Injectable cartilage tissue engineering

Expert Opinion on Biological Therapy

Volumn 4, Issue 12, 2004, Pages 1849-1859

  Elisseeff, Jennifer ^a  

^a Johns Hopkins University School of Medicine   (United States)

Author keywords

Biomaterials; Cartilage; Hydrogels; Injectable; Stem cells; Tissue engineering

Indexed keywords

ALGINIC ACID; ARGINYLGLYCYLASPARTIC ACID; BIOMATERIAL; CHONDROITIN SULFATE; COLLAGEN; COPOLYMER; FIBRIN GLUE; FIBRINOGEN; FUMARIC ACID DERIVATIVE; HYALURONIC ACID; MACROGOL; MATRIGEL; METHACRYLIC ACID; PEPTIDE DERIVATIVE; POLYGLACTIN; POLYGLYCOLIC ACID; POLYMER; POLYPROPYLENE; POLYPROPYLENE FUMARATE; POLYVINYL ALCOHOL; THROMBIN; UNCLASSIFIED DRUG;

AGING; CARTILAGE; CARTILAGE CELL; CELL FUNCTION; CELL TRANSPLANTATION; CELL TYPE; CROSS LINKING; HISTOPATHOLOGY; HUMAN; HYDROGEL; INJECTION; JOINT MOBILITY; NONHUMAN; REVIEW; STEM CELL; TECHNIQUE; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE REPAIR; TISSUE STRUCTURE;

ANIMALS; BIOCOMPATIBLE MATERIALS; BONE DISEASES; CARTILAGE; CHONDROCYTES; EMBRYO; HUMANS; INJECTIONS; MESENCHYMAL STEM CELLS; TISSUE ENGINEERING;

EID: 10344243969     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.4.12.1849     Document Type: Review

References (104)

1. LANGER R. VACANTI J: Tissue engineering, Science (1993) 260:920-926, Founding paper describing the field of tissue engineering.
2. BELL E, EHRLICH HP, SHER S et al.: Development and use of a living skin equivalent. Plast. Reconstr. Surg. (1981) 67(3):386-392.
3. BELL E, IVARSSON B, MERRILL C: Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad Sci. USA (1979) 76(3):1274-1278.
4. MOONEY DJ, MIKOS AG: Growing new organs. Sci. Am. (1999) 280(4):60-65. More recent review on tissue engineering.
5. QUINN TM, HUNZIKER EB: Controlled enzymatic matrix degradation for integrative cartilage repair: effects on viable cell density and proteoglycan deposition. Tissue Eng. (2002) 8(5):799-806.
6. MOW VC, RATCLIFFE A, POOLE AR: Cartilage and diarthrodial joints as paradigms fer hierarchical materials and structures. Biomaterials (1992) 13:67-97. Comprehensive review on cartilage structure and function.
7. ULRICH-VINTHER M, MALONEY MD, SCHWARZ EM, ROSIER R, O'KEEFE RJ: Articular cartilage biology. J. Am. Acad. Orthop. Surg. (2003) 11(6):421-430.
8. ASHHURST D: The cartilaginous skeleton of an elasmobranch fish does not heal. Matrix Biol. (2004) 23(1):15-22.
9. SIEBOLD R, LICHTENBERG S, HABERMEYER P: Combination of microftacture and periostal-flap for the treatment of focal full thickness articular cartilage lesions of the shoulder: a prospective study. Knee Surg. Sports Traumatol. Arthrosc. (2003) 11(3):183-189.
10. SLEDGE S: Microfracture techniques in the treatment of osteochondral injuries. Clin. Sports Med. (2001) 20(2):365-377.
11. MEYERS MH, CHATTERJEE SN: Osteochondral transplantation. Surg. Clin. North Am. (1978) 58(2):429-434.
12. CHOW JC, HANTES ME, HOULE JB, ZALAVRAS CG: Arthroscopic autogenous osteochondral transplantation for treating knee cartilage defects: a 2- to 5-year follow-up study. Arthroscopy (2004) 20(7):681-690.
13. JAKOB RP, FRANZ T, GAUTIER E, MAINIL-VARLET P: Autologous osteochondral grafting in the knee: indication, results, and reflections. Clin. Orthop. (2002) (401):170-184.
14. SHASHA N, AUBIN PP, CHEAH HK, DAVIS AM, AGNIDIS Z, GROSS AE: Long-term clinical experience with fresh osteochondral allografts for articular knee defects in high demand patients. Cell Tissue Bank (2002) 3(3):175-182.
15. FRIEDLAENDER GE, MANKIN HJ: Transplantation of osteochondral allografts. Annu. Rev. Med. (1984) 35:311-324.
16. GOLE MD, POULSEN D, MARZO JM, KO SH, ZIV I: Chondrocyte viability in press-fit cryopreserved osteochondral allografts. J. Orthop. Res. (2004) 22(4):781-787.
17. RONGA M, GRASSI FA, BULGHERONI P: Arthroscopic autologous chondrocyte implantation for the treatment of a chondral defect in the tibial plateau of the knee. Arthroscopy (2004) 20(1):79-84.
18. TRlPPEL S: Autologous chondrocyte transplantation. N. Engl. J. Med. (1995) 332(8):539-540.
19. PETERSON L, MINAS T, BRITTBERG M, NILSSON A, SJOGREN-JANSSON E, LINDAHL A: Two- to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin. Orthop. (2000) (374):212-234. Autologous chondrocyte transplatation update.
20. JOBANPUTRA P, PARRY D, FRY-SMITH A, BURLS A: Effectiveness of autologous chondrocyte transplantation for hyaline cartilage defects in knees: a rapid and systematic review. Health Technol. Assess. (2001) 5(11):1-57.
21. MINAS T, PETERSON L: Advanced techniques in autologous chondrocyte transplantation. Clin. Sports Med. (1999) 18(1):13-44, v-vi.
22. BRITTBERG M, TALLHEDEN T, SJOGREN-JANSSON B, LINDAHL A, PETERSON L: Autologous chondrocytes used for articular cartilage repair: an update. Clin. Orthop. (2001) (391 Suppl.):S337-S348.
23. SCHNABEL M, MARLOVITS S, ECKHOFF G et al.: Dedifferentiation-associated changes in morphology and gene expression in primary human articular chondrocytes in cell culture. Osteoarthritis Cartilage (2002) 10(1):62-70.
24. SAADEH PB, BRENT B, MEHRARA BJ et al.: Human cartilage engineering: chondrocyte extraction, proliferation, and characterization for construct development. Ann. Plast. Surg. (1999) 42(5):509-513.
25. THIRION S, BERENBAUM F: Culture and phenotyping of chondrocytes in primary culture. Methods Mol. Med. (2004) 100:1-14.
26. TEMENOFF JS, MIKOS AG: Review: tissue engineering for regeneration of articular cartilage. Biomaterials (2000) 21(5):431-440.
27. ELISSEEFF J, ANSETH K, SIMS D, MCINTOSH W, RANDOLPH M, LANGER R: Transdermal photopolymerization for minimally invasive implantation. Proc. Natl. Acad. Sci. USA (1999) 96:3104-3107. Injectable polymerising bioimaterial implantation.
28. FREED L, VUNJAK-NOVAKOVIC G: Tissue engineering of cartilage. In: The Biomedical Engineering Handbook. Bronzind J (Ed), CRC Press, Boca Raton, FL, USA (1995):1778-1796.
29. VUNJAK-NOVAKOVIC G, MARTIN I, OBRADOVIC B et al.: Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage. J. Orthop. Res. (1999) 17:130-138. Demonstrates bioreactor effects on engineered cartilage.
30. VUNJAK-NOVAKOVIC G, OBRADOVIC B, MARTIN I, FREED LE: Bioreactor studies of native and tissue engineered cartilage. Biorheology (2002) 39(1-2):259-268.
31. DEMARTEAU O, JAKOB M, SCHAFER D, HEBERER M, MARTIN I: Development and validation of a bioreactor for physical stimulation of engineered cartilage. Biorheology (2003) 40(1-3):331-336.
32. RAIMONDI MT, BOSCHETTI F, FALCONE L et al.: Mechanobiology of engineered cartilage cultured under a quantified fluid-dynamic environment. Biomech. Model Mechanobiol. (2002) 1(1):69-82.
33. HUNG CT, MAUCK RL, WANG CC et al.: A paradigm for functional tissue engineering of articular cartilage via applied physiologic deformational loading. Ann. Burned. Eng. (2004) 32(1):35-49.
34. LEE DA, MARTIN I: Bioreactor culture techniques for cartilage-tissue engineering. Methods Mol. Biol. (2004) 238:159-170.
35. DIMICCO MA, SAH RL: Integrative cartilage repair: adhesive strength is correlated with collagen deposition. J. Orthop. Res. (2001) 19(6):1105-1112.
36. DIMICCO MA, WATERS SN, AKESON WH, SAH RL et al.: Integrative articular cartilage repair: dependence on developmental stage and collagen metabolism. Osteoarthritis Cartilage (2002) 10(3):218-225.
37. OBRADOVIC B, MARTIN I, PADERA RF, TREPPO S, FREED LE, VUNJAK-NOVAKOVIC G: Integration of engineered cartilage. J. Orthop. Res. (2001) 19(6): 1089-1097.
38. TEMENOFF JS, MIKOS AG: Injectable biodegradable materials for orthopedic tissue engineering. Biomaterials (2000) 21(23):2405-2412. Review of injectable materials.
39. GUTOWSKA A, JEONG B, JASIONOWSKI M: Injectable gels for tissue engineering. Anat. Rec. (2001) 263(4):342-349.
40. SILVERMAN RP, BONASSER L, PASSARETTID, RANDOLPH MA, YAREMCHUK MJ: Adhesion of tissue-engineered cartilate to native cartilage. Plast. Reconstr. Surg. (2000) 105(4):1393-1398.
41. ANSETH KS, METTERS AT, BRYANT SJ, MARTENS PJ, ELISSEEFF JH, BOWMAN CN: In situ forming degradable networks and their application in tissue engineering and drug delivery. J. Control Release (2002) 78(1-3):199-209.
42. PEPPAS N: Hydrogels in Medicine and Pharmacy. Peppas N (Ed.), CRC Press, Boca Raton, FL, USA (1987). Comprehensive summary and characterisation of hydrogel properties.
43. ANSETH KS, BOWMAN CN, BRANNON-PEPPAS L: Mechanical properties of hydrogels and their experimental determination. Biomaterials (1996) 17(17):1647-1657.
