Lineage-associated tracts defining the anatomy of the Drosophila first instar larval brain

Developmental Biology

Volumn 406, Issue 1, 2015, Pages 14-39

  Hartenstein, Volker ^a   Younossi Hartenstein, Amelia ^a   Lovick, Jennifer K ^a   Kong, Angel ^a   Omoto, Jaison J ^a   Ngo, Kathy T ^a   Viktorin, Gudrun ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Brain; Development; Drosophila; Larval; Lineage

Indexed keywords

FRACTALKINE; CELL ADHESION MOLECULE; DROSOPHILA PROTEIN; FASCICLIN II; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; NRG PROTEIN, DROSOPHILA; NRT PROTEIN, DROSOPHILA;

ANIMAL EXPERIMENT; ANTENNA; ARCUATE FASCICULUS; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DENDRITIC CELL; DROSOPHILA; GENE EXPRESSION; LARVAL DEVELOPMENT; LOCOMOTION; NERVE FIBER; NEUROANATOMY; NEUROBLAST; NEUROPIL; NONHUMAN; OPTIC LOBE; PRIORITY JOURNAL; SPINAL CORD; VENTRAL ROOT; ANATOMY AND HISTOLOGY; ANIMAL; AXON; BIOSYNTHESIS; BRAIN; CELL LINEAGE; EMBRYOLOGY; LARVA; METABOLISM; NERVE CELL;

ANIMALS; AXONS; BRAIN; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; CELL LINEAGE; DROSOPHILA; DROSOPHILA PROTEINS; LARVA; MEMBRANE GLYCOPROTEINS; NEURONS; NEUROPIL;

EID: 84942195977     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.06.021     Document Type: Article

References (93)

