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Chromatolysis of dorsal root ganglion cells studied by cryofixation

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Summary

Cytoskeletal alterations in the cytoplasm of chromatolytic neurons of the dorsal root ganglia were studied in chickens after transection of the sciatic nerves. These studies were carried out using cryofixation with a nitrogencooled propane jet. By this method, the morphological complexity of the cytoskeleton in normal perikarya and cell processes can be visualized. The cytoskeleton of the dorsal root ganglion cells (DRG) is composed of an intricate network of microtubules, neurofilaments and microfilaments. The membrane-bounded cell organelles, as well as the cell nucleus and the plasmalemma, are linked to the microtubules and neurofilaments by microfilaments (or crosslinkers). As a result of the transection of the axon, chromatolysis takes place, characterized by dislocation of cell organelles, ↭ eccentric position of the nucleus and dispersion of the parallel cisternae of the rough endoplasmic reticulum throughout the cytoplasm. This characteristic phenomenon coincides with a regression of the neurocytoskeletal network. The neurofilaments and microtubules become shorter, and the microfilaments are replaced by strands of globular or granular material. The temporary regression of the microfilaments leads to a dispersion of the cell organelles. During the remodelling of the cytoskeletal structures, proliferation of the neurofilaments in the regenerating neurons may occasionally be observed. These results show that the cytoskeletal structures are responsible not only for the preservation of cell shape, but also for the maintenance of the normal distributional pattern (location and mobility) of the intracellular components.

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References

  • Andres KH (1961) Untersuchungen über morphologische Veränderungen in Spinalganglien während der retrograden Degeneration. Z Zellforsch 55:49–79

    Google Scholar 

  • Bray D (1976) Actin and Myosin: Their role in the growth of nerve cells. Biochem Soc Trans 4:543–544

    Google Scholar 

  • Bray D (1977) Actin and myosin in neurones: a first review. Biochimie 59:1–6

    Google Scholar 

  • Brodal A (1982) Anterograde and retrograde degeneration of nerve cells in the central nervous system. In: Haymaker W, Adams RD (eds) Histology and Histopathology of the Nervous System. Vol. 1. Charles C. Thomas Publisher, Springfield, Illinois, USA, pp 276–362

    Google Scholar 

  • Carbonetto S, Muller KJ (1982) Nerve fiber growth and the cellular response to axotomy. Curr Top Dev Biol 17:33–76

    Google Scholar 

  • Evans DHL, Gray EG (1961) Changes in the fine structure of ganglion cells during chromatolysis. Proc Anat Soc Great Britain and Ireland 1961:71–74

    Google Scholar 

  • Fifkova E (1985a) A possible mechanism of morphometric changes in dendritic spines induced by stimulation. Cell Mol Neurobiol 5:47–63

    Google Scholar 

  • Fifkova E (1985b) Actin in the nervous system. Brain Res Rev 9:187–215

    Google Scholar 

  • Fifkova E, Delay RJ (1982) Cytoplasmic actin in neuronal processas a possible mediator of synaptic plasticity. J Cell Biol 95:345–350

    Google Scholar 

  • Grafstein B (1975) The nerve cell body response to axotomy. Exp Neurol 48: No. 3: Part 2:32–51

    Google Scholar 

  • Grafstein B, McQuarrie IG (1978) The role of the nerve cell body in axonal regeneration. In: Cotman CW (ed) Neuronal Plasticity. Raven Press, New York, pp 155–195

    Google Scholar 

  • Gray EG (1975) Synaptic fine structure and nuclear, cytoplasmic and extracellular networks. The stereoframework concept. J Neurocytol 4:315–339

    Google Scholar 

  • Hillman DE (1969) Neuronal organization of the cerebellar cortex in Amphibia and Reptilia. In: Llinas R (ed) Neurobiology of Cerebellar Evolution and Development. American Medical Association, Chicago, III., pp 279–325

    Google Scholar 

  • Hirokawa N (1982) Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J Cell Biol 94:129–142

    Google Scholar 

  • Hirokawa N, Glicksman MA, Willard MB (1984) Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J Cell Biol 98:1523–1436

    Google Scholar 

  • Hirokawa N, Bloom GS, Vallee RB (1985) Cytoskeletal architecture and immunocytochemical localization of microtubule-associated proteins in regions of axons associated with rapid axonal transport: The β,‚β’-iminodipropionitrile-intoxicated axon as a model system. J Cell Biol 101:227–239

    Google Scholar 

  • Hoffman PN, Griffin JW, Price DL (1984) Control of axonal caliber by neurofilament transport. J Cell Biol 99:705–714

    Google Scholar 

  • Hoffman PN, Thompson GW, Griffin JW, Price DL (1985) Changes in neurofilament transport coincide temporally with alterations in the caliber of axons in regenerating motor fibers. J Cell Biol 101:1332–1340

    Google Scholar 

  • Kreutzberg GW (1972) neural degeneration and regeneration. In: Minckler J (ed) Pathology of the Nervous System. Vol. III. McGraw Hill, New York, p 2678–2687

    Google Scholar 

  • Kreutzberg GW (1982) Acute neural reaction to injury. In: Nicholls JG (ed) Repair and Regeneration of the Nervous System. Springer, Berlin Heidelberg New York, pp 57–69

