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. 1987 Oct;154:201–214.

Intranuclear inclusions in Schwann cells of aged fowl ciliary ganglia.

M G Fiori 1
PMCID: PMC1261846  PMID: 2833482

Abstract

Schwann cells in ciliary ganglia of fowls aged five to seven years were found to contain numerous intranuclear inclusions and pseudo-inclusions. Similar inclusions were usually absent from both neurons and non-neuronal cells, including connective tissue cells, and were rare in Schwann cells of chickens aged less than five years. Inclusions were of two different types: filamentous bundles and granulofibrillar bodies. Individual nuclei contained one to three inclusions. Pseudo-inclusions, i.e. cytoplasmic pockets invaginated into the nuclei, were found more rarely and accompanied one or both types of 'true' inclusions. The possible significance of these findings in relation to ageing phenomena is discussed. It is concluded that intranuclear inclusions appear to be a consequence of nuclear/cellular activation and may be regarded as aggregates of previously dispersed intranuclear proteins.

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Selected References

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

  1. Bianchi R., Gioia M. Morpho-quantitative analysis of nuclear inclusions in periaqueductal grey matter neurons in the cat. J Anat. 1985 Jan;140(Pt 1):159–164. [PMC free article] [PubMed] [Google Scholar]
  2. Bourgeois C. A., Hemon D., Bouteille M. Structural relationship between the nucleolus and the nuclear envelope. J Ultrastruct Res. 1979 Sep;68(3):328–340. doi: 10.1016/s0022-5320(79)90165-5. [DOI] [PubMed] [Google Scholar]
  3. Bouteille M., Kalifat S. R., Delarue J. Ultrastructural variations of nuclear bodies in human diseases. J Ultrastruct Res. 1967 Aug 30;19(5):474–486. doi: 10.1016/s0022-5320(67)80074-1. [DOI] [PubMed] [Google Scholar]
  4. Brion J. P., Couck A. M., Flament-Durand J. Intranuclear inclusions in the neurons of senescent rats. Acta Neuropathol. 1982;58(2):107–110. doi: 10.1007/BF00691649. [DOI] [PubMed] [Google Scholar]
  5. Burns E. R., Soloff B. L., Hamma C., Buxton D. F. Nuclear pockets associated with the nucleolus in normal and neoplastic cells. Cancer Res. 1971 Feb;31(2):159–165. [PubMed] [Google Scholar]
  6. Cantino D., Mugnaini E. Adrenergic innervation of the parasympathetic ciliary ganglion in the chick. Science. 1974 Jul 19;185(4147):279–281. doi: 10.1126/science.185.4147.279. [DOI] [PubMed] [Google Scholar]
  7. Cantino D., Mugnaini E. The structural basis for electrotonic coupling in the avian ciliary ganglion. A study with thin sectioning and freeze-fracturing. J Neurocytol. 1975 Oct;4(5):505–536. doi: 10.1007/BF01351535. [DOI] [PubMed] [Google Scholar]
  8. Chandler R. L., Willis R. An intranuclear fibrillar lattice in neurons. J Cell Sci. 1966 Sep;1(3):283–286. doi: 10.1242/jcs.1.3.283. [DOI] [PubMed] [Google Scholar]
  9. Coquet M., Vallat J. M., Vital C., Fournier M., Barat M., Orgogozo J. M., Julien J., Loiseau P. Nuclear inclusions in oculopharyngeal dystrophy. An ultrastructural study of six cases. J Neurol Sci. 1983 Jul;60(1):151–156. doi: 10.1016/0022-510x(83)90134-x. [DOI] [PubMed] [Google Scholar]
