Here are indicated the main papers that describe
Drosophila
embryonic and larval sensory organs.
Description
of each abdominal sensory organ cell
has been investigated and refined from 1930 to now on: additional
cells have been noticed, some mono-innervated organs have been found to
be actually bi-innervated organs, "no-dendrite neurons" have been found
retrospectively to be multidendritic etc.
Here are the descriptions of the abdominal sensory
organ pattern A1-A7, starting from 1930. Please note that there are slight
differences between most of these descriptions.
Hertweck, H. 1931. Anatomie und Variabilität des nervensystems und
der Sinnesorgane von
Drosophila
melanogaster (Meigen).
Z wiss
Zool 139, pp. 559-663.
Kankel, D. R., Ferrus, A., Garen, S. H., Harte, P. J. and Lewis, P.,
1980. The structure and development of the nervous system. In:
The Genetics of Drosophila, vol.
2d, ed. M. Ashburner and T.R. F. Wright, pp. 295-368. London. Academic
Press.
Campos-Ortega, J. A. and Hartenstein, V. 1985. The embryonic
development of
Drosophila
melanogaster. Berlin/Heidelberg/New-York/Tokyo.: Springer-Verlag.
Hartenstein, V. and Campos-Ortega, J. A. 1986. The peripheral nervous
system of mutants of early neurogenesis in
Drosophila melanogaster.
Roux's Arch. Dev. Biol. 195, pp. 210-221.
Dambly-Chaudiere, C. and Ghysen, A. 1986. The sense organs in the
Drosophila larva and their relation
to embryonic pattern of sensory neurons.
Roux's Arch. Dev. Biol. 195, pp. 222-228.
Ghysen, A., Dambly-Chaudiere, C., Aceves, E., Jan, L. Y. and Jan, Y. N.
1986. Sensory neurons and peripheral pathways in
Drosophila embryos.
Roux's Arch. Dev. Biol. 195, pp. 281-289.
Bodmer, R. and Jan, Y. N. 1987. Morphological differentiation of the
embryonic peripheral neurons in
Drosophila.
Roux's Arch. Dev. Biol. 196, pp. 69-77.
Hartenstein, V. 1988. Development of
Drosophila
larval sensory organs : spatiotemporal pattern of sensory neurones,
peripheral axonal pathways and sensilla differentiation.
Development 102, pp. 869-886.
Kuhn D.T., Sawyer M., Packert G., Turenchalk G., Mack J. A., Sprey
T. E., Gustavson E., Kornberg, T.B. 1992. Development of the
D.
melanogaster caudal segments involves suppression of the ventral
regions of A8, A9 and A10.
Development
116, pp. 11-20.
Medline
Kuhn D.T., Sawyer M., Ventimiglia, J. and Sprey
T. E. 1992. Cuticle morphology changes with each larval molt in
D. melanogaster.
D.I.S. 71, pp. 218-222.
Campos-Ortega, J.-A. and Hartenstein, V. 1997. The embryonic
development of
Drosophila
melanogaster. Berlin/Heidelberg/New-York/Tokyo.: Springer-Verlag.
Description
of the dendritic arborization of multidendritic neurons is given
in:
Bodmer, R. and Jan, Y. N. 1987. Morphological differentiation of the
embryonic peripheral neurons in
Drosophila.
Roux's Arch. Dev. Biol. 196, pp. 69-77.
Gao FB, Brenman JE, Jan LY, Jan YN. 1999. Genes
regulating dendritic outgrowth, branching, and routing in Drosophila.
Genes Dev.
13, pp. 2549-61.
Medline
Sweeney NT, Li W, Gao FB. 2002. Genetic
manipulation of single neurons in vivo reveals specific roles of
flamingo in neuronal morphogenesis.
Dev Biol 247, pp. 76-88.
Medline
Grueber,
W.B., Jan, L.Y. and Jan, Y.N., 2002. Tiling of the
Drosophila
epidermis by multidendritic sensory neurons.
Development 129,
pp. 2867–2878.
Medline
Description
of axonal pathways is given in:
Campos-Ortega, J. A. and Hartenstein, V. 1985. The embryonic
development of
Drosophila
melanogaster. Berlin/Heidelberg/New-York/Tokyo.: Springer-Verlag.
Ghysen, A., Dambly-Chaudiere, C., Aceves, E., Jan, L. Y. and Jan, Y. N.
1986. Sensory neurons and peripheral pathways in
Drosophila embryos.
