Advertisement

Molecular and chemical neuropathology

, Volume 21, Issue 2–3, pp 273–285 | Cite as

Influence of growth environment on the ganglioside composition of an experimental mouse brain tumor

  • Mohga El-Abbadi
  • Thomas N. Seyfried
Article

Abstract

Ganglioside composition was examined in an experimental mouse brain tumor growing as a solid tumor in vivo and as a cultured cell line in vitro. Gangliosides were also studied in the solid tmor rederived from the cultured tumor cell line. Although GM3-NeuAc was the major ganglioside in both the solid tumor and cultured tumor cells, several gangliosides expressed in the solid tumors (e.g., GM2-NeuGc, GM1, and GM1b) were not expressed in the cultured tumor cells. These gangliosides, however, are major components of mouse macrophages. Furthermore, significant amounts of gangliosides containingN-glycolylneuraminic acid (NeuGc) were found in the solid tumor growing in vivo, but only trace amounts were present in the cultured tumor cells. NeuGc is a common ganglioside sialic acid in mouse nonneural cells, whereasN-acetylneuraminic (NeuAc) is the predominant sialic acid in mouse brain. The trace amounts of NeuGc in the cultured cells are attributed to contamination from the fetal bovine serum. Radiolabeling of the cultured tumor cell gangliosides with [14C]galactose revealed that GM3-NeuAc was the only ganglioside synthesized by the tumor cells. The results suggest that nontumorinfiltrating cells, e.g., macrophages, lymphocytes, and endothelial cells, may contribute significantly to the total ganglioside composition of solid tumors growing in vivo.

Index Entries

Gangliosides brain tumors macrophages sialic acid cultured tumor cells N-acetylneuraminic acid N-glycolylneuraminic acid 

Abbreviations

NeuAc

N-acetylneuraminic acid

NeuGc

N-glycolylneuraminic acid

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ando S. and Yu R. K. (1977) Isolation and characterization of a novel trisialoganglioside, GT1a, from human brain.J. Biol. Chem. 252, 6247–6250.PubMedGoogle Scholar
  2. Ando S., Chang N. C., and Yu R. K. (1978) High performance thin layer chromatography and densitometric determination of brain gangliosides compositions of several species.Anal. Biochem. 89, 427–450.Google Scholar
  3. Ando S. and Yu R. K. (1979) Isolation and characterization of two isomers of brain tetrasialoganglioside.J. Biol. Chem. 254, 12224–12229.PubMedGoogle Scholar
  4. Ariga T., Yoshida K., Nemoto K., Seki M., Miyatani N., and Yu R. (1991) Glycolipid changes in murine myelogenous leukemias: neutral glycolipids as markers for specific populations of leukemias.Biochemistry 30, 7953–7961.PubMedGoogle Scholar
  5. Brigande J. V., Wievoszko A., Albert M. D., Balkema G. W., and Seyfried T. N. (1992) Biochemical correlates of epilepsy in the El mouse: analysis of glial fibrillary acid protein and gangliosides.J. Neurochem. 58, 752–760.PubMedGoogle Scholar
  6. Chou K. H., Ambers S. A., and Jungalwala F. B. (1979) Ganglioside composition of chemically induced rat neural tumors and characterization of hematoside from neurinomas.J. Neurochem. 33, 863–873.PubMedGoogle Scholar
  7. Crafts D. and Wilson C. B. (1977) Animal models of brain tumors.Natl. Cancer Inst. Monogr. 46, 11–17.PubMedGoogle Scholar
  8. Dawson G. and Stoolmiller A. C. (1976) Comparison of the ganglioside composition of established mouse neuroblastoma cell strains growingin vivo and in tissue culture.J. Neurochem. 26, 225–226.PubMedGoogle Scholar
  9. Duffard R. O., Fishman P. H., Bradley R. M., Lauter C. J., Brady R. O., and Trams E. G. (1977) Ganglioside composition and biosynthesis in cultured cells derived from CNS.J. Neurochem. 28, 1161–1166.PubMedGoogle Scholar
  10. Evans R. (1972) Macrophages in syngeneic animals tumors.Transplantation 14, 468–473.PubMedGoogle Scholar
  11. Evans R. (1977) Effect of X-irradiation on host-cell infiltration and growth of a murine fibrosarcoma.J. Cancer 35, 557–566.Google Scholar
  12. Evans R. and Eidlen D. (1981) Macrophage accumulations in transplanted tumors is not dependent on host immune responsiveness or presence of tumor-associated rejection antigens.J. Reticulo. Soc. 30, 425–437.Google Scholar
  13. Flavin H. J., Wieraszko A., and Seyfried T. N. (1991) Enhanced aspartate release from hippocampal slices of epileptic (EI) mice.J. Neurochem. 56, 1007–1011.PubMedGoogle Scholar
  14. Folch, J., Lees M., Sloane Stanley G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues.J. Biol. Chem. 226, 497–509.PubMedGoogle Scholar
  15. Fredman P. (1988) Gangliosides in human malignant gliomas, inNew Trends in Ganglioside Research: Neurochemical and Neurogenerative Aspects (Ledeen, R. W., Hogan E. L., Tettamanti G., Yates A., and Yu R. K. eds.), pp. 151–161, Liviana, Padova.Google Scholar
  16. Fredman P., vonHolst, H., Collins V. P., Dellheden B., and Svennerholm L. (1993) Expression of gangliosides GD3 and 3′-iso LM1 in autopsy brains from patients with malignant tumors.J. Neurochem. 60, 99–105.PubMedGoogle Scholar
  17. Hanisch F-G., Solter J., Jansen V., Lochner A., Peter-Katalinic J., and Uhlenbruck G. (1990) Glycosphingolipid expression on murine L1-fibrosarcoma cells: analysis of clonalin vivo andin vitro selected sublines with different lung colonisation potential.Br. J. Cancer 61, 813–820.PubMedPubMedCentralGoogle Scholar
  18. Higashi H., Hirabayashi, Y., Fukui Y., Naiki M., Matsumoto M., Veda S., and Kato S. (1985) Characterization of N-glycolylneuraminic acid containing gangliosides as tumor associated Hangantziu-Deichter antigen in human colon cancer.Cancer Res. 45, 3796–3802.PubMedGoogle Scholar
  19. Kawai T., Kato A., Higashi H., Kato S., and Naiki M. (1991) Quantitative determination of N-glycolylneuraminic acid expression in human cancerous tissues and avian lymphoma cell lines as a tumor-associated sialic acid by gas chromatography-mass spectrometry.Cancer Res. 51, 1242–1246.PubMedGoogle Scholar
  20. Laferte S., Fukuda M. N., Fukuda M., Dell A., and Dennis J. W. (1987) Glycosphingolipids of lectin-resistant mutants of the highly metastatic mouse tumor cell line, MDAY-D2.Cancer Res. 47, 150–159.PubMedGoogle Scholar
  21. Leeden, R. W., Yu R. K., and Eng L. F. (1973) Gangliosides of human mylen sialosylgalactosylceramide (G7) as a major component.J. Neurochem. 21, 829–839.Google Scholar
  22. Manuelidis L., Yu R. K., and Manuelidis E. E. (1977) Ganglioside content and pattern in human gliomas in culture.Acta Neuropath. (Berl.) 38, 129–135.Google Scholar
  23. Morantz R. A., Wood G. W., Foster M., Clark M., and Gollahon K. (1979) Macrophages in experimental and human brain tumors. Part 2: Studies of the macrophage content of human brain tumors.J. Neurosurg. 50, 305–311.PubMedGoogle Scholar
  24. Morimura T., Neuchrist C., Kitz K., Budka H., Scheiner O., Kraft D., and Lassmann H. (1990) Monocyte subpopulations in human gliomas: expression of Fc and complement receptors and correlation with tumor proliferation.Acta neuropathol. 80, 287–294.PubMedGoogle Scholar
  25. Morioka T., Baba T., Black K. L., and Streit W. J. (1992) Inflammatory cell infiltrates vary in experimental primary and metastatic brain tumors.Neurosurgery 30, 891–896.PubMedGoogle Scholar
  26. Muhlradt P. F., Muthing J., and Kleist J. V. (1989) Glycosphingolipid expression in murine T-cells and macrophages, inGangliosides and Cancer (Oettgen, H. F., ed.), pp. 187–195, VCH Publishers, New York.Google Scholar
  27. Nakamura K., Suzuki M., Taya C., Inagaki F., Yamakawa T., and Suzuki A. (1991) A sialidiase-susceptible ganglioside, IV3α (NeuGca2-8NeuGc)-Gg4 Cer, is a major disialoganglioside in WHT/Ht mouse thymoma and thymocytes.J. Biochem. 110, 832–842.PubMedGoogle Scholar
  28. Pross H. F., and Kerbel R. S. (1976) An assessment of intratumor phagocytic and surface marker-bearing cells in a series of autochthonous and early passaged chemically induced murine sarcomas.J. Natl. Cancer Inst. 57, 1157–1167.PubMedGoogle Scholar
  29. Ritter K., Hartl R., Bandlow G., and Thomssen R. (1986) Cytostatic effect of gangliosides present in the membrane of macrophages.Cell. Immunol. 97, 248–256.PubMedGoogle Scholar
  30. Rossi M. L., Hughes J. T., Esiri M. M., Coakham H. B., and Brownell D. B. (1987) Immunohistological study of mononnuclear cell infiltrate in malignant gliomas.Acta Neuropathol. 74, 269–277.PubMedGoogle Scholar
  31. Rossi M. L., Jones N. R., Candy E., Nicoll J. A. R., Compton J. S., Hughes J. T., Esiri M. M., Moss T. H., Cruz-Sanchez F. F., Coakham H. B. (1989) The mononuclear cell infiltrate compared with survival in high-grade astrocytomas.Acta Neuropathol. 78, 189–193.PubMedGoogle Scholar
  32. Rubin R., Sutton C. H., and Zimmerman H. M. (1968) Experimental ependymoblastoma (fine structure).J. Neuropathol. Exp. Neurol. 27, 421–438.Google Scholar
  33. Rubinstein L. J. (1977) Correlation of animal brian models with human neurooncology.Natl. Cancer Inst. Monogr. 46, 43–49.PubMedGoogle Scholar
  34. Schackert G., Simmons R. D., Buzbee T. M., Hume D. A., and Fidler I. J. (1988) Macrophage infiltration into experimental brain metastases: Occurrence through an intact blood-brain barrier.J. Natl. Canc. Inst. 80, 1027–1033.Google Scholar
  35. Schauer, R. (1985) Scialic acids and their roles as biochemical masks.Trends Biochem. Sci. 10, 357–360.Google Scholar
  36. Schold S. C. and Bigner D. D. (1983) A review of animal brain tumor models that have been used for therapeutic studies, inOncology of the Neurvous System (Walker M. D., ed.), pp. 31–64, Martinus Nijhoff, Boston.Google Scholar
  37. Seyfried T. N., Ando S., and Yu R. K. (1978a) Isolation and characterization of human liver hematoside.J. Lipid Res. 19, 538–543.PubMedGoogle Scholar
  38. Seyfried T. N., Glaser G. H., and Yu R. K. (1978b) Cerebral, cerebellar, and brain stem gangliosides in mice susceptible to audiogenic seizures.J. Neurochem. 31, 21–27.PubMedGoogle Scholar
