MMTV infectious cycle and the contribution of virus-encoded proteins to transformation of mammary tissue

Journal of Mammary Gland Biology and Neoplasia

Volumn 13, Issue 3, 2008, Pages 299-307

  Ross, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Mammary tumor; Mouse model; Retrovirus

Indexed keywords

ENVELOPE PROTEIN; VIRUS PROTEIN;

ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST MILK; BREAST TUMOR; CANCER MODEL; GENETIC RESISTANCE; HUMAN; LONG TERMINAL REPEAT; LYMPHOID CELL; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; ONCOGENE; RETROVIRUS INFECTION; TRANSGENE; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS TRANSMISSION;

ANIMALS; BREAST NEOPLASMS; GENOME, VIRAL; HUMANS; LYMPHOCYTES; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MODELS, BIOLOGICAL; MODELS, GENETIC; TERMINAL REPEAT SEQUENCES; TRANSGENES; VIRAL PROTEINS;

EID: 50949096842     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10911-008-9090-8     Document Type: Article

References (82)

1. Bittner JJ. Some possible effects of nursing on the mammary gland tumor incidence in mice. Science 1936;84:162. doi: 10.1126/science.84.2172.162.
2. Nandi S, McGrath CM. Mammary neoplasia in mice. Adv Cancer Res. 1973;17:353-414. doi: 10.1016/S0065-230X(08)60535-7.
3. Ross SR. Using genetics to probe host-virus interactions: The mouse mammary tumor virus model. Microbes Infect. 2000;2:1215-23. doi: 10.1016/ S1286-4579(00)01275-2.
4. Mink S, Hartig E, Jennewein P, Doppler W, Cato ACB. A mammary cell-specific enhancer in mouse mammary tumor virus DNA is composed of multiple regulatory elements including binding sites for CTF/NF-1 and novel transcription factor, mammary cell-activating factor. Mol Cell Biol. 1992;11:4906-18.
5. Mok E, Golovkina TV, Ross SR. A mouse mammary tumor virus (MMTV) mammary gland enhancer confers tissue-specific, but not lactation-dependent expression in transgenic mice. J Virol. 1992;66:7529-32.
6. Reuss FU, Coffin JM. Stimulation of mouse mammary tumor virus superantigen expression by an intragenic enhancer. Proc Natl Acad Sci U S A. 1995;92:9293-7. doi: 10.1073/pnas.92.20.9293.
7. Zhu Q, Maitra U, Johnston D, Lozano M, Dudley JP. The homeodomain protein CDP regulates mammary-specific gene transcription and tumorigenesis. Mol Cell Biol. 2004;24:4810-23. doi: 10.1128/ MCB.24.11.4810-4823.2004.
8. Vicent GP, Ballare C, Zaurin R, Saragueta P, Beato M. Chromatin remodeling and control of cell proliferation by progestins via cross talk of progesterone receptor with the estrogen receptors and kinase signaling pathways. Ann N Y Acad Sci. 2006;1089:59-72. doi: 10.1196/ annals.1386.025.
9. Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses. Cold Spring Harbor (NY): CSHL Press; 1997
10. Payne SL, Elder JH. The role of retroviral dUTPases in replication and virulence. Curr Protein Pept Sci. 2001;2:381-8. doi: 10.2174/ 1389203013381008.
11. Ross SR, Schofield JJ, Farr CJ, Bucan M. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc Natl Acad Sci U S A. 2002;99:12386-90. doi: 10.1073/pnas.192360099.
12. Schulman HMPPWA, Gauthier Y, Shyamala G. Transferrin receptor and ferritin levels during murine mammary gland development. Biochim Biophys Acta. 1989;1010:1-6. doi: 10.1016/0167-4889(89)90176-6.
13. Futran J, Kemp JD, Field EH, Vora A, Ashman RF. Transferrin receptor synthesis is an early event in B cell activation. J Immunol. 1989;143:787-92.
