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Effect of Breast Cancer and Adjuvant Therapy on Adipose-Derived Stromal Cells: Implications for the Role of ADSCs in Regenerative Strategies for Breast Reconstruction

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Abstract

Tissue engineering using Adipose Derived Stromal Cells (ADSCs) has emerged as a novel regenerative medicine approach to replace and reconstruct soft tissue damaged or lost as a result of disease process or therapeutic surgical resection. ADSCs are an attractive cell source for soft tissue regeneration due to the fact that they are easily accessible, multipotent, non-immunogenic and pro-angiogenic. ADSC based regenerative strategies have been successfully translated to the clinical setting for the treatment of Crohn’s fistulae, musculoskeletal pathologies, wound healing, and cosmetic breast augmentation (fat grafting). ADSCs are particularly attractive as a source for adipose tissue engineering as they exhibit preferential differentiation to adipocytes and support maintenance of mature adipose graft volume. The potential for reconstruction with an autologous tissue sources and a natural appearance and texture is particularly appealing in the setting of breast cancer; up to 40% of patients require mastectomy for locoregional control and current approaches to post-mastectomy breast reconstruction (PMBR) are limited by the potential for complications at the donor and reconstruction sites. Despite their potential, the use of ADSCs in breast cancer patients is controversial due to concerns regarding oncological safety. These concerns relate to the regeneration of tissue at a site where a malignancy has been treated and the impact this may have on stimulating local disease recurrence or dissemination. Pre-clinical data suggest that ADSCs exhibit pro-oncogenic characteristics and are involved in stimulating progression, and growth of tumour cells. However, there have been conflicting reports on the oncologic outcome, in terms of locoregional recurrence, for breast cancer patients in whom ADSC enhanced fat grafting was utilised as an alternative to reconstruction for small volume defects. A further consideration which may impact the successful translation of ADSC based regenerative strategies for post cancer reconstruction is the potential effects of cancer therapy. This review aims to address the effect of malignant cells, adjuvant therapies and patient-specific factors that may influence the success of regenerative strategies using ADSCs for post cancer tissue regeneration.

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References

  1. Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: a Cancer Journal for Clinicians, 68, 394–424. https://doi.org/10.3322/caac.21492.

    Article  Google Scholar 

  2. Wong, S. M., Freedman, R. A., Sagara, Y., Aydogan, F., Barry, W. T., & Golshan, M. (2017). Growing use of contralateral prophylactic mastectomy despite no improvement in long-term survival for invasive breast cancer. Annals of Surgery, 265(3), 581–589. https://doi.org/10.1097/SLA.0000000000001698.

    Article  PubMed  Google Scholar 

  3. Dragun, A. E., Huang, B., Tucker, T. C., & Spanos, W. J. (2012). Increasing mastectomy rates among all age groups for early stage breast cancer: A 10-year study of surgical choice. Breast Journal, 18(4), 318–325. https://doi.org/10.1111/j.1524-4741.2012.01245.x.

    Article  Google Scholar 

  4. Tuttle, T. M., Habermann, E. B., Grund, E. H., Morris, T. J., & Virnig, B. A. (2007). Increasing use of contralateral prophylactic mastectomy for breast cancer patients: A trend toward more aggressive surgical treatment. Journal of Clinical Oncology, 25(33), 5203–5209. https://doi.org/10.1200/JCO.2007.12.3141.

    Article  PubMed  Google Scholar 

  5. Mahmood, U., Hanlon, A. L., Koshy, M., Buras, R., Chumsri, S., Tkaczuk, K. H., Cheston, S. B., Regine, W. F., & Feigenberg, S. J. (2013). Increasing national mastectomy rates for the treatment of early stage breast cancer. Annals of Surgical Oncology, 20(5), 1436–1443. https://doi.org/10.1245/s10434-012-2732-5.

    Article  PubMed  Google Scholar 

  6. McCrate, F., Dicks, E., Powell, E., Chafe, J., Roome, R., Simmonds, C., & Etchegary, H. (2018). Surgical treatment choices for breast cancer in Newfoundland and Labrador: A retrospective cohort study. Canadian Journal of Surgery, 61(6), 377–384. https://doi.org/10.1503/cjs.015217.

    Article  PubMed Central  Google Scholar 

  7. Dicks, E., Roome, R., Chafe, J., Powell, E., McCrate, F., Simmonds, C., & Etchegary, H. (2019). Factors influencing surgical treatment decisions for breast cancer: A qualitative exploration of surgeon and patient perspectives. Current Oncology, 26(2), e216–e225. https://doi.org/10.3747/co.26.4305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Stavrou, D., Weissman, O., Polyniki, A., Papageorgiou, N., Haik, J., Farber, N., & Winkler, E. (2009). Quality of life after breast cancer surgery with or without reconstruction. Eplasty, 9, e18. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/19572009.

  9. O’Halloran, N., Courtney, D., Kerin, M. J., & Lowery, A. J. (2017). Adipose-derived stem cells in novel approaches to breast reconstruction: their suitability for tissue engineering and oncological safety. Breast Cancer : Basic and Clinical Research, 11, 1178223417726777. https://doi.org/10.1177/1178223417726777.

    Article  CAS  Google Scholar 

  10. Krzos, A., Stanisławek, A., Edrych, M. J., Łuczyk, M., & Slusarska, B. (2019). Satisfaction with the aesthetic effect and quality of life for women after breast conserving therapy (BCT)—Preliminary research. International Journal of Environmental Research and Public Health, 16(23). https://doi.org/10.3390/ijerph16234682.

  11. Choi, M., Small, K., Levovitz, C., Lee, C., Fadl, A., & Karp, N. S. (2013). The volumetric analysis of fat graft survival in breast reconstruction. Plastic and Reconstructive Surgery, 131(2), 185–191. https://doi.org/10.1097/PRS.0b013e3182789b13.

    Article  CAS  PubMed  Google Scholar 

  12. Varghese, J., Griffin, M., Mosahebi, A., & Butler, P. (2017). Systematic review of patient factors affecting adipose stem cell viability and function: Implications for regenerative therapy. Stem Cell Research & Therapy, 8(1), 45. https://doi.org/10.1186/s13287-017-0483-8.

    Article  CAS  Google Scholar 

  13. Frese, L., Dijkman, P. E., & Hoerstrup, S. P. (2016). Adipose tissue-derived stem cells in regenerative medicine. Transfusion Medicine and Hemotherapy : Offizielles Organ der Deutschen Gesellschaft fur Transfusionsmedizin und Immunhamatologie, 43(4), 268–274. https://doi.org/10.1159/000448180.

    Article  Google Scholar 

  14. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F. C., Krause, D. S., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8(4), 315–317. https://doi.org/10.1080/14653240600855905.

    Article  CAS  PubMed  Google Scholar 

  15. Han, S., Sun, H. M., Hwang, K. C., & Kim, S. W. (2015). Adipose-derived stromal vascular fraction cells: Update on clinical utility and efficacy. Critical Reviews in Eukaryotic Gene Expression, 25(2), 145–152. https://doi.org/10.1615/CritRevEukaryotGeneExpr.2015013057.

    Article  PubMed  Google Scholar 

  16. Hsu, V. M., Stransky, C. A., Bucky, L. P., & Percec, I. (2012). Fat grafting’s past, present, and future: Why adipose tissue is emerging as a critical link to the advancement of regenerative medicine. Aesthetic Surgery Journal, 32(7), 892–899. https://doi.org/10.1177/1090820X12455658.

    Article  PubMed  Google Scholar 

  17. Zwick, R. K., Guerrero-Juarez, C. F., Horsley, V., & Plikus, M. V. (2018). Anatomical, physiological, and functional diversity of adipose tissue. Cell Metabolism. Cell Press., 27, 68–83. https://doi.org/10.1016/j.cmet.2017.12.002.

    Article  CAS  Google Scholar 

  18. Saely, C. H., Geiger, K., & Drexel, H. (2012). Brown versus white adipose tissue: A mini-review. Gerontology, 58(1), 15–23. https://doi.org/10.1159/000321319.

    Article  PubMed  Google Scholar 

  19. Zwick, R. K., Rudolph, M. C., Shook, B. A., Holtrup, B., Roth, E., Lei, V., van Keymeulen, A., Seewaldt, V., Kwei, S., Wysolmerski, J., Rodeheffer, M. S., & Horsley, V. (2018). Adipocyte hypertrophy and lipid dynamics underlie mammary gland remodeling after lactation. Nature Communications, 9(1), 3592. https://doi.org/10.1038/s41467-018-05911-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Khan, M., & Joseph, F. (2014). Adipose tissue and adipokines: The association with and application of adipokines in obesity. Scientifica, 2014, 328592–328597. https://doi.org/10.1155/2014/328592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gonzalez, M. A., & Bernad, A. (2012). Characteristics of adult stem cells. Advances in Experimental Medicine and Biology, 741, 103–120. https://doi.org/10.1007/978-1-4614-2098-9_8.

    Article  CAS  PubMed  Google Scholar 

  22. Biehl, J. K., & Russell, B. (2009). Introduction to stem cell therapy. Journal of Cardiovascular Nursing, 24(2), 98–103. https://doi.org/10.1097/JCN.0b013e318197a6a5.

    Article  Google Scholar 

  23. Yu, G., Wu, X., Dietrich, M. A., Polk, P., Scott, L. K., Ptitsyn, A. A., & Gimble, J. M. (2010). Yield and characterization of subcutaneous human adipose-derived stem cells by flow cytometric and adipogenic mRNA analyzes. Cytotherapy, 12(4), 538–546. https://doi.org/10.3109/14653241003649528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li, J., Wong, W. H. S., Chan, S., Chim, J. C. S., Cheung, K. M. C., Lee, T. L., Au, W. Y., Ha, S. Y., Lie, A. K. W., Lau, Y. L., Liang, R. H. S., & Chan, G. C. F. (2011). Factors affecting mesenchymal stromal cells yield from bone marrow aspiration. Chinese Journal of Cancer Research, 23(1), 43–48. https://doi.org/10.1007/s11670-011-0043-1.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Tsuji, W. (2014). Adipose-derived stem cells: Implications in tissue regeneration. World Journal of Stem Cells, 6(3), 312–321. https://doi.org/10.4252/wjsc.v6.i3.312.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sterodimas, A., de Faria, J., Nicaretta, B., & Pitanguy, I. (2010). Tissue engineering with adipose-derived stem cells (ADSCs): Current and future applications. Journal of Plastic, Reconstructive & Aesthetic Surgery, 63(11), 1886–1892. https://doi.org/10.1016/j.bjps.2009.10.028.

    Article  Google Scholar 

  27. Panés, J., García-Olmo, D., Van Assche, G., Colombel, J. F., Reinisch, W., Baumgart, D. C., et al. (2016). Expanded allogeneic adipose-derived mesenchymal stem cells (Cx601) for complex perianal fistulas in Crohn’s disease: A phase 3 randomised, double-blind controlled trial. The Lancet, 388(10051), 1281–1290. https://doi.org/10.1016/S0140-6736(16)31203-X.

    Article  Google Scholar 

  28. Garcia-Olmo, D., Garcia-Arranz, M., & Herreros, D. (2008). Expanded adipose-derived stem cells for the treatment of complex perianal fistula including Crohn’s disease. Expert Opinion on Biological Therapy, 8(9), 1417–1423. https://doi.org/10.1517/14712598.8.9.1417.

    Article  CAS  PubMed  Google Scholar 

  29. Lendeckel, S., Jödicke, A., Christophis, P., Heidinger, K., Wolff, J., Fraser, J. K., Hedrick, M. H., Berthold, L., & Howaldt, H. P. (2004). Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: Case report. Journal of Cranio-Maxillofacial Surgery, 32(6), 370–373. https://doi.org/10.1016/j.jcms.2004.06.002.

    Article  PubMed  Google Scholar 

  30. Rigotti, G., Marchi, A., Galiè, M., Baroni, G., Benati, D., Krampera, M., et al. (2007). Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: A healing process mediated by adipose-derived adult stem cells. Plastic and Reconstructive Surgery, 119(5), 1409–1422. https://doi.org/10.1097/01.prs.0000256047.47909.71.

    Article  CAS  PubMed  Google Scholar 

  31. O’Halloran, N., Courtney, D., Kerin, M. J., & Lowery, A. J. (2017). Adipose-derived stem cells in novel approaches to breast reconstruction: Their suitability for tissue engineering and oncological safety. Breast Cancer: Basic and Clinical Research, 11, 117822341772677. https://doi.org/10.1177/1178223417726777.

    Article  CAS  Google Scholar 

  32. Kamakura, T., & Ito, K. (2011). Autologous cell-enriched fat grafting for breast augmentation. Aesthetic Plastic Surgery, 35(6), 1022–1030. https://doi.org/10.1007/s00266-011-9727-7.

    Article  PubMed  Google Scholar 

  33. Derby, B. M., Dai, H., Reichensperger, J., Cox, L., Harrison, C., Cosenza, N., Yang, M., Bueno, R. A., & Neumeister, M. W. (2014). Adipose-derived stem cell to epithelial stem cell transdifferentiation: A mechanism to potentially improve understanding of fat grafting’s impact on skin rejuvenation. Aesthetic Surgery Journal, 34(1), 142–153. https://doi.org/10.1177/1090820X13515700.

    Article  PubMed  Google Scholar 

  34. Pers, Y.-M., Rackwitz, L., Ferreira, R., Pullig, O., Delfour, C., Barry, F., et al. (2016). Adipose mesenchymal stromal cell-based therapy for severe osteoarthritis of the knee: A phase I dose-escalation trial. Stem Cells Translational Medicine, 5(7), 847–856. https://doi.org/10.5966/sctm.2015-0245.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kølle, S. T., Duscher, D., Taudorf, M., Fischer-Nielsen, A., Svalgaard, J. D., Munthe-Fog, L., et al. (2020). Ex vivo-expanded autologous adipose tissue-derived stromal cells ensure enhanced fat graft retention in breast augmentation: A randomized controlled clinical trial. STEM CELLS Translational Medicine, 1–10. https://doi.org/10.1002/sctm.20-0081.

  36. Guo, J., Widgerow, A. D., Banyard, D., Toranto, J., Wirth, G. A., Paydar, K., Tussardi, I. T., & Evans, G. R. D. (2015). Strategic sequences in fat graft survival. Annals of Plastic Surgery, 74(3), 376–382. https://doi.org/10.1097/SAP.0000000000000416.

    Article  CAS  PubMed  Google Scholar 

  37. Peltoniemi, H. H., Salmi, A., Miettinen, S., Mannerström, B., Saariniemi, K., Mikkonen, R., Kuokkanen, H., & Herold, C. (2013). Stem cell enrichment does not warrant a higher graft survival in lipofilling of the breast: A prospective comparative study. Journal of Plastic, Reconstructive and Aesthetic Surgery, 66(11), 1494–1503. https://doi.org/10.1016/j.bjps.2013.06.002.

    Article  PubMed  Google Scholar 

  38. Sterodimas, A., De Faria, J., Nicaretta, B., & Boriani, F. (2011). Autologous fat transplantation versus adipose-derived stem cell-enriched lipografts: A study. Aesthetic Surgery Journal, 31(6), 682–693. https://doi.org/10.1177/1090820X11415976.

    Article  PubMed  Google Scholar 

  39. Wu, W., Niklason, L., & Steinbacher, D. M. (2013). The effect of age on human adipose-derived stem cells. Plastic and Reconstructive Surgery, 131(1), 27–37. https://doi.org/10.1097/PRS.0b013e3182729cfc.

    Article  CAS  PubMed  Google Scholar 

  40. Efimenko, A., Dzhoyashvili, N., Kalinina, N., Kochegura, T., Akchurin, R., Tkachuk, V., & Parfyonova, Y. (2014). Adipose-derived mesenchymal stromal cells from aged patients with coronary artery disease keep mesenchymal stromal cell properties but exhibit characteristics of aging and have impaired angiogenic potential. Stem Cells Translational Medicine, 3(1), 32–41. https://doi.org/10.5966/sctm.2013-0014.

    Article  CAS  PubMed  Google Scholar 

  41. van Harmelen, V., Skurk, T., Röhrig, K., Lee, Y.-M., Halbleib, M., Aprath-Husmann, I., & Hauner, H. (2003). Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. International Journal of Obesity, 27(8), 889–895. https://doi.org/10.1038/sj.ijo.0802314.

    Article  PubMed  Google Scholar 

  42. Dufrane, D. (2017). Impact of age on human adipose stem cells for bone tissue engineering. Cell Transplantation, 26(9), 1496–1504. https://doi.org/10.1177/0963689717721203.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Choudhery, M. S., Badowski, M., Muise, A., Pierce, J., & Harris, D. T. (2014). Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. Journal of Translational Medicine, 12(1), 8. https://doi.org/10.1186/1479-5876-12-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kornicka, K., Marycz, K., Andrzej Tomaszewski, K., Marwdziak, M., & Umieszek, A. (2015). The effect of age on osteogenic and adipogenic differentiation potential of human adipose derived stromal stem cells (hASCs) and the impact of stress factors in the course of the differentiation process. Oxidative Medicine and Cellular Longevity, 2015(309169), 1–20. https://doi.org/10.1155/2015/309169.

    Article  Google Scholar 

  45. Aust, L., Devlin, B., Foster, S. J., Halvorsen, Y. D. C., Hicok, K., du Laney, T., Sen, A., Willingmyre, G. D., & Gimble, J. M. (2004). Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy, 6(1), 7–14. https://doi.org/10.1080/14653240310004539.

    Article  CAS  PubMed  Google Scholar 

  46. Roldan, M., Macias-Gonzalez, M., Garcia, R., Tinahones, F. J., & Martin, M. (2011). Obesity short-circuits stemness gene network in human adipose multipotent stem cells. The FASEB Journal, 25(12), 4111–4126. https://doi.org/10.1096/fj.10-171439.

    Article  CAS  PubMed  Google Scholar 

  47. Liu, J., Sato, C., Cerletti, M., & Wagers, A. (2010). Notch signaling in the regulation of stem cell self-renewal and differentiation. Current Topics in Developmental Biology, 92, 367–409. https://doi.org/10.1016/S0070-2153(10)92012-7.

    Article  CAS  PubMed  Google Scholar 

  48. Nusse, R. (2008). Wnt signaling and stem cell control. Cell Research, 18(5), 523–527. https://doi.org/10.1038/cr.2008.47.

    Article  CAS  PubMed  Google Scholar 

  49. Schweizer, R., Tsuji, W., Gorantla, V. S., Marra, K. G., Rubin, J. P., & Plock, J. A. (2015). The role of adipose-derived stem cells in breast cancer progression and metastasis. Stem Cells International, 2015, 1–17. https://doi.org/10.1155/2015/120949.

    Article  Google Scholar 

  50. Karastergiou, K., Smith, S. R., Greenberg, A. S., & Fried, S. K. (2012). Sex differences in human adipose tissues - the biology of pear shape. Biology of Sex Differences, 3(1), 13. https://doi.org/10.1186/2042-6410-3-13.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Abate, N., & Garg, A. (1995). Heterogeneity in adipose tissue metabolism: causes, implications and management of regional adiposity. Progress in Lipid Research, 34(1), 53–70. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7644553.

  52. Pallottini, V., Bulzomi, P., Galluzzo, P., Martini, C., & Marino, M. (2012). Estrogen regulation of adipose tissue functions: involvement of estrogen receptor isoforms. Infectious Disorders - Drug Targets, 8(1), 52–60. https://doi.org/10.2174/187152608784139631.

    Article  Google Scholar 

  53. Dieudonné, M. N., Leneveu, M. C., Giudicelli, Y., & Pecquery, R. (2004). Evidence for functional estrogen receptors α and β in human adipose cells: Regional specificities and regulation by estrogens. American Journal of Physiology - Cell Physiology, 286(3), 55–53. https://doi.org/10.1152/ajpcell.00321.2003.

    Article  Google Scholar 

  54. Park, Y. M., Erickson, C., Bessesen, D., Van Pelt, R. E., & Cox-York, K. (2017). Age- and menopause-related differences in subcutaneous adipose tissue estrogen receptor mRNA expression. Steroids, 121, 17–21. https://doi.org/10.1016/j.steroids.2017.03.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Goedecke, J. H., Tootla, M., & Keswell, D. (2019). Ethnic differences in regional adipose tissue oestrogen receptor gene expression. Endocrine Connections, 8(1), 32–38. https://doi.org/10.1530/EC-18-0531.

    Article  CAS  PubMed  Google Scholar 

  56. Frank, A. P., De, R., Santos, S., Palmer, B. F., & Clegg, D. J. (2019). Determinants of body fat distribution in humans may provide insight about obesity-related health risks. Journal of Lipid Research, 60(10), 1710–1719. Retrieved from www.jlr.org

  57. Karastergiou, K., & Fried, S. K. (2017). Cellular mechanisms driving sex differences in adipose tissue biology and body shape in humans and mouse models. In Advances in experimental medicine and biology (Vol. 1043, pp. 29–51). https://doi.org/10.1007/978-3-319-70178-3_3.

    Chapter  Google Scholar 

  58. Eaton, S. A., & Sethi, J. K. (2019). Immunometabolic links between estrogen, adipose tissue and female reproductive metabolism. Biology. MDPI AG., 8. https://doi.org/10.3390/biology8010008.

  59. Fu, Y., Li, R., Zhong, J., Fu, N., Wei, X., Cun, X., Deng, S., Li, G., Xie, J., Cai, X., & Lin, Y. (2014). Adipogenic differentiation potential of adipose-derived mesenchymal stem cells from ovariectomized mice. Cell Proliferation, 47(6), 604–614. https://doi.org/10.1111/cpr.12131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lim, S., Kim, I.-K., Choi, J.-W., Seo, H.-H., Lim, K. H., Lee, S., Lee, H. B., Kim, S. W., & Hwang, K.-C. (2017). Gender-dimorphic effects of adipose-derived stromal vascular fractions on HUVECs exposed to oxidative stress. International Journal of Medical Sciences, 14(9), 911–919. https://doi.org/10.7150/ijms.19998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Sukho, P., Kirpensteijn, J., Hesselink, J. W., van Osch, G. J. V. M., Verseijden, F., & Bastiaansen-Jenniskens, Y. M. (2017). Effect of cell seeding density and inflammatory cytokines on adipose tissue-derived stem cells: an in vitro study. Stem Cell Reviews, 13(2), 267–277. https://doi.org/10.1007/S12015-017-9719-3.

    Article  CAS  PubMed Central  Google Scholar 

  62. Hashemibeni, B., Atef, F., Salehi, H., Shabani, F., Sadeghi, F., & Esfandiari, E. (2015). The effect of estrogen on the expression of cartilage-specific genes in the chondrogenesis process of adipose-derived stem cells. Advanced Biomedical Research, 4(1), 43. https://doi.org/10.4103/2277-9175.151252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Feng, C., Hu, J., Liu, C., Liu, S., Liao, G., Song, L., & Zeng, X. (2016). Association of 17-β estradiol with adipose-derived stem cells: new strategy to produce functional myogenic differentiated cells with a nano-scaffold for tissue engineering. PLoS One, 11(10), e0164918. https://doi.org/10.1371/journal.pone.0164918.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Luo, S., Hao, L., Li, X., Yu, D., Diao, Z., Ren, L., & Xu, H. (2013). Adipose tissue-derived stem cells treated with estradiol enhance survival of autologous fat transplants. Tohoku Journal of Experimental Medicine, 231(2), 101–110. https://doi.org/10.1620/tjem.231.101.

    Article  CAS  Google Scholar 

  65. Hong, L., Colpan, A., Peptan, I. A., Daw, J., George, A., & Evans, C. A. (2007). 17-β estradiol enhances osteogenic and adipogenic differentiation of human adipose-derived stromal cells. Tissue Engineering, 13(6), 1197–1203. https://doi.org/10.1089/ten.2006.0317.

    Article  CAS  PubMed  Google Scholar 

  66. Cox-York, K. A., Erickson, C. B., Pereira, R. I., Bessesen, D. H., & Van Pelt, R. E. (2017). Region-specific effects of oestradiol on adipose-derived stem cell differentiation in post-menopausal women. Journal of Cellular and Molecular Medicine, 21(4), 677–684. https://doi.org/10.1111/jcmm.13011.

    Article  CAS  PubMed  Google Scholar 

  67. Steinberg, K. K., Thacker, S. B., Smith, S. J., Stroup, D. F., Zack, M. M., Flanders, W. D., & Berkelman, R. L. (1991). A meta-analysis of the effect of estrogen replacement therapy on the risk of breast cancer. JAMA: The Journal of the American Medical Association, 265(15), 1985–1990. https://doi.org/10.1001/jama.1991.03460150089030.

    Article  CAS  PubMed  Google Scholar 

  68. Ross, R. K., Paganini-Hill, A., Wan, P. C., & Pike, M. C. (2000). Effect of hormone replacement therapy on breast cancer risk: estrogen versus estrogen plus progestin. JNCI: Journal of the National Cancer Institute, 92(4), 328–332. https://doi.org/10.1093/jnci/92.4.328.

    Article  CAS  PubMed  Google Scholar 

  69. Group on Hormonal Factors in Breast Cancer, C. (2019). Type and timing of menopausal hormone therapy and breast cancer risk: individual participant meta-analysis of the worldwide epidemiological evidence. The Lancet, 394(10204), 1159–1168. https://doi.org/10.1016/S0140-6736(19)31709-X.

    Article  Google Scholar 

  70. Hamajima, N., Hirose, K., Tajima, K., Rohan, T., Friedenreich, C. M., Calle, E. E., et al. (2012). Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. The Lancet Oncology, 13(11), 1141–1151. https://doi.org/10.1016/S1470-2045(12)70425-4.

    Article  Google Scholar 

  71. Higgins, M. J., & Baselga, J. (2011). Targeted therapies for breast cancer. Journal of Clinical Investigation, 121(10), 3797–3803. https://doi.org/10.1172/JCI57152.

    Article  CAS  Google Scholar 

  72. Wahl, E. A., Schenck, T. L., Machens, H. G., & Egaña, J. T. (2016). Acute stimulation of mesenchymal stem cells with cigarette smoke extract affects their migration, differentiation, and paracrine potential. Scientific Reports, 6. https://doi.org/10.1038/srep22957.

  73. Barwinska, D., Traktuev, D. O., Merfeld-Clauss, S., Cook, T. G., Lu, H., Petrache, I., & March, K. L. (2018). Cigarette smoking impairs adipose stromal cell vasculogenic activity and abrogates potency to ameliorate ischemia. Stem Cells, 36(6), 856–867. https://doi.org/10.1002/stem.2813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Di Rocco, G., Baldari, S., Pani, G., & Toietta, G. (2019). Stem cells under the influence of alcohol: effects of ethanol consumption on stem/progenitor cells. Cellular and Molecular Life Sciences. Birkhauser Verlag AG., 76, 231–244. https://doi.org/10.1007/s00018-018-2931-8.

    Article  CAS  Google Scholar 

  75. Khacho, M., & Slack, R. S. (2018). Mitochondrial and reactive oxygen species signaling coordinate stem cell fate decisions and life long maintenance. Antioxidants and Redox Signaling. Mary Ann Liebert Inc., 28, 1090–1101. https://doi.org/10.1089/ars.2017.7228.

    Article  CAS  Google Scholar 

  76. Saeedi, P., Petersohn, I., Salpea, P., Malanda, B., Karuranga, S., Unwin, N., … Williams, R. (2019). Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation diabetes Atlas, 9th edition. Diabetes Research and Clinical Practice, 157. https://doi.org/10.1016/j.diabres.2019.107843.

  77. Forouhi, N. G., & Wareham, N. J. (2019). Epidemiology of diabetes. Medicine (United Kingdom). Elsevier Ltd. https://doi.org/10.1016/j.mpmed.2018.10.004.

  78. Rennert, R. C., Sorkin, M., Januszyk, M., Duscher, D., Kosaraju, R., Chung, M. T., Lennon, J., Radiya-Dixit, A., Raghvendra, S., Maan, Z. N., Hu, M. S., Rajadas, J., Rodrigues, M., & Gurtner, G. C. (2014). Diabetes impairs the angiogenic potential of adipose-derived stem cells by selectively depleting cellular subpopulations. Stem Cell Research & Therapy, 5(3), 79. https://doi.org/10.1186/scrt468.

    Article  CAS  Google Scholar 

  79. Minteer, D. M., Young, M. T., Lin, Y.-C., Over, P. J., Rubin, J. P., Gerlach, J. C., & Marra, K. G. (2015). Analysis of type II diabetes mellitus adipose-derived stem cells for tissue engineering applications. Journal of Tissue Engineering, 6, 204173141557921. https://doi.org/10.1177/2041731415579215.

    Article  CAS  Google Scholar 

  80. Minteer, D. M., Young, M. T., Lin, Y. C., Over, P. J., Rubin, J. P., Gerlach, J. C., & Marra, K. G. (2015). Analysis of type II diabetes mellitus adipose-derived stem cells for tissue engineering applications. Journal of Tissue Engineering, 6, 6. https://doi.org/10.1177/2041731415579215.

    Article  CAS  Google Scholar 

  81. Dzhoyashvili, N. A., Efimenko, A. Y., Kochegura, T. N., Kalinina, N. I., Koptelova, N. V., Sukhareva, O. Y., Shestakova, M. V., Akchurin, R. S., Tkachuk, V. A., & Parfyonova, Y. V. (2014). Disturbed angiogenic activity of adipose-derived stromal cells obtained from patients with coronary artery disease and diabetes mellitus type 2. Journal of Translational Medicine, 12(1), 337. https://doi.org/10.1186/s12967-014-0337-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Marycz, K., Tomaszewski, K. A., Kornicka, K., Henry, B. M., Wroński, S., Tarasiuk, J., & Maredziak, M. (2016). Metformin decreases reactive oxygen species, enhances osteogenic properties of adipose-derived multipotent mesenchymal stem cells in vitro, and increases bone density in vivo. Oxidative Medicine and Cellular Longevity, 2016. https://doi.org/10.1155/2016/9785890.

  83. Obregon, M.-J. (2008). Thyroid hormone and adipocyte differentiation. Thyroid, 18(2), 185–195. https://doi.org/10.1089/thy.2007.0254.

    Article  CAS  PubMed  Google Scholar 

  84. Haraguchi, K., Shimura, H., Kawaguchi, A., Ikeda, M., Endo, T., & Onaya, T. (1999). Effects of thyrotropin on the proliferation and differentiation of cultured rat preadipocytes. Thyroid, 9(6), 613–619. https://doi.org/10.1089/thy.1999.9.613.

    Article  CAS  PubMed  Google Scholar 

  85. Simsek, T., Duruksu, G., Okçu, A., Aksoy, A., Erman, G., Utkan, Z., & Karaöz, E. (2014). Effect of hypothyroidism in the thyroidectomized rats on immunophenotypic characteristics and differentiation capacity of adipose tissue derived stem cells. European Review for Medical and Pharmacological Sciences, 18(5), 617–29. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/24668701.

  86. López-Fontana, C. M., Pennacchio, G., Zyla, L. E., Toneatto, J., Bruna, F. A., Ortiz, N., Sassi, P. L., Santiano, F. E., García, S., Sasso, C. V., Pietrobon, E. O., Jahn, G. A., Pistone Creydt, V., Soaje, M., & Carón, R. W. (2019). Effects of hypothyroidism on the mesenteric and omental adipose tissue in rats. Molecular and Cellular Endocrinology, 490, 88–99. https://doi.org/10.1016/j.mce.2019.04.011.

    Article  CAS  PubMed  Google Scholar 

  87. Chazenbalk, G., Singh, P., Irge, D., Shah, A., Abbott, D. H., & Dumesic, D. A. (2013). Androgens inhibit adipogenesis during human adipose stem cell commitment to preadipocyte formation. Steroids, 78(9), 920–926. https://doi.org/10.1016/j.steroids.2013.05.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Eterno, V., Zambelli, A., Pavesi, L., Villani, L., Zanini, V., Petrolo, G., et al. (2014). Adipose-derived mesenchymal stem cells (ASCs) may favour breast cancer recurrence via HGF/c-Met signaling. Oncotarget, 5(3), 613–633. https://doi.org/10.18632/oncotarget.1359.

    Article  PubMed  Google Scholar 

  89. Chen, Y., He, Y., Wang, X., Lu, F., & Gao, J. (2019). Adipose-derived mesenchymal stem cells exhibit tumor tropism and promote tumorsphere formation of breast cancer cells. Oncology Reports, 41(4), 2126–2136. https://doi.org/10.3892/or.2019.7018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Scioli, M. G., Storti, G., D’Amico, F., Gentile, P., Kim, B.-S., Cervelli, V., & Orlandi, A. (2019). Adipose-derived stem cells in cancer progression: new perspectives and opportunities. International Journal of Molecular Sciences, 20(13), 3296. https://doi.org/10.3390/ijms20133296.

    Article  CAS  PubMed Central  Google Scholar 

  91. Jotzu, C., Alt, E., Welte, G., Li, J., Hennessy, B. T., Devarajan, E., Krishnappa, S., Pinilla, S., Droll, L., & Song, Y.-H. (2010). Adipose tissue-derived stem cells differentiate into carcinoma-associated fibroblast-like cells under the influence of tumor-derived factors. Analytical Cellular Pathology (Amsterdam), 33(2), 61–79. https://doi.org/10.3233/ACP-CLO-2010-0535.

    Article  CAS  Google Scholar 

  92. Dirat, B., Bochet, L., Dabek, M., Daviaud, D., Dauvillier, S., Majed, B., Wang, Y. Y., Meulle, A., Salles, B., le Gonidec, S., Garrido, I., Escourrou, G., Valet, P., & Muller, C. (2011). Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Research, 71(7), 2455–2465. https://doi.org/10.1158/0008-5472.CAN-10-3323.

    Article  CAS  PubMed  Google Scholar 

  93. Eterno, V., Zambelli, A., Pavesi, L., Villani, L., Zanini, V., Petrolo, G., et al. (2014). Adipose-derived mesenchymal stem cells (ASCs) may favour breast cancer recurrence via HGF/c-Met signaling. Oncotarget, 5(3), 613–633. https://doi.org/10.18632/oncotarget.1359.

    Article  PubMed  Google Scholar 

  94. Schweizer, R., Tsuji, W., Gorantla, V. S., Marra, K. G., Rubin, J. P., & Plock, J. A. (2015). The role of adipose-derived stem cells in breast cancer progression and metastasis. Stem Cells International, 2015, 1–17. https://doi.org/10.1155/2015/120949.

    Article  Google Scholar 

  95. Lapeire, L., Hendrix, A., Lecoutere, E., Van Bockstal, M., Vandesompele, J., Maynard, D., et al. (2017). Secretome analysis of breast cancer-associated adipose tissue to identify paracrine regulators of breast cancer growth. Oncotarget, 8(29), 47239–47249. https://doi.org/10.18632/oncotarget.17592.

    Article  PubMed  Google Scholar 

  96. Wang, S., Li, X., Xu, M., Wang, J., & Zhao, R. C. (2017). Reduced adipogenesis after lung tumor exosomes priming in human mesenchymal stem cells via TGFβ signaling pathway. Molecular and Cellular Biochemistry, 435(1–2), 59–66. https://doi.org/10.1007/s11010-017-3056-3.

    Article  CAS  PubMed  Google Scholar 

  97. Morgan, M. M., Arendt, L. M., Alarid, E. T., Beebe, D. J., & Johnson, B. P. (2019). Mammary adipose stromal cells derived from obese women reduce sensitivity to the aromatase inhibitor anastrazole in an organotypic breast model. FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology, 33(7), 8623–8633. https://doi.org/10.1096/fj.201802347RRR.

    Article  CAS  Google Scholar 

  98. Su, F., Ahn, S., Saha, A., DiGiovanni, J., & Kolonin, M. G. (2019). Adipose stromal cell targeting suppresses prostate cancer epithelial-mesenchymal transition and chemoresistance. Oncogene, 38(11), 1979–1988. https://doi.org/10.1038/s41388-018-0558-8.

    Article  CAS  PubMed  Google Scholar 

  99. Olea-Flores, M., Juárez-Cruz, J. C., Mendoza-Catalán, M. A., Padilla-Benavides, T., & Navarro-Tito, N. (2018). Signaling pathways induced by leptin during epithelial−mesenchymal transition in breast cancer. International Journal of Molecular Sciences. NLM (Medline)., 19. https://doi.org/10.3390/ijms19113493.

  100. Yan, D., Avtanski, D., Saxena, N. K., & Sharma, D. (2012). Leptin-induced epithelial-mesenchymal transition in breast cancer cells requires β-catenin activation via Akt/GSK3- and MTA1/Wnt1 protein-dependent pathways. Journal of Biological Chemistry, 287(11), 8598–8612. https://doi.org/10.1074/jbc.M111.322800.

    Article  CAS  Google Scholar 

  101. Bousquenaud, M., Fico, F., Solinas, G., Rüegg, C., & Santamaria-Martínez, A. (2018). Obesity promotes the expansion of metastasis-initiating cells in breast cancer. Breast Cancer Research, 20(1), 104. https://doi.org/10.1186/s13058-018-1029-4.

    Article  CAS  PubMed  Google Scholar 

  102. Shiga, K., Hara, M., Nagasaki, T., Sato, T., Takahashi, H., & Takeyama, H. (2015). Cancer-associated fibroblasts: their characteristics and their roles in tumor growth. Cancers. MDPI AG., 7, 2443–2458. https://doi.org/10.3390/cancers7040902.

    Article  Google Scholar 

  103. Moltó-García, R., González-Alonso, V., Villaverde-Doménech, M. E., & Novella-Maestre, E. (2017). Effect of human fat graft on breast cancer metastasis in a murine model. Plastic and Reconstructive Surgery, 139(5), 1119–1128. https://doi.org/10.1097/PRS.0000000000003274.

    Article  CAS  PubMed  Google Scholar 

  104. Chang, Y. H., Liu, H. W., Chu, T. Y., Wen, Y. T., Tsai, R. K., & Ding, D. C. (2017). Cisplatin-impaired adipogenic differentiation of adipose mesenchymal stem cells. Cell Transplantation, 26(6), 1077–1087. https://doi.org/10.3727/096368917X694886.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Furuhata, Y., Kikuchi, Y., Tomita, S., & Yoshimoto, K. (2016). Small spheroids of adipose-derived stem cells with time-dependent enhancement of IL-8 and VEGF-A secretion. Genes to Cells : Devoted to Molecular & Cellular Mechanisms, 21(12), 1380–1386. https://doi.org/10.1111/gtc.12448.

    Article  CAS  Google Scholar 

  106. Heo, S. C., Jeon, E. S., Lee, I. H., Kim, H. S., Kim, M. B., & Kim, J. H. (2011). Tumor necrosis factor-α-activated human adipose tissue-derived mesenchymal stem cells accelerate cutaneous wound healing through paracrine mechanisms. The Journal of Investigative Dermatology, 131(7), 1559–1567. https://doi.org/10.1038/jid.2011.64.

    Article  CAS  PubMed  Google Scholar 

  107. Liang, W., Xia, H., Li, J., & Zhao, R. C. (2011). Human adipose tissue derived mesenchymal stem cells are resistant to several chemotherapeutic agents. Cytotechnology, 63(5), 523–530. https://doi.org/10.1007/s10616-011-9374-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Liang, W., Xia, H., Li, J., & Zhao, R. C. (2011). Human adipose tissue derived mesenchymal stem cells are resistant to several chemotherapeutic agents. Cytotechnology, 63(5), 523–530. https://doi.org/10.1007/s10616-011-9374-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Saijo, H., Suzuki, K., Yoshimoto, H., Imamura, Y., Yamashita, S., & Tanaka, K. (2019). Paracrine effects of adipose-derived stem cells promote lymphangiogenesis in irradiated lymphatic endothelial cells. Plastic and Reconstructive Surgery, 143(6), 1189e–1200e. https://doi.org/10.1097/PRS.0000000000005669.

    Article  CAS  PubMed  Google Scholar 

  110. Qi, Z., Zhang, Y., Liu, L., Guo, X., Qin, J., & Cui, G. (2012). Mesenchymal stem cells derived from different origins have unique sensitivities to different chemotherapeutic agents. Cell Biology International, 36(9), 857–862. https://doi.org/10.1042/cbi20110637.

    Article  CAS  PubMed  Google Scholar 

  111. Gebremeskel, S., Gencarelli, J., Gareau, A. J., Levatte, T., Dugandzic, A., Johnston, B., & Bezuhly, M. (2019). Promotion of primary murine breast cancer growth and metastasis by adipose-derived stem cells is reduced in the presence of autologous fat graft. Plastic and Reconstructive Surgery, 143(1), 137–147. https://doi.org/10.1097/PRS.0000000000005142.

    Article  CAS  PubMed  Google Scholar 

  112. Wu, Q., Jin, C.-X., Chen, H., Li, X.-Y., & Li, Y.-J. (2017). Interaction of adipose-derived mesenchymal stem cells with MCF-7 cells in vitro: a study emphasizing signaling molecule expression and transcriptional changes. Turkish Journal of Biology, 41, 785–795. https://doi.org/10.3906/biy-1701-23.

    Article  CAS  Google Scholar 

  113. Mentoor, I., Engelbrecht, A.-M., van Jaarsveld, P. J., & Nell, T. (2018). Chemoresistance: intricate interplay between breast tumor cells and adipocytes in the tumor microenvironment. Frontiers in Endocrinology, 9, 758. https://doi.org/10.3389/fendo.2018.00758.

    Article  PubMed  PubMed Central  Google Scholar 

  114. Li, J., Law, H. K. W., Lau, Y. L., & Chan, G. C. F. (2004). Differential damage and recovery of human mesenchymal stem cells after exposure to chemotherapeutic agents. British Journal of Haematology, 127(3), 326–334. https://doi.org/10.1111/j.1365-2141.2004.05200.x.

    Article  CAS  PubMed  Google Scholar 

  115. Razmkhah, M., Jaberipour, M., Hosseini, A., Safaei, A., Khalatbari, B., & Ghaderi, A. (2010). Expression profile of IL-8 and growth factors in breast cancer cells and adipose-derived stem cells (ASCs) isolated from breast carcinoma. Cellular Immunology, 265(1), 80–85. https://doi.org/10.1016/j.cellimm.2010.07.006.

    Article  CAS  PubMed  Google Scholar 

  116. Myckatyn, T. M., Wagner, I. J., Mehrara, B. J., Crosby, M. A., Park, J. E., Qaqish, B. F., Moore, D. T., Busch, E. L., Silva, A. K., Kaur, S., Ollila, D. W., & Lee, C. N. (2017). Cancer risk after fat transfer: a multicenter case-cohort study. Plastic and Reconstructive Surgery, 139(1), 11–18. https://doi.org/10.1097/PRS.0000000000002838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Petit, J. Y., Botteri, E., Lohsiriwat, V., Rietjens, M., De lorenzi, F., Garusi, C., et al. (2012). Locoregional recurrence risk after lipofilling in breast cancer patients. Annals of Oncology, 23(3), 582–588. https://doi.org/10.1093/annonc/mdr158.

    Article  CAS  PubMed  Google Scholar 

  118. Stumpf, C. C., Biazus, J. V., Zucatto, F. S. Â. E., Cericatto, R., Cavalheiro, J. A. C., Damin, A. P. S., & Melo, M. P. (2017). Reconstrução imediata com enxerto autólogo de gordura: Influência na recorrência local de câncer de mama. Revista do Colegio Brasileiro de Cirurgioes, 44(2), 179–186. https://doi.org/10.1590/0100-69912017002012.

    Article  PubMed  Google Scholar 

  119. Silva-Vergara, C., Fontdevila, J., Descarrega, J., Burdio, F., Yoon, T. S., & Grande, L. (2016). Oncological outcomes of lipofilling breast reconstruction: 195 consecutive cases and literature review. Journal of Plastic, Reconstructive and Aesthetic Surgery, 69(4), 475–481. https://doi.org/10.1016/j.bjps.2015.12.029.

    Article  PubMed  Google Scholar 

  120. Brenelli, F., Rietjens, M., De Lorenzi, F., Pinto-Neto, A., Rossetto, F., Martella, S., et al. (2014). Oncological safety of autologous fat grafting after breast conservative treatment: a prospective evaluation. Breast Journal, 20(2), 159–165. https://doi.org/10.1111/tbj.12225.

    Article  Google Scholar 

  121. Waked, K., Colle, J., Doornaert, M., Cocquyt, V., & Blondeel, P. (2017). Systematic review: the oncological safety of adipose fat transfer after breast cancer surgery. Breast. Churchill Livingstone., 31, 128–136. https://doi.org/10.1016/j.breast.2016.11.001.

    Article  Google Scholar 

  122. Ragaz, J., Olivotto, I. A., Spinelli, J. J., Phillips, N., Jackson, S. M., Wilson, K. S., Knowling, M. A., Coppin, C. M. L., Weir, L., Gelmon, K., le, N., Durand, R., Coldman, A. J., & Manji, M. (2005). Locoregional radiation therapy in patients with high-risk breast cancer receiving adjuvant chemotherapy: 20-year results of the British Columbia randomized trial. JNCI Journal of the National Cancer Institute, 97(2), 116–126. https://doi.org/10.1093/jnci/djh297.

    Article  PubMed  Google Scholar 

  123. Cosar, R., Uzal, C., Tokatli, F., Denizli, B., Saynak, M., Turan, N., Uzunoglu, S., Ozen, A., Sezer, A., Ibis, K., Uregen, B., Yurut-Caloglu, V., & Kocak, Z. (2011). Postmastectomy irradiation in breast in breast cancer patients with T1-2 and 1-3 positive axillary lymph nodes: is there a role for radiation therapy? Radiation Oncology, 6(1), 28. https://doi.org/10.1186/1748-717X-6-28.

    Article  PubMed  Google Scholar 

  124. Shirato, H., Le, Q. T., Kobashi, K., Prayongrat, A., Takao, S., Shimizu, S., et al. (2018). Selection of external beam radiotherapy approaches for precise and accurate cancer treatment. Journal of Radiation Research, 59, i2–i10. https://doi.org/10.1093/jrr/rrx092.

    Article  PubMed  PubMed Central  Google Scholar 

  125. San-Marina, S., Voss, S., Crespo-Diaz, R., Wyles, C., Behfar, A., Stalboeger, P., & Janus, J. R. (2016). Adipose-derived mesenchymal stem cell features in patients with a history of head and neck radiation. Laryngoscope Investigative Otolaryngology, 1(3), 36–41. https://doi.org/10.1002/lio2.19.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Schröder, A., Kriesen, S., Hildebrandt, G., & Manda, K. (2019). First insights into the effect of low-dose X-ray irradiation in adipose-derived stem cells. International Journal of Molecular Sciences, 20(23). https://doi.org/10.3390/ijms20236075.

  127. Maria, O. M., Kumala, S., Heravi, M., Syme, A., Eliopoulos, N., & Muanza, T. (2016). Adipose mesenchymal stromal cells response to ionizing radiation. Cytotherapy, 18(3), 384–401. https://doi.org/10.1016/j.jcyt.2015.12.001.

    Article  CAS  PubMed  Google Scholar 

  128. Baaße, A., Machoy, F., Juerß, D., Baake, J., Stang, F., Reimer, T., Krapohl, B., & Hildebrandt, G. (2018). Radiation sensitivity of adipose-derived stem cells isolated from breast tissue. International Journal of Molecular Sciences, 19(7). https://doi.org/10.3390/ijms19071988.

  129. Van de putte, D., Demarquay, C., Van Daele, E., Moussa, L., Vanhove, C., Benderitter, M., et al. (2017). Adipose-derived mesenchymal stromal cells improve the healing of colonic anastomoses following high dose of irradiation through anti-inflammatory and angiogenic processes. Cell Transplantation, 26(12), 1919–1930. https://doi.org/10.1177/0963689717721515.

    Article  PubMed  Google Scholar 

  130. Chang, P., Qu, Y., Liu, Y., Cui, S., Zhu, D., Wang, H., & Jin, X. (2013). Multi-therapeutic effects of human adipose-derived mesenchymal stem cells on radiation-induced intestinal injury. Cell Death and Disease, 4(6), e685. https://doi.org/10.1038/cddis.2013.178.

    Article  CAS  PubMed  Google Scholar 

  131. Gilazieva, Z., Tazetdinova, L., Arkhipova, S., Solovyeva, V., & Rizvanov, A. (2016). Effect of cisplatin on ultrastructure and viability of adipose-derived mesenchymal stem cells. BioNanoScience, 6(4), 534–539. https://doi.org/10.1007/s12668-016-0283-0.

    Article  Google Scholar 

  132. Ho, I. L., Kuo, K. L., Liu, S. H., Chang, H. C., Hsieh, J. T., Wu, J. T., et al. (2015). MLN4924 synergistically enhances cisplatin-induced cytotoxicity via jnk and bcl-xl pathways in human urothelial carcinoma. Scientific Reports, 5. https://doi.org/10.1038/srep16948.

  133. Sahu, B. D., Kumar, J. M., & Sistla, R. (2015). Baicalein, a bioflavonoid, prevents cisplatin- induced acute kidney injury by up- regulating antioxidant defenses and down- regulating the MAPKs and NF-κB pathways. PLoS One, 10(7), e0134139. https://doi.org/10.1371/journal.pone.0134139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Beane, O. S., Fonseca, V. C., & Darling, E. M. (2014). Adipose-derived stem cells retain their regenerative potential after methotrexate treatment. Experimental Cell Research, 327(2), 222–233. https://doi.org/10.1016/j.yexcr.2014.06.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Choron, R. L., Chang, S., Khan, S., Villalobos, M. A., Zhang, P., Carpenter, J. P., Tulenko, T. N., & Liu, Y. (2015). Paclitaxel impairs adipose stem cell proliferation and differentiation. The Journal of Surgical Research, 196(2), 404–415. https://doi.org/10.1016/j.jss.2015.03.026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Harris, W. M., Zhang, P., Plastini, M., Ortiz, T., Kappy, N., Benites, J., Alexeev, E., Chang, S., Brockunier, R., Carpenter, J. P., & Brown, S. A. (2017). Evaluation of function and recovery of adipose-derived stem cells after exposure to paclitaxel. Cytotherapy, 19(2), 211–221. https://doi.org/10.1016/j.jcyt.2016.10.010.

    Article  CAS  PubMed  Google Scholar 

  137. Bonomi, A., Coccè, V., Cavicchini, L., Sisto, F., Dossena, M., Balzarini, P., et al. (2013). Adipose tissue-derived stromal cells primed in vitro with paclitaxel acquire anti-tumor activity. International Journal of Immunopathology and Pharmacology, 26(1_suppl), 33–41. https://doi.org/10.1177/03946320130260S105.

    Article  CAS  PubMed  Google Scholar 

  138. Scioli, M. G., Artuso, S., D’Angelo, C., Porru, M., D’Amico, F., Bielli, A., et al. (2018). Adipose-derived stem cell-mediated paclitaxel delivery inhibits breast cancer growth. PLoS One, 13(9), e0203426. https://doi.org/10.1371/journal.pone.0203426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Masoud, V., & Pagès, G. (2017). Targeted therapies in breast cancer: new challenges to fight against resistance. World Journal of Clinical Oncology, 8(2), 120–134. https://doi.org/10.5306/wjco.v8.i2.120.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Yue, W., Wang, J.-P., Li, Y., Fan, P., Liu, G., Zhang, N., Conaway, M., Wang, H., Korach, K. S., Bocchinfuso, W., & Santen, R. (2010). Effects of estrogen on breast cancer development: role of estrogen receptor independent mechanisms HHS public access. International Journal of Cancer, 127(8), 1748–1757. https://doi.org/10.1002/ijc.25207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Pike, S., Zhang, P., Wei, Z., Wu, N., Klinger, A., Chang, S., Jones, R., Carpenter, J., Brown, S. A., DiMuzio, P., Tulenko, T., & Liu, Y. (2015). In vitro effects of tamoxifen on adipose-derived stem cells. Wound Repair and Regeneration, 23(5), 728–736. https://doi.org/10.1111/wrr.12322.

    Article  PubMed  Google Scholar 

  142. Niada, S., Giannasi, C., Ferreira, L. M. J., Milani, A., Arrigoni, E., & Brini, A. T. (2016). 17β-estradiol differently affects osteogenic differentiation of mesenchymal stem/stromal cells from adipose tissue and bone marrow. Differentiation, 92(5), 291–297. https://doi.org/10.1016/j.diff.2016.04.001.

    Article  CAS  PubMed  Google Scholar 

  143. Fisher, B., Costantino, J. P., Wickerham, D. L., Cecchini, R. S., Cronin, W. M., Robidoux, A., Bevers, T. B., Kavanah, M. T., Atkins, J. N., Margolese, R. G., Runowicz, C. D., James, J. M., Ford, L. G., & Wolmark, N. (2005). Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. Journal of the National Cancer Institute, 97(22), 1652–1662. https://doi.org/10.1093/jnci/dji372.

    Article  CAS  PubMed  Google Scholar 

  144. Kavas, A., Keskin, D., Altunbaş, K., & Tezcaner, A. (2016). Raloxifene−/raloxifene-poly(ethylene glycol) conjugate-loaded microspheres: a novel strategy for drug delivery to bone forming cells. International Journal of Pharmaceutics, 510(1), 168–183. https://doi.org/10.1016/j.ijpharm.2016.06.053.

    Article  CAS  PubMed  Google Scholar 

  145. Ning, M., Zhou, C., Weng, J., Zhang, S., Chen, D., Yang, C., Wang, H., Ren, J., Zhou, L., Jin, C., & Wang, M.-W. (2009). Biological activities of a novel selective oestrogen receptor modulator derived from raloxifene (Y134). British Journal of Pharmacology, 150(1), 19–28. https://doi.org/10.1038/sj.bjp.0706960.

    Article  CAS  Google Scholar 

  146. Ernst, B., & Anderson, K. S. (2015). Immunotherapy for the treatment of breast cancer. Current Oncology Reports. Current Medicine Group LLC, 1, 5. https://doi.org/10.1007/s11912-014-0426-9.

    Article  CAS  Google Scholar 

  147. García-Aranda, M., & Redondo, M. (2019). Immunotherapy: a challenge of breast cancer treatment. Cancers, 11(12). https://doi.org/10.3390/cancers11121822.

  148. Duong, M. N., Cleret, A., Matera, E.-L., Chettab, K., Mathé, D., Valsesia-Wittmann, S., Clémenceau, B., & Dumontet, C. (2015). Adipose cells promote resistance of breast cancer cells to trastuzumab-mediated antibody-dependent cellular cytotoxicity. Breast Cancer Research, 17(1), 57. https://doi.org/10.1186/s13058-015-0569-0.

    Article  CAS  PubMed  Google Scholar 

  149. Daverey, A., Drain, A. P., & Kidambi, S. (2015). Physical intimacy of breast cancer cells with mesenchymal stem cells elicits trastuzumab resistance through Src activation. Scientific Reports, 5(13744). https://doi.org/10.1038/srep13744.

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Acknowledgements

RSC is funded by National Breast Cancer Research Institute, Galway, Ireland. Images were created using Biorender (Academic subscription).

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Authors and Affiliations

  1. Discipline of Surgery, Lambe Institute for Translational Research, National University of Ireland Galway, Galway, Ireland

    Ritihaas Surya Challapalli, Roisin M. Dwyer, Michael J. Kerin & Aoife J. Lowery

  2. University Hospital Galway, Galway, Ireland

    Niall McInerney

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  1. Ritihaas Surya Challapalli
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  2. Roisin M. Dwyer
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Correspondence to Aoife J. Lowery.

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Challapalli, R.S., Dwyer, R.M., McInerney, N. et al. Effect of Breast Cancer and Adjuvant Therapy on Adipose-Derived Stromal Cells: Implications for the Role of ADSCs in Regenerative Strategies for Breast Reconstruction. Stem Cell Rev and Rep 17, 523–538 (2021). https://doi.org/10.1007/s12015-020-10038-1

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