A developmentally inspired combined mechanical and biochemical signaling approach on zonal lineage commitment of mesenchymal stem cells in articular cartilage regeneration

Integrative Biology (United Kingdom)

Volumn 7, Issue 1, 2015, Pages 112-127

  Karimi, Tahereh ^a   Barati, Danial ^a   Karaman, Ozan ^a   Moeinzadeh, Seyedsina ^a   Jabbari, Esmaiel ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLIC ACID; HYDROXYAPATITE; MACROGOL; MESSENGER RNA; OSTEOGENIC PROTEIN 1; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; ARTICULAR CARTILAGE; CALCIFICATION; CELL DENSITY; CELL ENCAPSULATION; CELL LINEAGE; CELL VIABILITY; CHEMICAL ANALYSIS; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR MATRIX; HISTOLOGY; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYMAL STEM CELL; PROTEIN EXPRESSION; RIGIDITY; UPREGULATION; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CHONDROGENESIS; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; MECHANOTRANSDUCTION; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; PROCEDURES; REGENERATION; TISSUE ENGINEERING; TISSUE SCAFFOLD;

CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STROMAL CELLS; REGENERATION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84919777697     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c4ib00197d     Document Type: Article

References (101)

1. S. P. Grogan S. F. Duffy C. Pauli J. A. Koziol A. I. Su D. D. D'Lima M. K. Lotz Zone-specific gene expression patterns in articular cartilage Arthritis Rheum. 2013 65 418 428
2. F. Las Heras H. K. Gahunia K. P. Pritzker Articular cartilage development: A molecular perspective Orthop. Clin. North Am. 2012 43 155 171
3. T. J. Klein J. Malda R. L. Sah D. W. Hutmacher Tissue engineering of articular cartilage with biomimetic zones Tissue Eng., Part B 2009 15 143 157
4. L. Kock C. C. van Donkelaar K. Ito Tissue engineering of functional articular cartilage: The current status Cell Tissue Res. 2012 347 613 627
5. P. J. Yang J. S. Temenoff Engineering orthopedic tissue interfaces Tissue Eng., Part B 2009 15 127 141
6. P. H. Chao S. Yodmuang X. Wang L. Sun D. L. Kaplan G. Vunjak-Novakovic Silk hydrogel for cartilage tissue engineering J. Biomed. Mater. Res., Part B 2010 95 84 90
7. K. L. Spiller S. A. Maher A. M. Lowman Hydrogels for the repair of articular cartilage defects Tissue Eng., Part B 2011 17 281 299
8. C. S. Bahney C. W. Hsu J. U. Yoo J. L. West B. Johnstone A bioresponsive hydrogel tuned to chondrogenesis of human mesenchymal stem cells FASEB J. 2011 25 1486 1496
9. M. Pacifici E. Koyama Y. Shibukawa C. Wu Y. Tamamura M. Enomoto-Iwamoto M. Iwamoto Cellular and molecular mechanisms of synovial joint and articular cartilage formation Ann. N. Y. Acad. Sci. 2006 1068 74 86
10. K. W. Ng G. A. Ateshian C. T. Hung Zonal chondrocytes seeded in a layered agarose hydrogel create engineered cartilage with depth-dependent cellular and mechanical inhomogeneity Tissue Eng., Part A 2009 15 2315 2324
11. S. Moon S. K. Hasan Y. S. Song F. Xu H. O. Keles F. Manzur S. Mikkilineni J. W. Hong J. Nagatomi E. Haeggstrom A. Khademhosseini U. Demirci Layer by layer three-dimensional tissue epitaxy by cell-laden hydrogel droplets Tissue Eng., Part C 2010 16 157 166
12. B. Sharma C. G. Williams T. K. Kim D. Sun A. Malik M. Khan K. Leong J. H. Elisseeff Designing zonal organization into tissue-engineered cartilage Tissue Eng. 2007 13 405 414
13. X. Cui K. Breitenkamp M. G. Finn M. Lotz D. D. D'Lima Direct human cartilage repair using three-dimensional bioprinting technology Tissue Eng., Part A 2012 18 1304 1312
14. E. M. Darling K. A. Athanasiou Rapid phenotypic changes in passaged articular chondrocyte subpopulations J. Orthop. Res. 2005 23 425 432
15. U. R. Goessler K. Bieback P. Bugert R. Naim C. Schafer H. Sadick K. Hormann F. Riedel Human chondrocytes differentially express matrix modulators during in vitro expansion for tissue engineering Int. J. Mol. Med. 2005 16 509 515
16. U. R. Goessler P. Bugert K. Bieback A. Baisch H. Sadick T. Verse H. Kluter K. Hormann F. Riedel Expression of collagen and fiber-associated proteins in human septal cartilage during in vitro dedifferentiation Int. J. Mol. Med. 2004 14 1015 1022
17. S. Boeuf W. Richter Chondrogenesis of mesenchymal stem cells: Role of tissue source and inducing factors Stem Cell Res. Ther. 2010 1 31
18. L. H. Nguyen A. K. Kudva N. L. Guckert K. D. Linse K. Roy Unique biomaterial compositions direct bone marrow stem cells into specific chondrocytic phenotypes corresponding to the various zones of articular cartilage Biomaterials 2011 32 1327 1338
19. J. A. Hendriks L. Moroni J. Riesle J. R. de Wijn C. A. van Blitterswijk The effect of scaffold-cell entrapment capacity and physico-chemical properties on cartilage regeneration Biomaterials 2013 34 4259 4265
20. S. D. McCullen H. Autefage A. Callanan E. Gentleman M. M. Stevens Anisotropic fibrous scaffolds for articular cartilage regeneration Tissue Eng., Part A 2012 18 2073 2083
21. J. A. Steele S. D. McCullen A. Callanan H. Autefage M. A. Accardi D. Dini M. M. Stevens Combinatorial scaffold morphologies for zonal articular cartilage engineering Acta Biomater. 2014 10 2065 2075
22. J. A. Andrades S. C. Motaung P. Jimenez-Palomo S. Claros J. M. Lopez-Puerta J. Becerra T. M. Schmid A. H. Reddi Induction of superficial zone protein (szp)/lubricin/prg 4 in muscle-derived mesenchymal stem/progenitor cells by transforming growth factor-beta1 and bone morphogenetic protein-7 Arthritis Res. Ther. 2012 14 R72
23. A. D. Pearle R. F. Warren S. A. Rodeo Basic science of articular cartilage and osteoarthritis Clin. J. Sport Med. 2005 24 1 12
24. R. M. Schinagl D. Gurskis A. C. Chen R. L. Sah Depth-dependent confined compression modulus of full-thickness bovine articular cartilage J. Orthop. Res. 1997 15 499 506
25. R. A. Stockwel Interrelationship of cell density and cartilage thickness in mammalian articular cartilage J. Anat. 1971 109 411 421
26. V. Lefebvre P. Bhattaram Vertebrate skeletogenesis Curr. Top. Dev. Biol. 2010 90 291 317
27. E. M. Darling K. A. Athanasiou Growth factor impact on articular cartilage subpopulations Cell Tissue Res. 2005 322 463 473
28. S. V. Eleswarapu N. D. Leipzig K. A. Athanasiou Gene expression of single articular chondrocytes Cell Tissue Res. 2007 327 43 54
29. A. Khalafi T. M. Schmid C. Neu A. H. Reddi Increased accumulation of superficial zone protein (szp) in articular cartilage in response to bone morphogenetic protein-7 and growth factors J. Orthop. Res. 2007 25 293 303
30. E. Coates J. P. Fisher Gene expression of alginate-embedded chondrocyte subpopulations and their response to exogenous igf-1 delivery J. Tissue Eng. Regener. Med. 2012 6 179 192
31. Z. Lin C. Willers J. A. Xu M. H. Zheng The chondrocyte: Biology and clinical application Tissue Eng. 2006 12 1971 1984
32. D. G. Hickey S. R. Frenkel P. E. Di Cesare Clinical applications of growth factors for articular cartilage repair Am. J. Orthop. 2003 32 70 76
33. T. Sueyoshi K. Yamamoto H. Akiyama Conditional deletion of tgfbr2 in hypertrophic chondrocytes delays terminal chondrocyte differentiation Matrix Biol. 2012 31 352 359
