Evaluation of alginate microspheres for mesenchymal stem cell engraftment on solid organ

Cell Transplantation

Volumn 19, Issue 12, 2010, Pages 1623-1633

  Trouche, E ^a   Girod Fullana, S ^b,c   Mias, C ^a   Ceccaldi, C ^b,c   Tortosa, F ^a,b   Seguelas, M H ^a   Calise, D ^a   Parini, A ^a,b   Cussac, D ^a,b   Sallerin, Brigitte ^a,b  

^a CHU RANGUEIL   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c INSTITUT CARNOT CIRIMAT   (France)

Author keywords

Alginate; Mesenchymal stem cells; Microspheres

Indexed keywords

ALGINIC ACID; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; MICROSPHERE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL THERAPY; CELL VIABILITY; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; KIDNEY CAPSULE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROENCAPSULATION; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; RAT; SCANNING ELECTRON MICROSCOPY; THERAPY EFFECT; WESTERN BLOTTING;

ALGINATES; ANIMALS; BIOCOMPATIBLE MATERIALS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; DRUG COMPOUNDING; GLUCURONIC ACID; HEXURONIC ACIDS; MATERIALS TESTING; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICROSPHERES; PARTICLE SIZE; RATS; RATS, INBRED LEW;

EID: 79951844985     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X514297     Document Type: Article

References (56)

1. Aggarwal, S.; Pittenger, M. F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4):1815-1822; 2005.
2. Amir, G.; Miller, L.; Shachar, M.; Feinberg, M. S.; Holbova, R.; Cohen, S.; Leor, J. Evaluation of a peritoneal-generated cardiac patch in a rat model of heterotopic heart transplantation. Cell Transplant. 18(3):275-282; 2009.
3. Bartkowiak, A.; Lisiecki, S.; Orive, G.; Pedraz, J. L. The effect of selected parameters of formation on properties of alginate/Ca2+/oligochitosan capsules. J. Chem. Technol. Biotechnol. 81(4):511-518; 2006.
4. Chen, H.; Ouyang, W.; Lawuyi, B.; Lim, T.; Prakash, S. A new method for microcapsule characterization: use of fluorogenic genipin to characterize polymeric microcapsule membranes. Appl. Biochem. Biotechnol. 134(3):207-222; 2006.
5. de Vos, P.; Bucko, M.; Gemeiner, P.; Navratil, M.; Svitel, J.; Faas, M.; Strand, B. L.; Skjak-Braek, G.; Morch, Y. A.; Vikartovska, A.; Lacik, I.; Kollarikova, G.; Orive, G.; Poncelet, D.; Pedraz, J. L.; Ansorge-Schumacher, M. B. Multiscale requirements for bioencapsulation in medicine and biotechnology. Biomaterials 30(13):2559-2570; 2009.
6. de Vos, P.; Hoogmoed, C. G.; Busscher, H. J. Chemistry and biocompatibility of alginate-PLL capsules for immunoprotection of mammalian cells. J. Biomed. Mater. Res. 60(2):252-259; 2002.
7. Di Nicola, M.; Carlo-Stella, C.; Magni, M.; Milanesi, M.; Longoni, P. D.; Matteucci, P.; Grisanti, S.; Gianni, A. M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99(10):3838-3843; 2002.
8. Dufrane, D.; Steenberghe, M.; Goebbels, R. M.; Saliez, A.; Guiot, Y.; Gianello, P. The influence of implantation site on the biocompatibility and survival of alginate encapsulated pig islets in rats. Biomaterials 27(17):3201-3208; 2006.
9. Efthimiadou, A.; Lambropoulou, M.; Pagonopoulou, O.; Vakalopoulos, I.; Papadopoulos, N.; Nikolettos, N. The role of basic-fibroblast growth factor (b-FGF) in cyclosporine-induced nephrotoxicity. In Vivo 20(2):265-269; 2006.
10. Goosen, M. F. A.; O'shea, G. M.; Gharapetian, H. M.; Chous, S.; Sun, A. M. Optimization of microencapsulation parameters: Semipermeable microcapsules as a bioartificial pancreas. Biotechnol. Bioeng. 27:146-150; 1985.
11. Grellier, M.; Granja, P. L.; Fricain, J. C.; Bidarra, S. J.; Renard, M.; Bareille, R.; Bourget, C.; Amedee, J.; Barbosa, M. A. The effect of the co-immobilization of human osteoprogenitors and endothelial cells within alginate microspheres on mineralization in a bone defect. Biomaterials 30(19):3271-3278; 2009.
12. Hauser, O.; Prieschl-Grassauer, E.; Salmons, B. Encapsulated, genetically modified cells producing in vivo therapeutics. Curr. Opin. Mol. Ther. 6(4):412-420; 2004.
13. Herzog, E. L.; Chai, L.; Krause, D. S. Plasticity of marrow-derived stem cells. Blood 102(10):3483-3493; 2003.
14. Hui, T. Y.; Cheung, K. M.; Cheung, W. L.; Chan, D.; Chan, B. P. In vitro chondrogenic differentiation of human mesenchymal stem cells in collagen microspheres: Influence of cell seeding density and collagen concentration. Biomaterials 29(22):3201-3212; 2008.
15. Kale, S.; Karihaloo, A.; Clark, P. R.; Kashgarian, M.; Krause, D. S.; Cantley, L. G. Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J. Clin. Invest. 112(1):42-49; 2003.
16. Keyser, K. A.; Beagles, K. E.; Kiem, H. P. Comparison of mesenchymal stem cells from different tissues to suppress T-cell activation. Cell Transplant. 16(5):555-562; 2007.
17. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein, S. E. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 94(5):678-685; 2004.
18. Kochupura, P. V.; Azeloglu, E. U.; Kelly, D. J.; Doronin, S. V.; Badylak, S. F.; Krukenkamp, I. B.; Cohen, I. S.; Gaudette, G. R. Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 112(9 Suppl.):I144-149; 2005.
19. Leal, D.; Matsuhiro, B.; Rossi, M.; Caruso, F. FT-IR spectra of alginic acid block fractions in three species of brown seaweeds. Carbohydr. Res. 343(2):308-316; 2008.
20. Lim, F.; Sun, A. M. Microencapsulated islets as bioartificial endocrine pancreas. Science 210(4472):908-910; 1980.
21. Lubiatowski, P.; Kruczynski, J.; Gradys, A.; Trzeciak, T.; Jaroszewski, J. Articular cartilage repair by means of biodegradable scaffolds. Transplant. Proc. 38(1):320-322; 2006.
