Engineering endochondral bone: In vitro studies

Tissue Engineering - Part A

Volumn 15, Issue 3, 2009, Pages 625-634

  Oliveira, Serafim M ^a,b,c,d   Amaral, Isabel F ^b   Barbosa, Mário A ^b,c   Teixeira, Cristina C ^d  

^a POLYTECHNIC INSTITUTE OF VISEU   (Portugal)

^b INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; BODY FLUIDS; BONE; CARTILAGE; CELL MEMBRANES; CELL PROLIFERATION; CHITIN; CHITOSAN; LIGAMENTS; PATHOLOGY; SCAFFOLDS; TISSUE ENGINEERING;

ALKALINE PHOSPHATASE ACTIVITY; BONE FORMATION; CHICKEN EMBRYO; CHITOSAN SCAFFOLD; CHONDROCYTE; CHONDROCYTE MATURATION; CHONDROCYTES; CLINICAL APPLICATION; ENDOCHONDRAL OSSIFICATION; EXTRACELLULAR MATRICES; HYPERTROPHIC CHONDROCYTES; IN-VITRO; MATRIX SYNTHESIS; MECHANICAL ANALYSIS; RETINOIC ACIDS; TIME POINTS; TYPE X COLLAGEN;

MECHANICAL PROPERTIES;

ALKALINE PHOSPHATASE; CHITOSAN; COLLAGEN TYPE 10; RETINOIC ACID; TISSUE SCAFFOLD; DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL DAMAGE; CELL HYPERTROPHY; CELL ISOLATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENCHONDRAL OSSIFICATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; STERNUM; SYNTHESIS; TISSUE ENGINEERING; ANIMAL; BIOMECHANICS; BONE; CARTILAGE; CHICK EMBRYO; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION PROFILING; METABOLISM; METHODOLOGY; PHYSIOLOGY; POROSITY; SPONGE (PORIFERA);

STERNA;

ALKALINE PHOSPHATASE; ANIMALS; BIOMECHANICS; BONE AND BONES; CARTILAGE; CELLS, CULTURED; CHICK EMBRYO; CHITOSAN; CHONDROCYTES; COLLAGEN TYPE X; DNA; GENE EXPRESSION PROFILING; PORIFERA; POROSITY; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRETINOIN;

EID: 64549143844     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0051     Document Type: Article

References (65)