    Google Scholar 

  • Lasek RJ, Oblinger MM, Drake PF (1983) Molecular biology of neuronal geometry: Expression of neurofilament genes influences axonal diameter. Cold Spring Harbor Symp Quant Biol 48:731–744

    Google Scholar 

  • LeBeux YJ, Willemot J (1975) An ultrastructural study of the microfilaments in rat brain by means of heavy meromyosin labeling. I. The perikaryon, the dendrites and the axon. Cell Tissue Res 160:1–36

    Google Scholar 

  • Letourneau PC (1983) Differences in the organization of actin in the growth cones compared with the neurites of cultured neurons from chick embryos. J Cell Biol 97:963–973

    Google Scholar 

  • Lieberman AR (1974) Some factors affecting retrograde neuronal responses to axonal lesions. In: Bellairs R, Gray EG (eds) Essays on the Nervous System. A. Festschrift for Prof. J.Z. Young. Clarendon Press, Oxford, pp 71–105

    Google Scholar 

  • Mackey EA, Spiro D, Wiener J (1964) A study of chromatolysis in dorsal root ganglia at the cellular level. J Neuropathol Exp Neurol 23:508–526

    Google Scholar 

  • Margaritis LH, Elgsaeter A, Branton D (1977) Rotary replication for freeze-etching. J Cell Biol 72:47–56

    Google Scholar 

  • Markham JA, Fifkova E (1986) Actin filament organization within dendrites and dendritic spines during development. Dev Brain Res 27:263–269

    Google Scholar 

  • Matus A, Ackermann M, Pehling G, Byers HR, Fujiwara K (1982) High actin concentrations in brain dendritic spines and postsynaptic densities. Proc Natl Acad Sci USA 79:7590–7594

    Google Scholar 

  • Meller K (1985) Ultrastructural aspects of cryofixed nerves. Cell Tissue Res 242:289–300

    Google Scholar 

  • Meller K (1987a) The cytoskeleton of cryofixed Purkinje cells of the chicken cerebellum. Cell Tissue Res 247:155–165

    Google Scholar 

  • Meller K (1987b) Early structural changes in the axoplasmic cytoskeleton after axotomy studied by cryofixation. Cell Tissue Res 250:663–672

    Google Scholar 

  • Metuzals J, Hodge AJ, Lasek RJ, Kaiserman-Abramof IR (1983) Neurofilamentous network and filamentous matrix preserved and isolated by different techniques from squid giant axon. Cell Tissue Res 228:415–432

    Google Scholar 

  • Moor H, Kistler J, Müller M (1976) Freezing in a propane jet. Experientia 32:805

    Google Scholar 

  • Nissl F (1892) Über die Veränderungen der Ganglienzellen am Facialiskern des Kaninchens nach Ausreißung der Nerven. Allg Z Psychiat 48:197–198

    Google Scholar 

  • Pannese E (1963) Investigations on the ultrastructural changes of the spinal ganglion neurons in the course of axon regeneration and cell hypertrophy. I. Changes during axon regeneration. Z Zellforsch 60:711–740

    Google Scholar 

  • Porter KR (1984) The cytomatrix: A short history of its study. J Cell Biol 99:3s-12s

    Google Scholar 

  • Porter KR, Tucker JB (1981) The ground substance of the living cell. Sci Am 244:40–51

    Google Scholar 

  • Porter KR, Anderson KL (1982) The structure of the cytoplasmic matrix preserved by freeze-drying and freeze-substitution. Eur J Cell Biol 29:83–96

    Google Scholar 

  • Porter KR, McNiven MA (1982) The cytoplast: A unit structure in chromatophores. Cell 29:23–32

    Google Scholar 

  • Schlaepfer WW (1977) Immunological and ultrastructural studies of neurofilaments isolated from rat peripheral nerve. J Cell Biol 74:226–240

    Google Scholar 

  • Schlaepfer WW, Freeman LA (1978) Neurofilament proteins of rat peripheral nerve and spinal cord. J Cell Biol 78:653–662

    Google Scholar 

  • Schlaepfer WW, Micko S (1978) Chemical and structural changes of neurofilaments in transected rat sciatic nerve. J Cell Biol 78:369–378

    Google Scholar 

  • Schnapp BJ, Reese TS (1982) Cytoplasmic structure in rapidfrozen axons. J Cell Biol 94:667–679

    Google Scholar 

  • Tsukita S, Usukura J, Tsukita S, Ishikawa H (1982) The cytoskeleton in myelinated axons: A freeze-etch replica study. Neuroscience 7:2135–2147

    Google Scholar 

  • Venable JH, Coggeshall R (1964) A simplified lead-citrate stain for use in electron microscopy. J Cell Biol 25:407–408

    Google Scholar 

  • Wolosewick JJ, Porter KR (1976) Stereo high-voltage electron microscopy of whole cells of the human diploid line, Wi-38. Am J Ant 147:303–324

    Google Scholar 

  • Wolosewick JJ, Porter KR (1979) Microtrabecular lattice of the cytoplasmic ground substance. Artifact or reality. J Cell Biol 82:114–139

    Google Scholar 

Download references

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  1. Institut für Anatomie, Abteilung für Cytologie, Ruhr-Universitä t, Bochum, Germany

    Karl Meller

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  1. Karl Meller
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Meller, K. Chromatolysis of dorsal root ganglion cells studied by cryofixation. Cell Tissue Res. 256, 283–292 (1989). https://doi.org/10.1007/BF00218885

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