Distinct calcium signaling within neuronal growth cones and filopodia

Journal of Neurobiology

Volumn 31, Issue 1, 1996, Pages 1-15

  Davenport, Roger W ^a,c   Dou, Ping ^a   Mills, Linda R ^b   Kater, S B ^a,d  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

calcium; filopodia; growth cone; navigation; organelle

Indexed keywords

CALCIMYCIN; CALCIUM ION; DOPAMINE; EGTAZIC ACID; NEUROTRANSMITTER; SEROTONIN; THAPSIGARGIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL MOTION; CELL ORGANELLE; GROWTH CONE; NERVE CELL CULTURE; NERVE CELL GROWTH; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CALCIMYCIN; CALCIUM; CELLS, CULTURED; DOPAMINE; IONOPHORES; NEURITES; NEURONS; SENSE ORGANS; SEROTONIN; SIGNAL TRANSDUCTION; SNAILS; THAPSIGARGIN;

EID: 0029772336     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199609)31:1<1::AID-NEU1>3.0.CO;2-6     Document Type: Article

References (71)

1. BANDTLOW, C., ZACHLEDER, T., and SCHWAB, M. (1990). Oligodendrocytes arrest neurite growth by contact inhibition. J. Neurosci. 10:3837-3848.
2. BANDTLOW, C. E., SCHMIDT, M. F., HASSINGER, T. D., SCHWAB, M. E., and KATER, S. B. (1993). Intracellular calcium mediates growth cone collapse evoked by the CNS myelin-associated neurite growth inhibitor NI-35. Science 259:80-83.
3. BASTMEYER, M. and STUERMER, C. A. O. (1993). Behavior of fish retinal growth cones encountering chick caudal tectal membranes: a time-lapse study on growth cone collapse. J. Neurobiol. 24:37-50.
4. BEDLACK, R. S., Jr., WEI, M.-D., and LOEW, L. M. (1992). Localized membrane depolarizations and localized calcium influx during electric field-guided neurite growth. Neuron 9:398-404.
5. BENTLEY, D. and O'CONNOR, T. P. (1994). Cytoskeletal events in growth cone steering. Curr. Opin. Neurobiol. 4:43-48.
6. BENTLEY, D. and TOROIAN-RAYMOND, A. (1986). Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323:712-715.
7. BLEAKMAN, D., ROBACK, J. D., WAINER, B. H., MILLER, R. J., and HARRISON, N. L. (1993). Calcium homeostasis in rat septal neurons in tissue culture. Br. Res. 600:257-267.
8. BRIDGMAN, P. C. (1992). Functional anatomy of the growth cone in relation to its role in locomotion and neunte assembly. In: The Nerve Growth Cone. P. C. Letourneau, S. B. Kater, and E. R. Macagno, Eds. Raven Press, New York, pp. 39-53.
9. BURMEISTER, D. W., RIVAS, R. J., and GOLDBERG, D. J. (1991). Substrate-bound factors stimulate engorgement of growth cone lamellipodia during neurite elongation. Cell Motil. Cytoskeleton 19:255-268.
10. CHIEN, C. B., ROSENTHAL, D. E., HARRIS, W. A., and HOLT, C. E. (1993). Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11:237-251.
11. COHAN, C. S., CONNOR, J. A., and KATER, S. B. (1987). Electrically and chemically mediated increases in intracellular calcium in neuronal growth cones. J. Neurpsci. 7:3588-3599.
12. DAILEY, M. E. and BRIDGMAN, P. C. (1989). Dynamics of the endoplasmic reticulum and other membranous organelles in the growth cones of cultured neurons. J. Neurosci. 9:1897-1909.
13. DAVENPORT, R. W., Dou, P., REHDER, V., and KATER, S. B. (1993). A sensory role for neuronal growth cone filopodia. Nature 361:721-724.
14. DAVENPORT, R. W. and KATER, S. B. (1992). Local increases in intracellular calcium elicit local filopodial responses in Helisoma neuronal growth cones. Neuron 9:405-416.
15. DAVENPORT, R. W. and McCAIG, C. D. (1993). Hippocampal growth cone responses to focally applied electric fields. J. Neurobiol. 24:89-100.
16. DAVENPORT, R. W., THIES, E., and NELSON, P. G. (1996). Cellular localization of guidance cues in the establishment of retinotectal topography. J. Neurosci. 16.
17. FAN, J. and RAPER, J. A. (1995). Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14:263-274.
18. FIELDS, R. D., GUTHRIE, P. B., RUSSELL, J. T., KATER, S. B., MALHOTRA, B. S., and NELSON, P. G. (1993). Accommodation of mouse DRG growth cones to electrically induced collapse: kinetic analysis of calcium transients and set-point theory. J. Neurobiol. 24: 1080-1089.
19. FORSCHER, P., KACZMAREK, L. K., BUCHANAN, J. A., and SMITH, S. J. (1987). Cyclic AMP induces changes in distribution and transport of organelles within growth cones of Aplysia bag cell neurons. J. Neurosci. 7:3600-3611.
20. FORSCHER, P. and SMITH, S. J. (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107:1505-1516.
21. FOSKETT, J. K. and WONG, D. (1992). Calcium oscillations in parotid acinar cells induced by microsomal Ca2+-ATPase inhibition. Am. J. Physiol. 262:C656-C663.
22. GHOSH, T. K., BIAN, J., SHORT, A. D., RYBAK, S. L., wand GILL, D. L. (1991). Persistent intracellular calcium pool depletion by thapsigargin and its influence on cell growth. J. Biol. Chem. 266:24690-24697.
23. GIERER, A. (1981). Development of projections between areas of the nervous system. Biol. Cybernet. 42: 69-78.
24. GIERER, A. (1987). Directional cues for growing axons forming the retinotectal projection. Development 101: 479-489.
25. GOLDBERG, D. J. (1988). Local role of Ca2+ in formation of veils in growth cones. J. Neurosci. 8:2596-2605.
26. GOLDBERG, D. J., BURMEISTER, D. W., and RIVAS, R. J. (1992). Video microscopic analysis of events in the growth cone underlying axon growth and the regulation of these events by substrate-bound proteins. In: The Nerve Growth Cone. (P. C. Letourneau, S. B. Kater, E. R. Macagno), Eds. Raven Press, New York, pp. 79-95.
27. GOLDBERG, J. I. and KATER, S. B. (1989). Expression and function of the neurotransmitter serotonin during development of the Helisoma nervous system. Dev. Biol. 131:483-495.
28. GOMEZ, T. M., SNOW, D. M., and LETOURNEAU, P. C. (1995). Characterization of spontaneous calcium transients in nerve growth cones and their effect on growth cone migration. Neuron 14:1233-1246.
29. GRYNKIEWICZ, G., POENIE, M., and TSIEN, R. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450.
30. GUNDERSEN, R. W. and BARRETT, J. N. (1980). Characterization of the turning response of dorsal root neurites toward nerve growth factor. J. Cell Biol. 87:546-554.
31. HAYDON, P. G., MCCOBB, D. P., and KATER, S. B. (1984). Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons. Science 226:561-564.
32. 2+ mobilizing mechanisms in cultured rat cerebellar granule cells. J. Physiol (Lond.) 456:667-680.
33. 2+ sensitivities. Cell. Calcium 13:293-301.
34. KATER, S. B., MATTSON, M. P., COHAN, C. S., and CONNOR, J. A. (1988). Calcium regulation of the neuronal growth cone. TINS 11:315-321.
35. KATER, S. B. and MILLS, L. (1991). Regulation of growth cone behavior by calcium. J. Neurosci. 11: 891-899.
36. KIJIMA, Y., OGUNBUNMI, E., and FLEISCHER, S. (1991). Drug action of thapsigargin on the Ca2+ pump protein of sarcoplasmic reticulum. J. Biol. Chem. 266: 22912-22918.
37. LANKFORD, K. L. and LETOURNEAU, P. C. (1989). Evidence that calcium may control neunte outgrowth by regulating the stability of actin filaments. J. Cell Biol. 109:1229-1243.
38. LANKFORD, K. L. and LETOURNEAU, P. C. (1991). Roles of actin filaments and three second-messenger systems in short-term regulation of chick dorsal root ganglion neunte outgrowth. Cell. Motil. Cytoskeleton 20:7-29.
39. LEE, C. and CHEN, L. B. (1988). Dynamic behavior of endoplasmic reticulum in living cells. Cell 54:37-46.
40. LETOURNEAU, P. C., KATER, S. B., and MACAGNO, E. R. (1991). The Nerve Growth Cone. Raven Press, New York.
41. LIN, C. H., THOMPSON, C. A., and FORSCHER, P. (1994). Cytoskeletal reorganization underlying growth cone motility. Curr. Opin. Neurobiol. 4:640-647.
42. MATTSON, M. P. and KATER, S. B. (1987). Calcium regulation of neunte elongation and growth cone motility. J. Neurosci. 7:4034-4043.
43. MCCAIG, C. D. (1986). Dynamic aspects of amphibian neunte growth and the effects of an applied electric field. J. Physiol. 375:55-69.
44. MCCAIG, C. D. (1989). Nerve growth in the absence of growth cone filopodia and the effects of a small applied electric field. J. Cell Sci. 93:715-721.
