Skip to main content
NCBI home page
Journal of Anatomy logoLink to Journal of Anatomy
. 1987 Oct;154:215–227.

Origin and fate of neural macrophages in a stab wound of the brain of the young rat.

C Kaur 1, E A Ling 1, W C Wong 1
PMCID: PMC1261847  PMID: 3446660

Abstract

Colloidal carbon was injected intravenously into young rats to label circulating monocytes before making a stab wound in the brain. The rats were killed 3-16 days after the stab wound. Demonstration of non-specific esterase, thiamine pyrophosphatase and 5'-nucleotidase was carried out on the carbon-labelled macrophages at the site of lesion at various survival times. In rats killed 3-5 days after the injury numerous carbon-labelled macrophages were present in the needle passage as well as in the marginal area of the lesion and they showed a positive reaction for non-specific esterase. The reaction of the enzyme was found in some of the dense bodies in the form of punctate precipitates. The reaction for thiamine pyrophosphatase was seen in the Golgi saccules as well as on the plasma membrane, although in the latter the reaction was weaker. Intense reaction for 5'-nucleotidase was localised over the plasma membrane as well as over the dense bodies. The carbon-labelled macrophages displaying the activities of the above enzymes in the 3-5 days postoperative group were of the round type. However, in the 8-16 postoperative days animals, the cells were either oval or had assumed an elongated outline resembling the microglial cells seen in the tissue taken from the normal side. It is concluded that circulating monocytes are a main source of brain macrophage in traumatic brain lesions. In the healing process of the wound some of the cells regress to become microglial cells as shown by the presence of the carbon particles as well as non-specific esterase, thiamine pyrophosphatase and 5'-nucleotidase activity in the various stages of structural transformation.

Full text

PDF
215

Images in this article

218Fig. 1
on p.218
218Fig. 2
on p.218
219Fig. 3
on p.219
219Fig. 4
on p.219
220Fig. 5
on p.220
220Fig. 6
on p.220
221Fig. 7
on p.221
221Fig. 8
on p.221

Selected References

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

  1. ADRIAN E. K., Jr, WALKER B. E. Incorporation of thymidine-H3 by cells in normal and injured mouse spinal cord. J Neuropathol Exp Neurol. 1962 Oct;21:597–609. doi: 10.1097/00005072-196210000-00007. [DOI] [PubMed] [Google Scholar]
  2. Adrian E. K., Jr, Smothermon R. D. Leucocytic infiltration into the hypoglossal nucleus following injury to the hypoglossal nerve. Anat Rec. 1970 Jan;166(1):99–115. doi: 10.1002/ar.1091660108. [DOI] [PubMed] [Google Scholar]
  3. Adrian E. K., Jr, Williams M. G. Cell proliferation in injured spinal cord. An electron microscopic study. J Comp Neurol. 1973 Sep 1;151(1):1–24. doi: 10.1002/cne.901510102. [DOI] [PubMed] [Google Scholar]
  4. Adrian E. K., Jr, Williams M. G., George F. C. Fine structure of reactive cells in injured nervous tissue labeled with 3H-thymidine injected before injury. J Comp Neurol. 1978 Aug 15;180(4):815–839. doi: 10.1002/cne.901800412. [DOI] [PubMed] [Google Scholar]
  5. Berner A., Torvik A., Stenwig A. E. Origin of macrophages in traumatic lesions and Wallerian degeneration in peripheral nerves. Acta Neuropathol. 1973;25(3):228–236. doi: 10.1007/BF00685202. [DOI] [PubMed] [Google Scholar]
  6. Booz K. H., Felsing T. Uber ein transitorisches, perinatales subependymales Zellsystem der weissen Ratte. Z Anat Entwicklungsgesch. 1973;141(3):275–288. [PubMed] [Google Scholar]
  7. FIELD E. J. Observations on the development of microglia together with a note on the influence of cortisone. J Anat. 1955 Apr;89(2):201–208. [PMC free article] [PubMed] [Google Scholar]
  8. Fernando D. A. A third glial cell seen in retrograde degeneration of the hypoglossal nerve. Brain Res. 1971 Apr 2;27(2):365–368. doi: 10.1016/0006-8993(71)90262-9. [DOI] [PubMed] [Google Scholar]
  9. Horwitz D. A., Allison A. C., Ward P., Kight N. Identification of human mononuclear leucocyte populations by esterase staining. Clin Exp Immunol. 1977 Nov;30(2):289–298. [PMC free article] [PubMed] [Google Scholar]
  10. Huntington H. W., Terry R. D. The origin of the reactive cells in cerebral stab wounds. J Neuropathol Exp Neurol. 1966 Oct;25(4):646–653. doi: 10.1097/00005072-196610000-00010. [DOI] [PubMed] [Google Scholar]
  11. Imamoto K., Fujiwara R., Nagai T., Maeda T. Distribution and fate of macrophagic ameboid cells in the rat brain. Arch Histol Jpn. 1982 Dec;45(5):505–518. doi: 10.1679/aohc.45.505. [DOI] [PubMed] [Google Scholar]
  12. Imamoto K., Leblond C. P. Presence of labeled monocytes, macrophages and microglia in a stab wound of the brain following an injection of bone marrow cells labeled with 3H-uridine into rats. J Comp Neurol. 1977 Jul 15;174(2):255–279. doi: 10.1002/cne.901740205. [DOI] [PubMed] [Google Scholar]
  13. Innocenti G. M., Clarke S., Koppel H. Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways. Brain Res. 1983 Dec;313(1):55–66. doi: 10.1016/0165-3806(83)90201-8. [DOI] [PubMed] [Google Scholar]
  14. Innocenti G. M., Koppel H., Clarke S. Transitory macrophages in the white matter of the developing visual cortex. I. Light and electron microscopic characteristics and distribution. Brain Res. 1983 Dec;313(1):39–53. doi: 10.1016/0165-3806(83)90200-6. [DOI] [PubMed] [Google Scholar]
  15. KONIGSMARK B. W., SIDMAN R. L. ORIGIN OF BRAIN MACROPHAGES IN THE MOUSE. J Neuropathol Exp Neurol. 1963 Oct;22:643–676. doi: 10.1097/00005072-196310000-00006. [DOI] [PubMed] [Google Scholar]
  16. Kaplow L. S. Cytochemical heterogeneity of human circulating monocytes. Acta Cytol. 1975 Jul-Aug;19(4):358–365. [PubMed] [Google Scholar]
  17. Kaur C., Ling E. A., Wong W. C. Cytochemical localisation of 5'-nucleotidase in amoeboid microglial cells in postnatal rats. J Anat. 1984 Aug;139(Pt 1):1–7. [PMC free article] [PubMed] [Google Scholar]
  18. Kaur C., Ling E. A., Wong W. C. Localisation of thiamine pyrophosphatase in the amoeboid microglial cells in the brain of postnatal rats. J Anat. 1987 Jun;152:13–22. [PMC free article] [PubMed] [Google Scholar]
  19. Kaur C., Ling E. A., Wong W. C. Transformation of amoeboid microglial cells into microglia in the corpus callosum of the postnatal rat brain. An electron microscopical study. Arch Histol Jpn. 1985 Feb;48(1):17–25. doi: 10.1679/aohc.48.17. [DOI] [PubMed] [Google Scholar]
  20. Kerns J. M., Hinsman E. J. Neuroglial response to sciatic neurectomy. I. Light microscopy and autoradiography. J Comp Neurol. 1973 Oct 1;151(3):237–254. doi: 10.1002/cne.901510303. [DOI] [PubMed] [Google Scholar]
  21. Kerns J. M., Hinsman E. J. Neuroglial response to sciatic neurectomy. II. Electron microscopy. J Comp Neurol. 1973 Oct 1;151(3):255–280. doi: 10.1002/cne.901510304. [DOI] [PubMed] [Google Scholar]
  22. Kitamura T., Hattori H., Fujita S. Autoradiographic studies on histogenesis of brain macrophages in the mouse. J Neuropathol Exp Neurol. 1972 Jul;31(3):502–518. doi: 10.1097/00005072-197207000-00008. [DOI] [PubMed] [Google Scholar]
  23. Kreutzberg G. W., Barron K. D. 5'-Nucleotidase of microglial cells in the facial nucleus during axonal reaction. J Neurocytol. 1978 Oct;7(5):601–610. doi: 10.1007/BF01260892. [DOI] [PubMed] [Google Scholar]
  24. Kreutzberg G. W. Uber perineuronale Mikrogliazellen (Autoradiographische Untersuchungen) Acta Neuropathol. 1968;(Suppl):141–145. [PubMed] [Google Scholar]
  25. Li C. Y., Lam K. W., Yam L. T. Esterases in human leukocytes. J Histochem Cytochem. 1973 Jan;21(1):1–12. doi: 10.1177/21.1.1. [DOI] [PubMed] [Google Scholar]
  26. Ling E. A. Electron microscopic study of macrophages appearing in a stab wound of the brain of rats following intravenous injection of carbon particles. Arch Histol Jpn. 1979 Jan;42(1):41–50. doi: 10.1679/aohc1950.42.41. [DOI] [PubMed] [Google Scholar]
  27. Ling E. A., Kaur C., Wong W. C. Light and electron microscopic demonstration of non-specific esterase in amoeboid microglial cells in the corpus callosum in postnatal rats: a cytochemical link to monocytes. J Anat. 1982 Sep;135(Pt 2):385–394. [PMC free article] [PubMed] [Google Scholar]
  28. Ling E. A. Some aspects of amoeboid microglia in the corpus callosum and neighbouring regions of neonatal rats. J Anat. 1976 Feb;121(Pt 1):29–45. [PMC free article] [PubMed] [Google Scholar]
  29. Ling E. A., Tan C. K. Amoeboid microglial cells in the corpus callosum of neonatal rats. Arch Histol Jpn. 1974 Mar;36(4):265–280. doi: 10.1679/aohc1950.36.265. [DOI] [PubMed] [Google Scholar]
  30. Ling E. A. Transformation of monocytes into amoeboid microglia in the corpus callosum of postnatal rats, as shown by labelling monocytes by carbon particles. J Anat. 1979 Jun;128(Pt 4):847–858. [PMC free article] [PubMed] [Google Scholar]
  31. Ling E. A., Wong W. C., Yick T. Y., Leong S. K. Ultrastructural changes in the dorsal motor nucleus of monkey following bilateral cervical vagotomy. J Neurocytol. 1986 Feb;15(1):1–15. doi: 10.1007/BF02057900. [DOI] [PubMed] [Google Scholar]
  32. Matthews M. A., Kruger L. Electron microscopy of non-neuronal cellular changes accompanying neural degeneration in thalamic nuclei of the rabbit. I. Reactive hematogenous and perivascular elements within the basal lamina. J Comp Neurol. 1973 Apr 1;148(3):285–312. doi: 10.1002/cne.901480302. [DOI] [PubMed] [Google Scholar]
  33. Matthews M. A., Kruger L. Electron microscopy of non-neuronal cellular changes accompanying neural degeneration in thalamic nuclei of the rabbit. II. Reactive elements within the neuropil. J Comp Neurol. 1973 Apr 1;148(3):313–346. doi: 10.1002/cne.901480303. [DOI] [PubMed] [Google Scholar]
  34. McKeever P. E., Balentine J. D. Macrophages migration through the brain parenchyma to the perivascular space following particle ingestion. Am J Pathol. 1978 Oct;93(1):153–164. [PMC free article] [PubMed] [Google Scholar]
  35. McKenna O. C. Endocytic activity of subependymal microglial cells in the toad brain: a cytochemical study of peroxidase uptake. J Comp Neurol. 1979 Sep 1;187(1):169–189. doi: 10.1002/cne.901870110. [DOI] [PubMed] [Google Scholar]
  36. Mori S., Leblond C. P. Identification of microglia in light and electron microscopy. J Comp Neurol. 1969 Jan;135(1):57–80. doi: 10.1002/cne.901350104. [DOI] [PubMed] [Google Scholar]
  37. Mori S. Uptake of ( 3 H)thymidine by corpus callosum cells in rats following a stab wound of the brain. Brain Res. 1972 Nov 13;46:177–186. doi: 10.1016/0006-8993(72)90014-5. [DOI] [PubMed] [Google Scholar]
  38. Murabe Y., Sano Y. Morphological studies on neuroglia. V. Microglial cells in the cerebral cortex of the rat, with special reference to their possible involvement in synaptic function. Cell Tissue Res. 1982;223(3):493–506. doi: 10.1007/BF00218471. [DOI] [PubMed] [Google Scholar]
  39. Murabe Y., Sano Y. Thiaminepyrophosphatase activity in the plasma membrane of microglia. Histochemistry. 1981;71(1):45–52. doi: 10.1007/BF00592569. [DOI] [PubMed] [Google Scholar]
  40. NOVIKOFF A. B., GOLDFISCHER S. Nucleosidediphosphatase activity in the Golgi apparatus and its usefulness for cytological studies. Proc Natl Acad Sci U S A. 1961 Jun 15;47:802–810. doi: 10.1073/pnas.47.6.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Olsson Y., Sjöstrand J. Origin of macrophages in Wallerian degereration of peripheral nerves demonstrated autoradiographically. Exp Neurol. 1969 Jan;23(1):102–112. doi: 10.1016/0014-4886(69)90037-5. [DOI] [PubMed] [Google Scholar]
  42. Payne B. C., Kim H., Pangalis G. A., Rothman A., Rappaport H. A method for the ultrastructural demonstration of non-specific esterase in human blood and lymphoid tissue. Histochem J. 1980 Jan;12(1):71–86. doi: 10.1007/BF01066538. [DOI] [PubMed] [Google Scholar]
  43. Rozenszajn L., Leibovich M., Shoham D., Epstein J. The esterase activity in megaloblasts, leukaemic and normal haemopoietic cells. Br J Haematol. 1968 Jun;14(6):605–610. doi: 10.1111/j.1365-2141.1968.tb00366.x. [DOI] [PubMed] [Google Scholar]
  44. Schelper R. L., Adrian E. K., Jr Monocytes become macrophages; they do not become microglia: a light and electron microscopic autoradiographic study using 125-iododeoxyuridine. J Neuropathol Exp Neurol. 1986 Jan;45(1):1–19. doi: 10.1097/00005072-198601000-00001. [DOI] [PubMed] [Google Scholar]
  45. Schelper R. L., Adrian E. K., Jr Non-specific esterase activity in reactive cells in injured nervous tissue labeled with 3H-thymidine or 125iododeoxyuridine injected before injury. J Comp Neurol. 1980 Dec 15;194(4):829–844. doi: 10.1002/cne.901940408. [DOI] [PubMed] [Google Scholar]
  46. Sjöstrand J. Neuroglial proliferation in the hypoglossal nucleus after nerve injury. Exp Neurol. 1971 Jan;30(1):178–189. doi: 10.1016/0014-4886(71)90232-9. [DOI] [PubMed] [Google Scholar]
  47. Skoff R. P. The fine structure of pulse labeled (3-H-thymidine cells) in degenerating rat optic nerve. J Comp Neurol. 1975 Jun 15;161(4):595–611. doi: 10.1002/cne.901610408. [DOI] [PubMed] [Google Scholar]
  48. Skoff R. P., Vaughn J. E. An autoradiographic study of cellular proliferation in degenerating rat optic nerve. J Comp Neurol. 1971 Feb;141(2):133–155. doi: 10.1002/cne.901410202. [DOI] [PubMed] [Google Scholar]
  49. Stenwig A. E. The origin of brain macrophages in traumatic lesions, Wallerian degeneration, and retrograde degeneration. J Neuropathol Exp Neurol. 1972 Oct;31(4):696–704. doi: 10.1097/00005072-197210000-00011. [DOI] [PubMed] [Google Scholar]
  50. Torvik A. The relationship between microglia and brain macrophages. Experimental investigations. Acta Neuropathol Suppl. 1975;Suppl 6:297–300. doi: 10.1007/978-3-662-08456-4_52. [DOI] [PubMed] [Google Scholar]
  51. Vaughn J. E., Hinds P. L., Skoff R. P. Electron microscopic studies of Wallerian degeneration in rat optic nerves. I. The multipotential glia. J Comp Neurol. 1970 Oct;140(2):175–206. doi: 10.1002/cne.901400204. [DOI] [PubMed] [Google Scholar]
  52. Wong-Riley M. T. Terminal degeneration and glial reactions in the lateral geniculate nucleus of the squirrel monkey after eye removal. J Comp Neurol. 1972 Jan;144(1):61–91. doi: 10.1002/cne.901440104. [DOI] [PubMed] [Google Scholar]
  53. Yam L. T., Li C. Y., Crosby W. H. Cytochemical identification of monocytes and granulocytes. Am J Clin Pathol. 1971 Mar;55(3):283–290. doi: 10.1093/ajcp/55.3.283. [DOI] [PubMed] [Google Scholar]
  54. del Cerro M., Monjan A. A. Unequivocal demonstration of the hematogenous origin of brain macrophages in a stab wound by a double-label technique. Neuroscience. 1979;4(9):1399–1404. doi: 10.1016/0306-4522(79)90167-2. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES