Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1974 Dec;14(6):1559–1574. doi: 10.1128/jvi.14.6.1559-1574.1974

Murine Type-C Virus Group-Specific Antigens: Interstrain Immunochemical, Biophysical, and Amino Acid Sequence Differences

Stephen Oroszlan 1, Murray R Summers 1, Carol Foreman 1, Raymond V Gilden 1
PMCID: PMC355686  PMID: 4372411

Abstract

The 30,000-molecular-weight internal protein, p30, was purified from seven strains of mouse type-C viruses. The individual p30's showed variation in isoelectric points and also intrastrain heterogeneity. The individual p30's could be distinguished by peptide map and quantitative complement fixation techniques with relatedness estimates of >95%. Amino terminal sequence analysis showed variability at position 4 for several p30's with complete homology otherwise through 24 residues. The intrastrain heterogeneity in p30 isoelectric points could not be explained by common contaminants, as shown by peptide mapping, and is more likely based on post-transcriptional modifications. These data provide a chemical basis for the recently described type-specific immunological properties of individual p30's.

Full text

PDF
1559

Images in this article

1562Image
on p.1562
1564Image
on p.1564
1565Image
on p.1565
1565Image
on p.1565
1568Image
on p.1568
1570Image
on p.1570
1570Image
on p.1570
1572Image
on p.1572

Selected References

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

  1. Aaronson S. A., Stephenson J. R. Independent segregation of loci for activation of biologically distinguishable RNA C-type viruses in mouse cells. Proc Natl Acad Sci U S A. 1973 Jul;70(7):2055–2058. doi: 10.1073/pnas.70.7.2055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benveniste R. E., Todaro G. J. Homology between type-C viruses of various species as determined by molecular hybridization. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3316–3320. doi: 10.1073/pnas.70.12.3316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chiller J. M., Weigle W. O. Termination of tolerance to human gamma globulin in mice by antigen and bacterial lipopolysaccharide (endotoxin). J Exp Med. 1973 Mar 1;137(3):740–750. doi: 10.1084/jem.137.3.740. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chuat J. C., Bernard C., Laprevotte I., Seban C., Boiron M. Studies on mouse sarcoma virus. IV. The isoelectric point of the group-specific antigen. Int J Cancer. 1973 Nov 15;12(3):742–751. doi: 10.1002/ijc.2910120322. [DOI] [PubMed] [Google Scholar]
  5. Cocks G. T., Wilson A. C. Immunological detection of single amino acid substitutions in alkaline phosphatase. Science. 1969 Apr 11;164(3876):188–189. doi: 10.1126/science.164.3876.188. [DOI] [PubMed] [Google Scholar]
  6. Davis J., Gilden R. V., Oroszlan S. Isolation of an immunogenic polypeptide after limited trypsin hydrolysis of murine leukemia virus group-specific antigen. Virology. 1973 Nov;56(1):411–415. doi: 10.1016/0042-6822(73)90324-3. [DOI] [PubMed] [Google Scholar]
  7. Fairbanks G., Steck T. L., Wallach D. F. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 1971 Jun 22;10(13):2606–2617. doi: 10.1021/bi00789a030. [DOI] [PubMed] [Google Scholar]
  8. Fish W. W., Reynolds J. A., Tanford C. Gel chromatography of proteins in denaturing solvents. Comparison between sodium dodecyl sulfate and guanidine hydrochloride as denaturants. J Biol Chem. 1970 Oct 10;245(19):5166–5168. [PubMed] [Google Scholar]
  9. 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]
  10. Gilden R. V., Oroszlan S., Huebner R. J. Coexistence of intraspecies and interspecies specific antigenic determinants on the major structural polypeptide of mammalian C-type viruses. Nat New Biol. 1971 May 26;231(21):107–108. doi: 10.1038/newbio231107a0. [DOI] [PubMed] [Google Scholar]
  11. Gregoriades A., Old L. J. Isolation and some characteristics of a group-specific antigen of the murine leukemia viruses. Virology. 1969 Feb;37(2):189–202. doi: 10.1016/0042-6822(69)90198-6. [DOI] [PubMed] [Google Scholar]
  12. Hanke N., Prager E. M., Wilson A. C. Quantitative immunological and electrophoretic comparison of primate lysozymes. J Biol Chem. 1973 Apr 25;248(8):2824–2828. [PubMed] [Google Scholar]
  13. Hatanaka M., Twiddy E., Gilden R. V. Protein kinase associated with RNA tumor viruses and other budding RNA viruses. Virology. 1972 Feb;47(2):536–538. doi: 10.1016/0042-6822(72)90297-8. [DOI] [PubMed] [Google Scholar]
  14. Huebner R. J., Kelloff G. J., Sarma P. S., Lane W. T., Turner H. C., Gilden R. V., Oroszlan S., Meier H., Myers D. D., Peters R. L. Group-specific antigen expression during embryogenesis of the genome of the C-type RNA tumor virus: implications for ontogenesis and oncogenesis. Proc Natl Acad Sci U S A. 1970 Sep;67(1):366–376. doi: 10.1073/pnas.67.1.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LIEBERMAN M., KAPLAN H. S. Leukemogenic activity of filtrates from radiation-induced lymphoid tumors of mice. Science. 1959 Aug 14;130(3372):387–388. doi: 10.1126/science.130.3372.387. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Lerner R. A., Jensen F., Kennel S. J., Dixon F. J., Des Roches G., Francke U. Karyotypic, virologic, and immunologic analyses of two continuous lymphocyte lines established from New Zealand black mice: possible relationship of chromosomal mosaicism to autoimmunity. Proc Natl Acad Sci U S A. 1972 Oct;69(10):2965–2969. doi: 10.1073/pnas.69.10.2965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McAllister R. M., Nicolson M., Gardner M. B., Rongey R. W., Rasheed S., Sarma P. S., Huebner R. J., Hatanaka M., Oroszlan S., Gilden R. V. C-type virus released from cultured human rhabdomyosarcoma cells. Nat New Biol. 1972 Jan 5;235(53):3–6. doi: 10.1038/newbio235003a0. [DOI] [PubMed] [Google Scholar]
  19. Moss B., Rosenblum E. N. Hydroxylapatite chromatography of protein-sodium dodecyl sulfate complexes. A new method for the separation of polypeptide subunits. J Biol Chem. 1972 Aug 25;247(16):5194–5198. [PubMed] [Google Scholar]
  20. Nisonoff A., Reichlin M., Margoliash E. Immunological activity of cytochrome c. II. Localization of a major antigenic determinant of human cytochrome c. J Biol Chem. 1970 Mar 10;245(5):940–946. [PubMed] [Google Scholar]
  21. 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]
  22. Officer J. E., Tecson N., Estes J. D., Fontanilla E., Rongey R. W., Gardner M. B. Isolation of a neurotropic type C virus. Science. 1973 Sep 7;181(4103):945–947. doi: 10.1126/science.181.4103.945. [DOI] [PubMed] [Google Scholar]
  23. Okabe H., Gilden R. V., Hatanaka M. Specificity of the DNA product of RNA-dependent DNA polymerase in type C viruses. II. Quantitative analysis. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3923–3927. doi: 10.1073/pnas.70.12.3923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oroszlan S., Bova D., Huebner R. J., Gilden R. V. Major group-specific protein of rat type C viruses. J Virol. 1972 Oct;10(4):746–750. doi: 10.1128/jvi.10.4.746-750.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oroszlan S., Bova D., Martin White M. H., Toni R., Foreman C., Gilden R. V. Purification and immunological characterization of the major internal protein of the RD-114 virus. Proc Natl Acad Sci U S A. 1972 May;69(5):1211–1215. doi: 10.1073/pnas.69.5.1211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Oroszlan S., Copeland T., Summers M. R., Gilden R. V. Feline leukemia and RD-114 virus group-specific proteins: comparison of amino terminal sequence. Science. 1973 Aug 3;181(4098):454–456. doi: 10.1126/science.181.4098.454. [DOI] [PubMed] [Google Scholar]
  27. Oroszlan S., Foreman C., Kelloff G., Gilden R. V. The group-specific antigen and other structural proteins of hamster and mouse C-type viruses. Virology. 1971 Mar;43(3):665–674. doi: 10.1016/0042-6822(71)90290-x. [DOI] [PubMed] [Google Scholar]
  28. Oroszlan S., Huebner R. J., Gilden R. V. Species-specific and interspecific antigenic determinants associated with the structural protein of feline C-type virus. Proc Natl Acad Sci U S A. 1971 May;68(5):901–904. doi: 10.1073/pnas.68.5.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Parks W. P., Livingston D. M., Todaro G. J., Benveniste R. E., Scolnick E. M. Radioimmunoassay of mammalian type C viral proteins. 3. Detection of viral antigen in normal murine cells and tissues. J Exp Med. 1973 Mar 1;137(3):622–635. doi: 10.1084/jem.137.3.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Parks W. P., Scolnick E. M. Radioimmunoassay of mammalian type-C viral proteins: interspecies antigenic reactivities of the major internal polypeptide. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1766–1770. doi: 10.1073/pnas.69.7.1766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Prager E. M., Wilson A. C. The dependence of immunological cross-reactivity upon sequence resemblance among lysozymes. II. Comparison of precipitin and micro-complement fixation results. J Biol Chem. 1971 Nov 25;246(22):7010–7017. [PubMed] [Google Scholar]
  32. Rowe W. P., Hartley J. W., Bremner T. Genetic mapping of a murine leukemia virus-inducing locus of AKR mice. Science. 1972 Nov 24;178(4063):860–862. doi: 10.1126/science.178.4063.860. [DOI] [PubMed] [Google Scholar]
  33. Salaman M. R., Williamson A. R. Isoelectric focusing of proteins in the native and denatured states. Anomalous behaviour of plasma albumin. Biochem J. 1971 Mar;122(1):93–99. doi: 10.1042/bj1220093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schaffner W., Weissmann C. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem. 1973 Dec;56(2):502–514. doi: 10.1016/0003-2697(73)90217-0. [DOI] [PubMed] [Google Scholar]
  35. Strand M., August J. T. Protein kinase and phosphate acceptor proteins in Rauscher murine leukaemia virus. Nat New Biol. 1971 Sep 29;233(39):137–140. doi: 10.1038/newbio233137a0. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Theilen G. H., Kawakami T. G., Rush J. D., Munn R. J. Replication of cat leukemia virus in cell suspension cultures. Nature. 1969 May 10;222(5193):589–590. doi: 10.1038/222589b0. [DOI] [PubMed] [Google Scholar]
  38. Ting R. C. Biological and serological properties of viral particles from a nonproducer rat neoplasm induced by murine sarcoma virus (Moloney). J Virol. 1968 Sep;2(9):865–868. doi: 10.1128/jvi.2.9.865-868.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Todaro G. J., Arnstein P., Parks W. P., Lennette E. H., Huebner R. J. A type-C virus in human rhabdomyosarcoma cells after inoculation into NIH Swiss mice treated with antithymocyte serum. Proc Natl Acad Sci U S A. 1973 Mar;70(3):859–862. doi: 10.1073/pnas.70.3.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Vesterberg O., Svensson H. Isoelectric fractionation, analysis, and characterization of ampholytes in natural pH gradients. IV. Further studies on the resolving power in connection with separation of myoglobins. Acta Chem Scand. 1966;20(3):820–834. doi: 10.3891/acta.chem.scand.20-0820. [DOI] [PubMed] [Google Scholar]
  41. WEIGLE W. O. The immune response of rabbits tolerant to bovine serum albumin to the injection of other heterologous serum albumins. J Exp Med. 1961 Jul 1;114:111–125. doi: 10.1084/jem.114.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Weber K., Kuter D. J. Reversible denaturation of enzymes by sodium dodecyl sulfate. J Biol Chem. 1971 Jul 25;246(14):4504–4509. [PubMed] [Google Scholar]
  43. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]
  44. Weiner A. M., Platt T., Weber K. Amino-terminal sequence analysis of proteins purified on a nanomole scale by gel electrophoresis. J Biol Chem. 1972 May 25;247(10):3242–3251. [PubMed] [Google Scholar]
  45. Wright B. S., O'Brien P. A., Shibley G. P., Mayyasi S. A., Lasfargues J. C. Infection of an established mouse bone marrow cell line (JLS-V9) with Rauscher and Moloney murine leukemia viruses. Cancer Res. 1967 Sep;27(9):1672–1677. [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES