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Linking Neuroblasts to Their Corresponding Lineage

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Bossing, T., Doe, C. Q., Rickert, C., Schmidt, H., Technau, G. M., Udolph, G., Urban, J. and Vef, O.
G. M. Technau, Institute of Genetics, Becherweg 32, 55099 Mainz, Germany

Originally published in: Bossing et al., Dev Biol 179, 41-64(1996)
and Schmidt et al., Dev Biol 189, 186-204 (1997)


Introduction
Materials & Methods
Results
Discussion
References


Introduction

Development of the central nervous system (CNS) in Drosophila starts with the delamination from the neuroectoderm of about 30 neuroblasts (NBs) per hemineuromere, giving rise to approximately 330 - 350 neurons and 30 glial cells. Understanding the mechanisms leading to cell fate specification and differentiation in the CNS requires the identification of the NB lineages. Here we present the combined data from Bossing et al. (1996) and Schmidt et al. (1997), i.e. 29 embryonic NB lineages. With one exception we were able to link these lineages to the corresponding NBs. Two NBs give rise to glial progeny exclusively (GP, NB 6-4A), seven NB lineages are composed of glial cells as well as neurons (NB 1-1A, 1-3, 2-2T, 2-5, 5-6, 6-4T and 7-4) while the other NB lineages only contain neuronal cells.


Materials & Methods

Time of Delamination for Individual NBs Observed  in vivo

S/

NB

S1

S 1/2

S2

S2/3

S3

S3 /4

S4

S4/5

S5

NB 1-1

14

4

9


1

2




NB 2-5

27

2








NB 3-2

9

6

2



1




NB 3-5

17

1








NB 5-2

23

8

4

2

2





NB 5-3

8

5

2







NB 5-6

13

2

1



1




NB 7-1

18









NB 7-4

8









MP2

21

8

6


2





NB 2-2


5

13

3

7

1




NB 4-2

1

4

6







NB 6-2



3

1

1




1

NB 7-2


1

4

1





1

NB 1-2

2

7

5

3

9

2




NB 3-1



2

2

6





NB 4-1

1


1

3

11




1

NB 6-1

1

4

2


12

2



1

NB 6-4



3

1

7

2




NB 1-3





1

1




GP





1

1




NB 2-1






1

6

3


NB 3-3

1




1

3

3

2

1

NB 4-4






4

3

2

1

NB 5-4






2

5

3

2

NB 4-3






2

2

2

1

NB 7-3







5

1

3

NB 2-4






1

2

5

2

NB 5-1







6

For the assignment of the NBs to the five waves of segregation (S1-S5; Doe, 1992) the first division of the ventral midline cells was taken as an internal time reference. Ventral midline cell proliferation starts, depending on room temperature, 25 to 45 min after the onset of gastrulation. The following assignment corresponds to Doe (1992) and Bossing et al. (1996).

segregation wave

complete delamination of NB

[min after division of ventral midline cells]

embryonic stage

S1

30

8/9

S2

30-60

9/early 10

S3

60-100

10

S4

100 to beginning of stage

11 10/early 11

S5

later

11/late 11


Results

Interactive Neuroblasts

Click on each NB to see its lineage

NB map

Semi-schematic drawing of the arrangement and typical morphologies of the NBs as observed in vivo around late stage 11 (according to Bossing et al., 1996) . The NBs derived from the dorsal part of the neuroectoderm were described in Schmidt et al. (1997) and are outlined bold. The others were described in Bossing et al. (1996). A ventral view is shown, anterior is to the top, lateral to the right. To underline the often observed variabilities in shape and location of particular NBs (e.g., GP, NB 6-4), two hemisegments are drawn. Glial progenitors NB 6-4A and GP divide almost symmetrically (6-4a, 6-4b; GPa,GPb). The newly discovered NB 1-3 is introduced into the map. Colour code marks different types of progeny (motoneurons, interneurons, glia) as indicated. Since no lineage is assigned to NBs 2-3, 3-4 and 5-5, they are coloured grey. We found one lineage that we were not able to assign to a particular NB (click here to see).


Discussion

Nomenclature of Neurons

1. symbol

"X-X"

parent NB, from which the clone derived

2. symbol

"M" vs "I"

Motoneuron versus Interneuron

3. symbol

"i" vs "c"

ipsilateral versus contralateral axonal projection

4. symbol

"a" vs "p"

anterior versus posterior commissure

5. symbol

"s" vs "ar" vs "pr"

motoneuronal projection extending along the segmental nerve (s),

or the anterior (ar) or posterior root (pr) of the intersegmental nerve

6. symbol

numbers

neurons distinguishable by further criteria

The nomenclature is according to Bossing et al. (1996) and is described there in detail. Use of symbols is kept to a minimum, e.g., if a clone only comprises interneurons projecting contralaterally across the same commissure, they are simply refered to as "X-XI", without specification of the commissure concerned.

Nomenclature of Glial cells

Glial Subtype

Individual Cells

SPG: subperineurial glia

MD-SPG: Medial Dorsal SPG

LD-SPG: Lateral Dorsal SPG

DL-SPG: Dorsal Lateral SPG

VL-SPG: Ventral Lateral SPG

LV-SPG: Lateral Ventral SPG

MV-SPG: Medial Ventral SPG

CG: channel glia

D-CG: Dorsal CG

V-CG: Ventral CG

CBG: cell body glia

MM-CBG: MedialMost CBG (VUM support cell)

M-CBG: Medial CBG

VL-CBG:  Ventral Lateral CBG

L-CBG: Lateral CBG

ISNG: intersegmental nerve root glia

M-ISNG: Medial ISNG  (segment boundary cell)

L-ISNG:  Lateral ISNG

SNG: segmental nerve root glia

M-SNG: Medial SNG

L-SNG: Lateral SNG

IG: interface glia

(longitudinal glia)

D-IG: Dorsal IG

L-IG: Lateral IG

V-IG: Ventral IG

PG: peripheral glia

Only the nomenclature for the glial cells identified in this work is shown. The complete glial nomenclature is described in detail in Ito et al. (1995) . Former names of some of the glial cells are included in brackets.


References

Bate, C.M. (1993). The mesoderm and its derivatives. In The development of Drosophila melanogaster. (ed. M.Bate and A.Martinez Arias),Vol.2, 1013-1091. CSHL press.

Broadus, J., Skeath, J.B., Spana, E.P., Bossing, T., Technau, G.M. and Doe, C.Q. (1995). New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. of Develop. 53, 393-402.

Bossing, T. and Technau, G. M. (1994). The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 120, 1895-1906.

Bossing, T., Udolph, G., Doe, C. Q., and Technau, G. M. (1996). The embryonic central nervous system lineages of Drosophila melanogaster: I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179, 41-64.

Buenzow, D.E. and Holmgren, R. (1995) Expression of the Drosophila gooseberry locus defines a subset of neuroblast lineages in the central nervous system. Dev. Biol. 170, 338-349

Chu-LaGraff, Q., Schmid, A., Leidel, J., Brönner, G., Jäckle, H. and Doe, C.Q. (1995). huckebein specifies aspects of CNS precursor identity required for motoneuron axon pathfinding. Neuron 15, 1041-1051.

Crossley, C. (1978). The morphology and development of the Drosophila muscular system. In The genetics and biology of Drosophila (ed. M. Ashburner and T. Wright), Vol. 2b, pp. 499-560. Academic Press, New York.

Cui, X. and Doe, C.Q. (1992). ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116, 943-952.

Doe, C. Q. (1992). Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863.

Doe, C.Q., Hiromi, Y., Gehring, W.J. and Goodman C.S. (1988a). Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science 239, 170-175.

Goodman, C. S., Bastiani, M. J., Doe, C. Q., du Lac, S., Helfand, S. L., Kuwada, J. Y. and Thomas, J. B. (1984). Cell recognition during neuronal development. Science 225, 1271-1279.

Goodman, C. S. and Doe, C. Q. (1993). Embryonic development of the Drosophila central nervous system. In The development of Drosophila melanogaster. (ed. M. Bate and A. Martinez Arias) Vol.2, pp. 1131-1207. CSHL press.

Ito, K., Urban, J., and Technau, G. M. (1995). Distribution, classification , and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch. Dev. Biol. 204, 284-307.

Jacobs, J.R. and Goodman, C.S. (1989). Embryonic development of axon pathways in the Drosophila CNS. II. Behavior of Pioneer growth cones. J. Neurosci. 9, 2412-2422.

Klämbt, C. and Goodman, C. S. (1991). The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4, 205-213.

Patel, N. H., Schafer, B., Goodman, C. S. and Holmgren, R. (1989a). The role of segment polarity genes during Drosophila neurogenesis. Genes Dev. 3, 890-904.

Schmidt, H., Rickert, C., Bossing, T., Vef, O., Urban, J. and Technau, G.M. (1997). The embryonic central nervous system lineages of Drosophila melanogaster: II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189, 186-204.

Sink, H. and Whitington, P. M. (1991). Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J. Neurobiol. 12, 298-311.

Spana, E.P., Kopczynski, C., Goodman, C.S. and Doe, C.Q. (1995). Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121, 3489-3494.

Thomas, J. B., Bastiani, M. J., Bate, C. M. and Goodman, C. S. (1984). From grasshopper to Drosophila: a common plan for neuronal development. Nature 310, 203-207.

Udolph, G., Lüer, K., Bossing, T. and Technau, G.M. (1995). Commitment of CNS progenitors along the dorsoventral axis of Drosophila neuroectoderm. Science 269, 1278-1281.


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