Roux's Arch. Dev. Biol. 195, pp. 281-289.
Bodmer, R. and Jan, Y. N. 1987. Morphological differentiation of the
embryonic peripheral neurons in
Drosophila.
Roux's Arch. Dev. Biol. 196, pp. 69-77.
Hartenstein, V. 1988. Development of
Drosophila
larval sensory organs : spatiotemporal pattern of sensory neurones,
peripheral axonal pathways and sensilla differentiation.
Development
102, pp. 869-886.
Merritt, D. J. and Whitington, P. M. 1995. Central projections of
sensory neurons in the
Drosophila
embryo correlate with sensory modality, soma position, and proneural
gene function.
J Neurosci 15, pp. 1755-67.
Medline
(please note that the nomenclature used in this paper for dorsal
and
ventral md neuron does not fully correspond to the nomenclature used
here)
Campos-Ortega, J.-A. and Hartenstein, V. 1997. The embryonic
development of
Drosophila
melanogaster. Berlin/Heidelberg/New-York/Tokyo.: Springer-Verlag.
Schrader, S. and Merritt, D.J. 2000. Central projections of Drosophila
sensory neurons in the transition from embryo to larva.
J Comp Neurol. 425, pp. 34-44.
Medline
Harris, K.L. and Whitington, P.M. 2001. Pathfinding by sensory axons in
Drosophila: substrates and
choice points in early lch5 axon outgrowth.
J Neurobiol. 48, pp. 243-55.
Medline
Zlatic M, Landgraf M, Bate M. 2003. Genetic specification of axonal
arbors: atonal regulates robo3 to position terminal branches in the
Drosophila nervous system.
Neuron
37, pp. 41-51.
Medline
Grueber WB, Ye B, Yang CH, Younger S, Borden K, Jan LY, Jan YN. 2007.
Projections of Drosophila multidendritic neurons in the central nervous
system: links with peripheral dendrite morphology.
Development.
134(1):55-64. Medline
Description
of the developmental changes from late embryonic PNS to third
instar larva PNS, and even to the adult:
no gross change in
sensory organ pattern:
Dambly-Chaudiere, C. and Ghysen, A. 1986. The sense organs in the
Drosophila larva and their relation
to embryonic pattern of sensory neurons.
Roux's Arch. Dev. Biol. 195, pp. 222-228.
Kuhn D.T., Sawyer M., Ventimiglia, J. and Sprey
T. E. 1992. Cuticle morphology changes with each larval molt in
D. melanogaster.
D.I.S. 71, pp. 218-222.
Campos-Ortega, J.-A. and Hartenstein, V. 1997. The embryonic
development of
Drosophila
melanogaster. Berlin/Heidelberg/New-York/Tokyo.: Springer-Verlag.
remodeling of axons
and dendrites:
(not exhaustive)
Schrader S. and Merritt, D.J. 2000. Central projections of Drosophila
sensory neurons in the transition from embryo to larva.
J Comp Neurol. 425, pp. 34-44.
Medline
Zlatic M, Landgraf M, Bate M. 2003. Genetic specification of axonal
arbors: atonal regulates robo3 to position terminal branches in the
Drosophila nervous system.
Neuron
37, pp. 41-51.
Medline
Grueber, W. B., Ye, B., Moore, A. W., Jan, L. Y. and Jan, Y. N. 2003.
Dendrites of distinct classes of Drosophila sensory neurons show
different capacities for homotypic repulsion.
Curr Biol 13, pp. 618-26.
Medline
Sugimura, K., Yamamoto, M., Niwa, R., Satoh, D., Goto, S., Taniguchi,
M., Hayashi, S. and Uemura T. 2003. Distinct developmental modes and
lesion-induced reactions of dendrites of two classes of Drosophila
sensory neurons.
J Neurosci. 23, pp. 3752-60.
Medline
Williams, D.W. and Truman, J.W. 2004. Mechanisms of dendritic
elaboration of sensory neurons in Drosophila: insights from in vivo
time lapse. J Neurosci.
24,
pp.1541-50.
Medline
Kuo CT, Jan LY, Jan YN. Dendrite-specific remodeling of Drosophila
sensory neurons requires matrix metalloproteases, ubiquitin-proteasome,
and ecdysone signaling. Proc Natl Acad Sci U S A. 2005
102, pp. 15230-5.
