A peculiar molecular profile of umbilical cord-mesenchymal stromal cells drives their inhibitory effects on multiple myeloma cell growth and tumor progression

Stem Cells and Development

Volumn 24, Issue 12, 2015, Pages 1457-1470

  Ciavarella, Sabino ^a   Caselli, Anna ^a   Tamma, Antonella Valentina ^a   Savonarola, Annalisa ^a   Loverro, Giuseppe ^a   Paganelli, Roberto ^b   Tucci, Marco ^a   Silvestris, Franco ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TISSUE; ARTICLE; BONE MARROW CELL; CANCER GROWTH; CELL GROWTH; CELL PROLIFERATION; CLONOGENIC ASSAY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; MESENCHYMAL STROMA CELL; MULTIPLE MYELOMA; PRIORITY JOURNAL; TUMOR VOLUME; UMBILICAL CORD; ANIMAL; CARCINOGENESIS; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; MOUSE; TRANSPLANTATION;

MUS;

ADIPOSE TISSUE; ANIMALS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MULTIPLE MYELOMA; UMBILICAL CORD;

EID: 84930469241     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0254     Document Type: Article

References (61)

1. da Silva Meirelles L, PC Chagastelles and NB Nardi. (2006). Mesenchymal stem cells reside in virtually all postnatal organs and tissues. J Cell Sci 119:2204-2213.
2. Uccelli A, L Moretta and V Pistoia. (2008). Mesenchymal stem cells in health and disease. Nat Rev Immunol 8:726-733.
3. Crisan M, S Yap, L Casteilla, CW Chen, M Corselli, TS Park, G Andriolo, B Sun, B Zheng, et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301-313.
4. Ciavarella S, F Dammacco, M De Matteo, G Loverro and F Silvestris. (2009) Umbilical cord mesenchymal stem cells: role of regulatory genes in their differentiation to osteoblasts. Stem Cells Dev 18:1211-1220.
5. Klopp AH, A Gupta, E Spaeth, M Andreeff and F Marini. (2010). Dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29:11-19.
6. Roccaro AM, A Sacco, P Maiso, AK Azab, YT Tai, M Reagan, F Azab, LM Flores, F Campigotto, et al. (2013). BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. JCI 123:1542-1555.
7. Reagan MR and IM Ghobrial. (2012). Multiple myeloma mesenchymal stem cells: characterization, origin, and tumor-promoting effects. Clin Cancer Res 18:342-349.
8. Chauhan D, H Uchiyama, Y Akbarali, M Urashima, K Yamamoto, TA Libermann and KC Anderson. (1996). Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-kappa B. Blood 87:1104-1112.
9. Gupta D, SP Treon, Y Shima, T Hideshima, K Podar, YT Tai, B Lin, S Lentzsch, FE Davies, et al. (2001). Adherence of multiple myeloma cells to bone marrow stromal cells upregulates vascular endothelial growth factor secretion: therapeutic applications. Leukemia 15:1950-1961.
10. Mitsiades CS, NS Mitsiades, NC Munshi, PG Richardson and KC Anderson. (2006). The role of the bone microenvironment in the pathophysiology and therapeutic management of multiple myeloma: interplay of growth factors, their receptors and stromal interactions. Eur J Cancer 42:1564-1573.
11. Hideshima T, C Mitsiades, G Tonon, PG Richardson and KC Anderson. (2007). Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat Rev Cancer 7:585-598.
12. Gunn WG, A Conley, L Deininger, SD Olson, DJ Prockop and CA Gregory. (2006). A crosstalk between myeloma cells and marrow stromal cells stimulates production of DKK1 and interleukin-6: a potential role in the development of lytic bone disease and tumor progression in multiple myeloma. Stem Cells 24:986-991.
13. Atsuta I, S Liu, Y Miura, K Akiyama, C Chen, Y An, S Shi and Chen FM (2013). Mesenchymal stem cells inhibit multiple myeloma cells via the Fas/Fas ligand pathway. Stem Cell Res Ther 4:111-124.
14. Ciavarella S, G Grisendi, M Dominici, M Tucci, O Brunetti, F Dammacco and F Silvestris. (2012). In vitro antimyeloma activity of TRAIL-expressing adipose-derived mesenchymal stem cells. Br J Haematol 157:586-598.
15. Li X, W Ling, A Pennisi, Y Wang, S Khan, M Heidaran, A Pal, X Zhang, S He, et al. (2011). Human placenta-derived adherent cells prevent bone loss, stimulate bone formation, and suppress growth of multiple myeloma in bone. Stem Cells 29:263-273.
16. Martinez-Quintanilla J, D Bhere, P Heidari, D He, U Mahmood and K Shah. (2013). Therapeutic efficacy and fate of bimodal engineered stem cells in malignant brain tumors. Stem Cells 31:1706-1714.
17. Dembinski JL, SM Wilson, EL Spaeth, M Studeny, C Zompetta, I Samudio, K Roby, M Andreeff and FC Marini. (2013). Tumor stroma engraftment of gene-modified mesenchymal stem cells as anti-tumor therapy against ovarian cancer. Cytotherapy 15:20-32.
18. Loebinger MR, A Eddaoudi, D Davies and SM Janes. (2009). Mesenchymal stem cell delivery of TRAIL can eliminate metastatic cancer. Cancer Res 69:4134-4142.
19. Garayoa M, JL Garcia, C Santamaria, A Garcia-Gomez, JF Blanco, A Pandiella, JM Hernández, FM Sanchez-Guijo, MC del Cañizo, NC Gutiérrez and J San Miguel. (2009). Mesenchymal stem cells from multiple myeloma patients display distinct genomic profile as compared with those from normal donors. Leukemia 23:1515-1527.
20. Corre J, K Mahtouk, M Attal, M Gadelorge, A Huynh, S Fleury-Cappellesso, C Danho, P Laharrague, B Klein, T Rème and P Bourin. (2007). Bone marrow mesenchymal stem cells are abnormal in multiple myeloma. Leukemia 21:1079-1088.
21. Todoerti K, G Lisignoli, P Storti, L Agnelli, F Novara, C Manferdini, K Codeluppi, S Colla, M Crugnola, et al. (2010). Distinct transcriptional profiles characterize bone microenvironment mesenchymal cells rather than osteoblasts in relationship with multiple myeloma bone disease. Exp Hematol 2010;38:141-153.
22. Yaccoby S, MJ Wezeman, M Zangari, R Walker, M Cottler-Fox, D Gaddy, W Ling, R Saha, B Barlogie, G Tricot and J Epstein. (2006). Inhibitory effects of osteoblasts and increased bone formation on myeloma in novel culture systems and a myelomatous mouse model. Haematologica 91:192-199.
23. Noll JE, SA Williams, CM Tong, H Wang, JM Quach, LE Purton, K Pilkington, LB To, A Evdokiou, S Gronthos and AC Zannettino. (2013). Myeloma plasma cells alter the bone marrow microenvironment by stimulating the proliferation of mesenchymal stromal cells. Haematologica 99:163-171.
24. Li X, W Ling, S Khan and S Yaccoby. (2012). Therapeutic effects of intrabone and systemic mesenchymal stem cell cytotherapy on myeloma bone disease and tumor growth. J Bone Miner Res 27:1635-1648.
25. Lin HD, CY Fong, A Biswas, M Choolani and A Bongso. (2014). Human Wharton's jelly stem cells, its conditioned medium and cell-free lysate inhibit the growth of human lymphoma cells. Stem Cell Rev Rep 10:573-586.
26. Cooperman J, R Neely, DT Teachey, S Grupp and JK Choi. (2004). Cell division rates of primary human precursor B cells in culture reflect in vivo rates. Stem Cells 22:1111-1120.
27. Kim J, RA Denu, BA Dollar, LE Escalante, JP Kuether, NS Callander, F Asimakopoulos and P Hematti. (2012). Macrophages and mesenchymal stromal cells support survival and proliferation of multiple myeloma cells. Brit J Haematol 158:336-346.
28. Du X, AS Kazim, AJ Brown and H Yang. (2012). An essential role of Hrs/Vps27 in endosomal cholesterol trafficking. Cell Rep 1:29-35.
29. Ciavarella S, M Dominici, F Dammacco and F Silvestris. (2011). Mesenchymal stem cells: a new promise in anticancer therapy. Stem Cell Dev 20:1-10.
30. Manier S, A Sacco, X Leleu, IM Ghobrial and AM Roccaro. (2012). Bone marrow microenvironment in multiple myeloma progression. J Biomed Biotechnol 2012:157496.
31. André T, N Meuleman, B Stamatopoulos, C De Bruyn, K Pieters, D Bron and L Lagneaux. (2013). Evidences of early senescence in multiple myeloma bone marrow mesenchymal stromal cells. PloS One 8:e59756.
32. Akiyama K1, C Chen, D Wang, X Xu, C Qu, T Yamaza, T Cai, WChen, L Sun and S Shi. (2012). Mesenchymal-stemcell-induced immunoregulation involves FAS-ligand-/FASmediated T cell apoptosis. Cell Stem Cell 10:544-555.
33. Klein B, K Tarte, M Jourdan, K Mathouk, E Legouffe, J De Vos and JF Rossi. (2003). Survival and proliferation factors of normal and malignant plasma cells. Int J Hematol 78:106-113.
34. Menu E, E van Valckenborgh, B van Camp and K Vanderkerken. (2009). The role of the insulin-like growth factor 1 receptor axis in multiple myeloma. Arch Physiol Biochem 115:49-57.
35. Terpos E, M Politou, N Viniou and A Rahemtulla. (2005). Significance of macrophage inflammatory protein-1 alpha (MIP-1alpha) in multiple myeloma. Leuk Lymphoma 46:1699-1707.
36. Bolzoni M, P Storti, S Bonomini, K Todoerti, D Guasco, D Toscani, L Agnelli, A Neri, V Rizzoli and N Giuliani. (2013). Immunomodulatory drugs lenalidomide and pomalidomide inhibit multiple myeloma-induced osteoclast formation and the RANKL/OPG ratio in the myeloma microenvironment targeting the expression of adhesion molecules. Exp Hematol 41:387-397.
37. Möller C, T Strömberg, M Juremalm, K Nilsson and G Nilsson. (2003). Expression and function of chemokine receptors in human multiple myeloma. Leukemia 17:203-210.
38. Hjertner O, H Hjorth-Hansen, M Börset, C Seidel, A Waage and A Sundan. (2001). Bone morphogenetic protein-4 inhibits proliferation and induces apoptosis of multiple myeloma cells. Blood 97:516-522.
39. Wallace SR, MM Oken, KL Lunetta, A Panoskaltsis-Mortari and AM Masellis. (2001). Abnormalities of bone marrow mesenchymal cells in multiple myeloma patients. Cancer 91:1219-1230.
40. Arnulf B, S Lecourt, J Soulier, B Ternaux, MN Lacassagne, A Crinquette, J Dessoly, AK Sciaini, M Benbunan, et al. (2007). Phenotypic and functional characterization of bone marrow mesenchymal stem cells derived from patients with multiple myeloma. Leukemia 21:158-163.
41. Otjacques E, M Binsfeld, A Noel, Y Beguin, D Cataldo and J Caers. (2011). Biological aspects of angiogenesis in multiple myeloma. Int J Hematol 94:505-518.
42. Giuliani N, S Colla and V Rizzoli. (2004). Angiogenic switch in multiple myeloma. Hematology 9:377-381.
43. Corre J, B Hébraud and P Bourin. (2013). Concise review: growth differentiation factor 15 in pathology: a clinical role? Stem Cells Transl Med 2:946-952.
44. Ro TB, RU Holt, AT Brenne, H Hjorth-Hansen, A Sundan and M Borset. (2004). Bone morphogenetic protein-5,-6 and-7 inhibit growth and induce apoptosis in human myeloma cells. Oncogene 23:3024-3032.
45. Hose D, J Moreaux, T Meissner, A Seckinger, H Goldschmidt, A Benner, K Mahtouk, J Hillengass, T Rème, et al. (2009) Induction of angiogenesis by normal and malignant plasma cells. Blood 114:128-143.
46. Badrichani AZ, DM Stroka, G Bilbao, DT Curiel, FH Bach and C Ferran. (1999). Bcl-2 and Bcl-XL serve an antiinflammatory function in endothelial cells through inhibition of NF-kappaB. J Clin Invest 103:543-553.
47. Ma Y, X Hao, S Zhang and J Zhang. (2012). The in vitro and in vivo effects of human umbilical cord mesenchymal stem cells on the growth of breast cancer cells. Breast Cancer Res Treat 133:473-485.
48. Hsieh JY, HW Wang, SJ Chang, KH Liao, IH Lee, WS Lin, CH Wu, WY Lin and SM Cheng. (2013). Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS One 8:e72604.
49. Lepelletier Y, S Lecourt, A Renand, B Arnulf, V Vanneaux, JP Fernand, P Menasché, T Domet, JP Marolleau, O Hermine and J Larghero. (2010). Galectin-1, and semaphorine-3A are two soluble factors conferring T-cell immunosuppression to bone marrow mesenchymal stem cells. Stem Cell Dev 19: 1075-1079.
50. Huang YY, CH Peng, YP Yang, CC Wu, WM Hsu, HJ Wang, KH Chan, YP Chou, SJ Chen and YL Chang. (2007). Desipramine activated Bcl-2 expression and inhibited lipopolysaccharide-induced apoptosis in hippocampus-derived adult neural stem cells. J Pharmacol Sci 104:61-72.
51. Balda MS and K Matter. Tight junctions and the regulation of gene expression. (2009). Biochim Biophys Acta 1788: 761-767.
52. Brown AC, S Oddos, IM Dobbie, JM Alakoskela, RM Parton, P Eissmann, MA Neil, C Dunsby, PM French, I Davis and DM Davis. (2011). Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol 9:e1001152.
53. Bektas M and DS Rubenstein. (2011). The role of intracellular protein O-glycosylation in cell adhesion and disease. J Biomed Res 25:227-236.
54. Alpy F, A Rousseau, Y Schwab, F Legueux, I Stoll, C Wendling, C Spiegelhalter, P Kessler, C Mathelin, et al. 2013). STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER. J Cell Sci 126:5500-5512.
55. Knapek K, K Frondorf, J Post, S Short, D Cox and J Gomez-Cambronero. (2010). The molecular basis of phospholipase D2-induced chemotaxis: elucidation of differential pathways in macrophages and fibroblasts. Mol Cell Biol 30: 4492-4506.
56. Sartoris S, M Mazzocco, M Tinelli, M Martini, F Mosna, V Lisi, S Indraccolo, L Moserle, T Cestari, et al. (2011). Efficacy assessment of interferon-alpha-engineered mesenchymal stromal cells in a mouse plasmacytoma model. Stem Cells Dev 20:709-719.
57. Shah K. (2011). Mesenchymal stem cells engineered for cancer therapy. Adv Drug Deliv Rev 64:739-748.
58. Deuse T, M Stubbendorff, K Tang-Quan, N Phillips, MA Kay, T Eiermann, TT Phan, HD Volk, H Reichenspurner, RC Robbins and S Schrepfer. (2011). Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant 20:655-667.
59. Li L, S Liu, Y Xu, A Zhang, J Jiang, W Tan, J Xing, G Feng, H Liu, et al. (2013). Human umbilical cord-derived mesenchymal stem cells downregulate inflammatory responses by shifting the Treg/Th17 profile in experimental colitis. Pharmacology 92:257-264.
60. Tang Q, Q Chen, X Lai, S Liu, Y Chen, Z Zheng, Q Xie, M Maldonado, Z Cai, et al. (2013). Malignant transformation potentials of human umbilical cord mesenchymal stem cells both spontaneously and via 3-methycholanthrene induction. PLoS One 8:e81844.
61. Kim SM, JY Lim, SI Park, CH Jeong, JH Oh, M Jeong, et al. (2008). Gene therapy using TRAIL-secreting human umbilical cord blood-derived mesenchymal stem cells against intracranial glioma. Cancer Res 68:9614-9623.