Utilizing cell-matrix interactions to modulate gene transfer to stem cells inside hyaluronic acid hydrogels

Molecular Pharmaceutics

Volumn 8, Issue 5, 2011, Pages 1582-1591

  Gojgini, Shiva ^a   Tokatlian, Talar ^a   Segura, Tatiana ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

hyaluronic acid; hydrogel scaffolds; mesenchymal stem cell; nonviral gene delivery; poly(ethylene imine)

Indexed keywords

AMINO ACID; ARGINYLGLYCYLASPARAGINE; DNA; HYALURONIC ACID; MATRIX METALLOPROTEINASE; PHOSPHATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SPREADING; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE TRANSFER; HYDROGEL; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL;

ACRYLATES; ADULT STEM CELLS; ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; CELL-MATRIX JUNCTIONS; CLONE CELLS; CROSS-LINKING REAGENTS; EXTRACELLULAR MATRIX; GENE TRANSFER TECHNIQUES; HYALURONIC ACID; HYDROGELS; MATRIX METALLOPROTEINASES; MECHANICAL PHENOMENA; MESENCHYMAL STEM CELLS; MICE; NANOPARTICLES; OLIGOPEPTIDES; PHYSICOCHEMICAL PHENOMENA; PLASMIDS; POLYETHYLENEIMINE; TRANSGENES;

EID: 80053540036     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp200171d     Document Type: Article

References (52)

1. Kleinman, H. K.; Philp, D.; Hoffman, M. P. Role of the extracellular matrix in morphogenesis Curr. Opin. Biotechnol. 2003, 14 (5) 526-32 (Pubitemid 37298039)
2. Bottaro, D. P.; Liebmann-Vinson, A.; Heidaran, M. A. Molecular signaling in bioengineered tissue microenvironments Ann. N.Y. Acad. Sci. 2002, 961, 143-53 (Pubitemid 34721758)
3. Fraser, J. R.; Laurent, T. C.; Laurent, U. B. Hyaluronan: its nature, distribution, functions and turnover J. Int. Med. 1997, 242 (1) 27-33 (Pubitemid 27323862)
4. Leach, J. B.; Bivens, K. A.; Patrick, C. W.; Schmidt, C. E. Photocrosslinked hyaluronic acid hydrogels: Natural, biodegradable tissue engineering scaffolds Biotechnol. Bioeng. 2003, 82 (5) 578-589 (Pubitemid 36514267)
5. Park, Y. D.; Tirelli, N.; Hubbell, J. A. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks Biomaterials 2003, 24 (6) 893-900 (Pubitemid 36024167)
6. Shu, X. Z.; Liu, Y. C.; Palumbo, F. S.; Lu, Y.; Prestwich, G. D. In situ cross linkable hyaluronan hydrogels for tissue engineering Biomaterials 2004, 25 (7-8) 1339-1348 (Pubitemid 37476210)
7. Yeo, Y.; Highley, C. B.; Bellas, E.; Ito, T.; Marini, R.; Langer, R.; Kohane, D. S. In situ cross-linkable hyaluronic acid hydrogels prevent post-operative abdominal adhesions in a rabbit model Biomaterials 2006, 27 (27) 4698-705 (Pubitemid 43870121)
8. Chung, C.; Burdick, J. A. Influence of Three-Dimensional Hyaluronic Acid Microenvironments on Mesenchymal Stem Cell Chondrogenesis Tissue Eng., Part A 2009, 15 (2) 243-254
9. Gerecht, S.; Burdick, J. A.; Ferreira, L. S.; Townsend, S. A.; Langer, R.; Vunjak-Novakovic, G. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (27) 11298-303 (Pubitemid 47175135)
10. Kim, J.; Park, Y.; Tae, G.; Lee, K. B.; Hwang, C. M.; Hwang, S. J.; Kim, I. S.; Noh, I.; Sun, K. Characterization of low-molecular-weight hyaluronic acid-based hydrogel and differential stem cell responses in the hydrogel microenvironments J. Biomed. Mater. Res., Part A 2009, 88A (4) 967-975
11. Kim, J.; Park, Y.; Tae, G.; Lee, K. B.; Hwang, S. J.; Kim, I. S.; Noh, I.; Sun, K. Synthesis and characterization of matrix metalloprotease sensitive-low molecular weight hyaluronic acid based hydrogels J. Mater. Sci.: Mater. Med. 2008, 19 (11) 3311-3318
12. Pan, L. J.; Ren, Y. J.; Cui, F. Z.; Xu, Q. Y. Viability and Differentiation of Neural Precursors on Hyaluronic Acid Hydrogel Scaffold J. Neurosci. Res. 2009, 87 (14) 3207-3220
13. Aruffo, A.; Stamenkovic, I.; Melnick, M.; Underhill, C. B.; Seed, B. CD44 is the principal cell surface receptor for hyaluronate Cell 1990, 61 (7) 1303-13
14. Sherman, L.; Sleeman, J.; Herrlich, P.; Ponta, H. Hyaluronate Receptors-Key Players in Growth, Differentiation, Migration and Tumor Progression Curr. Opin. Cell Biol. 1994, 6 (5) 726-733 (Pubitemid 24295307)
15. Lei, Y.; Gojgini, S.; Lam, J.; Segura, T. The spreading, migration and proliferation of mouse mesenchymal stem cells cultured inside hyaluronic acid hydrogels Biomaterials 2011, 32 (1) 39-47
16. Bonadio, J.; Smiley, E.; Patil, P.; Goldstein, S. Localized, direct plasmid gene delivery in vivo: prolonged therapy results in reproducible tissue regeneration Nat. Med. 1999, 5 (7) 753-9 (Pubitemid 29318608)
17. Chun, K. W.; Lee, J. B.; Kim, S. H.; Park, T. G. Controlled release of plasmid DNA from photo-cross-linked pluronic hydrogels Biomaterials 2005, 26 (16) 3319-3326 (Pubitemid 39647264)
18. Quick, D. J.; Anseth, K. S. DNA delivery from photocrosslinked PEG hydrogels: encapsulation efficiency, release profiles, and DNA quality J. Controlled Release 2004, 96 (2) 341-351 (Pubitemid 38481514)
