Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1980 Apr;301:477–504. doi: 10.1113/jphysiol.1980.sp013219

The requirement for calcium ions and the effect of other ions on axoplasmic transport in mammalian nerve.

S Y Chan, S Ochs, R M Worth
PMCID: PMC1279412  PMID: 6157806

Abstract

1. Until recently it was believed that axoplasmic transport in vitro was not affected by Ca2+, transport being normal in Ca2+-free medium. This was found due to the presence of the relatively impermeable perineurial sheath around the nerve trunks. Using a desheathed cat peroneal nerve preparation, axoplasmic transport was shown to require an adequate level of Ca2+ in the external medium. In a buffered Ca2+-free medium, transport began to decline within 30 min and a complete block occurred in 2 . 6 hr. A concentration of 5 mM-Ca2+ added to a buffered isotonic sucrose of NaCl solution was able to maintain transport. With lower concentrations of Ca2+ of 1 . 5-3 . 0 mM, those usually present in the extracellular fluid or in a Ringer medium, some impairment of transport was seen but the addition of 4 mM-K+ restored the normal pattern of axoplasmic transport. With Ca2+ concentrations below 0 . 75 mM, however, 4 mM-K+ was unable to sustain transport. 2. Potassium by itself at a concentration of 4 mM when added to a buffered isotonic sucrose of NaCl medium was unable to prolong the time of transport block beyond that seen in buffered isotonic NaCl or sucrose solutions. In concentrations of K+ up to 25 mM, 1 . 5-5 mM-Ca2+ was required for normal transport. With moderately higher concentrations of K+ in the range of 50-100 mM, normal appearing transport was seen with or without Ca2+. This was seen whether or not Na+ was present in the medium. At higher levels of K+, 120-150 mM, decreased transport was seen, with or without the addition of either 15 mM-Na+ or Ca2+ in concentrations of 1 . 5-3 . 0 mM. 3. While Mg2+ could not substitute completely for Ca2+ in maintaining transport, it was able to prolong the time before block occurred. An extra 30-60 min of downflow was seen when 5 mM-Mg2+ was added to a buffered isotonic NaCl medium. Magnesium also acts synergistically with Ca2+. Concentration of Ca2+ as low as 0 . 25 mM was, with the addition of 1 . 5 mM-Mg2+, able to maintain transport. 4. The results are interpreted in the light of studies of the mechanism of Ca2+ regulation known to occur in giant nerve fibres and other clls controlling the level of free Ca2+. The relationship of Ca2+ to the mechanism considered to underlie axoplasmic transport in nerve fibres is also discussed.

