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Abstract:

Almost 60 years ago, Foulds carefully described for the first time a particular type of mouse mammary tumor that appeared in the glands of pregnant females and disappeared shortly after delivery. Since then, the attention that researchers paid to the Mouse Mammary Tumor Virus (MMTV)-induced pregnancy-dependent tumors has not vanished through the years. This was because the information obtained from mice carrying MMTV variants that were able to induce pregnancy-dependent tumors was meaningful for studying different aspects of mammary tumor biology. In addition, mice infected with these viral variants provided some of the few chances to use fully hormone-dependent estrogen receptor positive breast cancer models in the mouse. In the analysis of the association between tumor morphology and behavior, the mechanisms underlying progression towards autonomy, the impact of different genes during cancer initiation and development, and the relevance of host genetic background for tumor incidence and hormone-dependence, mouse strains carrying these MMTV variants have been very important tools that could not have been replaced with any other available model. The goal of this article is to provide a succinct chronicle of the experiments and observations made in the MMTV-induced pregnancy-dependent models that most significantly contributed to the mouse mammary tumor biology field. In addition, the possibility to use these MMTV variants as alternative models for analyzing mammary tumor stem cells and pregnancy-associated breast cancer in women is discussed. © Springer Science+Business Media, LLC 2008.

Registro:

Documento: Artículo
Título:MMTV-induced pregnancy-dependent mammary tumors: Early history and new perspectives
Autor:Kordon, E.C.
Filiación:Institute of Physiology, Molecular Biology and Neurosciences, School of Exact and Natural Sciences, University of Buenos Aires, Buenos Aires, Argentina
Laboratorio de Expresión Génica en Mama y Apoptosis (LEGMA), Facultad de Cs. Exactas y Naturales, Pabellón 2, 2do piso, 1428 Buenos Aires, Argentina
Palabras clave:Hormone dependency; Mammary tumors; MMTV; Tumor progression; estrogen receptor; progesterone receptor; article; breast cancer; breast carcinogenesis; breast hyperplasia; breast tumor; cancer invasion; cancer model; cancer stem cell; gene mutation; gene overexpression; hormone dependence; human; lactation; Mouse mammary tumor oncovirus; mouse strain; nonhuman; pregnancy; strain difference; tumor growth; Animals; Disease Models, Animal; Disease Progression; Female; History, 20th Century; Humans; Mammary Neoplasms, Experimental; Mammary Tumor Virus, Mouse; Medical Oncology; Mice; Models, Genetic; Pregnancy; Risk Factors; Species Specificity
Año:2008
Volumen:13
Número:3
Página de inicio:289
Página de fin:297
DOI: http://dx.doi.org/10.1007/s10911-008-9091-7
Título revista:Journal of Mammary Gland Biology and Neoplasia
Título revista abreviado:J. Mammary Gland Biol. Neoplasia
ISSN:10833021
CODEN:JMBNF
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_10833021_v13_n3_p289_Kordon

Referencias:

  • Wagner, K., Models of breast cancer: Quo vadis, animal modeling (2004) Breast Cancer Res, 6, pp. 31-38. , doi: 10.1186/bcr723
  • Heston, W.E., Vlahakis, G., Tsubura, Y., Strain, D.D., A new high mammary tumor strain, and comparison of DD strain with strain C3H (1964) J Natl Cancer Inst, 32, pp. 237-251
  • Foulds, L., Mammary tumors in hybrid mice: The presence and transmission of the mammary tumor agent (1949) Br J Cancer, 3, pp. 230-239