14. Brekelmans P, van Soest P, Voerman J, Platenburg PP, Leenen PJ, van Ewijk W. Transferrin receptor expression as a marker of immature cycling thymocytes in the mouse. Cell Immunol. 1994;159:331-9. doi: 10.1006/ cimm.1994.1319.
15. Ross SR. MMTV and the immune system. Adv Pharm. 1997;39:21-46.
16. Rassa JC, Meyers JL, Zhang Y, Kudaravalli R, Ross SR. Murine retroviruses activate B cells via interaction with Toll-like receptor 4. Proc Natl Acad Sci U S A. 2002;99:2281-6. doi: 10.1073/pnas.042355399.
17. Burzyn D, Rassa JC, Kim D, Nepomnaschy I, Ross SR, Piazzon I. Toll-like receptor 4-dependent activation of dendritic cells by a retrovirus. J Virol. 2004;78:576-84. doi: 10.1128/JVI.78.2.576-584.2004.
18. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783-801. doi: 10.1016/j.cell.2006.02.015.
19. Mertz JA, Simper MS, Lozano MM, Payne SM, Dudley JP. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J Virol. 2005;79:14737-47. doi: 10.1128/ JVI.79.23.14737-14747.2005.
20. Indik S, Gunzburg WH, Salmons B, Rouault F. A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virol. 2005;337:1-6. doi: 10.1016/j.virol.2005.03.040.
21. Salmons B, Erfle V, Brem G, Günzburg WH. Naf, a trans-regulating negative-acting factor within the mouse mammary tumor virus open reading frame region. J Virol. 1990;64:6355-9.
22. Rouault F, Nejad Asl SB, Rungaldier S, Fuchs E, Salmons B, Gunzburg WH. Promoter complex in the central part of the mouse mammary tumor virus long terminal repeat. J Virol. 2007;81:12572-81. doi: 10.1128/ JVI.00351-07.
23. Michalides R, van Nie R, Nusse R, Hynes NE, Groner B. Mammary tumor virus induction loci in GR and DBAf mice contain one provirus of the mouse mammary tumor virus. Cell 1981;23:165-73. doi: 10.1016/ 0092-674(81)90281-6.
24. Morris VL, Medeiros E, Ringold GM, Bishop JM, Varmus HE. Comparison of mouse mammary tumor virus-specific DNA in inbred, wild and Asian mice, and in tumors and normal organs from inbred mice. J Mol Biol. 1977;114:73-91. doi: 10.1016/0022-836(77)90284-4.
25. Baillie GJ, van de Lagemaat LN, Baust C, Mager DL. Multiple groups of endogenous betaretroviruses in mice, rats and other mammals. J Virol. 2004;78:5784-98. doi: 10.1128/JVI.78.11.5784-5798.2004.
26. Martin P, Ruiz SR, Martinez del Hoyo G, Anjuere F, Vargas HH, Lopez-Bravo M, et al. Dramatic increase in lymph node dendritic cell numbers during infection by the mouse mammary tumor virus occurs by a CD62L-dependent blood-borne DC recruitment. Blood 2002;99:1282-8. doi: 10.1182/blood.V99.4.1282.
27. Vacheron S, Luther SJ, Acha-Orbea H. Preferential infection of immature dendritic cells and B cells by mouse mammary tumor virus. J Immunol. 2002;168:3470-6.
28. Courreges MC, Burzyn D, Nepomnaschy I, Piazzon I, Ross SR. Critical role of dendritic cells in mouse mammary tumor virus in vivo infection. J Virol. 2007;81:3769-77. doi: 10.1128/JVI.02728-06.
29. O'Neill LAJ. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE 2000;2000(44):1-11.
30. Jude BA, Pobezinskaya Y, Bishop J, Parke S, Medzhitov RM, Chervonsky AV, et al. Subversion of the innate immune system by a retrovirus. Nat Immunol. 2003;4:573-8. doi: 10.1038/ni926.
31. Held W, Waanders G, Shakhov AN, Scarpellino L, Acha-Orbea H, MacDonald HR. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell 1993;74:529-40. doi: 10.1016/0092-8674(93)80054-I.
32. Ignatowicz L, Kappler J, Marrack P. The effects of chronic infection with a superantigen-producing virus. J Exp Med. 1992;175:917-23. doi: 10.1084/jem.175.4.917.
