Neural progenitor cells grown on hydrogel surfaces respond to the product of the transgene of encapsulated genetically engineered fibroblasts

Biomacromolecules

Volumn 11, Issue 11, 2010, Pages 2936-2943

  Shanbhag, Mihir S ^a   Lathia, Justin D ^b,c,d   Mughal, Mohamed R ^b,e   Francis, Nicola L ^a   Pashos, Nicholas ^a   Mattson, Mark P ^b   Wheatley, Margaret A ^a  

^a DREXEL UNIVERSITY   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d LERNER RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINATE; CELL CULTURE; ENZYME INHIBITION; GENETIC ENGINEERING; PEPTIDES; SCAFFOLDS;

BRAIN-DERIVED NEUROTROPHIC FACTORS; CENTRAL NERVOUS SYSTEMS; ENGINEERED TISSUES; GROWTH FACTOR; HYDROGEL SURFACES; LOCALIZED GROWTH; NEURAL PROGENITOR CELLS; NEUROTROPHIN-3; OPTIMAL GROWTH; TISSUE SCAFFOLDS; TRANSGENE;

HYDROGELS;

ALGINIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; DRUG VEHICLE; GROWTH FACTOR; NEUROTROPHIN 3; TISSUE SCAFFOLD; HYDROGEL; MICROCAPSULE; NERVE GROWTH FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL FATE; CELL GROWTH; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; FIBROBLAST; GENETIC ENGINEERING; HYDROGEL; IMPLANTATION; INJURY; NONHUMAN; PRIORITY JOURNAL; STEM CELL; TRANSGENE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; MICROCAPSULE; NEURAL STEM CELL; PARTICLE SIZE; RAT; SURFACE PROPERTY;

ANIMALS; CAPSULES; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; FIBROBLASTS; GENETIC ENGINEERING; HYDROGELS; NERVE GROWTH FACTORS; NEURAL STEM CELLS; PARTICLE SIZE; RATS; SURFACE PROPERTIES;

EID: 78650319041     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm100699q     Document Type: Article

References (59)

1. Nomura, H.; Tator, C. H.; Shoichet, M. S. Bioengineered strategies for spinal cord repair. J. Neurotrauma 2006, 23 (3-4), 496-507.
2. Dang, J. M.; Leong, K. W. Natural polymers for gene Delivery and tissue engineering. Adv. Drug Delivery Rev. 2006, 58 (4), 487-99.
3. Pearse, D. D.; Bunge, M. B. Designing cell- and gene-based regeneration strategies to repair the injured spinal cord. J. Neurotrauma 2006, 23 (3-4), 438-52.
4. Teng, Y. D.; Lavik, E. B.; Qu, X.; Park, K. I.; Ourednik, J.; Zurakowski, D.; Langer, R.; Snyder, E. Y. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (5), 3024-3029.
5. Tobias, C. A.; Dhoot, N. O.; Wheatley, M. A.; Tessler, A.; Murray, M. M.; Fischer, I. Grafting of encapsulated BDNF-producing fibroblasts into the injured spinal cord without immune suppression in adult rats. J. Neurotrauma 2001, 18 (3), 287-301.
6. Tuszynski, M. H.; Grill, R.; Jones, L. L.; Brant, A.; Blesch, A.; Lo, K.; Lacroix, S.; Lu, P. NT-3 gene Delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp. Neurol. 2003, 181 (1), 47-56.
7. Katz, A.; Meiri, N. Brain-derived neurotrophic factor is critically involved in thermal-experience-dependent Developmental plasticity. J. Neurosci. 2006, 26 (15), 3899-907.
8. Hapner, S. J.; Nielsen, K. M.; Chaverra, M.; Esper, R. M.; Loeb, J. A.; Lefcort., F. NT-3 and CNTF exert dose-dependent, pleiotropic effects on cells in the immature dorsal root ganglion: Neuregulin-mediated proliferation of progenitor cells and neuronal differentiation. Dev. Biol. 2006, 297, 182-197.
9. Nakahara, Y.; Gage, F. H.; Tuszynski, M. H. Grafts of fibroblasts genetically modified to secrete NGF, BDNF, NT-3, or basic FGF elicit differential responses in the adult spinal cord. Cell Transplant 1996, 5 (2), 191-204.
10. Kim, D. H.; Gutin, P. H.; Noble, L. J.; Nathan, D.; Yu, J. S.; Nockels, R. P. Treatment with genetically engineered fibroblasts producing NGF or BDNF can accelerate recovery from traumatic spinal cord injury in the adult rat. Neuroreport 1996, 7 (13), 2221-5.
11. Jin, Y.; Tessler, A.; Fischer, I.; Houle, J. D. Fibroblasts genetically modified to produce BDNF support regrowth of chronically injured serotonergic axons. Neurorehabil. Neural Repair 2000, 14 (4), 311-7.
12. Tobias, C. A.; Han, S. S. W.; Shumsky, J. S.; Kim, D.; Tumolo, M.; Dhoot, N. O.; Wheatley, M. A.; Fischer, I.; Tessler, A.; Murray, M. Alginate encapsulated BDNF-producing fibroblast grafts permit recovery of function after spinal cord injury in the absence of immune suppression. J. Neurotrauma 2005, 22 (1), 138-56.
13. Madhavan, L.; Ourednik, V.; Ouredni, J. Neural Stem/progenitor cells initiate the formation of cellular networks that provide neuroprotection by growth factor-modulated antioxidant expression. Stem Cells 2008, 26, 254-65.
14. Wu, S.; Suzuki, Y.; Kitada, M.; Kitaura, M.; Kataoka, K.; Takahashi, J.; Ide, C.; Nishimura, Y. Migration, integration, and differentiation of hippocampus-derived neurosphere cells after transplantation into injured rat spinal cord. Neurosci. Lett. 2001, 312 (3), 173-6.
15. Cummings, B. J.; Uchida, N.; Tamaki, S. J.; Anderson, A. J. Human neural stem cell differentiation following transplantation into spinal cord injured mice: association with recovery of locomotor function. Neurol. Res. 2006, 28 (5), 474-81.
16. Karimi-Abdolrezaee, S.; Eftekharpour, E.; Wang, J.; Morshead, C. M.; Fehlings, M. G. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci. 2006, 26 (13), 3377-89.
17. Korochkin, L. I.; Revishchin, A. V.; Okhotin, V. E. Neural stem cells and their role in recovery processes in the nervous system. Neurosci. Behav. Physiol. 2006, 36 (5), 499-512.
18. Enzmann, G. U.; Benton, R. L.; Talbott, J. F.; Cao, Q.; Whittemore, S. R. Functional considerations of stem cell transplantation therapy for spinal cord repair. J. Neurotrauma 2006, 23, 479-495.
19. Obermair, F.-J.; Schröter, A.; Thallmair, M. Endogenous neural progenitor cells as therapeutic target after spinal cord injury. Physiology 2008, 23, 296-304.
20. Dillon, G. P.; Yu, X. J.; Sridharan, A.; Ranieri, J. P.; Bellamkonda, R. V. The influence of physical structure and charge on neurite extension in a 3D hydrogel scaffold. J. Biomater. Sci., Polym. Ed. 1998, 9, 1049-1069.
21. Silva, G. A.; Czeisler, C.; Niece, K. L.; Beniash, E.; Harrington, D. A.; Kessler, J. A.; Stupp, S. I. Selective differentiation of neural progenitor cells by high epitope density nanofibers. Science 2004, 303, 1352-5.
22. Teixeira, A. I.; Duckworth, J. K.; Hermanson, O. Getting the right stuff: Controlling neural stem cell state and fate in vivo and in vitro with biomaterials. Cell Res. 2007, 17, 56-61.
23. Akiyamaa, Y.; Honmou, O.; Kato, T.; Uede, T.; Kazuo Hashi, K.; Kocsis, J. D. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp. Neurol. 2001, 167 (1), 27-39.
24. Cummings, B. J.; Uchida, N.; Tamaki, S. J.; Salazar, D. L.; Hooshmand, M.; Summers, R.; Levenberg, S.; Burdick, J. A.; Kraehenbuehl, T.; Langer, R. Neurotrophin-induced differentiation of human embryonic stem cells on three-dimensional polymeric scaffolds. Tissue Eng. 2005, 11 (3-4), 506-12.
25. Nakajima, M.; Ishimuro, T.; Kato, K.; Ko, I.-K.; Hiratac, I.; Arimaa, Y.; Iwata, H. Combinatorial protein display for the cell-based screening of biomaterials that direct neural stem cell differentiation. Biomaterials 2007, 28, 1048-1060.
26. Novikov, L. N.; Novikova, L. N.; Mosahebi, A.; Wiberg, M.; Terenghi, G.; Kellerth, J.-O. A novel biodegradable implant for neuronal rescue and regeneration after spinal cord injury. Biomaterials 2002, 23 (16), 3369-76.
27. Novikova, L. N.; Novikov, L. N.; Kellerth, J. O. Biopolymers and biodegradable smart implants for tissue regeneration after spinal cord injury. Curr. Opin. Neurol. 2003, 16 (6)), 711-5.
28. Novikova, L. N.; Mosahebi, A.; Wiberg, M.; Terenghi, G.; Kellerth, J.-O.; Novikov, L. N. Alginate hydrogel and matrigel as potential cell carriers for neurotransplantation. J. Biomed. Mater. Res., Part A 2006, 77 (2), 242-52.
29. Kataoka, K. , et al., 2001. Kataoka, K.; Suzuki, Y.; Kitada, M.; Ohnishi, K.; Suzuki, K.; Tanihara, M.; Ide, C.; Endo, K.; Nishimura, Y. Alginate, a bioresorbable material derived from brown seaweed, enhances elongation of amputated axons of spinal cord in infant rats. J. Biomed. Mater. Res. 2001, 54 (3), 373-84.
30. Kataoka, K.; Suzuki, Y.; Kitada, M.; Hashimoto, T.; Chou, H.; Bai, H.; Ohta, M.; Wu, S.; Suzuki, K.; Ide, C. Alginate enhances elongation of early regenerating axons in spinal cord of young rats. Tissue Eng. 2004, 10 (3-4), 493-504.
31. Dhoot, N. O.; Tobias, C. A.; Fischer, I.; Wheatley, M. A. Peptidemodified alginate surfaces as a growth permissive substrate for neurite outgrowth. J. Biomed. Mater. Res., Part A 2004, 71 (2), 191-200.
32. Goosen, M. F. A.; O'Shea, G. M.; Gharapetian, H. M.; Chou, S.; Sun, A. M. Optimization of microencapsulation parameters: Semipermeable microcapsules as a bioartificial pancreas. Biotechnol. Bioeng. 1985, XXVI, 146-150.
33. Kuo, C. K.; Ma, P. X. Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: Part 1. Structure, gelation rate, and mechanical properties. Biomaterials 2001, 22 (6), 511-21.
34. Liu, Y.; Himes, T.; Tryon, B.; Moul, J.; Chow, S. Y.; Jin, H.; Murray, M.; Tessler, A.; Fischer, I. Intraspinal grafting of fibroblasts genetically modified by recombinant adenoviruses. Neuroreport 1998, 9 (6), 1075-9.
35. Liu, Y.; Kim, D.; Himes, B. T.; Chow, S. Y.; Schallert, T.; Murray, M.; Tessler, A.; Fischer, I. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospina axons and recovery of forelimb function. J. Neurosci. 1999, 19, 4370-4387.
36. Tobias, C. A.; Shumsky, J. S.; Shibata, M.; Tuszynski, M. H.; Fischer, I.; Tessler, A.; Murray, M. Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration. Exp. Neurol. 2003, 84, 97-113.
37. Kanakasabai, S. Alginate Strings and Their Applications in Spinal Cord Regeneration, Ph.D. Thesis, Drexel University, Philadelphia, PA, 2007.
38. Vroemen, M.; Aigner, L.; Winkler, J.; Weidner, N. Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur. J. Neurosci. 2003, 18 (4), 743-5.
39. Read, T. A.; Stensvaag, V.; Vindenes, H.; Ulvestad, E.; Bjerkvig, R.; Thorsen, F. Cells encapsulated in alginate: a potential system for Delivery of recombinant proteins to malignant brain tumors. Int. J. Dev. Neurosci. 1999, 17 (5-6), 653-63.
40. Markusen, J. F.; Mason, C.; Hull, D. A.; Town, M. A.; Tabor, A. B.; Clements, M.; Boshoff, C. H.; Dunnill, P. Behavior of adult human mesenchymal stem cells entrapped in alginate-GRGDY beads. Tissue Eng. 2006, 12 (4), 821-30.
41. Dar, A.; Shachar, M; Leor, J.; Cohen, S. Optimization of cardiac cell seeding and distribution in 3D porous alginate scaffolds. Biotechnol. Bioeng. 2002, 80 (3), 305-12.
42. Ma, H. L.; Hung, S.-C.; Lin, S.-Y.; Chen, Y.-L.; Lo., W.-H. Chondrogenesis of human mesenchymal stem cells encapsulated in alginate beads. J. Biomed. Mater. Res., Part A 2003, 64 (2), 273-81.
43. Prang, P.; Müller, R.; Eljaouhari, A.; Heckmann, K.; Kunz, W.; Weber, T.; Faber, C.; Vroemen, M.; Bogdahn, U.; Weidner, N. The promotion of oriented axonal regrowth in the injured spinal cord by alginatebased anisotropic capillary hydrogels. Biomaterials 2006, 27, 3560-3569.
44. Ashton, R. S.; Banerjee, A.; Punyani, S.; Schaffer, D.; Kane, R. Scaffolds based on degradable alginate hydrogels and poly(lactidecoglycolide) microspheres for stem cell culture. Biomaterials 2007, 28 (36), 5518-25.
45. Solon, J.; Levental, I.; Sengupta, K.; Georges, P. C.; Janmey, P. A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 2007, 93, 4453-4461.
46. von Wichert, G.; Haimovich, B.; Feng, G. S.; Sheetz, M. P. Forcedependent integrin-cytoskeleton linkage formation requires downregulation of focal complex dynamics by Shp2. EMBO J. 2003, 22, 5023-5035.
47. Kong, H. J.; Polte, T. R.; Alsberg, E.; Mooney, D. J. FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 4300-4305.
48. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126, 677-689.
49. Kearns, S. M.; Laywell, E. D.; Kukekov, V. K.; Steindler, D. A. Extracellular matrix effects on neurosphere cell motility. Exp. Neurol. 2003, 182, 240-244.
50. Huebsch, N.; Arany, P. R.; Mao, A. S.; Shvartsman, D.; Omar, A.; Ali, O.; Sidi, A.; Bencherif1, A.; Rivera-Feliciano, J.; Mooney, D. A. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 2010, 9, 518-526.
51. Lachyankar, M. B.; Condon, P. J.; Quesenberry, P. J.; Litofsky, N. S.; Recht, L. D.; Ross, A. H. Embryonic precursor cells that express Trk receptors: Induction of different cell fates by NGF, BDNF, NT-3, and CNTF. Exp. Neurol. 1997, 144 (2), 350-60.
52. Englund, U.; Bjorklund, A.; Wictorin, K. Migration patterns and phenotypic differentiation of clong-term expanded human neural progenitor cells after transplantation into the adult rat brain. Brain Res. Dev. Brain Res. 2002, 134 (1-2), 123-41.
53. Ohyama, K.; Ellis, P.; Kimura, S.; Placzek, M. Directed differentiation of neural cells to hypothalamic dopaminergic neurons. Development 2005, 132 (23), 5185-97.
54. Jones, B.; Erin, N.; Mallapragada, S. K. Directed growth and differentiation of stem cells towards neural cell fates using soluble and surface-mediated cues. J. Biomater. Sci., Polym. Ed. 2007, 18 (8), 999-1015.
55. Caldwell, M A.; He, X.; Wilkie, N.; Pollack, S.; Marshall, G.; Wafford, K. A.; Svendsen, C. N. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 2001, 19 (5), 475-9.
56. Tabar, V.; Panagiotakos, G.; Greenberg, E. D.; Chan, B. K.; Sadelain, M.; Gutin, P. H.; Stude, L. Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat. Biotechnol. 2005, 23 (5), 601-6.
57. Goetz, A. K.; Scheffler, B.; Chen, H.-X.; Wang, S.; Suslov, O. H.; Brüstle, O.; Roper, S. N.; Steindler, D. A. Temporally restricted substrate interactions direct fate and specification of neural precursors derived from embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (29), 11063-8.
58. Levenberg, S.; Burdick, J. A.; Kraehenbuehl, T.; Langer, R. Neurotrophin-induced differentiation of human embryonic stem cells on three-dimensional polymeric scaffolds. Tissue Eng. 2005, 11 (3-4), 506-512.
59. Silva, G. A.; Czeisler, C.; Niece, K. L.; Beniash, E.; Harrington, D. A.; Kessler, J. A.; Stupp, S. I. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2008, 303, 1352-1355.