1. Asburner M., Drosophila: A Laboratory Manual, 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Bayraktar O.A., Boone J.Q., Drummond M.L., Doe C.Q. Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev. 2010, 5:26. 10.1186/1749-8104-5-26.
3. Bello B.C., Izergina N., Caussinus E., Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 2008, 3:5. 10.1186/1749-8104-3-5.
4. Betschinger J., Mechtler K., Knoblich J.A. Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 2006, 124:1241-1253.
5. Bieber A.J., Snow P.M., Hortsch M., Patel N.H., Jacobs J.R., Traquina Z.R., Schilling J., Goodman C.S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 1989, 59:447-460.
6. Birkholz O., Rickert C., Nowak J., CobanI C., Technau G.M. Bridging the gap between postembryonic cell lineages and identified embryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Biol. Open 2015, 4(4):420-434.
7. Boll W., Noll M. The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 2002, 129:5667-5681.
8. Bossing T., Udolph G., Doe C.Q., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 1996, 179:41-64.
9. Brody T., Odenwald W.F. Regulation of temporal identities during Drosophila neuroblast lineage development. Curr. Opin. Cell Biol. 2005, 17:672-675.
10. Caldwell J.C., Miller M.M., Wing S., Soll D.R., Eberl D.F. Dynamic analysis of larval locomotion in Drosophila chordotonal organ mutants. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:16053-16058.
11. Cardona A., Saalfeld S., Arganda I., Pereanu W., Schindelin J., Hartenstein V. Identifying neuronal lineages of Drosophila by sequence analysis of their axon tracts. J. Neurosci. 2010, 30:7538-7553.
12. Cardona A., Saalfeld S., Preibisch S., Schmid B., Cheng A., Pulokas J., Tomancak P., Hartenstein V. An integrated micro- and macroarchitectural analysis of the Drosophila brain by computer-assisted serial electron microscopy. PLoS Biol. 2010, 8:e1000502.
13. Cardona A., Saalfeld S., Schindelin J., Arganda-Carreras I., Preibisch S., Longair M., Tomancak P., Hartenstein V., Douglas R.J. TrakEM2 software for neural circuit reconstruction. PLoS One. 2012, 7:e38011.
14. Chang T., Younossi-Hartenstein A., Hartenstein V. Development of neural lineages derived from the sine oculis positive eye field of Drosophila. Arthropod. Struct. Dev. 2003, 32:303-317.
15. Choi J.C., Park D., Griffith L.C. Electrophysiological and morphological characterization of identified motor neurons in the Drosophila third instar larva central nervous system. J. Neurophysiol. 2004, 91:2353-2365.
16. Colomb J., Grillenzoni N., Ramaekers A., Stocker R.F. Architecture of the primary taste center of Drosophila melanogaster larvae. J. Comp. Neurol. 2007, 502:834-847.
17. Das A., Gupta T., Davla S., Prieto-Godino L.L., Diegelmann S., Reddy O.V., Raghavan K.V., Reichert H., Lovick J., Hartenstein V. Neuroblast lineage-specific origin of the neurons of the Drosophila larval olfactory system. Dev. Biol. 2013, 373:322-337.
18. de la Escalera S., Bockamp E.O., Moya F., Piovant M., Jiménez F. Characterization and gene cloning of neurotactin, a Drosophila transmembrane protein related to cholinesterases. EMBO J. 1990, 9:3593-3601.
19. Dumstrei K., Wang F., Nassif C., Hartenstein V. Early development of the Drosophila brain. V. Pattern of postembryonic neuronal lineages expressing Shg/DE-cadherin. J. Comp. Neurol. 2003, 455:451-462.
20. Friggi-Grelin F., Coulom H., Meller M., Gomez D., Hirsh J., Birman S. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 2003, 54:618-627.
21. Fung S., Wang F., Chase M., Godt D., Hartenstein V. Expression profile of the cadherin family in the developing Drosophila brain. J. Comp. Neurol. 2008, 506:469-488.
22. Gerber B., Stocker R.F. The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem. Senses 2007, 32:65-89.
23. Ghysen A., Dambly-Chaudière C., Jan L.Y., Jan Y.N. Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev. 1993, 7:723-733.
24. Goodman C.S., Doe C.Q. Embryonic development of the Drosophila central nervous system. In the Development of Drosophila melanogaster 1993, 941-1012. Cold Spring Harbor: Cold Spring Harbor Press. M. Bate, A. Martinez-Arias (Eds.).
25. Grenningloh G., Rehm E.J., Goodman C.S. Genetic analysis of growth-cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 1991, 67:45-57.
26. Hartenstein V. Development of the Drosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways, and sensilla differentiation. Development 1988, 102:869-886.
27. Hartenstein V., Spindler S., Pereanu W., Fung S. The development of the Drosophila larval brain. Adv. Exp. Med Biol. 2008, 628:1-31.
28. Hayashi S., Ito K., Sado Y., Taniguchi M., Akimoto A., Takeuchi H., Aigaki T., Matsuzaki F., Nakagoshi H., Tanimura T., Ueda R., Uemura T., Yoshihara M., Goto S. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 2002, 34:58-61.
29. Hortsch M., Patel N.H., Bieber A.J., Traquina Z.R., Goodman C.S. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 1990, 110:1327-1340.
30. Ito K., Hotta Y. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev. Biol. 1992, 149:134-148.
31. Ito M., Masuda N., Shinomiya K., Endo K., Ito K. Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr. Biol. 2013, 23:644-655.
