Development of nodes of Ranvier in feline nerves: An ultrastructural presentation

Microscopy Research and Technique

Volumn 34, Issue 5, 1996, Pages 399-421

  Berthold, Claes H ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Alpha motor axon; Axon; Cat; Degeneration; Development; Microvilli; Mitochondria; Myelin sheath; Node of Ranvier; Peripheral nervous system; Schwann cell

Indexed keywords

CELL MEMBRANES; CYTOLOGY; MITOCHONDRIA;

ALPHA MOTOR AXON; AXON; CAT; DEGENERATION; DEVELOPMENT; MICROVILLI; MITOCHONDRIAS; MOTOR AXONS; MYELIN SHEATHS; NODE OF RANVIER; PERIPHERAL NERVOUS SYSTEM; SCHWANN CELLS;

NEURONS;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAT; CELL ULTRASTRUCTURE; ELECTRON MICROSCOPY; MICROSCOPIC ANATOMY; MICROVILLUS; MYELIN SHEATH; MYELINATION; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; RANVIER NODE; SCHWANN CELL;

EID: 0029742255     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-0029(19960801)34:5<399::AID-JEMT1070340502>3.0.CO;2-N     Document Type: Article

References (95)

1. Allt, G. (1969) Ultrastructural features of the immature peripheral nerve. J. Anat., 105:283-293
2. Arbuthnott, E.R., Boyd, I.A., and Kalu, K.U. (1980) Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. J. Physiol. 308:125-157.
3. Armstrong, R., Toews, A.D., and Morell, P. (1987) Axonal transport through nodes of Ranvier. Brain Res., 412:196-199.
4. Berthold, C.-H. (1968) Ultrastructure of peripheral developing nodes of Ranvier. Acta Soc. Med. Upsal., 73:145-168.
5. Berthold, C.-H. (1973a) Histochemistry of postnatally developing feline spinal roots. I. A study with the OTAN (osmiumtetroxide-alpha-naphtylamine) method. Neurobiology, 3:275-290.
6. Berthold, C.-H. (1973b) Histochemistry of postnatally developing feline spinal roots. II. Occurrence of acid phosphatase activity as studied by light and electron microscopical methods. Neurobiology, 3:291-310.
7. Berthold, C.-H. (1973c) Local "demyelination" in developing feline nerve fibers. Neurobiology, 3:339-352.
8. Berthold, C.-H. (1974a) A comparative morphological study of the developing node-paranode region in lumbar spinal roots. I. Electronmicroscopy. Neurobiology, 4:82-104.
9. Berthold, C.-H. (1974b) A comparative morphological study of the developing node-paranode region in lumbar spinal roots. II. Light microscopy after osmiumtetroxide-alpha-naphtylamine(OTAN)-staining. Neurobiology, 4:117-131.
10. Berthold, C.-H. (1978) Morphology of normal peripheral axons. In: Physiology and Pathobiology of Axons. S.G. Waxman, ed. Raven Press, New York, pp. 3-63.
11. Berthold, C.-H., and Carlstedt, T. (1977) A lightmicroscopical and histochemical study of S1 dorsal rootlets in the developing kitten. Acta Physiol. Scand., Suppl. 446:73-85.
12. Berthold, C.-H., and Mellström, A. (1986) Peroxidase activity at consecutive nodes of Ranvier in the nerve to the medial gastrocnemius muscle after intramuscular administration of horseradish peroxidase. Neuroscience, 19:1349-1362.
13. Berthold, C.-H., and Nilsson, I. (1987) Redistribution of Schwann cells in developing feline L7 ventral spinal roots. J. Neurocytol., 16:811-828.
14. Berthold, C.-H., and Rydmark, M. (1983) Electron microscopic serial section analysis of nodes of Ranvier in lumbosacral spinal roots of the cat: Ultrastructural organization of nodal compartments in fibres of different sizes. J. Neurocytol. 12:475-505.
15. Berthold, C.-H., and Rydmark, M. (1995) Morphology of the normal peripheral axon. In: The Axon, S. Waxman, J. Kocsis, and P. Stys, eds. Oxford University Press, Inc., New York, pp. 13-48.
16. Berthold, C.-H., and Skoglund, S. (1967) Histochemical and ultrastructural demonstration of mitochondria in the paranodal region of developing feline spinal roots and nerves. Acta Soc. Med. Upsal., 72:37-70.
17. Berthold, C.-H., and Skoglund, S. (1968a) Postnatal development of feline paranodal myelin sheath segments. I. Lightmicroscopy. Acta Soc. Med. Upsal., 73:113-126.
18. Berthold, C.-H., and Skoglund, S. (1968b) Postnatal development of feline paranodal myelin sheath segments. II. Electronmicroscopy. Acta Soc. Med. Upsal., 73:127-144.
19. Berthold, C.-H., Nilsson, I., and Rydmark, M. (1983) Axon diameter and myelin sheath thickness in nerve fibers of the ventral spinal root of the seventh lumbar nerve of the adult and developing cat. J. Anat., 136:483-508.
20. Berthold, C.-H., Fabricius, C., Rydmark, M., and Andersen, B. (1993) Axoplasmic organelles at nodes of Ranvier. I. Distribution and occurrence in large myelinated spinal root axons of the adult cat. J. Neurocytol., 22:925-940.
21. Bertram, M., and Schröder, J.M. (1993) Developmental changes at the node and paranode in human sural nerves; morphometric and fine-structural evaluation. Cell Tissue Res., 273:499-599.
22. Bostock, H. (1993) Impulse propagation in experimental neuropathy. In: Peripheral Neuropathy. Third edition. P.J. Dyck, and P.K. Thomas, eds. W.B. Saunders Company, Philadelphia, pp. 109-120.
23. Chiu, S.Y. (1993) Channel functions in mammalian axons and support cells. In: Peripheral Neuropathy. Third edition. P.J. Dyck, and P.K. Thomas, eds. W.B. Saunders Company, Philadelphia, pp. 94-108.
24. De Vries, G.H. (1993) Schwann cell proliferation. In: Peripheral Neuropathy. Third edition. P.J. Dyck, and P.K. Thomas, eds. W.B. Saunders Company, Philadelphia, pp. 290-298.
25. deWaegh, S.M., and Brady, S.T. (1990) Altered slow axonal transport and regeneration in a myelin-deficient mutant mouse: The Trembler as an in vivo modal for Schwann cell-axon interactions. J. Neurosci. 10:1855-1865.
26. deWaegh, S.M., and Brady, S.T. (1991) Local control of axonal properties by Schwann cells: Neurofilaments and axonal transport in homologous and heterologous nerve grafts. J. Neurosci. Res. 30: 201-212.
27. deWaegh, S.M., Lee, V.M.-Y., and Brady, S.T. (1992) Local modulation of neurofilament phosphorylation, axonal caliber and slow axonal transport by myelinating Schwann cells. Cell 68:451-463.
28. Ekholm, J. (1967) Postnatal changes in cutaneous reflexes and in the discharge pattern of cutaneous and articular sense organs. Acta Physiol. Scand., Suppl. 297.
29. Ellisman, M. (1979) Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination. J. Neurocytol., 8:719-735.
30. Ellisman, M.H., and Lindsey, J.D. (1983) The axoplasmic reticulum within myelinated axons is not transported rapidly. J. Neurocytol., 12:393-411.
31. Friede, R.L., and Beuche, W. (1985) A new approach toward analyzing peripheral nerve fiber populations. I. Variance in sheath thickness corresponds to different geometric proportions of the internode. J. Neuropath. Exp. Neurol. 44:60-72.
32. Friede, R.L., and Bischhausen, R. (1982) How are sheath dimensions affected by axon calibre and internodal length? Brain Res. 235: 335-350.
33. Friede, R.L., Meier, T., and Diem, M. (1981) How is the exact length of an internode determined? J. Neurol. Sci. 50:217-228.
34. Gatzinsky, K.P., and Berthold, C.-H. (1990) Lysosomal activity at nodes of Ranvier during retrograde axonal transport of horseradish peroxidase in alpha-motor neurons of the cat. J. Neurocytol. 19: 989-1002.
35. Gatzinsky, K.P., Berthold, C.-H., and Corneliuson, O. (1988) Acid phosphatase activity at nodes of Ranvier in alpha-motor and dorsal root ganglion neurons of the cat. J. Neurocytol. 17:531-544.
36. Geren Uzman, B., and Nogueira-Graf, G., (1957) Electronmicroscope studies of the formation of nodes of Ranvier in mouse sciatic nerves. J. Biophys. Biochem. Cytol., 3:589-597.
37. Gorio, A. (1984) Sprouting and regeneration of peripheral nerve. In: The Node of Ranvier. J.C. Zagoren, and S. Fedoroff, eds. Academic Press, New York, pp. 353-388.
38. Gould, R.M., Jessen, K.R., Mirsky, R., and Tennekoon, G. (1992) The cell of Schwann: An update. In: Myelin: Biology and Chemistry. R.E. Martensen, ed. Boca Raton, FL, CRC Press, pp. 123-171.
39. Griffin, J.W. (1993) Interactions between axons and Schwann cells. In: Peripheral Neuropathy. Third edition. P.J. Dyck, and P.K. Thomas, eds. W.B. Saunders Company, Philadelphia, pp. 317-330.
40. Griffin, J.W., Rosenfeldt, J., Hoffman, P.N., Gold, B.G., and Trapp, B.D. (1988) The axonal cytoskeleton: Influences on nerve fiber form and Schwann cell behavior. In: Intrinsic determinants of neuronal form and functions. R.J. Lasek, M.M. Black, eds. New York, Alan R. Liss, Inc., pp. 403-439.
41. Hildebrand, C., Bowe, C.M., and Nilsson Remahl, I. (1994) Myelination and myelin sheath remodelling in normal and pathological pns nerve fibres. Progr. Neurobiol., 43/2:85-141.
42. Hirano, A. (1984) Nodes of Ranvier in pathological conditions. In: The Node of Ranvier. J.C. Zagoren, and S. Fedoroff, eds. Academic Press, pp. 213-243.
43. Hirano, A., and Dembitzer, H.A. (1982) Further studies on the transverse bands. J. Neurocytol., 11:861-866.
44. Hopkins, W.G., and Brown, M.C. (1982) The distribution of nodal sprouts in a paralysed or partly denervated mouse muscle. Neuroscience, 7:37-44.
45. Jacobs, J.M. (1984) Toxic effects on the node of Ranvier. In: The Node of Ranvier. J.C. Zagoren, and S. Fedoroff, eds. Academic Press, New York, pp. 245-272.
46. Janetzko, A., Zimmermann, H., and Volknandt, W. (1989) Intraneuronal distribution of a synaptic vesicle membrane protein: Antibody binding sites at axonal membrane compartments and trans-Golgi network and accumulation at nodes of Ranvier. Neuroscience, 32: 65-77.
47. Jessen, K.R., and Mirsky, R. (1992) Schwann cells: Early lineage, regulation of proliferation and control of myelin formation. Curr. Opin. Neurobiol., 2:575-581.
48. Jessen, K.R., Mirsky, R., and Morgan, L. (1991) Role of cyclic AMP and proliferation controls in Schwann cell differentiation. Ann. N.Y. Acad. Sci., 633:78-89.
49. Jessen, K.R., Brennan, A., Morgan, L., Mirsky, R., Kent, A., Hashimoto, Y., and Gavrilovic, J. (1994) The Schwann cell precursor and its fate: A study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron, 12:509-527.
50. Landon, D.N., and Hall, S. (1976) The myelinated nerve fibre. In: The Peripheral Nerve. D.N. London, ed. Chapman and Hall, London, pp. 1-105.
51. Landon, D.N., and Langley, O.K. (1971) The local chemical environment of nodes of Ranvier: A study of cation binding. J. Anat. (Lond.), 108:419-432.
52. Livingstone, R.B., Pfenninger, K., Moor, H., and Akert, K. (1973) Specialized paranodal and interparanodal glial-axonal junctions in the peripheral and central nervous system: A freeze-etching study. Brain Res., 58:1-24.
53. Martini, R. (1994) Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol., 23: 1-28.
54. Mata, M., Kupina, N., and Fink, D.J. (1992) Phosphorylation dependent neurofilament epitopes are reduced at the node of Ranvier. J. Neurocytol., 21:199-210.
55. McQuarrie, I.G. (1985) Effect of a conditioning lesion on axonal sprout formation at nodes of Ranvier. J. Comp. Neurol., 231:239-249.