33. Golovkina TV, Dudley JP, Ross SR. Superantigen activity is need for mouse mammary tumor virus spread within the mammary gland. J Immunol. 1998;161:2375-82.
34. Finke D, Acha-Orbea H. Differential migration of in vivo primed B and T lymphocytes to lymphoid and non-lymphoid organs. Eur J Immunol. 2001;31:2603-11. doi: 10.1002/ 1521-4141(200109)31:9<2603::AID-IMMU2603>3.0.CO;2-8.
35. Callahan R, Smith GH. MMTV-induced mammary tumorigenesis: Gene discovery, progression to malignancy and cellular pathways. Oncogene 2000;19:992-1001. doi: 10.1038/sj.onc.1203276.
36. Faschinger A, Rouault F, Sollner J, Lukas A, Salmons B, Gunzburg WH, et al. Mouse mammary tumor virus integration site selection in human and mouse genomes. J Virol. 2008;82:13601-7.
37. Golovkina TV, Prescott JA, Ross SR. Mouse mammary tumor virus-induced tumorigenesis in sag transgenic mice: A laboratory model of natural selection. J Virol. 1993;67:7690-4.
38. Katz E, Lareef MH, Rassa JC, Grande SM, King LB, Russo J, et al. MMTV Env encodes an ITAM responsible for transformation of mammary epithelial cells in three-dimensional culture. J Exp Med. 2005;201:431-9. doi: 10.1084/jem.20041471.
39. Ross SR, Schmidt JW, Katz E, Cappelli L, Hultine S, Gimmotty P, et al. An immunoreceptor tyrosine activation motif in the Mouse Mammary Tumor Virus envelope protein plays a role in virus-induced mammary tumors. J Virol. 2006;80:9000-8. doi: 10.1128/JVI.00788-06.
40. Lu J, Lin WH, Chen SY, Longnecker R, Tsai SC, Chen CL, et al. Syk tyrosine kinase mediates Epstein-Barr Virus latent membrane protein 2A-induced cell migration in epithelial cells. J Biol Chem. 2006;281:8806-14. doi: 10.1074/jbc.M507305200.
41. Morrison JA, Raab-Traub N. Roles of the ITAM and PY motifs of Epstein-Barr Virus latent membrane protein 2A in the inhibition of epithelial cell differentiation and activation of β -catenin signaling. J Virol. 2005;79:2375-82. doi: 10.1128/ JVI.79.4.2375-2382.2005.
42. Lee H, Guo J, Li M, Choi JK, DeMaria M, Rosenzweig M, et al. Identification of an immunoreceptor tyrosine-based activation motif of K1 transforming protein of Kaposi's sarcoma-associated herpesvirus. Mol Cell Biol. 1998;18:5219-28.
43. Maeda N, Palmarini M, Murgia C, Fan H. Direct transformation of rodent fibroblasts by jaagsiekte sheep retrovirus DNA. Proc Natl Acad Sci U S A. 2001;98:4449-54. doi: 10.1073/pnas.071547598.
44. Rai SK, Duh FM, Vigdorovich V, Danilkovitch-Miagkova A, Lerman MI, Miller AD. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc Natl Acad Sci U S A. 2001;98:4443-8. doi: 10.1073/pnas.071572898.
45. Wootton SK, Halbert CL, Miller AD. Sheep retrovirus structural protein induces lung tumours. Nature 2005;434:904-7. doi: 10.1038/nature03492.
46. Michalides R, Wagenaar E, Hilkens J, Hilgers J, Groner B, Hynes NE. Acquisition of proviral DNA of mouse mammary tumor virus in thymic leukemia cells from GR mice. J Virol. 1982;43:819-29.
47. Yanagawa SI, Kakimi K, Tanaka H, Murakami A, Nakagawa Y, Kubo Y, et al. Mouse mammary tumor virus with rearranged long terminal repeats causes murine lymphomas. J Virol. 1993;67:112-8.
48. Bhadra S, Lozano MM, Dudley JP. Conversion of mouse mammary tumor virus to a lymphomagenic virus. J Virol. 2005;79:12592-6. doi: 10.1128/ JVI.79.19.12592-12596.2005.
