Bioengineered Mesenchymal Stem/Stromal Cells in Anti-Cancer Therapy: Current Trends and Future Prospects
- Gil-Chinchilla, Jesús I. 2
- Zapata, Agustín G. 1
- Moraleda, Jose M. 23
- García-Bernal, David 24
- 1 Department of Cell Biology, Complutense University, 28040 Madrid, Spain
- 2 Hematopoietic Transplant and Cellular Therapy Unit, Instituto Murciano de Investigación Biosanitaria (IMIB) Pascual Parrilla, Virgen de la Arrixaca University Hospital, University of Murcia, 30120 Murcia, Spain
- 3 Department of Medicine, University of Murcia, 30120 Murcia, Spain
- 4 Department of Biochemistry, Molecular Biology and Immunology, University of Murcia, 30120 Murcia, Spain
ISSN: 2218-273X
Year of publication: 2024
Volume: 14
Issue: 7
Pages: 734
Type: Article
More publications in: Biomolecules
Abstract
Mesenchymal stem/stromal cells (MSCs) are one of the most widely used cell types inadvanced therapies due to their therapeutic potential in the regulation of tissue repair and homeostasis, and immune modulation. However, their use in cancer therapy is controversial: they caninhibit cancer cell proliferation, but also potentially promote tumour growth by supporting angiogenesis, modulation of the immune milieu and increasing cancer stem cell invasiveness. Thisopposite behaviour highlights the need for careful and nuanced use of MSCs in cancer treatment.To optimize their anti-cancer effects, diverse strategies have bioengineered MSCs to enhance theirtumour targeting and therapeutic properties or to deliver anti-cancer drugs. In this review, wehighlight the advanced uses of MSCs in cancer therapy, particularly as carriers of targeted treatmentsdue to their natural tumour-homing capabilities. We also discuss the potential of MSC-derivedextracellular vesicles to improve the efficiency of drug or molecule delivery to cancer cells. Ongoingclinical trials are evaluating the therapeutic potential of these cells and setting the stage for futureadvances in MSC-based cancer treatment. It is critical to identify the broad and potent applications ofbioengineered MSCs in solid tumour targeting and anti-cancer agent delivery to position them aseffective therapeutics in the evolving field of cancer therapy
Funding information
Funders
-
Instituto de Salud Carlos III
- RD21/0017/0010
- RD21/0017/0001
- ERDF-Next Generation EU “Plan de Recuperación, Transformación y Resiliencia”
- ERDF-Next Generation EU “Plan de Recuperación, Transformación y Resiliencia”
Bibliographic References
- Pittenger, (1999), Science, 284, pp. 143, 10.1126/science.284.5411.143
- Uccelli, (2008), Nat. Rev. Immunol., 8, pp. 726, 10.1038/nri2395
- Friedenstein, (1970), Cell Tissue Kinet., 3, pp. 393
- Mattar, (2015), Front. Immunol., 6, pp. 560, 10.3389/fimmu.2015.00560
- Puissant, (2005), Br. J. Haematol., 129, pp. 118, 10.1111/j.1365-2141.2005.05409.x
- Bueno, (2011), Int. Endod. J., 44, pp. 800, 10.1111/j.1365-2591.2011.01877.x
- Stappenbeck, (2009), Science, 324, pp. 1666, 10.1126/science.1172687
- Oviedo, (2010), Exp. Cell Res., 316, pp. 3109, 10.1016/j.yexcr.2010.08.008
- Salgado, (2010), Curr. Stem Cell Res. Ther., 5, pp. 103, 10.2174/157488810791268564
- Tian, R., Su, S., Yu, Y., Liang, S., Ma, C., Jiao, Y., Xing, W., Tian, Z., Jiang, T., and Wang, J. (2024). Revolutionizing osteoarthritis treatment: How mesenchymal stem cells hold the key. Biomed. Pharmacother., 173.
