Mesenchymal stem cells maintain their defining stem cell characteristics after treatment with cisplatin

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Nicolay, Nils H ^a,b,c   Perez, Ramon Lopez ^c   Rühle, Alexander ^b,c   Trinh, Thuy ^a,c   Sisombath, Sonevisay ^a,c   Weber, Klaus Josef ^a,b   Ho, Anthony D ^a   Debus, Jürgen ^a,b   Saffrich, Rainer ^a   Huber, Peter E ^a,b,c  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b Heidelberg Institute for Radiation Oncology (HIRO)   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN;

APOPTOSIS; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; DRUG RESISTANCE; FIBROBLAST; GENETICS; HUMAN; MESENCHYMAL STROMA CELL; PHENOTYPE; REGENERATION;

APOPTOSIS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CISPLATIN; DRUG RESISTANCE; FIBROBLASTS; HUMANS; MESENCHYMAL STROMAL CELLS; PHENOTYPE; REGENERATION;

EID: 84955465022     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20035     Document Type: Article

References (63)

1. Pasetto, L. M., D'Andrea, M. R., Brandes, A. A., Rossi, E., Monfardini, S. The development of platinum compounds and their possible combination. Crit Rev Oncol Hematol 60, 59-75 (2006).
2. Boulikas, T., Vougiouka, M. Recent clinical trials using cisplatin, carboplatin and their combination chemotherapy drugs (review). Oncol Rep 11, 559-95 (2004).
3. Jacobs, C. et al. A phase III randomized study comparing cisplatin and fluorouracil as single agents and in combination for advanced squamous cell carcinoma of the head and neck. J Clin Oncol 10, 257-63 (1992).
4. Filipits, M. et al. Cell cycle regulators and outcome of adjuvant cisplatin-based chemotherapy in completely resected non-small-cell lung cancer: the International Adjuvant Lung Cancer Trial Biologic Program. J Clin Oncol 25, 2735-40 (2007).
5. Dasari, S., Tchounwou, P. B. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol 740, 364-78 (2014).
6. Timerbaev, A. R., Hartinger, C. G., Aleksenko, S. S., Keppler, B. K. Interactions of antitumor metallodrugs with serum proteins: advances in characterization using modern analytical methodology. Chem Rev 106, 2224-48 (2006).
7. Jensen, M., Bjerring, M., Nielsen, N. C., Nerdal, W. Cisplatin interaction with phosphatidylserine bilayer studied by solid-state NMR spectroscopy. J Biol Inorg Chem 15, 213-23 (2010).
8. Wang, G., Reed, E., Li, Q. Q. Molecular basis of cellular response to cisplatin chemotherapy in non-small cell lung cancer (Review). Oncol Rep 12, 955-65 (2004).
9. Barabas, K., Milner, R., Lurie, D., Adin, C. Cisplatin: a review of toxicities and therapeutic applications. Vet Comp Oncol 6, 1-18 (2008).
10. Pabla, N., Dong, Z. Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int 73, 994-1007 (2008).
11. Parolini, O. et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells 26, 300-11 (2008).
12. Cavallo, C. et al. Comparison of alternative mesenchymal stem cell sources for cell banking and musculoskeletal advanced therapies. J Cell Biochem 112, 1418-30 (2011).
13. Moroni, L., Fornasari, P. M. Human mesenchymal stem cells: a bank perspective on the isolation, characterization and potential of alternative sources for the regeneration of musculoskeletal tissues. J Cell Physiol 228, 680-7 (2013).
14. Pittenger, M. F. et al. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-7 (1999).
15. Dominici, M. et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-7 (2006).
16. Ho, A. D., Wagner, W., Franke, W. Heterogeneity of mesenchymal stromal cell preparations. Cytotherapy 10, 320-30 (2008).
17. Nedeau, A. E. et al. A CXCL5-and bFGF-dependent effect of PDGF-B-activated fibroblasts in promoting trafficking and differentiation of bone marrow-derived mesenchymal stem cells. Exp Cell Res 314, 2176-86 (2008).
18. Kalinina, N. I., Sysoeva, V. Y., Rubina, K. A., Parfenova, Y. V., Tkachuk, V. A. Mesenchymal stem cells in tissue growth and repair. Acta Naturae 3, 30-7 (2011).
19. Nicolay, N. H., Lopez Perez, R., Debus, J., Huber, P. E. Mesenchymal stem cells-A new hope for radiotherapy-induced tissue damage? Cancer Lett 366, 133-40 (2015).
20. Zhang, Y., Liang, X., Lian, Q., Tse, H. F. Perspective and challenges of mesenchymal stem cells for cardiovascular regeneration. Expert Rev Cardiovasc Ther 11, 505-17 (2013).
21. Jo, C. H. et al. Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: a proof-of-concept clinical trial. Stem Cells 32, 1254-66 (2014).
22. Wilson, J. G. et al. Mesenchymal stem (stromal) cells for treatment of ARDS: a phase 1 clinical trial. Lancet Respir Med 3, 24-32 (2015).
23. Moghadasali, R. et al. Intra-renal arterial injection of autologous bone marrow mesenchymal stromal cells ameliorates cisplatininduced acute kidney injury in a rhesus Macaque mulatta monkey model. Cytotherapy 16, 734-49 (2014).
24. Yasuda, K. et al. Autologous cell therapy for cisplatin-induced acute kidney injury by using non-expanded adipose tissue-derived cells. Cytotherapy 14, 1089-100 (2012).
25. Kim, J. H. et al. Human adipose tissue-derived mesenchymal stem cells protect kidneys from cisplatin nephrotoxicity in rats. Am J Physiol Renal Physiol 302, F1141-50 (2012).
26. Eliopoulos, N. et al. Human marrow-derived mesenchymal stromal cells decrease cisplatin renotoxicity in vitro and in vivo and enhance survival of mice post-intraperitoneal injection. Am J Physiol Renal Physiol 299, F1288-98 (2010).
27. Morigi, M. et al. Life-sparing effect of human cord blood-mesenchymal stem cells in experimental acute kidney injury. Stem Cells 28, 513-22 (2010).
28. Urien, S., Lokiec, F. Population pharmacokinetics of total and unbound plasma cisplatin in adult patients. Br J Clin Pharmacol 57, 756-63 (2004).
29. Nygren, P., Larsson, R. Differential in vitro sensitivity of human tumor and normal cells to chemotherapeutic agents and resistance modulators. Int J Cancer 48, 598-604 (1991).
30. Reece, P. A. et al. Two-versus 24-hour infusion of cisplatin: pharmacokinetic considerations. J Clin Oncol 7, 270-5 (1989).
31. Liang, W., Xia, H., Li, J., Zhao, R. C. Human adipose tissue derived mesenchymal stem cells are resistant to several chemotherapeutic agents. Cytotechnology 63, 523-30 (2011).
32. Nicolay, N. H. et al. Mesenchymal stem cells retain their defining stem cell characteristics after exposure to ionizing radiation. Int J Radiat Oncol Biol Phys 87, 1171-8 (2013).
33. Li, J., Law, H. K., Lau, Y. L., Chan, G. C. Differential damage and recovery of human mesenchymal stem cells after exposure to chemotherapeutic agents. Br J Haematol 127, 326-34 (2004).
34. Nicolay, N. H. et al. Mesenchymal stem cells are sensitive to treatment with kinase inhibitors and ionizing radiation. Strahlenther Onkol 190, 1037-45 (2014).
35. Mueller, L. P. et al. Presence of mesenchymal stem cells in human bone marrow after exposure to chemotherapy: evidence of resistance to apoptosis induction. Stem Cells 24, 2753-65 (2006).
36. Prendergast, A. M., Cruet-Hennequart, S., Shaw, G., Barry, F. P., Carty, M. P. Activation of DNA damage response pathways in human mesenchymal stem cells exposed to cisplatin or gamma-irradiation. Cell Cycle 10, 3768-77 (2011).
37. Nicolay, N. H. et al. Mesenchymal stem cells are resistant to carbon ion radiotherapy. Oncotarget 6, 2076-87 (2015).
38. Liang, W., Lu, C., Li, J., Yin, J. Q., Zhao, R. C. p73alpha regulates the sensitivity of bone marrow mesenchymal stem cells to DNA damage agents. Toxicology 270, 49-56 (2010).
39. Nicolay, N. H., Lopez Perez, R., Saffrich, R., Huber, P. E. Radio-resistant mesenchymal stem cells: mechanisms of resistance and potential implications for the clinic. Oncotarget 6, 19366-80 (2015).
40. Zhang, B. et al. Cisplatin sensitizes human hepatocellular carcinoma cells, but not hepatocytes and mesenchymal stem cells, to TRAIL within a therapeutic window partially depending on the upregulation of DR5. Oncol Rep 25, 461-8 (2011).
41. Liu, W. H. et al. Cisplatin-selected resistance is associated with increased motility and stem-like properties via activation of STAT3/Snail axis in atypical teratoid/rhabdoid tumor cells. Oncotarget 6, 1750-68 (2015).
42. Bear, J. E., Haugh, J. M. Directed migration of mesenchymal cells: where signaling and the cytoskeleton meet. Curr Opin Cell Biol 30, 74-82 (2014).
43. Kopf-Maier, P., Muhlhausen, S. K. Changes in the cytoskeleton pattern of tumor cells by cisplatin in vitro. Chem Biol Interact 82, 295-316 (1992).
44. Shen, D. W., Liang, X. J., Gawinowicz, M. A., Gottesman, M. M. Identification of cytoskeletal [14C]carboplatin-binding proteins reveals reduced expression and disorganization of actin and filamin in cisplatin-resistant cell lines. Mol Pharmacol 66, 789-93 (2004).
45. Sharma, S. et al. Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells. Nanomedicine 8, 757-66 (2012).
46. Rebillard, A. et al. Cisplatin-induced apoptosis involves a Fas-ROCK-ezrin-dependent actin remodelling in human colon cancer cells. Eur J Cancer 46, 1445-55 (2010).
47. Francois, S. et al. Local irradiation not only induces homing of human mesenchymal stem cells at exposed sites but promotes their widespread engraftment to multiple organs: a study of their quantitative distribution after irradiation damage. Stem Cells 24, 1020-9 (2006).
48. Mouiseddine, M. et al. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br J Radiol 80 Spec No 1, S49-55 (2007).
49. Liu, J. et al. Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Mol Cells 37, 865-72 (2014).
50. Gupta, A. K., Jadhav, S. H., Tripathy, N. K., Nityanand, S. Fetal kidney stem cells ameliorate cisplatin induced acute renal failure and promote renal angiogenesis. World J Stem Cells 7, 776-88 (2015).
51. Jin, Y. W. et al. Comprehensive analysis of time-and dose-dependent patterns of gene expression in a human mesenchymal stem cell line exposed to low-dose ionizing radiation. Oncol Rep 19, 135-44 (2008).
52. Stewart, D. J. et al. Factors affecting human autopsy kidney-cortex and kidney-medulla platinum concentrations after cisplatin administration. Cancer Chemother Pharmacol 34, 14-22 (1994).
53. Stewart, D. J. et al. Renal and hepatic concentrations of platinum: relationship to cisplatin time, dose, and nephrotoxicity. J Clin Oncol 3, 1251-6 (1985).
54. Morigi, M. et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 15, 1794-804 (2004).
55. Patel, K. et al. Heat shock protein 90 (HSP90) is overexpressed in p16-negative oropharyngeal squamous cell carcinoma, and its inhibition in vitro potentiates the effects of chemoradiation. Cancer Chemother Pharmacol 74, 1015-22 (2014).
56. Arany, I., Clark, J. S., Reed, D. K., Ember, I., Juncos, L. A. Cisplatin enhances interaction between p66Shc and HSP27: its role in reorganization of the actin cytoskeleton in renal proximal tubule cells. Anticancer Res 32, 4759-63 (2012).
57. Baker, T. G. et al. Heat shock protein-mediated protection against Cisplatin-induced hair cell death. J Assoc Res Otolaryngol 16, 67-80 (2015).
58. Abu-Hadid, M., Wilkes, J. D., Elakawi, Z., Pendyala, L., Perez, R. P. Relationship between heat shock protein 60 (HSP60) mRNA expression and resistance to platinum analogues in human ovarian and bladder carcinoma cell lines. Cancer Lett 119, 63-70 (1997).
59. Ling, J. et al. Heat shock protein 10 regulated apoptosis of mouse ovarian granulosa cells. Gynecol Endocrinol 27, 63-71 (2011).
60. Yang, X. et al. Hsp70 promotes chemoresistance by blocking Bax mitochondrial translocation in ovarian cancer cells. Cancer Lett 321, 137-43 (2012).
61. Endo, H., Yano, M., Okumura, Y., Kido, H. Ibuprofen enhances the anticancer activity of cisplatin in lung cancer cells by inhibiting the heat shock protein 70. Cell Death Dis 5, e1027 (2014).
62. Ma, L. et al. Dual targeting of heat shock proteins 90 and 70 promotes cell death and enhances the anticancer effect of chemotherapeutic agents in bladder cancer. Oncol Rep 31, 2482-92 (2014).
63. Wagner, W. et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33, 1402-16 (2005).