Cited by 33Axon Guidance and Neuronal SignalingNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

Ultrastructural networks in growth cones and neurites of cultured central nervous system neurons.

Open access
Tsui, H C, Ris, H, Klein, W L·1983·Proceedings of the National Academy of Sciences

Abstract

We have examined growth cones and neurites of cultured central nervous system neurons by high-voltage electron microscopy. Embryonic chicken retina cells were cultured on polylysine-treated and Formvar-coated gold grids for 2-6 days, fixed, and critical point dried. Growth cones and neurites were examined as unembedded whole mounts. Three-dimensional images from stereo-pair electron micrographs of these regions showed a high degree of ultrastructural articulation, with distinct, non-tapering filaments (5-9 nm in diameter) joining both cytoskeletal and membranous components. In the central regions of growth cones, interconnected structures included microtubules, large membranous sacs (up to 400 nm), and irregular vesicles (25-75 nm). A denser filamentous network was prevalent at the edges of growth cones. This network, which frequently adjoined the surface membrane, linked vesicles of uniform size (35-40 nm). Such vesicles often were seen densely packed in growth cone protrusions that were about the size of small synaptic boutons. Prevalent structural interconnections within growth cones conceivably could play a logistic role in specific membrane assembly, intracellular transport, endocytosis, and secretion. Because such processes are not unique to growth cones, the extensive linkages we have observed may have implications for cytoplasmic structure in general.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1073/pnas.80.18.5779

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Rings of microtubules have been observed in the growth cones of sensory neurons in culture.

    “Rings of microtubules have been observed in the growth cones of sensory neurons in culture (Tsui et al., 1983).”

    From Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture (1986) · cites this paper as Tsui et al., 1983

    The Abstract reports microtubules in the growth cones of cultured embryonic chicken retina neurons. It does not describe rings of microtubules or identify the studied cells as sensory neurons, so those parts of the claim are unsupported by our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 34