1. Steinemann, S.G. Metal implants and surface reactions. Injury 27, 16, 1996.
2. Disegi, J.A., and Eschbach, L. Stainless steel in bone surgery. Injury 31, 2, 2000.
3. Reitman, R.D., Emerson, R., Higgins, L., and Head, W. Thirteen year results of total hip arthroplasty using a tapered titanium femoral component inserted without cement in patients with type C bone. J Arthroplasty 18, 116, 2003.
4. Epinette, J.A., Manley, M.T., D'Antonio, J.A., Edidin, A.A., and Capello, W.N. A 10-year minimum follow-up of hydroxyapatite-coated threaded cups: clinical, radiographic and survivorship analyses with comparison to the literature. J Arthroplasty 18, 140, 2003.
5. Xynos, I.D., Hukkanen, M.V., Batten, J.J., Buttery, L.D., Hench, L.L., and Polak, J.M. Bioglass 45S5 stimulates osteoblast turnover and enhances bone formation in vitro: implications and applications for bone tissue engineering. Calcif Tissue Int 67, 321, 2000.
6. Barrias, C.C., Ribeiro, C.C., and Barbosa, M.A. Adhesion and proliferation of human osteoblastic cells seeded on injectable hydroxyapatite microspheres. Bioceramics 254, 877, 2004.
7. Saito, N., and Takaoka, K. New synthetic biodegradable polymers as BMP carriers for bone tissue engineering. Biomaterials 24, 2287, 2003.
8. Suzuki, T., Kawamura, H., Kasahara, T., and Nagasaka, H. Resorbable poly-L-lactide plates and screws for the treatment of mandibular condylar process fractures: a clinical and radiologic follow-up study. J Oral Maxillofac Surg 62, 919, 2004.
9. Sittinger, M., Reitzel, D., Dauner, M., Hierlemann, H., Hammer, C., Kastenbauer, E., Planck, H., Burmester, G.R., and Bujia, J. Resorbable polyesters in cartilage engineering: affinity and biocompatibility of polymer fiber structures to chondrocytes. J Biomed Mater Res 33, 57, 1996.
10. Vaccaro, A.R., Singh, K., Haid, R., Kitchel, S., Wuisman, P., Taylor, W., Branch, C., and Garfin, S. The use of bioabsorbable implants in the spine. Spine J 3, 227, 2003.
11. Jianqi, H., Hong, H., Lieping, S., and Genghua, G. Comparison of calcium alginate film with collagen membrane for guided bone regeneration in mandibular defects in rabbits. J Oral Maxillofac Surg 60, 1449, 2002.
12. Chan, C., Thompson, I., Robinson, P., Wilson, J., and Hench, L. Evaluation of bioglass/dextran composite as a bone graft substitute. Int J Oral Maxillofac Surg 31, 73, 2002.
13. Mukherjee, D.P., Tunkle, A.S., Roberts, R.A., Clavenna, A., Rogers, S., and Smith, D. An animal evaluation of a paste of chitosan glutamate and hydroxyapatite as a synthetic bone graft material. J Biomed Mater Res B Appl Biomater 67B,603, 2003.
14. Sashiwa, H., and Aiba, S. Chemically modified chitin and chitosan as biomaterials. Prog Polym Sci 89, 887, 2004.
15. Hoekstra, A., Struszczyk, H., and Kivekas, O. Percutaneous microcrystalline chitosan application for sealing arterial puncture sites. Biomaterials 19, 1467, 1998.
16. Lee, K.Y., Ha, W.S., and Park, W.H. Blood compatibility and biodegradability of partially N-acylated chitosan derivatives. Biomaterials 16, 1211, 1995.
17. Suh, J.K., and Matthew, H.W. Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: a review. Biomaterials 21, 2589, 2000.
18. Hirano, S., Tsuchida, H., and Nagao, N. N-acetylation in chitosan and the rate of its enzymic hydrolysis. Biomaterials 10, 574, 1989.
19. Prashanth, K.V.H., and Tharanathan, R.N. Chitin/chitosan: modifications and their unlimited application potential-an overview. Trends Food Sci Technol 18, 117, 2007.
20. Chellat, F., Tabrizian, M., Dumitriu, S., Chornet, E., Hilaire, C., and Yahia, R. Study of biodegradation behavior of chitosan-xanthan microspheres in simulated physiological media. J Biomed Mater Res 53, 592, 2000.
21. Lahiji, A., Sohrabi, A., Hungerford, D.S., and Frondoza, C.G. Chitosan supports the expression of extracellular matrix proteins in human osteoblasts and chondrocytes. J Biomed Mater Res 51, 586, 2000.
22. Nettles, D.L., Elder, S.H., and Gilbert, J.A. Potential use of chitosan as a cell scaffold material for cartilage tissue engineering. Tissue Eng 8, 1009, 2002.
23. Lu, J.X., Prudhommeaux, F., Meunier, A., Sedel, L., and Guillemin, G. Effects of chitosan on rat knee cartilages. Biomaterials 20, 1937, 1999.
24. Abe, M., Takahashi, M., Tokura, S., Tamura, H., and Nagano, A. Cartilage-scaffold composites produced by bioresorbable beta-chitin sponge with cultured rabbit chondrocytes. Tissue Eng 10, 585, 2004.
25. Sechriest, V.F., Miao, Y.J., Niyibizi, C., Westerhausen-Larson, A., Matthew, H.W., Evans, C.H., Fu, F.H., and Suh, J.K. GAGaugmented polysaccharide hydrogel: a novel biocompatible and biodegradable material to support chondrogenesis. J Biomed Mater Res 49, 534, 2000.
26. Rajpurohit, R., Koch, C.J., Tao, Z., Teixeira, C.M., and Shapiro, I.M. Adaptation of chondrocytes to low oxygen tension: relationship between hypoxia and cellular metabolism. J Cell Physiol 168, 424, 1996.
27. Maes, C., Carmeliet, P., Moermans, K., Stockmans, I., Smets, N., Collen, D., Bouillon, R., and Carmeliet, G. Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 111, 61, 2002.
28. Petersen, W., Tsokos, M., and Pufe, T. Expression of VEGF121 and VEGF165 in hypertrophic chondrocytes of the human growth plate and epiphyseal cartilage. J Anat 201,153, 2002.
29. Pullig, O., Weseloh, G., Ronneberger, D., Kakonen, S., and Swoboda, B. Chondrocyte differentiation in human osteoarthritis: expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif Tissue Int 67, 230, 2000.
30. Hashimoto, S., Ochs, R.L., Rosen, F., Quach, J., McCabe, G., Solan, J., Seegmiller, J.E., Terkeltaub, R., and Lotz, M. Chondrocyte-derived apoptotic bodies and calcification of articular cartilage. Proc Natl Acad Sci USA 95, 3094, 1998.
31. Pullig, O., Weseloh, G., Gauer, S., and Swoboda, B. Osteopontin is expressed by adult human osteoarthritic chondrocytes: protein andmRNAanalysis of normal and osteoarthritic cartilage. Matrix Biol 19, 245, 2000.
32. Eerola, I., Salminen, H., Lammi, P., Lammi, M., von der Mark, K., Vuorio, E., and Saamanen, A.M. Type X collagen, a natural component of mouse articular cartilage: association with growth, aging, and osteoarthritis. Arthritis Rheum 41,1287, 1998.
33. Amaral, I.F., Sampaio, P., and Barbosa, M.A. Threedimensional culture of human osteoblastic cells in chitosan sponges: the effect of the degree of acetylation. J Biomed Mater Res A 76, 335, 2006.
34. Mow, V.C., Kuei, S.C., Lai, W.M., and Armstrong, C.G. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. J Biomech Eng 102,73, 1980.
35. Iwamoto, M., Shapiro, I.M., Yagami, K., Boskey, A.L., Leboy, P.S., Adams, S.L., and Pacifici, M. Retinoic acid induces rapid mineralization and expression of mineralizationrelated genes in chondrocytes. Exp Cell Res 207, 413, 1993.
36. Teixeira, C.C., Hatori, M., Leboy, P.S., Pacifici, M., and Shapiro, I.M. A rapid and ultrasensitive method for measurement of DNA, calcium and protein content, and alkaline phosphatase activity of chondrocyte cultures. Calcif Tissue Int 56, 252, 1995.
37. Nehrer, S., Breinan, H.A., Ramappa, A., Young, G., Shortkroff, S., Louie, L.K., Sledge, C.B., Yannas, I.V., and Spector, M. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials 18,769, 1997.
38. Karande, T.S., Ong, J.L., and Agrawal, C.M. Diffusion in musculoskeletal tissue engineering scaffolds: design issues related to porosity, permeability, architecture, and nutrient mixing. Ann Biomed Eng 32, 1728, 2004.
39. VandeVord, P.J., Matthew, H.W., DeSilva, S.P., Mayton, L., Wu, B., and Wooley, P.H. Evaluation of the biocompatibility of a chitosan scaffold in mice. J Biomed Mater Res 59, 585, 2002.
40. Hong, Y., Song, H., Gong, Y., Mao, Z., Gao, C., and Shen, J. Covalently crosslinked chitosan hydrogel: Properties of in vitro degradation and chondrocyte encapsulation. Acta Biomater 3, 23, 2007.
41. Ho, M., Wang, D., Hsieh, H., Liu, H.C., Hsien, T.Y., Lai, J.Y., and Hou, L.T. Preparation and characterization of RGDimmobilized chitosan scaffolds. Biomaterials 26, 3197, 2005.
42. Amaral, I.F., Cordeiro, A.L., Sampaio, P., and Barbosa, M.A. Attachment, spreading and short-term proliferation of human osteoblastic cells cultured on chitosan films with different degrees of acetylation. J Biomater Sci Polym Ed 18,469, 2007.
43. Hoemann, C.D., Sun, J., Legare, A., McKee, M.D., and Buschmann, M.D. Tissue engineering of cartilage using an injectable and adhesive chitosan-based cell-delivery vehicle. Osteoarthritis Cartilage 13, 318, 2005.
