Biological Trace Element Research

, Volume 56, Issue 1, pp 131–142 | Cite as

Possibilities of a viral etiology for human breast cancer

A review
  • Beatriz G. -T. Pogo
  • James F. Holland


Previous studies related mouse mammary tumor virus (MMTV) to human breast cancer. However, the presence of human endogenous retroviruses (HERs) confounded these results. We selected a 660-bp sequence of the MMTVenv gene with low homology to HER (or any other known gene) and searched for a sequence homologous to it, using the polymerase chain reaction (PCR). The 660-bp sequence was detected in 131 (39%) of 335 unselected breast cancers, in 2 (6.9%) of 29 fibroadenomas, and in 2 (1.65%) of 121 normal breast specimens. The sequence was not present in normal tissues, or in other human cancers or cell lines.

Cloning and sequencing of the 660-bp sequence revealed that it is 95–98% homologous to MMTVenv gene, but not the known HERs or other viral or human gene. Southern blot hybridization using labeled cloned sequences demonstrated that the 660-bp sequence was present in very low copy number as a 6–8 kbEcoRI fragment only in breast cancer samples and in some of the human breast cancer cell lines that were positive by PCR. Preliminary experiments using reverse transcriptase (RT)-PCR indicated that expression of the 660-bp sequence can be detected in 65% of the positive tumors. We were also able to identify in breast cancer DNA a segment of 1.6 kb comprising LTR andenv gene sequences, which are homologous to MMTV, but not to the HERs. The origin of the MMTV-like sequences in tumor DNA could be the result of integrated MMTV-like sequences derived from a human mammary virus.