Full text

PDF
477

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe T., Haga T., Kurokawa M. Rapid transport of phosphatidylcholine occurring simultaneously with protein transport in the frog sciatic nerve. Biochem J. 1973 Nov;136(3):731–740. doi: 10.1042/bj1360731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker P. F., Blaustein M. P., Keynes R. D., Manil J., Shaw T. I., Steinhardt R. A. The ouabain-sensitive fluxes of sodium and potassium in squid giant axons. J Physiol. 1969 Feb;200(2):459–496. doi: 10.1113/jphysiol.1969.sp008703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker P. F., Glitsch H. G. Does metabolic energy participate directly in the Na+-dependent extrusion of Ca2+ -Ca2+ ions from squid giant axons? J Physiol. 1973 Aug;233(1):44P–46P. [PubMed] [Google Scholar]
  4. Baker P. F. Transport and metabolism of calcium ions in nerve. Prog Biophys Mol Biol. 1972;24:177–223. doi: 10.1016/0079-6107(72)90007-7. [DOI] [PubMed] [Google Scholar]
  5. Banks P., Mayor D., Mraz P. Metabolic aspects of the synthesis and intra-axonal transport of noradrenaline storage vesicles. J Physiol. 1973 Mar;229(2):383–394. doi: 10.1113/jphysiol.1973.sp010144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bergmann C., Nonner W., Stämpfli R. Sustained spontaneous activity of Ranvier nodes induced by the combined actions of TEA and lack of calcium. Pflugers Arch. 1968;302(1):24–37. doi: 10.1007/BF00586780. [DOI] [PubMed] [Google Scholar]
  7. Blaustein M. P., Hodgkin A. L. The effect of cyanide on the efflux of calcium from squid axons. J Physiol. 1969 Feb;200(2):497–527. doi: 10.1113/jphysiol.1969.sp008704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blaustein M. P. The interrelationship between sodium and calcium fluxes across cell membranes. Rev Physiol Biochem Pharmacol. 1974;70:33–82. doi: 10.1007/BFb0034293. [DOI] [PubMed] [Google Scholar]
  9. CRESCITELLI F. Nerve sheath as a barrier to the action of certain substances. Am J Physiol. 1951 Aug;166(2):229–240. doi: 10.1152/ajplegacy.1951.166.2.229. [DOI] [PubMed] [Google Scholar]
  10. Clarke E., Bearn J. G. The spiral nerve bands of Fontana. Brain. 1972;95(1):1–20. doi: 10.1093/brain/95.1.1. [DOI] [PubMed] [Google Scholar]
  11. DiPolo R. Ca pump driven by ATP in squid axons. Nature. 1978 Jul 27;274(5669):390–392. doi: 10.1038/274390a0. [DOI] [PubMed] [Google Scholar]
  12. Duce I. R., Keen P. Can neuronal smooth endoplasmic reticulum function as a calcium reservoir? Neuroscience. 1978;3(9):837–848. doi: 10.1016/0306-4522(78)90036-2. [DOI] [PubMed] [Google Scholar]
  13. Edström A. Effects of Ca2+ and Mg2+ on rapid axonal transport of proteins in vitro in frog sciatic nerves. J Cell Biol. 1974 Jun;61(3):812–818. doi: 10.1083/jcb.61.3.812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. FRANKENHAEUSER B. The effect of calcium on the myelinated nerve fibre. J Physiol. 1957 Jul 11;137(2):245–260. doi: 10.1113/jphysiol.1957.sp005809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fink B. R., Kennedy R. D., Hendrickson A. E., Middaugh M. E. Lidocaine inhibition of rapid axonal transport. Anesthesiology. 1972 May;36(5):422–432. doi: 10.1097/00000542-197205000-00002. [DOI] [PubMed] [Google Scholar]
  16. HODGKIN A. L., KEYNES R. D. The potassium permeability of a giant nerve fibre. J Physiol. 1955 Apr 28;128(1):61–88. doi: 10.1113/jphysiol.1955.sp005291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HUXLEY A. F. Ion movements during nerve activity. Ann N Y Acad Sci. 1959 Aug 28;81:221–246. doi: 10.1111/j.1749-6632.1959.tb49311.x. [DOI] [PubMed] [Google Scholar]
  18. Hammerschlag R., Dravid A. R., Chiu A. Y. Mechanism of axonal transport: a proposed role for calcium ions. Science. 1975 Apr 18;188(4185):273–275. doi: 10.1126/science.47182. [DOI] [PubMed] [Google Scholar]
  19. Henkart M. P., Reese T. S., Brinley F. J., Jr Endoplasmic reticulum sequesters calcium in the squid giant axon. Science. 1978 Dec 22;202(4374):1300–1303. doi: 10.1126/science.725607. [DOI] [PubMed] [Google Scholar]
