Drosophila growth cones: A genetically tractable platform for the analysis of axonal growth dynamics

Developmental Neurobiology

Volumn 70, Issue 1, 2010, Pages 58-71

  Sánchez Soriano, Natalia ^a   Gonçalves Pimentel, Catarina ^a,b   Beaven, Robin ^a   Haessler, Ulrike ^a,c   Ofner Ziegenfuss, Lisa ^a,d   Ballestrem, Christoph ^a   Prokop, Andreas ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c EPFL   (Switzerland)

^d MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Axons; Cell culture; Cytoskeleton; Drosophila; Growth cones

Indexed keywords

ACTIN; F ACTIN;

ARTICLE; CELL CULTURE; CELL MOTILITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; GENETIC MANIPULATION; GENETICS; GROWTH CONE; MAMMAL; NERVE FIBER; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; VERTEBRATE;

ACTINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CELL ENLARGEMENT; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; GROWTH CONES; IMMUNOHISTOCHEMISTRY; MICROFILAMENT PROTEINS; MICROTUBULES; NEURONS; PSEUDOPODIA; TIME FACTORS;

EID: 73849088270     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20762     Document Type: Article

References (74)

1. Ahern-Djamali SM, Bachmann C, Hua P, Reddy SK, Kastenmeier AS, Walter U, Hoffmann FM. 1999. Identification of profilin and src homology 3 domains as binding partners for Drosophila enabled. Proc Natl Acad Sci USA 96:4977-4982.
2. Akhmanova A, Steinmetz MO. 2008. Tracking the ends: A dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9:309-322.
3. Araujo SJ, Tear G. 2003. Axon guidance mechanisms and molecules: Lessons from invertebrates. Nat Rev Neurosci 4:910-922.
4. Argiro V, Bunge MB, Johnson MI. 1985. A quantitative study of growth cone filopodial extension. J Neurosci Res 13:149-162.
5. Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS. 2000. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101:703-715.
6. Bentley D, Toroian-Raymond A. 1986. Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323:712-715.
7. + channels: Regulation of the soma-growth cone disparity and the quiescent state in Drosophila neurons. Neuroscience 142:629-644.
8. Bohil AB, Robertson BW, Cheney RE. 2006. Myosin-X is a molecular motor that functions in filopodia formation. Proc Natl Acad Sci USA 103:12411-12416.
9. Bonanomi D, Menegon A, Miccio A, Ferrari G, Corradi A, Kao HT, Benfenati F, Valtorta F. 2005. Phosphorylation of synapsin I by cAMP-dependent protein kinase controls synaptic vesicle dynamics in developing neurons. J Neurosci 25:7299-7308.
10. Bottenberg W, Sánchez-Soriano N, Alves-Silva J, Hahn I, Mende M, Prokop A. 2009. Context-specific requirements of functional domains of the Spectraplakin Short stop in vivo. Mech Dev 126:489-502.
11. Bray D, White JG. 1988. Cortical flow in animal cells. Science 239:883-888.
12. Brown J, Bridgman PC. 2003. Role of myosin II in axon outgrowth. J Histochem Cytochem 51:421-428.
13. Brown MD, Cornejo BJ, Kuhn TB, Bamburg JR. 2000. Cdc42 stimulates neurite outgrowth and formation of growth cone filopodia and lamellipodia. J Neurobiol 43:352-364.
14. Brown ME, Bridgman PC. 2003. Retrograde flow rate is increased in growth cones from myosin IIB knockout mice. J Cell Sci 116:1087-1094.
15. Campos-Ortega JA, Hartenstein V. 1997. The embryonic development of Drosophila melanogaster. Berlin: Springer Verlag, 227 p.
16. Challacombe JF, Snow DM, Letourneau PC. 1996. Actin filament bundles are required for microtubule reorientation during growth cone turning to avoid an inhibitory guidance cue. J Cell Sci 109 (Pt 8):2031-2040.
17. Chien CB, Rosenthal DE, Harris WA, Holt CE. 1993. Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11:237-251.
18. Chuckowree JA, Vickers JC. 2003. Cytoskeletal and morphological alterations underlying axonal sprouting after localized transection of cortical neuron axons in vitro. J Neurosci 23:3715-3725.
19. Conde C, Caceres A. 2009. Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319-332.
20. Delalle I, Pfleger CM, Buff E, Lueras P, Hariharan IK. 2005. Mutations in the Drosophila orthologs of the F-actin capping protein α- and β-subunits cause actin accumulation and subsequent retinal degeneration. Genetics 171:1757-1765.
21. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K. 1999. Reorganisation and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19:8894-8908.
22. Dent EW, Gertler FB. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209-227.
23. Dübendorfer A, Eichenberger-Glinz S. 1980. Development and metamorphosis of larval and adult tissues of Drosophila in vitro. In: Kurstak E, Maramorosch K, Dübendorfer A, Kurstak E, Maramorosch K, editors. Dübendorfer As. Invertebrate systems in vitro. Amsterdam: Elsevier North Holland, pp 169-185.
24. Duffy JB. 2002. GAL4 system in Drosophila: A fly geneticist's Swiss army knife. Genesis 34:1-15.
25. Forni JJ, Romani S, Doherty P, Tear G. 2004. Neuroglian and FasciclinII can promote neurite outgrowth via the FGF receptor Heartless. Mol Cell Neurosci 26:282-291.
26. Gehler S, Gallo G, Veien E, Letourneau PC. 2004. p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. J Neurosci 24:4363-4372.
27. Gertler FB, Comer AR, Juang J-L, Ahern SM, Clark MJ, Liebl EC, Hoffmann FM. 1995. Enabled, a dosage-sensitive suppressor of mutations in the Drosophila Abl tyrosine kinase, encodes an Abl substrate with SH3 domain-binding properties. Genes Dev 9:521-533.
28. 2+ signals. Trends Cell Biol 14:320-330.
29. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. 2003. Signaling at the growth cone: Ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509-563.
30. Hudson AM, Cooley L. 2002. A subset of dynamic actin rearrangements in Drosophila requires the Arp2/3 complex. J Cell Biol 156:677-687.
31. Janody F, Treisman JE. 2006. Actin capping protein α maintains vestigial-expressing cells within the Drosophila wing disc epithelium. Development 133:3349-3357.
32. Kaufmann N, Wills ZP, Van Vactor D. 1998. Drosophila Rac1 controls motor axon guidance. Development 125:453-461.
33. Komarova YA, Vorobjev IA, Borisy GG. 2002. Life cycle of MTs: Persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J Cell Sci 115:3527-3539.
34. Küppers B, Sánchez-Soriano N, Letzkus J, Technau GM, Prokop A. 2003. In developing Drosophila neurones the production of γ-amino butyric acid is tightly regulated downstream of glutamate decarboxylase translation and can be influenced by calcium. J Neurochem 84:939-951.
35. Küppers-Munther B, Letzkus J, Lüer K, Technau G, Schmidt H, Prokop A. 2004. A new culturing strategy optimises Drosophila primary cell cultures for structural and functional analyses. Dev Biol 269:459-478.
36. Lanier LM, Gates MA, Witke W, Menzies AS, Wehman AM, Macklis JD, Kwiatkowski D, Soriano P, Gertler FB. 1999. Mena is required for neurulation and commissure formation. Neuron 22:313-325.
37. Lee AC, Suter DM. 2008. Quantitative analysis of microtubule dynamics during adhesion-mediated growth cone guidance. Dev Neurobiol 68:1363-1377.
38. Lee S, Harris K-L, Whitington PM, Kolodziej PA. 2000. Short stop is allelic to kakapo, and encodes rod-like cytoskeletal-associated proteins required for axon extension. J Neurosci 20:1096-1108.
39. Lee S, Kolodziej PA. 2002. Short stop provides an essential link between F-actin and microtubules during axon extension. Development 129:1195-1204.
40. Letourneau PC, Ressler AH. 1984. Inhibition of neurite initiation and growth by taxol. J Cell Biol 98:1355-1362.
41. Letourneau PC, Shattuck TA, Ressler AH. 1987. "Pull" and "push" in neurite elongation: Observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskel 8:193-209.
42. Lin CH, Espreafico EM, Mooseker MS, Forscher P. 1996. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16:769-782.
43. Lin CH, Forscher P. 1995. Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14:763-771.
44. Liu R, Woolner S, Johndrow JE, Metzger D, Flores A, Parkhurst SM. 2008. Sisyphus, the Drosophila myosin XV homolog, traffics within filopodia transporting key sensory and adhesion cargos. Development 135:53-63.
45. Lowery LA, Van Vactor D. 2009. The trip of the tip: Understanding the growth cone machinery. Nat Rev Mol Cell Biol 10:332-343.
46. Luo L, Liao YJ, Jan LY, Jan YN. 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8:1787-1802.
47. Marsh L, Letourneau PC. 1984. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99:2041-2047.
48. Mattila PK, Lappalainen P. 2008. Filopodia: Molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9:446-454.
49. Matusek T, Gombos R, Szecsenyi A, Sánchez-Soriano N, Czibula A, Pataki C, Gedai A, Prokop A, Rasko I, Mihaly J. 2008. Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci 28:13310-13319.
50. Mlodzik M, Baker NE, Rubin GM. 1990. Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev 4:1848-1861.
51. Morrison EE. 2007. Action and interactions at microtubule ends. Cell Mol Life Sci 64:307-317.
52. Murray MJ, Merritt D, Brand AH, Whitington PM. 1998. In vivo dynamics of axon pathfinding in the Drosophila CNS: A time-lapse study of an identified motorneuron. J Neurobiol 37:607-621.
53. Pak CW, Flynn KC, Bamburg JR. 2008. Actin-binding proteins take the reins in growth cones. Nat Rev Neurosci 9:136-147.
54. Prokop A, Technau GM. 1993. Cell transplantation. In: Hartley D, editor. Hartley Ds. Cellular Interactions in Development: A Practical Approach. London: Oxford University Press, pp 33-57.
55. Prokop A, Uhler J, Roote J, Bate MC. 1998. The kakapo mutation affects terminal arborisation and central dendritic sprouting of Drosophila motorneurons. J Cell Biol 143:1283-1294.
56. Rochlin MW, Itoh K, Adelstein RS, Bridgman PC. 1995. Localization of myosin II A and B isoforms in cultured neurons. J Cell Sci 108 (Pt 12):3661-3670.
57. Röper K, Gregory SL, Brown NH. 2002. The 'Spectraplakins': Cytoskeletal giants with characteristics of both spectrin and plakin families. J Cell Sci 115:4215-4225.
58. Royou A, Sullivan W, Karess R. 2002. Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: Its role in nuclear axial expansion and its regulation by Cdc2 activity. J Cell Biol 158:127-137.
59. Sánchez-Soriano N, Löhr R, Bottenberg W, Haessler U, Kerassoviti A, Knust E, Fiala A, Prokop A. 2005. Are dendrites in Drosophila homologous to vertebrate dendrites? Dev Biol 288:126-138.
60. Sánchez-Soriano N, Prokop A. 2005. The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog FasciclinII. J Neurosci 25:78-87.
61. Sánchez-Soriano N, Tear G, Whitington P, Prokop A. 2007. Drosophila as a genetic and cellular model for studies on axonal growth. Neural Develop 2:9.
62. Sánchez-Soriano N, Travis M, Dajas-Bailador F, Goncalves-Pimentel C, Whitmarsh AJ, Prokop A. 2009. Mouse ACF7 and Drosophila Short stop modulate filopodia formation and microtubule organisation during neuronal growth. J Cell Sci 122:2534-2542.
63. Sasaki Y, Hayashi K, Shirao T, Ishikawa R, Kohama K. 1996. Inhibition by drebrin of the actin-bundling activity of brain fascin, a protein localized in filopodia of growth cones. J Neurochem 66:980-988.
64. Schneider I. 1964. Differentiation of larval Drosophila eyeantennal discs in vitro. J Exp Zool 156:91-104.
65. Svitkina TM, Verkhovsky AB, McQuade KM, Borisy GG. 1997. Analysis of the actin-myosin II system in fish epidermal keratocytes: Mechanism of cell body translocation. J Cell Biol 139:397-415.
66. Takagi Y, Nomizu M, Gullberg D, MacKrell AJ, Keene DR, Yamada Y, Fessler JH. 1996. Conserved neuron promoting activity in Drosophila and vertebrate laminin α1. J Biol Chem 271:18074-18081.
67. Teng J, Takei Y, Harada A, Nakata T, Chen J, Hirokawa N. 2001. Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155:65-76.
68. Theodosiou NA, Xu T. 1998. Use of FLP/FRT system to study Drosophila development. Methods 14:355-365.
69. 2+-calmodulin signaling in Drosophila growth cones leads to stalls in axon extension and errors in axon guidance. Neuron 14:43-56.
70. Verheyen EM, Cooley L. 1994. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120:717-728.
71. Verkhovsky AB, Svitkina TM, Borisy GG. 1995. Myosin II filament assemblies in the active lamella of fibroblasts: Their morphogenesis and role in the formation of actin filament bundles. J Cell Biol 131:989-1002.
72. Wills Z, Marr L, Zinn K, Goodman CS, Van Vactor D. 1999. Profilin and the Abl tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron 22:291-299.
73. Yao W-D, Rusch J, Poo M-m, Wu C-F. 2000. Spontaneous acetylcholine secretion from developing growth cones of Drosophila central neurons in culture: Effects of cAMPpathway mutations. J Neurosci 20:2626-2637.
74. Zanet J, Stramer B, Millard T, Martin P, Payre F, Plaza S. 2009. Fascin is required for blood cell migration during Drosophila embryogenesis. Development 136:2557-2565.