  10. Costa C. B., Paula-Barbosa M. M. Nuclear inclusions in the nerve cells of the sphenopalatine ganglion of the dog. Cell Tissue Res. 1979 Sep 3;201(2):289–294. doi: 10.1007/BF00235064. [DOI] [PubMed] [Google Scholar]
  11. Curcio C. A., McNelly N. A., Hinds J. W. Intranuclear inclusions in rat piriform cortex: increase with age and preferential location within superficial layer II. Anat Rec. 1984 Dec;210(4):657–662. doi: 10.1002/ar.1092100413. [DOI] [PubMed] [Google Scholar]
  12. Dahl E. The fine structure of nuclear inclusions. J Anat. 1970 Mar;106(Pt 2):255–262. [PMC free article] [PubMed] [Google Scholar]
  13. David S., Nathaniel E. J. Intranuclear inclusions in the developing neurons of the rat cuneate nuclei. Cell Tissue Res. 1978 Oct 30;193(3):525–532. doi: 10.1007/BF00225348. [DOI] [PubMed] [Google Scholar]
  14. DeLellis R. A., Suchow E., Wolfe H. J. Ultrastructure of nuclear "inclusions" in pheochromocytoma and paraganglioma. Hum Pathol. 1980 Mar;11(2):205–207. doi: 10.1016/s0046-8177(80)80147-x. [DOI] [PubMed] [Google Scholar]
  15. Feldman M. L., Peters A. Intranuclear rods and sheets in rat cochlear nucleus. J Neurocytol. 1972 Sep;1(2):109–127. doi: 10.1007/BF01099179. [DOI] [PubMed] [Google Scholar]
  16. Fernandez B., Suarez I., Gutierrez C. Intranuclear inclusions in hypothalamic neurons: a study in the ageing hamster. J Submicrosc Cytol. 1984 Jul;16(3):495–501. [PubMed] [Google Scholar]
  17. Field E. J., Peat A. Intranuclear inclusions in neurones and glia: a study in the ageing mouse. Gerontologia. 1971;17(3):129–138. doi: 10.1159/000211816. [DOI] [PubMed] [Google Scholar]
  18. Fiori M. G., Mugnaini E. Microglia-like cells in the chicken ciliary ganglion. Neuroscience. 1981;6(4):667–677. doi: 10.1016/0306-4522(81)90150-0. [DOI] [PubMed] [Google Scholar]
  19. Fitzgerald M., Padykula H. A. Differing functional responses of simple and complex nuclear bodies in uterine luminal epithelial cells following estrogenic stimuli. Anat Rec. 1983 Feb;205(2):131–141. doi: 10.1002/ar.1092050204. [DOI] [PubMed] [Google Scholar]
  20. Flaks B., Flaks A. Fine structure of nuclear inclusions in murine pulmonary tumor cells. Cancer Res. 1970 May;30(5):1437–1443. [PubMed] [Google Scholar]
  21. Gambetti P., Gonatas N. K. Fibrils and lattice-like intranuclear structures in nuclei of neurons. Riv Patol Nerv Ment. 1967 Mar-Apr;88(2):188–196. [PubMed] [Google Scholar]
  22. Gibson P. H. Electron microscopic study of intranuclear spheres of Bouteille type-III in astrocytes with special reference to liver carcinoma. Neuropathol Appl Neurobiol. 1982 Sep-Oct;8(5):413–418. doi: 10.1111/j.1365-2990.1982.tb00309.x. [DOI] [PubMed] [Google Scholar]
  23. Glant M. D., Berger E. K., Davey D. D. Intranuclear cytoplasmic inclusions in aspirates of follicular neoplasms of the thyroid. A report of two cases. Acta Cytol. 1984 Sep-Oct;28(5):576–580. [PubMed] [Google Scholar]
  24. Graham A. R., Payne C. M., Nagle R. B. A quantitative light- and electron-microscopic study of type IV nuclear bodies in crescentic glomerulonephritis. Am J Pathol. 1981 Mar;102(3):359–366. [PMC free article] [PubMed] [Google Scholar]
  25. Grunnet M. L. Nuclear bodies in Creutzfeldt-Jakob and Alzheimer's diseases. Neurology. 1975 Nov;25(11):1091–1093. doi: 10.1212/wnl.25.11.1091. [DOI] [PubMed] [Google Scholar]
  26. Hirabayashi K., Shimokawa K., Ikeda K., Orthner H. Uber "Kernkugeln" in Nervenzellen des menschlichen Hypothalamus. J Hirnforsch. 1979;20(5):455–465. [PubMed] [Google Scholar]
  27. Ishizeki K., Tachibana T., Sakakura Y., Nawa T. Intranuclear inclusions in the bone marrow cells of miniature pigs. Arch Histol Jpn. 1981 Nov;44(5):467–476. doi: 10.1679/aohc1950.44.467. [DOI] [PubMed] [Google Scholar]
  28. Johnson J. E., Jr, Miquel J. Fine structural changes in the lateral vestibular nucleus of aging rats. Mech Ageing Dev. 1974 Sep-Oct;3(3-4):203–224. doi: 10.1016/0047-6374(74)90017-7. [DOI] [PubMed] [Google Scholar]
  29. LEDUC E. H., WILSON J. W. An electron microscope study of intranuclear inclusions in mouse liver and hepatoma. J Biophys Biochem Cytol. 1959 Dec;6:427–430. doi: 10.1083/jcb.6.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. LaVelle A., Buschmann M. T. Nuclear envelope invaginations in hamster facial motor neurons during development and aging. Brain Res. 1983 Nov;312(2):171–175. doi: 10.1016/0165-3806(83)90134-7. [DOI] [PubMed] [Google Scholar]
  31. Lafarga M., Crespo D., Villegas J. Nuclear inclusions in immature glial cells of the rat hypothalamus during the postnatal period. Anat Embryol (Berl) 1983;167(2):263–271. doi: 10.1007/BF00298515. [DOI] [PubMed] [Google Scholar]
  32. Landmesser L., Pilar G. Selective reinnervation of two cell populations in the adult pigeon ciliary ganglion. J Physiol. 1970 Nov;211(1):203–216. doi: 10.1113/jphysiol.1970.sp009275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mann G. Histological Changes induced in Sympathetic, Motor, and Sensory Nerve Cells by Functional Activity (Preliminary note). J Anat Physiol. 1894 Oct;29(Pt 1):100–108.1. [PMC free article] [PubMed] [Google Scholar]
  34. Marwitt R., Pilar G., Weakly J. N. Characterization of two ganglion cell populations in avian ciliary ganglia. Brain Res. 1971 Jan 22;25(2):317–334. doi: 10.1016/0006-8993(71)90441-0. [DOI] [PubMed] [Google Scholar]
  35. Masurovsky E. B., Benitez H. H., Kim S. U., Murray M. R. Origin, development, and nature of intranuclear rodlets and associated bodies in chicken sympathetic neurons. J Cell Biol. 1970 Jan;44(1):172–191. doi: 10.1083/jcb.44.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Masurovsky E. B., Fields K. L. Monoclonal antibodies binding to nuclear structures and axons in adult avian dorsal root ganglia. Biol Cell. 1984;51(3):407–410. doi: 10.1111/j.1768-322x.1984.tb00318.x. [DOI] [PubMed] [Google Scholar]
  37. Nosal G. Neuronal involution during ageing. Ultrastructural study in the rat cerebellum. Mech Ageing Dev. 1979 Jun;10(5):295–314. doi: 10.1016/0047-6374(79)90043-5. [DOI] [PubMed] [Google Scholar]
  38. Ota M., Offord K., Dyck P. J. Morphometric evaluation of first sacral ganglia of man. J Neurol Sci. 1974 May;22(1):73–82. doi: 10.1016/0022-510x(74)90055-0. [DOI] [PubMed] [Google Scholar]
  39. Padykula H. A., Pockwinse S. M. Uterine simple and complex nuclear bodies are separate structural entities. Anat Rec. 1983 Feb;205(2):119–130. doi: 10.1002/ar.1092050203. [DOI] [PubMed] [Google Scholar]
  40. Payne C. M., Nagle R. B. An ultrastructural study of intranuclear rodlets in a malignant extracranial neuroepithelial neoplasm. Ultrastruct Pathol. 1983 Jul;5(1):1–13. doi: 10.3109/01913128309141814. [DOI] [PubMed] [Google Scholar]
  41. Périer O., Vanderhaeghen J. J., Pelc S. Subacute sclerosing leuco-encephalitis. Electron microscopic finding in two cases with inclusion bodies. Acta Neuropathol. 1967 Jul 5;8(4):362–380. doi: 10.1007/BF00696673. [DOI] [PubMed] [Google Scholar]
  42. SIEGESMUND K. A., DUTTA C. R., FOX C. A. THE ULTRASTRUCTURE OF THE INTRANUCLEAR RODLET IN CERTAIN NERVE CELLS. J Anat. 1964 Jan;98:93–97. [PMC free article] [PubMed] [Google Scholar]
  43. Seite R., Leonetti J., Luciani-Vullet J., Vio M. Cyclic AMP and ultrastructural organization of the nerve cell nucleus: stimulation of nuclear microtubules and microfilaments assembly in sympathetic neurons. Brain Res. 1977 Mar 18;124(1):41–51. doi: 10.1016/0006-8993(77)90862-9. [DOI] [PubMed] [Google Scholar]
  44. Seite R., Mei N., Couineau S. Modification quantitative des bâtonnets intranucléaires des neurons sympathiques sous l'influence de la stimulation électrique. Brain Res. 1971 Nov;34(2):277–290. doi: 10.1016/0006-8993(71)90281-2. [DOI] [PubMed] [Google Scholar]
  45. Seite R., Vuillet-Luciani J., Zerbib R., Cataldo C., Escaig J., Pebusque M. J., Autillo-Touati A. Thee-dimensional organization of tubular and filamentous nuclear inclusions and associated structures in sympathetic neurons as revealed by serial sections and tilting experiments. J Ultrastruct Res. 1979 Nov;69(2):211–231. doi: 10.1016/s0022-5320(79)90111-4. [DOI] [PubMed] [Google Scholar]
  46. Seïte R., Mei N., Vuillet-Luciani J. Effect of electrical stimulation on nuclear microfilaments and microtubules of sympathetic neurons submitted to cycloheximide. Brain Res. 1973 Feb 28;50(2):419–423. doi: 10.1016/0006-8993(73)90744-0. [DOI] [PubMed] [Google Scholar]
  47. TERZUOLO C. Ricerche sul ganglio ciliare degli uccelli; connessioni, mutamenti in-relazione all'eta e dopo recisione delle fibre pregangliari. Z Zellforsch Mikrosk Anat. 1951;36(3):255–267. [PubMed] [Google Scholar]
  48. Tavares M. A., Paula-Barbosa M. M. Cerebellar intranuclear inclusions in chronically alcoholized rats. Cell Tissue Res. 1981;216(1):227–230. doi: 10.1007/BF00234558. [DOI] [PubMed] [Google Scholar]
  49. Thiele B., Mahrle G. Intranuclear tonofilament-like filaments in skin carcinoma. J Cutan Pathol. 1983 Jun;10(3):201–206. doi: 10.1111/j.1600-0560.1983.tb00327.x. [DOI] [PubMed] [Google Scholar]
  50. Toper S., Bannister C. M., Lincoln J., Mann D. M., Yates P. O. Nuclear inclusions in Alzheimer's disease. Neuropathol Appl Neurobiol. 1980 Jul-Aug;6(4):245–253. doi: 10.1111/j.1365-2990.1980.tb00209.x. [DOI] [PubMed] [Google Scholar]