22. Ma, H. L.; Chen, T. H.; Low-Tone Ho, L.; Hung, S. C. Neocartilage from human mesenchymal stem cells in alginate: Implied timing of transplantation. J. Biomed. Mater. Res. A 74(3):439-446; 2005.
23. Maurel, A.; Hernandez, C.; Kunduzova, O.; Bompart, G.; Cambon, C.; Parini, A.; Frances, B. Age-dependent increase in hydrogen peroxide production by cardiac monoamine oxidase A in rats. Am. J. Physiol. Heart Circ. Physiol. 284(4):H1460-1467; 2003.
24. Mias, C.; Lairez, O.; Trouche, E.; Roncalli, J.; Calise, D.; Seguelas, M. H.; Ordener, C.; Piercecchi-Marti, M. D.; Auge, N.; Salvayre, A. N.; Bourin, P.; Parini, A.; Cussac, D. Mesenchymal stem cells promote matrix metalloproteinase secretion by cardiac fibroblasts and reduce cardiac ventricular fibrosis after myocardial infarction. Stem Cells 27(11):2734-2743; 2009.
25. Mias, C.; Trouche, E.; Seguelas, M. H.; Calcagno, F.; Dignat-George, F.; Sabatier, F.; Piercecchi-Marti, M. D.; Daniel, L.; Bianchi, P.; Calise, D.; Bourin, P.; Parini, A.; Cussac, D. Ex vivo pretreatment with melatonin improves survival, proangiogenic/mitogenic activity, and efficiency of mesenchymal stem cells injected into ischemic kidney. Stem Cells 26(7):1749-1757; 2008.
26. Mironova, E. V.; Evstratova, A. A.; Antonov, S. M. A fluorescence vital assay for the recognition and quantification of excitotoxic cell death by necrosis and apoptosis using confocal microscopy on neurons in culture. J. Neurosci. Methods 163(1):1-8; 2007.
27. Moscoso, I.; Centeno, A.; Lopez, E.; Rodriguez-Barbosa, J. I.; Santamarina, I.; Filgueira, P.; Sanchez, M. J.; Dominguez-Perles, R.; Penuelas-Rivas, G.; Domenech, N. Differentiation "in vitro" of primary and immortalized porcine mesenchymal stem cells into cardiomyocytes for cell transplantation. Transplant. Proc. 37(1):481-482; 2005.
28. Moustafa, T.; Girod, S.; Tortosa, F.; Li, R.; Sol, J. C.; Rodriguez, F.; Bastide, R.; Lazorthes, Y.; Sallerin, B. Viability and functionality of bovine chromaffin cells encapsulated into alginate-PLL microcapsules with a liquefied inner core. Cell Transplant. 15(2):121-133; 2006.
29. Muller-Ehmsen, J.; Whittaker, P.; Kloner, R. A.; Dow, J. S.; Sakoda, T.; Long, T. I.; Laird, P. W.; Kedes, L. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J. Mol. Cell. Cardiol. 34(2):107-116; 2002.
30. Nasseri, B. A.; Kukucka, M.; Dandel, M.; Knosalla, C.; Potapov, E.; Lehmkuhl, H. B.; Meyer, R.; Ebell, W.; Stamm, C.; Hetzer, R. Intramyocardial delivery of bone marrow mononuclear cells and mechanical assist device implantation in patients with end-stage cardiomyopathy. Cell Transplant. 16(9):941-949; 2007.
31. Orive, G.; Hernandez, R. M.; Gascon, A. R.; Igartua, M.; Pedraz, J. L. Development and optimisation of alginate-PMCG-alginate microcapsules for cell immobilisation. Int. J. Pharm. 259(1-2):57-68; 2003.
32. Orive, G.; Ponce, S.; Hernandez, R. M.; Gascon, A. R.; Igartua, M.; Pedraz, J. L. Biocompatibility of microcapsules for cell immobilization elaborated with different type of alginates. Biomaterials 23(18):3825-3831; 2002.
33. Orive, G.; Tam, S. K.; Pedraz, J. L.; Halle, J. P. Biocompatibility of alginate-poly-L-lysine microcapsules for cell therapy. Biomaterials 27(20):3691-3700; 2006.
34. Piao, H.; Kwon, J. S.; Piao, S.; Sohn, J. H.; Lee, Y. S.; Bae, J. W.; Hwang, K. K.; Kim, D. W.; Jeon, O.; Kim, B. S.; Park, Y. B.; Cho, M. C. Effects of cardiac patches engineered with bone marrow-derived mononuclear cells and PGCL scaffolds in a rat myocardial infarction model. Biomaterials 28(4):641-649; 2007.
35. Ponce, S.; Orive, G.; Hernandez, R.; Gascon, A. R.; Pedraz, J. L.; de Haan, B. J.; Faas, M. M.; Mathieu, H. J.; de Vos, P. Chemistry and the biological response against immunoisolating alginate-polycation capsules of different composition. Biomaterials 27(28):4831-4839; 2006.
36. Poulsom, R.; Forbes, S. J.; Hodivala-Dilke, K.; Ryan, E.; Wyles, S.; Navaratnarasah, S.; Jeffery, R.; Hunt, T.; Alison, M.; Cook, T.; Pusey, C.; Wright, N. A. Bone marrow contributes to renal parenchymal turnover and regeneration. J. Pathol. 195(2):229-235; 2001.
