The DOI matches its Crossref record; 40 of the 40 references it cites were found in a registry or an index.
Turning of nerve growth cones induced by neurotransmitters
Abstract
Pathfinding by growing nerve processes in the developing nervous system depends on the turning response of the growing tip, the growth cone, to extracellular guidance cues. There is evidence in vivo and in cell culture that some growth cones exhibit chemotropic behaviour, but the identity of endogenous chemoattractants remains elusive. Neurotransmitters appear early in the developing embryo and may have morphogenic roles in development. In cell culture a number of neurotransmitters were found to induce growth inhibition or retraction of neurites. Here we report positive turning responses of the nerve growth cone in a defined extracellular gradient of the neurotransmitter acetylcholine (ACh). The growth cone response depends on the activation of neuronal nicotinic ACh receptors, requires the presence of extracellular Ca2+, and appears to be mediated by Ca(2+)-calmodulin-dependent protein kinase II. Fluorescence imaging of cytosolic Ca2+ concentration ([Ca2+]i) at the growth cone showed a small but significant evaluation of [Ca2+]i within minutes of the onset of ACh application and before the turning of the growth cone. These findings suggest that neurotransmitters may serve as specific chemoattractants for growth cone guidance and that cytosolic Ca2+ may act as a second messenger in the cytoplasm of the growth cone to initiate the turning response.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“But even before the cholinergic projections arrive in the cortical areas, the nicotinic and muscarinic receptors are expressed on neural progenitors playing a role in proliferation/differentiation and axonal guidance events [214–217].”
From Development of prefrontal cortex (2022) · cites this paper as [217]
Citations
Cites
A new generation of Ca2+ indicators with greatly improved fluorescence properties.
Grynkiewicz, G., Poenie, M., & Tsien, R. Y. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83641-4 · Cited by 21,722
Banker, G. A., & Goslin, K. (1998) · Cited by 1,290
Chemotropic guidance of developing axons in the mammalian central nervous system
Tessier‐Lavigne, M., Placzek, M., Lumsden, A. G. S., Dodd, J., & Jessell, T. M. (1988) · Nature · doi:10.1038/336775a0 · Cited by 696
Principles of neural development
(1985) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(85)90519-5 · Cited by 644
Tokumitsu, H., Chijiwa, T., Hagiwara, M., Mizutani, A., Terasawa, M., & Hidaka, H. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)39565-1 · Cited by 624
Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons
Mattson, M. P., Dou, P., & Kater, S. B. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-06-02087.1988 · Cited by 557
Haydon, P. G., McCobb, D. P., & Kater, S. B. (1984) · Science · doi:10.1126/science.6093252 · Cited by 545
Neuronal Chemotaxis: Chick Dorsal-Root Axons Turn Toward High Concentrations of Nerve Growth Factor
Gundersen, R. W., & Barrett, J. N. (1979) · Science · doi:10.1126/science.493992 · Cited by 520
Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors
Vernino, S. A., Amador, M., Luetje, C. W., Patrick, J., & Dani, J. A. (1992) · Neuron · doi:10.1016/0896-6273(92)90114-s · Cited by 463
Calcium regulation of neurite elongation and growth cone motility
Mattson, M. P., & Kater, S. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-12-04034.1987 · Cited by 421
Lumsden, A. G. S., & Davies, A. M. (1983) · Nature · doi:10.1038/306786a0 · Cited by 356
Asymmetric modulation of cytosolic cAMP activity induces growth cone turning
Lohof, A. M., Quillan, M., Dan, Y., & Poo, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-04-01253.1992 · Cited by 352
Self-citationEffects of innervation on the distribution of acetylcholine receptors on cultured muscle cells.
Anderson, M. J., Cohen, M. W., & Zorychta, E. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp011879 · Cited by 339
Lankford, K. L., DeMello, F. G., & Klein, W. L. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.8.2839 · Cited by 307
Electrically and chemically mediated increases in intracellular calcium in neuronal growth cones
Cohan, C. S., Connor, J. A., & Kater, S. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-11-03588.1987 · Cited by 286
Self-citationChemotactic response of nerve fiber elongation to nerve growth factor
Letourneau, P. C. (1978) · Developmental Biology · doi:10.1016/0012-1606(78)90283-x · Cited by 277
Target Control of Collateral Extension and Directional Axon Growth in the Mammalian Brain
Heffner, C. D., Lumsden, A. G. S., & O’Leary, D. D. M. (1990) · Science · doi:10.1126/science.2294603 · Cited by 272
Nicotinic receptors that bind α-bungarotoxin on neurons raise intracellular free ca2+
Vijayaraghavan, S., Pugh, P. C., Zhang, Z., Rathouz, M. M., & Berg, D. K. (1992) · Neuron · doi:10.1016/0896-6273(92)90301-s · Cited by 260
Neurotransmitters as morphogens
Lauder, J. M. (1988) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60516-6 · Cited by 257
The development of the action potential mechanism of amphibian neurons isolated in culture.
Spitzer, N. C., & Lamborghini, J. E. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.5.1641 · Cited by 253
Nicotinic Antagonists Enhance Process Outgrowth by Rat Retinal Ganglion Cells in Culture
Lipton, S. A., Frosch, M. P., Phillips, M. D., Tauck, D. L., & Aizenman, E. (1988) · Science · doi:10.1126/science.3344435 · Cited by 225
Molecular bases of neural development
Gall, W. E., Cowan, W. M., & Edelman, G. M. (1985) · Medical Entomology and Zoology · Cited by 207
Xie, Z. P., & Poo, M. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.18.7069 · Cited by 188
Self-citationBedlack, R. S., Wei, M.-D., & Loew, L. M. (1992) · Neuron · doi:10.1016/0896-6273(92)90178-g · Cited by 184
Regulation of neuronal growth cone filopodia by intracellular calcium
Rehder, V., & Kater, S. B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-08-03175.1992 · Cited by 177
Dopamine and serotonin inhibition of neurite elongation of different identified neurons
McCobb, D. P., Haydon, P. G., & Kater, S. B. (1988) · Journal of Neuroscience Research · doi:10.1002/jnr.490190104 · Cited by 173
Mg, M. C., Js, C., & Levi‐Montalcini, R. (1978) · PubMed · Cited by 171
Studies of nerve-muscle interactions in Xenopus cell culture: analysis of early synaptic currents
Evers, J., Laser, M., Sun, Y., Xie, Z., & Poo, M. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01523.1989 · Cited by 161
Self-citationPerturbation of the direction of neurite growth by pulsed and focal electric fields
Patel, N. B., & Poo, M. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-12-02939.1984 · Cited by 146
Self-citationInteractive effects of serotonin and acetylcholine on neurite elongation
McCobb, D. P., Cohan, C. S., Connor, J. A., & Kater, S. B. (1988) · Neuron · doi:10.1016/0896-6273(88)90187-0 · Cited by 141
Self-citationGrowth Cone Motility And Guidance
Bray, D., & Hollenbeck, P. J. (1988) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.04.110188.000355 · Cited by 136
Ito, I., Hidaka, H., & Sugiyama, H. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90663-e · Cited by 124
Davenport, R. W., & Kater, S. B. (1992) · Neuron · doi:10.1016/0896-6273(92)90179-h · Cited by 116
Bixby, J. L., & Spitzer, N. C. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90065-4 · Cited by 100
Connor, J. A. (1993) · Cell Calcium · doi:10.1016/0143-4160(93)90066-f · Cited by 96
Self-citationYaginuma, H., & Oppenheim, R. W. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-08-02598.1991 · Cited by 54
Knoll, G., Grässle, A., Braun, C., Probst, W., Höhne-Zell, B., & Plattner, H. (1993) · Cell Calcium · doi:10.1016/0143-4160(93)90065-e · Cited by 52
Principles of neural development
Coleman, J. R. (1986) · Brain Research Bulletin · doi:10.1016/0361-9230(86)90047-x · Cited by 47
Myoblasts and myoblast‐conditioned medium attract the earliest spinal neurites from frog embryos.
McCaig, C. D. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016104 · Cited by 43
Axonal guidance and the formation of neuronal circuits
Landmesser, L. T. (1986) · Trends in Neurosciences · doi:10.1016/0166-2236(86)90156-6 · Cited by 13
Flagged first, then by citations
Research works printed but not linked: 3
- Menesini-Chen, M. G., Chen, J. S. & Levi-Montalcini, R. Arch. Ital. Biol. 116, 53–84 (1978).
- Buznikov, G. A., Chudakova, I. V., Berysheva, L. V. & Vyazmina, N. M. J. Embryol. exp. Morph. 20, 119–128 (1968).
- Connor, J. A. & Nikolakopoulou, G. Lec. Math. Life Sci. 15, 79–101 (1982).
Cited by
Sorted by citations
The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6.
Serafini, T., Kennedy, T. E., Gaiko, M. J., Mirzayan, C., Jessell, T., & Tessier-Lavigne, M. (1994) · Cell · doi:10.1016/0092-8674(94)90420-0 · Cited by 1,397
Controlling Cell Behavior Electrically: Current Views and Future Potential
McCaig, C., Rajnicek, A. M., Song, B., & Zhao, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00020.2004 · Cited by 1,098
Physiological Diversity of Nicotinic Acetylcholine Receptors Expressed by Vertebrate Neurons
McGehee, D. S., & Role, L. W. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.002513 · Cited by 1,022
Neuronal nicotinic receptors: from structure to pathology
Gotti, C., & Clementi, F. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.09.006 · Cited by 970
Absence Epilepsy in Tottering Mutant Mice Is Associated with Calcium Channel Defects
Fletcher, C., Lutz, C. M., O’Sullivan, T. N., Shaughnessy, J. D., Hawkes, R. B., Frankel, W. N., Copeland, N. G., & Jenkins, N. A. (1996) · Cell · doi:10.1016/s0092-8674(00)81381-1 · Cited by 772
Metadata
- Authors
- Zheng, J. Q., Felder, M., Connor, J. A., & Poo, M.-M.
- Affiliations
- Columbia University (US)
- Venue
- Nature
- Published
- 1994-03
- Volume
- 368
- Issue
- 6467
- Pages
- 140-144
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2078047724
- Cited by
- 580
- References
- 40
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 3 · 2022: 7 · 2021: 5 · 2020: 4 · 2019: 6 · 2018: 9 · 2017: 6 · 2016: 11 · 2015: 11 · 2014: 14 · 2013: 17 · 2012: 13
- FWCI
- 16.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM083889)
- 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 › Nerve injury and regeneration
- Keywords
- growth cone turning, acetylcholine, chemotropism, chemoattractants, neuronal nicotinic acetylcholine receptors, calcium signaling, calcium/calmodulin-dependent protein kinase II, intracellular calcium, neurite guidance, axon guidance
- MeSH terms
- Acetylcholine, Animals, Axons, Calcium, Cell Movement, Cells, Cultured, Chemotactic Factors, Image Processing, Computer-Assisted, Microscopy, Fluorescence, Receptors, Cholinergic, Xenopus, Calcium-Calmodulin-Dependent Protein Kinases, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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