Development and characterization of mammary intraductal (MIND) spontaneous metastasis models for triple-negative breast cancer in syngeneic mice.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 03 2020
13 03 2020
Historique:
received:
31
01
2019
accepted:
02
03
2020
entrez:
15
3
2020
pubmed:
15
3
2020
medline:
24
11
2020
Statut:
epublish
Résumé
Triple-negative breast cancer (TNBC) has a more aggressive phenotype and higher metastasis and recurrence rates than other breast cancer subtypes. TNBC currently lacks a transplantation model that is suitable for clinical simulations of the tumor microenvironment. Intraductal injection of tumor cells into the mammary duct could mimic the occurrence and development of breast cancer. Herein, we injected 4T1 cells into the mammary ducts of BALB/C mice to build a preclinical model of TNBC and optimized the related construction method to observe the occurrence and spontaneous metastasis of tumors. We compared the effects of different cell numbers on tumorigenesis rates, times to tumorigenesis, and metastases to determine the optimal number of cells for modelling. We demonstrated that 4T1-MIND model mice injected with 20,000 cells revealed a suitable tumor formation rate and time, thus indicating a potential treatment time window after distant metastasis. We also injected 20,000 cells directly into the breast fat pad or breast duct for parallel comparison. The results still showed that the 4T1-MIND model provides sufficient treatment time for lung metastases in mice and that it is a more reliable model for early tumor development. The 4T1-MIND model requires continuous improvement and optimization. A suitable and optimized model for translational research and studies on the microenvironment in TNBC should be developed.
Identifiants
pubmed: 32170125
doi: 10.1038/s41598-020-61679-8
pii: 10.1038/s41598-020-61679-8
pmc: PMC7070052
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4681Références
Bray, F. et al. Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: a cancer journal for clinicians, https://doi.org/10.3322/caac.21492 (2018).
DeSantis, C., Ma, J., Bryan, L. & Jemal, A. Breast cancer statistics, 2013. CA: a cancer J. clinicians 64, 52–62, https://doi.org/10.3322/caac.21203 (2014).
doi: 10.3322/caac.21203
Gauthier, M. L. et al. Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell 12, 479–491, https://doi.org/10.1016/j.ccr.2007.10.017 (2007).
doi: 10.1016/j.ccr.2007.10.017
pubmed: 17996651
pmcid: 17996651
Virnig, B. A., Tuttle, T. M., Shamliyan, T. & Kane, R. L. Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J. Natl Cancer Inst. 102, 170–178, https://doi.org/10.1093/jnci/djp482 (2010).
doi: 10.1093/jnci/djp482
DeSantis, C. E., Ma, J., Goding Sauer, A., Newman, L. A. & Jemal, A. Breast cancer statistics, 2017, racial disparity in mortality by state. CA: a cancer journal for clinicians, https://doi.org/10.3322/caac.21412 (2017).
Sleeman, J. & Steeg, P. S. Cancer metastasis as a therapeutic target. Eur. J. Cancer 46, 1177–1180, https://doi.org/10.1016/j.ejca.2010.02.039 (2010).
doi: 10.1016/j.ejca.2010.02.039
pubmed: 20307970
pmcid: 20307970
Bianchini, G., Balko, J. M., Mayer, I. A., Sanders, M. E. & Gianni, L. Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat. Rev. Clin. Oncol. 13, 674, https://doi.org/10.1038/nrclinonc.2016.66 (2016).
doi: 10.1038/nrclinonc.2016.66
pubmed: 27184417
pmcid: 27184417
Arrowsmith, J. Trial watch: phase III and submission failures: 2007–2010. Nat. reviews. Drug. discovery 10, 87, https://doi.org/10.1038/nrd3375 (2011).
doi: 10.1038/nrd3375
Sun, B. et al. Identification of metastasis-related proteins and their clinical relevance to triple-negative human breast cancer. Clin. Cancer Res. 14, 7050–7059, https://doi.org/10.1158/1078-0432.ccr-08-0520 (2008).
doi: 10.1158/1078-0432.ccr-08-0520
pubmed: 18981002
pmcid: 18981002
Simian, M., Manzur, T., Rodriguez, V., de Kier Joffe, E. B. & Klein, S. A spontaneous estrogen dependent, tamoxifen sensitive mouse mammary tumor: a new model system to study hormone-responsiveness in immune competent mice. Breast Cancer Res. Treat. 113, 1–8, https://doi.org/10.1007/s10549-007-9888-x (2009).
doi: 10.1007/s10549-007-9888-x
Fabris, V. T. From chromosomal abnormalities to the identification of target genes in mouse models of breast cancer. Cancer Genet. 207, 233–246, https://doi.org/10.1016/j.cancergen.2014.06.025 (2014).
doi: 10.1016/j.cancergen.2014.06.025
Lanari, C., Molinolo, A. A. & Pasqualini, C. D. Induction of mammary adenocarcinomas by medroxyprogesterone acetate in BALB/c female mice. Cancer Lett. 33, 215–223 (1986).
doi: 10.1016/0304-3835(86)90027-3
Currier, N. et al. Oncogenic signaling pathways activated in DMBA-induced mouse mammary tumors. Toxicol. Pathol. 33, 726–737, https://doi.org/10.1080/01926230500352226 (2005).
doi: 10.1080/01926230500352226
Mollard, S. et al. How can grafted breast cancer models be optimized? Cancer Biol. Ther. 12, 855–864, https://doi.org/10.4161/cbt.12.10.18139 (2011).
doi: 10.4161/cbt.12.10.18139
pubmed: 3280900
pmcid: 3280900
Krishnan, A. V., Swami, S. & Feldman, D. Equivalent anticancer activities of dietary vitamin D and calcitriol in an animal model of breast cancer: importance of mammary CYP27B1 for treatment and prevention. J. steroid Biochem. Mol. Biol. 136, 289–295, https://doi.org/10.1016/j.jsbmb.2012.08.005 (2013).
doi: 10.1016/j.jsbmb.2012.08.005
Ottewell, P. D., Coleman, R. E. & Holen, I. From genetic abnormality to metastases: murine models of breast cancer and their use in the development of anticancer therapies. Breast Cancer Res. Treat. 96, 101–113, https://doi.org/10.1007/s10549-005-9067-x (2006).
doi: 10.1007/s10549-005-9067-x
Bailey-Downs, L. C. et al. Development and characterization of a preclinical model of breast cancer lung micrometastatic to macrometastatic progression. PLoS ONE 9, e98624, https://doi.org/10.1371/journal.pone.0098624 (2014).
doi: 10.1371/journal.pone.0098624
pubmed: 4039511
pmcid: 4039511
Rashid, O. M. & Takabe, K. Animal models for exploring the pharmacokinetics of breast cancer therapies. Expert. Opin. Drug. Metab. Toxicol. 11, 221–230, https://doi.org/10.1517/17425255.2015.983073 (2015).
doi: 10.1517/17425255.2015.983073
pubmed: 25416501
pmcid: 25416501
Borst, G. R. et al. Neoadjuvant olaparib targets hypoxia to improve radioresponse in a homologous recombination-proficient breast cancer model. Oncotarget 8, 87638–87646, https://doi.org/10.18632/oncotarget.20936 (2017).
doi: 10.18632/oncotarget.20936
pubmed: 5675659
pmcid: 5675659
Sharpless, N. E. & Depinho, R. A. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat. reviews. Drug. discovery 5, 741–754, https://doi.org/10.1038/nrd2110 (2006).
doi: 10.1038/nrd2110
pubmed: 16915232
pmcid: 16915232
Yen, T. H. et al. Characterization of a murine xenograft model for contrast agent development in breast lesion malignancy assessment. J. Biomed. Sci. 23, 46, https://doi.org/10.1186/s12929-016-0261-4 (2016).
doi: 10.1186/s12929-016-0261-4
pubmed: 27188327
pmcid: 27188327
Zhao, X. et al. Quercetin inhibits angiogenesis by targeting calcineurin in the xenograft model of human breast cancer. Eur. J. Pharmacol., https://doi.org/10.1016/j.ejphar.2016.03.063 (2016).
Kawaguchi, T., Foster, B. A., Young, J. & Takabe, K. Current Update of Patient-Derived Xenograft Model for Translational Breast Cancer Research. J Mammary Gland Biol Neoplasia, https://doi.org/10.1007/s10911-017-9378-7 (2017).
Matossian, M. D. et al. A novel patient-derived xenograft model for claudin-low triple-negative breast cancer. Breast Cancer Res. Treat., https://doi.org/10.1007/s10549-018-4685-2 (2018).
Price, J. E. Metastasis from human breast cancer cell lines. Breast Cancer Res. Treat. 39, 93–102 (1996).
doi: 10.1007/BF01806081
pubmed: 8738609
pmcid: 8738609
Sloan, E. K. et al. Tumor-specific expression of alphavbeta3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res. 8, R20, https://doi.org/10.1186/bcr1398 (2006).
doi: 10.1186/bcr1398
pubmed: 16608535
pmcid: 16608535
Vargo-Gogola, T. & Rosen, J. M. Modelling breast cancer: one size does not fit all. Nat. reviews. Cancer 7, 659–672, https://doi.org/10.1038/nrc2193 (2007).
doi: 10.1038/nrc2193
pubmed: 17721431
pmcid: 17721431
Denzel, M. S. et al. Adiponectin deficiency limits tumor vascularization in the MMTV-PyV-mT mouse model of mammary cancer. Clin. Cancer Res. 15, 3256–3264, https://doi.org/10.1158/1078-0432.ccr-08-2661 (2009).
doi: 10.1158/1078-0432.ccr-08-2661
pubmed: 19447866
pmcid: 19447866
Herschkowitz, J. I. et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 8, R76, https://doi.org/10.1186/gb-2007-8-5-r76 (2007).
doi: 10.1186/gb-2007-8-5-r76
pubmed: 17493263
pmcid: 17493263
Lin, E. Y. et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 163, 2113–2126, https://doi.org/10.1016/s0002-9440(10)63568-7 (2003).
doi: 10.1016/s0002-9440(10)63568-7
pubmed: 1892434
pmcid: 1892434
Behbod, F. et al. An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ. Breast Cancer Res. 11, R66, https://doi.org/10.1186/bcr2358 (2009).
doi: 10.1186/bcr2358
pubmed: 2790841
pmcid: 2790841
Sflomos, G. et al. A Preclinical Model for ERalpha-Positive Breast Cancer Points to the Epithelial Microenvironment as Determinant of Luminal Phenotype and Hormone Response. Cancer Cell 29, 407–422, https://doi.org/10.1016/j.ccell.2016.02.002 (2016).
doi: 10.1016/j.ccell.2016.02.002
Ghosh, A. et al. MIND model for triple-negative breast cancer in syngeneic mice for quick and sequential progression analysis of lung metastasis. PLoS One 13, e0198143, https://doi.org/10.1371/journal.pone.0198143 (2018).
doi: 10.1371/journal.pone.0198143
pubmed: 5973560
pmcid: 5973560
Fiche, M. et al. Intraductal patient derived xenografts of estrogen receptor α positive (ER+) breast cancer recapitulate the histopathological spectrum and metastatic potential of human lesions. J. Pathol., https://doi.org/10.1002/path.5200 (2018).
C, J. et al. Expression profiling of purified normal human luminal and myoepithelial breast cells: identification of novel prognostic markers for breast cancer. Cancer research 64, 3037–3045, https://doi.org/10.1158/0008-5472.can-03-2028 (2004).
Adriance, M. C., Inman, J. L., Petersen, O. W. & Bissell, M. J. Myoepithelial cells: good fences make good neighbors. Breast cancer research: BCR 7, 190–197, https://doi.org/10.1186/bcr1286 (2005).
doi: 10.1186/bcr1286
Gudjonsson, T., Adriance, M. C., Sternlicht, M. D., Petersen, O. W. & Bissell, M. J. Myoepithelial cells: their origin and function in breast morphogenesis and neoplasia. J. mammary Gland. Biol. neoplasia 10, 261–272, https://doi.org/10.1007/s10911-005-9586-4 (2005).
doi: 10.1007/s10911-005-9586-4
pubmed: 2798159
pmcid: 2798159
Perou, C. M. et al. Molecular portraits of human breast tumours. Nat. 406, 747–752, https://doi.org/10.1038/35021093 (2000).
doi: 10.1038/35021093
de Visser, K. E., Eichten, A. & Coussens, L. M. Paradoxical roles of the immune system during cancer development. Nat. reviews. Cancer 6, 24–37, https://doi.org/10.1038/nrc1782 (2006).
doi: 10.1038/nrc1782
pubmed: 16397525
pmcid: 16397525
Keller, P. J. et al. Defining the cellular precursors to human breast cancer. Proc. Natl Acad. Sci. USA 109, 2772–2777, https://doi.org/10.1073/pnas.1017626108 (2012).
doi: 10.1073/pnas.1017626108
pubmed: 21940501
pmcid: 21940501
Tao, L., van Bragt, M. P. & Li, Z. A Long-Lived Luminal Subpopulation Enriched with Alveolar Progenitors Serves as Cellular Origin of Heterogeneous Mammary Tumors. Stem Cell Rep. 5, 60–74, https://doi.org/10.1016/j.stemcr.2015.05.014 (2015).
doi: 10.1016/j.stemcr.2015.05.014
Sirka, O. K., Shamir, E. R. & Ewald, A. J. Myoepithelial cells are a dynamic barrier to epithelial dissemination. J. Cell Biol., https://doi.org/10.1083/jcb.201802144 (2018).
Minn, A. J. et al. Genes that mediate breast cancer metastasis to lung. Nat. 436, 518–524, https://doi.org/10.1038/nature03799 (2005).
doi: 10.1038/nature03799
Wang, H. et al. The osteogenic niche promotes early-stage bone colonization of disseminated breast cancer cells. Cancer Cell 27, 193–210, https://doi.org/10.1016/j.ccell.2014.11.017 (2015).
doi: 10.1016/j.ccell.2014.11.017
pubmed: 25600338
pmcid: 25600338
Burnet, M. Cancer; a biological approach. I. The processes of control. Br. Med. J. 1, 779–786, https://doi.org/10.1136/bmj.1.5022.779 (1957).
doi: 10.1136/bmj.1.5022.779
pubmed: 13404306
pmcid: 13404306
Hao, N. B. et al. Macrophages in tumor microenvironments and the progression of tumors. Clin. developmental immunology 2012, 948098, https://doi.org/10.1155/2012/948098 (2012).
doi: 10.1155/2012/948098
Toh, B. et al. Immune predictors of cancer progression. Immunol. Res. 53, 229–234, https://doi.org/10.1007/s12026-012-8288-4 (2012).
doi: 10.1007/s12026-012-8288-4
pubmed: 22407576
pmcid: 22407576
Marabelle, A. et al. Depleting tumor-specific Tregs at a single site eradicates disseminated tumors. J. Clin. investigation 123, 2447–2463, https://doi.org/10.1172/jci64859 (2013).
doi: 10.1172/jci64859
Krause, S., Brock, A. & Ingber, D. E. Intraductal injection for localized drug delivery to the mouse mammary gland. J Vis Exp, https://doi.org/10.3791/50692 (2013).