Growth factor stimulation improves the structure and properties of scaffold-free engineered auricular cartilage constructs

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Rosa, Renata G ^a,b   Joazeiro, Paulo P ^b   Bianco, Juares ^a,b   Kunz, Manuela ^a   Weber, Joanna F ^a   Waldman, Stephen D ^a,c,d  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c RYERSON UNIVERSITY   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ELASTIN; GROWTH FACTOR; INSULIN; SOMATOMEDIN C; TISSUE SCAFFOLD; TRANSFORMING GROWTH FACTOR BETA1; COLLAGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BIOCHEMISTRY; CARTILAGE CELL; EAR CARTILAGE; EXTRACELLULAR MATRIX; FEMALE; NONHUMAN; PROTEIN EXPRESSION; THICKNESS; TISSUE ENGINEERING; TISSUE STRUCTURE; ANIMAL; BIOMECHANICS; CELL CULTURE; CYTOLOGY; METABOLISM; PHYSIOLOGY; RABBIT; TISSUE SCAFFOLD;

ANIMALS; BIOMECHANICAL PHENOMENA; CELLS, CULTURED; CHONDROCYTES; COLLAGEN; EAR CARTILAGE; ELASTIN; FEMALE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; RABBITS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84925418134     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105170     Document Type: Article

References (58)

1. Cao Y, Vacanti JP, Paige KT, Upton J, Vacanti CA (1997) Transplantation of chondrocytes utilizing a polymer-cell construct to produce tissue-engineered cartilage in the shape of a human ear. Plast Reconstr Surg 100: 297-302.
2. Langer R, Vacanti JP (1993) Tissue engineering. Science 260: 920-926. (Pubitemid 23209960)
3. Shieh SJ, Terada S, Vacanti JP (2004) Tissue engineering auricular reconstruction: in vitro and in vivo studies. Biomaterials 25: 1545-1557. (Pubitemid 38091534)
4. Yanaga H, Imai K, Koga M, Yanaga K (2012) Cell-engineered human elastic chondrocytes regenerate natural scaffold in vitro and neocartilage with neoperichondrium in the human body post-transplantation. Tissue Eng Pt A 18: 2020-2029. doi:10.1089/ten.TEA.2011.0370.
5. Walton RL, Beahm EK (2002) Auricular reconstruction for microtia: Part II. Surgical techniques. Plast Reconstr Surg 110: 234-249.
6. Naumann A, Dennis JE, Aigner J, Coticchia J, Arnold J, et al. (2004) Tissue engineering of autologous cartilage grafts in three-dimensional in vitro macroaggregate culture system. Tissue Eng 10: 1695-1706. doi:10.1089/ten.2004. 10.1695. (Pubitemid 40054211)
7. Hellingman CA, Verwiel ETP, Slagt I, Koevoet W, Poublon RML, et al. (2011) Differences in cartilage-forming capacity of expanded human chondrocytes from ear and nose and their gene expression profiles. Cell Transplant 20: 925-940. doi:10.3727/096368910X539119.
8. Madsen K, Moskalewski S, Mark von der K, Friberg U (1983) Synthesis of proteoglycans, collagen, and elastin by cultures of rabbit auricular chondrocytes- relation to age of the donor. Dev Biol 96: 63-73.
9. Bomhard von A, Veit J, Bermueller C, Rotter N, Staudenmaier R, et al. (2013) Prefabrication of 3D cartilage contructs: towards a tissue engineered auricle - a model tested in rabbits. PLoS One 8: e71667. doi:10.1371/journal. pone.0071667.
10. Yanaga H, Imai K, Yanaga K (2009) Generative surgery of cultured autologous auricular chondrocytes for nasal augmentation. Aesthetic Plast Surg 33: 795-802. doi:10.1007/s00266-009-9399-8.
11. Isogai N, Asamura S, Higashi T, Ikada Y, Morita S, et al. (2004) Tissue engineering of an auricular cartilage model utilizing cultured chondrocytepoly(L-lactide-epsilon-caprolactone) scaffolds. Tissue Eng 10: 673-687. doi:10.1089/1076327041348527. (Pubitemid 38880386)
12. Reiffel AJ, Kafka C, Hernandez KA, Popa S, Perez JL, et al. (2013) High-fidelity tissue engineering of patient-specific auricles for reconstruction of pediatric microtia and other auricular deformities. PLoS ONE 8: e56506. doi:10.1371/journal.pone.0056506.
13. Giardini-Rosa R, Joazeiro PP, Thomas K, Collavino K, Weber J, et al. (2014) Development of scaffold-free elastic cartilaginous constructs with structural similarities to auricular cartilage. Tissue Eng Pt A 20: 1012-1026. doi:10.1089/ten.TEA.2013.0159.
14. Moskalewski S (1981) The elastogenetic process in transplants and cultures of isolated auricular chondrocytes. Connect Tissue Res 8: 171-174.
15. Moskalewski S, Adamiec I, Gołaszewska A (1979) Maturation of rabbit auricular chondrocytes grown in vitro in monolayer culture. Am J Anat 155: 339-348. doi:10.1002/aja.1001550305. (Pubitemid 9221373)
16. Moskalewski S, Rybicka E (1977) The influence of the degree of maturation of donor tissue on the reconstruction of elastic cartilage by isolated chondrocytes. Acta Anat (Basel) 97: 231-240. (Pubitemid 8065424)
17. Nimeskern L, van Osch GJVM, Müller R, Stok KS (2014) Quantitative evaluation of mechanical properties in tissue-engineered auricular cartilage. Tissue Eng Pt B Rev 20: 17-27. doi:10.1089/ten.TEB.2013.0117.
18. Foster J, Rich CB, Florini JR (1987) Insulin-like growth factor I, somatomedin C, induces the synthesis of tropoelastin in aortic tissue. Coll Relat Res 7: 161-169. (Pubitemid 18067541)
19. Fujisawa T, Hattori T, Ono M, Uehara J, Kubota S, et al. (2008) CCN family 2/connective tissue growth factor (CCN2/CTGF) stimulates proliferation and differentiation of auricular chondrocytes. Osteoarthr Cartilage 16: 787-795. doi:10.1016/j.joca.2007.11.001.
20. Long JL, Tranquillo RT (2003) Elastic fiber production in cardiovascular tissueequivalents. Matrix Biol 22: 339-350. (Pubitemid 36993759)
21. Shi J, Wang A, Sen S, Wang Y, Kim HJ, et al. (2012) Insulin induces production of new elastin in cultures of human aortic smooth muscle cells. Am J Pathol 180: 715-726. doi:10.1016/j.ajpath.2011.10.022.
22. van der Kraan PM, Buma P, van Kuppevelt T, van den Berg WB (2002) Interaction of chondrocytes, extracellular matrix and growth factors: relevance for articular cartilage tissue engineering. Osteoarthr Cartilage 10: 631-637. (Pubitemid 34993949)
23. Yoon DM, Fisher JP (2006) Chondrocyte signaling and artificial matrices for articular cartilage engineering. Adv Exp Med Biol 585: 67-86.
24. Mishell RI, Shiigi JM, Mishell BB, Grabstein KH, Shiigi SM (1980) Prevention of the immunosuppressive effects of glucocorticosteroids by cell-free factors from adjuvant-activated accessory cells. Immunopharmacology 2: 233-245. (Pubitemid 12190046)
25. Brenner JM, Kunz M, Tse MY, Winterborn A, Bardana DD, et al. (2013) Development of large engineered cartilage constructs from a small population of cells. Biotechnol Prog 29: 213-221. doi:10.1002/btpr.1670.
26. Khan AA, Suits JMT, Kandel RA,Waldman SD (2009) The effect of continuous culture on the growth and structure of tissue-engineered cartilage. Biotechnol Prog 25: 508-515. doi:10.1002/btpr.108.
27. Jurvelin JS, Räsänen T, Kolmonen P, Lyyra T (1995) Comparison of optical, needle probe and ultrasonic techniques for the measurement of articular cartilage thickness. J Biomech 28: 231-235.
28. Hayes WC, Keer LM, Herrmann G, Mockros LF (1972) A mathematical analysis for indentation tests of articular cartilage. J Biomech 5: 541-551.
29. Jin H, Lewis JL (2004) Determination of Poisson's ratio of articular cartilage by indentation using different-sized indenters. J Biomech Eng 126: 138-145. (Pubitemid 38621126)
30. Kim YJ, Sah RL, Doong JY, Grodzinsky AJ (1988) Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174: 168-176. (Pubitemid 18261664)
31. 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)
32. Goldberg RL, Kolibas LM (1990) An improved method for determining proteoglycans synthesized by chondrocytes in culture. Connect Tissue Res 24: 265-275.
33. Woessner JF (1961) The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93: 440-447.
34. Heinegard D, Bayliss M, Lorenzo P (1998) Biochemistry and metabolism of normal and osteoarthritic cartilage. In: Brandt KD, Doherty M, Lohmander LS, Eds.Osteoarthritis. New York: Oxford University Press; 74-84.
35. Besl PJ, McKay ND (1992) A method for registration of 3-D shapes. IEEE T Pattern Anal 14: 239-256.
36. Brent B (1977) The acquired auricular deformity. A systematic approach to its analysis and reconstruction. Plast Reconstr Surg 59: 475-485.
37. Nagata S (1993) A new method of total reconstruction of the auricle for microtia. Plast Reconstr Surg 92: 187-201.
38. Tanzer RC (1959) Total reconstruction of the external ear. Plast Reconstr Surg Transplant Bull 23: 1-15.
39. Ng KW, O'Conor CJ, Kugler LE, Cook JL, Ateshian GA, et al. (2011) Transient supplementation of anabolic growth factors rapidly stimulates matrix synthesis in engineered cartilage. Ann Biomed Eng 39: 2491-2500. doi:10.1007/s10439-011-0356-8.
40. Arévalo-Silva CA, Cao Y, Weng Y, Vacanti M, Rodríguez A, et al. (2001) The effect of fibroblast growth factor and transforming growth factor-beta on porcine chondrocytes and tissue-engineered autologous elastic cartilage. Tissue Eng 7: 81-88. (Pubitemid 32175964)
41. Bos PK, Van Osch GJ, Frenz DA, Verhaar JA, Verwoerd-Verhoef HL (2001) Growth factor expression in cartilage wound healing: temporal and spatial immunolocalization in a rabbit auricular cartilage wound model. Osteoarthr Cartilage 9: 382-389. doi:10.1053/joca.2000.0399. (Pubitemid 32454782)
42. Goldring MB, Tsuchimochi K, Ijiri K (2006) The control of chondrogenesis. J Cell Biochem 97: 33-44. doi:10.1002/jcb.20652. (Pubitemid 43050970)
43. Gaissmaier C, Koh JL, Weise K (2008) Growth and differentiation factors for cartilage healing and repair. Injury 39 Suppl 1: S88-S96. doi:10.1016/j.injury.2008.01.035.
44. Kelly T-AN, Fisher MB, Oswald ES, Tai T, Mauck RL, et al. (2008) Low-serum media and dynamic deformational loading in tissue engineering of articular cartilage. Ann Biomed Eng 36: 769-779. doi:10.1007/s10439-008-9476-1.