32. Ito K., Shinomiya K., Ito M., Armstrong J.D., Boyan G., Hartenstein V., Harzsch S., Heisenberg M., Homberg U., Jenett A., Keshishian H., Restifo L.L., Rössler W., Simpson J.H., Strausfeld N.J., Strauss R., Vosshall L.B. A systematic nomenclature for the insect brain. Neuron 2014, 81:755-765.
33. Jenett A., Rubin G.M., Ngo T.T., Shepherd D., Murphy C., Dionne H., Pfeiffer B.D., Cavallaro A., Hall D., Jeter J., Iyer N., Fetter D., Hausenfluck J.H., Peng H., Trautman E.T., Svirskas R.R., Myers E.W., Iwinski Z.R., Aso Y., DePasquale G.M., Enos A., Hulamm P., Lam S.C., Li H.H., Laverty T.R., Long F., Qu L., Murphy S.D., Rokicki K., Safford T., Shaw K., Simpson J.H., Sowell A., Tae S., Yu Y., Zugates C.T. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2012, 2:991-1001.
34. Johansen J., Halpern M.E., Keshishian H. Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci. 1989, 9:4318-4332.
35. Kaneko M., Hall J.C. Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J. Comp. Neurol 2000, 422:66-94.
36. Kim M.D., Wen Y., Jan Y.N. Patterning and organization of motor neuron dendrites in the Drosophila larva. Dev. Biol. 2009, 336:213-221.
37. Kohsaka H., Okusawa S., Itakura Y., Fushiki A., Nose A. Development of larval motor circuits in Drosophila. Dev. Growth Differ. 2012, 54:408-419.
38. Kuert P.A., Bello B.C., Reichert H. The labial gene is required to terminate proliferation of identified neuroblasts in postembryonic development of the Drosophila brain. Biol. Open. 2012, 1:1006-1015.
39. Kuert P.A., Hartenstein V., Bello B.C., Lovick J.K., Reichert H. Neuroblast lineage identification and lineage-specific Hox gene action during postembryonic development of the subesophageal ganglion in the Drosophila central brain. Dev. Biol. 2014, 390:102-115.
40. Kumar A., Fung S., Lichtneckert R., Reichert H., Hartenstein V. Arborization pattern of engrailed-positive neural lineages reveal neuromere boundaries in the Drosophila brain neuropil. J. Comp. Neurol. 2009, 517:87-104.
41. Kwon J.Y., Dahanukar A., Weiss L.A., Carlson J.R. Molecular and cellular organization of the taste system in the Drosophila larva. J. Neurosci. 2011, 31:15300-15309.
42. Kunz T., Kraft K.F., Technau G.M., Urbach R. Origin of Drosophila mushroom body neuroblasts and generation of divergent embryonic lineages. Development 2012, 139:2510-2522.
43. Lai S.L., Awasaki T., Ito K., Lee T. Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 2008, 135:2883-2893.
44. Laissue P.P., Vosshall L.B. The olfactory sensory map in Drosophila. Adv. Exp. Med. Biol. 2008, 628:102-114.
45. Landgraf M., Jeffrey V., Fujioka M., Jaynes J.B., Bate M. Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila. PLoS Biol. 2003, 1:E41.
46. Landgraf M., Sánchez-Soriano N., Technau G.M., Urban J., Prokop A. Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites. Dev. Biol. 2003, 260:207-225.
47. Larsen C., Shy D., Spindler S., Fung S., Younossi-Hartenstein A., Hartenstein V. Patterns of growth, axonal extension and axonal arborization of neuronal lineages in the developing Drosophila brain. Dev. Biol. 2009, 335:289-304.
48. Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999, 126:4065-4076.
49. Liu L., Yermolaieva O., Johnson W.A., Abboud F.M., Welsh M.J. Identification and function of thermosensory neurons in Drosophila larvae. Nat. Neurosci. 2003, 6:267-273.
50. Lichtneckert R., Bello B., Reichert H. Cell lineage-specific expression and function of the empty spiracles gene in adult brain development of Drosophila melanogaster. Development 2007, 134:1291-1300.
51. Lovick J.K., Ngo K.T., Omoto J.J., Wong D.C., Nguyen J.D., Hartenstein V. Postembryonic lineages of the Drosophila brain: I. Development of the lineage-associated fiber tracts. Dev. Biol. 2013, 384:228-257.
52. Lovick J.K., Kong A., Omoto J.J., Ngo K.T., Younossi-Hartenstein A., Hartenstein V., 2015. Patterns of growth and tract formation during the early development of secondary lineages in the Drosophila larval brain, Devel Neurobio. http://dx.doi.org/10.1002/dneu.22325.
53. Masuda-Nakagawa L.M., Tanaka N.K., O'Kane C.J. Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19027-19032.
54. Masuda-Nakagawa L.M., Gendre N., O'Kane C.J., Stocker R.F. Localized olfactory representation in mushroom bodies of Drosophila larvae. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:10314-10319.
55. Milyaev N., Osumi-Sutherland D., Reeve S., Burton N., Baldock R.A., Armstrong J.D. The virtual fly brain browser and query interface. Bioinformatics 2012, 28:411-415.
56. Minocha, S., 2010. A Role of Pox Neuro in the Developing Drosophila Brain: Determination of Large-Field Neurons Essential for Ellipsoid Body Formation and of Ventral Projection Neurons (Doctoral dissertation). Retrieved from Zurich Open Repository and Archive.
57. Nassif C., Noveen A., Hartenstein V. Embryonic development of the Drosophila brain I. The pattern of pioneer tracts. J. Comp. Neurol. 1998, 402:10-31.
58. Nassif C., Noveen A., Hartenstein V. Early development of the Drosophila brain III. The pattern of neuropile founder tracts during the larval period. J. Comp. Neurol. 2003, 455:417-434.
59. Noveen A., Daniel A., Hartenstein V. The role of eyeless in the embryonic development of the Drosophila mushroom body. Development 2000, 127:3475-3488.
60. Pearson B.J., Doe C.Q. Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol. 2004, 20:619-647.
61. Pereanu W., Hartenstein V. Neural lineages of the Drosophila brain: a 3D digital atlas of the pattern of lineage location and projection at the late larval stage. J. Neurosci. 2006, 26:5534-5553.
62. Pereanu W., Kumar A., Jenett A., Reichert H., Hartenstein V. Development-based compartmentalization of the Drosophila central brain. J. Comp. Neurol. 2010, 518:2996-3023.
63. Power M.E. The thoraco-abdominal nervous system of an adult insect Drosophila melanogaster. J. Comp. Neurol. 1948, 88:347-409.
64. Python F., Stocker R.F. Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 2002, 445:374-387.
65. Rajashekhar K.P., Singh R.N. Neuroarchitecture of the tritocerebrum of Drosophila melanogaster. J. Comp. Neurol. 1994, 349:633-645.
66. Ramaekers A., Magnenat E., Marin E.C., Gendre N., Jefferis G.S., Luo L., Stocker R.F. Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 2005, 15:982-992.
67. Riebli N., Viktorin G., Reichert H. Early-born neurons in type II neuroblast lineages establish a larval primordium and integrate into adult circuitry during central complex development in Drosophila. Neural Dev. 2013, 8:6. 10.1186/1749-8104-8-6.
68. Rusan N.M., Peifer M. A role for novel centrosome cycle in asymmetric cell division. J. Cell Biol. 2007, 177:13-20.
69. Siebert M., Banovic D., Goellner B., Aberle H. Drosophila motor axons recognize and follow a Sidestep-labeled substrate pathway to reach their target fields. Genes Dev 2009, 23:1052-1062.
70. Selcho M., Pauls D., Han K.A., Stocker R.F., Thum A.S. The role of dopamine in Drosophila larval classical olfactory conditioning. PLoS One 2009, 4:e5897.
71. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
72. Schleyer M., Saumweber T., Nahrendorf W., Fischer B., von Alpen D., Pauls D., Thum A., Gerber B. A behavior-based circuit model of how outcome expectations organize learned behavior in larval Drosophila. Learn. Mem. 2011, 18:639-653.
73. Schmidt H., Rickert C., Bossing T., Vef O., Urban J., Technau G.M. Dev Biol. 1997, 189:186-204.
74. Schrader S., Merritt D.J. Central projections of Drosophila sensory neurons in the transition from embryo to larva. J. Comp. Neurol. 2000, 425:34-44.
75. Sink H., Whitington P.M. Early ablation of target muscles modulates the arborisation pattern of an identified embryonic Drosophila motor axon. Development 1991, 113:701-707.
76. Spindler S.R., Hartenstein V. The Drosophila neural lineages: a model system to study brain development and circuitry. Dev. Genes Evol. 2010, 220:1-10.
77. Spindler S.R., Hartenstein V. Bazooka mediates secondary axon morphology in Drosophila brain lineages. Neural Dev. 2011, 6:16. 10.1186/1749-8104-6-16.
78. Sprecher S., Reichert H., Hartenstein V. Gene expression patterns in primary neuronal clusters of the Drosophila embryonic brain. Gene Expr. Patterns 2007, 7:584-595.
79. Sprecher S.G., Cardona A., Hartenstein V. The Drosophila larval visual system: high-resolution analysis of a simple visual neuropil. Dev. Biol. 2011, 358:33-43.
80. Stocker R.F., Heimbeck G., Gendre N., de Belle J.S. Neuroblast ablation in Drosophila P[Gal4] lines reveals origins of olfactory interneurons. J. Neurobiol. 1997, 32:443-456.
81. Tabata T., Schwartz C., Gustavson E., Ali Z., Kornberg T.B. Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development 1995, 121:3359-3369.
82. Truman J.W., Bate M. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 1988, 125:145-157.
83. Truman J.W., Schuppe H., Shepherd D., Williams D.W. Developmental architecture of adult-specific lineages in the ventral CNS of Drosophila. Development 2004, 131:5167-5184.
84. Tyrer N.M., Gregory G.E. A guide to the neuroanatomy of locust suboesophageal and thoracic ganglia. Philos. Trans. R. Soc. Lond. B 1982, 297:91-123.
85. Urbach R., Technau G.M. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 2003, 130:3621-3637.
86. Urbach R., Technau G.M. Neuroblast formation and patterning during early brain development in Drosophila. Bioessays 2004, 26:739-751.
87. Vactor D.V., Sink H., Fambrough D., Tsoo R., Goodman C.S. Genes that control neuromuscular specificity in Drosophila. Cell 1993, 73:1137-1153.
88. Wong D.C., Lovick J.K., Ngo K.T., Borisuthirattana W., Omoto J.J., Hartenstein V. Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones. Dev. Biol. 2013, 384:258-289.
89. Yang J.S., Awasaki T., Yu H.H., He Y., Ding P., Kao J.C., Lee T. Diverse neuronal lineages make stereotyped contributions to the Drosophila locomotor control center, the central complex. J. Comp. Neurol. 2013, 521:2645-2662. (Spc1).
90. Younossi-Hartenstein A., Nassif C., Hartenstein V. Early neurogenesis of the Drosophila brain. J. Comp. Neurol. 1996, 370:313-329.
91. Younossi-Hartenstein A., Salvaterra P., Hartenstein V. Early development of the Drosophila brain IV. Larval neuropile compartments defined by glial septa. J. Comp. Neurol. 2003, 455:435-450.
92. Younossi-Hartenstein A., Shy D., Hartenstein V. The embryonic formation of the Drosophila brain neuropile. J. Comp. Neurol. 2006, 497:981-998.
93. Yu H.H., Awasaki T., Schroeder M.D., Long F., Yang J.S., He Y., Ding P., Kao J.C., Wu G.Y., Peng H., Myers G., Lee T. Clonal development and organization of the adult Drosophila central brain. Curr. Biol. 2013, 23:633-643.