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. 1989 Sep;135(3):529–540.

Uniform lineage of oligodendrogliomas.

S M de la Monte 1
PMCID: PMC1879866  PMID: 2675625

Abstract

Experimental observations provide evidence that galactocerebroside-containing (GC+) oligodendrocytes and glial fibrillary acidic protein-containing (GFAP+) type 2 astrocytes are derived from A2B5+ progenitor cells. Because the cytomorphologic features of oligodendrogliomas resemble those of non-neoplastic oligodendrocytes, it was speculated that neoplastic oligodendroglial cells also have A2B5+ lineage. This hypothesis was investigated by immunostaining histopathologic sections with monoclonal antibodies to GC, A2B5, and GFAP. In 28 tumors, ubiquitous immunolabeling of neoplastic cells with anti-GC and anti-A2B5 was observed. In addition, GFAP+/A2B5+ astrocytes were present in most mixed glial tumors. The findings suggest that oligodendrogliomas, whether or not they contain foci of astrocytoma, are uniformly derived from A2B5+ progenitor cells.

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Selected References

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

  1. Abney E. R., Williams B. P., Raff M. C. Tracing the development of oligodendrocytes from precursor cells using monoclonal antibodies, fluorescence-activated cell sorting, and cell culture. Dev Biol. 1983 Nov;100(1):166–171. doi: 10.1016/0012-1606(83)90207-5. [DOI] [PubMed] [Google Scholar]
  2. Bartlett P. F., Noble M. D., Pruss R. M., Raff M. C., Rattray S., Williams C. A. Rat neural antigen-2 (RAN-2): a cell surface antigen on astrocytes, ependymal cells, Müller cells and lepto-meninges defined by a monoclonal antibody. Brain Res. 1981 Jan 12;204(2):339–351. doi: 10.1016/0006-8993(81)90593-x. [DOI] [PubMed] [Google Scholar]
  3. Bishop M., de la Monte S. M. Dual lineage of astrocytomas. Am J Pathol. 1989 Sep;135(3):517–527. [PMC free article] [PubMed] [Google Scholar]
  4. Bologa L., Bisconte J. C., Joubert R., Marangos P. J., Derbin C., Rioux F., Herschkowitz N. Accelerated differentiation of oligodendrocytes in neuronal-rich embryonic mouse brain cell cultures. Brain Res. 1982 Dec 2;252(1):129–136. doi: 10.1016/0006-8993(82)90985-4. [DOI] [PubMed] [Google Scholar]
  5. Bologa L., Bisconte J. C., Joubert R., Margules S., Herschkowitz N. Proliferative activity and characteristics of immunocytochemically identified oligodendrocytes in embryonic mouse brain cell cultures. Exp Brain Res. 1983;50(1):84–90. doi: 10.1007/BF00238234. [DOI] [PubMed] [Google Scholar]
  6. Burger P. C. Malignant astrocytic neoplasms: classification, pathologic anatomy, and response to treatment. Semin Oncol. 1986 Mar;13(1):16–26. [PubMed] [Google Scholar]
  7. Burger P. C., Rawlings C. E., Cox E. B., McLendon R. E., Schold S. C., Jr, Bullard D. E. Clinicopathologic correlations in the oligodendroglioma. Cancer. 1987 Apr 1;59(7):1345–1352. doi: 10.1002/1097-0142(19870401)59:7<1345::aid-cncr2820590719>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  8. Burger P. C., Vogel F. S., Green S. B., Strike T. A. Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer. 1985 Sep 1;56(5):1106–1111. doi: 10.1002/1097-0142(19850901)56:5<1106::aid-cncr2820560525>3.0.co;2-2. [DOI] [PubMed] [Google Scholar]
  9. Dubois-Dalcq M., Behar T., Hudson L., Lazzarini R. A. Emergence of three myelin proteins in oligodendrocytes cultured without neurons. J Cell Biol. 1986 Feb;102(2):384–392. doi: 10.1083/jcb.102.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eccleston P. A., Silberberg D. H. The differentiation of oligodendrocytes in a serum-free hormone-supplemented medium. Brain Res. 1984 Sep;318(1):1–9. doi: 10.1016/0165-3806(84)90056-7. [DOI] [PubMed] [Google Scholar]
  11. Ffrench-Constant C., Raff M. C. Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature. 1986 Feb 6;319(6053):499–502. doi: 10.1038/319499a0. [DOI] [PubMed] [Google Scholar]
  12. Girdlestone J., Weston J. A. Identification of early neuronal subpopulations in avian neural crest cell cultures. Dev Biol. 1985 Jun;109(2):274–287. doi: 10.1016/0012-1606(85)90455-5. [DOI] [PubMed] [Google Scholar]
  13. Herpers M. J., Budka H. Glial fibrillary acidic protein (GFAP) in oligodendroglial tumors: gliofibrillary oligodendroglioma and transitional oligoastrocytoma as subtypes of oligodendroglioma. Acta Neuropathol. 1984;64(4):265–272. doi: 10.1007/BF00690392. [DOI] [PubMed] [Google Scholar]
  14. Kennedy P. G., Fok-Seang J. Studies on the development, antigenic phenotype and function of human glial cells in tissue culture. Brain. 1986 Dec;109(Pt 6):1261–1277. doi: 10.1093/brain/109.6.1261. [DOI] [PubMed] [Google Scholar]
  15. Levi G., Gallo V., Ciotti M. T. Bipotential precursors of putative fibrous astrocytes and oligodendrocytes in rat cerebellar cultures express distinct surface features and "neuron-like" gamma-aminobutyric acid transport. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1504–1508. doi: 10.1073/pnas.83.5.1504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Miller R. H., David S., Patel R., Abney E. R., Raff M. C. A quantitative immunohistochemical study of macroglial cell development in the rat optic nerve: in vivo evidence for two distinct astrocyte lineages. Dev Biol. 1985 Sep;111(1):35–41. doi: 10.1016/0012-1606(85)90432-4. [DOI] [PubMed] [Google Scholar]
  17. Mørk S. J., Halvorsen T. B., Lindegaard K. F., Eide G. E. Oligodendroglioma. Histologic evaluation and prognosis. J Neuropathol Exp Neurol. 1986 Jan;45(1):65–78. doi: 10.1097/00005072-198601000-00006. [DOI] [PubMed] [Google Scholar]
  18. Nakagawa Y., Perentes E., Rubinstein L. J. Immunohistochemical characterization of oligodendrogliomas: an analysis of multiple markers. Acta Neuropathol. 1986;72(1):15–22. doi: 10.1007/BF00687942. [DOI] [PubMed] [Google Scholar]
  19. Nelson J. S., Tsukada Y., Schoenfeld D., Fulling K., Lamarche J., Peress N. Necrosis as a prognostic criterion in malignant supratentorial, astrocytic gliomas. Cancer. 1983 Aug 1;52(3):550–554. doi: 10.1002/1097-0142(19830801)52:3<550::aid-cncr2820520327>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  20. Ogawa H., Sato Y., Takeshita I., Tateishi J., Kitamura K. Transient expression of glial fibrillary acidic protein in developing oligodendrocytes in vitro. Brain Res. 1985 Feb;350(1-2):133–141. doi: 10.1016/0165-3806(85)90257-3. [DOI] [PubMed] [Google Scholar]
  21. Raff M. C., Abney E. R., Fok-Seang J. Reconstitution of a developmental clock in vitro: a critical role for astrocytes in the timing of oligodendrocyte differentiation. Cell. 1985 Aug;42(1):61–69. doi: 10.1016/s0092-8674(85)80101-x. [DOI] [PubMed] [Google Scholar]
  22. Raff M. C., Abney E. R., Miller R. H. Two glial cell lineages diverge prenatally in rat optic nerve. Dev Biol. 1984 Nov;106(1):53–60. doi: 10.1016/0012-1606(84)90060-5. [DOI] [PubMed] [Google Scholar]
  23. Raff M. C., Miller R. H., Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature. 1983 Jun 2;303(5916):390–396. doi: 10.1038/303390a0. [DOI] [PubMed] [Google Scholar]
  24. Raff M. C., Williams B. P., Miller R. H. The in vitro differentiation of a bipotential glial progenitor cell. EMBO J. 1984 Aug;3(8):1857–1864. doi: 10.1002/j.1460-2075.1984.tb02059.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rostami A., Eccleston P. A., Silberberg D. H., Hirayama M., Lisak R. P., Pleasure D. E., Phillips S. M. Generation and biological properties of a monoclonal antibody to galactocerebroside. Brain Res. 1984 Apr 30;298(2):203–208. doi: 10.1016/0006-8993(84)91419-7. [DOI] [PubMed] [Google Scholar]
  26. Smith M. T., Ludwig C. L., Godfrey A. D., Armbrustmacher V. W. Grading of oligodendrogliomas. Cancer. 1983 Dec 1;52(11):2107–2114. doi: 10.1002/1097-0142(19831201)52:11<2107::aid-cncr2820521123>3.0.co;2-x. [DOI] [PubMed] [Google Scholar]
  27. Stallcup W. B., Beasley L. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci. 1987 Sep;7(9):2737–2744. doi: 10.1523/JNEUROSCI.07-09-02737.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Temple S., Raff M. C. Differentiation of a bipotential glial progenitor cell in a single cell microculture. Nature. 1985 Jan 17;313(5999):223–225. doi: 10.1038/313223a0. [DOI] [PubMed] [Google Scholar]
  29. Wilkinson I. M., Anderson J. R., Holmes A. E. Oligodendroglioma: an analysis of 42 cases. J Neurol Neurosurg Psychiatry. 1987 Mar;50(3):304–312. doi: 10.1136/jnnp.50.3.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Williams B. P., Abney E. R., Raff M. C. Macroglial cell development in embryonic rat brain: studies using monoclonal antibodies, fluorescence activated cell sorting, and cell culture. Dev Biol. 1985 Nov;112(1):126–134. doi: 10.1016/0012-1606(85)90126-5. [DOI] [PubMed] [Google Scholar]

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