45. MCCOBB, D. P., HAYDON, P. G., and KATER, S. B. (1988b). Dopamine and serotonin inhibition of neurite elongation on different identified neurons. J. Neurosci. Res. 19:19-26.
46. MILLS, L. R. (1994). Confocal calcium imaging. In: Three-Dimensional Confocal Microscopy. J. K. Stevens, L. R. Mills, and J. Trogadis, Eds. Academic Press, Orlando, FL.
47. MILLS, L. R. and KERR, R. (1994). Confocal imaging of organelles in living and fixed cells. In: Three-Dimensional Confocal Microscopy. J. K. Stevens, L. R. Mills, and J. Trogadis, Eds. Academic Press, Orlando, FL.
48. 2+ channels are located on somata, dendrites and a subpopulation of dendritic spines on live hippocampal pyramidal neurons. J. Neurosci. 14:6815-6824.
49. MILLS, L. R. and NURSE, C. A. (1993). Chronic hypoxia in vitro increases volume of dissociated carotid body chemoreceptors. NeuroReport 4:619-422.
50. NEELY, M. D. (1993). Role of substrate and calcium in neurite retraction of leech neurons following depolarization. J Neurosci. 13:1292-1301.
51. O'CONNOR, T. P., DUERR, J. S., and BENTLEY, D. (1990). Pioneer growth cone steering decisions mediated by single filopodial contacts in situ. J. Neurosci. 10:3935-3946.
52. OUYANG, Y., AIREY, J., SUKO, J. L., and ELLISMAN, M. H. (1994). Localization of ryanodine receptors at growth cones of cultured neurons. Soc. Neurosci. Abstr. 20:1082.
53. PARKER, I. and YAO, Y. (1991). Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc. R. Soc. Lond. 246: 269-274.
54. PATEL, N. and Poo, M.-M. (1982). Orientation of neurite growth by extracellular electric fields. J. Neurosci. 2:483-496.
55. PATEL, N. B. and Poo, M. (1984). Perturbation of the direction of neurite growth by probes and focal electric fields. J. Neurosci. 4:2939-2947.
56. REED, P. W. and LARDY, H. A. (1972). A23187: a divalent action ionophore. J. Biol. Chem. 247:6970-6977.
57. RENDER, V., JENSEN, J. R., Dou, P., and KATER, S. B. (1991). A comparison of calcium homeostasis in isolated and attached growth cones of the snail Helisoma. J. Neurobiol. 22:499-511.
58. REHDER, V. and KATER, S. B. (1992). Regulation of neuronal growth cone filopodia by intracellular calcium. J. Neurosci. 12:3175-3186.
59. RIVAS, R. J., BURMEISTER, D. W., and GOLDBERG, D. J. (1992). Rapid effects of laminin on the growth cone. Neuron 8:107-115.
60. SAGARA, Y., FERNANDEZBELDA, F., DEMEIS, L., and INESI, G. (1992). Characterization of the inhibition of intracellular Ca2+ transport ATPases by thapsigargin. J. Biol. Chem. 267:12606-12613.
61. SILVER, R. A., LAMB, A. G., and BOLSOVER, S. R. (1990). Calcium hotspots caused by L-channel clustering promote morphological changes in neuronal growth cones. Nature 343:751-754.
62. STEVENS, J. K., TROGADIS, J., MILLS, L. R., and LEITO, C. (1990). Three dimensional volume investigation of serial confocal data sets. Microscopy 90:375-380.
63. TERASAKI, M. and JAFFE, L. A. (1991). Organization of the sea urchin egg endoplasmic reticulum and its reorganization at fertilization. J. Cell Biol. 114:929-940.
64. 2+-ATPase inhibitor, thapsigargin. Agents Actions 29:8-15.
65. 2+-ATPase. Proc. Natl. Acad. Sci. USA 87:2466-2470.
66. 2+ concentrations. Cell. Calcium 12:29-37.
67. WONG, R. G., BARKER, D. L., KATER, S. B., and BODNAR, D. A. (1984). Nerve growth-promoting factor produced in culture media conditioned by specific CNS tissues of the snail Helisoma. Brain Res. 292:81-91.
68. WONG, R. G., HADLEY, R. D., KATER, S. B., and HAUSER, G. C. (1981). Neunte outgrowth in molluscan organ and cell cultures: the role of conditioning factor(s). J. Neurosci. 1:1008-1021.
69. WONG, R. G., MARTEL, E. C., and KATER, S. B. (1983). Conditioning factor(s) produced by several molluscan species promote neunte outgrowth in cell culture. J. Exp. Biol. 105:389-393.
70. ZHENG, J. Q., FELDER, M., CONNOR, J. A., and POO, M.-M. (1994). Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
71. ZHENG, J. Q., WAN, J., and POO, M.-M. (1996). Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16:1140-1149.