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. 1994 Oct 1;180(4):1511–1516. doi: 10.1084/jem.180.4.1511

Retroviral infection of neonatal Peyer's patch lymphocytes: the mouse mammary tumor virus model

PMCID: PMC2191709  PMID: 7931081

Abstract

Mouse mammary tumor virus is known to infect newborn mice via mother's milk. A proposed key step for viral spread to the mammary gland is by the infection of lymphocytes. We show here that although in suckling mice retroviral proteins are found in all epithelial cells of the gut, viral DNA is exclusively detectable in the Peyer's patches. As early as 5 d after birth the infection leads to a superantigen response in the Peyer's patches but not in other lymphoid organs draining the intestine. Viral DNA can be detected before the superantigen response and becomes first evident in the Peyer's patches followed by mesenteric lymph nodes and finally all lymphoid organs.

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Selected References

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  1. Acha-Orbea H., Held W., Waanders G. A., Shakhov A. N., Scarpellino L., Lees R. K., MacDonald H. R. Exogenous and endogenous mouse mammary tumor virus superantigens. Immunol Rev. 1993 Feb;131:5–25. doi: 10.1111/j.1600-065x.1993.tb01527.x. [DOI] [PubMed] [Google Scholar]
  2. Acha-Orbea H., Shakhov A. N., Scarpellino L., Kolb E., Müller V., Vessaz-Shaw A., Fuchs R., Blöchlinger K., Rollini P., Billotte J. Clonal deletion of V beta 14-bearing T cells in mice transgenic for mammary tumour virus. Nature. 1991 Mar 21;350(6315):207–211. doi: 10.1038/350207a0. [DOI] [PubMed] [Google Scholar]
  3. Beutner U., Frankel W. N., Cote M. S., Coffin J. M., Huber B. T. Mls-1 is encoded by the long terminal repeat open reading frame of the mouse mammary tumor provirus Mtv-7. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5432–5436. doi: 10.1073/pnas.89.12.5432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bevilacqua G., Marchetti A., Biondi R. Ultrastructural features of the intestinal absorption of mouse mammary tumor virus in newborn BALB/cfRIII mice. Gastroenterology. 1989 Jan;96(1):139–145. doi: 10.1016/0016-5085(89)90774-9. [DOI] [PubMed] [Google Scholar]
  5. Bittner J. J. SOME POSSIBLE EFFECTS OF NURSING ON THE MAMMARY GLAND TUMOR INCIDENCE IN MICE. Science. 1936 Aug 14;84(2172):162–162. doi: 10.1126/science.84.2172.162. [DOI] [PubMed] [Google Scholar]
  6. CLARK S. L., Jr The ingestion of proteins and colloidal materials by columnar absorptive cells of the small intestine in suckling rats and mice. J Biophys Biochem Cytol. 1959 Jan 25;5(1):41–50. doi: 10.1083/jcb.5.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Choi Y., Kappler J. W., Marrack P. A superantigen encoded in the open reading frame of the 3' long terminal repeat of mouse mammary tumour virus. Nature. 1991 Mar 21;350(6315):203–207. doi: 10.1038/350203a0. [DOI] [PubMed] [Google Scholar]
  8. Festenstein H., Berumen L. BALB.D2-Mlsa--a new congenic mouse strain. Transplantation. 1984 Mar;37(3):322–324. doi: 10.1097/00007890-198403000-00024. [DOI] [PubMed] [Google Scholar]
  9. Golovkina T. V., Chervonsky A., Dudley J. P., Ross S. R. Transgenic mouse mammary tumor virus superantigen expression prevents viral infection. Cell. 1992 May 15;69(4):637–645. doi: 10.1016/0092-8674(92)90227-4. [DOI] [PubMed] [Google Scholar]
  10. Gonnella P. A., Neutra M. R. Membrane-bound and fluid-phase macromolecules enter separate prelysosomal compartments in absorptive cells of suckling rat ileum. J Cell Biol. 1984 Sep;99(3):909–917. doi: 10.1083/jcb.99.3.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hainaut P., Francois C., Calberg-Bacq C. M., Vaira D., Osterrieth P. M. Peroral infection of suckling mice with milk-borne mouse mammary tumour virus: uptake of the main viral antigens by the gut. J Gen Virol. 1983 Dec;64(Pt 12):2535–2548. doi: 10.1099/0022-1317-64-12-2535. [DOI] [PubMed] [Google Scholar]
  12. Held W., Shakhov A. N., Izui S., Waanders G. A., Scarpellino L., MacDonald H. R., Acha-Orbea H. Superantigen-reactive CD4+ T cells are required to stimulate B cells after infection with mouse mammary tumor virus. J Exp Med. 1993 Feb 1;177(2):359–366. doi: 10.1084/jem.177.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Held W., Shakhov A. N., Waanders G., Scarpellino L., Luethy R., Kraehenbuhl J. P., MacDonald H. R., Acha-Orbea H. An exogenous mouse mammary tumor virus with properties of Mls-1a (Mtv-7). J Exp Med. 1992 Jun 1;175(6):1623–1633. doi: 10.1084/jem.175.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Held W., Waanders G. A., Shakhov A. N., Scarpellino L., Acha-Orbea H., MacDonald H. R. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell. 1993 Aug 13;74(3):529–540. doi: 10.1016/0092-8674(93)80054-i. [DOI] [PubMed] [Google Scholar]
  15. Keren D. F. Antigen processing in the mucosal immune system. Semin Immunol. 1992 Aug;4(4):217–226. [PubMed] [Google Scholar]
  16. Kraehenbuhl J. P., Bron C., Sordat B. Transfer of humoral secretory and cellular immunity from mother to offspring. Curr Top Pathol. 1979;66:105–157. doi: 10.1007/978-3-642-67205-7_4. [DOI] [PubMed] [Google Scholar]
  17. Kraehenbuhl J. P., Neutra M. R. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol Rev. 1992 Oct;72(4):853–879. doi: 10.1152/physrev.1992.72.4.853. [DOI] [PubMed] [Google Scholar]
  18. Liao N. S., Maltzman J., Raulet D. H. Positive selection determines T cell receptor V beta 14 gene usage by CD8+ T cells. J Exp Med. 1989 Jul 1;170(1):135–143. doi: 10.1084/jem.170.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Marrack P., Kushnir E., Kappler J. A maternally inherited superantigen encoded by a mammary tumour virus. Nature. 1991 Feb 7;349(6309):524–526. doi: 10.1038/349524a0. [DOI] [PubMed] [Google Scholar]
  20. Molina I. J., Cannon N. A., Hyman R., Huber B. T. Macrophages and T cells do not express Mlsa determinants. J Immunol. 1989 Jul 1;143(1):39–44. [PubMed] [Google Scholar]
  22. Payne J., Huber B. T., Cannon N. A., Schneider R., Schilham M. W., Acha-Orbea H., MacDonald H. R., Hengartner H. Two monoclonal rat antibodies with specificity for the beta-chain variable region V beta 6 of the murine T-cell receptor. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7695–7698. doi: 10.1073/pnas.85.20.7695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pullen A. M., Choi Y., Kushnir E., Kappler J., Marrack P. The open reading frames in the 3' long terminal repeats of several mouse mammary tumor virus integrants encode V beta 3-specific superantigens. J Exp Med. 1992 Jan 1;175(1):41–47. doi: 10.1084/jem.175.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tsubura A., Inaba M., Imai S., Murakami A., Oyaizu N., Yasumizu R., Ohnishi Y., Tanaka H., Morii S., Ikehara S. Intervention of T-cells in transportation of mouse mammary tumor virus (milk factor) to mammary gland cells in vivo. Cancer Res. 1988 Nov 15;48(22):6555–6559. [PubMed] [Google Scholar]
  25. Waanders G. A., Shakhov A. N., Held W., Karapetian O., Acha-Orbea H., MacDonald H. R. Peripheral T cell activation and deletion induced by transfer of lymphocyte subsets expressing endogenous or exogenous mouse mammary tumor virus. J Exp Med. 1993 May 1;177(5):1359–1366. doi: 10.1084/jem.177.5.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wolf J. L., Rubin D. H., Finberg R., Kauffman R. S., Sharpe A. H., Trier J. S., Fields B. N. Intestinal M cells: a pathway for entry of reovirus into the host. Science. 1981 Apr 24;212(4493):471–472. doi: 10.1126/science.6259737. [DOI] [PubMed] [Google Scholar]
  27. Woodland D. L., Happ M. P., Gollob K. J., Palmer E. An endogenous retrovirus mediating deletion of alpha beta T cells? Nature. 1991 Feb 7;349(6309):529–530. doi: 10.1038/349529a0. [DOI] [PubMed] [Google Scholar]

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