  39. Seyfried T. N., Itoh T., Miyazawa N., and Yu R. K. (1981) Cerebellar gangliosides and phosopholipids in mutant mice with ataxia and epilepsy: The tottering/ leaner syndrome.Brain Res. 216, 429–436.PubMedGoogle Scholar
  40. Seyfried T. N., Yu R. K., Saito M., and Albert M. (1987) Ganglioside composition of an experimental mouse brain tumor.Cancer Res. 47, 3538–3542.PubMedGoogle Scholar
  41. Seyfried T. N., El-Abbadi M., and Roy M. L. (1992) Ganglioside distribution in murine neural tumors.Mol. Chem. Neuropathol. 17, 147–167.PubMedGoogle Scholar
  42. Shinonaga M., Chang C. C., Suzuki N., Sato M., and Kuwabara T. (1988) Immunohistological evaluation of macrophage infiltrates in brain tumors.J. Neurosurg. 68, 259–265.PubMedGoogle Scholar
  43. Tsuchida T., Ravindranath M. H., Saxton R. E., and Irie R. (1987) Gangliosides of human melanoma: Altered expressionin vivo andin vitro.Cancer Res. 47, 1278–1281.PubMedGoogle Scholar
  44. Ueno K., Ando S., and Yu R. K. (1978) Gangliosides of human, cat and rabbit spinal cords and cord myelin.J. Lipid Res. 19, 863–871.PubMedGoogle Scholar
  45. Van Echten G. and Sandhoff K. (1989) Modulation of ganglioside biosynthesis in primary cultured neurons.J. Neurochem. 52, 207–214.PubMedGoogle Scholar
  46. Wikstrand C. J. M., He X., Fuller G. N., Bigner S. H., Fredman P., Svennerholm L., Bigner D. D. (1991) Occurrence of lacto series gangliosides 3′-isoLM1 and 3′,6′-IsoLD1 in human gliomasin vitro andin vivo.J. Neuropathol. Exp. Neurol. 50, 756–769.PubMedGoogle Scholar
  47. Wikstrand C. J., Longee D. C., McLendon R. E., Fuller G. N., Friedman H. S., Fredman P., et al. (1993) Lactotetraose series ganglioside 3′,6′-isoLD1 in tumors of central nervous and other systemsin vitro andin vivo.Cancer Res. 53, 120–126.PubMedGoogle Scholar
  48. Wood W. and Morantz R. A. (1979) Immunohistologic evaluation of the lymphoreticular infiltrate of human central nervous system tumors.J. Natl. Cancer Inst. 62, 485–490.PubMedGoogle Scholar
  49. Yates A. J. (1988) Glycolipids and gliomas: A review.Neurochem. Pathol. 8, 157–179.PubMedGoogle Scholar
  50. Yogeeswaran G., Wherret J. R., Chatterjee S., and Murry R. K. (1970) Gangliosides of cultured mouse cells: partial characterization of14C-glucosamine incorporation.J. Biol. Chem. 245, 6718–6725.PubMedGoogle Scholar
  51. Yohe H. C., Coleman D. L., and Ryan J. (1985) Ganglioside alteration in stimulated murine macrophages.Biochim. Biophys. Acta 818, 81–86.PubMedGoogle Scholar
  52. Yohe H. C., and Ryan J. L. (1986) Ganglioside expression in macrophages from endotoxin responder and nonendotoxin responder mice.J. Immunol. 137, 3921–3927.PubMedGoogle Scholar
  53. Yohe H. C., Berenson C. S., Cuny C. L., and Ryan J. L. (1990) Altered B-lymphocyte membrane architecture indicated by ganglioside accessibility in C3H/HeJ mice.Infect. and Immun. 58, 2888–2984.Google Scholar
  54. Yohe H. C., Cuny C. L., Macala L. J., Saito M., McMurray W. J., and Ryan J. L. (1991) The presence of sialidase-sensitive sialosylgangliotetraosyl ceramide (GM1b) in stimulated murine macrophages. Deficiency of GM1b inEscherichia coli-activated macrophages from the C3H/HeJ mouse.J. Immunol. 146, 1900–1908.PubMedGoogle Scholar
  55. Yohe H. C., Macala L. J., Giordano G., and McMurray W. J. (1992) GM1b and GM1b-GalNAc: major gangliosides of murine-derived macrophage-like WEHI-3 cells.Biochim. Biophys. Acta 1109, 210–217.PubMedGoogle Scholar
  56. Yu R. K. and Ledeen R. W. (1970) Gas-liquid chromatographic assaay of lipid-bound sialic acids: Measurement of gangliosides in brains of several species.J. Lipid Res. 11, 506–516.PubMedGoogle Scholar
  57. Zimmerman H. M. and Arnold H. (1941) Experimental brain tumors; I. Tumors produced with methylcholanthrene.Cancer Res. 1, 919–938.Google Scholar

Copyright information

© Humana Press Inc. 1994

Authors and Affiliations

  • Mohga El-Abbadi
    • 1
  • Thomas N. Seyfried
    • 1
  1. 1.Department of BiologyBoston CollegeChestnut Hill

Personalised recommendations