Hydrogel design for supporting neurite outgrowth and promoting gene delivery to maximize neurite extension

Biotechnology and Bioengineering

Volumn 109, Issue 3, 2012, Pages 830-839

  Shepard, Jaclyn A ^a   Stevans, Alyson C ^a   Holland, Samantha ^a   Wang, Christine E ^a   Shikanov, Ariella ^a   Shea, Lonnie D ^a,b,c  

^a Northwestern University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Dorsal root ganglia (DRG); Gene delivery; Hydrogel; Neurite outgrowth; Three dimensional

Indexed keywords

ADHESION SITES; ARG GLY ASPS; COCULTURE; COMBINATORIAL APPROACH; DORSAL ROOT GANGLIA; GENE DELIVERY; LIPOPLEXES; MULTIPLE BARRIER; NERVE GROWTH FACTOR; NERVE REGENERATION; NEURITE EXTENSION; NEURITE GROWTH; NEURITE OUTGROWTH; NEURITES; PEG HYDROGEL;

CELL ADHESION; CELL CULTURE; ENCAPSULATION; FIBROBLASTS; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; MOLECULAR BIOLOGY;

HYDROGELS;

ARGINYLGLYCYLASPARTIC ACID; LIPOPLEX; MACROGOL; NERVE GROWTH FACTOR;

ACCESSORY CELL; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL ADHESION; CELL ENCAPSULATION; CELL SURFACE; CELL VIABILITY; CELLULAR DISTRIBUTION; COCULTURE; CONTROLLED STUDY; ENZYME DEGRADATION; EXPLANT; FIBROBLAST; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSFECTION; HYDROGEL; IN VITRO STUDY; NERVE FIBER GROWTH; NONHUMAN; SPINAL GANGLION;

ANIMALS; CHICK EMBRYO; FIBROBLASTS; GANGLIA, SPINAL; GENE THERAPY; HYDROGEL; NEURITES; ORGAN CULTURE TECHNIQUES; POLYETHYLENE GLYCOLS; TRANSFECTION;

EID: 84855966966     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24355     Document Type: Article

References (43)

1. Andreopoulos F, Beckman E, Russell A. 1998. Light-induced tailoring of PEG-hydrogel properties. Biomaterials 19: 1343-1352.
2. Bengali Z, Pannier A, Segura T, Anderson B, Jang J, Mustoe T, Shea L. 2005. Gene delivery through cell culture substrate adsorbed DNA complexes. Biotechnol Bioeng 90: 290-302.
3. Bradbury E, Khemani S, King V, Priestley J, McMahon S. 1999. NT-3 promotes growth of lesined adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur J Neurosci 11: 3873-3883.
4. Burdick J, Ward M, Liang E, Young M, Langer R. 2006. Stimulation of neurite outgrowth by neurotrophins delivered from degradable hydrogels. Biomaterials 27: 452-459.
5. De Laporte L, Yan A, Shea L. 2009a. Local gene delivery from ECM-coated poly(lactide-co-glycolide) multiple channel bridges after spinal cord injury. Biomaterials 30: 2361-2368.
6. De Laporte L, Yang Y, Zelivyanskaya M, Cummings B, Anderson A, Shea L. 2009b. Plasmid releasing mutliple channel bridges for transgene expression after spinal cord injury. Mol Ther 17: 318-326.
7. des Rieux A, Shikanov A. Shea L, 2009. Fibrin hydrogels for non-viral vector delivery in vitro. J Control Release 136: 148-154.
8. Flanagan L, Ju Y, Marg B, Osterfield M, Janmey P. 2002. Neurite branching on deformable substrates. Neuroreport 13: 2411-2415.
9. Fukunaka Y, Iwanaga K, Morimoto K, Kakemi M, Tabata Y. 2002. Controlled release of plasmid DNA from cationized gelatin hydrogels based on hydrogel degradation. J Control Release 80: 333-343.
10. Gundersen R, Barrett J. 1980. Characterization of the turning response of dorsal root neurites toward nerve growth factor. J Cell Biol 87: 546-554.
11. Gunn J, Turner S, Mann B. 2005. Adhesive and mechanical properties of hydrogels influence neurite extension. J Biomed Mater Res A 72A: 91-97.
12. Houchin-Ray T, Huang A, West E, Zelivyanskaya M, Shea L. 2009a. Spatially patterned gene expression for guided neurite extension. J Neurosci Res 87: 844-856.
13. Houchin-Ray T, Swift L, Jang J, Shea L. 2007a. Patterned PLG substrates for localized DNA delivery and directed neurite extension. Biomaterials 28: 2603-2611.
14. Houchin-Ray T, Whittlesey K, Shea L. 2007b. Spattially patterned gene delivery for localized neuron survival and neurite extension. Mol Ther 15: 705-712.
15. Houchin-Ray T, Zelivyanskaya M, Huang A, Shea L. 2009b. Non-viral gene delivery tranfection profiles influence neuronal architecture in an in vitro co-culture model. Biotechnol Bioeng 103: 1023-1033.
16. Kong H, Liu J, Riddle K, Matsumoto T, Leach K, Mooney D. 2005. Non-viral gene delivery regulated by stiffness of cell adhesion substrates. Nature Mater 4: 460-464.
17. Leach J, Brown Q, Jacot J, DiMilla P, Wong J. 2007. Neurite outgrowth and branching of PC12cells on very soft substrates sharply decreases below a threshold of substrate rigidity. J Neural Eng 4: 26-34.
18. Lei Y, Segura T. 2009. DNA delivery from matrix metalloproteinase degradable poly(ethylene glycol) hydrogels to mouse mouse cloned mesenchymal stem cells. Biomaterials 30: 254-265.
19. Lu P, Tuszynski M. 2008. Growth factors and combinatorial therapies for CNS regeneration. Exp Neurol 209: 313-320.
20. Lutolf M, Lauer-Fields J, Schmoekel H, Metters A, Weber F, Fields G, Hubbell J. 2003. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: Engineering cell-invasion characteristics. Proc Natl Acad Sci USA 100: 5413-5418.
21. Mahoney M, Anseth K. 2006. Three-dimensional growth and function of neural tissue in degradable polyethylene glycol hydrogels. Biomaterials 27: 2265-2274.
22. Mahoney M, Chen R, Tan J, Saltzman W. 2005. The influence of microchannels on neurite growth and architecture. Biomaterials 26: 771-778.
23. Moore K, Macsween M, Shoichet M. 2006. Immobilized concentration gradients of neurotrophic factors guide neurite outgrowth of primary neurons in macroporous scaffolds. Tissue Eng 12: 267-278.
24. Musoke-Zawedde P, Shoichet M. 2006. Anisotropic three-dimensional peptide channels guide neurite outgrowth within a biodegradable hydrogel matrix. Biomed Mater 1: 162-169.
25. Nakahara Y, Gage F, Tuszynski M. 1996. Grafts of fibroblasts genetically modified to secrete NGF, BDNF, NT-3, or basic fgf elicit differential responses in the adult spinal cord. Cell Transplant 5: 191-204.
26. Peretti G, Xu J, Bonassar L, Kirchhoff C, Yaremchuk M, Randolph M. 2006. Review of injectable cartilage engineering using fibrin gel in mice and swine models. Tissue Eng 12: 1151-1168.
27. Quick D, Anseth K. 2004. DNA delivery from photocrosslinked PEG hydrogels: Encapsulation efficiency, release profiles, and DNA quality. J Control Release 96: 341-351.
28. Raeber G, Lutolf M, Hubbell J. 2005. Molecularly engineered PEG hydrogels: A novel model system for proteolytically mediated cell migration. Biophys J 89: 1374-1388.
29. Rajnicek A, Britland S, McCaig C. 1997. Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. J Cell Sci 110: 2905-2913.
30. Schense J, Bloch J, Aebischer P, Hubbell J. 2000. Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension. Nat Biotechnol 18: 415-419.
31. Schense J, Hubbell J. 2000. Three-dimensional migration of neurites is mediated by adhesion site density and affinity. J Biol Chem 275: 6813-6818.
32. Schmidt C, Leach J. 2003. Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng 5: 293-347.
33. Shepard J, Huang A, Shikanov A, Shea L. 2010. Balancing cell migration with matrix degradation enhances gene delivery to cells cultured three-dimensionally within hydrogels. J Control Release 146: 128-135.
34. Shepard J, Wesson P, Wang C, Stevans A, Holland S, Shikanov A, Grzybowski B, Shea L. 2011. Gene therapy vectors with enhanced transfection based on hydrogels modified with affinity peptides. Biomaterials 32: 5092-5099.
35. Tessier-Lavigne M, Goodman C. 1996. The molecular biology of axon guidance. Science 274: 1123-1133.
36. Thuret S, Moon L, Gage F. 2006. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7: 628-643.
37. Tuszynski M, Grill R, Jones L, Brant A, Blesch A, Low K, Lacroix S, Lu P. 2003. NT-3 gene delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp Neurol 181: 47-56.
38. Xia Y, McClelland J, Gupta R, Qin D, Zhao X, Sohn L, Celotta R, Whitesides G. 1997. Replica molding using polymeric materials: A practical step toward nanomanufacturing. Adv Mater 9: 147-149.
39. Xu X, Guenard V, Kleitman N, Aebischer P, Bunge M. 1995. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schawann cell grafts in adult rat thoracic spinal cord. Exp Neurol 134: 261-272.
40. Yang Y, De Laporte L, Zelivyanskaya M, Whittlesey K, Anderson A, Cummings B, Shea L. 2009. Multiple channel bridges for spinal cord injury: Cellular characterization of host response. Tissue Eng Part A 15: 3283-3295.
41. 2 activates pro-matrix metalloproteinase-2 through receptor tyrosine kinases/phosphatidylinositol 3-kinase/NF-κB pathway. J Biol Chem 277: 30271-30282.
42. Yu T, Shoichet M. 2005. Guided cell adhesion and outgrowth in peptide-modified channels for neural tissue engineering. Biomaterials 26: 1507-1514.
43. Zuo J, Ferguson T, Hernandez Y, Stetler-Stevenson W, Muir D. 1998. Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J Neurosci 18: 5203-5211.