34. T. Niikura A. H. Reddi Differential regulation of lubricin/superficial zone protein by transforming growth factor beta/bone morphogenetic protein superfamily members in articular chondrocytes and synoviocytes Arthritis Rheum. 2007 56 2312 2321
35. H. J. Pulkkinen V. Tiitu P. Valonen J. S. Jurvelin M. J. Lammi I. Kiviranta Engineering of cartilage in recombinant human type II collagen gel in nude mouse model in vivo Osteoarthritis Cartilage 2010 18 1077 1087
36. J. Kundu J. H. Shim J. Jang S. W. Kim D. W. Cho An additive manufacturing-based PCL-alginate-chondrocyte bioprinted scaffold for cartilage tissue engineering J. Tissue Eng. Regener. Med. 2013 10.1002/term.1682
37. H. Park B. Choi J. Hu M. Lee Injectable chitosan hyaluronic acid hydrogels for cartilage tissue engineering Acta Biomater. 2013 9 4779 4786
38. S. Moeinzadeh D. Barati X. He E. Jabbari Gelation characteristics and osteogenic differentiation of stromal cells in inert hydrolytically degradable micellar polyethylene glycol hydrogels Biomacromolecules 2012 13 2073 2086
39. C. Cha W. B. Liechty A. Khademhosseini N. A. Peppas Designing biomaterials to direct stem cell fate ACS Nano 2012 6 9353 9358
40. S. Moeinzadeh D. Barati S. K. Sarvestani O. Karaman E. Jabbari Nanostructure formation and transition from surface to bulk degradation in polyethylene glycol gels chain-extended with short hydroxy acid segments Biomacromolecules 2013 14 2917 2928
41. C. H. Lee J. L. Cook A. Mendelson E. K. Moioli H. Yao J. J. Mao Regeneration of the articular surface of the rabbit synovial joint by cell homing: A proof of concept study Lancet 2010 376 440 448
42. M. Falah G. Nierenberg M. Soudry M. Hayden G. Volpin Treatment of articular cartilage lesions of the knee Int. Orthop. 2010 34 621 630
43. S. Moeinzadeh S. N. Khorasani J. Ma X. He E. Jabbari Synthesis and gelation characteristics of photo-crosslinkable star poly(ethylene oxide-co-lactide-glycolide acrylate) macromonomers Polymer 2011 52 3887 3896
44. X. He J. Ma E. Jabbari Effect of grafting rgd and bmp-2 protein-derived peptides to a hydrogel substrate on osteogenic differentiation of marrow stromal cells Langmuir 2008 24 12508 12516
45. O. Karaman A. Kumar S. Moeinzadeh X. He T. Cui E. Jabbari Effect of surface modification of nanofibers with glutamic acid peptide on calcium phosphate nucleation and osteogenic differentiation of marrow stromal cells J. Tissue Eng. Regener. Med. 2013 10.1002/term.1775
46. W. Xu J. Ma E. Jabbari Material properties and osteogenic differentiation of marrow stromal cells on fiber-reinforced laminated hydrogel nanocomposites Acta Biomater. 2010 6 1992 2002
47. X. Yang S. K. Sarvestani S. Moeinzadeh X. He E. Jabbari Three-dimensional-engineered matrix to study cancer stem cells and tumorsphere formation: Effect of matrix modulus Tissue Eng., Part A 2013 19 669 684
48. A. S. Sarvestani E. Jabbari Modeling and experimental investigation of rheological properties of injectable poly(lactide ethylene oxide fumarate)/hydroxyapatite nanocomposites Biomacromolecules 2006 7 1573 1580
49. S. Kern H. Eichler J. Stoeve H. Kluter K. Bieback Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue Stem Cells 2006 24 1294 1301
50. X. Zhang M. Hirai S. Cantero R. Ciubotariu L. Dobrila A. Hirsh K. Igura H. Satoh I. Yokomi T. Nishimura S. Yamaguchi K. Yoshimura P. Rubinstein T. A. Takahashi Isolation and characterization of mesenchymal stem cells from human umbilical cord blood: Reevaluation of critical factors for successful isolation and high ability to proliferate and differentiate to chondrocytes as compared to mesenchymal stem cells from bone marrow and adipose tissue J. Cell. Biochem. 2011 112 1206 1218