  51. Topilko A., Zakrzewski A., Pichard E., Viron A. Ultrastructural cytochemistry of intranuclear dense granules in nasopharyngeal angiofibroma. Ultrastruct Pathol. 1984;6(2-3):221–228. doi: 10.3109/01913128409018576. [DOI] [PubMed] [Google Scholar]
  52. Uehara M., Ueshima T. Nuclear vacuoles and nuclear bodies in cells of chicken spinal cord. Anat Anz. 1984;156(4):337–340. [PubMed] [Google Scholar]
  53. Vallat J. M., Leboutet M. J., Loubet A., Corvisier N., Dumas M. Nonviral intranuclear inclusions in a nerve biopsy: an ultrastructural study. Muscle Nerve. 1983 Feb;6(2):167–169. doi: 10.1002/mus.880060215. [DOI] [PubMed] [Google Scholar]
  54. Vallat J. M., Vital C. Unusual nuclear inclusions in four nerve biopsies. An ultrastructural study. Biomedicine. 1980 Sep-Oct;33(5):153–156. [PubMed] [Google Scholar]
  55. Vital C., Vallat J. M., Deminiere C., Loubet A., Leboutet M. J. Peripheral nerve damage during multiple myeloma and Waldenstrom's macroglobulinemia: an ultrastructural and immunopathologic study. Cancer. 1982 Oct 15;50(8):1491–1497. doi: 10.1002/1097-0142(19821015)50:8<1491::aid-cncr2820500808>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
  56. Volk B., Maletz J. Nuclear inclusions following chronic ethanol administration. An electron-microscopic investigation of the rat parietal cortex. Acta Neuropathol. 1985;67(1-2):170–173. doi: 10.1007/BF00688140. [DOI] [PubMed] [Google Scholar]
  57. Vuillet-Luciani J., Vio M., Cataldo C., Seïte R. Frequency and distribution of tubulo-filamentous nuclear inclusions in the celiac ganglion of the cat as revealed by serial sections. Experientia. 1979 Mar 15;35(3):394–396. doi: 10.1007/BF01964373. [DOI] [PubMed] [Google Scholar]
  58. Welch W. J., Suhan J. P. Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol. 1985 Oct;101(4):1198–1211. doi: 10.1083/jcb.101.4.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Wergin W. P., Gruber P. J., Newcomb E. H. Fine structural investigation of nuclear inclusions in plants. J Ultrastruct Res. 1970 Mar;30(5):533–557. doi: 10.1016/s0022-5320(70)90051-1. [DOI] [PubMed] [Google Scholar]
  60. Wyatt R. B., Schochet S. S., Jr, McCormick W. F. Rhabdomyoma. Light and electron microscopic study of a case with intranuclear inclusions. Arch Otolaryngol. 1970 Jul;92(1):32–39. doi: 10.1001/archotol.1970.04310010058006. [DOI] [PubMed] [Google Scholar]
  61. Yasuzumi F., Sakamoto H., Mii Y., Yabumoto N., Yasuzumi G. Electron microscopic cytochemical analysis of paracrystalline intranuclear inclusions in human osteosarcoma cells. Okajimas Folia Anat Jpn. 1982 Mar;58(4-6):369–382. doi: 10.2535/ofaj1936.58.4-6_369. [DOI] [PubMed] [Google Scholar]
  62. Yasuzumi G., Yabumoto N., Shirai T., Nakai Y., Yasuzumi F. Functions of nuclear bodies as revealed by ultrastructural autoradiography and cytochemistry. Experientia. 1981 Oct 15;37(10):1072–1073. doi: 10.1007/BF02085016. [DOI] [PubMed] [Google Scholar]
  63. de THE, RIVIERE M., BERNHARD W. [Examination by electron microscope of the VX2 tumor of the domestic rabbit derived from the Shope papilloma]. Bull Assoc Fr Etud Cancer. 1960 Oct-Dec;47:570–584. [PubMed] [Google Scholar]

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