56. Neuberger, T.J., and DeVries, G.H. (1992) Axonal contact as a determinant of oligodendrocyte and Schwann cell function. In: Myelin: Biology and Chemistry. R.E. Martenson, ed. Boca Raton, FL, CRC Press, pp. 173-193.
57. Nilsson, I. (1988) Proliferation of Schwann cells in a developing feline lumbar ventral root. Dev. Brain Res., 38:1-7.
58. Nilsson, I., and Berthold, C.-H. (1988) Axon classes and internodal growth in the ventral spinal root L7 of adult and developing cats. J. Anat., 156:71-96.
59. Price, D.L., and Griffin, J.W. (1980) Neurons and ensheathing cells as targets of disease processes. In: Experimental and Clinical Neurotoxicology. P.S. Spencer and H.H. Schaumburg, eds. Williams and Wilkins, pp. 2-23.
60. Quick, D.C., and Waxman, S.G. (1977) Specific staining of the axon membrane at nodes of Ranvier with ferric ion and ferrocyanide. J. Neurol. Sci., 31:1-12.
61. Raine, C.S., Finch, H., and Masone, A. (1983) Axoplasmic asymmetry at the node of Ranvier. J. Neurocytol., 12:533-536.
62. Reles, A., and Friede, R.L. (1991) Axonal cytoskeleton at the nodes of Ranvier. J. Neurocytol., 20:450-458.
63. Remahl, S., Cullheim, S., and Ulfhake, B. (1985) Dimensions and branching patterns of triceps surae alpha-motor axons and their recurrent axon collaterals in the spinal cord during the postnatal development of the cat. Dev. Brain Res., 23:193-200.
64. Rieger, F., Daniloff, J.K., Pincon-Raymond, M., Crossin, K.L., Grumet, M., and Edelman, G.M. (1986) Neuronal cell adhesion molecules and cytotactin are colocalized at the node of Ranvier. J. Cell Biol., 103:379-391.
65. Risling, M., Hildebrand, C., and Aldskogius, H. (1981) Postnatal increase of unmyelinated axon profiles in the feline ventral root L7. J. Comp. Neurol., 201:343-351.
66. Rogart, R. (1984) Structural and functional relationships of ion conduction in the myelinated and demyelinated axon. In: The Node of Ranvier. J.C. Zagoren and S. Fedoroff, eds. Academic Press, New York, pp. 109-152.
67. Rosenbluth, J. (1984) Membrane specializations at the nodes of Ranvier and paranodal and juxtaparanodal regions of myelinated central and peripheral nerve fibers. In: The Node of Ranvier. J.C. Zagoren, and S. Fedoroff, eds. Academic Press, New York, pp. 31-67.
68. Rushton, W.A.H. (1951) A theory on the effects of fiber size in medullated nerve. J. Physiol. (London), 115:101-122.
69. Rydmark, M., and Berthold, C.-H. (1983) Electron microscopic serial section analysis of nodes of Ranvier in lumbar spinal roots of the cat. A morphometric study of nodal compartments in fibres of different sizes. J. Neurocytol. 12:537-565.
70. Schnapp, B., and Mugnaini, E. (1978) Membrane architecture of myelinated fibers as seen by freeze-fracture. In: Physiology and Pathobiology of Axons. S.G. Waxman, ed. Raven Press, New York, pp. 83-123.
71. Skoglund, S. (1966) Muscle afferents and motor control in the kitten. In: Muscular Afferents and Motor Control, Nobel Symposium I.R. Granit, ed. Almquist & Wiksell, Stockholm, pp. 245-259.
72. Skoglund, S. (1969) Growth and differentiation with special emphasis on the central nervous system. Ann. Rev. Physiol., 31:19-42.
73. Skoglund, S., and Romero, C. (1965) Postnatal growth of spinal nerves and roots. A morphological study in the cat with physiological correlations. Acta Physiol. Scand. 66, Suppl. 260.
74. Smith, R.S. (1980) The short term accumulation of axonally transported organelles in the region of localized lesions of single myelinated axons. J. Neurocytol., 9:39-65.