44. Griffon, D.J., Sedighi, M.R., Schaeffer, D.V., Eurell, J.A., and Johnson, A.L. Chitosan scaffolds: interconnective pore size and cartilage engineering. Acta Biomater 2, 313, 2006.
45. Underhill, T.M., and Weston, A.D. Retinoids and their receptors in skeletal development. Microsc Res Tech 43, 137, 1998.
46. Cohen, A.J., Lassova, L., Golden, E.B., Niu, Z., and Adams, S.L. Retinoids directly activate the collagen X promoter in prehypertrophic chondrocytes through a distal retinoic acid response element. J Cell Biochem 99, 269, 2006.
47. Pacifici, M., Golden, E.B., Iwamoto, M., and Adams, S.L. Retinoic acid treatment induces type X collagen gene expression in cultured chick chondrocytes. Exp Cell Res 195,38, 1991.
48. Gentili, C., Bianco, P., Neri, M., Malpeli, M., Campanile, G., Castagnola, P., Cancedda, R., and Cancedda, F.D. Cellproliferation, extracellular-matrix mineralization, and ovotransferrin transient expression during in-vitro differentiation of chick hypertrophic chondrocytes into osteoblast-like cells. J Cell Biol 122, 703, 1993.
49. Naumann, A., Dennis, J.E., Awadallah, A., Carrino, D.A., Mansour, J.M., Kastenbauer, E., and Caplan, A.I. Immunochemical and mechanical characterization of cartilage subtypes in rabbit. J Histochem Cytochem 50, 1049, 2002.
50. Wang, W., and Kirsch, T. Retinoic acid stimulates annexinmediated growth plate chondrocyte mineralization. J Cell Biol 157, 1061, 2002.
51. Whyte, M.P. Hypophosphatasia and the role of alkaline phosphatase in skeletal mineralization. Endocr Rev 15, 439, 1994.
52. Lewinson, D., Toister, Z., and Silbermann, M. Quantitative and distributional changes in the activity of alkaline phosphatase during the maturation of cartilage. J Histochem Cytochem 30, 261, 1982.
53. Amaral, I.F., Sampaio, P., and Barbosa, M.A. Threedimensional culture of human osteoblastic cells in chitosan sponges: the effect of the degree of acetylation. J Biomed Mater Res A 76, 335, 2005.
54. Park, J.H., Park, B.H., Kim, H.K., Park, T.S., and Baek, H.S. Hypoxia decreases Runx2/Cbfa1 expression in human osteoblast-like cells. Mol Cell Endocrinol 192, 197, 2002.
55. Utting, J.C., Robins, S.P., Brandao-Burch, A., Orriss, I.R., Behar, J., and Arnett, T.R. Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp Cell Res 312, 1693, 2006.
56. Warren, S.M., Steinbrech, D.S., Mehrara, B.J., Saadeh, P.B., Greenwald, J.A., Spector, J.A., Bouletreau, P.J., and Longaker, M.T. Hypoxia regulates osteoblast gene expression. J Surg Res 99, 147, 2001.
57. Salim, A., Nacamuli, R.P., Morgan, E.F., Giaccia, A.J., and Longaker, M.T. Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J Biol Chem 279, 40007, 2004.
58. Vu, T.H., Shipley, J.M., Bergers, G., Berger, J.E., Helms, J.A., Hanahan, D., Shapiro, S.D., Senior, R.M., and Werb, Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411, 1998.
59. Skawina, A., Litwin, J.A., Gorczyca, J., and Miodonski, A.J. The vascular system of human fetal long bones: a scanning electron microscope study of corrosion casts. J Anat 185,369, 1994.
60. Pfander, D., Cramer, T., Schipani, E., and Johnson, R.S. HIF-1alpha controls extracellular matrix synthesis by epiphyseal chondrocytes. J Cell Sci 116, 1819, 2003.
61. Deckers, M.M., Karperien, M., van der Bent, C., Yamashita, T., Papapoulos, S.E., and Lowik, C.W. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141, 1667, 2000.
62. Gerber, H.P., Vu, T.H., Ryan, A.M., Kowalski, J., Werb, Z., and Ferrara, N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5, 623, 1999.
63. Nakagawa, M., Kaneda, T., Arakawa, T., Morita, S., Sato, T., Yomada, T., Hanada, K., Kumegawa, M., and Hakeda, Y. Vascular endothelial growth factor (VEGF) directly enhances osteoclastic bone resorption and survival of mature osteoclasts. FEBS Lett 473, 161, 2000.
64. Pfander, D., Kortje, D., Zimmermann, R.,Weseloh, G., Kirsch, T., Gesslein, M., Cramer, T., and Swoboda, B. Vascular endothelial growth factor in articular cartilage of healthy and osteoarthritic human knee joints. Ann RheumDis 60, 1070, 2001.
65. Oliveira, S.M., Turner, G., Mijares, D., Amaral, I.F., Barbosa, M.A., and Teixeira, C.C. Engineering endochondral bone: in vivo studies. 2007.