49. Yanagawa S, Lee JS, Kakimi K, Matsuda Y, Honjo T, Ishimoto A. Identification of Notch1 as a frequent target for provirus insertional mutagenesis in T-cell lymphomas induced by leukemogenic mutants of mouse mammary tumor virus. J Virol. 2000;74:9786-91. doi: 10.1128/ JVI.74.20.9786-9791.2000.
50. Broussard DR, Mertz JA, Lozano M, Dudley JP. Selection for c-myc integration sites in polyclonal T-cell lymphomas. J Virol. 2002;76:2087-99. doi: 10.1128/jvi.76.5.2087-2099.2002.
51. Bentvelzen P, Brinkhof J, Haaijman JJ. Genetic control of endogenous murine mammary tumour viruses reinvestigated. Eur J Cancer 1978;14:1137-47. doi: 10.1016/0014-2964(78)90070-1.
52. Outzen HC, Morrow D, Shultz LD. Attenuation of exogenous murine mammary tumor virus virulence in the C3H/HeJ mouse substrain bearing the Lps mutation. J Natl Cancer Inst. 1985;75:917-23.
53. Held W, Waanders GA, MacDonald HR, Acha-Orbea H. MHC class II hierarchy of superantigen presentation predicts efficiency of infection with mouse mammary tumor virus. Int Immunol. 1994;6:1403-7. doi: 10.1093/intimm/ 6.9.1403.
54. Pucillo C, Cepeda R, Hodes RJ. Expression of a MHC Class II transgene determines superantigenicity and susceptibility to mouse mammary tumor virus infection. J Exp Med. 1993;178:1441-5. doi: 10.1084/jem.178.4.1441.
55. Beutner U, Draus E, Kitamura D, Rajewsky K, Huber BT. B cells are essential for murine mammary tumor virus transmission, but not for presentation of endogenous superantigens. J Exp Med. 1994;179:1457-66. doi: 10.1084/jem.179.5.1457.
56. Pobezinskaya Y, Chervonsky AV, Golovkina TV. Initial stages of mammary tumor virus infection are superantigen independent. J Immunol. 2004;172:5582-7.
57. Purdy A, Case L, Duvall M, Overstrom-Coleman M, Monnier N, Chervonsky A, et al. Unique resistance of I/LnJ mice to a retrovirus is due to sustained IFN-gamma dependent production of virus-neutralizing antibodies. J Exp Med. 2003;197:233-43. doi: 10.1084/jem.20021499.
58. Okeoma CM, Shen M, Ross SR. A novel block to mouse mammary tumor virus infection of lymphocytes in B10.BR mice. J Virol. 2008;82:1314-22. doi: 10.1128/JVI.01848-07.
59. MacDearmid CC, Case LK, Starling CL, Golovkina TV. Gradual elimination of retroviruses in YBR/Ei mice. J Virol. 2006;80:2206-15. doi: 10.1128/ JVI.80.5.2206-2215.2006.
60. Bhadra S, Lozano MM, Payne SM, Dudley JP. Endogenous MMTV proviruses induce susceptibility to both viral and bacterial pathogens. PLoS Pathog. 2006;2w:e128. doi: 10.1371/journal.ppat.0020128.
61. Czarneski J, Meyers J, Peng T, Abraham V, Ross SR. Interleukin-4 up-regulates mouse mammary tumor virus expression but is not required for in vivo virus spread. J Virol. 2001;75:11886-90. doi: 10.1128/ JVI.75.23.11886-11890.2001.
62. Day NK, Witkin SS, Sarkar NH, Kinne D, Jussawalla DJ, Levin A, et al. Antibodies reactive with murine mammary tumor virus in sera of patients with breast cancer: Geographic and family studies. Proc Natl Acad Sci U S A. 1981;78:2483-7. doi: 10.1073/pnas.78.4.2483.
63. Mesa-Tejada R, Oster MW, Fenoglio CM, Magidson J, Spiegelman S. Diagnosis of primary breast carcinoma through immunohistochemical detection of antigen related to mouse mammary tumor virus in metastatic lesions: A report of two cases. Cancer 1982;49:261-8. doi: 10.002/ 1097-0142(19820115)49:2<261::AID-CNCR2820490211>3.0.CO;2-3.
64. Goedert JJ, Rabkin CS, Ross SR. Prevalence of serologic reactivity against four strains of mouse mammary tumor virus among U.S. women with breast cancer. Br J Cancer 2006;94:548-51. doi: 10.1038/sj.bjc.6602977.
