Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: A new approach for drug delivery

Journal of Controlled Release

Volumn 192, Issue , 2014, Pages 262-270

  Pascucci, Luisa ^a   Coccè, Valentina ^b   Bonomi, Arianna ^b   Ami, Diletta ^c   Ceccarelli, Piero ^a   Ciusani, Emilio ^e   Viganò, Lucia ^d   Locatelli, Alberta ^d   Sisto, Francesca ^b   Doglia, Silvia Maria ^c   Parati, Eugenio ^e   Bernardo, Maria Ester ^f   Muraca, Maurizio ^f   Alessandri, Giulio ^e   Bondiolotti, Gianpietro ^b   Pessina, Augusto ^b  

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e DEPARTMENT OF NEUROSURGERY   (Italy)

^f BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

Author keywords

Drug delivery; Exosome; Mesenchymal stromal cells; Microvesicles; Paclitaxel

Indexed keywords

ABSORPTION SPECTROSCOPY; CELLS; DRUG DELIVERY; FLOWCHARTING; FOURIER TRANSFORM INFRARED SPECTROSCOPY; SCANNING ELECTRON MICROSCOPY; TUMORS;

ANTI-PROLIFERATIVE ACTIVITIES; ANTI-TUMOR ACTIVITIES; EXOSOME; MESENCHYMAL STROMAL CELLS; MICROVESICLES; PACLITAXEL; PANCREATIC CELL LINES; TUMOR MICROENVIRONMENT; EXOSOMES; IN-VITRO; NEW APPROACHES; TUMOR GROWTH;

CELL CULTURE; DRUG DELIVERY;

PACLITAXEL; ANTINEOPLASTIC AGENT;

ABSORPTION SPECTROSCOPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CELL ISOLATION; CELL VACUOLE; CULTURE MEDIUM; DRUG DELIVERY SYSTEM; DRUG RELEASE; EXOSOME; FOURIER TRANSFORM INFRARED PHOTOACOUSTIC SPECTROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; SCANNING TRANSMISSION ELECTRON MICROSCOPY; TARGET CELL; TRANSMISSION ELECTRON MICROSCOPY; TUMOR GROWTH; ULTRACENTRIFUGATION; ANIMAL; CELL LINE; CYTOLOGY; METABOLISM; NEOPLASMS; PATHOLOGY; PROCEDURES; TUMOR CELL LINE; ANIMAL CELL; CONTROLLED STUDY; INFRARED SPECTROSCOPY; PANCREAS ADENOCARCINOMA; SCANNING ELECTRON MICROSCOPY; TUMOR MICROENVIRONMENT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; EXOSOMES; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; NEOPLASMS; PACLITAXEL;

EID: 84907228576     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.07.042     Document Type: Article

References (54)

1. M.R. Loebinger, and S.M. Janes Stem cells as vectors for antitumour therapy Thorax 65 2010 362 369
2. L.G. Menon, V.J. Shi, and R.S. Carroll Mesenchymal stromal cells as a drug delivery system The Stem Cell Research Community StemBook 2009 10.3824/stembook.1.35.1.C
3. Belmar-Lopez, G. Mendoza, D. Oberg, J. Burnet, C. Simon, I. Cervello, M. Iglesias, Juan C. Ramirez, P. Lopez-Larrubia, M. Quintanilla, and P. Martin-Duque Tissue-derived mesenchymal stromal cells used as vehicles for anti-tumor therapy exert different in vivo effects on migration capacity and tumor growth BMC Med. 139 2013 10.1186/1741-7015-11-139
4. K. Shah Mesenchymal stem cells engineered for cancer therapy Adv. Drug Deliv. Rev. 64 2012 739 748
5. D. Gjorgieva, N. Zaidman, and D. Bosnakovsk Mesenchymal stem cells for anti-cancer drug delivery Recent Pat. Anticancer Drug Discov. 8 2013 310 318
6. A. Ebrahimi, and N. Lalvand Drug delivery using genetically modified mesenchymal stem cells: a promising targeted-delivery method Hygeia J. Drugs Med. 5 2013 90 104
7. A. Pessina, A. Bonomi, V. Coccè, G. Invernici, S. Navone, L. Cavicchini, F. Sisto, M. Ferrari, L. Viganò, A. Locatelli, E. Ciusani, G. Cappelletti, D. Cartelli, C. Arnaldo, E. Parati, G. Marfia, R. Pallini, M.L. Falchetti, and G. Alessandri Mesenchymal stromal cells primed with paclitaxel provide a new approach for cancer therapy PLoS One 6 2011 e28321
8. A. Pessina, V. Coccè, L. Pascucci, A. Bonomi, L. Cavicchini, F. Sisto, M. Ferrari, E. ciusani, A. Crovace, M.L. Falchetti, S. Zicari, A. Caruso, S. Navone, G. Marfia, A. Benetti, P. Ceccarelli, E. Parati, and G. Alessandri Mesenchymal stromal cells primed with Paclitaxel attract and kill leukaemia cells, inhibit angiogenesis and improve survival of leukaemia-bearing mice Br. J. Haematol. 160 2013 766 778 10.1111/bjh.12196
9. A. Bonomi, V. Coccè, L. Cavicchini, F. Sisto, M. Dossena, P. Balzarini, N. Portolani, E. ciusani, E. Parati, G. Alessandri, and A. Pessina Adipose tissue-derived stromal cells primed in vitro with paclitaxel acquire anti-tumor activity Int. J. Immunopathol. Pharmacol. 26 2013 33 41
10. A. Pessina, V. Coccè, A. Bonomi, L. Cavicchini, F. Sisto, M. Ferrari, E. Ciusani, S. Navone, G. Marfia, E. Parati, and G. Alessandri Human skin-derived fibroblasts acquire in vitro anti-tumor potential after priming with Paclitaxel Anticancer Agents Med. Chem. 13 2013 523 530
11. A. Scanu, N. Molnarfi, K.J. Brandt, L. Gruaz, J.M. Dayer, and D. Burger Stimulated T cells generate microparticles, which mimic cellular contact activation of human monocytes: differential regulation of pro- and anti-inflammatory cytokine production by high-density lipoproteins J. Leukoc. Biol. 83 2008 921 992
12. B. Hugel, M.C. Martinez, C. Kunzelmann, and J.M. Freyssinet Membrane microparticles: two sides of the coin Physiology 20 2005 22 27 (Pubitemid 40363367)
13. J. Ratajczak, M. Wysoczynski, F. Hayek, A. Janowska-Wieczorek, and M.Z. Ratajczak Membrane derived microvesicles: important and underappreciated mediators of cell-to-cell communication Leukemia 20 2006 1487 1495 (Pubitemid 44264090)
14. S. Bruno, C. Grange, M.C. Deregibus, R.A. Calogero, S. Saviozzi, F. Collino, L. Morando, A. Busca, M. Falda, B. Bussolati, C. Tetta, and G. Camussi Mesenchymal stem cell-derived microvesicles protect against acute tubular injury J. Am. Soc. Nephrol. 20 2009 1053 1067
15. S.M. van Dommelen, P. Vader, S. Lakhal, W.W. van Solinge, M.J.A. Wood, and R.M. Schiffelers Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery J. Control. Release 161 2012 635 644
16. R.C. Lai, R.W. Yeo, K.H. Tan, and S.K. Lim Exosomes for drug delivery - a novel application for the mesenchymal stem cell Biotechnol. Adv. 31 2013 543 551 10.1016/j.biotechadv.2012.08.008
17. P. Rameshwar Mesenchymal stem cells can be a conduit for the delivery of therapeutic MicroRNA J. Stem Cell Res. Ther. 3 2013 e112 10.4172/2157-7633. 1000e112
18. H.O. Kim, S.M. Choi, and H.S. Kim Mesenchymal stem cell-derived secretome and microvesicles as a cell-free therapeutics for neurodegenerative disorders Tissue Eng. Regen. Med. 10 2013 93 101 10.1007/s13770-013-0010-7
19. C. Tetta, S. Bruno, V. Fonsato, M.C. Deregibus, and G. Camussi The role of microvesicles in tissue repair Organogenesis 7 2011 105 115
20. A.H. Klopp, A. Gupta, E. Spaeth, M. Andreeff, and F. Marini Concise review: dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29 2011 11 19
21. S. Bruno, F. Collino, M.C. Deregibus, C. Grange, C. Tetta, and G. Camussi Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth Stem Cells Dev. 22 2013 758 771 10.1089/scd.2012.0304
22. A.M. Roccaro, A. Sacco, P. Maiso, A.K. Azab, Y.T. Tai, M. Reagan, F. Azab, L.M. Flores, F. Campigotto, E. Weller, K.C. Anderson, D.T. Scadden, and I.M. Ghobrial BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression J. Clin. Invest. 123 2013 1542 1555
23. R.M. Hoffman Stromal-cell and cancer-cell exosomes leading the metastatic exodus for the promised niche Breast Cancer Res. 15 2013 310
24. B. Shen, N. Wu, J.M. Yang, and S.J. Gould Protein targeting to exosomes/microvesicles by plasma membrane anchors J. Biol. Chem. 286 2011 14383 14395
25. J.C. McIntosh, R.A. Schoumacher, and R.E. Tiller Pancreatic adenocarcinoma in a patient with cystic fibrosis Am. J. Med. 85 1988 592
26. R.A. Schoumacher, J. Ram, M.C. Iannuzzi, N.A. Bradbury, R.W. Wallace, C.T. Hon, D.R. Kelly, S.M. Schmid, F.B. Gelder, and T.A. Rado A cystic fibrosis pancreatic adenocarcinoma cell line Proc. Natl. Acad. Sci. U. S. A. 87 1990 4012 4016
27. A. Pessina, E. Mineo, M.G. Neri, L. Gribaldo, R. Colombi, P. Brambilla, and G. Zaleskis Establishment and characterization of a new murine cell line (SR-4987) derived from marrow stromal cells Cytotechnology 8 1992 93 102
28. A. Pessina, M.G. Neri, E. Mineo, M. Piccirillo, L. Gribaldo, P. Brambilla, G. Zaleskis, and P. Ujhazy Expression of B cell markers on SR-4987 cells derived from murine marrow stroma Exp. Hematol. 25 1997 536 541 (Pubitemid 27293517)
29. A. Pessina, F. Sisto, V. Coccè, L. Cavicchini, E. Ciusani, L. Gribaldo, and A. Bonomi Mesenchymal stromal cell line resistant to paclitaxel that spontaneously differentiates into osteoblast-like cells Cell Biol. Toxicol. 27 2011 169 180
30. T. Mossman Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. Methods 65 1983 55 63
31. L. Gianni, C.M. Kearns, A. Giani, G. Capri, L. Viganò, A. Locatelli, G. Bonadonna, and M.J. Egorin Nonlinear pharmacokinetic of paclitaxel and its pharmacokinetic/pharmacodynamic relationships in humans J. Clin. Oncol. 13 1995 180 190
32. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with folin phenol reagent J. Biol. Chem. 193 1951 265
33. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J.J. Lee, and J.O. Lötvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 9 2007 654 659 (Pubitemid 47214727)
34. L.J. Reed, and H. Muench A simple method of estimating fifty percent endpoints Am. J. Hyg. 27 1938 493 497
35. M.F. Hayat Principles and Techniques of Electron Microscopy: Biological Applications 4th edition 2000 Cambridge University Press
36. A. Natalello, A.M. Frana, A. Relini, A. Apicella, G. Invernizzi, C. Casari, A. Gliozzi, S.M. Doglia, P. Tortora, and M.E. Regonesi A major role for side-chain polyglutamine hydrogen bonding in irreversible Ataxin-3 aggregation PLoS One 6 2011 e18789
37. E. Goormaghtigh, V. Raussens, and J.M. Ruysschaert Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes Biochim. Biophys. Acta 1422 1999 105 185 (Pubitemid 29313327)
38. K. Paál, J. Müller, and L. Hegedûs High affinity binding of paclitaxel to human serum albumin Eur. J. Biochem. 268 2001 2187 2191 (Pubitemid 32852961)
39. G. Kumar, S. Ray, T. Walle, Y. Huang, M. Willingham, S. Self, and K. Bhalla Comparative in vitro cytotoxic effects of taxol and its major human metabolite 6 alphahydroxytaxol Cancer Chemother. Pharmacol. 36 1995 129 135
40. A.M.C. Yvon, P. Wadsworth, and M.A. Jordan Taxol suppresses dynamics of individual microtubules in living human tumor cells Mol. Biol. Cell 10 1999 947 959 (Pubitemid 29193723)
41. D. Ami, A. Natalello, and S.M. Doglia Fourier transform infrared microspectroscopy of complex biological systems: from intact cells to whole organisms Methods Mol. Biol. 895 2012 85 100
42. L.K. Tamm, and S.A. Tatulian Infrared spectroscopy of proteins and peptides in lipid bilayers Q. Rev. Biophys. 30 1997 365 429 (Pubitemid 28260614)
43. B.A. Weaver, and D.W. Cleveland Decoding the links between mitosis, cancer, and chemotherapy: the mitotic checkpoint, adaptation, and cell death Cancer Cell 8 1 2005 7 12 (Pubitemid 40991810)
44. Y. Wang, J. Liu, J. Zhang, L. Wang, J. Chan, H. Wang, Y. Jin, L. Yu, D.W. Grainger, and W. Ying A cell-based pharmacokinetics assay for evaluating tubulin-binding drugs Int. J. Med. Sci. 11 2014 479 487
45. R.A. Veldhoen, S.L. Banman, D.R. Hemmerling, R. Odsen, T. Simmen, A.J. Simmonds, D.A. Underhill, and I.S. Goping The chemotherapeutic agent paclitaxel inhibits autophagy through two distinct mechanisms that regulate apoptosis Oncogene 32 6 2013 736 746
46. G.E. Palade, and P. Siekevitz Liver microsomes; an integrated morphological and biochemical study J. Biophys. Biochem. Cytol. 25 1956 171 200
47. Y. Fang, N. Wu, X. Gan, W. Yan, J.C. Morrell, and S.J. Gould Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes PLoS Biol. 5 2007 e158
48. D.H. Hsu, P. Paz, G. Villaflor, A. Rivas, A. Mehta-Damani, E. Angevin, L. Zitvogel, and J.B. Le Pecq Exosomes as a tumor vaccine: enhancing potency through direct loading of antigenic peptides J. Immunother. 26 2003 440 450 (Pubitemid 37128556)
49. K.R. Qazi, U. Gehrmann, E. Domange Jordo, M.C. Karlsson, and S. Gabrielsson Antigen-loaded exosomes alone induce Th1-type memory through a B-cell-dependent mechanism Blood 113 2009 2673 2683
50. A. Janowska-Wieczorek, M. Wysoczynski, J. Kijowski, L. Marquez-Curtis, B. Machalinski, J. Ratajczak, and M.Z. Ratajczak Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int. J. Cancer 113 2005 752 760 (Pubitemid 40101256)
51. M. Hulsmans, and P. Holvoet MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease Cardiovasc. Res. 2013 10.1093/cvr/cvt161
52. J.Y. Jang, J.K. Lee, Y.K. Jeon, and C.W. Kim Exosome derived from epigallocatechin gallate treated breast cancer cells suppresses tumor growth by inhibiting tumor-associated macrophage infiltration and M2 polarization BMC Cancer 13 2013 421
53. J. Skog, T. Wurdinger, S. Van Rijn, D.H. Meijer, L. Gainche, M. Sena-Esteves, W.T. Curry Jr., B.S. Carter, A.M. Krichevsky, and X.O. Breakefield Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat. Cell Biol. 10 2008 1470 1476
54. G. Rabinowits, C. Gerçel-Taylor, J.M. Day, D.D. Taylor, and G.H. Kloecker Exosomal microRNA: a diagnostic marker for lung cancer Clin. Lung Cancer 10 2009 42 46 10.3816/CLC.2009.n.006