Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1976 Aug 1;70(2):338–347. doi: 10.1083/jcb.70.2.338

Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons

PMCID: PMC2109828  PMID: 939781

Abstract

The structure of membranes at junctions between the plasma membrane and underlying cisterns of endoplasmic reticulum in amphioxus muscle and mouse cerebellar neurons was studied using the freeze-fracture technique. In amphioxus muscle, subsurface cisterns of sarcoplasmic reticulum form junctions with the surface membrane at the level of the sarcomere I bands. On the protoplasmic leaflet of the sarcolemma overlying these junctions were aggregates of large particles. On the protoplasmic leaflet of the membranes of cerebellar basket, stellate and Purkinie cells there were similar aggregates of large particles. In both tissues, the corresponding external membrane halves had arrays of pits apparently complementary to the aggregates of large particles. Cross fractures through junctions showed that the particle aggregates in neuronal and muscle membranes were consistently located over intracellular cisterns closely applied to the plasma membrane. Thus, a similar plasma membrane specialization is found at subsurface cisterns in mammalian neurons and amphioxus muscle. This similarity supports the hypothesis that subsurface cisterns in neurons, like those in muscle, couple some intracellular activity to the electrical activity of the plasma membrane.

Full Text

The Full Text of this article is available as a PDF (3.7 MB).