44. BRYANT SJ, NUTTELMAN CR, ANSETH KS: The effects of crosslinking density on cartilage formation in photocrosslinkable hydrogels. Biomed. Sci. Instrum. (1999) 35:309-314.
45. SAIM AB, CAO Y, WENG Y et al.: Engineering autogenous cartilage in the shape of a helix using an injectable hydrogel scaffold. Laryngoscope (2000) 110(10 Pt 1):1694-1697.
46. SCHNAPER HW, KLEINMAN HK: Regulation of cell function by extracellular matrix Pediatr. Nephrol. (1993) 7(1):96-104.
47. KLEINMAN HK, MCGARVEY ML, HASSELL JR et al.: Basement membrane complexes with biological activity. Biochemistry (1986) 24:312-318. Discovery of Matrigel.
48. SILVERMAN R, PASSARETTI D, HUANG W, RANDOLPH MA, YAREMCHUK MJ: Injectable tissue-engineered cartilage using a fibrin glue polymer. Plast. Reconstr. Surg. (1999) 103:1809-1818.
49. IBUSUKI S, FUJII Y, IWAMOTO Y, MATSUDA T: Tissue-engineered cartilage using an injectable and in situ gelable thermoresponsive gelatin: fabrication and in vitro performance. Tissue Eng. (2003) 9(2):371-384.
50. JEONG B, LEE KM, GUTOWSKA A, AN YH: Thermogelling biodegradable copolymer aqueous solutions for injectable protein delivery and tissue engineering. Biomacromolecules (2002) 3(4):865-868.
51. AYDELOTTE MB, THONAR EJ, MOLLENHAUER J, FLECHTENMACHER J: Culture of chondrocytes in alginate gel: variations in conditions of gelation influence the structure of the alginate gel, and the arrangement and morphology of proliferating chondrocytes. In Vitro Cell. Dev. Biol. Anim. (1998) 34(2):123-130.
52. ALSBERG E, ANDERSON KW, ALBEIRUTI A, ROWLEY JA, MOONEY DJ: Engineering growing tissues. Proc. Natl. Acad. Sci. USA (2002) 99(19):12025-12030.
53. ATALA A, CIMA LG, KIM W et al.: Injectable alginate seeded with chondrocytes as a potential treatment for vesicoureteral reflux. J. Urol. (1993) 150:745-747.
54. TEMENOFF JS, SHIN H, CONWAY DE, ENGEL PS, MIKOS AG: In vitro cytotoxicity of redox radical initiators for cross-linking of oligo(poly(ethylene glycol) rumarate) macromers. Biomacromolecules (2003) 4(6):1605-1613.
55. TEMENOFF JS, PARK H, JABBARI E et al.: Thermally cross-linked oligo(poly(ethylene glycol) fumarate) hydrogels support osteogenic differentiation of encapsulated marrow stromal cells in vitro. Biomacromolecules (2004) 5(1):5-10.
56. LUTOLF MP, WEBER FE, SCHMOEKEL HG et al.: Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat. Biotechnol. (2003) 21(5):513-518.
57. LUTOLF MP, TIRELLI N, CERRITELLI S, CAVALLI L, HUBBELL JA: Systematic modulation of Michael-type reactivity of thiols through the use of charged amino acids. Bioconjug. Chem. (2001) 12(6):1051-1056.
58. HEALY KE, REZANIA A, STILE RA: Designing biomaterials to direct biological responses. Ann. NY Acad. Sci. (1999) 875:24-35.
59. BRYANT SJ, ANSETH KS: Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. J. Biomed. Mater. Res. (2003) 64(1):70-79.
60. BURDICK JA, ANSETH KS: Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials (2002) 23(22):4315-4323.
61. SCHENSE JC, BLOCH J, AEBISCHER P, HUBBELL JA: Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension. Nat. Biotechnol. (2000) 18(4):415-419.
62. WEST J, HUBBELL J: Polymeric biomaterial with degradation sites for proteases involved in cell migration. Macromolecules (1999) 32(1):241-244.
63. LI Q, WILLIAMS CG, SUN DD, WANG J, LEONG K, ELISSEEFF JH: Photocrosslinkable polysaccharides based on chondroitin sulfate. J. Biomed. Mater. Res. (2004) 68A(1):28-33.
64. PARK YD, TIRELLI N, HUBBELL JA: Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials (2003) 24(6):893-900.
