Fabrication and evaluation of biomimetic-synthetic nanofibrous composites for soft tissue regeneration

Cell and Tissue Research

Volumn 347, Issue 3, 2012, Pages 803-813

  Gee, Albert O ^a   Baker, Brendon M ^a,b   Silverstein, Amy M ^a,b   Montero, Giana ^a,b   Esterhai, John L ^c   Mauck, Robert L ^b,c,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Electrospinning; Mechanical properties; Mesenchymal stem cells; Nanofiber; Scaffolds; Tissue engineering

Indexed keywords

COLLAGEN TYPE 1; GENIPIN; NANOFIBER; POLYCAPROLACTONE;

ARTICLE; BIOMIMETICS; CELL ADHESION; CELL CULTURE; CELL INFILTRATION; CELL POPULATION; COMPOSITE MATERIAL; CONTROLLED STUDY; CROSS LINKING; FRACTIONATION; IN VITRO STUDY; MESENCHYMAL STEM CELL; NANOFABRICATION; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROCESS OPTIMIZATION; PROTEIN STRUCTURE; TISSUE ENGINEERING; TISSUE REGENERATION;

ANIMALS; BIOMECHANICS; BIOMIMETIC MATERIALS; CATTLE; CELL ADHESION; CELL SHAPE; COLLAGEN TYPE I; CROSS-LINKING REAGENTS; EXTRACELLULAR MATRIX; MESENCHYMAL STEM CELLS; NANOFIBERS; POLYESTERS; REGENERATION; SHEEP; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84859422788     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-011-1308-1     Document Type: Article

References (67)

