A genetic cascade involving klumpfuss, nab and castor specifies the abdominal leucokinergic neurons in the Drosophila CNS

Development

Volumn 137, Issue 19, 2010, Pages 3327-3336

  Benito Sipos, Jonathan ^a,c   Estacio Gómez, Alicia ^a   Moris Sanz, Marta ^a   Baumgardt, Magnus ^b   Thor, Stefan ^b   Díaz Benjumea, Fernando J ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b LINKÖPING UNIVERSITY   (Sweden)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

ABLK; CNS development; Drosophila; Leucokinin; Neuronal fate specification

Indexed keywords

CASTOR GENE; DROSOPHILA PROTEIN; KLUMPFUSS GENE; NAB GENE; NOTCH RECEPTOR; UNCLASSIFIED DRUG; CASTOR PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOKININ PROTEIN, DROSOPHILA; KLU PROTEIN, DROSOPHILA; NAB PROTEIN, DROSOPHILA; NEUROPEPTIDE; NOTCH PROTEIN, DROSOPHILA; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL FATE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; GENE EXPRESSION; NERVE CELL; NEUROBLAST; NONHUMAN; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; CELL LINEAGE; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ANIMALS; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NEUROPEPTIDES; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 77956584154     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.052233     Document Type: Article

References (76)

1. Al-Anzi, B., Armand, E., Nagamei, P., Olszewski, M., Sapin, V., Waters, C., Zinn, K., Wyman, R. J. and Benzer, S. (2010) The leucokinin pathway and its neurons regulate meal size in Drosophila. Curr. Biol. 20, 969-978.
2. Allan, D. W., St Pierre, S. E., Miguel-Aliaga, I. and Thor, S. (2003). Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113, 73-86.
3. Allan, D. W., Park, D., St Pierre, S. E., Taghert, P. H. and Thor, S. (2005). Regulators acting in combinatorial codes also act independently in single differentiating neurons. Neuron 45, 689-700.
4. Almeida, M. S. and Bray, S. J. (2005). Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech. Dev. 122, 1282-1293.
5. Babaoglan, A. B., O'Connor-Giles, K. M., Mistry, H., Schickedanz, A., Wilson, B. A. and Skeath, J. B. (2009). Sanpodo: a context-dependent activator and inhibitor of Notch signaling during asymmetric divisions. Development 136, 4089-4098.
6. Baumgardt, M., Miguel-Aliaga, I., Karlsson, D., Ekman, H. and Thor, S. (2007). Specification of neuronal identities by feedforward combinatorial coding. PLoS Biol. 5, e37.
7. Baumgardt, M., Karlsson, D., Terriente, J., Diaz-Benjumea, F. J. and Thor, S. (2009). Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell 139, 969-982.
8. Bier, E., Vaessin, H., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1992). deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 6, 2137-2151.
9. 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.
10. Brody, T. and Odenwald, W. F. (2000). Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev. Biol. 226, 34-44.
11. Brohl, D., Strehle, M., Wende, H., Hori, K., Bormuth, I., Nave, K. A., Muller, T. and Birchmeier, C. (2008). A transcriptional network coordinately determines transmitter and peptidergic fate in the dorsal spinal cord. Dev. Biol. 322, 381-393.
12. 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.
13. Campos-Ortega, J. A. and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster. Berlin: Springer-Verlag.
14. Cantera, R. and Nassel, D. R. (1992). Segmental peptidergic innervation of abdominal targets in larval and adult dipteran insects revealed with an antiserum against leucokinin I. Cell Tissue Res. 269, 459-471.
15. Cau, E. and Blader, P. (2009). Notch activity in the nervous system: to switch or not switch? Neural Dev. 4, 36.
16. Cenci, C. and Gould, A. P. (2005). Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts. Development 132, 3835-3845. (Pubitemid 41410249)
17. Certel, S. J. and Thor, S. (2004). Specification of Drosophila motoneuron identity by the combinatorial action of POU and LIM-HD factors. Development 131, 5429-5439.
18. Cheah, P. Y., Chia, W. and Yang, X. (2000). Jumeaux, a novel Drosophila winged-helix family protein, is required for generating asymmetric sibling neuronal cell fates. Development 127, 3325-3335.
19. Chu-LaGraff, Q., Schmid, A., Leidel, J., Bronner, G., Jackle, H. and Doe, C. Q. (1995). huckebein specifies aspects of CNS precursor identity required for motoneuron axon pathfinding. Neuron 15, 1041-1051.
20. Cleary, M. D. and Doe, C. Q. (2006). Regulation of neuroblast competence: multiple temporal identity factors specify distinct neuronal fates within a single early competence window. Genes Dev. 20, 429-434.
21. Clements, M., Duncan, D. and Milbrandt, J. (2003). Drosophila NAB (dNAB) is an orphan transcriptional co-repressor required for correct CNS and eye development. Dev. Dyn. 226, 67-81.
22. De Graeve, F., Jagla, T., Daponte, J. P., Rickert, C., Dastugue, B., Urban, J. and Jagla, K. (2004). The ladybird homeobox genes are essential for the specification of a subpopulation of neural cells. Dev. Biol. 270, 122-134.
23. Doe, C. Q. (1992). Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863.
24. Dumstrei, K., Wang, F., Nassif, C. and Hartenstein, V. (2003). Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J. Comp. Neurol. 455, 451-462.
25. Dye, C. A., Lee, J. K., Atkinson, R. C., Brewster, R., Han, P. L. and Bellen, H. J. (1998). The Drosophila sanpodo gene controls sibling cell fate and encodes a tropomodulin homolog, an actin/tropomyosin-associated protein. Development 125, 1845-1856.
26. Garces, A. and Thor, S. (2006). Specification of Drosophila aCC motoneuron identity by a genetic cascade involving even-skipped, grain and zfh1. Development 133, 1445-1455. (Pubitemid 43732958)
27. Grosskortenhaus, R., Pearson, B. J., Marusich, A. and Doe, C. Q. (2005). Regulation of temporal identity transitions in Drosophila neuroblasts. Dev. Cell 8, 193-202.
28. Grosskortenhaus, R., Robinson, K. J. and Doe, C. Q. (2006). Pdm and Castor specify late-born motor neuron identity in the NB7-1 lineage. Genes Dev. 20, 2618-2627.
29. Hamanaka, Y., Park, D., Yin, P., Annangudi, S. P., Edwards, T. N., Sweedler, J., Meinertzhagen, I. A. and Taghert, P. H. (2010). Transcriptional orchestration of the regulated secretory pathway in neurons by the bHLH protein DIMM. Curr. Biol. 20, 9-18.
30. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
31. Herrero, P., Magarinos, M., Torroja, L. and Canal, I. (2003). Neurosecretory identity conferred by the apterous gene: lateral horn leucokinin neurons in Drosophila. J. Comp. Neurol. 457, 123-132.
32. Herrero, P., Magarinos, M., Molina, I., Benito, J., Dorado, B., Turiegano, E., Canal, I. and Torroja, L. (2007). Squeeze involvement in the specification of Drosophila leucokinergic neurons: Different regulatory mechanisms endow the same neuropeptide selection. Mech. Dev. 124, 427-440.
33. Hewes, R. S. and Taghert, P. H. (2001). Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 11, 1126-1142.
34. Hewes, R. S., Park, D., Gauthier, S. A., Schaefer, A. M. and Taghert, P. H. (2003). The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130, 1771-1781.
35. Isshiki, T., Pearson, B., Holbrook, S. and Doe, C. Q. (2001). Drosophila neuroblast sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511-521.
36. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