Medline
Williams DW, Truman JW. Cellular mechanisms of dendrite pruning in
Drosophila: insights from in vivo time-lapse of remodeling dendritic
arborizing sensory neurons. Development. 2005
132, pp. 3631-42.
Medline
apoptosis of
specific sensory cells, survival of others during metamorphosis:
Shepherd, D. and Smith, S. A. 1996. Central projections of persistent
larval sensory neurons prefigure adult sensory pathways in the CNS of
Drosophila.
Development 122, pp. 2375-84.
Medline
Williams, D. W. and Shepherd, D. 1999. Persistent larval sensory
neurons in adult
Drosophila
melanogaster.
J Neurobiol 39, pp. 275-86.
Medline
Usui-Ishihara, A., Simpson, P. and Usui, K. 2000. Larval multidendrite
neurons survive metamorphosis and participate in the formation of
imaginal sensory axonal pathways in the notum of
Drosophila.
Dev Biol 225, pp. 357-69.
Medline
Williams, D. W. and Shepherd, D. 2002. Persistent larval sensory
neurones are required for the normal development of the adult sensory
afferent projections in
Drosophila.
Development 129:617-24.
Medline
Williams DW, Truman JW. Cellular mechanisms of dendrite pruning in
Drosophila: insights from in vivo time-lapse of remodeling dendritic
arborizing sensory neurons. Development. 2005
132:3631-42.
Medline
probable
functions of multidendritic neurons:
tension-sensitive, mechanoreceptor,
proprioceptor:
Osborne, M.P., 1963. The sensory neurones and sensilla in the abdomen
and thorax of the blowfly larva.
Quart.
J. Micr. Sci. 104:
227-241. Medline
Such a function was suggested by the author for Calliphora
multidendritic neurons according to their dendritic arborization. This
paper has later been cited as an indication of the possible same
function in D. melanogaster.
Adams, C.M., Anderson, M.G., Motto, D.G.,
Price, M.P., Johnson, W.A., Welsh, M.J., 1998. Ripped pocket and
pickpocket, novel Drosophila DEG/ENaC subunits expressed in early
development and in mechanosensory neurons.
J Cell Biol. 140: 143-52.
Medline
Schrader S. and Merritt, D.J. 2000. Central projections of Drosophila
sensory neurons in the transition from embryo to larva.
J Comp Neurol. 425, pp. 34-44.
Medline
Grueber,
W.B., Jan, L.Y. and Jan, Y.N., 2002. Tiling of the
Drosophila
epidermis by multidendritic sensory neurons.
Development 129: 2867-2878.
Medline
Hughes, C.L., and Thomas, J.B. 2007. A sensory feedback circuit coordinates muscle activity in Drosophila.
Mol Cell Neurosci 35: 383-396.
Song, W., Onishi, M., Jan, L.Y., and Jan, Y.N. 2007. Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior
in Drosophila larvae.
PNAS 104: 5199-5204.
temperature-sensitive:
Liu, L., Yermolaieva, O., Johnson, W.A., Abboud, F.M., Welsh, M.J.
2003. Identification and function of thermosensory neurons in
Drosophila larvae.
Nat Neurosci.
6, pp. 267-73.
Medline
Tracey, W.D. Jr, Wilson, R.I., Laurent, G., Benzer, S. 2003. painless,
a Drosophila gene essential for nociception.
Cell 113,pp. 261-73.
Medline
nociceptor:
Tracey, W.D. Jr, Wilson, R.I., Laurent, G., Benzer, S. 2003. painless,
a Drosophila gene essential for nociception.
Cell 113,pp. 261-73.
Medline
Zhang, W., Ge, W., Wang, Z. 2007. A toolbox for light control of Drosophila behaviors through Channelrhodopsin 2-mediated photoactivation
of targeted neurons.
Eur J Neurosci 26: 2405-2416.
Hwang, R.W., Zhong, L., Xu, Y., Johnson, T., Zhang, F., Deisseroth, K., Tracey W.D. Jr. 2007.
Nociceptive neurons protect Drosophila larvae from parasitiod wasps
Curr Biol 17, pp. 2105-2116.
Medline
neurosecretory:
Hewes, R.S., Park, D., Gauthier, S.A., Schaefer, A.M., Taghert,
P.H. 2003. The bHLH protein Dimmed controls neuroendocrine cell
differentiation in Drosophila.
Development
130, pp. 1771-81.
Medline
Description
of sensory organ development:
(not exhaustive)
proneural genes:
Dambly-Chaudiere, C. and Ghysen, A. 1987.
