Paracrine effects of mesenchymal stem cells induce senescence and differentiation of glioblastoma stem-like cells

Cell Transplantation

Volumn 24, Issue 4, 2015, Pages 631-644

  Kološa, Katja ^a   Motaln, Helena ^a   Herold Mende, Christel ^b   Koršič, Marjan ^c   Lah, Tamara T ^a,d  

^a NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Cell differentiation; Glioblastoma multiforme (GBM); Mesenchymal stem cells (MSCs); Senescence; Stem like cancer cells; Therapy response

Indexed keywords

ATM PROTEIN; CITED2 PROTEIN; COLLAGEN TYPE 1A; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; FLUOROURACIL; FN1 PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HERMES ANTIGEN; MORC3 PROTEIN; NOTCH1 RECEPTOR; PRKCD PROTEIN; PROTEIN; PROTEIN P16; PROTEIN P21; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SERPINE 1; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 5; TEMOZOLOMIDE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; VIMENTIN; CULTURE MEDIUM;

ANALYSIS; APOPTOSIS; ARTICLE; BONE MARROW; CANCER STEM CELL; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; GENE ONTOLOGY; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; KEGG ANALYSIS; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PARACRINE SIGNALING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; SIGNAL TRANSDUCTION; UMBILICAL CORD; UPREGULATION; AGED; BONE MARROW CELL; CELL AGING; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; MALE; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHARMACOLOGY; TUMOR CELL CULTURE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; APOPTOSIS; BONE MARROW CELLS; CELL AGING; CELL DIFFERENTIATION; CULTURE MEDIA, CONDITIONED; CYCLIN D1; FEMALE; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION; GLIOBLASTOMA; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MESENCHYMAL STROMAL CELLS; PARACRINE COMMUNICATION; TUMOR CELLS, CULTURED; UMBILICAL CORD;

EID: 84927604747     PISSN: 09636897     EISSN: 15553892     Source Type: Journal    
DOI: 10.3727/096368915X687787     Document Type: Article

References (54)

1. Ardebili, S. Y; Zajc, I.; Gole, B.; Campos, B.; Herold Mende, C.; Drmota, S.; Lah, T. T. CD133/prominin1 is prognostic for GBM patient’s survival, but inversely correlated with cysteine cathepsins’ expression in glioblastoma derived spheroids. Radiol. Oncol. 45:102–115; 2011.
2. Bago, J. R.; Alieva, M.; Soler, C.; Rubio, N.; Blanco J. Endothelial differentiation of adipose tissue-derived mesenchymal stromal cells in glioma tumors: Implications for cell-based therapy. Mol. Ther. 21(9):1758–1766; 2013.
3. Balbous, A.; Cortes, U.; Guilloteau, K.; Villalva, C.; Flamant, S.; Gaillard, A.; Milin, S.; Wager, M.; Sorel, N.; Guilhot, J.; Bennaceur-Griscelli, A.; Turhan, A.; Chomel, J. C.; Karayan-Tapon, L. A mesenchymal glioma stem cell profile is related to clinical outcome. Oncogenesis 3:2157– 2166; 2014.
4. Bao, S.; Wu, Q.; McLendon, R. E.; Hao, Y.; Shi, Q.; Hjelmeland, A. B.; Dewhirst, M. W.; Binger, D. D.; Rich, J. N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760; 2006.
5. Ben-Porath, I.; Weinberg, R. A. The signals and pathways activating cellular senescence. Int. J. Biochem. Cell. Biol. 37:961–976; 2005.
6. Bjerkvig, R.; Tysnes, B. B.; Aboody, K. S.; Najbauer, J.; Terzis, A. J. Opinion: The origin of the cancer stem cell: Current controversies and new insights. Nat. Rev. Cancer. 5(11):899–904; 2005.
7. Bleeker, F. E.; Molenaar, R. J.; Leenstra, S. Recent advances in the molecular understanding of glioblastoma. J. Neurooncol. 108:11–27; 2012.
8. Campos, B.; Herold-Mende, C. C. Insight into the complex regulation of CD133 in glioma. In. J. Cancer. 128:501–510; 2011.
9. Campos, B.; Wan, F.; Farhadi, M.; Ernst, A.; Zeppernick, F.; Taherer, K. E.; Ahmadi, R.; Lohr, J.; Dictus, C.; Gdynia, G.; Combs, S. E.; Goidts, V.; Helmke, B. M.; Eckstein, V.; Roth, W.; Beckhove, P.; Lichter, P.; Unterberg, A.; Radlwimmer, B.; Herold-Mende, C. Differentiation therapy exerts antitumor effexts on stem-like glioma cells. Clin. Cancer. Res. 16:2715–2728; 2010.
10. Campos, B.; Zeng, L.; Daotrong, P. H.; Eckstein, V.; Unterberg, A.; Mairbäurl, H.; and Herold-Mende, C. Expression and regulation of AC133 and CD133 in glioblastoma. Glia 59(12):1974–1986; 2011.
11. Capper, D.; Gaiser, T.; Hartmann, C.; Habel, A.; Mueller, W.; Herold-Mende, C., Stem-cell-like glioma cells are resistant to TRAIL/Apo2L and exhibit downregulation of caspase-8 by promoter methylation. Acta. Neuropathol. 117:445–456; 2009.
12. Childs, B. G.; Baker, D. J.; Kirkland, J. L.; Campisi, J.; van Deursen, J.M.. Senescence and apoptosis: Duelling or complementary cell fates? EMBO Rep. 15(11):1139–1153; 2014.
13. Dasari, V. R.; Velpula, K. K.; Kaur, K.; Fassett, D.; Klopfenstein, J. D.; Dinh, D. H.; Gujrati, M.; Rao, J. S. Cord blood stem cell-mediated induction of apoptosis in glioma downregulates X-linked inhibitor of apoptosis protein (XIAP). PLoS One 5(7): e11813; 2010.
14. Dimri, G. P.; Lee, X.; Basile, G., A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci.USA. 92:9363–9367; 1995.
15. Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.; Krause, D.; Deans, R.; Keating, A.; Prockop, D. J.; Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315– 317; 2006.
16. Eyler, C. E.; Rich, J. N. Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis. J. Clin. Oncol. 26:2839–2845; 2008.
17. Gondi, C. S.; Gogineni, V. R.; Chetty, C.; Dasari, R. V.; Gorantla, B.; Gujrati, M.; Dinh, D. H.; Rao, J. S. Induction of apoptosis in glioma cells requires cell-to-cell contact with human umbilical cord blood stem cells. Int. J. Oncol. 31:1165–1173; 2010.
18. Jeon, H.-M.; Sohn, Y.-M.; Oh, S.-Y.; Kim, S.-H.; Beck, S.; Kim, S.; Kim, H. ID4 imparts chemoresistance and cancer stemness to glioma cells by derepressing mir-9*–mediated suppression of Sox2. Cancer Res. 71(9):3410–3421; 2011.
19. Jiao, H.; Guan, F.; Yang, B.; Li, J.; Song, L.; Hu, X.; Du, Y. Human umbilical cord blood-derived mesenchymal stem cells inhibit C6 glioma via downregulation of cyclin D1. Neurol. India. 59(2):241–248; 2011.
20. Jiao, H.; Yang, B.; Guan, F.; Li, J.; Song, L.; Song, L.; Hu, X.; Liang, S.; Du, Y.; Jiang, C. The mixed human umbilical cord blood-derived mesenchymal stem cells show higher antitumor effect against C6 cells than the single in vitro. Neurol. Res. 33(4):405–414; 2011.
21. Kang, S.-G.; Jeun, S. S.; Lim, J. Y.; Kim, S. M.; Yang, Y. S.; Oh, W. I.; Huh, P.-W.; Park, C. K. Cytotoxicity of human umbilical cord blood-derived mesenchymal stem cells against human malignant glioma cells. Childs Nerv. Syst. 24:293–302; 2008.
22. Kim, K. S.; Seu, Y. B.; Baek, S. H.; Kim, M. J.; Kim, K. J.; Kim, J. H.; Kim, J. R. Induction of cellular senescence by insulin-like growth factor binding protein-5 through a p53dependent mechanism. Mol. Biol. Cell. 18(11):4543–4552; 2007.
23. Kleinschmidt, K.; Klinge, P. M.; Stopa, E.; Wallrapp, C.; Glage, S.; Geigle, P.; Brinker, T. Alginate encapsulated human mesenchymal stem cells suppress syngeneic glioma growth in the immunocompetent rat. J. Microencaps. 28(7):621–628; 2011.
24. Klopp, A. H.; Gupta, A.; Spaeth, E.; Andreeff, M.; Marini, F. Concise review: Dissecting a discrepancy in the literature: Do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29:11–19; 2011.
25. Köritzer, J.; Boxhammer, V.; Schäfer, A.; Shimizu, T.; Klämpfl, T. G.; Li, Y.-F.; Welz, C., Schwenk-Zieger, S.; Morfill, G. E.; Zimmermann, J. L.; Schlegel, J. Restoration of sensitivity in chemo-resistant glioma cells by cold atmospheric plasma. PloS One 8(5), e64498; 2013.
26. Kortlever, R. M.; Higgins, P. J.; Bernards, R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat. Cell. Biol. 8:877–884; 2006.
27. Kucerova, L.; Matuskova, M.; Hlubinova, K.; Altanerova, V.; Altaner, C. Tumor cell behaviour modulation by mesenchymal stromal cells. Mol. Cancer. 9:129–144; 2010.
28. Liu, G.; Yuan, X.; Zeng, Z.; Tunici, P.; Ng, H.; Abdulkadir, I. R.; Lu, L.; Irvin, D.; Black, K. L.; Yu, J.S.. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer. 5:67–79; 2006.
29. Metellus, P.; Nanni-Metellus, I.; Delfino, C.; Colin, C.; Tchogandjian, A.; Coulibaly, B.; Fina, F.; Loundou, A.; Barrie, M.; Chinot, O.; Ouafik, L.; Figarella-Branger, D. Prognostic impact of CD133 mRNA expression in 48 glioblastoma patients treated with concomitant radiochemotherapy: A prospective patient cohort at a single institution. Ann. Surg. Oncol. 18(10):2937–2945; 2011.
30. Moiseeva, O.; Mallette, F. A.; Mukhopadhyay, U. K.; Moores, A.; Ferbeyre, G., DNA damage signaling and p53dependent senescence after prolonged-interferon stimulation. Mol. Biol.Cell. 17:1583–1592; 2006.
31. Motaln, H.; Schichor, C.; Lah, T. T. Human mesenchymal stem cells and their use in cell-based therapies. Cancer 116(11):2519–2530; 2010.
32. Motaln, H.; Gruden, K.; Hren, M.; Schichor, C.; Primon, M.; Rotter, A.; Lah, T. T. Human mesenchymal stem cells exploit the immune response mediating chemokines to impact the phenotype of glioblastoma. Cell Transplant. 21(7):1529–1545; 2012.
33. Nakamura, K.; Ito, Y.; Kawano, Y.; Kurozumi, K.; Kobune, M.; Tsuda, H.; Bizen, A.; Honmou, O.; Niitsu, Y.; Hamada, H. Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther. 11:1155– 1164; 2004.
34. Nam, T. J.; Busby, W., Jr.; Clemmons, D. R. Insulin-like growth factor binding protein-5 binds to plasminogen activator inhibitor-I. Endocrinology 138:2972–2978; 1997.
35. Nduom, E. K.; Hadjipanayis, C. G.; Van Meir, E. G. Glioblastoma cancer stem-like cells: Implications for pathogenesis and treatment. Cancer J. 18(1): 100–106; 2012.
36. Passos, J. F.; Nelson, G.; Wang, C.; Richter, T.; Simillion, C.; Proctor, C. J.; Miwa, S.; Olijslagers, S.; Hallinan, J.; Wipat, A.; Saretzki, G.; Rudolph, K. L.; Kirkwood, T. B.; von Zglinicki, T., Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol. System Biol. 6:347–361; 2010.
37. Podergajs, N.; Brekka N.; Radlwimmer, B.; Herold-Mende, C.; Talasila, K. M.; Tiemann, K.; Rajcevic, U.; Lah, T. T.; Bjerkvig, R.; Miletic, H. Expansive growth of two glioblastoma stem-like cell lines is mediated by bFGF and not by EGF. Radiol. Oncol. 47(4):330–337; 2013.
38. Sabin, R. J.; Anderson, R.M.. Cellular Senescence - Its role in cancer and the response to ionizing radiation. Gen. Integrity. 2:7–16; 2011.
39. Saito, N.; Fu, J.; Zheng, S.; Yao, J.; Wang, S.; Liu, D. D.; Yuan, Y.; Sulman, E. P.; Lang, F. F.; Colman, H.; Verhaak, R. G.; Yung, A. W. K.; Koul, D. A high Notch pathway activation predicts response to g secretase inhibitors in proneural subtype of glioma tumor-initiating cells. Stem cells 32:301–312; 2013.
40. Sart, S.; Tsai, A. C.; Ma, T. Three-dimensional aggregates of mesenchymal stem cells: Cellular mechanisms, biological properties, and applications. Tissue Eng. Part B Rev. 20(5):365–380; 2014.
41. Shapiro G. I. Cyclin-dependent kinase pathway as targets for cancer treatment. J. Clin. Oncol. 24(11): 1770–1783; 2006.
42. Singh, S. K.; Clarke, I. D.; Terasaki, M.; Bonn, V. E.; Hawkins, C.; Squire, J.; Dirks, P. B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63:5821– 5828; 2003.
43. Takahashi, K.; Yoshida, N.; Murakami, N.; Kawata, K.; Ishizaki, H.; Tanaka-Okamoto, M.; Miyoshi, J.; Zinn, A. R.; Shime, H.; Inoue, N., Dynamic regulation of p53 subnuclear localization and senescence by MORC3. Mol. Biol. Cell. 18:1701–1709; 2003.
44. Ulasov, I. V.; Nandi, S.; Dey, M.; Sonabend, A. M.; Lesniak, M.S.. Inhibition of Sonic Hedgehog and Notch pathways enhances sensitivity of CD133+ glioma stem cells to temozolomide therapy. Mol. Med. 17:103–112; 2011.
45. Visvader, J. E.; Lindeman, G.J.. Stem cells and cancer – The promise and puzzles. Mol. Oncol. 4:369–372; 2010.
46. Wan, F.; Zhang, S.; Xie, R.; Gao, B.; Campos, B.; Herold Mende, C.; Lei, T. The utility and limitations of neurosphere assay, CD133 immunophenotyping and side population assay in glioma stem cell research. Brain pathology (Zurich,Switzerland), 20(5):877–889; 2010.
47. Wang, J.; Wakeman, T. P.; Latha, J. D.; Hjelmeland, A. B.; Wang, X. F.; White, R. R.; Rich J. N.; Bruce A.; Sullenger B. A. Notch promotes radioresistance of glioma stem cells. Stem Cells 28(1):17–28; 2010.
48. Wang, S. H.; Hung, C. S.; Peng, T. S.; Huang, C. C.; Wei, M. H.; Guo, J. Y.; Fu, S. Y.; Lai, C. M.; Chen, C. C. Mesenchymal stem cells in the Wharton’s jelly of the human umbilical cord. Stem Cells 22:1330–1337; 2004.
49. Weyemi, U.; Boufraqech, M.; Prenois, F.; Courtin, F.; Caillou, B.; Talbot, M.; Dardalhon, M.; Al Ghuzlan, A.; Bidart, J. M.; Schlumberger, M.; Dupuy, C. ROS-generating NADPH oxidase NOX4 is a critical mediator in oncogenic H-Ras-induced DNA damage and subsequent senescence. Oncogene 31:1117–1129; 2012.
50. Yang, C.; Lei, D.; Ouyang, W.; Ren, J.; Li, H.; Hu, J.; Huang, S.. Conditioned media from human adipose tissuederived mesencymal stem cell and umbilical cord-derived mesenchymal stem cells efficiently induced the apoptosis and differentiation in human glioma cell lines in vitro. Biomed. Res. Int. 2014; 2014:109389.
51. Yeh, H. Y.; Liu, B. H.; Sieber, M.; Hsu, S. H. Substratedependent gene regulation of self-assembled human MSC spheroids on chitosan membranes. BMC Genomics 15:10–24; 2014.
52. Zeppernick, F.; Ahmadi, R.; Campos, B.; Dictus, C.; Helmke, B. M.; Becker, N. P.; Unterberg, A.; Radlwimmer, B.; HeroldMende, C. C. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin. Cancer Res. 14(1):123–129; 2008.
53. Zheng, M.; Bocangel, D.; Ramesh, R.; Ekmekcioglu, S.; Poindexter, N.; Grimm, E. A., Chada, S., IL-24 overcomes TMZ-resistance and enhances cell death by downregulation of MGMT in human melanoma cells. Mol. Cancer Ther. 7(12):3842–3851; 2008.
54. Zölzer, F.; Streffer, C., Quiescence in S-phase and G1 arrest induced by irradiation and/or hyperthermia in six human tumour cell lines of different p53 status. Int. J. Radiat. Biol. 76(5):717–725; 2000.