51. C. R. Correia L. S. Moreira-Teixeira L. Moroni R. L. Reis C. A. van Blitterswijk M. Karperien J. F. Mano Chitosan scaffolds containing hyaluronic acid for cartilage tissue engineering Tissue Eng., Part C 2011 17 717 730
52. J. L. Ruan N. L. Tulloch V. Muskheli E. E. Genova P. D. Mariner K. S. Anseth C. E. Murry An improved cryosection method for polyethylene glycol hydrogels used in tissue engineering Tissue Eng., Part C 2013 19 794 801
53. L. Gao T. J. Sheu Y. Dong D. M. Hoak M. J. Zuscik E. M. Schwarz M. J. Hilton R. J. O'Keefe J. H. Jonason Tak1 regulates sox9 expression in chondrocytes and is essential for postnatal development of the growth plate and articular cartilages J. Cell Sci. 2013 126 5704 5713
54. J. A. Henderson X. He E. Jabbari Concurrent differentiation of marrow stromal cells to osteogenic and vasculogenic lineages Macromol. Biosci. 2008 8 499 507
55. L. G. Cima S. T. Lopina Network structures of radiation-cross-linked star polymer gels Macromolecules 1995 28 6787 6794
56. J. Coburn M. Gibson P. A. Bandalini C. Laird H. Q. Mao L. Moroni D. Seliktar J. Elisseeff Biomimetics of the extracellular matrix: An integrated three-dimensional fiber-hydrogel composite for cartilage tissue engineering Smart Struct. Syst. 2011 7 213 222
57. L. Wu C. Bluguermann L. Kyupelyan B. Latour S. Gonzalez S. Shah Z. Galic S. Ge Y. Zhu F. A. Petrigliano A. Nsair S. G. Miriuka X. Li K. M. Lyons G. M. Crooks D. R. McAllister B. Van Handel J. S. Adams D. Evseenko Human developmental chondrogenesis as a basis for engineering chondrocytes from pluripotent stem cells Stem Cell Rev. Rep. 2013 1 575 589
58. P. Julkunen J. Iivarinen P. A. Brama J. Arokoski J. S. Jurvelin H. J. Helminen Maturation of collagen fibril network structure in tibial and femoral cartilage of rabbits Osteoarthritis Cartilage 2010 18 406 415
59. I. Gadjanski K. Spiller G. Vunjak-Novakovic Time-dependent processes in stem cell-based tissue engineering of articular cartilage Stem Cell Rev. 2012 8 863 881
60. T. Iwakura R. Sakata A. H. Reddi Induction of chondrogenesis and expression of superficial zone protein in synovial explants with tgf-beta 1 and bmp-7 Tissue Eng., Part A 2013 19 2638 2644
61. H. Lans J. M. Lindvall K. Thijssen A. E. Karambelas D. Cupac O. Fensgard G. Jansen J. H. Hoeijmakers H. Nilsen W. Vermeulen DNA damage leads to progressive replicative decline but extends the life span of long-lived mutant animals Cell Death Differ. 2013 20 1709 1718
62. V. Dexheimer S. Frank W. Richter Proliferation as a requirement for in vitro chondrogenesis of human mesenchymal stem cells Stem Cells Dev. 2012 21 2160 2169
63. M. L. Alves da Silva A. Martins A. R. Costa-Pinto P. Costa S. Faria M. Gomes R. L. Reis N. M. Neves Cartilage tissue engineering using electrospun PCL nanofiber meshes and MSCs Biomacromolecules 2010 11 3228 3236
64. A. N. Buxton C. S. Bahney J. U. Yoo B. Johnstone Temporal exposure to chondrogenic factors modulates human mesenchymal stem cell chondrogenesis in hydrogels Tissue Eng., Part A 2011 17 371 380
65. R. L. Mauck X. Yuan R. S. Tuan Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture Osteoarthritis Cartilage 2006 14 179 189
66. M. Zhang M. Wang X. Tan T. F. Li Y. E. Zhang D. Chen Smad3 prevents beta-catenin degradation and facilitates beta-catenin nuclear translocation in chondrocytes J. Biol. Chem. 2010 285 8703 8710