  • Mühlbock, O., Note on a new inbred mouse strain (1965) Eur J Cancer, 1, pp. 123-124. , doi: 10.1016/0014-2964(65)90003-4
  • Squartini, F., Responsiveness and progression of mouse mammary tumors in high-cancer strain mice (1962) J Natl Cancer Inst, 28, pp. 911-926
  • Foulds, L., The histologic analysis of mammary tumors in mice. I-IV (1956) J Natl Cancer Inst, 17, pp. 701-801
  • Benveltzen, P., Daams, J.H., Mammary tumor virus activity in brain and liver of GR strain mice (1970) Eur J Cancer, 6, pp. 273-276. , doi: 10.1016/0014-2964(70)90090-3
  • Foulds, L., Mammary tumors in hybrid mice: A sex factor in transplantation (1947) Br J Cancer, 1, pp. 326-370
  • Foulds, L., Mammary tumors in hybrid mice: Growth and progression of spontaneous tumors (1949) Br J Cancer, 3, pp. 345-375
  • Smith, J.A., King, R.J.B., Biochemical Studies on Hormone Responsive mammary tumors in BR6 mice (1970) Cancer Res, 30, pp. 2055-2060
  • Foulds, L., Mammary tumors in hybrid mice: Hormone responses of transplanted tumors (1949) Br J Cancer, 3, pp. 240-246
  • Squartini, F., Responsiveness and progression of mammary tumors in high cancer-strain mice (1962) J Natl Cancer Inst, 28, pp. 911-926
  • Squartini, F., Rossi, G., Paoletti, I., Characters of mammary tumors in BALB/c female mice foster nursed by C3H and RIII mothers (1963) Nature, 197, pp. 505-506. , doi: 10.1038/197505a0
  • Golovkina, T., Piazzon, I., Nepomnaschy, I., Buggiano, V., Olano Vela, M., Ross, S., Generation of tumorigenic milk-born mouse mammary tumor virus by recombination between exogenous and endogenous viruses (1997) J Virol, 71, pp. 3895-3903
  • Piazzon, G.A., Torello, S., Nepomnaschy, I., Deroche, A., Dran, G., Transmission of a Mls-la-like superantigen to BALB/c mice by foster nursing on F1 Mls-1 mothers (1994) J Immunol, 153, pp. 1553-1562
  • Buggiano, V., Schere-Levy, C., Abe, K., Vanzulli, S., Piazzon, I., Smith, G.H., Impairment of mammary lobular development induced by expression of TGFb1 under the control of WAP promoter does not suppress tumorigenesis in MMTV-infected transgenic mice (2001) Int J Cancer, 92, pp. 568-576
  • Moreau, H., Recherches experimentales sur la transmissibilite de certain neoplasmes (epithelioma cilindriques) (1894) Arch Med Exp Anat Path, 6, pp. 677-705
  • Dobrovolskaia-Zavadskaia, N., Sur une tumeur de souris a evolution lente et descontinue et son compartement hereditaire (1930) Compt Rend Soc Biol, 103, pp. 994-996
  • Haddow, A., The biological characters of spontaneous tumours of the mouse, with special reference to rate of growth (1938) J Path Bact, 47, pp. 553-565. , doi: 10.1002/path.1700470315
  • Gardner, W.U., The effect of estrogen on the incidence of mammary and pituitary tumors in hybrid mice (1941) Cancer Res, 1, pp. 345-358
  • Nandi, S., Bern, H.A., DeOme, K.B., Effect of hormones on growh and neoplastic development of transplanted hyperplastic alveolar nodules found in the mammary gland of old females C3H/Crgl mice (1960) J Natl Cancer Inst, 24, pp. 883-903
  • Huseby, R.A., Bittner, J.J., A comparative morphological study of the mammary glands with reference to the known factyor that influencing the development of mammary carcinomas in mice (1946) Cancer Res, 6, pp. 240-255
  • DeOme, K.B., Faulkin Jr., L.J., Bern, H.A., Blair, P.B., Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice (1959) Cancer Res, 19, pp. 515-520
  • DeOme, K.B., Bern, H.A., Nandi, S., Pitelka, D.R., Faulkin Jr., L.J., The precancerous nature of the hyperplastic alveolar nodules found in the mammary gland of old female C3H/Crgl mice (1959) Genetics and Cancer, pp. 327-348. , In: Austin: Univ Texas Press
  • Squartini, F., Mammogenesis and breast carcinogenesis in virgin female mice of BALB/cf substrain with the milk agent (1959) J Natl Cancer Inst, 23, pp. 1227-1238
  • Nathanson, I.T., Andervont, H.B., Effect of testosterone propionate on development and growth of mammary carcinoma in female mice (1939) Proc Soc Exp Biol Med, 40, pp. 421-422
  • Haagensen, C.D., Randall, H.T., Auchincloss, R., Failure of thyrotropic pituitary hormone to prevent spontaneous mammary cancer in mice (1940) Proc Soc Exp Biol Med, 45, pp. 820-823
  • Jones, E.E., The effect of testosterone propionate on mammary tumors in mice of the C3H strain (1941) Cancer Res, 1, pp. 787-789
  • Gardner, W.U., Persistence and growth of spontaneous mammary tumors and hyperplastic nodules in hypophysectomized mice (1942) Cancer Res, 2, pp. 476-488
  • Muhlbock, O., Studies on the hormone dependence of experimental breast tumors in mice (1958) Endocrine Aspects of Breast Cancer, pp. 291-296. , In: Currie AR, editor. Edinburgh: E & S.Livingstone Ltd
  • Korteweg, R., Thomas, F., Tumor induction andf tumor growth in hypophysectomized mice (1939) Am J Cancer, 37, pp. 36-44
  • DeOme, K.B., Miyamoto, M.J., Osborn, R.C., Guzman, R.C., Lum, K., Effect of parity on recovery of inapparent nodule-transformed mammary gland cells in vivo (1978) Cancer Res, 38, pp. 4050-4053
  • Heston, W.E., Vlahakis, G., Mammary tumors, plaques and hyperplastic alveolar nodules in various combinations of mouse inbred strains and the different lines of the mammary tumor virus (1971) Int J Cancer, 7, pp. 141-148. , doi: 10.1002/ijc.2910070116
  • Aidells, B.D., Daniel, C.W., Hormone-dependent mammary tumors in Strain GR/A Mice. I. Alternation between ductal and tumorous phases of growth during serial transplantation (1974) J Natl Cancer Inst, 52, pp. 1855-1863
  • Callahan, R., Smith, G.H., MMTV-induced mammary tumorigenesis: Gene discovery, progression to malignancy and cellularpathways (2000) Oncogene, 19, pp. 992-1001. , doi: 10.1038/sj.onc.1203276
  • Kordon, E.C., Smith, G.H., An entire functional mammary gland may comprise the progeny from a single cell (1998) Development, 125, pp. 1921-1930
  • Peters, G., Lee, A.E., Dickson, C., Activation of a cellular gene by mouse mammary tumor virus may occur early in mammary tumor development (1984) Nature, 309, pp. 273-275. , doi: 10.1038/309273a0
  • Michalides, R., Wagenaar, E., Sluyser, M., Mammary tumor virus DNA as a marker for genotypic variance within hormoneresponsive GR mouse mammary tumors (1982) Cancer Res, 42, pp. 1154-1158
  • Sluyser, M., Moncharment, B., Van Der Valk, M.A., DeGoeij, C.C., Evers, S.G., Different int-1 region DNA rearrangements within different zones of a single mouse mammary tumor (1988) Virology, 163, pp. 11-18. , doi: 10.1016/0042-6822(88)90228-0
  • Sarkar, N.H., Clonal variations among multiple primary mammary tumors and within a tumor of individual mice: Insertion mutations of INT oncogenes (1995) Virology, 212, pp. 490-499. , doi: 10.1006/viro.1995.1507
  • Cardiff, R.D., Fanning, T.G., Morris, D.W., Ashley, R.L., Faulkin, L.J., Restriction endonuclease studies of hyperplastic outgrowth lines from BALB/cfC3H mouse hyperplastic mammary nodules (1981) Cancer Res, 41, pp. 3024-3029
  • Buggiano, V., Schere-Levy, C., Gattelli, A., Cirio, M.C., Marfil, M., Nepomnaschy, I., Origin and progression of pregnancy-dependent mammary tumors induced by new mouse mammary tumor virus variants (2002) Breast Cancer Res Treat, 75, pp. 191-202. , doi: 10.1023/A:1019932516887
  • Gattelli, A., Cirio, M.C., Quaglino, A., Schere-Levy, C., Martinez, N., Binaghi, M., Progression of pregnancy-dependent mouse mammary tumors after long dormancy periods. involvement of wnt pathway activation (2004) Cancer Res, 64, pp. 5193-5199. , doi: 10.1158/0008-5472.CAN-03-3992
  • Gattelli, A., Zimberlin, M., Castilla, L., Kordon, E., Selection of early occurring mutations dictates hormone-independency progression in mouse mammary tumor lines (2006) J Virol, 80, pp. 11409-11415. , doi: 10.1128/JVI.00234-06
  • Sluyser, M., Van Nie, R., Estrogen receptor content and hormone-responsive growth of mouse mammary tumors (1974) Cancer Res, 34, pp. 3253-3257
  • Dabre, P.D., King, R.J.B., Progression to steroid autonomy in S115 mouse mammary tumor cells: Role of DNA methylation (1984) J Cell Biol, 99, pp. 1410-1415. , doi: 10.1083/jcb.99.4.1410
  • Kordon, E., Lanari, C., Meiss, R., Elizalde, P., Charreau, E., Dosne Pasqualini, C., Hormone-dependence of a mouse mammary tumor line induced in vivo by medroxyprogesterone acetate (1990) Breast Cancer Res Treat, 17, pp. 33-43. , doi: 10.1007/BF01812682
  • Dabre, P.D., King, R.J.B., Progression to steroid insensitivity can occur irrespective of the presence of functional steroid receptors (1987) Cell, 51, pp. 521-528. , doi: 10.1016/0092-8674(87)90121-8
  • Kordon, E., Guerra, F., Molinolo, A., Elizalde, P., Charreau, E., Dosne Pasqualini, C., Effect of sialoadenectomy on medroxyprogesteroneacetate-induced mammary carcinogenesis in BALB/c mice. Correlation between histology and epidermal growth-factor receptor content (1994) Int J Cancer, 59, pp. 196-203. , doi: 10.1002/ijc.2910590210
  • Sluyser, M., Moncharment, B., Van Der Valk, M.A., DeGoeij, C.C., Evers, S.G., Different int-1 region DNA rearrangements within different zones of a single mouse mammary tumor (1988) Virology, 163, pp. 11-18. , doi: 10.1016/0042-6822(88)90228-0
  • Aghorne, C., Thomas, M., Lagarde, A., Kerbel, R.S., Breitman, M.L., Genetic evidence for progressive selection and overgrowth ofprimary tumors by metastatic cell subpopulations (1988) Cancer Res, 48, pp. 6109-6114
  • Nusse, R., Varmus, H.E., Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome (1982) Cell, 31, pp. 99-109. , doi: 10.1016/0092-8674(82)90409-3
  • Dickson, C., Smith, R., Brookes, S., Peters, G., Tumorigenesis by mouse mammary tumor virus: Proviral activation of a cellular gene in the common integration region int-2 (1984) Cell, 37, pp. 529-536. , doi: 10.1016/0092-8674(84)90383-0
  • Tsukamoto, A.S., Grosschedl, R., Guzman, R.C., Parslow, T., Varmus, H.E., Expression of the Int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinoma in male and female mice (1988) Cell, 55, pp. 619-625. , doi: 10.1016/0092-8674(88)90220-6
  • Muller, W.J., Lee, F.S., Dickson, C., Peters, G., The int-2 gene product act as an epithelial growth factor in transgenic mice (1990) EMBO J, (9), pp. 907-913
  • Callahan, R., MMTV-induced mutation in mouse mammary tumors: Their potential relevance to human breast cancer (1996) Breast Cancer Res Treat, 39, pp. 33-44. , doi: 10.1007/BF01806076
  • Marchetti, A., Robbins, J., Campbell, G., Buttitta, F., Squartini, M., Bistocchi, M., Callahan, R., Host genetic background effect on the frequency of mouse mammary tumor virus-induced rearrangements in the int-1 and int-2 loci in mouse mammary tumors (1991) J Virol, 65, pp. 4550-4554
  • Peters, G., Lee, A.E., Dickson, C., Concerted activation of two potential proto-oncogenes in carcinomas induced by mouse mammary tumor virus (1986) Nature, 320, pp. 628-631. , doi: 10.1038/320628a0
  • Mester, J., Wagenaar, E., Sluyser, M., Nusse, R., Activation of int-1 and int-2 mammary oncogenes in hormone-dependent and -independent mammary tumors of GR mice (1987) J Virol, 61, pp. 1073-1078
  • Li, Y., Welm, B., Podsypanina, K., Huang, S., Chamorro, M., Zhang, X., Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells (2003) Proc Natl Acad Sci U S A, 100, pp. 15853-15858. , doi: 10.1073/pnas.2136825100
  • Liu, B.Y., McDermott, S.P., Khwaja, S.S., Alexander, C.M., The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells (2004) Proc Natl Acad Sci U S A, 101, pp. 4158-4163. , doi: 10.1073/pnas.0400699101
  • Wagner, K.U., Boulanger, C.A., Henry, M.D., Sgagias, M., Hennighausen, L., Smith, G.H., An adjunct mammary epithelial cell population in parous females: Its role in functional adaptation and tissue renewal (2002) Development, 129, pp. 1377-1386
  • Boulanger, C.A., Wagner, K.U., Smith, G.H., Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression (2005) Oncogene, 24, pp. 552-560. , doi: 10.1038/sj.onc.1208185
  • Henry, M.D., Triplett, A.A., Oh, K.B., Smith, G.H., Wagner, K.U., Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice (2004) Oncogene, 23, pp. 6980-6985. , doi: 10.1038/sj.onc.1207827
  • Kordon, E., Mc Knight, R., Jhappan, C., Hennighausen, L., Merlino, G., Smith, G.H., Ectopic TGFb1 expression in the secretory mammary epithelium induces early senescence of the epithelial stem cell population (1995) Dev Biol, 168, pp. 47-61. , doi: 10.1006/dbio.1995.1060
  • Boulanger, C.A., Smith, G.H., Reducing mammary cancer risk through premature stem cell senescence (2001) Oncogene, 20, pp. 2264-2722. , doi: 10.1038/sj.onc.1204312
  • Boulanger, C.A., Wagner, K.U., Smith, G.H., Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression (2005) Oncogene, 24, pp. 552-560. , doi: 10.1038/sj.onc.1208185
  • Feng, Y., Manka, D., Wagner, K.U., Khan, S.A., Estrogen receptor-alpha expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice (2007) Proc Natl Acad Sci U S A, 104, pp. 14718-14723. , doi: 10.1073/pnas.0706933104
  • Polyak, K., Pregnancy and breast cancer: The other side of the coin (2006) Cancer Cell, 9, pp. 151-153. , doi: 10.1016/j.ccr.2006.02.026
  • Albrektsen, G., Heuch, I., Thoresen, S., Kvåle, G., Clinical stage of breast cancer by parity, age at birth, and time since birth: A progressive effect of pregnancy hormones (2006) Cancer Epidemiol Biomarkers Prev, 15, pp. 65-69. , doi: 10.1158/1055-9965.EPI-05-0634
  • Schedin, P., Pregnancy-associated breast cancer and metastasis (2006) Nat Rev Cancer, 6, pp. 281-291. , doi: 10.1038/nrc1839

Citas:

---------- APA ----------
(2008) . MMTV-induced pregnancy-dependent mammary tumors: Early history and new perspectives. Journal of Mammary Gland Biology and Neoplasia, 13(3), 289-297.
http://dx.doi.org/10.1007/s10911-008-9091-7
---------- CHICAGO ----------
Kordon, E.C. "MMTV-induced pregnancy-dependent mammary tumors: Early history and new perspectives" . Journal of Mammary Gland Biology and Neoplasia 13, no. 3 (2008) : 289-297.
http://dx.doi.org/10.1007/s10911-008-9091-7
---------- MLA ----------
Kordon, E.C. "MMTV-induced pregnancy-dependent mammary tumors: Early history and new perspectives" . Journal of Mammary Gland Biology and Neoplasia, vol. 13, no. 3, 2008, pp. 289-297.
http://dx.doi.org/10.1007/s10911-008-9091-7
---------- VANCOUVER ----------
Kordon, E.C. MMTV-induced pregnancy-dependent mammary tumors: Early history and new perspectives. J. Mammary Gland Biol. Neoplasia. 2008;13(3):289-297.
http://dx.doi.org/10.1007/s10911-008-9091-7