Index Entries

Breast cancer retroviral sequences 


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  1. 1.
    Y. Miki, J. Swensen, D. Shattuck-Eidens, P. A. Futreal, K. Harshman, et al., A strong candidate for the breast and ovarian cancer susceptibility Gene RRCA1,Science 266, 66–71 (1994).PubMedCrossRefGoogle Scholar
  2. 2.
    R. Wooster, S. L. Neuhausen, J. Mangion, Y. Quirk, D. Ford, et al., Localization of a breast cancer susceptibility gene BRCA2, chromosome 13q12–13.Science 265, 2088–2090 (1994).PubMedCrossRefGoogle Scholar
  3. 3.
    K. Hoskins and F. L. Weber, Recent advances in breast cancer biology.Curr. Opinion Oncol. 7, 495–500 (1995).CrossRefGoogle Scholar
  4. 4.
    Y. Chen, C-F Chen, D. J. Riley, D. C. Allred, P-L Chen, D. Von Hoff, C. K. Osborne, and W-H Lee, Aberrant Subcellular localization of BRCA-1 in breast cancer.Science 270, 789–791 (1995).PubMedCrossRefGoogle Scholar
  5. 5.
    N. Collins, R. McManus, R. Wooster, J. Mangion, S. Seal, S. R. Lakhani, W. Orminston, P. A. Daly, D. Ford, D. F. Easton, and M. R. StrattonOncogene 10, 1673–1675 (1995).PubMedGoogle Scholar
  6. 6.
    R. A. Jensen, M. E. Thompson, T. L. Jetton, C. I. Szabo, R. van der Meer, B. Helou, S. R. Tronick, D. L. Page, M-C King, and J. T. Holt, BRCA1 is secreted and exhibits properties of a granin.Nature Genet. 12, 303–308 (1996).PubMedCrossRefGoogle Scholar
  7. 7.
    I. Bieche, M. H. Champene, D. Matifas, C. Cropp, R. Callahan, and R. Lidereau, Maintenance of p53 alterations throughout breast cancer progression.Cancer Res. 53, 1990–199 (1993).PubMedGoogle Scholar
  8. 8.
    A. M. Davidoff, B-J M. Kerns, J. D. Iglehart, and J. R. Marks, Maintenance of p53 alterations throughout breast cancer progression.Cancer Res. 51, 2605–2610 (1991).PubMedGoogle Scholar
  9. 9.
    D. J. Slamon, W. Godolphin, L. A. Jones, J. A. Holt, S. G. Wong, D. E. Keith, W. J. Levin, S. G. Stuart, J. Udove, A. Ullrich, and M. F. Press, Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene.Science 244, 707–712 (1989).PubMedCrossRefGoogle Scholar
  10. 10.
    D. J. Slamon, G. M. Clark, S. G. Wong, W. J. Levin, A. Ullrich, and W. L. McGuire, Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene.Science 235, 177–182 (1987).PubMedCrossRefGoogle Scholar
  11. 11.
    G. Casey, R. Smith, D. McGillivray, G. Peters, and C. Dickson, Characterization and chromosome assignments of the human homolog of int-2, a potential protooncogene.Mol. and Cell. Biol. 6, 502–510 (1986).Google Scholar
  12. 12.
    R. Lidereau, R. Callahan, C. Dickson, G. Peters, C. Escot, and I. U. Ali, Amplification of the int-2 gene in primary human breast tumors.Oncogene Res. 2, 285–291 (1988).PubMedGoogle Scholar
  13. 13.
    D. J. Zhou, G. Casey, and M. J. Cline, Amplification of human int-2 in breast cancers and squamous carcinomas.Oncogene 2, 279–282 (1988).PubMedGoogle Scholar
  14. 14.
    D. S. Liscia, G. R. Merlo, C. Garrett, D. French, R. Marini-Constantini, and R. Callahan, Expression of int-2 mRNA in human tumors amplified at the int-2 locus.Oncogene 4, 1219–1224 (1989).PubMedGoogle Scholar
  15. 15.
    Lammie, G. A., Fantl, V., Smith, R., Schuuring, E., Brookes, S., Michalides, R., Dickson, R., Arnold, A., and Peters, G., D11S287, a putative oncogene on chromosome 11q13, is amplified and expressed in squamous cell and mammary carcinomas and linked to BCL-1,Oncogene 6, 439–444 (1991).PubMedGoogle Scholar
  16. 16.
