Roux's archives of developmental biology

, Volume 202, Issue 2, pp 112–122 | Cite as

Tracing neurons with a kinesin-β-galactosidase fusion protein

  • Edward Giniger
  • William Wells
  • Lily Yeh Jan
  • Yuh Nung Jan
Original Articles

Summary

We have analyzed the development of neuronal projections inDrosophila by fusing the gene encodingDrosophila kinesin, a microtubule-associated motor protein, toEscherichia coli lacZ, and employing the resulting chimeric protein as a reporter molecule for labelling cells by the “enhancer-trap” method. Expression of kinesin-β-galactosidase in neurons has afforded a detailed view of the morphologies and projections of neurons. The images of cells provided by this method will facilitate anatomical and genetic investigations of theDrosophila nervous system as well as other cell types.

Key words

Axon guidance Drosophila Enhancer trap Kinesin-lacZ Neural development 

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References

  1. Ashburner M (1989) Drosophila: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NYGoogle Scholar
  2. Bastiani MJ, Harrelson AL, Snow PM, Goodman CS (1987) Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grosshopper. Cell 48:745–755Google Scholar
  3. Bellen HJ, O'Kane CJ, Wilson C, Grossniklaus U, Gehring WJ (1989) P-Element-mediated enhancer detection: a versatile method to study development inDrosophila. Genes Dev 3:1288–1300Google Scholar
  4. Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E, Jan LY, Jan YN (1989) Searching for pattern and mutation in theDrosophila genome with a P-lacZ vector. Genes Dev 3:1273–1287Google Scholar
  5. Bodmer R, Jan YN (1987) Morphological differentiation of the embryonic peripheral neurons in Drosophila. Roux's Arch Dev Biol 196:69–77Google Scholar
  6. Campos-Ortega J, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New YorkGoogle Scholar
  7. Endow SA, Hatsumi M (1991) A multimember kinesin gene family inDrosophila. Proc Natl Acad Sci USA 88:4424–4427Google Scholar
  8. Fehon RG, Johansen K, Rebay I, Artavanis-Tsakonis S (1991) Complex cellular and subcellular regulation ofNotch expression during embryonic and imaginal development ofDrosophila: Implications forNotch function. J Cell Biol 113:657–669Google Scholar
  9. Fredieu JR, Mahowald AP (1989) Glial interactions with neurons duringDrosophila embryogenesis. Development 106:739–748Google Scholar
  10. Ghysen A (1978) Sensory axons recognize defined pathways inDrosophila central nervous system. Nature 271:869–872Google Scholar
  11. Ghysen A (1991) Le developpement du Système nerveux chez la drosophile. These d'agregation de l'enseignement supérieur, Université Libre de Bruxelles, BrusselsGoogle Scholar
  12. Ghysen A, Dambly-Chaudiere C, Aceves E, Jan LY, Jan YN (1986) Sensory neurons and peripheral pathways inDrosophila embryos. Roux's Arch Dev Biol 195:281–289Google Scholar
  13. Greningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance inDrosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45–57Google Scholar
  14. Halpern ME, Chiba A, Johansen J, Keshishian H (1991) Growth cone behavior underlying the development of stereotypic connections inDrosophila embryos. J Neurosci 11:3227–3238Google Scholar
  15. Hartenstein V (1988) Development ofDrosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation. Development 102:869–886Google Scholar
  16. Hartenstein V, Jan YN (1992) StudyingDrosophila embryogenesis with P-IacZ enhancer trap lines. Roux's Arch Dev Biol 201:194–220Google Scholar
  17. Innis MA, Gelfand DH, Sininsky JJ, White TJ (1990) PCR protocols: a guide to methods and applications. Academic Press, San DiegoGoogle Scholar
  18. Jacobs JR, Goodman CS (1989) Embryonic development of axon pathways in theDrosophila CNS: I. A glial scaffold appears before the first growth cones. J Neurosci 9:2402–2411Google Scholar
  19. Jacobs JR, Hiromi Y, Patel NH, Goodman CS (1989) Lineages migration and morphogenesis of longitudinal glia in theDrosophila CNS as revealed by a molecular lineage marker. Neuron 2:1625–1631Google Scholar
  20. Johansen J, Halpern ME, Keshishian H (1989) Axonal guidance and the development of muscle fiber-specific innervation inDrosophila embryos. J Neurosci 9:4318–4332Google Scholar
  21. Klambt C, Jacobs JR, Goodman CS (1991) The midline of theDrosophila central nervous system: a model for the genetic analysis of cell fate, cell migration and growth cone guidance. Cell 64:801–815Google Scholar
