Large, stratified, and mechanically functional human cartilage grown in vitro by mesenchymal condensation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 19, 2014, Pages 6940-6945

  Bhumiratana, Sarindr ^a   Eton, Ryan E ^a   Oungoulian, Sevan R ^a   Wan, Leo Q ^b   Ateshian, Gerard A ^a   Vunjak Novakovic, Gordana ^a  

^a Department of Earth and Environmental Sciences   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Biomimetic; Cartilage mechanics; Cartilage repair; Regenerative medicine; Tissue engineering

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; FIBRONECTIN; GLYCOSAMINOGLYCAN; SYNDECAN 3; TENASCIN; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; ARTICULAR CARTILAGE; BIOMECHANICS; BONE MATRIX; CARTILAGE; CELL ADHESION; CELL DIFFERENTIATION; CELL FUSION; CHONDROGENESIS; FRICTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL CONDENSATION; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; TISSUE CULTURE TECHNIQUE; TISSUE GROWTH; TISSUE STRUCTURE; YOUNG MODULUS;

BIOMIMETIC; CARTILAGE MECHANICS; CARTILAGE REPAIR; REGENERATIVE MEDICINE; TISSUE ENGINEERING;

ANIMALS; BIOMECHANICAL PHENOMENA; BIOMIMETICS; BONE AND BONES; CARTILAGE DISEASES; CARTILAGE, ARTICULAR; CATTLE; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA; ELASTIC MODULUS; FRICTION; HUMANS; MESENCHYMAL STROMAL CELLS; TISSUE ENGINEERING;

EID: 84900495398     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1324050111     Document Type: Article

References (44)

1. Langer RS, Vacanti JP (1999) Tissue engineering: The challenges ahead. Sci Am 280(4): 86-89.
2. Nakao K, et al. (2007) The development of a bioengineered organ germ method. Nat Methods 4(3):227-230.
3. Tew SR, Kwan AP, Hann A, Thomson BM, Archer CW (2000) The reactions of articular cartilage to experimental wounding: Role of apoptosis. Arthritis Rheum 43(1): 215-225.
4. Quinn TM, Allen RG, Schalet BJ, Perumbuli P, Hunziker EB (2001) Matrix and cell injury due to sub-impact loading of adult bovine articular cartilage explants: Effects of strain rate and peak stress. J Orthop Res 19(2):242-249.
5. Chen CT, Burton-Wurster N, Lust G, Bank RA, Tekoppele JM (1999) Compositional and metabolic changes in damaged cartilage are peak-stress, stress-rate, and loading-duration dependent. J Orthop Res 17(6):870-879.
6. Züger BJ, et al. (2001) Laser solder welding of articular cartilage: Tensile strength and chondrocyte viability. Lasers Surg Med 28(5):427-434.
7. O'Driscoll SW, Keeley FW, Salter RB (1986) The chondrogenic potential of free autogenous periosteal grafts for biological resurfacing of major full-thickness defects in joint surfaces under the influence of continuous passive motion. An experimental investigation in the rabbit. J Bone Joint Surg Am 68(7):1017-1035.
8. Hangody L, Kish G, Kárpáti Z, Szerb I, Udvarhelyi I (1997) Arthroscopic autogenous osteochondral mosaicplasty for the treatment of femoral condylar articular defects. A preliminary report. Knee Surg Sports Traumatol Arthrosc 5(4):262-267.
9. Brittberg M, Nilsson A, Lindahl A, Ohlsson C, Peterson L (1996) Rabbit articular cartilage defects treated with autologous cultured chondrocytes. Clin Orthop Relat Res (326):270-283.
10. Vunjak-Novakovic G, et al. (1999) Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage. J Orthop Res 17(1):130-138.
11. Pazzano D, et al. (2000) Comparison of chondrogensis in static and perfused bio-reactor culture. Biotechnol Prog 16(5):893-896.
12. Mauck RL, et al. (2000) Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122(3):252-260.
13. Lima EG, et al. (2004) Functional tissue engineering of chondral and osteochondral constructs. Biorheology 41(3-4):577-590.
14. Hu JC, Athanasiou KA (2006) A self-assembling process in articular cartilage tissue engineering. Tissue Eng 12(4):969-979.
15. Lima EG, et al. (2007) The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-beta3. Osteoarthritis Cartilage 15(9):1025-1033.
16. Mauck RL, Yuan X, Tuan RS (2006) Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteo-arthritis Cartilage 14(2):179-189.
17. Mackay AM, et al. (1998) Chondrogenic differentiation of cultured human mesen-chymal stem cells from marrow. Tissue Eng 4(4):415-428.
18. Murdoch AD, et al. (2007) Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: Generation of scaffold-free cartilage. Stem Cells 25(11): 2786-2796.
19. Hall BK, Miyake T (2000) All for one and one for all: Condensations and the initiation of skeletal development. Bioessays 22(2):138-147.
20. DeLise AM, Fischer L, Tuan RS (2000) Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8(5):309-334.
21. Mackie EJ, Murphy LI (1998) The role of tenascin-C and related glycoproteins in early chondrogenesis. Microsc Res Tech 43(2):102-110.
22. Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chon-drogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105(6 Pt 1):2569-2579.
23. Sekiya I, Vuoristo JT, Larson BL, Prockop DJ (2002) In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci USA 99(7): 4397-4402.
24. Tuli R, et al. (2003) Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J Biol Chem 278(42):41227-41236.
25. Pretzel D, et al. (2013) A novel in vitro bovine cartilage punch model for assessing the regeneration of focal cartilage defects with biocompatible bacterial nanocellulose. Arthritis Res Ther 15(3):R59.
26. Obradovic B, et al. (2001) Integration of engineered cartilage. J Orthop Res 19(6): 1089-1097.
27. Brittberg M, et al. (1994) Treatment of deep cartilage defects in the knee with au-tologous chondrocyte transplantation. N Engl J Med 331(14):889-895.
28. Mastbergen SC, Saris DB, Lafeber FP (2013) Functional articular cartilage repair: Here, near, or is the best approach not yet clear? Nat Rev Rheumatol 9(5):277-290.
29. Koyama E, Leatherman JL, Shimazu A, Nah HD, Pacifici M (1995) Syndecan-3, tenascin-C, and the development of cartilaginous skeletal elements and joints in chick limbs. Dev Dyn 203(2):152-162.
30. Chiquet-Ehrismann R, Kalla P, Pearson CA, Beck K, Chiquet M (1988) Tenascin interferes with fibronectin action. Cell 53(3):383-390.
31. Hsia HC, Schwarzbauer JE (2005) Meet the tenascins: multifunctional and mysterious. J Biol Chem 280(29):26641-26644.
32. Tuli R, et al. (2004) Human mesenchymal progenitor cell-based tissue engineering of a single-unit osteochondral construct. Tissue Eng 10(7-8):1169-1179.
33. Freed LE, Langer R, Martin I, Pellis NR, Vunjak-Novakovic G (1997) Tissue engineering of cartilage in space. Proc Natl Acad Sci USA 94(25):13885-13890.
34. Carter MJ, Basalo IM, Ateshian GA (2007) The temporal response of the friction coefficient of articular cartilage depends on the contact area. J Biomech 40(14): 3257-3260.
35. Eyre D (2002) Collagen of articular cartilage. Arthritis Res 4(1):30-35.
36. Pacifici M (1995) Tenascin-C and the development of articular cartilage. Matrix Biol 14(9):689-698.
37. Scotti C, et al. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci USA 107(16):7251-7256.
38. Schubert T, et al. (2009) Long-term effects of chondrospheres on cartilage lesions in an autologous chondrocyte implantation model as investigated in the SCID mouse model. Int J Mol Med 23(4):455-460.
39. Arthur A, Zannettino A, Gronthos S (2009) The therapeutic applications of multipo-tential mesenchymal/stromal stem cells in skeletal tissue repair. J Cell Physiol 218(2): 237-245.
40. Oldershaw RA, et al. (2010) Directed differentiation of human embryonic stem cells toward chondrocytes. Nat Biotechnol 28(11):1187-1194.
41. Teramura T, et al. (2010) Induction of mesenchymal progenitor cells with chondro-genic property from mouse-induced pluripotent stem cells. Cell Reprogramming 12(3):249-261.
42. Grayson WL, et al. (2008) Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng Part A 14(11):1809-1820.
43. Grayson WL, et al. (2010) Engineering anatomically shaped human bone grafts. Proc Natl Acad Sci USA 107(8):3299-3304.
44. Tognana E, et al. (2005) Adjacent tissues (cartilage, bone) affect the functional integration of engineered calf cartilage in vitro. Osteoarthritis Cartilage 13(2):129-138.