    M. C. Yoshida, M. Wada, H. Satoh, T. Yoshida, H. Sakamoto, K. Miyagawa, J. Yokota, T. Koda, M. Kakinuma, T. Sugimura, and M. Terada, Human HST1 (HSTF1) gene maps to chromosome band 11q13 and coamplifies with the INT2 gene in human cancer.Proc. Natl. Acad. Sci. USA85, 4861–4864 (1988).PubMedCrossRefGoogle Scholar
  17. 17.
    M. F. Buckley, K. J. E. Sweeney, J. A. Hamilton, R. L. Sini, D. L. Manning, R. I. Nicholson, A. de Fazio, C. K. W. Watts, E. A. Musgrove, and R. L. Sutherland, Expression and Amplification of cyclin genes in human breast cancer.Oncogene 8, 2127–2133 (1983).Google Scholar
  18. 18.
    D. Weinstat-Saslow, M. J. Merino, R. E. Manrow, J. A. Lawrence, R. F. Bluth, K. D. Winttenbel, J. F. Simpson, D. L. Page, and P. S. Steeg, Overexpression of cyclin D mRNA distinguishes invasive and in situ breast carcinomas from non-malignant lesions.Nature Med. 1, 1257–1260 (1995).PubMedCrossRefGoogle Scholar
  19. 19.
    S. Lejeune, E. E. Huguet, A. Hamby, R. Poulsom, and A. L. Harris, Wnt5a cloning, expression and up-regulation in human primary breast cancer.Clin. Cancer Res. 1, 215–222 (1995).PubMedGoogle Scholar
  20. 20.
    V. Papa, F. Gliozzo, G. M. Clark, W. L. McGuire, D. Moore, F-Y Yoko, R. Vigneri, I. D. Goldfine, and V. Pezzino, Insulin growth factor-I receptors are overexpressed and predict a low risk in human breast cancer.Cancer Research 53, 3736–3740 (1993).PubMedGoogle Scholar
  21. 21.
    R. Pelligrini, S. Martignone, E. Tagliabue, D. Belotti, R. Bufalino, N. Cascinelli, S. Menard, and M. I. Colnaghi, Prognostic significance of laminin production in relation with its receptor expression in human breast carcinomas.Breast Cancer Res. and Treatment 35, 195–199 (1995).CrossRefGoogle Scholar
  22. 22.
    M. M. Zutter, S. A. Santoro, W. D. Staatz, and Y. L. Tsung, Reexpression of the α2β1 integrin abrogates the malignant phenotype of breast carcinoma cells.Proc. Natl. Acad. Sci. USA 92, 7411–7415 (1995).PubMedCrossRefGoogle Scholar
  23. 23.
    M. A. Schwartz, Signaling by integrins.Cancer Res. 53, 1503–1506 (1993).PubMedGoogle Scholar
  24. 24.
    J. R. Graff, J. G. Herman, R. G. Lapidus, H. Chopra, R. Xu, D. F. Jarrad, W. B. Isaacs, P. M. Pitha, N. E. Davidson, and S. B. Baylin, E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas.Cancer Research 55, 5195–5199 (1995).PubMedGoogle Scholar
  25. 25.
    T. Sato, H. Saito, J. Swensen, A. Olifant, C. Wood, D. Danner, T. Sakamoto, K. Takita, F. Kasumi, Y. Miki, M. Skolnick, and Y. Nakamura, The human prohibitin gene located on chromosone 17q21 is mutated in sporadic breast cancer.Cancer Res. 52, 1643–1646 (1992).PubMedGoogle Scholar
  26. 26.
    E. Larsson, N. Kato, and M. Cohen, Human Endogenous Proviruses.Curr. Top. Microbiol. Immunol. 148, 115–132 (1989).PubMedGoogle Scholar
  27. 27.
    C. Leib-Mosch, R. Brack-Werner, T. Werner, M. Bachman, O. Faff, V. Erfle, and R. Hehlmann, Endogenous retroviral elements in human DNA.Cancer Res. (Suppl.)50, 5636s-5642s (1990).PubMedGoogle Scholar
  28. 28.
    M. Ono, M. Kawakami, and H. Ushikuo, Stimulation of expression of the human endogenous retrovirus genome by female steroid hormones in human breast cancer cell line T47D.J. Virol. 61, 2059–2062 (1987).PubMedGoogle Scholar
  29. 29.
    B. R. Westley and F. E. B. May, Oestrogen regulates cathepsin D mRNA levels in oestrogen responsive human breast cancer cells.Nucleic Acids Res. 15, 3773–3786 (1987).PubMedCrossRefGoogle Scholar
  30. 30.
    G. C. Franklin, S. Chretien, I. M. Hanson, H. Rochefort, F. E. B. May, and B. R. Westley, Expression of human sequences related to those of mouse mammary tumor virus.J. Virol. 62, 1203–1210 (1988).PubMedGoogle Scholar
  31. 31.
    P. Medstrand, M. Linkeskog, and J. J. Blomberg, Expression of human endogenous retroviral sequences in peripheral blood mononuclear cells of healthy individuals,Gen. Virol. 73, 2463–2466, (1992).CrossRefGoogle Scholar
  32. 32.
    I. Brodsky, B. Foley, D. Haines, J. Johnston, and D. Gillispie, Expression of HERV-K provirus in human leukocytes,Blood 81, 2369–2374 (1993).PubMedGoogle Scholar
  33. 33.
    M. Simon, M. Haltmeier, G. Papakonstatinou, T. Werner, R. Hehlmann, and C. Leib-Mosch, Transcription of Herv-K-related LTR’s in human placenta and leukemic cells,Leukemia Suppl. V.8, suppl. S12-S17 (1994).Google Scholar
  34. 34.
    R. Lower, J. Lower, C. Tondera-Koch, and R. Kurth, A general method for the identification of transcribed retrovirus sequences (R-U5 PCR) reveals the expression of the human endogenous retrovirus loci HERV-H and HERV-K in teratocarcinoma cells,Virology 192, 501–511 (1993).PubMedCrossRefGoogle Scholar
  35. 35.
    K. P. Medstrand and J. Blomberg, Characterization of novel reverse transcriptase encoding human endogenous retroviral sequences similar to type A and type B retroviruses: Differential transcription in normal human tissues,J. Virol. 67, 6778–6787 (1993).PubMedGoogle Scholar
  36. 36.
    D. G. Poirier, J. Poley, K. Cuddy, I. Brodsky, J. Brodsky, and D. Gillispie, Independent expression of int-2 mRNA and HERV-Kenv mRNA in human breast tumors. Abstract inProc. Am. Assoc. Cancer Res. 35, 549 (1994).Google Scholar
  37. 37.
    M. Sauter, S. Schommer, E. Kremmer, K. Remberger, G. Dolken, I. Lemm, M. Buck, B. Best, D. Neumann-Haefelin, and N. Mueller-Lantzsch, Human endogenous retrovirus K10: expression of gag protein and detection of antibodies in patients with seminomas.J. Virol. 69, 414–421 (1995).PubMedGoogle Scholar
  38. 38.
    N. L. DiFronzo and C. A. Holland, A direct demonstration of recombination between an injected virus and endogenous viral sequences, resulting in the generation of mink cell focus inducing viruses in AKR mice.J. Virol. 67, 3763–3770 (1993).PubMedGoogle Scholar
  39. 39.
    T. Golovkina, A. B. Jaffe, and S. R. Ross, Coexpression of exogenous and endogenous mouse mammary tumor virus RNA in vivo results in viral recombination and broadens the virus host range.J. Virol. 68, 5019–5026 (1994).PubMedGoogle Scholar
  40. 40.
    T. Tchenio and T. Heidmann, Defective retrovirus can disperse in the human genome by intracellular transposition.J. Virol. 65, 2113–2118 (1991).PubMedGoogle Scholar
  41. 41.
    S. Imai, M. Okumoto, M. Iwai, S. Haga, N. Mori, N. Miyashita, K. Moriwaki, J. Hilgers, and N. H. Sarkar, Distribution of mouse mammary tumor virus in asian wild mice.J. Virol. 68, 3437–3442 (1994).PubMedGoogle Scholar
  42. 42.
    R. Nusse, Insertional mutagenesis in mouse mammary tumorigenesis,Curr. Top. Microbiol. Immunol. 171, 43–65 (1991).PubMedGoogle Scholar
  43. 43.
    A. Marchetti, Buttitta, S. Miyazaki, D. Gallahan, G. H. Smith, and R. Callahan, Host genetic background effect on the frequency of mouse mammary tumor virus-induced rearrangements of the int-1 and int-2 loci in mouse mammary tumors,J. Virol. 69, 1932–1938 (1995).PubMedGoogle Scholar
  44. 44.