  20. Hindelang-Gertner C., Stoeckel M. E., Porte A., Stutinsky F. Colchicine effects on neurosecretory neurons and other hypothalamic and hypophysial cells, with special reference to changes in the cytoplasmic membranes. Cell Tissue Res. 1976 Jul 20;170(1):17–41. doi: 10.1007/BF00220108. [DOI] [PubMed] [Google Scholar]
  21. Iqbal Z., Ochs S. Fast axoplasmic transport of a calcium-binding protein in mammalian nerve. J Neurochem. 1978 Aug;31(2):409–418. doi: 10.1111/j.1471-4159.1978.tb02656.x. [DOI] [PubMed] [Google Scholar]
  22. Kalix P. Uptake and release of calcium in rabbit vagus nerve. Pflugers Arch. 1971;326(1):1–14. doi: 10.1007/BF00586791. [DOI] [PubMed] [Google Scholar]
  23. Khan M. A., Ochs S. Magnesium or calcium activated ATPase in mammalian nerve. Brain Res. 1974 Dec 13;81(3):413–426. doi: 10.1016/0006-8993(74)90840-3. [DOI] [PubMed] [Google Scholar]
  24. Kumara-Siri M. H. Batrachotoxin inhibits axonal transport without affecting membrane potential in single neurons of Aplysia californica. J Neurobiol. 1979 Sep;10(5):509–512. doi: 10.1002/neu.480100508. [DOI] [PubMed] [Google Scholar]
  25. Lavoie P. A., Bolen F., Hammerschlag R. Divalent cation specificity of the calcium requirement for fast transport of proteins in axons of desheathed nerves. J Neurochem. 1979 Jun;32(6):1745–1751. doi: 10.1111/j.1471-4159.1979.tb02287.x. [DOI] [PubMed] [Google Scholar]
  26. Lehninger A. L., Carafoli E., Rossi C. S. Energy-linked ion movements in mitochondrial systems. Adv Enzymol Relat Areas Mol Biol. 1967;29:259–320. doi: 10.1002/9780470122747.ch6. [DOI] [PubMed] [Google Scholar]
  27. Narahashi T., Albuquerque E. X., Deguchi T. Effects of batrachotoxin on membrane potential and conductance of squid giant axons. J Gen Physiol. 1971 Jul;58(1):54–70. doi: 10.1085/jgp.58.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ochs S. Fast transport of materials in mammalian nerve fibers. Science. 1972 Apr 21;176(4032):252–260. doi: 10.1126/science.176.4032.252. [DOI] [PubMed] [Google Scholar]
  29. Ochs S., Hollingsworth D. Dependence of fast axoplasmic transport in nerve on oxidative metabolism. J Neurochem. 1971 Jan;18(1):107–114. doi: 10.1111/j.1471-4159.1971.tb00172.x. [DOI] [PubMed] [Google Scholar]
  30. Ochs S., Ranish N. Characteristics of the fast transport system in mammalian nerve fibers. J Neurobiol. 1969;1(2):247–261. doi: 10.1002/neu.480010211. [DOI] [PubMed] [Google Scholar]
  31. Ochs S. Rate of fast axoplasmic transport in mammalian nerve fibres. J Physiol. 1972 Dec;227(3):627–645. doi: 10.1113/jphysiol.1972.sp010051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ochs S., Smith C. Low temperature slowing and cold-block of fast axoplasmic transport in mammalian nerves in vitro. J Neurobiol. 1975 Jan;6(1):85–102. doi: 10.1002/neu.480060112. [DOI] [PubMed] [Google Scholar]
  33. Ochs S., Worth R. M., Chan S. Y. Calcium requirement for axoplasmic transport in mammalian nerve. Nature. 1977 Dec 22;270(5639):748–750. doi: 10.1038/270748a0. [DOI] [PubMed] [Google Scholar]
  34. Ochs S., Worth R. Batrachotoxin block of fast axoplasmic transport in mammalian nerve fibers. Science. 1975 Mar 21;187(4181):1087–1089. doi: 10.1126/science.46619. [DOI] [PubMed] [Google Scholar]
  35. Partlow L. M., Ross C. D., Motwani R., McDougal D. B., Jr Transport of axonal enzymes in surviving segments of frog sciatic nerve. J Gen Physiol. 1972 Oct;60(4):388–405. doi: 10.1085/jgp.60.4.388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sabri M. I., Ochs S. Relation of ATP and creatine phosphate to fast axoplasmic transport in mammalian nerve. J Neurochem. 1972 Dec;19(12):2821–2828. doi: 10.1111/j.1471-4159.1972.tb03819.x. [DOI] [PubMed] [Google Scholar]
  37. Schlaepfer W. W. Experimental alterations of neurofilaments and neurotubules by calcium and other ions. Exp Cell Res. 1971 Jul;67(1):73–80. doi: 10.1016/0014-4827(71)90622-7. [DOI] [PubMed] [Google Scholar]
  38. Theron J. J., Meyer B. J., Boekkooi S., Loots J. M. Ultrastructural localisation of calcium in peripheral nerves of the rat. S Afr Med J. 1975 Oct 11;49(43):1795–1798. [PubMed] [Google Scholar]
  39. Warnick J. E., Albuquerque E. X. Models of paraplegia in animals: trophic relationships. Fed Proc. 1978 Dec;37(14):2811–2817. [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES