Cell Adhesion Molecules Regulate Ca2+-mediated Steering of Growth Cones Via Cyclic AMP and Ryanodine Receptor Type 3

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2005 Sep 21

PMID 16172206

Citations 38

Authors

Noriko Ooashi

Akira Futatsugi

Fumie Yoshihara

Katsuhiko Mikoshiba

Hiroyuki Kamiguchi

Affiliations

Soon will be listed here.

Abstract

Axonal growth cones migrate along the correct paths during development, not only directed by guidance cues but also contacted by local environment via cell adhesion molecules (CAMs). Asymmetric Ca2+ elevations in the growth cone cytosol induce both attractive and repulsive turning in response to the guidance cues (Zheng, J.Q. 2000. Nature. 403:89-93; Henley, J.R., K.H. Huang, D. Wang, and M.M. Poo. 2004. Neuron. 44:909-916). Here, we show that CAMs regulate the activity of ryanodine receptor type 3 (RyR3) via cAMP and protein kinase A in dorsal root ganglion neurons. The activated RyR3 mediates Ca2+-induced Ca2+ release (CICR) into the cytosol, leading to attractive turning of the growth cone. In contrast, the growth cone exhibits repulsion when Ca2+ signals are not accompanied by RyR3-mediated CICR. We also propose that the source of Ca2+ influx, rather than its amplitude or the baseline Ca2+ level, is the primary determinant of the turning direction. In this way, axon-guiding and CAM-derived signals are integrated by RyR3, which serves as a key regulator of growth cone navigation.

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References

Futatsugi A, Kato K, Ogura H, Li S, Nagata E, Kuwajima G . Facilitation of NMDAR-independent LTP and spatial learning in mutant mice lacking ryanodine receptor type 3. Neuron. 1999; 24(3):701-13. DOI: 10.1016/s0896-6273(00)81123-x. View

Henley J, Huang K, Wang D, Poo M . Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron. 2004; 44(6):909-16. PMC: 3121244. DOI: 10.1016/j.neuron.2004.11.030. View

Hong K, Nishiyama M, Henley J, Tessier-Lavigne M, Poo M . Calcium signalling in the guidance of nerve growth by netrin-1. Nature. 2000; 403(6765):93-8. DOI: 10.1038/47507. View

Castellani V, Chedotal A, Schachner M, Rougon G . Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron. 2000; 27(2):237-49. DOI: 10.1016/s0896-6273(00)00033-7. View

Doherty P, Williams G, Williams E . CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci. 2000; 16(4):283-95. DOI: 10.1006/mcne.2000.0907. View

Gomez T, Robles E, Poo M, Spitzer N . Filopodial calcium transients promote substrate-dependent growth cone turning. Science. 2001; 291(5510):1983-7. DOI: 10.1126/science.1056490. View

Perrin F, Rathjen F, Stoeckli E . Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. Neuron. 2001; 30(3):707-23. DOI: 10.1016/s0896-6273(01)00315-4. View

Kamiguchi H, Yoshihara F . The role of endocytic l1 trafficking in polarized adhesion and migration of nerve growth cones. J Neurosci. 2001; 21(23):9194-203. PMC: 6763905. View

Lokuta A, Komai H, McDowell T, Valdivia H . Functional properties of ryanodine receptors from rat dorsal root ganglia. FEBS Lett. 2002; 511(1-3):90-6. DOI: 10.1016/s0014-5793(01)03312-9. View

10.

Cheng S, Geddis M, Rehder V . Local calcium changes regulate the length of growth cone filopodia. J Neurobiol. 2002; 50(4):263-75. DOI: 10.1002/neu.10027. View

11.

Neumann S, Bradke F, Tessier-Lavigne M, Basbaum A . Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron. 2002; 34(6):885-93. DOI: 10.1016/s0896-6273(02)00702-x. View

12.

Qiu J, Cai D, Dai H, McAtee M, Hoffman P, Bregman B . Spinal axon regeneration induced by elevation of cyclic AMP. Neuron. 2002; 34(6):895-903. DOI: 10.1016/s0896-6273(02)00730-4. View

13.

Castellani V, De Angelis E, Kenwrick S, Rougon G . Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J. 2002; 21(23):6348-57. PMC: 136949. DOI: 10.1093/emboj/cdf645. View

14.

Nakai Y, Kamiguchi H . Migration of nerve growth cones requires detergent-resistant membranes in a spatially defined and substrate-dependent manner. J Cell Biol. 2002; 159(6):1097-108. PMC: 2173975. DOI: 10.1083/jcb.200209077. View

15.

Tang F, Dent E, Kalil K . Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth. J Neurosci. 2003; 23(3):927-36. PMC: 6741922. View

16.

Robles E, Huttenlocher A, Gomez T . Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain. Neuron. 2003; 38(4):597-609. DOI: 10.1016/s0896-6273(03)00260-5. View

17.

Nishiyama M, Hoshino A, Tsai L, Henley J, Goshima Y, Tessier-Lavigne M . Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature. 2003; 423(6943):990-5. DOI: 10.1038/nature01751. View

18.

Bouchard R, Pattarini R, Geiger J . Presence and functional significance of presynaptic ryanodine receptors. Prog Neurobiol. 2003; 69(6):391-418. DOI: 10.1016/s0301-0082(03)00053-4. View

19.

Huber A, Kolodkin A, Ginty D, Cloutier J . Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci. 2003; 26:509-63. DOI: 10.1146/annurev.neuro.26.010302.081139. View

20.

Augustine G, Santamaria F, Tanaka K . Local calcium signaling in neurons. Neuron. 2003; 40(2):331-46. DOI: 10.1016/s0896-6273(03)00639-1. View