  22. Lindsley DL, Grell EH (1968) Genetic variations in Drosophila melanogaster. Publication no 627 Carnegie Institution of Washington, Washington, DCGoogle Scholar
  23. Mahowald AP, Kambysellis MP (1977) Oogenesis. In: Ashburner M, Wright TRF (eds) Biology ofDrosophila, part 2D. Academic Press, New York, pp 141–224Google Scholar
  24. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NYGoogle Scholar
  25. Meinertzhagen IA, O'Neil SD (1991) Synaptic organization of columnar elements in the lamina of the wild type inDrosophila melanogaster. J Comp Neurol 305:232–263Google Scholar
  26. Moses K, Rubin GM (1991)glass Encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the devolopingDrosophila eye. Genes Dev 5:583–593Google Scholar
  27. Nose A, Mahajan VB, Goodman CS (1992) Connectin: a hemophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them inDrosophila. Cell 70:553–567Google Scholar
  28. O'Kane CJ, Gehring WJ (1987) Detection in situ of genomic regulatory elements inDrosophila. Proc Natl Acad Sci USA 80:9123–9127Google Scholar
  29. Palka J, Malone MA, Ellison RL, Wigston DJ (1986) Central projections of identifiedDrosophila sensory neurons in relation to their time of development. J Neurosci 6:1822–1830Google Scholar
  30. Patel NH, Snow PM, Goodman CS (1987) Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways inDrosophila. Cell 48:975–988Google Scholar
  31. Rubin GM, Spradling AC (1982) Genetic transformation ofDrosophila with transposable element vectors. Science 218:348–353Google Scholar
  32. Simpson P, Carteret C (1990) Proneural clusters: equivalence groups in the epithelium ofDrosophila. Development 110:927–932Google Scholar
  33. Sink H, Whitington PM (1991) Pathfinding in the central nervous system and periphery by identified embryonicDrosophila motor axons. Development 112:307–316Google Scholar
  34. Spradling AC, Rubin GM (1982) Transposition of cloned P elements intoDrosophila germ line chromosomes. Science 218:341–347Google Scholar
  35. Steward RJ, Pesavento PA, Woerpel DN, Goldstein LS (1991) Identification and partial characterization of six members of the kinesin superfamily inDrosophila. Proc Natl Acad Sci USA 88:8470–8474Google Scholar
  36. Thomas JB, Bastiani MJ, Bate M, Goodman CS (1984) From grasshopper toDrosophila: a common plan for neuronal development. Nature 310:203–207Google Scholar
  37. Thummel C, Boulet AM, Lipshitz HD (1988) Vectors forDrosophila P-element-mediated transformation and tissue culture transfection. Gene 74:445–456Google Scholar
  38. Vale RD, Schnapp BJ, Reese TS, Sheetz MP (1985a) Organelle, bead and microtubule translocations promoted by soluble factors from the squid giant axon. Cell 40:559–569Google Scholar
  39. Vale RD, Reese TS, Sheetz MP (1985b) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39–50Google Scholar
  40. Vale RD, Schnapp BJ, Mitchison T, Steuer E, Reese TS, Sheetz MP (1985c) Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell 43:623–632Google Scholar
  41. Vallee RB, Bloom GS (1991) Mechanisms of fast and slow axonal transport. Annu Rev Neurosci 14:59–92Google Scholar
  42. Wyman RJ, Thomas JB (1983) What genes are necessary to make an identified synapse? Cold Spring Harbor Symposia on Quantitative Biology 48:641–652Google Scholar
  43. Yang JT, Saxton WM, Goldstein LS (1988) Isolation and characterization of the gene encoding the heavy chain ofDrosophila kinesin. Proc Natl Acad Sci USA 85:1864–1868Google Scholar
  44. Yang JT, Laymon RA, Goldstein LS (1989) A three-domain structure of kinesin heavy chain revealed by DNA sequencing and microtubule binding analysis. Cell 56:879–889Google Scholar
  45. Yang JT, Saxton WM, Stewart RJ, Raff EC, Goldstein LS (1990) Evidence that the head of kinesin is sufficient for force generation and motility in vitro. Science 249:42–47Google Scholar
  46. Zipursky SL, Venkatesh TR, Teplow DB, Benzer S (1984) Neuronal development in theDrosophila retina: monoclonal antibodies as molecular probes. Cell 36:15–26Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Edward Giniger
    • 1
  • William Wells
    • 1
  • Lily Yeh Jan
    • 1
  • Yuh Nung Jan
    • 1
  1. 1.Howard Hughes Medical Institute and Departments of Biochemistry and Biophysics and of Physiology, Rm U-426University of California, San FranciscoSan FranciscoUSA

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