- Rasmusson, (2004), Lancet, 363, pp. 1439, 10.1016/S0140-6736(04)16104-7
- Vincent, (2024), Physiol. Rev., 104, pp. 659, 10.1152/physrev.00009.2023
- Zhu, (2009), Leukemia, 23, pp. 925, 10.1038/leu.2008.384
- Qiao, (2008), Cell Res., 18, pp. 500, 10.1038/cr.2008.40
- Otsu, (2009), Blood, 113, pp. 4197, 10.1182/blood-2008-09-176198
- Francois, (2019), Stem Cells Transl. Med., 8, pp. 285, 10.1002/sctm.18-0117
- Huang, (2013), Cancer Gene Ther., 20, pp. 308, 10.1038/cgt.2013.22
- Beckermann, (2008), Br. J. Cancer, 99, pp. 622, 10.1038/sj.bjc.6604508
- Poggi, (2018), Front. Immunol., 9, pp. 262, 10.3389/fimmu.2018.00262
- Karnoub, (2007), Nature, 449, pp. 557, 10.1038/nature06188
- Luo, (2014), Oncogene, 33, pp. 2768, 10.1038/onc.2013.233
- Slama, Y., Ah-Pine, F., Khettab, M., Arcambal, A., Begue, M., Dutheil, F., and Gasque, P. (2023). The Dual Role of Mesenchymal Stem Cells in Cancer Pathophysiology: Pro-Tumorigenic Effects versus Therapeutic Potential. Int. J. Mol. Sci., 24.
- Papait, A., Stefani, F.R., Cargnoni, A., Magatti, M., Parolini, O., and Silini, A.R. (2020). The Multifaceted Roles of MSCs in the Tumor Microenvironment: Interactions With Immune Cells and Exploitation for Therapy. Front. Cell Dev. Biol., 8.
- Ridge, (2017), Mol. Cancer, 16, pp. 31, 10.1186/s12943-017-0597-8
- Kidd, (2009), Stem Cells, 27, pp. 2614, 10.1002/stem.187
- Quante, (2011), Cancer Cell, 19, pp. 257, 10.1016/j.ccr.2011.01.020
- Taheri, (2024), Med. Res. Rev., 44, pp. 1596, 10.1002/med.22023
- Taeb, S., Rostamzadeh, D., Amini, S.M., Rahmati, M., Golshekan, M., Abedinzadeh, M., Ahmadi, E., Neha, S., and Najafi, M. (2024). Revolutionizing Cancer Treatment: Harnessing the Power of Mesenchymal Stem Cells for Precise Targeted Therapy in the Tumor Microenvironment. Curr. Top. Med. Chem.
- Han, (2022), Signal Transduct. Target. Ther., 7, pp. 92, 10.1038/s41392-022-00932-0
- Chen, (2019), Nat. Reviews. Drug Discov., 18, pp. 99, 10.1038/s41573-018-0004-1
- Ma, (2015), Cell Transplant., 24, pp. 2585, 10.3727/096368915X687462
- Xie, (2017), Stem Cells Transl. Med., 6, pp. 1120, 10.1002/sctm.16-0204
- Smith, (2015), Stem Cells Transl. Med., 4, pp. 239, 10.5966/sctm.2014-0149
- Rattigan, (2010), Exp. Cell Res., 316, pp. 3417, 10.1016/j.yexcr.2010.07.002
- Ringe, (2007), J. Cell. Biochem., 101, pp. 135, 10.1002/jcb.21172
- Schar, (2015), Clin. Orthop. Relat. Res., 473, pp. 1635, 10.1007/s11999-015-4192-2
- Kalimuthu, (2017), Stem Cells Int., 2017, pp. 8085637, 10.1155/2017/8085637
- Kidd, S., Spaeth, E., Watson, K., Burks, J., Lu, H., Klopp, A., Andreeff, M., and Marini, F.C. (2012). Origins of the tumor microenvironment: Quantitative assessment of adipose-derived and bone marrow-derived stroma. PLoS ONE, 7.
- Housman, (2014), Cancers, 6, pp. 1769, 10.3390/cancers6031769
- Christodoulou, (2018), Stem Cell Res. Ther., 9, pp. 336, 10.1186/s13287-018-1078-8
- Kraitchman, (2005), Circulation, 112, pp. 1451, 10.1161/CIRCULATIONAHA.105.537480
- Barbash, (2003), Circulation, 108, pp. 863, 10.1161/01.CIR.0000084828.50310.6A
- Kean, (2013), Stem Cells Int., 2013, pp. 732742, 10.1155/2013/732742
- Garcia-Bernal, D., Garcia-Arranz, M., Yanez, R.M., Hervas-Salcedo, R., Cortes, A., Fernandez-Garcia, M., Hernando-Rodriguez, M., Quintana-Bustamante, O., Bueren, J.A., and Garcia-Olmo, D. (2021). The Current Status of Mesenchymal Stromal Cells: Controversies, Unresolved Issues and Some Promising Solutions to Improve Their Therapeutic Efficacy. Front. Cell Dev. Biol., 9.
- Bai, (2017), J. Cell. Mol. Med., 21, pp. 2077, 10.1111/jcmm.13131
- Lazennec, (2016), Biochim. Biophys. Acta, 1866, pp. 290
- Li, (2019), J. Neuropathol. Exp. Neurol., 78, pp. 315, 10.1093/jnen/nlz016
- Magne, (2020), J. Investig. Dermatol., 140, pp. 688, 10.1016/j.jid.2019.07.721
- Tsai, (2011), Stroke, 42, pp. 2932, 10.1161/STROKEAHA.110.612788
- Yu, (2011), Mol. Med. Rep., 4, pp. 31
- Najafi, (2013), Expert Opin. Biol. Ther., 13, pp. 959, 10.1517/14712598.2013.782390
- Zheng, (2019), Gastroenterol. Rep., 7, pp. 127, 10.1093/gastro/goy017
- Shao, (2019), Biomed. Pharmacother., 109, pp. 1233, 10.1016/j.biopha.2018.10.108
- Kumar, (2007), FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol., 21, pp. 3917
- Levy, (2013), Blood, 122, pp. e23, 10.1182/blood-2013-04-495119
- Bueren, (2023), Front. Immunol., 14, pp. 1062086, 10.3389/fimmu.2023.1062086
- Sackstein, (2008), Nat. Med., 14, pp. 181, 10.1038/nm1703
- Blanquer, (2022), NPJ Regen. Med., 7, pp. 61, 10.1038/s41536-022-00258-z
- Garcia-Bernal, D., Garcia-Arranz, M., Garcia-Guillen, A.I., Garcia-Hernandez, A.M., Blanquer, M., Garcia-Olmo, D., Sackstein, R., Moraleda, J.M., and Zapata, A.G. (2020). Exofucosylation of Adipose Mesenchymal Stromal Cells Alters Their Secretome Profile. Front. Cell Dev. Biol., 8.
- Sarkar, (2008), Bioconjugate Chem., 19, pp. 2105, 10.1021/bc800345q
- Cheng, (2012), Biomaterials, 33, pp. 5004, 10.1016/j.biomaterials.2012.03.065
- Lo, (2013), Biomaterials, 34, pp. 8213, 10.1016/j.biomaterials.2013.07.033
- Won, (2014), Biomaterials, 35, pp. 5627, 10.1016/j.biomaterials.2014.03.070
- Abels, (2016), Cell. Mol. Neurobiol., 36, pp. 301, 10.1007/s10571-016-0366-z
- Bui, (2018), Tissue Barriers, 6, pp. e1431038, 10.1080/21688370.2018.1431038
- Mendt, (2019), Bone Marrow Transplant., 54, pp. 789, 10.1038/s41409-019-0616-z
- Parolini, (2009), J. Biol. Chem., 284, pp. 34211, 10.1074/jbc.M109.041152
- Zhu, (2012), Cancer Lett., 315, pp. 28, 10.1016/j.canlet.2011.10.002
- Weng, (2021), J. Hematol. Oncol., 14, pp. 136, 10.1186/s13045-021-01141-y
- Dong, (2018), Cell Death Dis., 9, pp. 218, 10.1038/s41419-018-0323-5
- Ren, (2019), J. Exp. Clin. Cancer Res. CR, 38, pp. 62, 10.1186/s13046-019-1027-0
- Casson, (2018), J. Tissue Eng., 9, pp. 2041731418810093, 10.1177/2041731418810093
- Ji, (2015), Cell Cycle, 14, pp. 2473, 10.1080/15384101.2015.1005530
- Ono, (2014), Sci. Signal., 7, pp. ra63, 10.1126/scisignal.2005231
- Wu, S., Ju, G.Q., Du, T., Zhu, Y.J., and Liu, G.H. (2013). Microvesicles derived from human umbilical cord Wharton’s jelly mesenchymal stem cells attenuate bladder tumor cell growth in vitro and in vivo. PLoS ONE, 8.
- Zhang, (2020), Cancer Lett., 490, pp. 54, 10.1016/j.canlet.2020.07.008
- Pakravan, (2017), Cell. Oncol., 40, pp. 457, 10.1007/s13402-017-0335-7
- Herrmann, (2021), Nat. Nanotechnol., 16, pp. 748, 10.1038/s41565-021-00931-2
- Walker, (2019), Theranostics, 9, pp. 8001, 10.7150/thno.37097
- Haney, (2019), Adv. Healthc. Mater., 8, pp. e1801271, 10.1002/adhm.201801271
- Fuhrmann, (2015), J. Control. Release Off. J. Control. Release Soc., 205, pp. 35, 10.1016/j.jconrel.2014.11.029
- Cho, (2013), Materials, 6, pp. 3294, 10.3390/ma6083294
- Cocce, (2017), Sci. Rep., 7, pp. 9376, 10.1038/s41598-017-09175-4
- Abas, B.I., Demirbolat, G.M., and Cevik, O. (2022). Wharton jelly-derived mesenchymal stem cell exosomes induce apoptosis and suppress EMT signaling in cervical cancer cells as an effective drug carrier system of paclitaxel. PLoS ONE, 17.
- Hamilton, (2022), Expert Opin. Biol. Ther., 22, pp. 67, 10.1080/14712598.2021.1954156
- Song, (2023), Front. Oncol., 13, pp. 1299384, 10.3389/fonc.2023.1299384
- Munoz, (2013), Mol. Ther. Nucleic Acids, 2, pp. e126, 10.1038/mtna.2013.60
- Katakowski, (2013), Cancer Lett., 335, pp. 201, 10.1016/j.canlet.2013.02.019
- Lee, (2013), Oncotarget, 4, pp. 346, 10.18632/oncotarget.868
- Lou, (2015), J. Hematol. Oncol., 8, pp. 122, 10.1186/s13045-015-0220-7
- Lang, (2018), Neuro-oncology, 20, pp. 380, 10.1093/neuonc/nox152
- Roccaro, (2013), J. Clin. Investig., 123, pp. 1542, 10.1172/JCI66517
- Yuan, (2017), J. Extracell. Vesicles, 6, pp. 1265291, 10.1080/20013078.2017.1265291
- Ye, (2018), ACS Appl. Mater. Interfaces, 10, pp. 12341, 10.1021/acsami.7b18135
- Bagheri, (2020), Life Sci., 261, pp. 118369, 10.1016/j.lfs.2020.118369
- Dembinski, (2013), Cytotherapy, 15, pp. 20, 10.1016/j.jcyt.2012.10.003
- Zischek, (2009), Ann. Surg., 250, pp. 747, 10.1097/SLA.0b013e3181bd62d0
- Shams, F., Pourjabbar, B., Hashemi, N., Farahmandian, N., Golchin, A., Nuoroozi, G., and Rahimpour, A. (2023). Current progress in engineered and nano-engineered mesenchymal stem cells for cancer: From mechanisms to therapy. Biomed. Pharmacother., 167.
- Bonomi, (2017), Hematol. Oncol., 35, pp. 693, 10.1002/hon.2306
- Pessina, A., Bonomi, A., Cocce, V., Invernici, G., Navone, S., Cavicchini, L., Sisto, F., Ferrari, M., Vigano, L., and Locatelli, A. (2011). Mesenchymal stromal cells primed with paclitaxel provide a new approach for cancer therapy. PLoS ONE, 6.
- Babajani, A., Soltani, P., Jamshidi, E., Farjoo, M.H., and Niknejad, H. (2020). Recent Advances on Drug-Loaded Mesenchymal Stem Cells With Anti-neoplastic Agents for Targeted Treatment of Cancer. Front. Bioeng. Biotechnol., 8.
- Taeb, (2024), Curr. Mol. Med., 24, pp. 98, 10.2174/1566524023666221226143814
- Alemany, (2010), Cancer Gene Ther., 17, pp. 476, 10.1038/cgt.2010.4
- Hmadcha, A., Martin-Montalvo, A., Gauthier, B.R., Soria, B., and Capilla-Gonzalez, V. (2020). Therapeutic Potential of Mesenchymal Stem Cells for Cancer Therapy. Front. Bioeng. Biotechnol., 8.
- Lan, (2021), J. Hematol. Oncol., 14, pp. 195, 10.1186/s13045-021-01208-w
- Zhao, (2017), Sci. Rep., 7, pp. 44758, 10.1038/srep44758
- Petrella, (2017), Biomed. Pharmacother., 87, pp. 755, 10.1016/j.biopha.2017.01.118
- Clavreul, (2017), J. Exp. Clin. Cancer Res. CR, 36, pp. 135, 10.1186/s13046-017-0605-2
- Rimoldi, (2018), Biomed. Pharmacother., 108, pp. 111, 10.1016/j.biopha.2018.09.040
- Pacioni, (2017), Stem Cell Res. Ther., 8, pp. 53, 10.1186/s13287-017-0516-3
- Brini, (2016), Expert Opin. Drug Deliv., 13, pp. 789, 10.1517/17425247.2016.1167037
- Hung, (2015), Cancer Lett., 359, pp. 233, 10.1016/j.canlet.2015.01.017
- Bosco, D.B., Kenworthy, R., Zorio, D.A., and Sang, Q.X. (2015). Human mesenchymal stem cells are resistant to Paclitaxel by adopting a non-proliferative fibroblastic state. PLoS ONE, 10.
- Wang, (2019), Acta Pharm. Sin. B, 9, pp. 167, 10.1016/j.apsb.2018.08.006
- Kalimuthu, (2018), Front. Pharmacol., 9, pp. 1116, 10.3389/fphar.2018.01116
- Vizoso, F.J., Eiro, N., Cid, S., Schneider, J., and Perez-Fernandez, R. (2017). Mesenchymal Stem Cell Secretome: Toward Cell-Free Therapeutic Strategies in Regenerative Medicine. Int. J. Mol. Sci., 18.
- Bonomi, (2015), Cytotherapy, 17, pp. 1687, 10.1016/j.jcyt.2015.09.005
- Pessina, (2013), Br. J. Haematol., 160, pp. 766, 10.1111/bjh.12196
- Golinelli, (2020), Front. Pharmacol., 11, pp. 529921, 10.3389/fphar.2020.529921
- Studeny, (2002), Cancer Res., 62, pp. 3603
- Mueller, (2011), Cancer Gene Ther., 18, pp. 229, 10.1038/cgt.2010.68
- Nakamura, (2004), Gene Ther., 11, pp. 1155, 10.1038/sj.gt.3302276
- Chen, (2008), Mol. Ther. J. Am. Soc. Gene Ther., 16, pp. 749, 10.1038/mt.2008.3
- Ryu, (2011), Hum. Gene Ther., 22, pp. 733, 10.1089/hum.2010.187
- Jing, (2014), Mol. Cancer Ther., 13, pp. 2127, 10.1158/1535-7163.MCT-14-0175
- Sun, (2014), Int. J. Mol. Sci., 15, pp. 3729, 10.3390/ijms15033729
- Tang, (2014), Anticancer Res., 34, pp. 729
- Ren, (2008), Stem Cells, 26, pp. 2332, 10.1634/stemcells.2008-0084
- Li, (2006), Hematol. Oncol., 24, pp. 151, 10.1002/hon.779
- Zhao, (2020), J. Cancer, 11, pp. 5345, 10.7150/jca.38062
- Kim, (2015), Stem Cells Dev., 24, pp. 2808, 10.1089/scd.2015.0103
- Takayama, (2021), Expert Opin. Drug Deliv., 18, pp. 1627, 10.1080/17425247.2021.1960309
- Kim, (2014), Stem Cells Transl. Med., 3, pp. 172, 10.5966/sctm.2013-0132
- Yan, (2013), Mol. Pharm., 10, pp. 142, 10.1021/mp300261e
- Yang, P.M., Hsieh, Y.Y., Du, J.L., Yen, S.C., and Hung, C.F. (2020). Sequential Interferon beta-Cisplatin Treatment Enhances the Surface Exposure of Calreticulin in Cancer Cells via an Interferon Regulatory Factor 1-Dependent Manner. Biomolecules, 10.
- Yang, (2014), Cancer Cell, 25, pp. 37, 10.1016/j.ccr.2013.12.004
- Xu, (2015), Oncol. Rep., 34, pp. 1915, 10.3892/or.2015.4174
- Mirlekar, B., and Pylayeva-Gupta, Y. (2021). IL-12 Family Cytokines in Cancer and Immunotherapy. Cancers, 13.
- Gao, (2010), Cancer Lett., 290, pp. 157, 10.1016/j.canlet.2009.08.031
- Chen, (2018), Cell Cycle, 17, pp. 858, 10.1080/15384101.2018.1442624
- Musso, (2014), Haematologica, 99, pp. 131, 10.3324/haematol.2013.097311
- Kanehira, (2007), Cancer Gene Ther., 14, pp. 894, 10.1038/sj.cgt.7701079
- Choi, (2015), Mol. Ther. J. Am. Soc. Gene Ther., 23, pp. 235, 10.1038/mt.2014.214
- Mangraviti, (2016), Biomaterials, 100, pp. 53, 10.1016/j.biomaterials.2016.05.025
- Guo, (2016), Oncotarget, 7, pp. 55529, 10.18632/oncotarget.10835
- Guo, (2016), Oncol. Lett., 11, pp. 2733, 10.3892/ol.2016.4297
- Asija, (2023), Front. Immunol., 14, pp. 1118246, 10.3389/fimmu.2023.1118246
- Zheng, (2019), Mol. Ther. Oncolytics, 15, pp. 234, 10.1016/j.omto.2019.10.007
- Hemminki, (2020), J. Hematol. Oncol., 13, pp. 84, 10.1186/s13045-020-00922-1
- Moreno, (2021), J. Immunother. Cancer, 9, pp. e001684, 10.1136/jitc-2020-001684
- Kaufman, (2015), Nat. Rev. Drug Discov., 14, pp. 642, 10.1038/nrd4663
- Reale, A., Calistri, A., and Altomonte, J. (2021). Giving Oncolytic Viruses a Free Ride: Carrier Cells for Oncolytic Virotherapy. Pharmaceutics, 13.
- Hadrys, (2020), Eur. J. Pharmacol., 874, pp. 172991, 10.1016/j.ejphar.2020.172991
- Ruano, (2020), Mol. Ther. J. Am. Soc. Gene Ther., 28, pp. 1033, 10.1016/j.ymthe.2020.01.019
- Chulpanova, (2018), Front. Pharmacol., 9, pp. 259, 10.3389/fphar.2018.00259
- Liang, W., Chen, X., Zhang, S., Fang, J., Chen, M., and Xu, Y. (2021). Mesenchymal stem cells as a double-edged sword in tumor growth: Focusing on MSC-derived cytokines. Cell Mol. Biol. Lett., 26.
- Gambera, (2018), Cancer Immunol. Immunother. CII, 67, pp. 1589, 10.1007/s00262-018-2220-2
- Gambera, (2021), J. Immunother. Cancer, 9, pp. e001703, 10.1136/jitc-2020-001703
- Rincon, (2017), Oncotarget, 8, pp. 45415, 10.18632/oncotarget.17557
- Hoyos, (2015), Mol. Ther. J. Am. Soc. Gene Ther., 23, pp. 1497, 10.1038/mt.2015.110
- Moreno, (2017), Stem Cells Int., 2017, pp. 3615729, 10.1155/2017/3615729
- Moreno, (2019), Mol. Cancer Ther., 18, pp. 127, 10.1158/1535-7163.MCT-18-0431
- Barlabe, (2020), Cancer Gene Ther., 27, pp. 383, 10.1038/s41417-019-0110-1
- He, (2015), Mol. Ther. J. Am. Soc. Gene Ther., 23, pp. 108, 10.1038/mt.2014.204
- Cejalvo, (2018), Cancer Res., 78, pp. 4891, 10.1158/0008-5472.CAN-17-3754
- Delgado-Bonet, P., Tomeo-Martin, B.D., Ortiz-Diez, G., and Perise-Barrios, A.J. (2022). Tumor-Homing of Mesenchymal Stem Cells Infected with Oncolytic Virus in a Canine Patient. Vet. Sci., 9.
- Hsiao, (2012), Mol. Pharm., 9, pp. 1396, 10.1021/mp200649g
- Na, (2019), J. Control. Release Off. J. Control. Release Soc., 305, pp. 75, 10.1016/j.jconrel.2019.04.040
- Nilson, R., Krutzke, L., Wienen, F., Rojewski, M., Zeplin, P.H., Funk, W., Schrezenmeier, H., Kochanek, S., and Kritzinger, A. (2023). Evaluation of Human Mesenchymal Stromal Cells as Carriers for the Delivery of Oncolytic HAdV-5 to Head and Neck Squamous Cell Carcinomas. Viruses, 15.
- Wang, P., Zhang, J., Zhang, Q., and Liu, F. (2023). Mesenchymal stem cells loaded with Ad5-Ki67/IL-15 enhance oncolytic adenovirotherapy in experimental glioblastoma. Biomed. Pharmacother., 157.
- Hakkarainen, (2007), Hum. Gene Ther., 18, pp. 627, 10.1089/hum.2007.034
- Yuan, (2016), Cancer Lett., 381, pp. 85, 10.1016/j.canlet.2016.07.019
- Hammer, (2015), Int. J. Cancer, 137, pp. 978, 10.1002/ijc.29442
- Komarova, (2006), Mol. Cancer Ther., 5, pp. 755, 10.1158/1535-7163.MCT-05-0334
- Kaczorowski, (2016), Oncotarget, 7, pp. 9046, 10.18632/oncotarget.7031
- Li, (2016), Oncotarget, 7, pp. 51815, 10.18632/oncotarget.10122
- Yoon, (2019), Cancer Res., 79, pp. 4503, 10.1158/0008-5472.CAN-18-3900
- Mahasa, (2020), Sci. Rep., 10, pp. 425, 10.1038/s41598-019-57240-x
- Muhammad, (2019), Stem Cell Res. Ther., 10, pp. 190, 10.1186/s13287-019-1268-z
- Rivera, (2007), Breast Cancer Res. Treat., 105, pp. 157, 10.1007/s10549-006-9449-8
- Ho, C.T., Wu, M.H., Chen, M.J., Lin, S.P., Yen, Y.T., and Hung, S.C. (2021). Combination of Mesenchymal Stem Cell-Delivered Oncolytic Virus with Prodrug Activation Increases Efficacy and Safety of Colorectal Cancer Therapy. Biomedicines, 9.
- Guo, (2019), Stem Cells Dev., 28, pp. 882, 10.1089/scd.2018.0222
- Bolontrade, (2012), Stem Cells Dev., 21, pp. 2689, 10.1089/scd.2011.0643
- Sonabend, (2008), Stem Cells, 26, pp. 831, 10.1634/stemcells.2007-0758
- Ahmed, (2010), Mol. Ther. J. Am. Soc. Gene Ther., 18, pp. 1846, 10.1038/mt.2010.131
- Zhang, (2022), Mol. Ther. Oncolytics, 24, pp. 486, 10.1016/j.omto.2022.01.007
- Dembinski, (2010), Cancer Gene Ther., 17, pp. 289, 10.1038/cgt.2009.67
- Yong, (2009), Cancer Res., 69, pp. 8932, 10.1158/0008-5472.CAN-08-3873
- Shinojima, (2013), Cancer Res., 73, pp. 2333, 10.1158/0008-5472.CAN-12-3086
- Shimizu, (2022), J. Neurosurg., 136, pp. 757, 10.3171/2021.3.JNS203045
- Zhang, (2021), Cancer Lett., 509, pp. 26, 10.1016/j.canlet.2021.03.027
- He, (2023), J. Transl. Med., 21, pp. 688, 10.1186/s12967-023-04539-z
- Du, (2017), Proc. Natl. Acad. Sci. USA, 114, pp. E6157, 10.1073/pnas.1700363114
- Leoni, (2015), Oncotarget, 6, pp. 34774, 10.18632/oncotarget.5793
- Nguyen, D.H., Herrmann, T., Hartl, B., Draganov, D., Minev, I., Neuharth, F., Gomez, A., Alamillo, A., Schneider, L.E., and Kleinholz, D. (2022). Development of Allogeneic Stem Cell-Based Platform for Delivery and Potentiation of Oncolytic Virotherapy. Cancers, 14.
- Petrov, I., Gentschev, I., Vyalkova, A., Elashry, M.I., Klymiuk, M.C., Arnhold, S., and Szalay, A.A. (2020). Canine Adipose-Derived Mesenchymal Stem Cells (cAdMSCs) as a “Trojan Horse” in Vaccinia Virus Mediated Oncolytic Therapy against Canine Soft Tissue Sarcomas. Viruses, 12.
- Draganov, (2019), J. Transl. Med., 17, pp. 100, 10.1186/s12967-019-1829-z
- Sochanik, (2020), Mol. Ther. Oncolytics, 18, pp. 335, 10.1016/j.omto.2020.07.003
- Jazowiecka-Rakus, J., Hadrys, A., Rahman, M.M., McFadden, G., Fidyk, W., Chmielik, E., Pazdzior, M., Grajek, M., Kozik, V., and Sochanik, A. (2021). Myxoma Virus Expressing LIGHT (TNFSF14) Pre-Loaded into Adipose-Derived Mesenchymal Stem Cells Is Effective Treatment for Murine Pancreatic Adenocarcinoma. Cancers, 13.
- Jazowiecka-Rakus, J., Sochanik, A., Hadrys, A., Fidyk, W., Chmielik, E., Rahman, M.M., and McFadden, G. (2022). Combination of LIGHT (TNFSF14)-Armed Myxoma Virus Pre-Loaded into ADSCs and Gemcitabine in the Treatment of Experimental Orthotopic Murine Pancreatic Adenocarcinoma. Cancers, 14.
- Josiah, (2010), Mol. Ther. J. Am. Soc. Gene Ther., 18, pp. 377, 10.1038/mt.2009.265
- Mader, (2009), Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res., 15, pp. 7246, 10.1158/1078-0432.CCR-09-1292
- Mader, (2013), J. Transl. Med., 11, pp. 20, 10.1186/1479-5876-11-20
- Ong, (2013), J. Hepatol., 59, pp. 999, 10.1016/j.jhep.2013.07.010
- Castleton, (2014), Blood, 123, pp. 1327, 10.1182/blood-2013-09-528851
- Dorostkar, (2023), Infect. Agents Cancer, 18, pp. 46, 10.1186/s13027-023-00521-y
- Keshavarz, (2020), Virol. J., 17, pp. 64, 10.1186/s12985-020-01326-w
- Kazimirsky, (2016), Stem Cell Res. Ther., 7, pp. 149, 10.1186/s13287-016-0414-0
- Soleimanjahi, (2021), Cancer Cell Int., 21, pp. 244, 10.1186/s12935-021-01848-5
- Babaei, (2021), Adv. Pharm. Bull., 11, pp. 361
- Babaei, A., Soleimanjahi, H., Soleimani, M., and Arefian, E. (2021). Mesenchymal stem cells loaded with oncolytic reovirus enhances antitumor activity in mice models of colorectal cancer. Biochem. Pharmacol., 190.
- Banijamali, (2021), J. Cell. Biochem., 122, pp. 1360, 10.1002/jcb.29955
- Wang, (2021), Oncol. Lett., 21, pp. 238, 10.3892/ol.2021.12499
- Zarogoulidis, (2013), J. Genet. Syndr. Gene Ther., 4, pp. 16849
- Moolten, (1986), Cancer Res., 46, pp. 5276
- Fillat, (2003), Curr. Gene Ther., 3, pp. 13, 10.2174/1566523033347426
- Zhang, (2015), J. Control. Release Off. J. Control. Release Soc., 209, pp. 260, 10.1016/j.jconrel.2015.05.007
- Leng, (2014), Biomaterials, 35, pp. 5162, 10.1016/j.biomaterials.2014.03.014
- Alieva, M., Bago, J.R., Aguilar, E., Soler-Botija, C., Vila, O.F., Molet, J., Gambhir, S.S., Rubio, N., and Blanco, J. (2012). Glioblastoma therapy with cytotoxic mesenchymal stromal cells optimized by bioluminescence imaging of tumor and therapeutic cell response. PLoS ONE, 7.
- Yang, (2019), Cancer Manag. Res., 11, pp. 8443, 10.2147/CMAR.S209880
- Chang, (2020), Am. J. Cancer Res., 10, pp. 1429
- NguyenThai, (2015), J. Gene Med., 17, pp. 87, 10.1002/jgm.2826
- Nowakowski, (2016), Stem Cells Dev., 25, pp. 1513, 10.1089/scd.2016.0120
- Abrate, (2014), Eur. J. Cancer, 50, pp. 2478, 10.1016/j.ejca.2014.06.014
- Kim, (2023), Am. J. Cancer Res., 13, pp. 2439
- Choi, (2012), Eur. J. Cancer, 48, pp. 129, 10.1016/j.ejca.2011.04.033
- Amara, (2016), J. Control. Release Off. J. Control. Release Soc., 239, pp. 82, 10.1016/j.jconrel.2016.08.019
- Yamamoto, (2003), Cancer Gene Ther., 10, pp. 179, 10.1038/sj.cgt.7700551
- Ryu, (2012), Biochem. Biophys. Res. Commun., 421, pp. 585, 10.1016/j.bbrc.2012.04.050
- Sun, (2022), Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res., 28, pp. 4392, 10.1158/1078-0432.CCR-22-0622
- Duhrsen, (2019), Oncotarget, 10, pp. 6049, 10.18632/oncotarget.27071
- Melen, (2016), Cancer Lett., 371, pp. 161, 10.1016/j.canlet.2015.11.036
- Peter, (2017), Oncotarget, 8, pp. 80156, 10.18632/oncotarget.20964