Fabrication of endothelial cell-laden carrageenan microfibers for microvascularized bone tissue engineering applications

Biomacromolecules

Volumn 15, Issue 8, 2014, Pages 2849-2860

  Mihaila, Silvia M ^a   Popa, Elena G ^a   Reis, Rui L ^a   Marques, Alexandra P ^a   Gomes, Manuela E ^a  

^a UNIVERSITY OF MINHO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; BONE; CYTOLOGY; ENDOTHELIAL CELLS; FIBERS; HISTOLOGY; TISSUE; TISSUE ENGINEERING;

BONE TISSUE ENGINEERING; BUILDING BLOCKES; CELL-CELL INTERACTION; CELLULAR BEHAVIORS; MULTIPLE CELL TYPES; OSTEOBLAST-LIKE CELLS; POLYELECTROLYTE COMPLEXATION; TWO-STEP PROCEDURE;

HYDROGELS;

BONE PROSTHESIS; CARRAGEENAN; HYDROGEL;

BONE PROSTHESIS; CELL COMMUNICATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; ENDOTHELIUM CELL; HUMAN; HYDROGEL; METABOLISM; TISSUE ENGINEERING; TISSUE SCAFFOLD;

BONE SUBSTITUTES; CARRAGEENAN; CELL COMMUNICATION; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; HYDROGELS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84905821696     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm500036a     Document Type: Article

References (61)

1. Berthiaume, F.; Maguire, T. J.; Yarmush, M. L. Tissue engineering and regenerative medicine: history, progress, and challenges Annu. Rev. Chem. Biomol. Eng. 2011, 2, 403-30
2. Kannan, R. Y.; Salacinski, H. J.; Sales, K.; Butler, P.; Seifalian, A. M. The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review Biomaterials 2005, 26 (14) 1857-75
3. Bae, H.; Puranik, A. S.; Gauvin, R.; Edalat, F.; Carrillo-Conde, B.; Peppas, N. A.; Khademhosseini, A. Building vascular networks Sci. Transl. Med. 2012, 4 (160) 160ps23
4. Lovett, M.; Lee, K.; Edwards, A.; Kaplan, D. L. Vascularization strategies for tissue engineering Tissue Eng., Part B 2009, 15 (3) 353-70
5. Phelps, E. A.; Garcia, A. J. Engineering more than a cell: vascularization strategies in tissue engineering Curr. Opin. Biotechnol. 2010, 21 (5) 704-9
6. Geckil, H.; Xu, F.; Zhang, X.; Moon, S.; Demirci, U. Engineering hydrogels as extracellular matrix mimics Nanomedicine 2010, 5 (3) 469-84
7. Drury, J. L.; Mooney, D. J. Hydrogels for tissue engineering: scaffold design variables and applications Biomaterials 2003, 24 (24) 4337-51
8. Malafaya, P. B.; Silva, G. A.; Reis, R. L. Natural-origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications Adv. Drug Delivery Rev. 2007, 59 (4-5) 207-33
9. Fedorovich, N. E.; Wijnberg, H. M.; Dhert, W. J.; Alblas, J. Distinct tissue formation by heterogeneous printing of osteo- and endothelial progenitor cells Tissue Eng., Part A 2011, 17 (15-16) 2113-21
10. Kang, E.; Jeong, G. S.; Choi, Y. Y.; Lee, K. H.; Khademhosseini, A.; Lee, S. H. Digitally tunable physicochemical coding of material composition and topography in continuous microfibres Nat. Mater. 2011, 10 (11) 877-83
11. Aubin, H.; Nichol, J. W.; Hutson, C. B.; Bae, H.; Sieminski, A. L.; Cropek, D. M.; Akhyari, P.; Khademhosseini, A. Directed 3D cell alignment and elongation in microengineered hydrogels Biomaterials 2010, 31 (27) 6941-6951
12. Liu, Y.; Sakai, S.; Taya, M. Production of endothelial cell-enclosing alginate-based hydrogel fibers with a cell adhesive surface through simultaneous cross-linking by horseradish peroxidase-catalyzed reaction in a hydrodynamic spinning process J. Biosci. Bioeng. 2012, 114 (3) 353-9
13. Takei, T.; Sakai, S.; Ijima, H.; Kawakami, K. Development of mammalian cell-enclosing calcium-alginate hydrogel fibers in a co-flowing stream Biotechnol. J. 2006, 1 (9) 1014-7
14. Sakai, S.; Yamaguchi, S.; Takei, T.; Kawakami, K. Oxidized alginate-cross-linked alginate/gelatin hydrogel fibers for fabricating tubular constructs with layered smooth muscle cells and endothelial cells in collagen gels Biomacromolecules 2008, 9 (7) 2036-41
15. Enea, D.; Henson, F.; Kew, S.; Wardale, J.; Getgood, A.; Brooks, R.; Rushton, N. Extruded collagen fibres for tissue engineering applications: effect of crosslinking method on mechanical and biological properties J. Mater. Sci. Mater. Med. 2011, 22 (6) 1569-78
16. Oliveira, J. T.; Martins, L.; Picciochi, R.; Malafaya, P. B.; Sousa, R. A.; Neves, N. M.; Mano, J. F.; Reis, R. L. Gellan gum: a new biomaterial for cartilage tissue engineering applications J. Biomed. Mater. Res., Part A 2010, 93 (3) 852-63
17. Berger, J.; Reist, M.; Mayer, J. M.; Felt, O.; Peppas, N. A.; Gurny, R. Structure and interactions in covalently and ionically crosslinked chitosan hydrogels for biomedical applications Eur. J. Pharm. Biopharm. 2004, 57 (1) 19-34
18. Popa, E. G.; Gomes, M. E.; Reis, R. L. Cell delivery systems using alginate-carrageenan hydrogel beads and fibers for regenerative medicine applications Biomacromolecules 2011, 12 (11) 3952-61
19. Kirsch, P. P. Carrageenan: a safe additive Environ. Health Perspect. 2002, 110 (6) A288 author reply A288.
20. Popa, E. G.; Reis, R. L.; Gomes, M. E. Chondrogenic phenotype of different cells encapsulated in kappa-carrageenan hydrogels for cartilage regeneration strategies Biotechnol. Appl. Biochem. 2012, 59 (2) 132-41
21. Popa, E. G.; Rodrigues, M. T.; Coutinho, D. F.; Oliveira, M. B.; Mano, J. F.; Reis, R. L.; Gomes, M. E. Cryopreservation of cell laden natural origin hydrogels for cartilage regeneration strategies Soft Matter 2013, 9 (3) 875-885
22. Santo, V. E.; Frias, A. M.; Carida, M.; Cancedda, R.; Gomes, M. E.; Mano, J. F.; Reis, R. L. Carrageenan-based hydrogels for the controlled delivery of PDGF-BB in bone tissue engineering applications Biomacromolecules 2009, 10 (6) 1392-401
23. Salgueiro, A. M.; Daniel-da-Silva, A. L.; Fateixa, S.; Trindade, T. kappa-Carrageenan hydrogel nanocomposites with release behavior mediated by morphological distinct Au nanofillers Carbohydr. Polym. 2013, 91 (1) 100-9
24. Kuo, C. K.; Ma, P. X. Maintaining dimensions and mechanical properties of ionically crosslinked alginate hydrogel scaffolds in vitro J. Biomed. Mater. Res., Part A 2008, 84 (4) 899-907
25. Mihaila, S. M.; Gaharwar, A. K.; Reis, R. L.; Marques, A. P.; Gomes, M. E.; Khademhosseini, A. Photocrosslinkable kappa-carrageenan hydrogels for tissue engineering applications Adv. Healthcare Mater. 2013, 2 (6) 895-907
26. Hezaveh, H.; Muhamad, I. I.; Noshadi, I.; Shu Fen, L.; Ngadi, N. Swelling behaviour and controlled drug release from cross-linked kappa-carrageenan/NaCMC hydrogel by diffusion mechanism J. Microencapsulation 2012, 29 (4) 368-79
27. Amici, E.; Clark, A. H.; Normand, V.; Johnson, N. B. Interpenetrating network formation in agarose-kappa-carrageenan gel composites Biomacromolecules 2002, 3 (3) 466-74
28. Granero, A. J.; Razal, J. M.; Wallace, G. G.; Panhuis, M. i. h. Conducting gel-fibres based on carrageenan, chitosan and carbon nanotubes J. Mater. Chem. 2010, 20, 7953-7956
29. Colinet, I.; Dulong, V.; Mocanu, G.; Picton, L.; Le Cerf, D. Effect of chitosan coating on the swelling and controlled release of a poorly water-soluble drug from an amphiphilic and pH-sensitive hydrogel Int. J. Biol. Macromol. 2010, 47 (2) 120-5
30. Chang, H. H.; Wang, Y. L.; Chiang, Y. C.; Chen, Y. L.; Chuang, Y. H.; Tsai, S. J.; Heish, K. H.; Lin, F. H.; Lin, C. P. A novel chitosan-gammaPGA polyelectrolyte complex hydrogel promotes early new bone formation in the alveolar socket following tooth extraction PLoS One 2014, 9 (3) e92362
31. Grenha, A.; Gomes, M. E.; Rodrigues, M.; Santo, V. E.; Mano, J. F.; Neves, N. M.; Reis, R. L. Development of new chitosan/carrageenan nanoparticles for drug delivery applications J. Biomed. Mater. Res., Part A 2010, 92 (4) 1265-72
32. Piyakulawat, P.; Praphairaksit, N.; Chantarasiri, N.; Muangsin, N. Preparation and evaluation of chitosan/carrageenan beads for controlled release of sodium diclofenac AAPS PharmSciTech 2007, 8 (4) E97
33. Pinheiro, A. C.; Bourbon, A. I.; Medeiros, B. G. d. S.; Silva, L. s. H. M. d.; Silva, M. C. H. d.; Carneiro-da-Cunha, M. G.; Coimbra, M. A.; Vicente, A. n. A. Interactions between k-carrageenan and chitosan in nanolayered coatings-Structural and transport properties Carbohydr. Polym. 2012, 87, 1081-1090
34. Mihaila, S. M.; Frias, A. M.; Pirraco, R. P.; Rada, T.; Reis, R. L.; Gomes, M. E.; Marques, A. P. Human adipose tissue-derived SSEA-4 subpopulation multi-differentiation potential towards the endothelial and osteogenic lineages Tissue Eng., Part A 2013, 19 (1-2) 235-46
35. Signini, R.; Filho, S. P. C. Characteristics and properties of purified chitosan in the neutral, acetate and hydrochloride forms Polím. Ciênc. Tecnol. 2001, 11, 58-64
36. Cho, J.; Heuzey, M. C.; Begin, A.; Carreau, P. J. Physical gelation of chitosan in the presence of beta-glycerophosphate: the effect of temperature Biomacromolecules 2005, 6 (6) 3267-75
37. Huh, D.; Hamilton, G. A.; Ingber, D. E. From 3D cell culture to organs-on-chips Trends Cell Biol. 2011, 21 (12) 745-54
38. Hahn, M. S.; Miller, J. S.; West, J. L. Three-dimensional biochemical and biomechanical patterning of hydrogels for guiding cell behavior Adv. Mater. 2006, 18 (20) 2679-2684
39. Oliveira, J. T.; Gardel, L. S.; Rada, T.; Martins, L.; Gomes, M. E.; Reis, R. L. Injectable gellan gum hydrogels with autologous cells for the treatment of rabbit articular cartilage defects J. Orthop. Res. 2010, 28 (9) 1193-9
40. Kim, I. L.; Khetan, S.; Baker, B. M.; Chen, C. S.; Burdick, J. A. Fibrous hyaluronic acid hydrogels that direct MSC chondrogenesis through mechanical and adhesive cue Biomaterials 2013, 34 (22) 5571-80
41. Popa, E. G.; Caridade, S. G.; Mano, J. F.; Reis, R. L.; Gomes, M. E. Chondrogenic potential of injectable kappa-carrageenan hydrogel with encapsulated adipose stem cells for cartilage tissue-engineering applications J. Tissue Eng. Regen. Med. 2013, 10.1002/term.1683
42. Pereira, R. C.; Scaranari, M.; Castagnola, P.; Grandizio, M.; Azevedo, H. S.; Reis, R. L.; Cancedda, R.; Gentili, C. Novel injectable gel (system) as a vehicle for human articular chondrocytes in cartilage tissue regeneration J. Tissue Eng. Regen. Med. 2009, 3 (2) 97-106
43. Fedorovich, N. E.; De Wijn, J. R.; Verbout, A. J.; Alblas, J.; Dhert, W. J. Three-dimensional fiber deposition of cell-laden, viable, patterned constructs for bone tissue printing Tissue Eng., Part A 2008, 14 (1) 127-33
44. Coutinho, D. F.; Sant, S. V.; Shin, H.; Oliveira, J. T.; Gomes, M. E.; Neves, N. M.; Khademhosseini, A.; Reis, R. L. Modified Gellan Gum hydrogels with tunable physical and mechanical properties Biomaterials 2010, 31 (29) 7494-502
45. Stephen, A. M.; Phillips, G. O.; Williams, P. A. Food Polysaccharides and their Applications, 2 nd ed.; Press, C., Ed.; Taylor & Francis Group: New York, 2006.
46. Polk, A.; Amsden, B.; De Yao, K.; Peng, T.; Goosen, M. F. Controlled release of albumin from chitosan-alginate microcapsules J. Pharm. Sci. 1994, 83 (2) 178-85
47. Naciri, M.; Kuystermans, D.; Al-Rubeai, M. Monitoring pH and dissolved oxygen in mammalian cell culture using optical sensors Cytotechnology 2008, 57 (3) 245-50
48. Baker, L. G.; Specht, C. A.; Donlin, M. J.; Lodge, J. K. Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans Eukaryotic Cell 2007, 6 (5) 855-67
49. Popa, E. G.; Carvalho, P. P.; Dias, A. F.; Santos, T. C.; Santo, V. E.; Marques, A. P.; Viegas, C. A.; Dias, I. R.; Gomes, M. E.; Reis, R. L. Evaluation of the in vitro and in vivo biocompatibility of carrageenan-based hydrogels J. Biomed. Mater. Res., Part A 2014, 10.1002/jbm.a.35081
50. Popa, E.; Reis, R.; Gomes, M. Chondrogenic phenotype of different cells encapsulated in kappa-carrageenan hydrogels for cartilage regeneration strategies Biotechnol. Appl. Biochem. 2012, 59 (2) 132-41
51. Fedorovich, N. E.; Haverslag, R. T.; Dhert, W. J.; Alblas, J. The role of endothelial progenitor cells in prevascularized bone tissue engineering: development of heterogeneous constructs Tissue Eng., Part A 2010, 16 (7) 2355-67
52. Urbich, C.; Dimmeler, S. Endothelial progenitor cells: characterization and role in vascular biology Circulation Res. 2004, 95 (4) 343-53
53. Kong, H. J.; Smith, M. K.; Mooney, D. J. Designing alginate hydrogels to maintain viability of immobilized cells Biomaterials 2003, 24 (22) 4023-9
54. Lutolf, M. P.; Gilbert, P. M.; Blau, H. M. Designing materials to direct stem-cell fate Nature 2009, 462 (7272) 433-41
55. Bryant, S. J.; Anseth, K. S. The effects of scaffold thickness on tissue engineered cartilage in photocrosslinked poly(ethylene oxide) hydrogels Biomaterials 2001, 22 (6) 619-26
56. Park, J. H.; Chung, B. G.; Lee, W. G.; Kim, J.; Brigham, M. D.; Shim, J.; Lee, S.; Hwang, C. M.; Durmus, N. G.; Demirci, U.; Khademhosseini, A. Microporous cell-laden hydrogels for engineered tissue constructs Biotechnol. Bioeng. 2010, 106 (1) 138-48
57. Bai, Z.; Mendoza Reyes, J. M.; Montazami, R.; Hashemi, N. On-chip development of hydrogel microfibers from round to square/ribbon shape J. Mater. Chem. A 2014, 2, 4878-4884
58. Adams, C. S.; Mansfield, K.; Perlot, R. L.; Shapiro, I. M. Matrix regulation of skeletal cell apoptosis. Role of calcium and phosphate ions J. Biol. Chem. 2001, 276 (23) 20316-22
59. Murphy, C. L.; Sambanis, A. Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes Tissue Eng. 2001, 7 (6) 791-803
60. Pirraco, R. P.; Melo-Ferreira, B.; Santos, T. C.; Frias, A. M.; Marques, A. P.; Reis, R. L. Adipose stem cell-derived osteoblasts sustain the functionality of endothelial progenitors from the mononuclear fraction of umbilical cord blood Acta Biomater. 2013, 9 (2) 5234-42
61. Pirraco, R. P.; Marques, A. P.; Reis, R. L. Cell interactions in bone tissue engineering J. Cell. Mol. Med. 2010, 14 (1-2) 93-102