65. PRESTWICH GD, MARECAK DM, MARECEK JF, VERCRUYSSE KP, ZIEBELL MR: Controlled chemical modification of hyaluronic acid: synthesis, applications, and biodegradation of hydrazide derivatives. J. Control. Release (1998) 53(1-3):93-103.
66. FREED LE, MARQUIS JC, NOHRIA A, EMMANUAL J, MIKOS AG, LANGER R: Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J. Biomed. Mater. Res. (1993) 27(1):11-23. One of the earliest papers using a tissue engineering technique for cartilage.
67. CAO Y, VACANTI JP, PAIGE KT, UPTON J, VACANTI CA: Transplantation of chondrocytes utilizing a polymer-cell construct to produce tissue-engineered cartilage in the shape of a human ear. Plast. Reconstr. Surg. (1997) 100(2):297-302; discussion 303-304.
68. KIM WS, VACANTI JP, CIMA L et al.: Cartilage engineered in predetermined shapes employing cell transplantation on synthetic biodegradable polymers. Plast. Reconstr. Surg. (1994) 94:233-237; discussion 238-240.
69. ALSBERG E, HILL EE, MOONEY DJ: Craniofacial tissue engineering. Crit. Rev. Oral Biol. Med. (2001) 12(1):64-75.
70. VACANTI CA, KIM W, UPTON J et al.: Tissue-engineered growth of bone and cartilage. Transplant. Proc. (1993) 25:1019-1021.
71. ELISSEEFF J, MCINTOSH W, ANSETH K, RILEY S, RAGAN P, LANGER R: Photoencapsulation of chondrocytes in poly(ethylene oxide)-based semi-interpenetrating networks. J. Biomed. Mater. Res. (2000) 51(2):164-171. First application of photopolymerisation for cartilage tissue engineering.
72. TING V, SIMS CD, BRECHT LE et al.: In vitro prefabrication of human cartilage shapes using fibrin glue and human chondrocytes. Ann. Plast. Surg. (1998) 40(4):413-420; discussion 420-421.
73. BINETTE F, MCQUAID DP, HAUDENSCHILD DR, YAEGER PC, MCPHERSON JM, TUBO R: Expression of a stable articular cartilage phenotype without evidence of hypertrophy by adult human articular chondrocytes in vitro. J. Orthop. Res. (1998) 16(2):207-216.
74. CHUBINSKAYA S, HUCH K, SCHULZE M, OTTEN L, AYDELOTTE MB, COLE AA: Gene expression by human articular chondrocytes cultured in alginate beads. J. Histochem. Cytochem. (2001) 49(10):1211-1220.
75. GUO JF, JOURDIAN GW, MACCALLUM DK: Culture and growth characteristics of chondrocytes encapsulated in alginate beads. Connect. Tissue Res. (1989) 19:277-297.
76. LEMARE F, STEIMBERG N, LE GRIEL C, DEMIGNOT S, ADOLPHE M: Dedifferentiated chondrocytes cultured in alginate beads: restoration of the differentiated phenotype and of the metabolic responses to interleukin-1β. J. Cell. Physiol (1998) 176:303-313.
77. LYSAGHT MJ, REYES J: The growth of tissue engineering. Tissue Eng. (2001) 7(5):485-493.
78. LYSAGHT MJ, HAZLEHURST AL: Tissue engineering: the end of the beginning. Tissue Eng. (2004) 10(1-2):309-320. Review of the commercial aspects and challenges in tissue engineering.
79. JOHNSTONE B, HERING TM, CAPLAN AI, GOLDBERG VM, YOO JU: In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. (1998) 238(1):265-272.
80. PITTENGER MF, MACKAY AM, BECK SC et al.: Multilineage potential of adult human mesenchymal stem cells. Science (1999) 284(5411):143-147. Important description of MSCs.
81. CAO B, HUARD J: Muscle-derived stem cells. Cell Cycle (2004) 3(2):104-107.
82. GIMBLE J, GUILAK F: Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy (2003) 5(5):362-369.
83. ZUK PA, ZHU M, ASHJIAN P et al.: Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell (2002) 13(12):4279-4295.
84. SMITH A: Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. (2001) 17:435-462.