  1. Bennett V., Davis J., Fowler W. E. Brain spectrin, a membrane-associated protein related in structure and function to erythrocyte spectrin. Nature. 1982 Sep 9;299(5879):126–131. doi: 10.1038/299126a0. [DOI] [PubMed] [Google Scholar] · DOI
  2. Birks R. I., Mackey M. C., Weldon P. R. Organelle formation from pinocytotic elements in neurites of cultured sympathetic ganglia. J Neurocytol. 1972 Dec;1(4):311–340. doi: 10.1007/BF01102938. [DOI] [PubMed] [Google Scholar] · DOI
  3. Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  4. Bray D., Bunge M. B. Serial analysis of microtubules in cultured rat sensory axons. J Neurocytol. 1981 Aug;10(4):589–605. doi: 10.1007/BF01262592. [DOI] [PubMed] [Google Scholar] · DOI
  5. Bray D. Surface movements during the growth of single explanted neurons. Proc Natl Acad Sci U S A. 1970 Apr;65(4):905–910. doi: 10.1073/pnas.65.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  6. Bunge M. B. Initial endocytosis of perioxidase or ferritin by growth cones of cultured nerve cells. J Neurocytol. 1977 Aug;6(4):407–439. doi: 10.1007/BF01178226. [DOI] [PubMed] [Google Scholar] · DOI
  7. Droz B., Rambourg A., Koenig H. L. The smooth endoplasmic reticulum: structure and role in the renewal of axonal membrane and synaptic vesicles by fast axonal transport. Brain Res. 1975 Jul 25;93(1):1–13. doi: 10.1016/0006-8993(75)90282-6. [DOI] [PubMed] [Google Scholar] · DOI
  8. Ellisman M. H., Porter K. R. Microtrabecular structure of the axoplasmic matrix: visualization of cross-linking structures and their distribution. J Cell Biol. 1980 Nov;87(2 Pt 1):464–479. doi: 10.1083/jcb.87.2.464. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  9. Feldman E. L., Axelrod D., Schwartz M., Heacock A. M., Agranoff B. W. Studies on the localization of newly added membrane in growing neurites. J Neurobiol. 1981 Nov;12(6):591–598. doi: 10.1002/neu.480120607. [DOI] [PubMed] [Google Scholar] · DOI
  10. Frank E., Fischbach G. D. Early events in neuromuscular junction formation in vitro: induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses. J Cell Biol. 1979 Oct;83(1):143–158. doi: 10.1083/jcb.83.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  11. Heuser J. E., Kirschner M. W. Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J Cell Biol. 1980 Jul;86(1):212–234. doi: 10.1083/jcb.86.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  12. Hirokawa N. Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J Cell Biol. 1982 Jul;94(1):129–142. doi: 10.1083/jcb.94.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  13. Kidokoro Y., Yeh E. Initial synaptic transmission at the growth cone in Xenopus nerve-muscle cultures. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6727–6731. doi: 10.1073/pnas.79.21.6727. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  14. Kondo H., Wolosewick J. J., Pappas G. D. The microtrabecular lattice of the adrenal medulla revealed by polyethylene glycol embedding and stereo electron microscopy. J Neurosci. 1982 Jan;2(1):57–65. doi: 10.1523/JNEUROSCI.02-01-00057.1982. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  15. Kuczmarski E. R., Rosenbaum J. L. Studies on the organization and localization of actin and myosin in neurons. J Cell Biol. 1979 Feb;80(2):356–371. doi: 10.1083/jcb.80.2.356. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  16. Lavail J. H., Rapisardi S., Sugino I. K. Evidence against the smooth endoplasmic reticulum as a continuous channel for the retrograde axonal transport of horseradish peroxidase. Brain Res. 1980 Jun 2;191(1):3–20. doi: 10.1016/0006-8993(80)90311-x. [DOI] [PubMed] [Google Scholar] · DOI
  17. Letourneau P. C. Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation. Exp Cell Res. 1979 Nov;124(1):127–138. doi: 10.1016/0014-4827(79)90263-5. [DOI] [PubMed] [Google Scholar] · DOI
  18. Letourneau P. C. Immunocytochemical evidence for colocalization in neurite growth cones of actin and myosin and their relationship to cell--substratum adhesions. Dev Biol. 1981 Jul 15;85(1):113–122. doi: 10.1016/0012-1606(81)90240-2. [DOI] [PubMed] [Google Scholar] · DOI
  19. Levine J., Willard M. Fodrin: axonally transported polypeptides associated with the internal periphery of many cells. J Cell Biol. 1981 Sep;90(3):631–642. doi: 10.1083/jcb.90.3.631. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  20. Maupin-Szamier P., Pollard T. D. Actin filament destruction by osmium tetroxide. J Cell Biol. 1978 Jun;77(3):837–852. doi: 10.1083/jcb.77.3.837. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  21. NAKAI J. Dissociated dorsal root ganglia in tissue culture. Am J Anat. 1956 Jul;99(1):81–129. doi: 10.1002/aja.1000990105. [DOI] [PubMed] [Google Scholar] · DOI
  22. Pfenninger K. H., Maylié-Pfenninger M. F. Lectin labeling of sprouting neurons. II. Relative movement and appearance of glycoconjugates during plasmalemmal expansion. J Cell Biol. 1981 Jun;89(3):547–559. doi: 10.1083/jcb.89.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  23. Puro D. G., De Mello F. G., Nirenberg M. Synapse turnover: the formation and termination of transient synapses. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4977–4981. doi: 10.1073/pnas.74.11.4977. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  24. Rambourg A., Droz B. Smooth endoplasmic reticulum and axonal transport. J Neurochem. 1980 Jul;35(1):16–25. doi: 10.1111/j.1471-4159.1980.tb12484.x. [DOI] [PubMed] [Google Scholar] · DOI
  25. Rees R. P., Reese T. S. New structural features of freeze-substituted neuritic growth cones. Neuroscience. 1981;6(2):247–254. doi: 10.1016/0306-4522(81)90060-9. [DOI] [PubMed] [Google Scholar] · DOI
  26. Shaw G., Osborn M., Weber K. Arrangement of neurofilaments, microtubules and microfilament-associated proteins in cultured dorsal root ganglia cells. Eur J Cell Biol. 1981 Apr;24(1):20–27. [PubMed] [Google Scholar]
  27. Siman R. G., Klein W. L. Differential regulation of muscarinic and nicotinic receptors by cholinergic stimulation in cultured avian retina cells. Brain Res. 1983 Feb 28;262(1):99–108. doi: 10.1016/0006-8993(83)90473-0. [DOI] [PubMed] [Google Scholar] · DOI
  28. Small J. V. Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks. J Cell Biol. 1981 Dec;91(3 Pt 1):695–705. doi: 10.1083/jcb.91.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  29. Tsukita S., Ishikawa H. The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J Cell Biol. 1980 Mar;84(3):513–530. doi: 10.1083/jcb.84.3.513. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  30. Tsukita S., Usukura J., Tsukita S., Ishikawa H. The cytoskeleton in myelinated axons: a freeze-etch replica study. Neuroscience. 1982;7(9):2135–2147. doi: 10.1016/0306-4522(82)90125-7. [DOI] [PubMed] [Google Scholar] · DOI
  31. Wolosewick J. J., Porter K. R. Microtrabecular lattice of the cytoplasmic ground substance. Artifact or reality. J Cell Biol. 1979 Jul;82(1):114–139. doi: 10.1083/jcb.82.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  32. Wolosewick J. J., Porter K. R. Stereo high-voltage electron microscopy of whole cells of the human diploid line, WI-38. Am J Anat. 1976 Nov;147(3):303–323. doi: 10.1002/aja.1001470305. [DOI] [PubMed] [Google Scholar] · DOI
  33. Yamada K. M., Spooner B. S., Wessells N. K. Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol. 1971 Jun;49(3):614–635. doi: 10.1083/jcb.49.3.614. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  34. Yankner B. A., Shooter E. M. The biology and mechanism of action of nerve growth factor. Annu Rev Biochem. 1982;51:845–868. doi: 10.1146/annurev.bi.51.070182.004213. [DOI] [PubMed] [Google Scholar] · DOI

Authors
Tsui, H. C., Ris, H., & Klein, W. L.
Affiliations
Northwestern University (US)
Venue
Proceedings of the National Academy of Sciences
Published
1983-09
Volume
80
Issue
18
Pages
5779-5783
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2035110628
Cited by
33
References
0
Citations by year
2025: 1
FWCI
1.29
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
growth cones, neurites, central nervous system neurons, microtubules, vesicles, cytoskeleton, membrane assembly, intracellular transport, endocytosis, secretion, neuronal ultrastructure
MeSH terms
Animals, Chick Embryo, Cytoskeleton, Microscopy, Electron, Neurons, Retina, Synaptic Vesicles

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review