Design and characterization of microporous hyaluronic acid hydrogels for in vitro gene transfer to mMSCs

Acta Biomaterialia

Volumn 8, Issue 11, 2012, Pages 3921-3931

  Tokatlian, Talar ^a   Cam, Cynthia ^b   Siegman, Shayne N ^a   Lei, Yuguo ^a   Segura, Tatiana ^a  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell mediated release; Controlled release; Enzymatically degradable; Non viral gene delivery; Porous hydrogel

Indexed keywords

CYTOLOGY; DNA; EFFICIENCY; GENE EXPRESSION; GENE THERAPY; HYALURONIC ACID; HYDROGELS; MICROPOROSITY; NANOPARTICLES; ORGANIC ACIDS; PORE SIZE; SCAFFOLDS (BIOLOGY); TISSUE REGENERATION;

CELL-MEDIATED RELEASE; CONTROLLED RELEASE; ENZYMATICALLY DEGRADABLE; HYALURONIC ACID HYDROGELS; MEDIATED RELEASE; MICROPOROUS; NON-VIRAL GENE DELIVERY; POLYPLEXES; POROUS HYDROGELS; TRANSGENE EXPRESSION;

GENE TRANSFER;

DNA LOADED HYDROGEL SCAFFOLD; HYALURONIC ACID DERIVATIVE; MOLECULAR SCAFFOLD; SMALL INTERFERING RNA LOADED HYDROGEL SCAFFOLD; UNCLASSIFIED DRUG; 2'-DEOXYCYTIDINE 5'-TRIPHOSPHATE; DEOXYCYTIDINE PHOSPHATE; DEOXYCYTIDINE TRIPHOSPHATE; DNA; HYALURONIC ACID; LUCIFERASE; POLYETHYLENEIMINE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL ENCAPSULATION; CELL PROLIFERATION; CELL SPREADING; CELL VIABILITY; CONTROLLED STUDY; DNA CONTENT; DNA DEGRADATION; DRUG DESIGN; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE TARGETING; HYDROGEL; IN VITRO GENE TRANSFER; KINETICS; MALE; MESENCHYMAL STEM CELL; MOUSE; NANOENCAPSULATION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCANNING ELECTRON MICROSCOPY; STABLE TRANSFECTION; SUSTAINED DRUG RELEASE; TISSUE ENGINEERING; TRANSGENE; ANIMAL; BAGG ALBINO MOUSE; CELL SURVIVAL; CHEMISTRY; GENE TRANSFER; MESENCHYMAL STROMA CELL; METABOLISM; PLASMID; POROSITY; STAINING;

ANIMALS; CELL SURVIVAL; DEOXYCYTOSINE NUCLEOTIDES; DNA; GENE TRANSFER TECHNIQUES; HYALURONIC ACID; HYDROGELS; LUCIFERASES; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, SCANNING; PLASMIDS; POLYETHYLENEIMINE; POROSITY; STAINING AND LABELING;

EID: 84873940453     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.07.014     Document Type: Article

References (61)

1. Novosel EC, Kleinhans C, Kluger PJ. Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 2011;63:300-11.
2. Chiu Y-C, Cheng M-H, Engel H, Kao S-W, Larson JC, Gupta S, et al. The role of pore size on vascularization and tissue remodeling in PEG hydrogels. Biomaterials 2011;32:6045-51.
3. Huang X, Zhang Y, Donahue H, Lowe T. Porous thermoresponsive- cobiodegradable hydrogels as tissue-engineering scaffolds for 3-dimensional in vitro culture of chondrocytes. Tissue Eng 2007;13:2645-52. (Pubitemid 350076760)
4. Huang YC, Riddle K, Rice KG, Mooney DJ. Long-term in vivo gene expression via delivery of PEI-DNA condensates from porous polymer scaffolds. Hum Gene Ther 2005;16:609-17. (Pubitemid 40740928)
5. Jang JH, Rives CB, Shea LD. Plasmid delivery in vivo from porous tissueengineering scaffolds: Transgene expression and cellular transfection. Mol Ther 2005;12:475-83. (Pubitemid 41150133)
6. Nam YS, Yoon JJ, Park TG. A novel fabrication method of macroporous biodegradable polymer scaffolds using gas foaming salt as a porogen additive. J Biomed Mater Res 2000;53:1-7. (Pubitemid 30056615)
7. Iyer P, Walker KJ, Madihally SV. Increased matrix synthesis by fibroblasts with decreased proliferation on synthetic chitosan-gelatin porous structures. Biotechnol Bioeng 2011;109:1314-25.
8. Kang H-W, Tabata Y, Ikada Y. Fabrication of porous gelatin scaffolds for tissue engineering. Biomaterials 1999;20:1339-44. (Pubitemid 29281386)
9. Kang JY, Chung CW, Sung J-H, Park B-S, Choi J-Y, Lee SJ, et al. Novel porous matrix of hyaluronic acid for the three-dimensional culture of chondrocytes. Inter J Pharm 2009;369:114-20.
10. Van Vlierberghe S, Cnudde V, Masschaele B, Dubruel P, De Paepe I, Jacobs PJS, et al. Porous gelatin cryogels as cell delivery tool in tissue engineering. J Controlled Release 2006;116:e95-8.
11. Galperin A, Long TJ, Ratner BD. Degradable, thermo-sensitive poly(N-isopropyl acrylamide)-based scaffolds with controlled porosity for tissue engineering applications. Biomacromolecules 2010;11:2583-92.
12. Madden LR, Mortisen DJ, Sussman EM, Dupras SK, Fugate JA, Cuy JL, et al. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc Natl Acad Sci 2010;107:15211-6.
13. Saul JM, Linnes MP, Ratner BD, Giachelli CM, Pun SH. Delivery of non-viral gene carriers from sphere-templated fibrin scaffolds for sustained transgene expression. Biomaterials 2007;28:4705-16. (Pubitemid 47260703)
14. Stachowiak AN, Bershteyn A, Tzatzaloz E, Irvine DJ. Bioactive hydrogels with an ordered cellular structure combine interconnected macroporosity and robust mechanical properties. Adv Mater 2005;17:5.
15. 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;5:753-9. (Pubitemid 29318608)
16. Chun KW, Lee JB, Kim SH, Park TG. Controlled release of plasmid DNA from photo-cross-linked pluronic hydrogels. Biomaterials 2005;26:3319-26. (Pubitemid 39647264)
17. Kasper FK, Jerkins E, Tanahashi K, Barry MA, Tabata Y, Mikos AG. Characterization of DNA release from composites of oligo(poly(ethylene glycol) fumarate) and cationized gelatin microspheres in vitro. J Biomed Mater Res A 2006;78A:823-35. (Pubitemid 44300036)
18. Kong HJ, Kim ES, Huang YC, Mooney DJ. Design of biodegradable hydrogel for the local and sustained delivery of angiogenic plasmid DNA. Pharm Res 2008;25:1230-8.
19. Quick DJ, Anseth KS. DNA delivery from photocrosslinked PEG hydrogels: encapsulation efficiency, release profiles, and DNA quality. J Controlled Release 2004;96:341-51. (Pubitemid 38481514)
20. Lei P, Padmashali RM, Andreadis ST. Cell-controlled and spatially arrayed gene delivery from fibrin hydrogels. Biomaterials 2009;30:3790-9.
