hedgehog, a member of a family of putative signalling moledules, is implicated in the regulation of CNS polarity. (1993) Y Echelard, DJ Epstein, B St-Jacques, L Shen, J Mohler, JA McMahon, AP McMahon. Cell 75, 1417-1430.

Sonic hedgehog mediates the polarizing activity of the ZPA (1993) RD Diddle, RL Johnson, E Laufer, C Tabin Cell 75, 1401-1416.

A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. (1993) S Krauss, J-P Concoredt, PW Ingham. Cell 75, 1431-1444.

Floor plate and motor neuron induction by vhh-1, a vertegrate homolog of hedgehog expressed by the notochord. (1994) H Roelink, A Augsburger, J Heemskerk, V Korzh, S Norlin, A Ruis i Altaba, Y Tanabe, M Placzek, T Edlund, TM Jessell, J Dodd. Cell 76, 761-775.

Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. (1994) Li X, M Noll. Nature 367, 83-87. (paired, gooseberry, gooseberry neuro: prd activates gsb, wg, en. gsb maintains exp. of wg. gsb activates gsbn).

I. Cell-cell communication in Drosophila: Wingless (Ubx and dpp: visceral mesoderm induction of gut)

Drosophila development: Exploring signalling pathways. (1994) Brown NH, DA Hartley (News & Views) Nature 370, 414-415. (Review of 1994 Crete meeting.)

Drosophila Wingless: a paradigm for the function and mechanisms of Wnt signaling (1994) E Siefgried, N Perrimon BioEssays 16, 395-404.

Components of wingless signalling in Drosophila. (1994) Siegfried, EL Wilder, N Perrimon. Nature 367, 76-80 .

dishevelled and armadillo act in the Wingless signalling pathway in Drosophila. (1994) Noordermeer, J Klingensmith, N Perrimon, R Nusse. Nature 367, 80-83.

II. Vertebrate wnt (wingless homolog): early patterning in Xenopus laevis.
Axis determination in Xenopus: gradients and signals. (1994) Dawid IB, M Taira BioEssays 16(June), 385-386.

Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction. (1992) Kimelman D, JL Christian, RT Moon Development 116, 1-9.

The homeobox gene goosecoid controls cell migration in Xenopus embryos. (1993) Niehrs C, R Keller, SWY Cho, EM De Robertis. Cell 72, 491-503.

Mesodermal patterning by a gradient of the vertebrate homeobox gene goosecoid. (1993) Niehrs C, H Steinbeisser, EM De Robertis. Science 263, 817-820.

In pursuit of the functions of the Wnt family of developmental regulators: insights from Xenopus laevis. (1993) RT Moon BioEssays 15, 91-97.

When cells take fate into their own hands: differential competence to respond to inducing signals generates diversity in the embryonic mesoderm. (1993) JL Christian, RT Moon BioEssays 15, 135-140.

Intercellular signaling and gene regulation during early development of Xenopus laevis. (1994) Dawid IB J. Biol. Chem. 269, 6259-6262.

• Development of the larval CNS and PNS
  
• Hierarchical specification of sensory type
  
• Postembryonic neurogenesis

  I. The initial pattern: specification of neuroblasts.

  Early neurogenesis in Drosophila melanogaster. (1993) Campos-Ortega JA. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.1091-1129. Cold Spring Harbor Laboratory Press.

  Embryonic development of identified neurons: differentiation from neuroblast to neuron. (1979) Goodman CS, NC Spitzer. Nature 280, 208-214.

  Embryonic development of the Drosophila central nervous system. (1993) CS Goodman, CQ Doe. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.1131-1206. Cold Spring Harbor Laboratory Press.

  II. Initial development of neural circuits: axonal pathfinding and target recognition.
  Embryonic development of identified neurons: differentiation from neuroblast to neuron. (1979) Goodman CS, NC Spitzer. Nature 280, 208-214.

  Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. (1993) Seeger M, G Tear, D Ferres-Marco, CS Goodman. Neuron10, 409-426.

  Neuromuscular development in Drosophila: insights from single neurons and single genes. (1993) Keshishian H & A Chiba. Trends in Neuroscience 16(7), 278-283.

  Neurobiology, just a chemical attraction. (1994) Smith SJ. (News & Views) Nature 368, 101-102.

  Turning of nerve growth cones induced by neurotransmitters. (1994) Zheng JQ, M Felder, JA Connor, M-m Poo. Nature 368, 140-144.

I. Larval PNS I
The specification of sensory neuron identity in Drosophila. (1993) Ghysen A, C Dambly-Chaudiere. BioEssays 15(May), 293-298.

The peripheral nervous system. (1993) Jan YH, LY Jan. in The Development of Drosophila melanogaster ed. M Bate & AM Arias. pp.1207-1243. Cold Spring Harbor Laboratory Press.

The role of the cut gene in the specification of central projections by sensory axons in Drosophila. (1993) Merritt DJ, A Hawken, PM Whitington. Neuron 10, 741-752.

The gene poxn controls different steps of the formation of chemosensory organs in Drosophila. (1994) Nottebohm E, A Usui, S Therianos, K-i Kimura, C Dambly-Chaudiere, A Ghysen. Neuron 12, 25-34.

II. Larval PNS II, some recent developments.
Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. (1994) Salzberg A, D D'Evelyn, KL Schulze, J-K Lee, D Strumpf, L Tsai, HJ Bellen. Neuron 13, 269-287.

atonal is the proneural gene for Drosophila photoreceptors. (1994) Jarman AP, EH Grell, L Ackerman, LY Han, YN Jan. Nature 369, 398-400.

The Drosophila sine oculi locus encodes a homeodomain-containing protein required for the development of the entire visual system. (1994) Cheyette BNR, PJ Green, K Martin, H Garren, V Hartenstein, SL Zipursky. Neuron 12, 977-996.

III. Hierarchical specification of patterned gene expression in the CNS
Cell type - specific transcriptional regulation of the Drosophila FMRFamide neuropeptide gene. (1993) Schneider LE, MS Roberts, PH Taghert. Neuron 10, 279-291.

I. Imaginal Disc Development; reexpression of embryonic genes.
Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. (1994) Williams JA, SW Paddock, K Vorwerk, SB Carroll. Nature 368, 299-305.

The origin, patterning and evolution of insect appendages. (1993) Williams JA, SB Carroll BioEssays 15(September), 567.

In search of the machinery for spatial patterning of animal epithelia. (1993) Whittle R, R Phillips BioEssays 15(November), 757. (Dros. leg; paper review.)

Imaginal disc development (1993) Cohen SM. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.747-841. Cold Spring Harbor Laboratory Press.

II. Imaginal Disc Development; regulation of postembryonic development.
Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. (1994) Williams JA, SW Paddock, K Vorwerk, SB Carroll. Nature 368, 299-305.

The origin, patterning and evolution of insect appendages. (1993) Williams JA, SB Carroll BioEssays 15(September), 567.

In search of the machinery for spatial patterning of animal epithelia. (1993) Whittle R, R Phillips BioEssays 15(November), 757. (Dros. leg; paper review.)

Imaginal disc development (1993) Cohen SM. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.747-841. Cold Spring Harbor Laboratory Press.

0. Hormonal Regulation of Insect Development: Juvenile Hormone and Ecdysone.
Hormone receptors and the regulation of insect metamorphosis. (1993) Riddiford, LM, JW Truman. American Zoologist 33, 340-347.

Hormones and Drosophila development. (1993) Riddiford LM. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.899-939. Cold Spring Harbor Laboratory Press.

I. Mechanisms of steroid action: ecdysone and the ecdysone receptor family.
Puffs and gene regulation - molecular insights into the Drosophila ecdysone regulatory hierarchy. (1990) Thummel CS. BioEssays 12, 561-568.