67. E. Labbe A. Letamendia L. Attisano Association of smads with lymphoid enhancer binding factor 1/t cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways Proc. Natl. Acad. Sci. U. S. A. 2000 97 8358 8363
68. F. Z. Lu Z. Y. Jiang X. X. Wang Y. H. Luo X. F. Li H. L. Liu Role of the insulin-like growth factor system in epiphyseal cartilage on the development of langshan and arbor acres chickens, gallus domesticus Poult. Sci. 2010 89 956 965
69. Y. Wang Z. Cheng H. Z. Elalieh E. Nakamura M. T. Nguyen S. Mackem T. L. Clemens D. D. Bikle W. Chang IGF-1r signaling in chondrocytes modulates growth plate development by interacting with the pthrp/ihh pathway J. Bone Miner. Res. 2011 26 1437 1446
70. A. A. Worster B. D. Brower-Toland L. A. Fortier S. J. Bent J. Williams A. J. Nixon Chondrocytic differentiation of mesenchymal stem cells sequentially exposed to transforming growth factor-beta1 in monolayer and insulin-like growth factor-I in a three-dimensional matrix J. Orthop. Res. 2001 19 738 749
71. L. Longobardi L. O'Rear S. Aakula B. Johnstone K. Shimer A. Chytil W. A. Horton H. L. Moses A. Spagnoli Effect of igf-I in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of tgf-beta signaling J. Bone Miner. Res. 2006 21 626 636
72. S. Y. Lee T. Nakagawa A. H. Reddi Induction of chondrogenesis and expression of superficial zone protein (szp)/lubricin by mesenchymal progenitors in the infrapatellar fat pad of the knee joint treated with tgf-beta1 and bmp-7 Biochem. Biophys. Res. Commun. 2008 376 148 153
73. E. E. Coates J. P. Fisher Engineering superficial zone chondrocytes from mesenchymal stem cells Tissue Eng., Part C 2014 20 630 640
74. T. M. Quinn E. B. Hunziker H. J. Hauselmann Variation of cell and matrix morphologies in articular cartilage among locations in the adult human knee Osteoarthritis Cartilage 2005 13 672 678
75. A. R. Gannon T. Nagel D. J. Kelly The role of the superficial region in determining the dynamic properties of articular cartilage Osteoarthritis Cartilage 2012 20 1417 1425
76. R. K. Korhonen M. Wong J. Arokoski R. Lindgren H. J. Helminen E. B. Hunziker J. S. Jurvelin Importance of the superficial tissue layer for the indentation stiffness of articular cartilage Med. Eng. Phys. 2002 24 99 108
77. A. J. Steward D. R. Wagner D. J. Kelly The pericellular environment regulates cytoskeletal development and the differentiation of mesenchymal stem cells and determines their response to hydrostatic pressure Eur. Cells Mater. 2013 25 167 178
78. Q. S. Chen B. Suki K. N. An Dynamic mechanical properties of agarose gels modeled by a fractional derivative model J. Biomech. Eng. 2004 126 666 671
79. H. Akiyama V. Lefebvre Unraveling the transcriptional regulatory machinery in chondrogenesis J. Bone Miner. Metab. 2011 29 390 395
80. B. S. Yoon D. A. Ovchinnikov I. Yoshii Y. Mishina R. R. Behringer K. M. Lyons Bmpr1a and bmpr1b have overlapping functions and are essential for chondrogenesis in vivo Proc. Natl. Acad. Sci. U. S. A. 2005 102 5062 5067
81. N. T. Khanarian N. M. Haney R. A. Burga H. H. Lu A functional agarose-hydroxyapatite scaffold for osteochondral interface regeneration Biomaterials 2012 33 5247 5258
82. Y. Huang X. Niu W. Song C. Guan Q. Feng Y. Fao Combined effect of mechanical strain and hydroxyapatite/collagen composite on osteogenic differentiation of rat bone marrow derived mesenchymal stem cells J. Nanomater. 2013 2013 343909
83. J. L. Allen M. E. Cooke T. Alliston Ecm stiffness primes the tgfbeta pathway to promote chondrocyte differentiation Mol. Biol. Cell 2012 23 3731 3742
84. J. C. H. Leijten L. S. M. Teixeira E. B. M. Landman C. A. van Blitterswijk M. Karperien Hypoxia inhibits hypertrophic differentiation and endochondral ossification in explanted tibiae PLoS One 2012 7 e49896 10.1371/journal.pone.0049896
85. M. B. Eslaminejad S. Nadri Murine mesenchymal stem cell isolated and expanded in low and high density culture system: Surface antigen expression and osteogenic culture mineralization In Vitro Cell. Dev. Biol.: Anim. 2009 45 451 459
86. M. Honda Y. Watanabe T. Tsuchiya N. Kanzawa M. Aizawa Selective differentiation of bone marrow-derived mesenchymal stromal cells into osteocytes via endochondral ossification in an apatite-fiber scaffold J. Ceram. Soc. Jpn. 2013 121 759 765
87. A. J. Engler S. Sen H. L. Sweeney D. E. Discher Matrix elasticity directs stem cell lineage specification Cell 2006 126 677 689
88. Y. R. Shih K. F. Tseng H. Y. Lai C. H. Lin O. K. Lee Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells J. Bone Miner. Res. 2011 26 730 738
89. S. Liu D. A. Calderwood M. H. Ginsberg Integrin cytoplasmic domain-binding proteins J. Cell Sci. 2000 113 3563 3571
90. A. Mukherjee P. Rotwein Akt promotes bmp2-mediated osteoblast differentiation and bone development J. Cell Sci. 2009 122 716 726
91. G. Mbalaviele S. Sheikh J. P. Stains V. S. Salazar S. L. Cheng D. Chen R. Civitelli Beta-catenin and bmp-2 synergize to promote osteoblast differentiation and new bone formation J. Cell. Biochem. 2005 94 403 418
92. C. Chenu A. Valentin-Opran P. Chavassieux S. Saez P. J. Meunier P. D. Delmas Insulin like growth factor I hormonal regulation by growth hormone and by 1, 25(oh)2d3 and activity on human osteoblast-like cells in short-term cultures Bone 1990 11 81 86
93. G. Morel P. Chavassieux B. Barenton P. M. Dubois P. J. Meunier G. Boivin Evidence for a direct effect of growth hormone on osteoblasts Cell Tissue Res. 1993 273 279 286
94. S. J. Bryant K. S. Anseth Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels J. Biomed. Mater. Res. 2002 59 63 72
95. P. J. Wipff D. B. Rifkin J. J. Meister B. Hinz Myofibroblast contraction activates latent tgf-beta1 from the extracellular matrix J. Cell Biol. 2007 179 1311 1323
96. J. L. Wrana Regulation of smad activity Cell 2000 100 189 192
97. T. Furumatsu M. Tsuda N. Taniguchi Y. Tajima H. Asahara Smad3 induces chondrogenesis through the activation of sox9 via creb-binding protein/p300 recruitment J. Biol. Chem. 2005 280 8343 8350
98. L. H. Nguyen A. K. Kudva N. S. Saxena K. Roy Engineering articular cartilage with spatially-varying matrix composition and mechanical properties from a single stem cell population using a multi-layered hydrogel Biomaterials 2011 32 6946 6952
99. S. D. Thorpe T. Nagel S. F. Carroll D. J. Kelly Modulating gradients in regulatory signals within mesenchymal stem cell seeded hydrogels: A novel strategy to engineer zonal articular cartilage PLoS One 2013 8 e60764 10.1371/journal.pone.0060764
100. T. W. Spitters C. M. Mota S. C. Uzoechi B. Slowinska D. E. Martens L. Moroni M. Karperien Glucose gradients influence zonal matrix deposition in 3D cartilage constructs Tissue Eng., Part A 2014 10.1089/ten.tea.2014.0059
101. K. Chatterjee S. Lin-Gibson W. E. Wallace S. H. Parekh Y. J. Lee M. T. Cicerone M. F. Young C. G. Simon, Jr. The effect of 3D hydrogel scaffold modulus on osteoblast differentiation and mineralization revealed by combinatorial screening Biomaterials 2010 31 5051 5062