37. Rajab, A.; Buss, J.; Diakoff, E.; Hadley, G. A.; Osei, K.; Ferguson, R. M. Comparison of the portal vein and kidney subcapsule as sites for primate islet autotransplantation. Cell Transplant. 17(9):1015-1023; 2008.
38. Reinecke, H.; Zhang, M.; Bartosek, T.; Murry, C. E. Survival, integration, and differentiation of cardiomyocyte grafts: A study in normal and injured rat hearts. Circulation 100(2):193-202; 1999.
39. Rosellini, E.; Cristallini, C.; Barbani, N.; Vozzi, G.; Giusti, P. Preparation and characterization of alginate/gelatin blend films for cardiac tissue engineering. J. Biomed. Mater. Res. A 91(2):447-453; 2009.
40. Shoichet, M. S.; Rein, D. H. In vivo biostability of a polymeric hollow fibre membrane for cell encapsulation. Biomaterials 17(3):285-290; 1996.
41. Silva, C. M.; Ribeiro, A. J.; Ferreira, D.; Veiga, F. Insulin encapsulation in reinforced alginate microspheres prepared by internal gelation. Eur. J. Pharm. Sci. 29(2):148-159; 2006.
42. Takagi, M.; Umetsu, Y.; Fujiwara, M.; Wakitani, S. High inoculation cell density could accelerate the differentiation of human bone marrow mesenchymal stem cells to chondrocyte cells. J. Biosci. Bioeng. 103(1):98-100; 2007.
43. Tam, S. K.; de Haan, B. J.; Faas, M. M.; Halle, J. P.; Yahia, L.; de Vos, P. Adsorption of human immunoglobulin to implantable alginate-poly-L-lysine microcapsules: Effect of microcapsule composition. J. Biomed. Mater. Res. A 89(3):609-615; 2009.
44. Tambara, K.; Sakakibara, Y.; Sakaguchi, G.; Lu, F.; Premaratne, G. U.; Lin, X.; Nishimura, K.; Komeda, M. Transplanted skeletal myoblasts can fully replace the infarcted myocardium when they survive in the host in large numbers. Circulation 108(Suppl. 1):II259-263; 2003.
45. Tanaka, H.; Matsumura, M.; Veliky, I. A. Diffusion characteristics of substrates in Ca-alginate gel beads. Biotechnol. Bioeng. 26(1):53-58; 1984.
46. Thanos, C. G.; Calafiore, R.; Basta, G.; Bintz, B. E.; Bell, W. J.; Hudak, J.; Vasconcellos, A.; Schneider, P.; Skinner, S. J.; Geaney, M.; Tan, P.; Elliot, R. B.; Tatnell, M.; Escobar, L.; Qian, H.; Mathiowitz, E.; Emerich, D. F. Formulating the alginate-polyornithine biocapsule for prolonged stability: Evaluation of composition and manufacturing technique. J. Biomed. Mater. Res. A 83(1):216-224; 2007.
47. Togel, F.; Weiss, K.; Yang, Y.; Hu, Z.; Zhang, P.; Westenfelder, C. Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am. J. Physiol. Renal Physiol. 292(5):F1626-1635; 2007.
48. Toma, C.; Pittenger, M. F.; Cahill, K. S.; Byrne, B. J.; Kessler, P. D. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105(1):93-98; 2002.
49. Tse, W. T.; Pendleton, J. D.; Beyer, W. M.; Egalka, M. C.; Guinan, E. C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: Implications in transplantation. Transplantation 75(3):389-397; 2003.
50. Uludag, H.; De Vos, P.; Tresco, P. A. Technology of mammalian cell encapsulation. Adv. Drug Deliv. Rev. 42(1-2):29-64; 2000.
51. Wei, H. J.; Chen, C. H.; Lee, W. Y.; Chiu, I.; Hwang, S. M.; Lin, W. W.; Huang, C. C.; Yeh, Y. C.; Chang, Y.; Sung, H. W. Bioengineered cardiac patch constructed from multilayered mesenchymal stem cells for myocardial repair. Biomaterials 29(26):3547-3556; 2008.
52. Wei, H. J.; Yang, H. H.; Chen, C. H.; Lin, W. W.; Chen, S. C.; Lai, P. H.; Chang, Y.; Sung, H. W. Gelatin microspheres encapsulated with a nonpeptide angiogenic agent, ginsenoside Rg1, for intramyocardial injection in a rat model with infarcted myocardium. J. Control. Release 120(1-2):27-34; 2007.
53. Wu, T. J.; Huang, H. H.; Hsu, Y. M.; Lyu, S. R.; Wang, Y. J. A novel method of encapsulating and cultivating adherent mammalian cells within collagen microcarriers. Biotechnol. Bioeng. 98(3):578-585; 2007.
54. Xiang, M. X.; He, A. N.; Wang, J. A.; Gui, C. Protective paracrine effect of mesenchymal stem cells on cardiomyocytes. J. Zhejiang Univ. Sci. B 10(8):619-624; 2009.
55. Xu, W.; Zhang, X.; Qian, H.; Zhu, W.; Sun, X.; Hu, J.; Zhou, H.; Chen, Y. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp. Biol. Med. (Maywood) 229(7): 623-631; 2004.
56. Zhang, H.; Zhu, S. J.; Wang, W.; Wei, Y. J.; Hu, S. S. Transplantation of microencapsulated genetically modified xenogeneic cells augments angiogenesis and improves heart function. Gene Ther. 15(1):40-48; 2008.