On the temporal control of puffing activity in polytene chromosomes. (1974) Ashburner M, C Chihara, P Meltzer, G Richards. Cold Spring Harbor Symp. Quant. Biol. 38, 655-662.

Something old, some things new: the steroid receptor superfamily in Drosophila, minireview. (1991) Seagraves WA. Cell 67, 225-228. (orphan receptors)

The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. (1991) Koelle MR, WS Talbot, WA Seagraves, MT Bender, P Cherbas, DS Hogness. Cell 67, 59-77.

II. Mechanisms underlying diverse EcR action: heterodimers and spliced varients.
Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. (1992) Yao TP, WA Seagraves, AE Oro, M McKeown, RM Evans. Cell 71, 63-72.

Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiricle. (1993) Thomas HE, HG Stunnenberg, AF Stewart. Nature 362, 471-475.

Functional ecdysone receptor is the product of EcR andUltraspiracle genes. (1993) Yao T-P, BM Forman, Z Jiang, L Cherbas, J-D Chen, M McKeown, P Cherbas, RM Evans. Nature 366, 476-479.

Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. (1993) Talbot WS, EA Swyryd, DS Hogness. Cell 73, 1323-1337.

Hormones, solving the specificity puzzle. (1994) Williams GR (News & Views) Nature 370, 330-331. (retinoic acid / heterodimer receptors)

Vitamin D3-thyroid hormone receptor heterodimer polarity directs ligand sensitivity of transactivation. (1994) Schrader M, KM Muller, S Nayeri, J-P Kahlen, C Carlberg. Nature 370, 382-386. (Heterodimer of VDR and T3R binds to different response elements in a polarity (i.e. orientation) dependent manner!)

I. Adult CNS: Neurogenesis; Respecification; Cell Death.
Metamorphosis of the central nervous system of Drosophila. (1990) JW Truman. J. Neurobiology 21, 1072-1084.

Formation of the adult nervous system. (1993) JW Truman, BJ Taylor, TA Awad. in The Development of Drosophila melanogaster. ed. M Bate & AM Arias. pp.1245-1275. Cold Spring Harbor Laboratory Press.

Hormonal control of rates of metamorphic development in the moth Manduca sexta. (1983) Schwartz LM, JW Truman. Developmental Biology 99, 103-114.

Steroid regulation of neuronal death in the moth nervous system. (1984) Truman JW, LM Schwartz J. Neuroscience 4, 274-280.

Developmental neuroethology of insect metamorphosis. (1992) Truman JW J. Neurobiology 23, 1404-1422.

II. Expression of alternative EcR forms correspond with specific cell fates in CNS.
Programmed cell death in the Drosophila CNS is edcsone-regulated and coupled with a specific ecdysone receptor isoform. (1993) S Robinow, WS Talbot, DS Hogness, JW Truman. Development 119, 1251-1259.

Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. (1994) JW Truman, WS Talbot, SE Fahrbach, DS Hogness Development 120, 219-234.

Papers:
Developmental Biology, catch of the decade. (1994) Concordet J-P, P Ingham (News & Views) Nature 369, 19-20.

Also see: Science (1994, May 13, p. 904)

Embryonic mutant screens of Nusslein-Volhard & Driever.

Zebrafish retinal tectal mutants Science (May 13, p. 904)

Chemoaffinity in the orderly growth of nerve fiber patterns and connections. (1963) Sperry RW. Proc. Nat. Acad. Sci. USA 50, 703-710.

Developmental mechanisms that generate precise patterns of neuronal connectivity. (1993) Goodman CS, CJ Schatz Cell 72(Supplement), 77-98. (Also Neuron 10, Supplement, 77-98).

The molecular basis of retinotectal topography. (1994) Kaprielian Z, PHPatterson. BioEssays 16(January), 1-11.