45. Kisiday JD, Kurz B, DiMicco MA, Grodzinsky AJ (2005) Evaluation of medium supplemented with insulin-transferrin-selenium for culture of primary bovine calf chondrocytes in three-dimensional hydrogel scaffolds. Tissue Eng 11: 141-151. doi:10.1089/ten.2005.11.141. (Pubitemid 40515182)
46. Cigan AD, Nims RJ, Albro MB, Esau JD, Dreyer MP, et al. (2013) Insulin, ascorbate, and glucose have a much greater influence than transferrin and selenous acid on the in vitro growth of engineered cartilage in chondrogenic media. Tissue Eng Pt A 19: 1941-1948. doi:10.1089/ten.TEA.2012.0596.
47. Maor G, Silbermann M, Mark von der K, Heingard D, Laron Z (1993) Insulin enhances the growth of cartilage in organ and tissue cultures of mouse neonatal mandibular condyle. Calcified Tissue Int 52: 291-299. (Pubitemid 23097161)
48. Jensen DE, Rich CB, Terpstra AJ, Farmer SR, Foster JA (1995) Transcriptional regulation of the elastin gene by insulin-like growth factor-I involves disruption of Sp1 binding. Evidence for the role of Rb in mediating Sp1 binding in aortic smooth muscle cells. J Biol Chem 270: 6555-6563.
49. Hinton RJ, Serrano M, So S (2009) Differential gene expression in the perichondrium and cartilage of the neonatal mouse temporomandibular joint. Orthod Craniofac Res 12: 168-177. doi:10.1111/j.1601-6343.2009.01450.x.
50. Shibata S, Fukuoka H, Sato R, Abe T, Suzuki Y (2012) An in situ hybridization study of the insulin-like growth factor system in developing condylar cartilage of the fetal mouse mandible. Eur J Histochem 56: e23. doi:10.4081/ejh.2012.23.
51. Togo T, Utani A, Naitoh M, Ohta M, Tsuji Y, et al. (2006) Identification of cartilage progenitor cells in the adult ear perichondrium: utilization for cartilage reconstruction. Lab Invest 86: 445-457. doi:10.1038/labinvest.3700409.
52. Van Osch GJ, Van Der Veen SW, Burger EH, Verwoerd-Verhoef HL (2000) Chondrogenic potential of in vitro multiplied rabbit perichondrium cells cultured in alginate beads in defined medium. Tissue Eng 6: 321-330. doi:10.1089/107632700418047. (Pubitemid 30655942)
53. Lammi PE, Lammi MJ, Hyttinen MM, Panula H, Kiviranta I, et al. (2002) Sitespecific immunostaining for type X collagen in noncalcified articular cartilage of canine stifle knee joint. Bone 31: 690-696. (Pubitemid 36092092)
54. Pelttari K, Steck E, Richter W (2008) The use of mesenchymal stem cells for chondrogenesis. Injury 39 Suppl 1: S58-S65. doi:10.1016/j.injury.2008.01. 038.
55. Wang J, Zhou J, Bondy CA (1999) IGF promotes longitudinal bone growth by insulin-like actions augmenting chondrocyte hypertrophy. FASEB J 13: 1985-1990. (Pubitemid 29517628)
56. Kamil SH, Vacanti MP, Aminuddin BS, Jackson MJ, Vacanti CA, et al. (2004) Tissue engineering of a human sized and shaped auricle using a mold. Laryngoscope 114: 867-870. doi:10.1097/00005537-200405000-00015. (Pubitemid 38625539)
57. Yotsuyanagi T, Urushidate S, Watanabe M, Sawada Y (1999) Reconstruction of a Three-Dimensional Structure Using Cartilage Regenerated from the Perichondrium of Rabbits. Plast Reconstr Surg 103: 1120.
58. Nimeskern L, Martínez Ávila H, Sundberg J, Gatenholm P, Müller R, et al. (2013) Mechanical evaluation of bacterial nanocellulose as an implant material for ear cartilage replacement. J Mech Behav Biomed Mater 22: 12-21. doi:10.1016/j.jmbbm.2013.03.005.