Home LiteratureArticle Details
PMID: 8227150 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Accumulation of actin in subsets of pioneer growth cone filopodia in response to neural and epithelial guidance cues in situ.

The Journal of cell biology ·Vol. 123 ·No. 4 ·1993-11-00 ·Pages 935-48

O'Connor TP, Bentley D

Abstract

Directed outgrowth of neural processes must involve transmission of signals from the tips of filopodia to the central region of the growth cone. Here, we report on the distribution and dynamics of one possible element in this process, actin, in live growth cones which are reorienting in response to in situ guidance cues. In grasshopper embryonic limbs, pioneer growth cones respond to at least three types of guidance cues: a limb axis cue, intermediate target cells, and a circumferential band of epithelial cells. With time-lapse imaging of intracellularly injected rhodamine-phalloidin and rhodamine-actin, we monitored the distribution of actin during growth cone responses to these cues. In distal limb regions, accumulation of actin in filopodia and growth cone branches accompanies continued growth, while reduction of actin accompanies withdrawal. Where growth cones are reorienting to intermediate target cells, or along the circumferential epithelial band, actin selectively accumulates in the proximal regions of those filopodia that have contacted target cells or are extending along the band. Actin accumulations can be retrogradely transported along filopodia, and can extend into the central region of the growth cone. These results suggest that regulation and translocation of actin may be a significant element in growth cone steering.

MeSH Terms
Actins/metabolism Animals Axons/metabolism Epithelium/growth & development Femur/innervation Grasshoppers Larva Microscopy, Fluorescence Neurons/physiology Phalloidine Rabbits Rhodamines Signal Transduction
Chemicals
Actins Rhodamines Phalloidine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
O'Connor T P
Department of Molecular and Cell Biology, University of California, Berkeley 94720.
Bentley D
References (66)
66 references, click to expand
  1. Cytoskeletal dynamics and nerve growth.
    Neuron. 1988 Nov;1(9):761-72 PMID: 3078414
  2. Roles of actin filaments and three second-messenger systems in short-term regulation of chick dorsal root ganglion neurite outgrowth.
    Cell Motil Cytoskeleton. 1991;20(1):7-29 PMID: 1661642
  3. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone.
    J Cell Biol. 1988 Oct;107(4):1505-16 PMID: 3170637
  4. Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper.
    Cell. 1987 Mar 13;48(5):745-55 PMID: 3545496
  5. Mechanotransduction across the cell surface and through the cytoskeleton.
    Science. 1993 May 21;260(5111):1124-7 PMID: 7684161
  6. Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments.
    Biochemistry. 1991 Feb 19;30(7):1973-80 PMID: 1899622
  7. A role for proteoglycans in the guidance of a subset of pioneer axons in cultured embryos of the cockroach.
    Neuron. 1992 Apr;8(4):701-14 PMID: 1567620
  8. Expression of epithelial alkaline phosphatase in segmentally iterated bands during grasshopper limb morphogenesis.
    Development. 1993 Jun;118(2):651-63 PMID: 8223284
  9. Protein kinase C is involved in laminin stimulation of neurite outgrowth.
    Neuron. 1989 Sep;3(3):287-97 PMID: 2561968
  10. Direct proof that the primary site of action of cytochalasin on cell motility processes is actin.
    J Cell Biol. 1992 Feb;116(4):933-41 PMID: 1734024
  11. The organization of F-actin and microtubules in growth cones exposed to a brain-derived collapsing factor.
    J Cell Biol. 1993 May;121(4):867-78 PMID: 8491778
  12. Molecular links between the cytoskeleton and membranes.
    Curr Opin Cell Biol. 1991 Feb;3(1):120-6 PMID: 1854476
  13. The organization of myosin and actin in rapid frozen nerve growth cones.
    J Cell Biol. 1989 Jan;108(1):95-109 PMID: 2642912
  14. Fasciclin IV: sequence, expression, and function during growth cone guidance in the grasshopper embryo.
    Neuron. 1992 Nov;9(5):831-45 PMID: 1418998
  15. Regulation of neuronal growth cone filopodia by intracellular calcium.
    J Neurosci. 1992 Aug;12(8):3175-86 PMID: 1494951
  16. The nucleation-release model of actin filament dynamics in cell motility.
    Trends Cell Biol. 1992 Aug;2(8):219-22 PMID: 14731477
  17. Calcium influx into neurons can solely account for cell contact-dependent neurite outgrowth stimulated by transfected L1.
    J Cell Biol. 1992 Nov;119(4):883-92 PMID: 1429842
  18. Evidence for microtubule capture by filopodial actin filaments in growth cones.
    Neuroreport. 1991 Oct;2(10):573-6 PMID: 1756237
  19. Inhibition of actin filament depolymerization by the Dictyostelium 30,000-D actin-bundling protein.
    J Cell Biol. 1992 Nov;119(3):559-67 PMID: 1328254
  20. Differences in the organization of actin in the growth cones compared with the neurites of cultured neurons from chick embryos.
    J Cell Biol. 1983 Oct;97(4):963-73 PMID: 6352712
  21. Sensitivity of neurite outgrowth to microfilament disruption varies with adhesion molecule substrate.
    J Neurobiol. 1993 Mar;24(3):344-55 PMID: 8492111
  22. The role of actin polymerization in cell motility.
    Annu Rev Physiol. 1991;53:585-605 PMID: 2042972
  23. Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos.
    Proc Natl Acad Sci U S A. 1982 Apr;79(8):2700-4 PMID: 6806816
  24. On the crawling of animal cells.
    Science. 1993 May 21;260(5111):1086-94 PMID: 8493552
  25. A sensory role for neuronal growth cone filopodia.
    Nature. 1993 Feb 25;361(6414):721-4 PMID: 8441465
  26. Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity.
    J Cell Biol. 1992 Dec;119(5):1219-43 PMID: 1447299
  27. Pioneer growth cone adhesion in vivo to boundary cells and neurons after enzymatic removal of basal lamina in grasshopper embryos.
    J Neurosci. 1989 Aug;9(8):2687-96 PMID: 2671293
  28. Laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons.
    Nature. 1990 Dec 6;348(6301):548-50 PMID: 2247163
  29. Molecular gradients along the proximal-distal axis of embryonic insect legs: possible guidance cues of pioneer axon growth.
    Development. 1992 Oct;116(2):467-79 PMID: 1286619
  30. Novel form of growth cone motility involving site-directed actin filament assembly.
    Nature. 1992 Jun 11;357(6378):515-8 PMID: 1608453
  31. Pioneer growth cone steering along a series of neuronal and non-neuronal cues of different affinities.
    J Neurosci. 1986 Jun;6(6):1781-95 PMID: 3712010
  32. Comparison of actin and cell surface dynamics in motile fibroblasts.
    J Cell Biol. 1992 Oct;119(2):367-77 PMID: 1400580
  33. Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment.
    Nature. 1986 Oct 23-29;323(6090):712-5 PMID: 3773996
  34. Purification of muscle actin.
    Methods Enzymol. 1982;85 Pt B:164-81 PMID: 7121269
  35. Local increases in intracellular calcium elicit local filopodial responses in Helisoma neuronal growth cones.
    Neuron. 1992 Sep;9(3):405-16 PMID: 1524824
  36. Growth cone dynamics during the migration of an identified commissural growth cone.
    J Neurosci. 1993 Jan;13(1):127-43 PMID: 8423468
  37. Disruption of pioneer growth cone guidance in vivo by removal of glycosyl-phosphatidylinositol-anchored cell surface proteins.
    Development. 1992 Feb;114(2):507-19 PMID: 1317292
  38. Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting.
    J Cell Biol. 1990 May;110(5):1825-32 PMID: 2335571
  39. Microtubule behavior during guidance of pioneer neuron growth cones in situ.
    J Cell Biol. 1991 Oct;115(2):381-95 PMID: 1918146
  40. Neuronal cytomechanics: the actin-based motility of growth cones.
    Science. 1988 Nov 4;242(4879):708-15 PMID: 3055292
  41. Cytoskeletal remodeling during growth cone-target interactions.
    J Cell Biol. 1993 Jun;121(6):1369-83 PMID: 8509456
  42. Release of myosin II from the membrane-cytoskeleton of Dictyostelium discoideum mediated by heavy-chain phosphorylation at the foci within the cortical actin network.
    J Cell Biol. 1992 Jun;117(6):1231-9 PMID: 1607385
  43. Neural cell adhesion molecules influence second messenger systems.
    Neuron. 1989 Jul;3(1):13-20 PMID: 2559759
  44. Pioneer growth cone steering decisions mediated by single filopodial contacts in situ.
    J Neurosci. 1990 Dec;10(12):3935-46 PMID: 2269892
  45. Behaviour of microtubules and actin filaments in living Drosophila embryos.
    Development. 1988 Aug;103(4):675-86 PMID: 3248521
  46. Pioneer neuron pathfinding from normal and ectopic locations in vivo after removal of the basal lamina.
    Neuron. 1989 Oct;3(4):427-39 PMID: 2642004
  47. Position-specific expression of the annulin protein during grasshopper embryogenesis.
    Dev Biol. 1992 Nov;154(1):129-42 PMID: 1426622
  48. Pioneer neurones use basal lamina as a substratum for outgrowth in the embryonic grasshopper limb.
    Development. 1988 Dec;104(4):601-8 PMID: 3268405
  49. Actin dynamics in growth cones.
    J Neurosci. 1991 Jul;11(7):1918-29 PMID: 1712377
  50. A cytomechanical investigation of neurite growth on different culture surfaces.
    J Cell Biol. 1992 Aug;118(3):655-61 PMID: 1639849
  51. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling.
    J Cell Biol. 1985 Aug;101(2):597-602 PMID: 4040521
  52. Pathfinding by pioneer neurons in isolated, opened and mesoderm-free limb buds of embryonic grasshoppers.
    Dev Biol. 1987 Feb;119(2):466-80 PMID: 3542637
  53. Annulin, a protein expressed at limb segment boundaries in the grasshopper embryo, is homologous to protein cross-linking transglutaminases.
    Dev Biol. 1992 Nov;154(1):143-59 PMID: 1358727
  54. The role of cytoskeleton in organizing growth cones: a microfilament-associated growth cone component depends upon microtubules for its localization.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1621-31 PMID: 2677024
  55. Incorporation and turnover of biotin-labeled actin microinjected into fibroblastic cells: an immunoelectron microscopic study.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1581-95 PMID: 2677022
  56. The submicroscopic properties of cytoplasm as a determinant of cellular function.
    Annu Rev Biophys Biophys Chem. 1988;17:369-96 PMID: 3293592
  57. Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens.
    J Embryol Exp Morphol. 1979 Dec;54:47-74 PMID: 575157
  58. The actin filament severing protein actophorin promotes the formation of rigid bundles of actin filaments crosslinked with alpha-actinin.
    J Cell Biol. 1991 Dec;115(6):1621-8 PMID: 1757466
  59. The cytoskeletons of isolated, neuronal growth cones.
    Neuroscience. 1987 Jun;21(3):977-89 PMID: 2888041
  60. An actin-associated protein present in the microtubule organizing center and the growth cones of PC-12 cells.
    J Neurosci. 1992 Mar;12(3):750-61 PMID: 1372044
  61. Growth cone behavior and production of traction force.
    J Cell Biol. 1990 Nov;111(5 Pt 1):1949-57 PMID: 2229183
  62. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization.
    Nature. 1992 May 21;357(6375):257-60 PMID: 1589024
  63. Lachesin: an immunoglobulin superfamily protein whose expression correlates with neurogenesis in grasshopper embryos.
    Development. 1993 Jun;118(2):509-22 PMID: 8223276
  64. Actin.
    Curr Opin Cell Biol. 1990 Feb;2(1):33-40 PMID: 2183841
  65. Pioneer neurones in an insect embryo.
    Nature. 1976 Mar 4;260(5546):54-6 PMID: 1264194
  66. Polymorphonuclear leukocyte adherence induces actin polymerization by a transduction pathway which differs from that used by chemoattractants.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1561-9 PMID: 2507552
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.123.4.935
Published
1993-11-00
Pages
935-48
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2200150
Subset
IM
Grants
NINDS NIH HHS · NS09074-22 · United States
External Links
PubMed source DOI: 10.1083/jcb.123.4.935 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2