Independent subpatterns of sense organs require independent genes of
the achaete-scute complex in Drosophila larvae.
Genes & Development
1, pp. 297-306.
Jarman, A. P., Grau, Y., Jan, L. Y. and Jan,
Y. N. 1993.
atonal is a
proneural gene that directs chordotonal organ
formation in the Drosophila peripheral nervous system.
Cell 73, pp.
1307-1321.
Medline
Ruiz-Gomez, M. and Ghysen, A. 1993. The expression and role of a
proneural gene, achaete, in the development of the larval nervous
system of Drosophila.
EMBO J.
12, pp. 1121-30.
Medline
Huang, M.-H., Hsu, C.-H. and Chien, C.-T.
2000. The proneural gene amos promotes multiple dendritic neuron
formation in the Drosophila peripheral nervous system.
Neuron 25, pp.
57-67.
Medline
Marcellini S, Gibert JM, Simpson P. achaete, but not scute, is
dispensable for the peripheral nervous system of Drosophila. Dev Biol.
2005 Sep 15;285(2):545-53.
Medline
cell lineages:
Bodmer,
R. and Jan, Y.N., 1987. Morphological differentiation of the embryonic
peripheral neurons in
Drosophila.
Roux's Arch. Dev. Biol.
196, pp. 69–77.
Brewster,
R. and Bodmer, R., 1995. Origin and specification of type II sensory
neurons in
Drosophila.
Development 121,
pp. 2923–2936.
Medline
Vervoort, M., Merritt, D. J., Ghysen, A. and Dambly-Chaudiere, C. 1997.
Genetic basis of the formation and identity of type I and type II
neurons in Drosophila embryos.
Development
124, pp. 2819-2828.
Medline
Orgogozo,
V.,
Schweisguth, F. and Bellaïche, Y., 2001. Lineage, cell polarity
and
inscuteable function in the peripheral nervous system of the
Drosophila
embryo.
Development 128, pp. 631–643.
Medline
Orgogozo,
V., Schweisguth, F. and Bellaiche, Y., 2002. Binary cell death decision
regulated by unequal partitioning of Numb at mitosis.
Development
129, pp. 4677–4684.
Medline
Umesono,
Y., Hiromi, Y. and Hotta, Y., 2002. Context-dependent utilization of
Notch activity in
Drosophila glial determination.
Development
129, pp. 2391–2399.
Medline
Lai, E.C. and Orgogozo, V., 2004. A hidden
program in Drosophila peripheral neurogenesis revealed: fundamental
principles underlying sensory organ diversity.
Dev Biol. 269, pp. 1-17.
Medline
(review)
cell recruitment:
zur
Lage, P., Jan, Y.N. and Jarman, A.P., 1997. Requirement for EGF
receptor signalling in neural recruitment during formation of
Drosophila
chordotonal sense organ clusters [see comments] .
Curr. Biol. 7,
pp. 166–175.
Medline
Okabe,
M. and Okano, H., 1997. Two-step induction of chordotonal organ
precursors in
Drosophila embryogenesis.
Development 124,
pp. 1045–1053.
Medline
Rusten,
T.E., Cantera,
R., Urban, J., Technau, G., Kafatos, F.C. and Barrio, R., 2001. Spalt
modifies EGFR-mediated induction of chordotonal precursors in the
embryonic PNS of
Drosophila promoting the development of
oenocytes.
Development 128, pp. 711–722.
Medline
Elstob, P.R., Brodu, V. and Gould, A.P. 2001.
Spalt-dependent switching between two cell fates that are induced by
the Drosophila EGF receptor.
Development.
128, pp. 723-32.
Medline
Gould, A. P., Elstob, P. R. and Brodu, V.
2001. Insect oenocytes: a model system for studying cell-fate
specification by Hox genes.
J Anat 199, pp. 25-33.
Medline
(review)
Lai, E.C. and Orgogozo, V., 2004. A hidden
program in Drosophila peripheral neurogenesis revealed: fundamental
principles underlying sensory organ diversity.
Dev Biol. 269, pp. 1-17.
Medline
(review)
Inbal, A., Volk, T. and Salzberg, A. 2004. Recruitment of ectodermal
attachment cells via an EGFR-dependent mechanism during the
organogenesis of Drosophila proprioceptors. Dev Cell.
7, pp.241-50.
Medline
Comments and additions are welcome at:
Virginie.Orgogozo snv.jussieu.fr