1. Ayres C, Bowlin GL, Henderson SC, Taylor L, Shultz J, Alexander J, Telemeco TA, Simpson DG (2006) Modulation of anisotropy in electrospun tissue-engineering scaffolds: analysis of fiber alignment by the fast Fourier transform. Biomaterials 27:5524-5534 (Pubitemid 44176139)
2. Baker BM, Mauck RL (2007) The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomaterials 28:1967-1977 (Pubitemid 46176172)
3. Baker BM, Gee AO, Metter RB, Nathan AS, Marklein RA, Burdick JA, Mauck RL (2008) The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials 29:2348-2358
4. Baker BM, Handorf AM, Ionescu LC, Li WJ, Mauck RL (2009a) New directions in nanofibrous scaffolds for soft tissue engineering and regeneration. Expert Rev Med Devices 6:515-532
5. Baker BM, Nathan AS, Huffman GR, Mauck RL (2009b) Tissue engineering with meniscus cells derived from surgical debris. Osteoarthritis Cartilage 17:336-345
6. Baker BM, Nerurkar NL, Burdick JA, Elliott DM, Mauck RL (2009c) Fabrication and modeling of dynamic multipolymer nanofibrous scaffolds. J Biomech Eng 131:101012
7. Baker BM, Nathan AS, Gee AO, Mauck RL (2010) The influence of an aligned nanofibrous topography on human mesenchymal stem cell fibrochondrogenesis. Biomaterials 31:6190-6200
8. Bank RA, Bayliss MT, Lafeber FP, Maroudas A, Tekoppele JM (1998) Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage. The age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage. Biochem J 330:345-351
9. Barnes CP, Sell SA, Boland ED, Simpson DG, Bowlin GL (2007a) Nanofiber technology: designing the next generation of tissue engineering scaffolds. Adv Drug Deliv Rev 59:1413-1433 (Pubitemid 350122771)
10. Barnes CP, Pemble CW, Brand DD, Simpson DG, Bowlin GL (2007b) Cross-linking electrospun type II collagen tissue engineering scaffolds with carbodiimide in ethanol. Tissue Eng 13:1593-1605 (Pubitemid 47105766)
11. Birk DE, Zycband E (1994) Assembly of the tendon extracellular matrix during development. J Anat 184:457-463 (Pubitemid 24186468)
12. Birk DE, Zycband EI, Winkelmann DA, Trelstad RL (1989) Collagen fibrillogenesis in situ: fibril segments are intermediates in matrix assembly. Proc Natl Acad Sci USA 86:4549-4553 (Pubitemid 19164589)
13. Birk DE, Nurminskaya MV, Zycband EI (1995) Collagen fibrillogenesis in situ: fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Dev Dyn 202:229-243
14. Bursac P, Arnoczky S, York A (2009a) Dynamic compressive behavior of human meniscus correlates with its extra-cellular matrix composition. Biorheology 46:227-237
15. Bursac P, York A, Kuznia P, Brown LM, Arnoczky SP (2009b) Influence of donor age on the biomechanical and biochemical properties of human meniscal allografts. Am J Sports Med 37:884-889
16. Buschmann MD, Gluzband YA, Grodzinsky AJ, Kimura JH, Hunziker EB (1992) Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix. J Orthop Res 10:745-758
17. Buttafoco L, Kolkman NG, Engbers-Buijtenhuijs P, Poot AA, Dijkstra PJ, Vermes I, Feijen J (2006) Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials 27:724-734 (Pubitemid 41483823)
18. Casper CL, Yamaguchi N, Kiick KL, Rabolt JF (2005) Functionalizing electrospun fibers with biologically relevant macromolecules. Biomacromolecules 6:1998-2007 (Pubitemid 41052192)
19. Casper CL, Yang W, Farach-Carson MC, Rabolt JF (2007) Coating electrospun collagen and gelatin fibers with perlecan domain I for increased growth factor binding. Biomacromolecules 8:1116-1123 (Pubitemid 46672688)
20. Courtney T, Sacks MS, Stankus J, Guan J, Wagner WR (2006) Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy. Biomaterials 27:3631-3638
21. Dalton PD, Lleixa Calvet J, Mourran A, Klee D, Moller M (2006) Melt electrospinning of poly-(ethylene glycol-block-epsilon-caprolactone). Biotechnol J 1:998-1006
22. Dalton PD, Woodfield T, Hutmacher DW (2009) Snapshot: polymer scaffolds for tissue engineering. Biomaterials 30:701-702
23. Ding B, Kimura E, Sato T, Fujita S, Shiratori S (2004) Fabrication of blend biodegradable nanofibrous nonwoven mats via multi-jet electrospinning. Polymer 45:1895-1902 (Pubitemid 38224321)