19. Kong, H. J.; Kim, E. S.; Huang, Y. C.; Mooney, D. J. Design of biodegradable hydrogel for the local and sustained delivery of angiogenic plasmid DNA Pharm. Res. 2008, 25 (5) 1230-1238
20. Kasper, F. K.; Jerkins, E.; Tanahashi, K.; Barry, M. A.; Tabata, Y.; Mikos, A. G. Characterization of DNA release from composites of oligo(poly(ethylene glycol) fumarate) and cationized gelatin microspheres in vitro J. Biomed. Mater. Res., Part A 2006, 78A (4) 823-835 (Pubitemid 44300036)
21. Megeed, Z.; Haider, M.; Li, D.; O'Malley, B. W., Jr.; Cappello, J.; Ghandehari, H. In vitro and in vivo evaluation of recombinant silk-elastinlike hydrogels for cancer gene therapy J. Controlled Release 2004, 94 (2-3) 433-45 (Pubitemid 38117153)
22. Jang, J. H.; Rives, C. B.; Shea, L. D. Plasmid delivery in vivo from porous tissue-engineering scaffolds: transgene expression and cellular transfection Mol. Ther. 2005, 12 (3) 475-83 (Pubitemid 41150133)
23. Lei, P.; Padmashali, R. M.; Andreadis, S. T. Cell-controlled and spatially arrayed gene delivery from fibrin hydrogels Biomaterials 2009, 30 (22) 3790-3799
24. Wieland, J. A.; Houchin-Ray, T. L.; Shea, L. D. Non-viral vector delivery from PEG-hyaluronic acid hydrogels J. Controlled Release 2007, 120 (3) 233-241 (Pubitemid 47058636)
25. Saul, J. M.; Linnes, M. P.; Ratner, B. D.; Giachelli, C. M.; Pun, S. H. Delivery of non-viral gene carriers from sphere-templated fibrin scaffolds for sustained transgene expression Biomaterials 2007, 28 (31) 4705-4716 (Pubitemid 47260703)
26. Trentin, D.; Hall, H.; Wechsler, S.; Hubbell, J. A. Peptide-matrix- mediated gene transfer of an oxygen-insensitive hypoxia-inducible factor-1 alpha variant for local induction of angiogenesis Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (8) 2506-2511
27. Trentin, D.; Hubbell, J.; Hall, H. Non-viral gene delivery for local and controlled DNA release J. Controlled Release 2005, 102 (1) 263-275 (Pubitemid 40093791)
28. Kong, H. J.; Liu, J.; Riddle, K.; Matsumoto, T.; Leach, K.; Mooney, D. J. Non-viral gene delivery regulated by stiffness of cell adhesion substrates Nat. Mater. 2005, 4 (6) 460-4 (Pubitemid 40774051)
29. Kong, H. J.; Hsiong, S.; Mooney, D. J. Nanoscale cell adhesion ligand presentation regulates nonviral gene delivery and expression Nano Lett. 2007, 7 (1) 161-6 (Pubitemid 46225846)
30. Shepard, J. A.; Huang, A.; Shikanov, A.; Shea, L. D. Balancing cell migration with matrix degradation enhances gene delivery to cells cultured three-dimensionally within hydrogels J. Controlled Release 2010, 146 (1) 128-35
31. Lei, Y. G.; Segura, T. DNA delivery from matrix metal lop roteinase degradable poly(ethylene glycol) hydrogels to mouse cloned mesenchymal stem cells Biomaterials 2009, 30 (2) 254-265
32. Lungwitz, U.; Breunig, M.; Blunk, T.; Gopferich, A. Polyethylenimine- based non-viral gene delivery systems Eur. J. Pharm. Biopharm. 2005, 60 (2) 247-266 (Pubitemid 40804565)
33. Abdallah, B.; Hassan, A.; Benoist, C.; Goula, D.; Behr, J. P.; Demeneix, B. A. A powerful nonviral vector for in vivo gene transfer into the adult mammalian brain: Polyethylenimine Hum. Gene Ther. 1996, 7 (16) 1947-1954 (Pubitemid 26390233)
34. Wang, S.; Ma, N.; Gao, S. J.; Yu, H.; Leong, K. W. Transgene expression in the brain stem effected by intramuscular injection of polyethylenimine/DNA complexes Mol. Ther. 2001, 3 (5) 658-664 (Pubitemid 32509862)
35. Wiseman, J. W.; Goddard, C. A.; McLelland, D.; Colledge, W. H. A comparison of linear and branched polyethylenimine (PEI) with DCChol/DOPE liposomes for gene delivery to epithelial cells in vitro and in vivo Gene Ther. 2003, 10 (19) 1654-1662 (Pubitemid 37069493)
