Abstract
The Drosophila neuromusculin (nrm) gene encodes an immunoglobulin-like (Ig-like) cell adhesion molecule expressed in the precursors of the embryonic peripheral nervous system (PNS), in the midline precursors of the central nervous system (CNS), and in muscles. During the initial phases of CNS axonogenesis, nrm is expressed in cells involved in the development of commissures and longitudinal tracts. Mutations which alter expression of nrm mRNAs cause aberrant development of commissures and longitudinal axon pathways. Defects in the PNS and muscles of nrm mutants are also observed. In most nrm embryos, abnormal development can be detected in a subset of abdominal segments; however, in approximately 1 of 10 nrm embryos, the defects extend to all segments. Herein, we present evidence that nrm plays an important role in early morphogenesis, possibly by mediating or facilitating inductive cell contacts and movements.
Similar content being viewed by others
References
Bennett RL, Hoffmann MF (1992) Increased levels of the Drosophila Abelson tyrosine kinase in nerves and muscles: subcellular localization and mutant phenotypes imply a role in cell-cell interactions. Development 116:953–966
Bellen HJ, O'Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring W (1989) P-element mediated enhancer detection: a versatile method to study development in Drosophila. Gen Dev 3:1288–1300
Bieber AJ, Snow PM, Hortsch M, Patel NH, Jacobs JR, Traquina ZR, Schilling J, Goodman CS (1989) Drosophila neuroglian: A member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59:447–460
Cabrera CV (1992) The generation of cell diversity during early neurogenesis in Drosophila. Development 115:893–901
Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin
Canal I, Ferrus A (1986) The pattern of early neuronal differentiation in Drosophila melanogaster. J Neurogen 3:293–319
DeSimone SM, White K (1993) The Drosophila erect wing gene, which is important for both neuronal and muscle development, encodes a protein which is similar to the sea urchin P3A2 DNA binding protein. Mol Cell Biol 13:3641–3649
Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila nervous system. Development 116:855–864
Elkins T, Zinn K, McAllister L, Hoffmann FM, Goodman CS (1990) Genetic analysis of a Drosophila neural cell adhesion molecule: Interaction of fasciclin I and abelson tyrosine kinase mutations. Cell 60:565–575
Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL (1982) Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci USA 79:7929–7933
Ghysen A, O'Kane C (1989) Neural enhancer-like elements as specific cell markers in Drosophila. Development 105:35–52
Ghysen A, Dambly-Chaudiere C, Jan LY, Jan YN (1993) Cell interactions and gene interactions in peripheral neurogenesis. Gen Dev 7:723–733
Goodman CS, Bastiani MJ, Doe CQ, du Lac S, Helfand SL, Kuwada KY, Thomas JB (1984) Cell recognition during neuronal development. Science 225:1271–1279
Goodman CS, Doe CQ (1993) Embryonic development of the Drosophila central nervous system. In: The development of Drosphila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67:45–57
Hortsch M, Goodman CS (1992) Cell and substrate adhesion molecules in Drosophila. Annu Rev Cell Biol 7:505–557
Huang F, Dambly-Chaudiere C, Ghysen A (1991) The emergence of sense organs in the wing disc of Drosophila. Development 111:1087–1095
Ingham PW, Taylor AM, Nakano Y (1991) Role of the Drosophila patched gene in positional signalling. Nature 353:184–186
Jacobs IR, Goodman CS (1989a) Embryonic development of axon pathways in the Drosophila CNS: I. A glial scaffold appears before the first growth cones. J Neurosci 9:2402–2411
Jacobs IR, Goodman CS (1989b) Embryonic development of axon pathways in the Drosophila CNS: II. Behavior of pioneer growth cones. J Neurosci 9:2412–2422
Kania A, Han P-L, Kim Y-T, Bellen H (1993) neuromusculan, a Drosophila gene expressed in peripheral neuronal precursors and muscles encodes a cell adhesion molecule. Neuron 11:673–687
Klambt C, Jacobs IR, Goodman CS (1991) The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration and growth cone guidance. Cell 64:801–815
Lefevre G, Watkins W (1986) The question of the total gene number in Drosophila melanogaster. Genetics 113:869–895
Lindsley DL, Zimm GG (1990) The genome of Drosophila melanogaster. Academic Press, San Diego
Menne TV, Klambt C (1994) The formation of commissures in the Drosophila CNS depends on the midline cells and on the Notch gene. Development 120:123–133
Nose A, Mahajan VB, Goodman CS (1992) Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motorneurons that innervate them in Drosophila. Cell 70:553–567
Patel NH, Snow PM, Goodman CS (1987) Characterization and cloning of fasciclin III: A glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48:975–988
Sambrook J, Fritsh EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Seeger MA, Tear G, Ferrus-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance in Drosophila: Genes necessary for guidance towards or away from the midline. Neuron 10:409–426
Thomas JB, Bastiani MJ, Bate CM, Goodman CS (1984) From grasshopper to Drosophila: A common plan for neuronal development. Nature 310:203–207
Van Vactor D, Sink H, Fambrough D, Tsoo R, Goodman CS (1993) Genes that control neuromuscular specificity in Drosophila. Cell 73:1137–1153
Whitlock KE (1993) Development of Drosophila wing sensory neurons in mutants with missing or modified cell surface molecules. Development 117:1251–1260
Wu CT, Goldberg ML (1989) The Drosophila zeste gene and transvection. Trends Genet 5:189–194
Wu C-T (1993) Transvection, nuclear structure and chromatin proteins. J Cell Biol 120:587–590
Younossi-Hartenstein A, Hartenstein V (1993) The role of the tracheae and musculature during pathfinding of Drosophila embryonic sensory axons. Dev Biol 158:430–447
Zipursky SL, Venkatesh TR, Teplow DB, Benzer S (1984) Neuronal development in the Drosophila retina: Monoclonal antibodies as molecular probes. Cell 36:15–26
Rights and permissions
About this article
Cite this article
Kania, A., Bellen, H.J. Mutations in neuromusculin, a gene encoding a cell adhesion molecule, cause nervous system defects. Roux's Arch Dev Biol 204, 259–270 (1995). https://doi.org/10.1007/BF00208493
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00208493