24. Ekaputra AK, Prestwich GD, CoolSM, HutmacherDW(2008) Combining electrospun scaffolds with electrosprayed hydrogels leads to three-dimensional cellularization of hybrid constructs. Biomacromolecules 9:2097-2103
25. Ekaputra AK, Prestwich GD, Cool SM, Hutmacher DW (2011) The three-dimensional vascularization of growth factor-releasing hybrid scaffold of poly (varepsilon-caprolactone)/collagen fibers and hyaluronic acid hydrogel. Biomaterials 32:8108-8117
26. Farndale RW, Buttle DJ, Barrett AJ (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883:173-177 (Pubitemid 16027978)
27. Huang AH, Stein A, Tuan RS, Mauck RL (2009) Transient exposure to transforming growth factor beta 3 improves the mechanical properties of mesenchymal stem cell-laden cartilage constructs in a density-dependent manner. Tissue Eng Part A 15:3461-3472
28. Hutmacher DW, Dalton PD (2011) Melt electrospinning. Chem Asian J 6:44-56
29. Ionescu LC, Lee GC, Sennett BJ, Burdick JA, Mauck RL (2010) An anisotropic nanofiber/microsphere composite with controlled release of biomolecules for fibrous tissue engineering. Biomaterials 31:4113-4120
30. Kidoaki S, Kwon IK, Matsuda T (2005) Mesoscopic spatial designs of nano- and microfiber meshes for tissue-engineering matrix and scaffold based on newly devised multilayering and mixing electrospinning techniques. Biomaterials 26:37-46 (Pubitemid 38759470)
31. Ladd MR, Lee SJ, Stitzel JD, Atala A, Yoo JJ (2011) Co-electrospun dual scaffolding system with potential for muscle-tendon junction tissue engineering. Biomaterials 32:1549-1559
32. Lee SJ, Yoo JJ, Lim GJ, Atala A, Stitzel J (2007) In vitro evaluation of electrospun nanofiber scaffolds for vascular graft application. J Biomed Mater Res A 83:999-1008 (Pubitemid 350231760)
33. Li M, Mondrinos MJ, Gandhi MR, Ko FK, Weiss AS, Lelkes PI (2005a) Electrospun protein fibers as matrices for tissue engineering. Biomaterials 26:5999-6008 (Pubitemid 40805606)
34. Li WJ, Mauck RL, Tuan RS (2005b) Electrospun nanofibrous scaffolds: production, characterization, and applications for tissue engineering and drug delivery. J Biomed Nanotechnol 1:259-275
35. Li WJ, Mauck RL, Cooper JA, Yuan X, Tuan RS (2007) Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering. J Biomech 40:1686-1693 (Pubitemid 46702147)
36. Liang HC, Chang WH, Lin KJ, Sung HW (2003) Genipin-crosslinked gelatin microspheres as a drug carrier for intramuscular administration: in vitro and in vivo studies. J Biomed Mater Res A 65:271-282
37. Liang HC, Chang Y, Hsu CK, Lee MH, Sung HW (2004) Effects of crosslinking degree of an acellular biological tissue on its tissue regeneration pattern. Biomaterials 25:3541-3552 (Pubitemid 38327043)
38. Ma Z, He W, Yong T, Ramakrishna S (2005) Grafting of gelatin on electrospun poly(caprolactone) nanofibers to improve endothelial cell spreading and proliferation and to control cell Orientation. Tissue Eng 11:1149-1158 (Pubitemid 41321418)
39. Matthews JA, Wnek GE, Simpson DG, Bowlin GL (2002) Electrospinning of collagen nanofibers. Biomacromolecules 3:232-238 (Pubitemid 34257140)
40. Mauck RL, Yuan X, Tuan RS (2006) Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 14:179-189 (Pubitemid 43079315)
41. Mauck RL, Baker BM, Nerurkar NL, Burdick JA, Li WJ, Tuan RS, Elliott DM (2009) Engineering on the straight and narrow: the mechanics of nanofibrous assemblies for fiber-reinforced tissue regeneration. Tissue Eng Part B Rev 15:171-193
42. Nathan AS, Baker BM, Nerurkar NL, Mauck RL (2010) Mechanotopographic modulation of stem cell nuclear shape on nanofibrous scaffolds. Acta Biomater 7:57-66
43. NerurkarNL, Elliott DM,Mauck RL (2007) Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J Orthop Res 25:1018-1028 (Pubitemid 47233078)
44. Nerurkar NL, Baker BM, Sen S, Wible EE, Elliott DM, Mauck RL (2009) Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nat Mater 8:986-992
45. Pham QP, Sharma U, Mikos AG (2006a) Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng 12:1197-1211 (Pubitemid 44024491)
46. Pham QP, Sharma U, Mikos AG (2006b) Electrospun poly(epsilon- caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules 7:2796-2805 (Pubitemid 44615263)
47. Powell HM, Boyce ST (2006) EDC cross-linking improves skin substitute strength and stability. Biomaterials 27:5821-5827 (Pubitemid 44287022)
48. Rho KS, Jeong L, Lee G, Seo BM, Park YJ, Hong SD, Roh S, Cho JJ, Park WH, Min BM (2006) Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing. Biomaterials 27:1452-1461 (Pubitemid 41739571)
49. Sefcik LS, Neal RA, Kaszuba SN, Parker AM, Katz AJ, Ogle RC, Botchwey EA (2008) Collagen nanofibres are a biomimetic substrate for the serum-free osteogenic differentiation of human adipose stem cells. J Tissue Eng Regen Med 2:210-220
50. Sell SA,McClure MJ, Barnes CP, Knapp DC,Walpoth BH, Simpson DG, Bowlin GL (2006) Electrospun polydioxanone-elastin blends: potential for bioresorbable vascular grafts. Biomed Mater 1:72-80 (Pubitemid 43964734)
51. Shields KJ, Beckman MJ, Bowlin GL, Wayne JS (2004) Mechanical properties and cellular proliferation of electrospun collagen type II. Tissue Eng 10:1510-1517 (Pubitemid 39557854)
52. Skaggs DL, Weidenbaum M, Iatridis JC, Ratcliffe A, Mow VC (1994) Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19:1310-1319 (Pubitemid 24219932)
53. Solorio L, Zwolinski C, Lund AW, Farrell MJ, Stegemann JP (2010) Gelatin microspheres crosslinked with genipin for local delivery of growth factors. J Tissue Eng Regen Med 4:514-523
54. Somers P, De Somer F, Cornelissen M, Bouchez S, Gasthuys F, Narine K, Cox E, Van Nooten G (2008) Genipin blues: an alternative non-toxic crosslinker for heart valves? J Heart Valve Dis 17:682-688
55. Stankus JJ, Freytes DO, Badylak SF, Wagner WR (2008) Hybrid nanofibrous scaffolds from electrospinning of a synthetic biodegradable elastomer and urinary bladder matrix. J Biomater Sci Polym Ed 19:635-652 (Pubitemid 351535786)
56. Stegemann H, Stalder K (1967) Determination of hydroxyproline. Clin Chim Acta 18:267-273
57. Stella JA, Liao J, Hong Y, David Merryman W, Wagner WR, Sacks MS (2008) Tissue-to-cellular level deformation coupling in cell microintegrated elastomeric scaffolds. Biomaterials 29:3228-3236
58. Stitzel J, Liu J, Lee SJ, Komura M, Berry J, Soker S, Lim G, Van Dyke M, Czerw R, Yoo JJ, Atala A (2006) Controlled fabrication of a biological vascular substitute. Biomaterials 27:1088-1094 (Pubitemid 41566702)
59. Sung HW, Chang Y, Liang IL, Chang WH, Chen YC (2000) Fixation of biological tissues with a naturally occurring crosslinking agent: fixation rate and effects of pH, temperature, and initial fixative concentration. J Biomed Mater Res 52:77-87 (Pubitemid 30490982)
60. Sung HW, Liang IL, Chen CN, Huang RN, Liang HF (2001) Stability of a biological tissue fixed with a naturally occurring crosslinking agent (genipin). J Biomed Mater Res 55:538-546 (Pubitemid 32336284)
61. Telemeco TA, Ayres C, Bowlin GL, Wnek GE, Boland ED, Cohen N, Baumgarten CM, Mathews J, Simpson DG (2005) Regulation of cellular infiltration into tissue engineering scaffolds composed of submicron diameter fibrils produced by electrospinning. Acta Biomater 1:377-385 (Pubitemid 43348774)
62. Teo WE, Ramakrishna S (2006) A review on electrospinning design and nanofibre assemblies. Nanotechnology 17:R89-R106 (Pubitemid 43996759)
63. Venugopal J, Ma LL, Yong T, Ramakrishna S (2005) In vitro study of smooth muscle cells on polycaprolactone and collagen nanofibrous matrices. Cell Biol Int 29:861-867 (Pubitemid 41368055)
64. Verzijl N, DeGroot J, Ben ZC, Brau-Benjamin O,Maroudas A, Bank RA, Mizrahi J, Schalkwijk CG, Thorpe SR, Baynes JW, Bijlsma JW, Lafeber FP, TeKoppele JM (2002) Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possiblemechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum 46:114-123 (Pubitemid 34121657)
65. Yannas IV, Tzeranis DS, Harley BA, So PT (2010) Biologically active collagen-based scaffolds: advances in processing and characterization. Philos Transact A Math Phys Eng Sci 368:2123-2139
66. Zeugolis DI, Khew ST, Yew ES, Ekaputra AK, Tong YW, Yung LY, Hutmacher DW, Sheppard C, Raghunath M (2008) Electrospinning of pure collagen nano-fibres - just an expensive way to make gelatin? Biomaterials 29:2293-2305
67. Zhong S, Teo WE, Zhu X, Beuerman RW, Ramakrishna S, Yung LY (2006) An aligned nanofibrous collagen scaffold by electrospinning and its effects on in vitro fibroblast culture. J Biomed Mater Res A 79:456-463 (Pubitemid 44845158)