In vitro model of mesenchymal condensation during chondrogenic development

Biomaterials

Volumn 30, Issue 33, 2009, Pages 6530-6540

  Ghosh, Sourabh ^a,b   Laha, Michael ^a   Mondal, Sourav ^b   Sengupta, Sejuti ^a   Kaplan, David L ^a  

^a Tufts University   (United States)

^b INDIAN INSTITUTE OF TECHNOLOGY DELHI   (India)

Author keywords

Chondrogenesis; Condensation; Electrospinning; In vitro model system

Indexed keywords

AGGREGATED MORPHOLOGY; CELL-CELL INTERACTION; CHONDROGENESIS; CHONDROGENIC; DEVELOPMENTAL BIOLOGY; EMBRYONIC DEVELOPMENT; GAIN INSIGHT; HUMAN MESENCHYMAL STEM CELLS; IN VITRO MODEL SYSTEM; IN-VITRO; MATRIX; MESENCHYMAL CELLS; SILK PROTEINS; UNDERLYING MECHANISM;

BIOLOGICAL MATERIALS; CARTILAGE; CELL CULTURE; CELL MEMBRANES; CONDENSATION; ELECTROSPINNING; MORPHOLOGY; STIFFNESS; STIFFNESS MATRIX; TISSUE ENGINEERING;

BIOMATERIALS;

AGGRECAN; ALPHA5 INTEGRIN; BETA1 INTEGRIN; BIOMATERIAL; CD51 ANTIGEN; COLLAGEN TYPE 2; FIBRONECTIN RECEPTOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; NANOFIBER; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SILK FIBROIN; TRANSCRIPTION FACTOR SOX9;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL INTERACTION; CELL MIGRATION; CELL STRUCTURE; CHONDROGENESIS; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; ELASTICITY; EMBRYO DEVELOPMENT; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; SILKWORM; TISSUE ENGINEERING;

ACTINS; ANIMALS; BOMBYX; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SHAPE; CELLS, CULTURED; CHONDROGENESIS; COLLAGEN TYPE II; DNA; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HUMANS; MESENCHYMAL STEM CELLS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; MODELS, BIOLOGICAL; NANOFIBERS; RNA, MESSENGER; VINCULIN;

EID: 70349267496     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2009.08.019     Document Type: Article

References (60)

1. Lysaght M.J., and Hazlehurst A.L. Tissue engineering: the end of the beginning. Tissue Eng 10 (2004) 309-320
2. Fischbach C., Chen R., Matsumoto T., Schmelzle T., Brugge J.C., Polverini P.J., et al. Engineering tumors with 3D scaffolds. Nat Methods 4 (2007) 855-860
3. Ghosh S., and Kaplan D.L. In vitro 3D human tissue models for osteochondral diseases. In: Polak L. (Ed). Advances in tissue engineering (2008), Imperial College Press, UK 781-805
4. Rosowski M., Falb M., Tschirschmann M., and Lauster R. Initiation of mesenchymal condensation in alginate hollow spheres-a useful model for understanding cartilage repair?. Artif Organs 30 (2006) 775-784
5. Mondrinos M.J., Koutzaki S., Lelkes P.I., and Finck C.M. A tissue-engineered model of fetal distal lung tissue. Am J Physiol Lung Cell Mol Physiol 293 (2007) L639-L650
6. Nesbitt T.L., Patel P.A., Yost M.J., Goodwin R.L., and Potts J.D. A 3-D model of coronary vessel development. In Vitro Cell Dev Biol Anim 43 (2007) 10-16
7. Clark C.C., Tolin B.S., and Brighton C.T. The effect of oxygen tension on proteoglycan synthesis and aggregation in mammalian growth plate chondrocyte. J Orthop Res 9 (1991) 477-484
8. Wang Y., Blasioli D.J., Kim H.J., Kim H.S., and Kaplan D.L. Cartilage tissue engineering with silk scaffolds and human articular chondrocytes. Biomaterials 27 (2006) 4434-4442
9. Zanetti N.C., and Solursh M. Induction of chondrogenesis in limb mesenchymal cultures by disruption of the actin cytoskeleton. J Cell Biol 99 (1984) 115-123
10. Brown P.D., and Benya P.D. Alterations in chondrocyte cytoskeletal architecture during phenotypic modulation by retinoic acid and dihydrocytochalasin B-induced reexpression. J Cell Biol 106 (1988) 171-179
11. Mallein-Gerin F., Garrone R., and Van der Rest M. Proteoglycan and collagen synthesis are correlated with actin organisation in dedifferentiating chondrocytes. Eur J Cell Biol 56 (1991) 364-373
12. Motta C., Fodor J., Szijgyarto Z., Juhasz T., Gergely P., Csernoch L., et al. Cytosolic free Ca(2+) concentration exhibits a characteristic temporal pattern during in vitro cartilage differentiation: a possible regulatory role of calcineurin in Ca-signalling of chondrogenic cells. Cell Calcium 44 (2008) 310-323
13. Jakob M., Demarteau O., Schafer D., Hintermann B., Dick W., Heberer M., et al. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81 (2001) 368-377
14. Engler A.J., Sen S., Sweeney H.L., and Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 126 (2006) 677-689
15. Peyton S.R., Ghajar C.M., Khatiwala C.B., and Putnam A.J. The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochem Biophys 47 (2007) 300-320
16. Lutolf M.P., and Hubbell J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23 (2005) 47-55
17. Ghosh K., Pan Z., Guan E., Ge S., Liu Y., Nakamura T., et al. Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials 28 (2007) 671-679
18. Ghosh K., and Ingber D. Micromechanical control of cell and tissue development: implications for tissue engineering. Adv Drug Deliv Rev 59 (2007) 1306-1318
19. Lee S.K., Malpeli M., Cancedda R., Utani A., Yamada Y., and Kleinman H.K. Laminin chain expression by chick chondrocytes and mouse cartilaginous tissues in vitro and in vivo. Exp Cell Res 236 (1997) 212-222
20. French M.M., Smith E., Akanbi T., Sanford T., Hecht J., Farach-Carson M.C., et al. Expression of the heparin sulfate proteoglycan, perlecan, during mouse embryogenesis and perlecan chondrogenic activity in vitro. J Cell Biol 145 (1999) 1103-1115
21. Salmivitra K., Talts J.F., Olsson M., Sasaki T., Timpl T., and Ekblom P. Binding of mouse nidogen-2 to basement membrane components and cells and its expression in embryogenic and adult tissue suggest complementary functions of the two nidogens. Exp Cell Res 279 (2002) 188-201
22. SundarRaj N., Fite D., Ledbetter S., Chakravarti S., and Hassell J.R. Perlecan is a component of cartilage matrix and promotes chondrocyte attachment. J Cell Sci 108 (1995) 2663-2672
23. Kvist A.J., Nystrom A., Hultenby K., Sasaki K., Talts J.F., and Aspberg A. The major basement membrane components localize to the chondrocytes pericellular matrix- a cartilage basement membrane equivalent?. Matrix Biol 27 (2007) 22-33
24. Solursh M., and Jensen K.L. The accumulation of basement membrane components during the onset of chondrogenesis and myogenesis in the chick wing bud. Development 104 (1988) 41-49
25. Stott N.S., Jiang T.X., and Choung C. Successive formative stages of precartilaginous mesenchymal condensations in vitro: modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 180 (1999) 314-324
26. Niswander L. Pattern formation: old models out on a limb. Nat Rev Genet 4 (2003) 133-143
27. Tickle C. Patterning systems - from one end of the limb to the other. Dev Cell 4 (2003) 449-458
28. Tacchetti C., Tavella S., Dozin B., Quarto R., Robino G., and Cancedda R. Cell condensation in chondrogenic differentiation. Exp Cell Res 200 (1992) 26-33
29. Kavalkovich K.W., Boynton R.E., Murphy J.M., and Barry F. Chondrogenic differentiation of human mesenchymal stem cells within an alginate layer culture system. In Vitro Cellular & Developmental Biology - Animal 38 (2002) 457-466