    G. Peters, S. Brookers, R. Smith, and C. Dickson, Tumorigenesis by mouse mammary tumor virus: evidence for a common region for provirus integration in mammary tumors,Cell 33, 369–377 (1983).PubMedCrossRefGoogle Scholar
  45. 45.
    G. M. Shackleford, C. A. MacArthur, H. C. Kwan, and H. E. Varmus, Mouse mammary tumor virus infection accelerates mammary carcinogenesis in Wnt-1 transgenic mice by insertional activation of int-2/Fgf-3 and hst/Fgf-4,Proc. Natl. Acad. Sci. USA 90, 740–744 (1993).PubMedCrossRefGoogle Scholar
  46. 46.
    C. A. MacArthur, D. A. Shankar, and G. M. Shackleford, Fgf-8, activated by proviral insertion, cooperates with the Wnt-1 transgene in murine mammary tumorigenesis,J. Virol. 69, 2501–2507 (1995).PubMedGoogle Scholar
  47. 47.
    S-I Yanagawa, K. Kakimi, H. Tanaka, A. Murakami, Y. Nakagawa, Y. Kubo, Y. Yamada, H. Hiai, K. Kuribayashi, T. Masuda, and A. Ishimoto, Identification of a novel mammary cell line-specific enhancer element in the long terminal repeat of mouse mammary tumor virus, which interacts with its hormone-responsive element,J. Virol. 67, 112–118 (1993).PubMedGoogle Scholar
  48. 48.
    P. Marrack, E. Kushnir, and J. Kappler, A maternally inherited superantigen encoded by a mammary tumor virus,Nature 349, 524–526 (1991).PubMedCrossRefGoogle Scholar
  49. 49.
    W. Held, G. A. Waanders, H. Acha-Orbea, and H. R. MacDonald, Reverse transcriptase-dependent and-independent phases of infection with mouse mammary tumor virus: implications for superantigen function.J. Exp. Med. 180, 2347–2351 (1994).PubMedCrossRefGoogle Scholar
  50. 50.
    R. Mukhopadhyay, M. Medina, and J. S. Butel, Expression of the mouse mammary tumor virus long terminal repeat open reading frame promotes tumorigenic potential of hyperplastic mouse mammary epithelial cells,Virology 211, 84–93 (1995).CrossRefGoogle Scholar
  51. 51.
    A. S. Dion, Retrovirus association with breast cancer: A critical appraisal,Breast Cancer Res. and Treatment 9, 155–156 (1987).CrossRefGoogle Scholar
  52. 52.
    R. Mesa-Tejada, I. Keydar, M. Ramanarayanan, T. Ohno, C. Fenoglio, and S. Spiegelman, Detection in human breast carcinomas of an antigen mmunologically related to a group-specific antigen of mouse mammary tumor virus,Proc. Natl. Acad. Sci. USA 75, 1529–1533 (1978).PubMedCrossRefGoogle Scholar
  53. 53.
    P. Levine, N. Mourali, F. Tabbave, J. Costa, R. Mesa-Tejada, S. Spiegelman, and J. G. Bekesi, Immunopathologic features of rapidly progressing breast cancer (RPBC) in Tunisia,Proc. Am. Assoc. Cancer Res. 21, 170 (1980).Google Scholar
  54. 54.
    R. Lloyd, P. P. Rosen, N. H. Sarkar, D. Jimenez, D. W. Kinne, C. Menendez-Botet, and M. K. Schwartz, Murine mammary tumor virus related antigen in human male mammary carcinoma,Cancer 51, 654–661 (1983).PubMedCrossRefGoogle Scholar
  55. 55.
    S. V. Litvinov and T. V. Golovkina, Expression of proteins immunologically related to murine mammary tumour virus (MMTV) core proteins in the cells of breast cancer continuous lines MCF-7, T47D, MDA-231 and cells from human milk,Acta Virologica 33, 137–142 (1989).PubMedGoogle Scholar
  56. 56.
    S. Zotter, C. Kemmer, A. Lossnitzer, H. Grossmann, and B. A. Johannsen, Mouse mammary tumour virus-related antigens in core-like density fractions from large samples of women’s milk,Eur. J. Cancer 16, 455–467 (1980).PubMedGoogle Scholar
  57. 57.
