Mesenchymal stem cells in cancer therapy; the art of harnessing a foe to a friend

Document Type : Review Article

Authors

1 Department of Pathology, School of Medicine, Gonabad University of Medical Sciences, Gonabad, Iran

2 Department of Pathology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

3 Department of Medical Laboratory Sciences, Varastegan Institute for Medical Sciences, Mashhad, Iran

4 Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of ‎Medical Sciences, Mashhad, Iran

5 Department of Medical Laboratory Sciences, Mashhad University of Medical Sciences, Mashhad, Iran

6 Department of Medical Laboratory Sciences, Ilam Institute for Medical Sciences, Ilam, Iran

7 Surgical Oncology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

For a long time, mesenchymal stem cells (MSCs) were discussed only as stem cells which could give rise to different types of cells. However, when it became clear that their presence in the tumor microenvironment (TME) was like a green light for tumorigenesis, they emerged from the ashes. This review was arranged to provide a comprehensive and precise description of MSCs’ role in regulating tumorigenesis and to discuss the dark and the bright sides of cancer treatment strategies using MSCs.
To gather the details about MSCs, we made an intensive literature review using keywords, including MSCs, tumor microenvironment, tumorigenesis, and targeted therapy. Through transferring cytokines, growth factors, and microRNAs, MSCs maintain the cancer stem cell population, increase angiogenesis, provide a facility for cancer metastasis, and shut down the anti-tumor activity of the immune system. Although MSCs progress tumorigenesis, there is a consensus that these cells could be used as a vehicle to transfer anti-cancer agents into the tumor milieu. This feature opened a new chapter in MSCs biology, this time from the therapeutic perspective. Although the data are not sufficient, the advent of new genetic engineering methods might make it possible to engage these cells as Trojan horses to eliminate the malignant population. So many years of investigation showed that MSCs are an important group of cells, residing in the TME, studying the function of which not only could add a delicate series of information to the process of tumorigenesis but also could revolutionize cancer treatment strategies.

Keywords

References

1. Li C, Zhao H, Wang B. Mesenchymal stem/stromal cells: developmental origin, tumorigenesis and translational cancer therapeutics. Trans Oncol 2021; 14:1-10.
2. Lee J-K, Park S-R, Jung B-K, Jeon Y-K, Lee Y-S, Kim M-K, et al. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PloS one 2013; 8:1-11.
3. Huang W, Chang M, Tsai K, Hung M, Chen H, Hung S. Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene 2013; 32:4343-4354.
4. Del Fattore A, Luciano R, Saracino R, Battafarano G, Rizzo C, Pascucci L, et al. Differential effects of extracellular vesicles secreted by mesenchymal stem cells from different sources on glioblastoma cells. Expert opin biol ther 2015; 15:495-504.
5. Bruno S, Collino F, Deregibus MC, Grange C, Tetta C, Camussi G. Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem cell dev 2013; 22:758-771.
6. Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 2011; 71:614-624.
7. Wu X-B, Liu Y, Wang G-H, Xu X, Cai Y, Wang H-Y, et al. Mesenchymal stem cells promote colorectal cancer progression through AMPK/mTOR-mediated NF-κB activation. Sci Rep 2016; 6:1-12.
8. Sun Z, Wang S, Zhao RC. The roles of mesenchymal stem cells in tumor inflammatory microenvironment. J Hematol Oncol 2014; 7:1-10.
9. McLean K, Gong Y, Choi Y, Deng N, Yang K, Bai S, et al. Human ovarian carcinoma–associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production. The J Clin Invest 2011; 121:3206-3219.
10. Coffman LG, Choi Y-J, McLean K, Allen BL, di Magliano MP, Buckanovich RJ. Human carcinoma-associated mesenchymal stem cells promote ovarian cancer chemotherapy resistance via a BMP4/HH signaling loop. Oncotarget 2016; 7:6916-6933.
11. Hossain A, Gumin J, Gao F, Figueroa J, Shinojima N, Takezaki T, et al. Mesenchymal stem cells isolated from human gliomas increase proliferation and maintain stemness of glioma stem cells through the IL‐6/gp130/STAT3 pathway. Stem cells 2015; 33:2400-2415.
12. Shamai Y, Alperovich DC, Yakhini Z, Skorecki K, Tzukerman M. Reciprocal reprogramming of cancer cells and associated mesenchymal stem cells in gastric cancer. Stem cells 2019; 37:176-189.
13. Maleknia M, Valizadeh A, Pezeshki S, Saki N. Immunomodulation in leukemia: cellular aspects of anti-leukemic properties. Clin Trans Oncol 2020; 22:1-10.
14. Arneth B. Tumor microenvironment. Medicina 2020; 56:15-32.
15. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. cell 2011; 144:646-674.
16. Spill F, Reynolds DS, Kamm RD, Zaman MH. Impact of the physical microenvironment on tumor progression and metastasis. Curr Opin Biotechnol 2016; 40:41-48.
17. Del Prete A, Schioppa T, Tiberio L, Stabile H, Sozzani S. Leukocyte trafficking in tumor microenvironment. Curr Opin Pharmacol 2017; 35:40-47.
18. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140:883-899.
19. LeBleu V. Imaging the tumor microenvironment. Cancer J (Sudbury, Mass) 2015; 21:174-191.
20. Korneev KV, Atretkhany K-SN, Drutskaya MS, Grivennikov SI, Kuprash DV, Nedospasov SA. TLR-signaling and proinflammatory cytokines as drivers of tumorigenesis. Cytokine 2017; 89:127-135.
21. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells—what challenges do they pose? Nat Rev Drug Discov 2014; 13:497-512.
22. Liao D, Luo Y, Markowitz D, Xiang R, Reisfeld RA. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PloS one 2009; 4:1-10.
23. Walker C, Mojares E, del Río Hernández A. Role of extracellular matrix in development and cancer progression. Int J Mol Sci 2018; 19:3028-3059.
24. Feig C, Jones JO, Kraman M, Wells RJ, Deonarine A, Chan DS, et al. Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti–PD-L1 immunotherapy in pancreatic cancer. Proc Natl Acad Sci 2013; 110:20212-20217.
25. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7:211-228.
26. Minguell JJ, Erices A, Conget P. Mesenchymal stem cells. Exp Biol Med 2001; 226:507-520.
27. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells. Nat Rev Mol Cell Biol 2011; 12:126-131.
28. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9:641-650.
29. Friedenstein AJ. Precursor cells of mechanocytes. Int Rev Cyt 1976; 47:327-359.
30. Friedenstein A, Chailakhjan R, Lalykina K. The development of fibroblast colonies in monolayer cultures of guinea‐pig bone marrow and spleen cells. Cell Prolif 1970; 3:393-403.
31. Murphy MB, Moncivais K, Caplan AI. Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp Mol Med 2013; 45:1-16.
32. Dazzi F, Ramasamy R, Glennie S, Jones SP, Roberts I. The role of mesenchymal stem cells in haemopoiesis. Blood Rev 2006; 20:161-171.
33. Miana VV, González EAP. Adipose tissue stem cells in regenerative medicine. Ecancermedicalscience 2018; 12:1-14.
34. Leuning DG, Beijer NR, Du Fossé NA, Vermeulen S, Lievers E, Van Kooten C, et al. The cytokine secretion profile of mesenchymal stromal cells is determined by surface structure of the microenvironment. Sci Rep 2018; 8:1-9.
35. Klingemann H, Matzilevich D, Marchand J. Mesenchymal stem cells–sources and clinical applications. Transfus Med Hemother 2008; 35:272-277.
36. Hwang NS, Zhang C, Hwang YS, Varghese S. Mesenchymal stem cell differentiation and roles in regenerative medicine. Wiley Interdiscip Rev Syst Biol Medicine 2009; 1:97-106.
37. Wang Y, Chen X, Cao W, Shi Y. Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat immunol 2014; 15:1009-1016.
38. Fitzsimmons RE, Mazurek MS, Soos A, Simmons CA. Mesenchymal stromal/stem cells in regenerative medicine and tissue engineering. Stem Cells Int 2018; 19:1-16.
39. DiMarino AM, Caplan AI, Bonfield TL. Mesenchymal stem cells in tissue repair. Front Immunol 2013; 4:201-210.