85. THOMSON JA, ITSKOVlTZ-ELDOR J, SHAPIRO SS et al.: Embryonic stem cell lines derived from human blastocysts. Science (1998) 282(5391):1145-1147. Discovery of human ES cells.
86. SHAMBLOTT MJ, AXELMAN J, WANG S et al.: Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc. Natl. Acad. Sci. USA (1998) 95(23):13726-13731. Discovery of human embryonic gem cells.
87. DEVINE SM, PETER S, MARTIN BJ, BARRY F, MCINTOSH KR: Mesenchymal stem cells: stealth and suppression. Cancer J. (2001) 7(Suppl. 2):S76-S82.
88. KRAMER J, HEGERT C, GUAN K, WOBUS AM, MULLER PK, ROHWEDEL J: Embryonic stem cell-derived chondrogenic differentiation in vitro: activation by BMP-2 and BMP-4. Mech. Dev. (2000) 92(2):193-205. First paper investigating chondrogenic differentiation of ES cells.
89. KRAMER J, HEGERT C, ROHWEDEL J: In vitro differentiation of mouse ES cells: bone and cartilage. Methods Enzymol. (2003) 365:251-268.
90. GEARHART J: New potential for human embryonic stem cells [comment]. Science (1998) 282(5391):1061-1062.
91. PAIGE KT, CIMA LG, YAREMCHUK MJ, VACANTI JP, VACANTI CA: Injectable cartilage. Plast. Reconstr. Surg. (1995) 96:1390-1400.
92. PAIGE KT, CIMA LG, YAREMCHUK MJ, SCHLOO BL, VACANTI JP, VACANTI CA: De novo cartilage generation using calcium alginate-chondrocyte constructs. Plast. Reconstr. Surg. (1996)97:168-178.
93. SIMS D, BUTLER PE, CASANOVA R et al.: Injectable cartilage using polyethylene oxide polymer substrates. Plast. Reconstr. Surg. (1996) 98:843-850.
94. ISOGAI N, LANDIS WJ, MORI R et al.: Experimental use of fibrin glue to induce site-directed osteogenesis from cultured periosteal cells. Plast. Rcconstr. Surg. (2000) 105(3):953-963.
95. FUSSENEGGER M, MEINHART J, HOBLING W, KULLICH W, FUNK S, BERNATZKY G: Stabilized autologous fibrin-chondrocyte constructs for cartilage repair in vivo. Ann. Plast. Surg. (2003) 51(5):493-498.
96. KAFIENAH W, JAKOB M, DEMARTEAU O et al.: Three-dimensional tissue engineering of hyaline cartilage: comparison of adult nasal and articular chondrocytes. Tissue Eng. (2002) 8(5):817-826.
97. CHIA SH, SCHUMACHER BL, KLEIN TJ et al.: Tissue-engineered human nasal septal cartilage using the alginate-recovered-chondrocyte method. Laryngoscope (2004) 114(1):38-45.
98. XU JW, ZAPOROJAN V, PERETTI GM et al.: Injectable tissue-engineered cartilage with different chondrocyte sources. Plast. Reconstr. Surg. (2004) 113(5):1361-1371. Comparison of different chondrocyte sources for cartilage tissue engineering.
99. KIM TK, SHARMA B, WILLIAMS CG et al.: Experimental model for cartilage tissue engineering to regenerate the zonal organization of articular cartilage. Osteoarthritis Cartilage (2003) 11(9):653-664.
100. ELISSEEFF J, ANSETH K, SIMS D et al.: Transdermal photopolymerization of polyethylene oxide)-based injectable hydrogels for tissue-engineered cartilage. Plast Reconstr. Surg. (1999) 104(4):1014-1022.
101. TIMMER MD, CARTER C, AMBROSE CG, MIKOS AG: Fabrication of poly(propylene fumarate)-based orthopaedic implants by photo-crosslinking through transparent silicone molds. Biomaterials (2003) 24(25):4707-4714.
102. MERCIER NR, COSTANTINO HR, TRACT MA, BONASSAR LJ: A novel injectable approach for cartilage formation in vivo using PLG microspheres. Ann. Biomed. Eng. (2004) 32(3):418-429.
103. LEVENBERG S, HUANG NF, LAVIK E, ROGERS AB, ITSKOVITZ-ELDOR J, LANGER R: Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc. Natl. Acad. Sci. USA (2003) 100(22):12741-12746. First paper applying auman ES cells to cartilage tissue engineering.
104. KIM MS, HWANG NS, LEE J et al.: Musculoskeletal differentiation of cells derived from human embryonic germ cells. Stem Cells (2004) (In Press).