Selected References

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

  1. Armstrong C. M., Bezanilla F. M., Horowicz P. Twitches in the presence of ethylene glycol bis( -aminoethyl ether)-N,N'-tetracetic acid. Biochim Biophys Acta. 1972 Jun 23;267(3):605–608. doi: 10.1016/0005-2728(72)90194-6. [DOI] [PubMed] [Google Scholar]
  2. BOROWITZ J. L., FUWA K., WEINER N. DISTRIBUTION OF METALS AND CATECHOLAMINES IN BOVINE ADRENAL MEDULLA SUB-CELLULAR FRACTIONS. Nature. 1965 Jan 2;205:42–43. doi: 10.1038/205042a0. [DOI] [PubMed] [Google Scholar]
  3. Brodwick M. S., Junge D. Post-stimulus hyperpolarization and slow potassium conductance increase in Aplysia giant neurone. J Physiol. 1972 Jun;223(2):549–570. doi: 10.1113/jphysiol.1972.sp009862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Diamond I., Goldberg A. L. Uptake and release of 45Ca by brain microsomes, synaptosomes and synaptic vesicles. J Neurochem. 1971 Aug;18(8):1419–1431. doi: 10.1111/j.1471-4159.1971.tb00005.x. [DOI] [PubMed] [Google Scholar]
  5. Ebashi S., Endo M. Calcium ion and muscle contraction. Prog Biophys Mol Biol. 1968;18:123–183. doi: 10.1016/0079-6107(68)90023-0. [DOI] [PubMed] [Google Scholar]
  6. Ebashi S., Endo M., Otsuki I. Control of muscle contraction. Q Rev Biophys. 1969 Nov;2(4):351–384. doi: 10.1017/s0033583500001190. [DOI] [PubMed] [Google Scholar]
  7. Endo M., Tanaka M., Ogawa Y. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature. 1970 Oct 3;228(5266):34–36. doi: 10.1038/228034a0. [DOI] [PubMed] [Google Scholar]
  8. FRANZINI-ARMSTRONG C. FINE STRUCTURE OF SARCOPLASMIC RETICULUM AND TRANVERSE TUBULAR SYSTEM IN MUSCLE FIBERS. Fed Proc. 1964 Sep-Oct;23:887–895. [PubMed] [Google Scholar]
  9. Felz A., Krnjević K., Lisiewicz A. Intracellular free Ca 2+ and membrane properties of motoneurones. Nat New Biol. 1972 Jun 7;237(75):179–181. doi: 10.1038/newbio237179a0. [DOI] [PubMed] [Google Scholar]
  10. Ford L. E., Podolsky R. J. Regenerative calcium release within muscle cells. Science. 1970 Jan 2;167(3914):58–59. doi: 10.1126/science.167.3914.58. [DOI] [PubMed] [Google Scholar]
  11. Franzini-Armstron C. Freeze fracture of skeletal muscle from the Tarantula spider. Structural differentiations of sarcoplasmic reticulum and transverse tubular system membranes. J Cell Biol. 1974 May;61(2):501–513. doi: 10.1083/jcb.61.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Franzini-Armstrong C. Membrane particles and transmission at the triad. Fed Proc. 1975 Apr;34(5):1382–1389. [PubMed] [Google Scholar]
  13. Franzini-Armstrong C. Studies of the triad. IV. Structure of the junction in frog slow fibers. J Cell Biol. 1973 Jan;56(1):120–128. doi: 10.1083/jcb.56.1.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hagiwara S., Henkart M. P., Kidokoro Y. Excitation-contraction coupling in amphioxus muscle cells. J Physiol. 1971 Dec;219(1):233–251. doi: 10.1113/jphysiol.1971.sp009659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hagiwara S., Kidokoro Y. Na and Ca components of action potential in amphioxus muscle cells. J Physiol. 1971 Dec;219(1):217–232. doi: 10.1113/jphysiol.1971.sp009658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Howell J. N. Intracellular binding of ruthenium red in frog skeletal muscle. J Cell Biol. 1974 Jul;62(1):242–247. doi: 10.1083/jcb.62.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ishikawa H., Bischoff R., Holtzer H. Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J Cell Biol. 1969 Nov;43(2):312–328. [PMC free article] [PubMed] [Google Scholar]
  18. Kelly D. E. The fine structure of skeletal muscle triad junctions. J Ultrastruct Res. 1969 Oct;29(1):37–49. doi: 10.1016/s0022-5320(69)80054-7. [DOI] [PubMed] [Google Scholar]
  19. Krnjević K., Lisiewicz A. Injections of calcium ions into spinal motoneurones. J Physiol. 1972 Sep;225(2):363–390. doi: 10.1113/jphysiol.1972.sp009945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Landis D. M., Reese T. S. Arrays of particles in freeze-fractured astrocytic membranes. J Cell Biol. 1974 Jan;60(1):316–320. doi: 10.1083/jcb.60.1.316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lieberman E. M., Palmer R. F., Collins G. H. Calcium ion uptake by crustacean peripheral nerve subcellular particles. Exp Cell Res. 1967 May;46(2):412–418. doi: 10.1016/0014-4827(67)90077-8. [DOI] [PubMed] [Google Scholar]
  22. Meech R. W. The sensitivity of Helix aspersa neurones to injected calcium ions. J Physiol. 1974 Mar;237(2):259–277. doi: 10.1113/jphysiol.1974.sp010481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Otsuka M., Ohtsuki I., Ebashi S. ATP-dependent Ca binding of brain microsomes. J Biochem. 1965 Aug;58(2):188–190. doi: 10.1093/oxfordjournals.jbchem.a128184. [DOI] [PubMed] [Google Scholar]
  24. Ozawa E. Activation of phosphorylase kinase from brain by small amounts of calcium ion. J Neurochem. 1973 May;20(5):1487–1488. doi: 10.1111/j.1471-4159.1973.tb00263.x. [DOI] [PubMed] [Google Scholar]
  25. Peachey L. D. Transverse tubules in excitation-contraction coupling. Fed Proc. 1965 Sep-Oct;24(5):1124–1134. [PubMed] [Google Scholar]
  26. Podolsky R. J. Muscle activation: the current status. Fed Proc. 1975 Apr;34(5):1374–1378. [PubMed] [Google Scholar]
  27. Politoff A. L., Rose S., Pappas G. D. The calcium binding sites of synaptic vesicles of the frog sartorius neuromuscular junction. J Cell Biol. 1974 Jun;61(3):818–823. doi: 10.1083/jcb.61.3.818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Puszkin S., Berl S., Puszkin E., Clarke D. D. Actomyosin-like protein isolated from mammalian brain. Science. 1968 Jul 12;161(3837):170–171. doi: 10.1126/science.161.3837.170. [DOI] [PubMed] [Google Scholar]
  29. ROSENBLUTH J. Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol. 1962 Jun;13:405–421. doi: 10.1083/jcb.13.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sandow A. Excitation-contraction coupling in skeletal muscle. Pharmacol Rev. 1965 Sep;17(3):265–320. [PubMed] [Google Scholar]
  31. Siegesmund K. A. The fine structure of subsurface cisterns. Anat Rec. 1968 Oct;162(2):187–196. doi: 10.1002/ar.1091620206. [DOI] [PubMed] [Google Scholar]
  32. Takahashi K., Wood R. L. Subsurface cisterns in the Purkinje cells of cerebellum of Syrian hamster. Z Zellforsch Mikrosk Anat. 1970;110(3):311–320. doi: 10.1007/BF00321144. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES