A specific subpopulation of mesenchymal stromal cell carriers overrides melanoma resistance to an oncolytic adenovirus

Stem Cells and Development

Volumn 21, Issue 14, 2012, Pages 2689-2702

  Bolontrade, Marcela F ^a,b   Sganga, Leonardo ^a,b   Piaggio, Eduardo ^a   Viale, Diego L ^a,f   Sorrentino, Miguel A ^c   Robinson, Anibal ^c   Sevlever, Gustavo ^d   Garcia, Mariana G ^b,e   Mazzolini, Guillermo ^b,e   Podhajcer, Osvaldo L ^a,b  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c Hospital Naval Pedro Mallo   (Argentina)

^d FLENI   (Argentina)

^e UNIVERSIDAD AUSTRAL   (Argentina)

^f UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; ALPHA3 INTEGRIN; ALPHA5 INTEGRIN; METALLOPROTEINASE; ONCOLYTIC ADENOVIRUS;

ARTICLE; BONE MARROW; BREAST CANCER; CANCER CELL CULTURE; CANCER RESISTANCE; CELL ADHESION; CELL ISOLATION; CELL MIGRATION; CELL STRAIN MCF 7; CELL SUBPOPULATION; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MELANOMA; MESENCHYMAL STROMA CELL; MULTIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ADENOVIRIDAE; ANIMALS; ANTINEOPLASTIC AGENTS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; CHONDROGENESIS; CULTURE MEDIA, CONDITIONED; HUMANS; INTEGRIN ALPHA CHAINS; MELANOMA; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, NUDE; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PHENANTHROLINES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

ADENOVIRIDAE; MUS;

EID: 84866252920     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0643     Document Type: Article

References (71)

1. Shirley D, D Marsh, G Jordan, S McQuaid and G Li. (2005). Systemic recruitment of osteoblastic cells in fracture healing. J Orthop Res 23:1013-1021. (Pubitemid 41245423)
2. Mori L, A Bellini, MA Stacey, M Schmidt and S Mattoli. (2005). Fibrocytes contribute to the myofibroblast population in wounded skin and originate from the bone marrow. Exp Cell Res 304:81-90. (Pubitemid 40222079)
3. Duncan AW, C Dorrell and M Grompe. (2009). Stem cells and liver regeneration. Gastroenterology 137:466-481.
4. Natsu K, M Ochi, Y Mochizuki, H Hachisuka, S Yanada and Y Yasunaga. (2004). Allogeneic bone marrow-derived mesenchymal stromal cells promote the regeneration of injured skeletal muscle without differentiation into myofibers. Tissue Eng 10:1093-1112. (Pubitemid 39223789)
5. Krupp S. (1976). [Transformation of monocytes into fibroblasts in wound healing (author's transl)]. Res Exp Med (Berl) 167:85-126.
6. Friedenstein AJ, S Piatetzky, II and KV Petrakova. (1966). Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 16:381-390.
7. Gao J, JE Dennis, RF Muzic, M Lundberg and AI Caplan. (2001). The dynamic in vivo distribution of bone marrowderived mesenchymal stem cells after infusion. Cells Tissues Organs 169:12-20. (Pubitemid 32437040)
8. Kyriakou C, N Rabin, A Pizzey, A Nathwani and K Yong. (2008). Factors that influence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model. Haematologica 93:1457-1465.
9. Francois S, M Bensidhoum, M Mouiseddine, C Mazurier, B Allenet, A Semont, J Frick, A Sache, S Bouchet, et al. (2006). 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 24:1020-1029. (Pubitemid 44464735)
10. Anderson DJ, FH Gage and IL Weissman. (2001). Can stem cells cross lineage boundaries? Nat Med 7:393-395. (Pubitemid 32298529)
11. Pevsner-Fischer M, S Levin and D Zipori. (2011). The origins of mesenchymal stromal cell heterogeneity. Stem Cell Rev 7:560-568.
12. Sethe S, A Scutt and A Stolzing. (2006). Aging of mesenchymal stem cells. Ageing Res Rev 5:91-116. (Pubitemid 43139669)
13. Aquino JB, MF Bolontrade, MG Garcia, OL Podhajcer and G Mazzolini. (2010). Mesenchymal stem cells as therapeutic tools and gene carriers in liver fibrosis and hepatocellular carcinoma. Gene Ther 17:692-708.
14. Phinney DG. (2007). Biochemical heterogeneity of mesenchymal stem cell populations: clues to their therapeutic efficacy. Cell Cycle 6:2884-2889.
15. McKenzie JL, K Takenaka, OI Gan, M Doedens and JE Dick. (2007). Low rhodamine 123 retention identifies long-term human hematopoietic stem cells within the Lin-CD34 + CD38-population. Blood 109:543-545. (Pubitemid 46105951)
16. Quirici N, D Soligo, P Bossolasco, F Servida, C Lumini and GL Deliliers. (2002). Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30:783-791. (Pubitemid 34835685)
17. Gronthos S, AC Zannettino, SJ Hay, S Shi, SE Graves, A Kortesidis and PJ Simmons. (2003). Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116:1827-1835. (Pubitemid 36582169)
18. Sacchetti B, A Funari, S Michienzi, S Di Cesare, S Piersanti, I Saggio, E Tagliafico, S Ferrari, PG Robey, M Riminucci and P Bianco. (2007). Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131:324-336. (Pubitemid 47592917)
19. Delorme B, J Ringe, N Gallay, Y Le Vern, D Kerboeuf, C Jorgensen, P Rosset, L Sensebe, P Layrolle, T Haupl and P Charbord. (2008). Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 111:2631-2635.
20. Digirolamo CM, D Stokes, D Colter, DG Phinney, R Class and DJ Prockop. (1999). Propagation and senescence of human marrow stromal cells in culture: a simple colonyforming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 107: 275-281. (Pubitemid 29530211)
21. Javazon EH, KJ Beggs and AW Flake. (2004). Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 32:414-425. (Pubitemid 38624325)
22. Studeny M, FC Marini, RE Champlin, C Zompetta, IJ Fidler and M Andreeff. (2002). Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res 62:3603-3608. (Pubitemid 34728832)
23. Klopp AH, EL Spaeth, JL Dembinski, WA Woodward, A Munshi, RE Meyn, JD Cox, M Andreeff and FC Marini. (2007). Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res 67:11687-11695.
24. Nakamura K, Y Ito, Y Kawano, K Kurozumi, M Kobune, H Tsuda, A Bizen, O Honmou, Y Niitsu and H Hamada. (2004). Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther 11:1155-1164. (Pubitemid 39117311)
25. Nakamizo A, F Marini, T Amano, A Khan, M Studeny, J Gumin, J Chen, S Hentschel, G Vecil, et al. (2005). Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 65:3307-3318. (Pubitemid 40524615)
26. Hung SC, WP Deng, WK Yang, RS Liu, CC Lee, TC Su, RJ Lin, DM Yang, CW Chang, et al. (2005). Mesenchymal stem cell targeting of microscopic tumors and tumor stroma development monitored by noninvasive in vivo positron emission tomography imaging. Clin Cancer Res 11:7749-7756. (Pubitemid 41611618)
27. Ren C, S Kumar, D Chanda, J Chen, JD Mountz and S Ponnazhagan. (2008). Therapeutic potential of mesenchymal stem cells producing interferon-alpha in a mouse melanoma lung metastasis model. Stem Cells 26:2332-2338.
28. Komarova S, J Roth, R Alvarez, DT Curiel and L Pereboeva. (2010). Targeting of mesenchymal stem cells to ovarian tumors via an artificial receptor. J Ovarian Res 3:12.
29. Jain RK. (1990). Physiological barriers to delivery of monoclonal antibodies and other macromolecules in tumors. Cancer Res 50:814s-819s.
30. Cairns R, I Papandreou and N Denko. (2006). Overcoming physiologic barriers to cancer treatment by molecularly targeting the tumor microenvironment. Mol Cancer Res 4:61-70.
31. McDonald DM and P Baluk. (2002). Significance of blood vessel leakiness in cancer. Cancer Res 62:5381-5385. (Pubitemid 35024617)
32. Lei Y, H Haider, J Shujia and ES Sim. (2004). Therapeutic angiogenesis. Devising new strategies based on past experiences. Basic Res Cardiol 99:121-132.
33. Smith J, RE Kontermann, J Embleton and S Kumar. (2005). Antibody phage display technologies with special reference to angiogenesis. FASEB J 19:331-341. (Pubitemid 40316521)
34. Muruve DA. (2004). The innate immune response to adenovirus vectors. Hum Gene Ther 15:1157-1166. (Pubitemid 40052429)
35. Ahmed AU, CE Rolle, MA Tyler, Y Han, S Sengupta, DA Wainwright, IV Balyasnikova, IV Ulasov and MS Lesniak. (2010). Bone marrow mesenchymal stem cells loaded with an oncolytic adenovirus suppress the anti-adenoviral immune response in the cotton rat model. Mol Ther 18:1846-1856.
36. Le Blanc K, C Tammik, K Rosendahl, E Zetterberg and O Ringden. (2003). HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31:890-896. (Pubitemid 37211373)
37. Aggarwal S and MF Pittenger. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815-1822. (Pubitemid 40223708)
38. Beyth S, Z Borovsky, D Mevorach, M Liebergall, Z Gazit, H Aslan, E Galun and J Rachmilewitz. (2005). Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105:2214-2219. (Pubitemid 40731815)
39. Corcione A, F Benvenuto, E Ferretti, D Giunti, V Cappiello, F Cazzanti, M Risso, F Gualandi, GL Mancardi, V Pistoia and A Uccelli. (2006). Human mesenchymal stem cells modulate B-cell functions. Blood 107:367-372. (Pubitemid 43053565)
40. Mader EK, Y Maeyama, Y Lin, GW Butler, HM Russell, E Galanis, SJ Russell, AB Dietz and KW Peng. (2009). Mesenchymal stem cell carriers protect oncolytic measles viruses from antibody neutralization in an orthotopic ovarian cancer therapy model. Clin Cancer Res 15:7246-7255.
41. Stoff-Khalili MA, AA Rivera, JM Mathis, NS Banerjee, AS Moon, A Hess, RP Rocconi, TM Numnum, M Everts, et al. (2007). Mesenchymal stem cells as a vehicle for targeted delivery of CRAds to lung metastases of breast carcinoma. Breast Cancer Res Treat 105:157-167. (Pubitemid 47366887)
42. Garcia-Castro J, R Alemany, M Cascallo, J Martinez-Quintanilla, M Arriero Mdel, A Lassaletta, L Madero and M Ramirez. (2010). Treatment of metastatic neuroblastoma with systemic oncolytic virotherapy delivered by autologous mesenchymal stem cells: an exploratory study. Cancer Gene Ther 17:476-483.
43. Dominici M, K Le Blanc, I Mueller, I Slaper-Cortenbach, F Marini, D Krause, R Deans, A Keating, D Prockop and E Horwitz. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317. (Pubitemid 44269669)
44. Potapova I, A Plotnikov, Z Lu, P Danilo, Jr., V Valiunas, J Qu, S Doronin, J Zuckerman, IN Shlapakova, et al. (2004). Human mesenchymal stem cells as a gene delivery system to create cardiac pacemakers. Circ Res 94:952-959. (Pubitemid 38490073)
45. Kim SH, HH Moon, HA Kim, KC Hwang, M Lee and D Choi. (2011). Hypoxia-inducible vascular endothelial growth factor-engineered mesenchymal stem cells prevent myocardial ischemic injury. Mol Ther 19:741-750.
46. Kumar S, TR Nagy and S Ponnazhagan. (2010). Therapeutic potential of genetically modified adult stem cells for osteopenia. Gene Ther 17:105-116.
47. Hodgkinson CP, JA Gomez, M Mirotsou and VJ Dzau. (2010). Genetic engineering of mesenchymal stem cells and its application in human disease therapy. Hum Gene Ther 21:1513-1526.
48. Barbash IM, P Chouraqui, J Baron, MS Feinberg, S Etzion, A Tessone, L Miller, E Guetta, D Zipori, et al. (2003). Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 108:863-868. (Pubitemid 37022130)
49. Nagaya N, T Fujii, T Iwase, H Ohgushi, T Itoh, M Uematsu, M Yamagishi, H Mori, K Kangawa and S Kitamura. (2004). Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 287:H2670-H2676. (Pubitemid 39557139)
50. Phinney DG and DJ Prockop. (2007). Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25:2896-2902. (Pubitemid 350127874)
51. Deschaseaux F, F Gindraux, R Saadi, L Obert, D Chalmers and P Herve. (2003). Direct selection of human bone marrow mesenchymal stem cells using an anti-CD49a antibody reveals their CD45med,low phenotype. Br J Haematol 122: 506-517. (Pubitemid 36951637)
52. Vogel W, F Grunebach, CA Messam, L Kanz, W Brugger and HJ Buhring. (2003). Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica 88:126-133. (Pubitemid 37101490)
53. Buhring HJ, VL Battula, S Treml, B Schewe, L Kanz and W Vogel. (2007). Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 1106:262-271. (Pubitemid 47443036)
54. Sorrentino A, M Ferracin, G Castelli, M Biffoni, G Tomaselli, M Baiocchi, A Fatica, M Negrini, C Peschle and M Valtieri. (2008). Isolation and characterization of CD146 + multipotent mesenchymal stromal cells. Exp Hematol 36:1035-1046.
55. Spaeth E, A Klopp, J Dembinski, M Andreeff and F Marini. (2008). Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther 15:730-738. (Pubitemid 351627356)
56. Ley K, C Laudanna, MI Cybulsky and S Nourshargh. (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7:678-689. (Pubitemid 47327397)
57. Ruster B, S Gottig, RJ Ludwig, R Bistrian, S Muller, E Seifried, J Gille and R Henschler. (2006). Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 108:3938-3944. (Pubitemid 44864580)
58. Veevers-Lowe J, SG Ball, A Shuttleworth and CM Kielty. (2011). Mesenchymal stem cell migration is regulated by fibronectin through alpha5beta1-integrin-mediated activation of PDGFR-beta and potentiation of growth factor signals. J Cell Sci 124:1288-1300.
59. Guo HB, I Lee, M Kamar, SK Akiyama and M Pierce. (2002). Aberrant N-glycosylation of beta1 integrin causes reduced alpha5beta1 integrin clustering and stimulates cell migration. Cancer Res 62:6837-6845. (Pubitemid 35424070)
60. Steingen C, F Brenig, L Baumgartner, J Schmidt, A Schmidt and W Bloch. (2008). Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J Mol Cell Cardiol 44:1072-1084.
61. Mueller MM and NE Fusenig. (2004). Friends or foes-bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4:839-849. (Pubitemid 39472951)
62. Garcia MG, J Bayo, MF Bolontrade, L Sganga, M Malvicini, L Alaniz, JB Aquino, E Fiore, MM Rizzo, et al. (2011). Hepatocellular carcinoma cells and their fibrotic microenvironment modulate bone marrow-derived mesenchymal stromal cell migration in vitro and in vivo. Mol Pharm 8:1538-1548.
63. Schrepfer S, T Deuse, H Reichenspurner, MP Fischbein, RC Robbins and MP Pelletier. (2007). Stem cell transplantation: the lung barrier. Transplant Proc 39:573-576. (Pubitemid 46386222)
64. Parato KA, D Senger, PA Forsyth and JC Bell. (2005). Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer 5:965-976. (Pubitemid 41766784)
65. Eager RM and J Nemunaitis. (2011). Clinical development directions in oncolytic viral therapy. Cancer Gene Ther 18:305-317.
66. Stohrer M, Y Boucher, M Stangassinger and RK Jain. (2000). Oncotic pressure in solid tumors is elevated. Cancer Res 60:4251-4255. (Pubitemid 30636613)
67. Lopez MV, DL Viale, EG Cafferata, AI Bravo, C Carbone, D Gould, Y Chernajovsky and OL Podhajcer. (2009). Tumor associated stromal cells play a critical role on the outcome of the oncolytic efficacy of conditionally replicative adenoviruses. PLoS One 4:e5119.
68. Yang JT, BL Bader, JA Kreidberg, M Ullman-Cullere, JE Trevithick and RO Hynes. (1999). Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. Dev Biol 215:264-277.
69. Wolf K, I Mazo, H Leung, K Engelke, UH von Andrian, EI Deryugina, AY Strongin, EB Brocker and P Friedl. (2003). Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160:267-277. (Pubitemid 36254960)
70. Kitsiou PV, AK Tzinia, WG Stetler-Stevenson, AF Michael, WW Fan, B Zhou and EC Tsilibary. (2003). Glucose-induced changes in integrins and matrix-related functions in cultured human glomerular epithelial cells. Am J Physiol Renal Physiol 284:F671-F679. (Pubitemid 36336973)
71. Weissman IL. (2000). Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157-168. (Pubitemid 30046304)