    N. K. Day, S. S. Witkin, N. H. Sarkar, D. Kinne, D. J. Jussawalla, A. Levin, C. C. Hsia, N. Geller, and R. A. Good, Antibodies reactive with murine mammary tumor virus in sera of patients with breast cancer: Geographic and family studies,Proc. Natl. Acad. Sci. USA 78, 2483–2487 (1981).PubMedCrossRefGoogle Scholar
  58. 58.
    A. Segal-Eiras, M. V. Croce, and Chr. D. Pasqualini, Antibodies presumably cross-reacting with mouse retrovirus type B and C in the sera of both leukemia-lymphoma and mammary cancer patients,Arch. Geschwulstforsch. 53, 321–327 (1983).PubMedGoogle Scholar
  59. 59.
    S. S. Witkin, N. H. Sarkar, D. W. Kinne, C. N. Breed, R. A. Good, and N. K. Day, Antigens and antibodies cross-reactive to the murine mammary tumor virus in human breast cyst fluids,J. Clin. Invest. 67, 216–222 (1981).PubMedGoogle Scholar
  60. 60.
    I. Keydar, T. Ohno, R. Nayak, R. Sweet, F. Simoni, F. Weiss, S. Karby, R. Mesa-Tejada, and S. Spiegelman, Properties of retrovirus-like particles produced by a human breast carcinoma cell line: Immunological relationship with mouse mammary tumor virus proteins,Proc. Natl. Acad. Sci. USA 81, 4188–4192 (1984).PubMedCrossRefGoogle Scholar
  61. 61.
    D. de Ricqles, A. Olomucki, F. Gosselin, and R. Ridereau, Breast cancer and T-cell-mediated immunityt to proteins of the mouse mammary tumour virus (MMTV),Eur. Cytokine Netw. 4, 153–160, (1993).PubMedGoogle Scholar
  62. 62.
    R. Callahan, W. Drohan, S. Tronick, and J. Schlom, Detection and cloning of human DNA sequences related to the mouse mammary tumor virus genome,Proc. Natl. Acad. Sci. USA 79, 5503–5507 (1982).PubMedCrossRefGoogle Scholar
  63. 63.
    R. Axel, J. Schlom, and S. Spiegelman, Presence in human breast cancer of RNA homologous to mouse mammary tumor virus RNA,Nature 235, 32–36 (1972).PubMedCrossRefGoogle Scholar
  64. 64.
    M. Crepin, R. Lidereau, J. C. Chermann, P. Pouillart, H. Magdamenat, and L. Montagnier, Sequences related to mouse mammary tumor virus genome in tumor cells and lymphocytes from patients with breast cancer,Biochem. Biophysic. Ress. Commun. 118, 324–331 (1984).CrossRefGoogle Scholar
  65. 65.
    A. M. Al-Sumidaie, C. A. Hart, S. J. Leinster, and C. D. Green, Particles with properties of retroviruses in monocytes from patients with breast cancer,Lancet 1, 5–8 (1988).PubMedCrossRefGoogle Scholar
  66. 66.
    C. M. McGrath, P. M. Grant, H. D. Soule, T. Glancy, and M. A. Rich, Replication of oncornavirus-like particle in human breast carcinoma cell line MCF-7,Nature 252, 247–250 (1972).CrossRefGoogle Scholar
  67. 67.
    B. Westley and F. E. B. May, The human genome contains multiple sequences of varying homology to mouse mammary tumour virus DNA,Gene 28, 221–227 (1984).PubMedCrossRefGoogle Scholar
  68. 68.
    M. Ono, T. Yasunaga, T. Miyata, and H. Ushikubo, Nucleotide sequence of human endogenous retrovirus genome related to the mouse mammary tumor virus genome,J. Virol 60, 589–598 (1986).PubMedGoogle Scholar
  69. 69.
    O. Faff, A. B. Murray, J. Schmidt, C. Leib-Mosch, V. Erfle, and R. Hehlmann, Retrovirus-like particles from the human T47D cell line are related to mouse mammary tumor virus and are of endogenous origin,J. Gen. Virol. 73, 1087–1097 (1992).PubMedGoogle Scholar
  70. 70.
    M. Hareuveni and R. Lathe, Breast cancer sequences identified by mouse mammary tumor virus (MMTV) antiserum are unrelated to MMTV,Int. J. Cancer 46, 1134–1135 (1990).PubMedCrossRefGoogle Scholar
  71. 71.
    F. E. B. May and B. R. Westley, Characterization of sequences related to the mouse mammary tumor virus that are specific to MCF-7 breast cancer cells,Cancer Res. 49, 3879–3883 (1989).PubMedGoogle Scholar