40. Werts E, DeGowin R, Knapp S, Gibson D. Characterization of marrow stromal (fibroblastoid) cells and their association with erythropoiesis. Exp hematol 1980; 8:423-433.
41. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, Benayahu D, et al. Single‐colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997; 12:1335-1347.
42. Colter DC, Sekiya I, Prockop DJ. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci 2001; 98:7841-7845.
43. Han Z, Du W, Han Z, Liang L. New insights into the heterogeneity and functional diversity of human mesenchymal stem cells. Biomed Mater Eng 2017; 28:29-45.
44. Timaner M, Tsai KK, Shaked Y, editors. The multifaceted role of mesenchymal stem cells in cancer. Semin Cancer Biol 2020; 60:225-237.
45. Waterman RS, Tomchuck SL, Henkle SL, Betancourt AM. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. PloS one 2010; 5:1-14.
46. Waterman RS, Henkle SL, Betancourt AM. Mesenchymal stem cell 1 (MSC1)-based therapy attenuates tumor growth whereas MSC2-treatment promotes tumor growth and metastasis. PloS one 2012; 7:1-11.
47. Qiao L, Xu Z-l, Zhao T-j, Ye L-h, Zhang X-d. Dkk-1 secreted by mesenchymal stem cells inhibits growth of breast cancer cells via depression of Wnt signalling. Cancer lett 2008; 269:67-77.
48. Dasari VR, Kaur K, Velpula KK, Gujrati M, Fassett D, Klopfenstein JD, et al. Upregulation of PTEN in glioma cells by cord blood mesenchymal stem cells inhibits migration via downregulation of the PI3K/Akt pathway. PloS one 2010; 5:1-12.
49. Dvorak HF. Tumors: wounds that do not heal. N Eng J Med 1986; 315:1650-1659.
50. De Becker A, Van Riet I. Homing and migration of mesenchymal stromal cells: how to improve the efficacy of cell therapy? World J Stem Cells 2016; 8:73-89.
51. Ponte AL, Marais E, Gallay N, Langonné A, Delorme B, Hérault O, et al. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 2007; 25:1737-1745.
52. Schmidt A, Ladage D, Schinköthe T, Klausmann U, Ulrichs C, Klinz FJ, et al. Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem cells 2006; 24:1750-1758.
53. Li L, Madu CO, Lu A, Lu Y. HIF-1α promotes a hypoxia-independent cell migration. Open Biol J 2010; 3:8-22.
54. Dwyer R, Potter-Beirne S, Harrington K, Lowery A, Hennessy E, Murphy J, et al. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 2007; 13:5020-5027.
55. Chen M-S, Lin C-Y, Chiu Y-H, Chen C-P, Tsai P-J, Wang H-S. IL-1β-induced matrix metalloprotease-1 promotes mesenchymal stem cell migration via PAR1 and G-protein-coupled signaling pathway. Stem Cells intl 2018; 5:1-11.
56. Dubon MJ, Yu J, Choi S, Park KS. Transforming growth factor β induces bone marrow mesenchymal stem cell migration via noncanonical signals and N‐cadherin. J Cell physiol 2018; 233:201-213.
57. Lourenco S, Teixeira VH, Kalber T, Jose RJ, Floto RA, Janes SM. Macrophage migration inhibitory factor–CXCR4 is the dominant chemotactic axis in human mesenchymal stem cell recruitment to tumors. J Immunol 2015; 194:3463-3474.
58. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nat 2007; 449:557-563.
59. Klopp AH, Spaeth EL, Dembinski JL, Woodward WA, Munshi A, Meyn RE, et al. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer res 2007; 67:11687-11695.
60. Tu B, Peng Z-X, Fan Q-M, Du L, Yan W, Tang T-T. Osteosarcoma cells promote the production of pro-tumor cytokines in mesenchymal stem cells by inhibiting their osteogenic differentiation through the TGF-β/Smad2/3 pathway. Exp Cell res 2014; 320:164-173.
61. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer cell 2011; 19:257-272.
62. Fotia C, Massa A, Boriani F, Baldini N, Granchi D. Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells. Cytotechnology 2015; 67:1073-1084.
63. Atashzar MR, Baharlou R, Karami J, Abdollahi H, Rezaei R, Pourramezan F, et al. Cancer stem cells: a review from origin to therapeutic implications. J Cell Physiol 2020; 235:790-803.
64. Carke M. Cancer stem cells-perspectives on current status and future directions. Cancer Res 2006; 66:9339-9344.
65. Papaccio F, Paino F, Regad T, Papaccio G, Desiderio V, Tirino V. Concise review: cancer cells, cancer stem cells, and mesenchymal stem cells: influence in cancer development. Stem Cells Trans Med 2017; 6:2115-2125.
66. Li H-J, Reinhardt F, Herschman HR, Weinberg RA. Cancer-stimulated mesenchymal stem cells create a carcinoma stem cell niche via prostaglandin E2 signaling. Cancer discov 2012; 2:840-855.
67. Tsai KS, Yang SH, Lei YP, Tsai CC, Chen HW, Hsu CY, et al. Mesenchymal stem cells promote formation of colorectal tumors in mice. Gastroenterology 2011; 141:1046-1056.
68. Timaner M, Letko-Khait N, Kotsofruk R, Benguigui M, Beyar-Katz O, Rachman-Tzemah C, et al. Therapy-educated mesenchymal stem cells enrich for tumor-initiating cells. Cancer res 2018; 78:1253-1265.
69. Cuiffo BG, Campagne A, Bell GW, Lembo A, Orso F, Lien EC, et al. MSC-regulated microRNAs converge on the transcription factor FOXP2 and promote breast cancer metastasis. Cell Stem Cell 2014; 15:762-774.
70. Lazennec G, Lam PY. Recent discoveries concerning the tumor-mesenchymal stem cell interactions. Biochim Biophys Acta Rev Cancer 2016; 1866:290-299.
71. Pinilla S, Alt E, Khalek FA, Jotzu C, Muehlberg F, Beckmann C, et al. Tissue resident stem cells produce CCL5 under the influence of cancer cells and thereby promote breast cancer cell invasion. Cancer lett 2009; 284:80-85
72. Kabashima‐Niibe A, Higuchi H, Takaishi H, Masugi Y, Matsuzaki Y, Mabuchi Y, et al. Mesenchymal stem cells regulate epithelial–mesenchymal transition and tumor progression of pancreatic cancer cells. Cancer sci 2013; 104:157-164.
73. Du WJ, Chi Y, Yang ZX, Li ZJ, Cui JJ, Song BQ, et al. Heterogeneity of proangiogenic features in mesenchymal stem cells derived from bone marrow, adipose tissue, umbilical cord, and placenta. Stem Cell Res Ther 2016; 7:1-11.
74. Feng B, Chen L. Review of mesenchymal stem cells and tumors: executioner or coconspirator? Cancer Biother Radiopharm 2009; 24:717-721.
75. Beckermann B, Kallifatidis G, Groth A, Frommhold D, Apel A, Mattern J, et al. VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer 2008; 99:622-631.
76. Vartanian A, Karshieva S, Dombrovsky V, Belyavsky A. Melanoma educates mesenchymal stromal cells towards vasculogenic mimicry. Oncol lett 2016; 11:4264-4268.
77. Dhar K, Dhar G, Majumder M, Haque I, Mehta S, Van Veldhuizen PJ, et al. Tumor cell-derived PDGF-B potentiates mouse mesenchymal stem cells-pericytes transition and recruitment through an interaction with NRP-1. Mol Cancer 2010; 9:1-12.
78. Brindle NP, Saharinen P, Alitalo K. Signaling and functions of angiopoietin-1 in vascular protection. Circ Res 2006; 98:1014-1023.
79. Li Y, Zheng L, Xu X, Song L, Li Y, Li W, et al. Mesenchymal stem cells modified with angiopoietin-1 gene promote wound healing. Stem Cell Res Ther 2013; 4:1-10.
80. Zacharek A, Chen J, Li A, Cui X, Li Y, Roberts C, et al. Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J Cereb Blood Flow Metab 2007; 27:1684-1691.
81. Kalluri R. The biology and function of fibroblasts in cancer. Nat Rev Cancer 2016; 16:582-599.
82. Gu W, Hong X, Le Bras A, Nowak WN, Bhaloo SI, Deng J, et al. Smooth muscle cells differentiated from mesenchymal stem cells are regulated by microRNAs and suitable for vascular tissue grafts. J Biol Chem 2018; 293:8089-8102.
83. Caplan AI. New MSC: MSCs as pericytes are sentinels and gatekeepers. J Orthop Res 2017; 35:1151-1159.
84. Sarvaiya PJ, Guo D, Ulasov I, Gabikian P, Lesniak MS. Chemokines in tumor progression and metastasis. Oncotarget 2013; 4:2171-2176.
85. Halpern JL, Kilbarger A, Lynch CC. Mesenchymal stem cells promote mammary cancer cell migration in vitro via the CXCR2 receptor. Cancer Lett 2011; 308:91-99.
86. Berger L, Shamai Y, Skorecki KL, Tzukerman M. Tumor specific recruitment and reprogramming of mesenchymal stem cells in tumorigenesis. Stem Cells 2016; 34:1011-1026.
87. McAndrews KM, McGrail DJ, Ravikumar N, Dawson MR. Mesenchymal stem cells induce directional migration of invasive breast cancer cells through TGF-β. Sci rep 2015; 5:1-13.
88. Goulet CR, Pouliot F. TGFβ signaling in the tumor microenvironment tumor microenvironment. Springer 2020;  89-105.
89. Halvorsen EC, Mahmoud SM, Bennewith KL. Emerging roles of regulatory T cells in tumour progression and metastasis. Cancer Metastasis Rev 2014; 33:1025-1041.
90. Asari S, Itakura S, Ferreri K, Liu C-P, Kuroda Y, Kandeel F, et al. Mesenchymal stem cells suppress B-cell terminal differentiation. Exp Hematol 2009; 37:604-615.
91. Rivera-Cruz CM, Shearer JJ, Figueiredo Neto M, Figueiredo ML. The immunomodulatory effects of mesenchymal stem cell polarization within the tumor microenvironment niche. Stem Cells Int 2017; 1-17.
92. Poggi A, Varesano S, Zocchi MR. How to hit mesenchymal stromal cells and make the tumor microenvironment immunostimulant rather than immunosuppressive. Front Immunol 2018; 9:262-279.
93. Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, Miller SD, et al. Human bone marrow‐derived mesenchymal stem cells induce Th2‐polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 2009; 57:1192-1203.
94. Fiorina P, Jurewicz M, Augello A, Vergani A, Dada S, La Rosa S, et al. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol 2009; 183:993-1004.
95. Duffy MM, Ritter T, Ceredig R, Griffin MD. Mesenchymal stem cell effects on T-cell effector pathways. Stem cell Res Ther 2011; 2:1-9.
96. Niu J, Yue W, Le-Le Z, Bin L, Hu X. Mesenchymal stem cells inhibit T cell activation by releasing TGF-β1 from TGF-β1/GARP complex. Oncotarget 2017; 8:99784-99801.
97. Ungerer C, Quade-Lyssy P, Radeke HH, Henschler R, Königs C, Köhl U, et al. Galectin-9 is a suppressor of T and B cells and predicts the immune modulatory potential of mesenchymal stromal cell preparations. Stem Cells dev 2014; 23:755-766.
98. Lee HJ, Ko JH, Jeong HJ, Ko AY, Kim MK, Wee WR, et al. Mesenchymal stem/stromal cells protect against autoimmunity via CCL2-dependent recruitment of myeloid-derived suppressor cells. J Immunol 2015; 194:3634-3645.
99. Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L. MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2. Blood Am J Hematol 2009; 113:6576-6583.
100. Chen B, Ni Y, Liu J, Zhang Y, Yan F. Bone marrow-derived mesenchymal stem cells exert diverse effects on different macrophage subsets. Stem Cells Int 2018; 24:1-9.
101. Mohammadi F, Soltani A, Ghahremanloo A, Javid H, Hashemy SI. The thioredoxin system and cancer therapy: a review. Cancer Chemother Pharmacol 2019; 84:925-935.
102. Javid H, Mohammadi F, Zahiri E, Hashemy SI. The emerging role of substance P/neurokinin-1 receptor signaling pathways in growth and development of tumor cells. J Physiol Biochemi 2019; 75:415-421.
103. Ebrahimi S, Javid H, Alaei A, Hashemy SI. New insight into the role of substance P/neurokinin‐1 receptor system in breast cancer progression and its crosstalk with microRNAs. Clin Genet 2020; 98:322-330.
104. Zhong Z, Virshup DM. Wnt signaling and drug resistance in cancer. Mol pharmacol 2020; 97:72-89.
105. Akbari Dilmaghani N, Safaroghli‐Azar A, Pourbagheri‐Sigaroodi A, Bashash D. The PI3K/Akt/mTORC signaling axis in head and neck squamous cell carcinoma: possibilities for therapeutic interventions either as single agents or in combination with conventional therapies. IUBMB Life 2021;.
106. Xiu M-x, Liu Y-m, Kuang B-h. The oncogenic role of Jagged1/Notch signaling in cancer. Biomed Pharmacother 2020; 129:110416-110427.
107. Hashemy SI. The human thioredoxin system: modifications and clinical applications. Iran J Basic Med Sci 2011; 14:191-204.
108. Ebrahimi S, Hashemy SI. MicroRNA-mediated redox regulation modulates therapy resistance in cancer cells: clinical perspectives. Cell Oncol (Dordr) 2019; 42:131-141.
109. Moitra K. Overcoming multidrug resistance in cancer stem cells. BioMed Res int 2015; 1-8.
110. Steinbichler TB, Dudás J, Skvortsov S, Ganswindt U, Riechelmann H, Skvortsova I-I, et al. Therapy resistance mediated by cancer stem cells. Semin Cancer Biol 2018; 53:156-167.
111. Daverey A, Drain AP, Kidambi S. Physical intimacy of breast cancer cells with mesenchymal stem cells elicits trastuzumab resistance through Src activation. Sci rep 2015; 5:1-13.
112. Teng I-W, Hou P-C, Lee K-D, Chu P-Y, Yeh K-T, Jin VX, et al. Targeted methylation of two tumor suppressor genes is sufficient to transform mesenchymal stem cells into cancer stem/initiating cells. Cancer res 2011; 71:4653-4663.
113. Vianello F, Villanova F, Tisato V, Lymperi S, Ho K-K, Gomes AR, et al. Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis. Haematologica 2010; 95:1081-1090.
114. Balakrishnan K, Burger JA, Quiroga MP, Henneberg M, Ayres ML, Wierda WG, et al. Influence of bone marrow stromal microenvironment on forodesine-induced responses in CLL primary cells. Blood J Am Hematol 2010; 116:1083-1091.
115. Scherzed A, Hackenberg S, Froelich K, Kessler M, Koehler C, Hagen R, et al. BMSC enhance the survival of paclitaxel treated squamous cell carcinoma cells in vitro. Cancer biol Ther 2011; 11:349-357.
116. Lis R, Touboul C, Mirshahi P, Ali F, Mathew S, Nolan DJ, et al. Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int J Cancer 2011; 128:715-725.
117. Dreuw A, Hermanns HM, Heise R, Joussen S, Rodríguez F, Marquardt Y, et al. Interleukin-6-type cytokines upregulate expression of multidrug resistance-associated proteins in NHEK and dermal fibroblasts. J Invest Dermatol 2005; 124:28-37.
118. Roodhart J, Daenen L, Stigter E, Prins H, Gerrits J, Houthuijzen J, et al. Mesenchymal stem cells induce resistance to chemotherapy through the release of platinum-induced fatty acids. Cancer Cell 2011; 20:370-383.
119. Hmadcha A, Martin-Montalvo A, Gauthier BR, Soria B, Capilla-Gonzalez V. Therapeutic potential of mesenchymal stem cells for cancer therapy. Front Bioeng Biotechnol 2020; 8:43-56.
120. Gjorgieva D, Zaidman N, Bosnakovski D. Mesenchymal stem cells for anti-cancer drug delivery. Recent pat Anti-cancer drug discov 2013; 8:310-318.
121. Gao Z, Zhang L, Hu J, Sun Y. Mesenchymal stem cells: a potential targeted-delivery vehicle for anti-cancer drug loaded nanoparticles. Nanomed Nanotechnol Biol Med 2013; 9:174-184.
122. Kerrigan BCP, Shimizu Y, Andreeff M, Lang FF. Mesenchymal stromal cells for the delivery of oncolytic viruses in gliomas. Cytotherapy 2017; 19:445-457.
123. Hombach AA, Geumann U, Günther C, Hermann FG, Abken H. IL7-IL12 engineered mesenchymal stem cells (MSCs) improve a CAR T cell attack against colorectal cancer cells. Cells 2020; 9:873-888.
124. Xie M, Tao L, Zhang Z, Wang W. Mesenchymal stem cells mediated drug delivery in tumor-targeted therapy. Curr Drug deliv 2020; 17.
125. Zhang J, Hou L, Wu X, Zhao D, Wang Z, Hu H, et al. Inhibitory effect of genetically engineered mesenchymal stem cells with Apoptin on hepatoma cells in vitro and in vivo. Mol Cellular Bioch 2016; 416:193-203.
126. Pessina A, Coccè V, Pascucci L, Bonomi A, Cavicchini L, Sisto F, et al. Mesenchymal stromal cells primed with P aclitaxel attract and kill leukaemia cells, inhibit angiogenesis and improve survival of leukaemia‐bearing mice. Brit J Haematol 2013; 160:766-778.
127. Duchi S, Sotgiu G, Lucarelli E, Ballestri M, Dozza B, Santi S, et al. Mesenchymal stem cells as delivery vehicle of porphyrin loaded nanoparticles: effective photoinduced in vitro killing of osteosarcoma. Journal Control Release 2013; 168:225-237.
128. Pessina A, Piccirillo M, Mineo E, Catalani P, Gribaldo L, Marafante E, et al. Role of SR-4987 stromal cells in the modulation of doxorubicin toxicity to in vitro granulocyte-macrophage progenitors (CFU-GM). Life sci 1999; 65:513-523.
129. Bonomi A, Ghezzi E, Pascucci L, Aralla M, Ceserani V, Pettinari L, et al. Effect of canine mesenchymal stromal cells loaded with paclitaxel on growth of canine glioma and human glioblastoma cell lines. Vet J 2017; 223:41-47.
130. Miller HJ, Leong T, Khandekar JD, Greipp PR, Gertz MA, Kyle RA. Paclitaxel as the initial treatment of multiple myeloma: an eastern cooperative oncology group study (E1A93). Ame J Clin Oncol 1998; 21:553-556.
131. De Lena M, Lorusso V, Latorre A, Fanizza G, Gargano G, Caporusso L, et al. Paclitaxel, cisplatin and lonidamine in advanced ovarian cancer: a phase II study. Eur J Cancer 2001; 37:364-368.
132. Maeda S, Motoi F, Onogawa T, Morikawa T, Shigeru O, Sakata N, et al. Paclitaxel as second-line chemotherapy in patients with gemcitabine-refractory pancreatic cancer: a retrospective study. Int J Clin Oncol 2011; 16:539-545.
133. Hodi FS, Soiffer RJ, Clark J, Finkelstein DM, Haluska FG. Phase II study of paclitaxel and carboplatin for malignant melanoma. Am J Clin Oncol 2002; 25:283-286.
134. Shukuya T, Ishiwata T, Hara M, Muraki K, Shibayama R, Koyama R, et al. Carboplatin plus weekly paclitaxel treatment in non-small cell lung cancer patients with interstitial lung disease. Anticancer res 2010; 30:4357-4361.
135. Bonomi A, Steimberg N, Benetti A, Berenzi A, Alessandri G, Pascucci L, et al. Paclitaxel‐releasing mesenchymal stromal cells inhibit the growth of multiple myeloma cells in a dynamic 3D culture system. Hematol Oncol 2017; 35:693-702.
136. Brini AT, Coccè V, Ferreira LMJ, Giannasi C, Cossellu G, Giannì AB, et al. Cell-mediated drug delivery by gingival interdental papilla mesenchymal stromal cells (GinPa-MSCs) loaded with paclitaxel. Expert Opinion Drug Deliv 2016; 13:789-798.
137. Nicolay NH, Perez RL, Rühle A, Trinh T, Sisombath S, Weber K-J, et al. Mesenchymal stem cells maintain their defining stem cell characteristics after treatment with cisplatin. Sci rep 2016; 6:1-11.
138. Liu S, Dai M, You L, Zhao Y. Advance in herpes simplex viruses for cancer therapy. Sci China Life Sci 2013; 56:298-305.
139. Zochowska M, Paca A, Schoehn G, Andrieu J-P, Chroboczek J, Dublet B, et al. Adenovirus dodecahedron, as a drug delivery vector. PLoS One 2009; 4:1-12.
140. Emeagi P, Goyvaerts C, Maenhout S, Pen J, Thielemans K, Breckpot K. Lentiviral vectors: a versatile tool to fight cancer. Curr Mol Med 2013; 13:602-625.
141. Uchibori R, Okada T, Ito T, Urabe M, Mizukami H, Kume A, et al. Retroviral vector‐producing mesenchymal stem cells for targeted suicide cancer gene therapy. J Gene Med 2009; 11:373-381.
142. Lee WY, Zhang T, Lau CP, Wang C, Chan K-M, Li G. Immortalized human fetal bone marrow-derived mesenchymal stromal cell expressing suicide gene for anti-tumor therapy in vitro and in vivo. Cytotherapy 2013; 15:1484-1497.
143. Song C, Xiang J, Tang J, Hirst DG, Zhou J, Chan K-M, et al. Thymidine kinase gene modified bone marrow mesenchymal stem cells as vehicles for antitumor therapy. Hum Gene Ther 2011; 22:439-449.
144. Cavarretta IT, Altanerova V, Matuskova M, Kucerova L, Culig Z, Altaner C. Adipose tissue–derived mesenchymal stem cells expressing prodrug-converting enzyme inhibit human prostate tumor growth. Mol Ther 2010; 18:223-231.
145. Ali I. Nano anti-cancer drugs: pros and cons and future perspectives. Curr Cancer Drug Targets 2011; 11:131-134.
146. Minion LE, Chase DM, Farley JH, Willmott LJ, Monk BJ. Safety and efficacy of salvage nano-particle albumin bound paclitaxel in recurrent cervical cancer: a feasibility study. Gynecol Oncol Res Pract 2016; 3:1-4.
147. Yousefi A-M, Safaroghli-Azar A, Fakhroueian Z, Bashash D. ZnO/CNT@ Fe3O4 induces ROS-mediated apoptosis in chronic myeloid leukemia (CML) cells: an emerging prospective for nanoparticles in leukemia treatment. Artifi Cells Nanomed Biotechnol 2020; 48:735-745.
148. Wang X, Chen H, Zeng X, Guo W, Jin Y, Wang S, et al. Efficient lung cancer-targeted drug delivery via a nanoparticle/MSC system. Acta Pharm Sin B 2019; 9:167-176.
149. Saulite L, Pleiko K, Popena I, Dapkute D, Rotomskis R, Riekstina U. Nanoparticle delivery to metastatic breast cancer cells by nanoengineered mesenchymal stem cells. Beilstein J Nanotechnol 2018; 9:321-332.
150. Cao B, Yang M, Zhu Y, Qu X, Mao C. Stem cells loaded with nanoparticles as a drug carrier for in vivo breast cancer therapy. Adv Mater 2014; 26:4627-4631.
151. Kang S, Bhang SH, Hwang S, Yoon J-K, Song J, Jang H-K, et al. Mesenchymal stem cells aggregate and deliver gold nanoparticles to tumors for photothermal therapy. ACS Nano 2015; 9:9678-9690.
152. Lenna S, Bellotti C, Duchi S, Martella E, Columbaro M, Dozza B, et al. Mesenchymal stromal cells mediated delivery of photoactive nanoparticles inhibits osteosarcoma growth in vitro and in a murine in vivo ectopic model. J Exp Clin Cancer Res 2020; 39:1-15.
153. Kibria G, Ramos EK, Wan Y, Gius DR, Liu H. Exosomes as a drug delivery system in cancer therapy: potential and challenges. Mol Pharm 2018; 15:3625-3633.
154. Chulpanova DS, Kitaeva KV, Tazetdinova LG, James V, Rizvanov AA, Solovyeva VV. Application of
mesenchymal stem cells for therapeutic agent delivery in anti-tumor treatment. Front Pharmacol 2018; 9:259-269.
155. Studeny M, Marini FC, Champlin RE, Zompetta C, Fidler IJ, Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-β delivery into tumors. Cancer Res 2002; 62:3603-3608.
156. Ren C, Kumar S, Chanda D, Kallman L, Chen J, Mountz JD, et al. Cancer gene therapy using mesenchymal stem cells expressing interferon-β in a mouse prostate cancer lung metastasis model. Gene Ther 2008; 15:1446-1453.
157. Ok Ahn J, woo Lee H, won Seo K, keun Kang S, chan Ra J, young Youn H. Anti-tumor effect of adipose tissue derived-mesenchymal stem cells expressing interferon-β and treatment with cisplatin in a xenograft mouse model for canine melanoma. PloS one 2013; 8:1-11.
158. Nakamizo A, Marini F, Amano T, Khan A, Studeny M, Gumin J, et al. Human bone marrow–derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 2005; 65:3307-3318.
159. Li X, Lu Y, Huang W, Xu H, Chen X, Geng Q, et al. In vitro effect of adenovirus‐mediated human Gamma Interferon gene transfer into human mesenchymal stem cells for chronic myelogenous leukemia. Hematol Oncol 2006; 24:151-158.
160. Wang X-J, Xiang B-Y, Ding Y-H, Chen L, Zou H, Mou X-Z, et al. Human menstrual blood-derived mesenchymal stem cells as a cellular vehicle for malignant glioma gene therapy. Oncotarget 2017; 8:1-13.
161. Xia L, Peng R, Leng W, Jia R, Zeng X, Yang X, et al. TRAIL-expressing gingival-derived mesenchymal stem cells inhibit tumorigenesis of tongue squamous cell carcinoma. J Dent Res 2015; 94:219-228.
162. Cafforio P, Viggiano L, Mannavola F, Pellè E, Caporusso C, Maiorano E, et al. pIL6-TRAIL-engineered umbilical cord mesenchymal/stromal stem cells are highly cytotoxic for myeloma cells both in vitro and in vivo. Stem Cell Res Ther 2017; 8:1-13.
163. Yan C, Song X, Yu W, Wei F, Li H, Lv M, et al. Human umbilical cord mesenchymal stem cells delivering sTRAIL home to lung cancer mediated by MCP-1/CCR2 axis and exhibit antitumor effects. Tumor Biol 2016; 37:8425-8435.
164. Guiho R, Biteau K, Grisendi G, Taurelle J, Chatelais M, Gantier M, et al. TRAIL delivered by mesenchymal stromal/stem cells counteracts tumor development in orthotopic Ewing sarcoma models. Int J Cancer 2016; 139:2802-2811.
165. Lathrop M, Sage E, Macura S, Brooks E, Cruz F, Bonenfant N, et al. Antitumor effects of TRAIL-expressing mesenchymal stromal cells in a mouse xenograft model of human mesothelioma. Cancer Gen Ther 2015; 22:44-54.
166. Zhang B, Shan H, Li D, Li Z-R, Zhu K-S, Jiang Z-B. The inhibitory effect of MSCs expressing TRAIL as a cellular delivery vehicle in combination with cisplatin on hepatocellular carcinoma. Cancer Biol Ther 2012; 13:1175-1184.
167. Yang Z-s, Tang X-J, Guo X-R, Zou D-D, Sun X-Y, Feng J-B, et al. Cancer cell-oriented migration of mesenchymal stem cells engineered with an anticancer gene (PTEN): an imaging demonstration. OncoTargets Ther 2014; 7:441-447.
168. Guo XR, Hu QY, Yuan YH, Tang XJ, Yang ZS, Zou DD, et al. PTEN‑mRNA engineered mesenchymal stem cell‑mediated cytotoxic effects on U251 glioma cells. Oncol Lett 2016; 11:2733-2740.
169. Du J, Zhang Y, Xu C, Xu X. Apoptin-modified human mesenchymal stem cells inhibit growth of lung carcinoma in nude mice. Mol Med Rep 2015; 12:1023-1029.
170. Sharif S, Ghahremani M, Soleimani M. Delivery of exogenous miR-124 to glioblastoma multiform cells by Wharton’s jelly mesenchymal stem cells decreases cell proliferation and migration, and confers chemosensitivity. Stem Cell Rev Rep 2018; 14:236-246.
171. Lee HK, Finniss S, Cazacu S, Bucris E, Ziv-Av A, Xiang C, et al. Mesenchymal stem cells deliver synthetic microRNA mimics to glioma cells and glioma stem cells and inhibit their cell migration and self-renewal. Oncotarget 2013; 4:346-362.
172. Shi Y, Su J, Roberts AI, Shou P, Rabson AB, Ren G. How mesenchymal stem cells interact with tissue immune responses. Trends Immunol 2012; 33:136-143.
173. Zhao RC, Liao L, Han Q. Mechanisms of and perspectives on the mesenchymal stem cell in immunotherapy. J Lab Clin Med 2004; 143:284-291.
174. Stagg J, Lejeune L, Paquin A, Galipeau J. Marrow stromal cells for interleukin-2 delivery in cancer immunotherapy. Hum Gene Ther 2004; 15:597-608.
175. Nakamura K, Ito Y, Kawano Y, Kurozumi K, Kobune M, Tsuda H, et al. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther 2004; 11:1155-1164.
176. Zhao W, Cheng J, Shi P, Huang J. Human umbilical cord mesenchymal stem cells with adenovirus-mediated interleukin 12 gene transduction inhibits the growth of ovarian carcinoma cells both in vitro and in vivo. South Med J 2011; 31:903-907.
177. Ryu CH, Park S-H, Park SA, Kim SM, Lim JY, Jeong CH, et al. Gene therapy of intracranial glioma using interleukin 12–secreting human umbilical cord blood–derived mesenchymal stem cells. Hum Gen Ther 2011; 22:733-743.
178. Kim N, Nam Y-S, Im K-I, Lim J-Y, Lee E-S, Jeon Y-W, et al. IL-21-expressing mesenchymal stem cells prevent lethal B-cell lymphoma through efficient delivery of IL-21, which redirects the immune system to target the tumor. Stem Cells Dev 2015; 24:2808-2821.
179. Xin H, Kanehira M, Mizuguchi H, Hayakawa T, Kikuchi T, Nukiwa T, et al. Targeted delivery of CX3CL1 to multiple lung tumors by mesenchymal stem cells. Stem Cells 2007; 25:1618-1626.
180. Xin H, Sun R, Kanehira M, Takahata T, Itoh J, Mizuguchi H, et al. Intratracheal delivery of CX3CL1-expressing mesenchymal stem cells to multiple lung tumors. Mol Med 2009; 15:321-327.
181. Levy O, Kuai R, Siren EM, Bhere D, Milton Y, Nissar N, et al. Shattering barriers toward clinically meaningful MSC therapies. Sci Adv 2020; 6:1-18.
182. Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011; 9:1-14.
183. Shi Y, Wang Y, Li Q, Liu K, Hou J, Shao C, et al. Immunoregulatory mechanisms of mesenchymal stem and stromal cells in inflammatory diseases. Nat Rev Nephrol 2018; 14:493-507.
184. Juneja SC, Viswanathan S, Ganguly M, Veillette C. A simplified method for the aspiration of bone marrow from patients undergoing hip and knee joint replacement for isolating mesenchymal stem cells and in vitro chondrogenesis. Bone Marrow Res 2016; 1-18.
185. Yin JQ, Zhu J, Ankrum JA. Manufacturing of primed mesenchymal stromal cells for therapy. Nat Biomed Eng 2019; 3:90-104.
186. François M, Romieu-Mourez R, Li M, Galipeau J. Human MSC suppression correlates with cytokine induction of indoleamine 2, 3-dioxygenase and bystander M2 macrophage differentiation. Mol Ther 2012; 20:187-195.
187. Russell AL, Lefavor R, Durand N, Glover L, Zubair AC. Modifiers of mesenchymal stem cell quantity and quality. Transfusion 2018; 58:1434-1440.
188. Chinnadurai R, Rajan D, Qayed M, Arafat D, Garcia M, Liu Y, et al. Potency analysis of mesenchymal stromal cells using a combinatorial assay matrix approach. Cell Rep 2018; 22:2504-2517.
189. Ho SS, Murphy KC, Binder BY, Vissers CB, Leach JK. Increased survival and function of mesenchymal stem cell spheroids entrapped in instructive alginate hydrogels. Stem Cells Transl Med 2016; 5:773-781.
190. Bunpetch V, Zhang Z-Y, Zhang X, Han S, Zongyou P, Wu H, et al. Strategies for MSC expansion and MSC-based microtissue for bone regeneration. Biomaterials 2019; 196:67-79.
191. Rao VV, Vu MK, Ma H, Killaars AR, Anseth KS. Rescuing mesenchymal stem cell regenerative properties on hydrogel substrates post serial expansion. Bioeng Transl Med 2019; 4:51-60.
192. Ozay EI, Vijayaraghavan J, Gonzalez-Perez G, Shanthalingam S, Sherman HL, Garrigan Jr DT, et al. Cymerus™ iPSC-MSCs significantly prolong survival in a pre-clinical, humanized mouse model of Graft-vs-host disease. Stem Cell Res 2019; 35:101401-101430.
193. Vodyanik MA, Yu J, Zhang X, Tian S, Stewart R, Thomson JA, et al. A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 2010; 7:718-729.
194. Hu X, Li L, Yu X, Zhang R, Yan S, Zeng Z, et al. CRISPR/Cas9-mediated reversibly immortalized mouse bone marrow stromal stem cells (BMSCs) retain multipotent features of mesenchymal stem cells (MSCs). Oncotarget 2017; 8:111847-111866.
195. François M, Copland IB, Yuan S, Romieu-Mourez R, Waller EK, Galipeau J. Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-γ licensing. Cytotherapy 2012; 14:147-152.
196. Moll G, Alm JJ, Davies LC, von Bahr L, Heldring N, Stenbeck‐Funke L, et al. Do cryopreserved mesenchymal stromal cells display impaired immunomodulatory and therapeutic properties? Stem Cells 2014; 32:2430-2442.
197. Moll G, Ankrum JA, Kamhieh-Milz J, Bieback K, Ringdén O, Volk H-D, et al. Intravascular mesenchymal stromal/stem cell therapy product diversification: time for new clinical guidelines. Trends Mol Med 2019; 25:149-163.
198. Toma C, Wagner WR, Bowry S, Schwartz A, Villanueva F. Fate of culture-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circ Res 2009; 104:398-402.
199. Wu Z, Zhang S, Zhou L, Cai J, Tan J, Gao X, et al. Thromboembolism induced by umbilical cord mesenchymal stem cell infusion: a report of two cases and literature review. Transplant Proc 2017; 49:1656-1658.
200. Moll G, Ignatowicz L, Catar R, Luecht C, Sadeghi B, Hamad O, et al. Different procoagulant activity of therapeutic mesenchymal stromal cells derived from bone marrow and placental decidua. Stem Cells Dev 2015; 24:2269-2279.
201. Nilsson B, Korsgren O, Lambris JD, Ekdahl KN. Can cells and biomaterials in therapeutic medicine be shielded from innate immune recognition? Trends Immunol 2010; 31:32-38.
202. Kamperman T, Karperien M, Le Gac S, Leijten J. Single-cell microgels: technology, challenges, and applications. Trends Biotechnol 2018; 36:850-865.
203. Yanai A, Häfeli UO, Metcalfe AL, Soema P, Addo L, Gregory-Evans CY, et al. Focused magnetic stem cell targeting to the retina using superparamagnetic iron oxide nanoparticles. Cell Transplant 2012; 21:1137-1148.
204. de Witte SF, Luk F, Sierra Parraga JM, Gargesha M, Merino A, Korevaar SS, et al. Immunomodulation by therapeutic mesenchymal stromal cells (MSC) is triggered through phagocytosis of MSC by monocytic cells. Stem Cells 2018; 36:602-615.
205. Galleu A, Riffo-Vasquez Y, Trento C, Lomas C, Dolcetti L, Cheung TS, et al. Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation. Sci Transl Med 2017; 9:1-15.
206. Salem N, Salem MY, Elmaghrabi MM, Elawady MA, Elawady MA, Sabry D, et al. Does vitamin C have the ability to augment the therapeutic effect of bone marrow-derived mesenchymal stem cells on spinal cord injury? Neural Regen Res 2017; 12:2050-2058.
207. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 2001; 169:12-20.
208. Kyriakou C, Rabin N, Pizzey A, Nathwani A, Yong K. Factors that influence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model. haematologica 2008; 93:1457-1465.
209. Xing F, Saidou J, Watabe K. Cancer associated fibroblasts (CAFs) in tumor microenvironment. Front Biosci 2010; 15:166-179.
210. Shiga K, Hara M, Nagasaki T, Sato T, Takahashi H, Takeyama H. Cancer-associated fibroblasts: their characteristics and their roles in tumor growth. Cancers 2015; 7:2443-2458.
211. Spaeth EL, Dembinski JL, Sasser AK, Watson K, Klopp A, Hall B, et al. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PloS one 2009; 4:1-11.
212. Plaks V, Kong N, Werb Z. The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 2015; 16:225-238.
213. Lam PY. Biological effects of cancer-secreted factors on human mesenchymal stem cells. Stem Cell Res Ther 2013; 4:1-2.
214. Lv L, Pan K, Li X-d, She K-l, Zhao J-j, Wang W, et al. The accumulation and prognosis value of tumor infiltrating IL-17 producing cells in esophageal squamous cell carcinoma. PloS one 2011; 6:1-7.
215. Klebanoff CA, Gattinoni L, Restifo NP. CD8+ T‐cell memory in tumor immunology and immunotherapy. Immunol Rev 2006; 211:214-224.
216. Hsieh C-S, Lee H-M, Lio C-WJ. Selection of regulatory T cells in the thymus. Nat Rev Immunol 2012; 12:157-167.
217. Balkwill FR, Capasso M, Hagemann T. The tumor microenvironment at a glance. The Company of Biologists Ltd 2012; 125:5591-5596.
218. Birbrair A, Zhang T, Wang Z-M, Messi ML, Olson JD, Mintz A, et al. Type-2 pericytes participate in normal and tumoral angiogenesis. Am J Physiol Cell Physiol 2014; 307:25-38.
219. Wang S-C, Hong J-H, Hsueh C, Chiang C-S. Tumor-secreted SDF-1 promotes glioma invasiveness and TAM tropism toward hypoxia in a murine astrocytoma model. Lab Invest 2012; 92:151-162.
220. Relation T, Dominici M, Horwitz EM. Concise review: an (im) penetrable shield: how the tumor microenvironment protects cancer stem cells. Stem Cells 2017; 35:1123-1130.
221. Guan J, Chen J. Mesenchymal stem cells in the tumor microenvironment. Biomed Rep 2013; 1:517-521.
222. Paino F, La Noce M, Di Nucci D, Nicoletti GF, Salzillo R, De Rosa A, et al. Human adipose stem cell differentiation is highly affected by cancer cells both in vitro and in vivo: implication for autologous fat grafting. Cell Death Dis 2018; 8:2568-2568.
223. Anderson BO, Cazap E, El Saghir NS, Yip C-H, Khaled HM, Otero IV, et al. Optimisation of breast cancer management in low-resource and middle-resource countries: executive summary of the Breast Health Global Initiative consensus. Lancet Oncol 2011; 12:387-398.
224. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nat 2008; 454:436-444.
Iranian Journal of Basic Medical Sciences
Volume 24, Issue 10
October 2021
Pages 1307-1323

Files

Share

How to cite

Statistics