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. 1977 Aug;23(2):302–314. doi: 10.1128/jvi.23.2.302-314.1977

Characterization of Molecular Species Carrying Gross Cell Surface Antigen

Harry W Snyder Jr 1, Elisabeth Stockert 1, Erwin Fleissner 1
PMCID: PMC515832  PMID: 69725

Abstract

The Gross cell surface antigen (GCSA), associated with expression of endogenous Gross-type murine leukemia virus (G-MuLV) in tissues of mice, is defined by the cytotoxic reaction of a C57BL/6 antiserum, anti-AKR spontaneous leukemia K36, with cells of the Gross virus-induced C57BL/6 leukemia, E♂G2. Sequential lactoperoxidase-catalyzed radioiodination of E♂G2 cells, Nonidet P-40 lysis, precipitation with anti-K36 serum, and sodium dodecyl sulfate-polyacrylamide gel electrophoresis identified molecules with properties of polyproteins encoded by the gag region of the viral genome. These cell surface species could also be labeled by in vitro culturing of E♂G2 with radioactive glucosamine. The viral specificity of these molecules and their participation in the GCSA typing system were established as follows. (i) Absorption of anti-K36 serum with GCSA+, but not GCSA−, leukemias led to a marked decrease in precipitation of these proteins. (ii) The same E♂G2 cell surface proteins were also precipitated by antisera against the MuLV virion proteins p30 and p15. (iii) Anti-K36 was shown to possess antibodies against Gross virus p30 and p15. (iv) “Clearing” the E♂G2 lysate of molecules reactive with anti-p30 or anti-p15 sera removed molecules reactive with anti-K36 serum. (v) Absorption of anti-K36 serum with disrupted G-MuLV virions or with Gross p30 or p15 removed GCSA cytotoxic antibodies; partial absorption was achieved with disrupted Rauscher-MuLV (R-MuLV) or with R-MuLV p30, and no absorption was found with R-MuLV p15. These data show that E♂G2 cells express, on their surfaces, MuLV core polyproteins that apparently can be glycosylated and on which the determinants of GCSA are located.

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Selected References

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  1. Aoki T., Boyse E. A., Old L. J., De Harven E., Hämmerling U., Wood H. A. G (Gross) and H-2 cell-surface antigens: location on Gross leukemia cells by electron microscopy with visually labeled antibody. Proc Natl Acad Sci U S A. 1970 Mar;65(3):569–576. doi: 10.1073/pnas.65.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aoki T., Boyse E. A., Old L. J. Wild-type Gross leukemia virus. I. Soluble antigen (GSA) in the plasma and tissues of infected mice. J Natl Cancer Inst. 1968 Jul;41(1):89–96. [PubMed] [Google Scholar]
  3. Arcement L. J., Karshin W. L., Naso R. B., Jamjoom G., Arlinghaus R. B. Biosynthesis of Rauscher leukemia viral proteins: presence of p30 and envelope p15 sequences in precursor polypeptides. Virology. 1976 Feb;69(2):763–774. doi: 10.1016/0042-6822(76)90504-3. [DOI] [PubMed] [Google Scholar]
  4. August J. T., Bolognesi D. P., Fleissner E., Gilden R. V., Nowinski R. C. A proposed nomenclature for the virion proteins of oncogenic RNA viruses. Virology. 1974 Aug;60(2):595–600. doi: 10.1016/0042-6822(74)90356-0. [DOI] [PubMed] [Google Scholar]
  5. Boyse E. A., Old L. J., Stockert E. An approach to the mapping of antigens on the cell surface. Proc Natl Acad Sci U S A. 1968 Jul;60(3):886–893. doi: 10.1073/pnas.60.3.886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buchhagen D. L., Stutman O., Fleissner E. Chromatographic Separation and Antigenic Analysis of Proteins of the Oncornaviruses IV. Biochemical Typing of Murine Viral Proteins. J Virol. 1975 May;15(5):1148–1157. doi: 10.1128/jvi.15.5.1148-1157.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collins J. J., Bolio L. D., Denny T. P., Bolognesi D. P. Interspecies determinants of Friend leukemia virus antigens involved in cytolysis of virus-pfoducing cells. J Virol. 1977 Jan;21(1):113–118. doi: 10.1128/jvi.21.1.113-118.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Famulari N. G., Buchhagen D. L., Klenk H. D., Fleissner E. Presence of murine leukemia virus envelope proteins gp70 and p15(E) in a common polyprotein of infected cells. J Virol. 1976 Nov;20(2):501–508. doi: 10.1128/jvi.20.2.501-508.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ferrer J. F. Cell-surface and virion-envelope antigens shared by radiation leukemia virus (RadLV) and other murine c-type viruses. Int J Cancer. 1973 Sep 15;12(2):378–388. doi: 10.1002/ijc.2910120209. [DOI] [PubMed] [Google Scholar]
  10. Fleissner E. Chromatographic separation and antigenic analysis of proteins of the oncornaviruses. I. Avian leukemia-sarcoma viruses. J Virol. 1971 Nov;8(5):778–785. doi: 10.1128/jvi.8.5.778-785.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fleissner E., Tress E. Chromatographic and electrophoretic analysis of viral proteins from hamster and chicken cells transformed by Rous sarcoma virus. J Virol. 1973 Feb;11(2):250–262. doi: 10.1128/jvi.11.2.250-262.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Friedman M., Lilly F., Nathenson S. G. Cell surface antigen induced by Friend murine leukemia virus is also in the virion. J Virol. 1974 Nov;14(5):1126–1131. doi: 10.1128/jvi.14.5.1126-1131.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Geering G., Old L. J., Boyse E. A. Antigens of leukemias induced by naturally occurring murine leukemia virus: their relation to the antigens of gross virus and other murine leukemia viruses. J Exp Med. 1966 Oct 1;124(4):753–772. doi: 10.1084/jem.124.4.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gielkens A. L., Van Zaane D., Bloemers H. P., Bloemendal H. Synthesis of Rauscher murine leukemia virus-specific polypeptides in vitro. Proc Natl Acad Sci U S A. 1976 Feb;73(2):356–360. doi: 10.1073/pnas.73.2.356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hogg N. M. Specificity of serum from rodents immune to Moloney C-type virus-induced tumours. Int J Cancer. 1976 Oct 15;18(4):439–447. doi: 10.1002/ijc.2910180407. [DOI] [PubMed] [Google Scholar]
  16. Hunsmann G., Claviez M., Moennig V., Schwarz H., Schäfer W. Properties of mouse leukemia viruses. X. Occurrence of viral structural antigens on the cell surface as revealed by a cytotoxicity test. Virology. 1976 Jan;69(1):157–168. doi: 10.1016/0042-6822(76)90203-8. [DOI] [PubMed] [Google Scholar]
  17. Ihle J. N., Hanna M. G., Jr, Roberson L. E., Kenney F. T. Autogenous immunity to endogenous RNA tumor virus. Identification of antibody reactivity to select viral antigens. J Exp Med. 1974 Jun 1;139(6):1568–1581. doi: 10.1084/jem.139.6.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ihle J. N., Jr, Hanna M. G., Schafer W., Hunsmann G., Bolognesi D. P., HUPER G. Polypeptides of mammalian oncornaviruses. III. Localization of p 15 and reactivity with natural antibody. Virology. 1975 Jan;63(1):60–67. doi: 10.1016/0042-6822(75)90370-0. [DOI] [PubMed] [Google Scholar]
  19. Ikeda H., Hardy W., Jr, Tress E., Fleissner E. Chromatographic separation and antigenic analysis of proteins of the oncornaviruses. V. Identification of a new murine viral protein, p15(E). J Virol. 1975 Jul;16(1):53–61. doi: 10.1128/jvi.16.1.53-61.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ikeda H., Pincus T., Yoshiki T., Strand M., August J. T., Boyse E. A., Mellors R. C. Biological expression of antigenic determinants of murine leukemia virus proteins gp69-71 and p30. J Virol. 1974 Nov;14(5):1274–1280. doi: 10.1128/jvi.14.5.1274-1280.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kawashima K., Ikeda H., Hartley J. W., Stockert E., Rowe W. P., Old L. J. Changes in expression of murine leukemia virus antigens and production of xenotropic virus in the late preleukemic period in AKR mice. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4680–4684. doi: 10.1073/pnas.73.12.4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kawashima K., Ikeda H., Stockert E., Takahashi T., Old L. J. Age-related changes in cell surface antigens of preleukemic AKR thymocytes. J Exp Med. 1976 Jul 1;144(1):193–208. doi: 10.1084/jem.144.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kerr I. M., Olshevsky U., Lodish H. F., Baltimore D. Translation of murine leukemia virus RNA in cell-free systems from animal cells. J Virol. 1976 May;18(2):627–635. doi: 10.1128/jvi.18.2.627-635.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Knight R. A., Mitchison N. A., Shellam G. R. Studies on a gross-virus-induced lymphoma in the rat. II. The role of cell-membrane-associated and serum P30 antigen in the antibody and cell-mediated response. Int J Cancer. 1975 Mar 15;15(3):417–428. doi: 10.1002/ijc.2910150308. [DOI] [PubMed] [Google Scholar]
  25. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  26. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  27. Ledbetter J., Nowinski R. C., Emery S. Viral proteins expressed on the surface of murine leukemia cells. J Virol. 1977 Apr;22(1):65–73. doi: 10.1128/jvi.22.1.65-73.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ledbetter J., Nowinski R. C. Identification of the Gross cell surface antigen associated with murine leukemia virus-infected cells. J Virol. 1977 Aug;23(2):315–322. doi: 10.1128/jvi.23.2.315-322.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lejneva O. M., Abelev G. I., Dorfman N. A., Strand M., August J. T. Localization of a murine oncornavirus 15,000-dalton virion protein on the membrane of neoplastic cells: analysis by immunofluorescence and immunoelectron microscopy. Virology. 1976 Dec;75(2):281–292. doi: 10.1016/0042-6822(76)90028-3. [DOI] [PubMed] [Google Scholar]
  30. Moroni C., Robert-Guroff M., Martin D. Virion and non-virion murine leukemia membrane antigens: analysis with virus-absorbed antisera. Intervirology. 1974;3(5-6):292–304. doi: 10.1159/000149767. [DOI] [PubMed] [Google Scholar]
  31. Naso R. B., Arcement L. J., Arlinghaus R. B. Biosynthesis of Rauscher leukemia viral proteins. Cell. 1975 Jan;4(1):31–36. doi: 10.1016/0092-8674(75)90130-0. [DOI] [PubMed] [Google Scholar]
  32. Naso R. B., Arcement L. J., Wood G., Saunders T. E., Arlinghaus R. B. The cell-free translation of Rauscher leukemia virus RNA into high molecular weight polypeptides. Biochim Biophys Acta. 1975 Mar 10;383(2):195–206. doi: 10.1016/0005-2787(75)90261-0. [DOI] [PubMed] [Google Scholar]
  33. Nowinski R. C., Fleissner E., Sarkar N. H., Aoki T. Chromatographic separation and antigenic analysis of proteins of the oncornaviruses. II. Mammalian leukemia-sarcoma viruses. J Virol. 1972 Feb;9(2):359–366. doi: 10.1128/jvi.9.2.359-366.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nowinski R. C. Genetic control of natural immunity to ecotropic mouse leukemia viruses: immune response genes. Infect Immun. 1976 Apr;13(4):1098–1102. doi: 10.1128/iai.13.4.1098-1102.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nowinski R. C., Watson A. Immune response of the mouse to the major core protein (p30) of ecotropic leukemia viruses. J Immunol. 1976 Aug;117(2):693–696. [PubMed] [Google Scholar]
  36. O'Donnell P. V., Stockert E. Induction of GIX antigen and gross cell surface antigen after infection by ecotropic and xenotropic murine leukemia viruses in vitro. J Virol. 1976 Dec;20(3):545–554. doi: 10.1128/jvi.20.3.545-554.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. OLD L. J., BOYSE E. A. ANTIGENIC PROPERTIES OF EXPERIMENTAL LEUKEMIAS. I. SEROLOGICAL STUDIES IN VITRO WITH SPONTANEOUS AND RADIATION-INDUCED LEUKEMIAS. J Natl Cancer Inst. 1963 Oct;31:977–995. [PubMed] [Google Scholar]
  38. OLD L. J., BOYSE E. A., STOCKERT E. TYPING OF MOUSE LEUKAEMIAS BY SEROLOGICAL METHODS. Nature. 1964 Feb 22;201:777–779. doi: 10.1038/201777a0. [DOI] [PubMed] [Google Scholar]
  39. Obata Y., Ikeda H., Stockert E., Boyse E. A. Relation of GIX antigen of thymocytes to envelope glycoprotein of murine leukemia virus. J Exp Med. 1975 Jan 1;141(1):188–197. doi: 10.1084/jem.141.1.188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Old L. J., Boyse E. A. Current enigmas in cancer research. Harvey Lect. 1973;67:273–315. [PubMed] [Google Scholar]
  41. Old L. J., Boyse E. A., Stockert E. The G (Gross) leukemia antigen. Cancer Res. 1965 Jul;25(6):813–819. [PubMed] [Google Scholar]
  42. Parks W. P., Noon M. C., Gilden R., Scolnick E. M. Serological studies with low-molecular-weight polypeptides from the Moloney strain of murine leukemia virus. J Virol. 1975 Jun;15(6):1385–1395. doi: 10.1128/jvi.15.6.1385-1395.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Schafer W., Hunsmann G., Moennig V., Noranha F., Bolognesi D. P., Green R. W., Hüper G. Polypeptides of mammalian oncornaviruses. II Characterization of murine leukemia virus polypeptide (p 15) bearing interspecies reactivity. Virology. 1975 Jan;63(1):48–59. doi: 10.1016/0042-6822(75)90369-4. [DOI] [PubMed] [Google Scholar]
  44. Schwarz H., Hunsmann G., Moenning V., Schäfer W. Properties of mouse leukemia viruses. XI. Immunoelectron microscopic studies on viral structural antigens on the cell surface. Virology. 1976 Jan;69(1):169–178. doi: 10.1016/0042-6822(76)90204-x. [DOI] [PubMed] [Google Scholar]
  45. Shapiro S. Z., Strand M., August J. T. High molecular weight precursor polypeptides to structural proteins of Rauscher murine leukemia virus. J Mol Biol. 1976 Nov 15;107(4):459–477. doi: 10.1016/s0022-2836(76)80078-2. [DOI] [PubMed] [Google Scholar]
  46. Snyder H. W., Jr, Pincus T., Fleissner E. Specificities of human immunoglobulins reactive with antigens in preparations of several mammalian type-C viruses. Virology. 1976 Nov;75(1):60–73. doi: 10.1016/0042-6822(76)90007-6. [DOI] [PubMed] [Google Scholar]
  47. Stephenson J. R., Peters R. L., Hino S., Donahoe R. M., Long L. K., Aaronson S. A., Kelloff G. J. Natural immunity in mice to structural polypeptides of endogenous type C RNA viruses. J Virol. 1976 Sep;19(3):890–898. doi: 10.1128/jvi.19.3.890-898.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Strand M., August J. T. Structural proteins of mammalian oncogenic RNA viruses: multiple antigenic determinants of the major internal protein and envelope glycoprotein. J Virol. 1974 Jan;13(1):171–180. doi: 10.1128/jvi.13.1.171-180.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Strand M., Wilsnack R., August J. T. Structural proteins of mammalian oncogenic RNA viruses: immunological characterization of the p15 polypeptide of Rauscher murine virus. J Virol. 1974 Dec;14(6):1575–1583. doi: 10.1128/jvi.14.6.1575-1583.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tung J. S., Fleissner E., Vitetta E. S., Boyse E. A. Expression of murine leukemia virus envelope glycoprotein gp69/71 on mouse thymocytes. Evidence for two structural variants distinguished by presence vs. absence of GIX antigen. J Exp Med. 1975 Aug 1;142(2):518–523. doi: 10.1084/jem.142.2.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Tung J. S., Pinter A., Fleissner E. Two species of type C viral core polyprotein on AKR mouse leukemia cells. J Virol. 1977 Aug;23(2):430–435. doi: 10.1128/jvi.23.2.430-435.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Tung J. S., Vitetta E. S., Fleissner E., Boyse E. A. Biochemical evidence linking the GIX thymocyte surface antigen to the gp69/71 envelope glycoprotein of murine leukemia virus. J Exp Med. 1975 Jan 1;141(1):198–205. doi: 10.1084/jem.141.1.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Tung J. S., Yoshiki T., Fleissner E. A core polyprotein of murine leukemia virus on the surface of mouse leukemia cells. Cell. 1976 Dec;9(4 Pt 1):573–578. doi: 10.1016/0092-8674(76)90039-8. [DOI] [PubMed] [Google Scholar]
  54. Van Zaane D., Dekker-Michielsen J. A., Bloemers H. P. Virus-specific precursor polypeptides in cells infected with Rauscher leukemia virus: synthesis, identification, and processing. Virology. 1976 Nov;75(1):113–129. doi: 10.1016/0042-6822(76)90011-8. [DOI] [PubMed] [Google Scholar]
  55. Vitetta E. S., Baur S., Uhr J. W. Cell surface immunoglobulin. II. Isolation and characterization of immunoglobulin from mouse splenic lymphocytes. J Exp Med. 1971 Jul 1;134(1):242–264. doi: 10.1084/jem.134.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Yoshiki T., Mellors R. C., Hardy W. D., Jr, Fleissner E. Common cell surface antigen associated with mammalian C-type RNA viruses. Cell membrane-bound gs antigen. J Exp Med. 1974 Apr 1;139(4):925–942. doi: 10.1084/jem.139.4.925. [DOI] [PMC free article] [PubMed] [Google Scholar]

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