65. Pogo BGT, Melana SM, Holland JF, Mandeli JF, Polotti S, Casalini P, et al. Sequences homologous to the mouse mammary tumor virus env gene in human breast cancer correlate with overexpression of laminin receptor. Clin Cancer Res. 1999;5:2108-11.
66. Wang Y, Holland JF, Bleiweiss IJ, Melana S, Liu X, Pelisson I, et al. Detection of mammary tumor virus ENV gene-like sequences in human breast cancer. Cancer Res. 1995;35:5173-9.
67. Etkind P, Du J, Khan A, Pillitteri J, Wiernik PH. Mouse mammary tumor virus-like ENV gene sequences in human breast tumors and in a lymphoma of a breast cancer patient. Clin Cancer Res. 2000;6:1273-8.
68. Liu B, Wang Y, Melana SM, Pelisson I, Najfeld V, Holland JF, et al. Identification of a proviral structure in human breast cancer. Cancer Res. 2001;61:1754-9.
69. Mant C, Hodgson S, Hobday R, D'Arrigo C, Cason J. A viral aetiology for breast cancer: Time to re-examine the postulate. Intervirol. 2003;47:2-13. doi: 10.1159/000076636.
70. Witt A, Hartmann B, Marton E, Zeillinger R, Schreiber M, Kubista E. The mouse mammary tumor virus-like env gene sequence is not detectable in breast cancer tissue of Austrian patients. Oncol Rep. 2003;10:1025-9.
71. Bindra A, Muradrasoli S, Kisekka R, Nordgren H, Warnberg F, Blomberg J. Search for DNA of exogenous mouse mammary tumor virus-related virus in human breast cancer samples. J Gen Virol. 2007;88:1806-9. doi: 10.1099/ vir.0.82767-0.
72. Lasfargues EY, Coutinho WG, Dion AS. A human breast tumor cell line (BT474) that supports mammary tumor virus replication. In Vitro 1979;15:723-8. doi: 10.1007/BF02618252.
73. Howard DK, Schlom J. Isolation of a series of novel variants of murine mammary tumor viruses with broadened host range. Int J Cancer 1980;25:647-54. doi: 10.1002/ijc.2910250515.
74. Wang E, Albritton L, Ross SR. Identification of the segments of the mouse transferrin receptor 1 required for mouse mammary tumor virus infection. J Biol Chem. 2006;281:10243-9. doi: 10.1074/jbc.M511572200.
75. Zhang Y, Rassa JC, deObaldia EM, Albritton L, Ross SR. Identification of the mouse mammary tumor virus envelope receptor-binding domain. J Virol. 2003;77:10468-78. doi: 10.1128/JVI.77.19.10468-10478.2003.
76. Indik S, Gunzburg WH, Salmons B, Rouault F. Mouse mammary tumor virus infects human cells. Cancer Res. 2005;65:6651-9. doi: 10.1158/ 0008-5472.CAN-04-2609.
77. Indik S, Gunzburg WH, Kulich P, Salmons B, Rouault F. Rapid spread of mouse mammary tumor virus in cultured human breast cells. Retrovirol. 2007;4:73. doi: 10.1186/1742-4690-4-73.
78. Titus-Ernstoff L, Egan KM, Newcomb PA, Baron JA, Stampfer M, Greenberg ER, et al. Exposure to breast milk in infancy and adult breast cancer risk. J Natl Cancer Inst. 1998;12:921-4. doi: 10.1093/jnci/90.12.921.
79. Kampert JB, Whittemore AS, Paffenbarger RS Jr. Combined effect of childbearing, menstrual events, and body size on age-specific breast cancer risk. Am J Epidemiol. 1988;128:962-79.
80. MacMahon B, Cole P, Brown J. Etiology of human breast cancer: A review. Natl Canc Inst. 1973;50:21-42.
81. Stewart THM, Sage RD, Stewart AFR, Cameron DW. Breast cancer incidence highest in the range of one species of house mouse, Mus domesticus. Br J Cancer 2000;82:446-51. doi: 10.1054/bjoc.1999.0941.
82. Luther SA, Maillard I, Luthi F, Scarpellino L, Diggelmann H, Acha-Orbea H. Early neutralizing antibody response against mouse mammary tumor virus; critical role of viral infection and superantigen-reactive T cells. J Immunol. 1997;159:2807-14.