36. Kichler, A.; Chillon, M.; Leborgne, C.; Danos, O.; Frisch, B. Intranasal gene delivery with a polyethylenimine-PEG conjugate J. Controlled Release 2002, 81 (3) 379-388 (Pubitemid 34607157)
37. Rudolph, C.; Schillinger, U.; Plank, C.; Gessner, A.; Nicklaus, P.; Muller, R. H.; Rosenecker, J. Nonviral gene delivery to the lung with copolymer-protected and transferrin-modified polyethylenimine Biochim. Biophys. Acta 2002, 1573 (1) 75-83 (Pubitemid 35279791)
38. Gautam, A.; Densmore, C. L.; Golunski, E.; Xu, B.; Waldrep, J. C. Transgene expression in mouse airway epithelium by aerosol gene therapy with PEI-DNA complexes Mol. Ther. 2001, 3 (4) 551-556 (Pubitemid 32509849)
39. Segura, T.; Schmokel, H.; Hubbell, J. A. RNA interference targeting hypoxia inducible factor 1α reduces post-operative adhesions in rats J. Surg. Res. 2007, 141 (2) 162-70 (Pubitemid 47042044)
40. Iwai, M.; Harada, Y.; Tanaka, S.; Muramatsu, A.; Mori, T.; Kashima, K.; Imanishi, J.; Mazda, O. Polyethylenimine-mediated suicide gene transfer induces a therapeutic effect for hepatocellular carcinoma in vivo by using an Epstein-Barr virus-based plasmid vector Biochem. Biophys. Res. Commun. 2002, 291 (1) 48-54 (Pubitemid 34681136)
41. Aoki, K.; Furuhata, S.; Hatanaka, K.; Maeda, M.; Remy, J. S.; Behr, J. P.; Terada, M.; Yoshida, T. Polyethylenimine-mediated gene transfer into pancreatic tumor dissemination in the murine peritoneal cavity Gene Ther. 2001, 8 (7) 508-514 (Pubitemid 32409525)
42. Coll, J. L.; Chollet, P.; Brambilla, E.; Desplanques, D.; Behr, J. P.; Favrot, M. In vivo delivery to tumors of DNA complexed with linear polyethylenimine Hum. Gene Ther. 1999, 10 (10) 1659-1666 (Pubitemid 29328210)
43. Saha, K.; Keung, A. J.; Irwin, E. F.; Li, Y.; Little, L.; Schaffer, D. V.; Healy, K. E. Substrate modulus directs neural stem cell behavior Biophys. J. 2008, 95 (9) 4426-38
44. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix elasticity directs stem cell lineage specification Cell 2006, 126 (4) 677-89 (Pubitemid 44233625)
45. Huebsch, N.; Arany, P. R.; Mao, A. S.; Shvartsman, D.; Ali, O. A.; Bencherif, S. A.; Rivera-Feliciano, J.; Mooney, D. J. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate Nat. Mater. 2010, 9 (6) 518-26
46. Zhang, J.; Lei, Y.; Dhaliwal, A.; Ng, Q. K.; Du, J.; Yan, M.; Lu, Y.; Segura, T. Protein-polymer nanoparticles for nonviral gene delivery Biomacromolecules 2011, 12 (4) 1006-14
47. Godbey, W. T.; Wu, K. K.; Mikos, A. G. Poly(ethylenimine) and its role in gene delivery J. Controlled Release 1999, 60 (2-3) 149-160 (Pubitemid 29335941)
48. Dhaliwal, A.; Maldonado, M.; Han, Z.; Segura, T. Differential uptake of DNA-poly(ethylenimine) polyplexes in cells cultured on collagen and fibronectin surfaces Acta Biomater. 2010, 6 (9) 3436-47
49. Hsiong, S. X.; Huebsch, N.; Fischbach, C.; Kong, H. J.; Mooney, D. J. Integrin-adhesion ligand bond formation of preosteoblasts and stem cells in three-dimensional RGD presenting matrices Biomacromolecules 2008, 9 (7) 1843-1851
50. Petrie, T. A.; Raynor, J. E.; Dumbauld, D. W.; Lee, T. T.; Jagtap, S.; Templeman, K. L.; Collard, D. M.; Garcia, A. J. Multivalent integrin-specific ligands enhance tissue healing and biomaterial integration Sci. Transl. Med. 2010, 2 (45) 45ra60
51. Ng, Q. K.; Su, H.; Armijo, A. L.; Czernin, J.; Radu, C. G.; Segura, T. Clustered arg-gly-asp peptides enhances tumor targeting of nonviral vectors ChemMedChem 2011, 6 (4) 623-7
52. Ng, Q. K.; Sutton, M. K.; Soonsawad, P.; Xing, L.; Cheng, H.; Segura, T. Engineering clustered ligand binding into nonviral vectors: αvβ3 targeting as an example Mol. Ther. 2009, 17 (5) 828-36