  72. 72.
    J. G. Szakaacs and L. C. Moscinski, Sequence homology of deoxyribonucleic acid to mouse mammary tumor virus genome in human breast tumors,Ann. Clin. Lab. Sci. 21, 402–412 (1991).Google Scholar
  73. 73.
    S. L. Meyers, M. T. O’Brien, T. Smith, and J. P. Dudley, Analysis of the int-1, int-2, c-myc, and neu oncogenes in human breast carcinomas,Cancer Res. 50, 5911–5918 (1990).PubMedGoogle Scholar
  74. 74.
    N. Barnabas-Sohi, M. R. Simha, V. A. Parikh, F. Feiulhade, A. Kurkure, J. C. Kouyoumdjian, D. J. Jussawalla, V. M. Doctor, and A. Therwath, Breast carcinoma in a high-risk population: structural alterations in neu, int-2 and p53 genes,Breast Dis. 6, 13–26 (1993).Google Scholar
  75. 75.
    E. Schuwring, E. Verhoeven, H. van Tinteren, L. Peterse, B. Nunnink, F. B. J. M. Thunnissen, P. Devilee, C. J. Cornelisse, M. J. van de Vijver, and W. J. Mooi, Amplification of genes within chromosome 11q13 region is indicative of poor prognosis with operable breast cancer,Cancer Research 52, 5229–5234 (1992).Google Scholar
  76. 76.
    M-H Champeme, I. Bieche, S. Lizard, and R. Lidereau, Amplification of genes within chromosome 11q13 region is indicative of poor prognosis with operable breast cancer,Genes Chromosomes and Cancer 12, 128–133 (1995).PubMedCrossRefGoogle Scholar
  77. 77.
    E. L. Huguet, J. A. McMahon, A. P. McMahon, R. Bicknell, and A. L. Harris, Differential expression of human Wnt genes 2,3,4, and 7B in human breast cell lines and normal and disease states of human breast tissue,Cancer Res. 54, 2615–2621 (1994).PubMedGoogle Scholar
  78. 78.
    G. N. Schrauzer and D. Ishmael, Effects of selenium and of arsenic on the genesis of spontaneous mammary tumors in inbred C3H mice,Ann. Clin. and Lab. Sci. 4, 441–447 (1974).Google Scholar
  79. 79.
    G. N. Schrauzer, D. A. White, and C. J. Schneider, Inhibition of the genesis of spontaneous mammary tumors in C3H mice: Effects of selenium and of selenium-antagonistic elements and their possible role in human breast cancer.Bioinorg. Chem. 6, 265–270 (1976).PubMedCrossRefGoogle Scholar
  80. 80.
    D. Medina and F. Shepherd, Selenium-mediated inhibition of mouse mammary tumorigenesis,Cancer Lett. 8, 241–245 (1980).PubMedCrossRefGoogle Scholar
  81. 81.
    T. Stewart, S-C J. Tsai, H. Grayson, R. Henderson, and G. Opetz, Incidence of de-novo breast cancer in women chronically immunosuppressed after organ transplantation,The Lancet 346, 796–798 (1995).CrossRefGoogle Scholar
  82. 82.
    Y. Wang, J. F. Holland, I. K. Bleiweiss, S. Melana, X. Liu, I. Pelisson, A. Cantarella, K. Stellrecht, S. Mani, and B. G. T. Pogo, Detection of mammary tumor virus env gene-like sequences in human breast cancer,Cancer Res. 55, 5173–5179 (1995).PubMedGoogle Scholar
  83. 83.
    Y. Wang, I. Pelisson, V. Go, J. F. Holland, and B. G. T. Pogo, Identification and expression of MMTV-like sequences in human breast cancer,Proc. Am. Assoc. Cancer Res. 37, 565 (1996).Google Scholar

Copyright information

© Humana Press Inc. 1997

Authors and Affiliations

  • Beatriz G. -T. Pogo
    • 1
    • 2
  • James F. Holland
    • 1
  1. 1.Division of Neoplastic Diseases, Department of Medicine, Mount Sinai School of MedicineCUNYNew York
  2. 2.Department of Microbiology, Mount Sinai School of MedicineCUNYNew York

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