30. Ichinose S., Tagami M., Muneta T., and Sekiya I. Morphological examination during in vitro cartilage formation by human mesenchymal stem cells. Cell Tissue Res 322 (2005) 217-226
31. Daniels K., Reiter R., and Solursh M. Micromass cultures of limb and other mesenchyme. Methods Cell Biol 51 (1996) 237-247
32. Oster G.F., Murraray J.D., and Harris A.K. Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morphol 78 (1983) 83-125
33. Wolpert L., and Hornbruch A. Double anterior chick limb buds and models for cartilage rudiment specification. Development 109 (1990) 961-966
34. Ghosh S., Parker S.T., Wang X., Kaplan D.L., and Lewis J.A. Direct-write assembly of micro-periodic silk fibroin scaffolds for tissue engineering applications. Adv Funct Mater 18 (2008) 1883-1889
35. Li C., Vepari C., Jin H.J., Kim H.J., and Kaplan D.L. Electrospun silk-BMP-2 scaffolds for bone tissue engineering. Biomaterials 27 (2006) 3115-3124
36. Jin H.J., Fridrikh S.V., Rutledge G.C., and Kaplan D.L. Electrospinning Bombyx mori silk with poly(ethylene oxide). Biomacromolecules 3 (2002) 1233-1239
37. Wang M., Jin H.J., Kaplan D.L., and Rutledge G.C. Mechanical properties of electrospun silk fibers. Macromolecules 37 (2004) 6856-6864
38. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., and Crombrugghe de B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 6 (2002) 2813-2828
39. Wright E., Hargrave M.R., Christiansen J., Cooper L., Kun J., Evans T., et al. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat Genet 9 (1995) 15-20
40. Kulyk W., Upholt W.B., and Kosher R.A. Fibronectin gene expression during limb cartilage differentiation. Development 106 (1989) 449-455
41. Holmes D.F., Graham H.K., Trotter J.A., and Kadler K.E. STEM/TEM studies of collagen fibril assembly. Micron 32 (2001) 273-285
42. Yang K.G., Saris D.B., Geuze R.E., Helm Y.J., Rijen M.H., Verbout A.J., et al. Impact of expansion and redifferentiation conditions on chondrogenic capacity of cultured chondrocytes. Tissue Eng 12 (2006) 2435-2447
43. Kramer J., Klinger M., Kruse C., Faza M., Hargus G., and Rohwedel J. Ultrastructural analysis of mouse embryonic stem cell-derived chondrocytes. Anat Embryol 210 (2005) 175-185
44. Candiello J., Balasubramani M., Schreiber E.M., Cole G.J., Mayer U., Halfter W., et al. Biomechanical properties of native basement membranes. FEBS J 274 (2007) 2897-2908
45. Welling L.W., Zupka M.T., and Welling D.J. Mechanical properties of basement membrane. News Physiol Sci 10 (1995) 30-35
46. Li W.J., Jiang Y.J., and Tuan R.S. Chondrocyte phenotype in engineered fibrous matrix is regulated by fiber size. Tissue Eng 12 (2006) 1775-1785
47. Hartmann A., Boukamp P., and Friedl P. Confocal reflection imaging of 3D fibrin polymers. Blood Cells Mol Dis 36 (2006) 191-193
48. Zaman M.H., Trapani L.M., Siemeski A., MacKellar D., Gong H.Y., Kamm R.D., et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci U S A 103 (2006) 10889-10894
49. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., and de Crombrugghe B. Sox9 is required for cartilage formation. Mol Cell Biol 17 (1997) 2336-2346
50. Miura T., and Shiota K. TGF-β2 acts as an 'activator' molecule in reaction-diffusion model and is involved in cell sorting phenomenon in mouse limb micromass culture. Dev Dyn 217 (2000) 241-249
51. Frenz D.A., Jaikaria N.S., and Newman S.A. The mechanism of precartilage mesenchymal condensation: a major role for interaction of the cell surface with the amino-terminal heparin-binding domain of fibronectin. Dev Biol 136 (1989) 97-103
52. Widelitz R.B., and Jiang T.X. Adhesion molecules in skeletogenesis: II. Neural cell adhesion molecules mediate precartilaginous mesenchymal condensations and enhance chondrogenesis. J Cell Physiol 156 (1993) 399-411
53. Hall B.K., and Miyake T. All for one and one for all. Bioessays 22 (2000) 138-147
54. Häusler G., Helmreich M., Marlovits S., and Egerbacher M. Integrins and extracellular matrix proteins in the human childhood and adolescent growth plate. Calcif Tissue Int 71 (2002) 212-218
55. Wright M.O., Nishida K., Bavington C., Godolphin J.L., Dunne E., Walmsley S., et al. Hyperpolarisation of cultured human chondrocytes following cyclical pressure-induced strain: evidence of a role for alpha 5 beta 1 integrin as a chondrocyte mechanoreceptor. J Orthop Res 15 (1997) 742-747
56. Hall A. Rho GTPases and the actin cytoskeleton. Science 279 (1998) 509-514
57. McBeath R., Pirone D.M., Nelson C.M., Bhadriraju K., and Chen C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6 (2004) 483-495
58. Coelho C.N., and Kosher R.A. Gap junctional communication of cartilage: in vitro evaluation. Dev Biol 144 (1991) 47-53
59. Zimmermann B. Assembly and disassembly of gap junctions during mesenchymal cell condensation and early chondrogenesis in limb bud of mouse embryo. J Anat 138 (1984) 351-363
60. Barna M., and Niswander L. Visualization of cartilage formation: insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev Cell 12 (2007) 931-941