Hydrogels as carriers for stem cell transplantation

IEEE Transactions on Biomedical Engineering

Volumn 61, Issue 5, 2014, Pages 1474-1481

  Alvarado Velez, Melissa ^a   Pai, S Balakrishna ^a   Bellamkonda, Ravi V ^a  

^a Emory University   (United States)

Author keywords

Immunomodulation; injectable hydrogels; stem cell transplantation

Indexed keywords

DISEASE CONTROL; HYDROGELS; IMMUNE SYSTEM;

CELL REPLACEMENT THERAPY; CURRENT LIMITATION; DEGENERATIVE DISEASE; HOST IMMUNE RESPONSE; IMMUNO MODULATIONS; INJECTABLE HYDROGELS; STEM CELL DIFFERENTIATION; STEM CELL TRANSPLANTATION;

STEM CELLS;

ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; DEGENERATIVE DISEASE; ELECTROCONDUCTIVE HYDROGEL; GELLING HYDROGEL; HOST; HYDROGEL; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOMODULATORY HYDROGEL; PHOTOPOLYMERIZABLE HYDROGEL; STEM CELL TRANSPLANTATION; THERMORESPONSIVE HYDROGEL; ANIMAL; HUMAN; MOUSE;

HYDROGEL;

ANIMALS; CELL DIFFERENTIATION; HUMANS; HYDROGELS; MICE; STEM CELL TRANSPLANTATION;

EID: 84899679236     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2014.2305753     Document Type: Article

References (71)

1. M. P. Lutolf, P. M. Gilbert, and H. M. Blau, "Designing materials to direct stem-cell fate," Nature, vol. 462, pp. 433-441, Nov. 26, 2009.
2. M. Mimeault, R. Hauke, and S. K. Batra, "Stem cells: A revolution in therapeutics-recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies," Clin. Pharmacol. Therapy, vol. 82, pp. 252-264, Sep. 2007.
3. O. Lindvall, Z. Kokaia, and A. Martinez-Serrano, "Stem cell therapy for human neurodegenerative disorders-how to make it work," Nature Med., vol. 10, pp. S42-S50, Jul. 2004.
4. P. S. Hume and K. S. Anseth, "Inducing local T cell apoptosis with anti-Fas-functionalized polymeric coatings fabricated via surface-initiated photopolymerizations," Biomaterials, vol. 31, pp. 3166-3174, Apr. 2010.
5. S. Yang, K. F. Leong, Z. Du, and C. K. Chua, "The design of scaffolds for use in tissue engineering-Part I: Traditional factors," Tissue Eng., vol. 7, pp. 679-689, Dec. 2001.
6. J. L. Drury and D. J. Mooney, "Hydrogels for tissue engineering: Scaffold design variables and applications," Biomaterials, vol. 24, pp. 4337-4351, Nov. 2003.
7. V. L. Tsang and S. N. Bhatia, "Three-dimensional tissue fabrication," Adv. Drug Del. Rev., vol. 56, pp. 1635-1647, Sep. 22 2004.
8. S. Woerly, P. Petrov, E. Sykova, T. Roitbak, Z. Simonova, and A. R. Harvey, "Neural tissue formation within porous hydrogels implanted in brain and spinal cord lesions: Ultrastructural, immunohistochemical, and diffusion studies," Tissue Eng., vol. 5, pp. 467-488, Oct. 1999.
9. S. E. Hanson, S. N. King, J. Kim, X. Chen, S. L. Thibeault, and P. Hematti, "The effect of mesenchymal stromal cell-hyaluronic acid hydrogel constructs on immunophenotype of macrophages," Tissue Eng. Part A, vol. 17, pp. 2463-2471, Oct. 2011.
10. A. J. Nauta and W. E. Fibbe, "Immunomodulatory properties of mes-enchymal stromal cells," Blood, vol. 110, pp. 3499-3506, Nov. 15, 2007.
11. Y. Zhong and R. V. Bellamkonda, "Biomaterials for the central nervous system," J. Roy. Soc. Interface, vol. 5, pp. 957-975, Sep. 6, 2008.
12. A. M. Bratt-Leal, R. L. Carpenedo, M. D. Ungrin, P. W. Zandstra, and T. C. McDevitt, "Incorporation of biomaterials in multicellular aggregates modulates pluripotent stem cell differentiation," Biomaterials, vol. 32, pp. 48-56, Jan. 2011.
13. A. J. Engler, H. L. Sweeney, D. E. Discher, and J. E. Schwarzbauer, "Extracellular matrix elasticity directs stem cell differentiation," J. Muscu-loskelet. Neuronal Interact., vol. 7, p. 335, Oct.-Dec. 2007.
14. A. J. Engler, M. A. Griffin, S. Sen, C. G. Bonnemann, H. L. Sweeney, and D. E. Discher, "Myotubes differentiate optimally on substrates with tissue-like stiffness: Pathological implications for soft or stiff microenvironments," J. Cell Biol., vol. 166, pp. 877-887, Sep. 13, 2004.
15. A. Banerjee, M. Arha, S. Choudhary, R. S. Ashton, S. R. Bhatia, D. V. Schaffer, and R. S. Kane, "The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells," Biomaterials, vol. 30, pp. 4695-4699, Sep. 2009.
16. B. Jeong, S. W. Kim, and Y. H. Bae, "Thermosensitive sol-gel reversible hydrogels," Adv. Drug Del. Rev., vol. 54, pp. 37-51, Jan. 17, 2002.
17. E. Ruel-Gariepy and J. C. Leroux, "In situ-forming hydrogels-Review of temperature-sensitive systems," Eur. J. Pharm Biopharm., vol. 58, pp. 409-426, Sep. 2004.
18. T. G. P. Hyun Jung Chung, "Self-assembled and nanostructured hydrogels for drug delivery and tissue engineering, "Nano Today, vol. 4, pp. 429-437, 2009.
19. H. A. Awad, M. Q. Wickham, H. A. Leddy, J. M. Gimble, and F. Guilak, "Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds," Biomaterials, vol. 25, pp. 3211-22, Jul. 2004.
20. M. M. Pakulska, B. G. Ballios, and M. S. Shoichet, "Injectable hydrogels for central nervous system therapy," Biomed. Mater., vol. 7, p. 024101, Apr. 2012.
21. C. C. Tate, D. A. Shear, M. C. Tate, D. R. Archer, D. G. Stein, and M. C. LaPlaca, "Laminin and fibronectin scaffolds enhance neural stem cell transplantation into the injured brain," J. Tissue Eng. Regen. Med., vol. 3, pp. 208-217, Mar. 2009.
22. W. N. Lu, S. H. Lu, H. B. Wang, D. X. Li, C. M. Duan, Z. Q. Liu, T. Hao, W. J. He, B. Xu, Q. Fu, Y. C. Song, X. H. Xie, and C. Y. Wang, "Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel," Tissue Eng. Part A, vol. 15, pp. 1437-1447, Jun. 2009.
23. J. Gao, R. Liu, J. Wu, Z. Liu, J. Li, J. Zhou, T. Hao, Y. Wang, Z. Du, C. Duan, and C. Wang, "The use of chitosan based hydrogel for enhancing the therapeutic benefits of adipose-derived MSCs for acute kidney injury," Biomaterials, vol. 33, pp. 3673-3681, May 2012.
24. S. Lu, H. Wang, W. Lu, S. Liu, Q. Lin, D. Li, C. Duan, T. Hao, J. Zhou, Y. Wang, S. Gao, and C. Wang, "Both the transplantation of somatic cell nuclear transfer-and fertilization-derived mouse embryonic stem cells with temperature-responsive chitosan hydrogel improve myocardial performance in infarcted rat hearts," Tissue Eng. Part A, vol. 16, pp. 1303-1315, Apr. 2010.
25. M. C. Tate, D. A. Shear, S. W. Hoffman, D. G. Stein, and M. C. LaPlaca, "Biocompatibility of methylcellulose-based constructs designed for in-tracerebral gelation following experimental traumatic brain injury," Biomaterials, vol. 22, pp. 1113-1123, May 2001.
26. N. E. Fedorovich, M. H. Oudshoorn, D. van Geemen, W. E. Hennink, J. Alblas, and W. J. Dhert, "The effect of photopolymerization on stem cells embedded in hydrogels," Biomaterials, vol. 30, pp. 344-353, Jan. 2009.
27. S. Khetan and J. A. Burdick, "Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels," Biomaterials, vol. 31, pp. 8228-8234, Nov. 2010.
28. K. Shapira-Schweitzer, M. Habib, L. Gepstein, and D. Seliktar, "A pho-topolymerizable hydrogel for 3-D culture of human embryonic stem cell-derived cardiomyocytes and rat neonatal cardiac cells," J. Mol. Cell Car-diol., vol. 46, pp. 213-224, Feb. 2009.
29. C. N. Salinas and K. S. Anseth, "The enhancement of chondrogenic differentiation of human mesenchymal stem cells by enzymatically regulated RGD functionalities," Biomaterials, vol. 29, pp. 2370-2377, May 2008.
30. K. T. Nguyen and J. L. West, "Photopolymerizable hydrogels for tissue engineering applications," Biomaterials, vol. 23, pp. 4307-4314, Nov. 2002.
31. C. G. Williams, A. N. Malik, T. K. Kim, P. N. Manson, and J. H. Elisseeff, "Variable cytocompatibility of six cell lines with photoinitiators used for polymerizing hydrogels and cell encapsulation," Biomaterials, vol. 26, pp. 1211-1218, Apr. 2005.
32. B. Sharma, C. G. Williams, M. Khan, P. Manson, and J. H. Elisseeff, "In vivo chondrogenesis of mesenchymal stem cells in a photopolymerized hydrogel," Plast. Reconstr. Surg., vol. 119, pp. 112-120, Jan. 2007.
33. C. A. Rossi, M. Flaibani, B. Blaauw, M. Pozzobon, E. Figallo, C. Reggiani, L. Vitiello, N. Elvassore, and P. De Coppi, "In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel," FASEBJ., vol. 25, pp. 2296-2304, Jul. 2011.
34. S. C., C. C. Tseng, Z. X. Liao, H. H. Chen, Y. D. Kang, C. L. Wang, Y. Hwu, and G. Margaritondo, "Controlled hydrogel photopolymerization inside live systems by X-ray irradiation," Soft Matter, vol. 8, pp. 1420-1427, 2012.
35. J. W. Streilein, "Ocular immune privilege: Therapeutic opportunities from an experiment of nature," Nat. Rev. Immunol., vol. 3, pp. 879-889, Nov. 2003.
36. M. Fijak and A. Meinhardt, "The testis in immune privilege," Immunol. Rev., vol. 213, pp. 66-81, Oct. 2006.
37. A. Filippini, A. Riccioli, F. Padula, P. Lauretti, A. D'Alessio, P. De Cesaris, L. Gandini, A. Lenzi, and E. Ziparo, "Immunology and immunopathology of the male genital tract: Control and impairment of immune privilege in the testis and in semen," Human Reproduction Update, vol. 7, pp. 444-449, Sep. 1, 2001.
38. A. Uccelli, V. Pistoia, and L. Moretta, "Mesenchymal stem cells: A new strategy for immunosuppression?," Trends Immunol., vol. 28, pp. 219-226, May 2007.
39. T. F. Ng, E. Lavik, H. Keino, A. W. Taylor, R. S. Langer, and M. J. Young, "Creating an immune-privileged site using retinal progenitor cells and biodegradable polymers," Stem Cells, vol. 25, pp. 1552-1559, Jun. 2007.
40. J. A. Hubbell, S. N. Thomas, and M. A. Swartz, "Materials engineering for immunomodulation," Nature, vol. 462, pp. 449-460, Nov. 26, 2009.
41. P. S. Hume, J. He, K. Haskins, and K. S. Anseth, "Strategies to reduce dendritic cell activation through functional biomaterial design," Biomaterials, vol. 33, pp. 3615-3625, May 2012.
42. P. S. Hume, C. N. Bowman, and K. S. Anseth, "Functionalized PEG hydrogels through reactive dip-coating for the formation of immunoactive barriers," Biomaterials, vol. 32, pp. 6204-6212, Sep. 2011.
43. M. B. Nourse, D. E. Halpin, M. Scatena, D. J. Mortisen, N. L. Tulloch, K. D. Hauch, B. Torok-Storb, B. D. Ratner, L. Pabon, and C. E. Murry, "VEGF induces differentiation of functional endothelium from human embryonic stem cells: Implications for tissue engineering," Arterioscler Thromb Vascular Biol., vol. 30, pp. 80-89, Jan. 2010.
44. Y. Chen, I. Amende, T. G. Hampton, Y. Yang, Q. Ke, J. Y. Min, Y. F. Xiao, and J. P. Morgan, "Vascular endothelial growth factor promotes cardiomy-ocyte differentiation of embryonic stem cells," Am. J. Physiol. Heart Circ. Physiol., vol. 291, pp. H1653-H1658, Oct. 2006.
45. M. Schuldiner, R. Eiges, A. Eden, O. Yanuka, J. Itskovitz-Eldor, R. S. Goldstein, and N. Benvenisty, "Induced neuronal differentiation of human embryonic stem cells," Brain Res., vol. 913, pp. 201-5, Sep. 21, 2001.
46. G. Bain, D. Kitchens, M. Yao, J. E. Huettner, and D. I. Gottlieb, "Embryonic stem cells express neuronal properties in vitro," Developmental Biol., vol. 168, pp. 342-357, Apr. 1995.
47. L. S. Ferreira, S. Gerecht, J. Fuller, H. F. Shieh, G. Vunjak-Novakovic, and R. Langer, "Bioactive hydrogel scaffolds for controllable vascular differentiation of human embryonic stem cells," Biomaterials, vol. 28, pp. 2706-2717, Jun. 2007.
48. N. D. Leipzig, R. G. Wylie, H. Kim, and M. S. Shoichet, "Differentiation of neural stem cells in three-dimensional growth factor-immobilized chitosan hydrogel scaffolds," Biomaterials, vol. 32, pp. 57-64, Jan. 2011.
49. K. C. Butterfield, A. W. Conovaloff, and A. Panitch, "Development of affinity-based delivery of NGF from a chondroitin sulfate biomaterial," Biomatter, vol. 1, pp. 174-181, Oct.-Dec. 2011.
50. M. C. Dodla and R. V. Bellamkonda, "Anisotropic scaffolds facilitate enhanced neurite extension in vitro," J. Biomed. Mater. Res. A, vol. 78, pp. 213-221, Aug. 2006.
51. M. Zhao, H. Bai, E. Wang, J. V. Forrester, and C. D. McCaig, "Electrical stimulation directly induces pre-angiogenic responsesinvascular endothe-lial cells by signaling through VEGF receptors," J. Cell Sci., vol. 117, pp. 397-405, Jan. 26, 2004.
52. J. G. Hardy, J. Y. Lee, and C. E. Schmidt, "Biomimetic conducting polymer-based tissue scaffolds, ". (Apr. 8 2013). Current Opinion Biotech-nol., vol. 24, pp. 847-854, Apr. 8 2013.
53. H. Sauer, G. Rahimi, J. Hescheler, and M. Wartenberg, "Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells," J. Cell Biochem., vol. 75, pp. 710-723, Dec. 15, 1999.
54. L. Wen, C. Zhang, Y. Nong, Q. Yao, and Z. Song, "Mild electrical pulse current stimulation upregulates S100A4 and promotes cardiogenesis in MSC and cardiac myocytes coculture monolayer," Cell Biochem. Bio-phys., vol. 65, pp. 43-55, Jan. 2013.
55. M. Yamada, K. Tanemura, S. Okada, A. Iwanami, M. Nakamura, H. Mizuno, M. Ozawa, R. Ohyama-Goto, N. Kitamura, M. Kawano, K. Tan-Takeuchi, C. Ohtsuka, A. Miyawaki, A. Takashima, M. Ogawa, Y. Toyama, H. Okano, and T. Kondo, "Electrical stimulation modulates fate determination of differentiating embryonic stem cells," Stem Cells, vol. 25, pp. 562-570, Mar. 2007.
56. A. Guiseppi-Elie, "Electroconductive hydrogels: Synthesis, characterization and biomedical applications," Biomaterials, vol. 31, pp. 2701-2716, Apr. 2010.
57. G. G.-E. Justin and Anthony, "Electroconductive Blends of Poly(HEMA-co-PEGMA-co-HMMA-co-SPMA) and Poly(Py-co-PyBA): In vitro bio-compatibility," J. Bioactive Compatible Polymers, vol. 25, pp. 121-140, 2010.
58. P. Y. Lee, E. Cobain, J. Huard, and L. Huang, "Thermosensitive hydrogel PEG-PLGA-PEG enhances engraftment of muscle-derived stem cells and promotes healing in diabetic wound," Mol. Therapy, vol. 15, pp. 1189-1194, Jun. 2007.
59. K. H. Park and K. Na, "Effect of growth factors on chondrogenic differentiation of rabbit mesenchymal cells embedded in injectable hydrogels," J. Biosci. Bioeng., vol. 106, pp. 74-79, Jul. 2008.
60. B. G. Ballios, M. J. Cooke, D. van der Kooy, and M. S. Shoichet, "A hydrogel-based stem cell delivery system to treat retinal degenerative diseases," Biomaterials, vol. 31, pp. 2555-2564, Mar. 2010.
61. C. Fuoco, M. L. Salvatori, A. Biondo, K. Shapira-Schweitzer, S. Santo-leri, S. Antonini, S. Bernardini, F. S. Tedesco, S. Cannata, D. Seliktar, G. Cossu, and C. Gargioli, "Injectable polyethylene glycol-fibrinogen hydro-gel adjuvant improves survival and differentiation of transplanted mesoan-gioblasts in acute and chronic skeletal-muscle degeneration," Skeletal Muscle, vol. 2, p. 24, 2012.
62. A. Michelucci, T. Heurtaux, L. Grandbarbe, E. Morga, and P. Heuschling, "Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: Effects of oligomeric and fibrillar amyloid-beta," J. Neuroimmunol., vol. 210, pp. 3-12, May 29, 2009.
63. N. Mokarram, A. Merchant, V. Mukhatyar, G. Patel, and R. V. Bellamkonda, "Effect of modulating macrophage phenotype on peripheral nerve repair," Biomaterials, vol. 33, pp. 8793-801, Dec. 2012.
64. S. Rutella, S. Danese, and G. Leone, "Tolerogenic dendritic cells: Cy-tokine modulation comes of age," Blood, vol. 108, pp. 1435-1440, Sep. 1, 2006.
65. C. Dani, A. G. Smith, S. Dessolin, P. Leroy, L. Staccini, P. Villageois, C. Darimont, and G. Ailhaud, "Differentiation of embryonic stem cells into adipocytes in vitro," J. Cell Sci., vol. 110, pp. 1279-1285, Jun. 1997.
66. E. Dupin and N. M. Le Douarin, "Retinoic acid promotes the differentiation of adrenergic cells and melanocytes in quail neural crest cultures," Developmental Biol., vol. 168, pp. 529-548, Apr. 1995.
67. M. Schuldiner, O. Yanuka, J. Itskovitz-Eldor, D. A. Melton, and N. Benvenisty, "Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells," Proc. Nat. Acad. Sci. USA, vol. 97, pp. 11307-11312, Oct. 10, 2000.
68. G. Chamberlain, J. Fox, B. Ashton, and J. Middleton, "Concise review: Mesenchymal stem cells: their phenotype, differentiation capacity, im-munological features, and potential for homing," Stem Cells, vol. 25, pp. 2739-2749, Nov. 2007.
69. N. D. Leipzig, C. Xu, T. Zahir, and M. S. Shoichet, "Functional immobilization of interferon-gamma induces neuronal differentiation of neural stem cells," J. Biomed. Mater. Res. A, vol. 93, pp. 625-633, May 2010.
70. S. Ahmed, B. A. Reynolds, and S. Weiss, "BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors," J. Neurosci., vol. 15, pp. 5765-5778, Aug. 1995.
71. R. E. Allen and L. K. Boxhorn, "Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor," J. Cell Physiol., vol. 138, pp. 311-315, Feb. 1989.