75. Smith, R.S. (1989) Real-time imaging of axonally transported subresolution organelles in vertebrate myelinated axons. J. Neurosci. Meth., 26:203-209.
76. Snyder, R.E. (1989) Loss of material from the retrograde axonal transport system in frog sciatic nerve. J. Neurobiol., 20:81-94.
77. Spencer, P.S., and Thomas, P.K. (1974) Ultrastructural studies of the dying-back process II. The sequestration and removal by Schwann cells and oligodendrocytes of organelles from normal and diseased axons. J. Neurocytol. 3:763-783.
78. Svärd, C., Berthold, C.-H., Nilsson-Remahl, I., and Rydmark, M. (1995) Axonal constriction at Ranvier's node increases during development. Neurosci. Lett., 190:159-162.
79. Tao-Cheng, J.-H., and Rosenbluth, J. (1983) Axolemmal differentiation in myelinated fibers of rat peripheral nerves. Dev. Brain Res., 9:251-263.
80. Thomas, P.K., Berthold, C.-H., and Ochoa, J. (1993) Microscopic anatomy of the peripheral nervous system. In: Peripheral Neuropathy. Third edition. P.J. Dyck, and P.K. Thomas, eds. W.B. Saunders Company, Philadelphia, pp. 28-91.
81. Tsukita, S., and Ishikawa, H. (1980) The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J. Cell Biol., 84: 513-530.
82. Vignal, W. (1883a) Memoire sur le developpement des tubes nerveux chez les embryons de mammiferes. Archs Physiol., 15:513-533.
83. Vignal, W. (1883b) Accroissement en longeur des tubes nerveux par la formation des segments intercalaires. Arch. Physiol., 15:536-548.
84. Vizoso, A.D., and Young, J.Z. (1948) Internode length and fiber diameter in developing and regenerating nerves. J. Anat. (London), 82: 110-134.
85. Waxman, S.G. (1987) Rules governing membrane reorganization and axon-glial interactions during the development of myelinated fibers. In: Progress in Brain Research, Vol. 71. F.J. Seil, E. Herbert, and B.M. Carlson, eds. Elsevier Science Publishers B.V., New York, pp. 121-141.
86. Waxman, S.G., and Ritchie, J.M. (1993) Molecular dissection of the myelinated axon. Ann. Neurol., 33:121-136.
87. Webster, H. deF. (1962) Transient, focal accumulation of axonal mitochondria during the early stages of Wallerian degeneration. J. Cell Biol. 12:361-375.
88. Webster, H. deF. (1993) Development of peripheral nerve fibers. In: Peripheral Neuropathy. Third edition. P.J. Dyck, and P.K. Thomas, eds. W.B. Saunders company, Philadelphia, pp. 243-266.
89. Wiley, C.A., and Ellisman, M.H. (1980) Rows of dimeric-particles within the axolemma and juxtaposed particles within glia, incorporated into a new model for the paranodal glial-axonal junction at the node of Ranvier. J. Cell Biol., 84:261-280.
90. Wiley-Livingston, C.A., and Ellisman, M. (1980) Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration. Dev. Biol. 79:334-355.
91. Williams, P.L., and Hall, S.M. (1971) Prolonged in vivo observations of normal peripheral nerve fibres and their acute reactions to crush and deliberate trauma. J. Anat., 108:397-408.
92. Yates, A.J., Bouchard, J.-P., and Wherrett, J.R. (1976) Relation of axon membrane to myelin membrane in sciatic nerve during development: Comparison of morphological and chemical parameters. Brain Res., 104:261-271.
93. Young, J.Z. (1945) History of the shape of a nerve fiber. In: Essays on Growth and Form. W.E. Le Gros Clark and P.B. Medawar, eds. Clarendon Press, Oxford, pp. 41-93.
94. Zagoren, J.C. (1984) Cation binding at the node of Ranvier. In: The Node of Ranvier. J.C. Zagoren, and S. Fedoroff, eds. Academic Press, New York, pp. 69-91.
95. Zimmermann, H., and Vogt, M. (1989) Membrane proteins and synaptic vesicles and cytoskeletal specializations at the node of Ranvier in electric ray and rat. Cell Tissue Res., 258:617-629.