37. Kambadur, R., Koizumi, K., Stivers, C., Nagle, J., Poole, S. J. and Odenwald, W. F. (1998). Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12, 246-260.
38. Karcavich, R. E. (2005). Generating neuronal diversity in the Drosophila central nervous system: a view from the ganglion mother cells. Dev. Dyn. 232, 609-616.
39. Karcavich, R. and Doe, C. Q. (2005). Drosophila neuroblast 7-3 cell lineage: a model system for studying programmed cell death, Notch/Numb signaling, and sequential specification of ganglion mother cell identity. J. Comp. Neurol. 481, 240-251.
40. Klein, T. and Campos-Ortega, J. A. (1997). klumpfuss, a Drosophila gene encoding a member of the EGR family of transcription factors, is involved in bristle and leg development. Development 124, 3123-3134.
41. Kuwada, J. Y. and Goodman, C. S. (1985). Neuronal determination during embryonic development of the grasshopper nervous system. Dev. Biol. 110, 114-126.
42. Landgraf, M. and Thor, S. (2005). Development of Drosophila motoneurons: Specification and morphology. Semin. Cell Dev. Biol. 17, 3-11.
43. Lundell, M. J., Lee, H. K., Perez, E. and Chadwell, L. (2003). The regulation of apoptosis by Numb/Notch signaling in the serotonin lineage of Drosophila. Development 130, 4109-4121.
44. Maurange, C., Cheng, L. and Gould, A. P. (2008). Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133, 891-902.
45. Miguel-Aliaga, I., Allan, D. W. and Thor, S. (2004). Independent roles of the dachshund and eyes absent genes in BMP signaling, axon pathfinding and neuronal specification. Development 131, 5837-5848. (Pubitemid 40123901)
46. Nassel, D. R. (2002). Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Prog. Neurobiol. 68, 1-84.
47. Novotny, T., Eiselt, R. and Urban, J. (2002). Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. Development 129, 1027-1036.
48. O'Connor-Giles, K. M. and Skeath, J. B. (2003). Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev. Cell 5, 231-243.
49. Park, D., Veenstra, J. A., Park, J. H. and Taghert, P. H. (2008). Mapping peptidergic cells in Drosophila: where DIMM fits in. PLoS ONE 3, e1896.
50. Pearson, B. J. and Doe, C. Q. (2003). Regulation of neuroblast competence in Drosophila. Nature 425, 624-628.
51. Pearson, B. J. and Doe, C. Q. (2004). Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol. 20, 619-647.
52. Petcherski, A. G. and Kimble, J. (2000a). LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway. Nature 405, 364-368.
53. Petcherski, A. G. and Kimble, J. (2000b). Mastermind is a putative activator for Notch. Curr. Biol. 10, R471-R473.
54. Prokop, A. and Technau, G. M. (1991). The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111, 79-88.
55. Rebay, I., Fehon, R. G. and Artavanis-Tsakonas, S. (1993). Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74, 319-329.
56. Rogulja-Ortmann, A., Luer, K., Seibert, J., Rickert, C. and Technau, G. M. (2007). Programmed cell death in the embryonic central nervous system of Drosophila melanogaster. Development 134, 105-116.
57. Rusconi, J. C., Fink, J. L. and Cagan, R. (2004). klumpfuss regulates cell death in the Drosophila retina. Mech. Dev. 121, 537-546.
58. Schmid, A., Chiba, A. and Doe, C. Q. (1999). Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126, 4653-4689.
59. 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.
60. Schuldt, A. J. and Brand, A. H. (1999). Mastermind acts downstream of notch to specify neuronal cell fates in the Drosophila central nervous system. Dev. Biol. 205, 287-295.
61. Shirasaki, R. and Pfaff, S. L. (2002). Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25, 251-281.
62. Skeath, J. B. and Doe, C. Q. (1998). Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development 125, 1857-1865.
63. Skeath, J. B. and Thor, S. (2003). Genetic control of Drosophila nerve cord development. Curr. Opin. Neurobiol. 13, 8-15.
64. Spana, E. P. and Doe, C. Q. (1996). Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17, 21-26.
65. Struhl, G. and Basler, K. (1993). Organizing activity of Wingless protein in Drosophila. Cell 72, 527-540. (Pubitemid 23077741)
66. Struhl, G., Fitzgerald, K. and Greenwald, I. (1993). Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74, 331-345.
67. Svaren, J., Sevetson, B. R., Apel, E. D., Zimonjic, D. B., Popescu, N. C. and Milbrandt, J. (1996). NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol. Cell. Biol. 16, 3545-3553.
68. Terhzaz, S., O'Connell, F. C., Pollock, V. P., Kean, L., Davies, S. A., Veenstra, J. A. and Dow, J. A. (1999). Isolation and characterization of a leucokinin-like peptide of Drosophila melanogaster. J. Exp. Biol. 202, 3667-3676.
69. Terriente, J., Magarinos, M. and Diaz-Benjumea, F. J. (2007). Nab controls the activity of the zinc-finger transcription factors Squeeze and Rotund in Drosophila development. Development 134, 1845-1852.
70. Thor, S. (2008). Cell specification in the nervous system: an outlook from the Drosophila peptidergic FMRFamide Tv neuron. In Encyclopedia of Neuroscience (ed. L. R. Squire). Oxford, UK: Academic Press.
71. Tran, K. T. and Doe, C. (2008). Pdm and Castor close successive temporal identity windows in the NB3-1 lineage. Development 135, 3491-3499.
72. Tsuji, T., Hasegawa, E. and Isshiki, T. (2008). Neuroblast entry into quiescence is regulated intrinsically by the combined action of spatial Hox proteins and temporal identity factors. Development 135, 3859-3869.
73. Udolph, G., Prokop, A., Bossing, T. and Technau, G. M. (1993). A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants. Development 118, 765-775.
74. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steller, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
75. Wildonger, J., Sosinsky, A., Honig, B. and Mann, R. S. (2005). Lozenge directly activates argos and klumpfuss to regulate programmed cell death. Genes Dev. 19, 1034-1039.
76. Yang, X., Bahri, S., Klein, T. and Chia, W. (1997). Klumpfuss, a putative Drosophila zinc finger transcription factor, acts to differentiate between the identities of two secondary precursor cells within one neuroblast lineage. Genes Dev. 11, 1396-1408.