21. Trentin D, Hall H, Wechsler S, Hubbell JA. Peptide-matrix-mediated gene transfer of an oxygen-insensitive hypoxia-inducible factor-1 alpha variant for local induction of angiogenesis. Proc Nat Acad Sci USA 2006;103:2506-11.
22. Trentin D, Hubbell J, Hall H. Non-viral gene delivery for local and controlled DNA release. J Controlled Release 2005;102:263-75. (Pubitemid 40093791)
23. Lei Y, Ng QKT, Segura T. Two and three-dimensional gene transfer from enzymatically degradable hydrogel scaffolds. Microsci Res Technol 2010;73:910-7.
24. Lei Y, Segura T. DNA delivery from matrix metalloproteinase degradable poly(ethylene glycol) hydrogels to mouse cloned mesenchymal stem cells. Biomaterials 2009;30:254-65.
25. Wieland JA, Houchin-Ray TL, Shea LD. Non-viral vector delivery from PEG-hyaluronic acid hydrogels. J Controlled Release 2007;120:233-41. (Pubitemid 47058636)
26. Lungwitz U, Breunig M, Blunk T, Gopferich A. Polyethylenimine-based nonviral gene delivery systems. Eur J Pharm Biopharm 2005;60:247-66. (Pubitemid 40804565)
27. Abdallah B, Hassan A, Benoist C, Goula D, Behr JP, Demeneix BA. A powerful nonviral vector for in vivo gene transfer into the adult mammalian brain: polyethylenimine. Hum Gene Ther 1996;7:1947-54. (Pubitemid 26390233)
28. Wang S, Ma N, Gao SJ, Yu H, Leong KW. Transgene expression in the brain stem effected by intramuscular injection of polyethylenimine/DNA complexes. Mol Ther 2001;3:658-64. (Pubitemid 32509862)
29. Gautam A, Densmore CL, Golunski E, Xu B, Waldrep JC. Transgene expression in mouse airway epithelium by aerosol gene therapy with PEI-DNA complexes. Mol Ther 2001;3:551-6. (Pubitemid 32509849)
30. Kichler A, Chillon M, Leborgne C, Danos O, Frisch B. Intranasal gene delivery with a polyethylenimine-PEG conjugate. J Controlled Release 2002;81:379-88. (Pubitemid 34607157)
31. Rudolph C, Schillinger U, Plank C, Gessner A, Nicklaus P, Muller RH, et al. Nonviral gene delivery to the lung with copolymer-protected and transferrinmodified polyethylenimine. Biochimica et Biophysica Acta-General Sub 2002;1573:75-83. (Pubitemid 35279791)
32. Wiseman JW, Goddard CA, McLelland D, Colledge WH. 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;10:1654-62. (Pubitemid 37069493)
33. Segura T, Schmokel H, Hubbell JA. RNA interference targeting hypoxia inducible factor 1 [alpha] reduces post-operative adhesions in rats. J Surg Res 2007;141:162-70. (Pubitemid 47042044)
34. Aoki K, Furuhata S, Hatanaka K, Maeda M, Remy JS, Behr JP, et al. Polyethylenimine-mediated gene transfer into pancreatic tumor dissemination in the murine peritoneal cavity. Gene Ther 2001;8:508-14. (Pubitemid 32409525)
35. Coll JL, Chollet P, Brambilla E, Desplanques D, Behr JP, Favrot M. In vivo delivery to tumors of DNA complexed with linear polyethylenimine. Hum Gene Ther 1999;10:1659-66. (Pubitemid 29328210)
36. Iwai M, Harada Y, Tanaka S, Muramatsu A, Mori T, Kashima K, et al. Polyethylenimine-mediated suicide gene transfer induces a therapeutic effect for hepatocellular carcinoma in vivo by using an Epstein-Barr virusbased plasmid vector. Biochem Biophys Res Commun 2002;291:48-54. (Pubitemid 34681136)
37. Fraser JR, Laurent TC, Laurent UB. Hyaluronan: Its nature, distribution, functions and turnover. J Intern Med 1997;242:27-33. (Pubitemid 27323862)
38. Leach JB, Bivens KA, Patrick CW, Schmidt CE. Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol Bioeng 2003;82:578-89. (Pubitemid 36514267)
39. Park YD, Tirelli N, Hubbell JA. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials 2003;24:893-900. (Pubitemid 36024167)
40. Shu XZ, Liu YC, Palumbo FS, Lu Y, Prestwich GD. In situ crosslinkable hyaluronan hydrogels for tissue engineering. Biomaterials 2004;25:1339-48. (Pubitemid 37476210)
41. Yeo Y, Highley CB, Bellas E, Ito T, Marini R, Langer R, et al. In situ cross-linkable hyaluronic acid hydrogels prevent post-operative abdominal adhesions in a rabbit model. Biomaterials 2006;27:4698-705. (Pubitemid 43870121)
42. Eldridge L, Moldobaeva A, Wagner EM. Increased hyaluronan fragmentation during pulmonary ischemia. Am J Physiol-Lung Cell Mol Physiol 2011;301:L782-8.
43. Gao F, Liu Y, He Y, Yang C, Wang Y, Shi X, et al. Hyaluronan oligosaccharides promote excisional wound healing through enhanced angiogenesis. Matrix Biol 2010;29:107-16.
44. Voelcker V, Gebhardt C, Averbeck M, Saalbach A, Wolf V, Weih F, et al. Hyaluronan fragments induce cytokine and metalloprotease upregulation in human melanoma cells in part by signalling via TLR4. Exp Dermatol 2008;17:100-7.
45. Chung C, Burdick JA. Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. Tissue Eng Part A 2009;15:243-54.
46. Gerecht S, Burdick JA, Ferreira LS, Townsend SA, Langer R, Vunjak-Novakovic G. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci USA 2007;104:11298-303. (Pubitemid 47175135)
47. Kim J, Park Y, Tae G, Lee KB, Hwang CM, Hwang SJ, et al. 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:967-75.
48. Pan LJ, Ren YJ, Cui FZ, Xu QY. Viability and differentiation of neural precursors on hyaluronic acid hydrogel scaffold. J Neurosci Res 2009;87:3207-20.
49. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990;61:1303-13.
50. Sherman L, Sleeman J, Herrlich P, Ponta H. Hyaluronate receptors-key players in growth, differentiation, migration and tumor progression. Curr Opin Cell Biol 1994;6:726-33. (Pubitemid 24295307)
51. 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;32:39-47.
52. Kim J, Park Y, Tae G, Lee KB, Hwang SJ, Kim IS, et al. Synthesis and characterization of matrix metalloprotease sensitive-low molecular weight hyaluronic acid based hydrogels. J Mater Sci-Mater Med 2008;19:3311-8.
53. Gojgini S, Tokatlian T, Segura T. Utilizing cell-matrix interactions to modulate gene transfer to stem cells inside hyaluronic acid hydrogels. Mol Pharm 2011;8:1582-91.
54. Lei Y, Huang S, Sharif-Kashani P, Chen Y, Kavehpour P, Segura T. Incorporation of active DNA/cationic polymer polyplexes into hydrogel scaffolds. Biomaterials 2010;31:9106-16.
55. Lei Y, Rahim M, Ng Q, Segura T. Hyaluronic acid and fibrin hydrogels with concentrated DNA/PEI polyplexes for local gene delivery. J Controlled Release 2011;153:255-61.
56. Peyton SR, Kalcioglu ZI, Cohen JC, Runkle AP, Van Vliet KJ, Lauffenburger DA, et al. Marrow-Derived stem cell motility in 3D synthetic scaffold is governed by geometry along with adhesivity and stiffness. Biotechnol Bioeng 2011;108:1181-93.
57. Stachowiak AN, Irvine DJ. Inverse opal hydrogel-collagen composite scaffolds as a supportive microenvironment for immune cell migration. J Biomed Mater Res A 2008;85:815-28. (Pubitemid 351632895)
58. Tokatlian T, Shrum CT, Kadoya WM, Segura T. Protease degradable tethers for controlled and cell-mediated release of nanoparticles in 2-And 3-dimensions. Biomaterials 2010;31:8072-80.
59. Schrementi ME, Ferreira AM, Zender C, DiPietro LA. Site-specific production of TGF-b in oral mucosal and cutaneous wounds. Wound Repair Regen 2008;16:80-6.
60. Szpaderska AM, Zuckerman JD, DiPietro LA. Differential injury responses in oral mucosal and cutaneous wounds. J Dent Res 2003;82:621-6. (Pubitemid 41766145)
61. Bitter T, Muir HM. A modified uronic acid carbazole reaction. Anal Biochem 1962;4:330-4.