Tissue-engineered cartilage with inducible and tunable immunomodulatory properties

Biomaterials

Volumn 35, Issue 22, 2014, Pages 5921-5931

  Glass, Katherine A ^a,b   Link, Jarrett M ^a,b   Brunger, Jonathan M ^a,b   Moutos, Franklin T ^a   Gersbach, Charles A ^a,b   Guilak, Farshid ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Duke University   (United States)

Author keywords

Bioactive biomaterial; Cartilage repair; Immunoengineering; Lentivirus; Mesenchymal stem cell; Osteoarthritis

Indexed keywords

BIOMECHANICS; CELL CULTURE; FLOWCHARTING; GENE THERAPY; GENE TRANSFER; SCAFFOLDS (BIOLOGY); STEM CELLS; TISSUE;

CARTILAGE REPAIR; IMMUNOENGINEERING; LENTIVIRUS; MESENCHYMAL STEM CELL; OSTEOARTHRITIS;

CARTILAGE;

DEXAMETHASONE; DOXYCYCLINE; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; LENTIVIRUS VECTOR; MATRIX METALLOPROTEINASE; PROSTAGLANDIN E2;

ARTICLE; BIOCHEMICAL COMPOSITION; CARTILAGE; CELL ISOLATION; CHONDROGENESIS; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; MESENCHYMAL STEM CELL; MONOLAYER CULTURE; PRIORITY JOURNAL; TISSUE ENGINEERING; UPREGULATION; VIRAL GENE THERAPY; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENE THERAPY; GENETICS; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; OSTEOARTHRITIS; PHYSIOLOGY; PROCEDURES; TISSUE SCAFFOLD;

LENTIVIRUS;

CARTILAGE; CELLS, CULTURED; CHONDROGENESIS; GENETIC THERAPY; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; MESENCHYMAL STROMAL CELLS; OSTEOARTHRITIS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; UP-REGULATION;

EID: 84899908328     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.03.073     Document Type: Article

References (76)

1. Lawrence R.C., Felson D.T., Helmick C.G., Arnold L.M., Choi H., Deyo R.A., et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum 2008, 58(1):26-35.
2. Abramson S.B., Attur M. Developments in the scientific understanding of osteoarthritis. Arthritis Res Ther 2009, 11(3):227.
3. Anderson D.D., Chubinskaya S., Guilak F., Martin J.A., Oegema T.R., Olson S.A., et al. Post-traumatic osteoarthritis: improved understanding and opportunities for early intervention. JOrthop Res 2011, 29(6):802-809.
4. Chung C., Burdick J.A. Engineering cartilage tissue. Adv Drug Deliv Rev 2008, 60(2):243-262.
5. Johnstone B., Alini M., Cucchiarini M., Dodge G.R., Eglin D., Guilak F., et al. Tissue engineering for articular cartilage repair - the state of the art. Eur Cell Mater 2013, 25:248-267.
6. Vacanti J.P., Langer R. Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet 1999, 354(Suppl.1):SI32-SI34.
7. Moutos F.T., Freed L.E., Guilak F. Abiomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 2007, 6(2):162-167.
8. Moutos F.T., Guilak F. Functional properties of cell-seeded three-dimensionally woven poly(epsilon-caprolactone) scaffolds for cartilage tissue engineering. Tissue Eng Part A 2010, 16(4):1291-1301.
9. Valonen P.K., Moutos F.T., Kusanagi A., Moretti M.G., Diekman B.O., Welter J.F., et al. Invitro generation of mechanically functional cartilage grafts based on adult human stem cells and 3D-woven poly(epsilon-caprolactone) scaffolds. Biomaterials 2010, 31(8):2193-2200.
10. Diekman B.O., Guilak F. Stem cell-based therapies for osteoarthritis: challenges and opportunities. Curr Opin Rheumatol 2013, 25(1):119-126.
11. Jacques C., Gosset M., Berenbaum F., Gabay C. The role of IL-1 and IL-1Ra in joint inflammation and cartilage degradation. Vitam Horm 2006, 74:371-403.
12. Kapoor M., Martel-Pelletier J., Lajeunesse D., Pelletier J.P., Fahmi H. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol 2011, 7(1):33-42.
13. Schlaak J.F., Pfers I., Meyer Zum Buschenfelde K.H., Marker-Hermann E. Different cytokine profiles in the synovial fluid of patients with osteoarthritis, rheumatoid arthritis and seronegative spondylarthropathies. Clin Exp Rheumatol 1996, 14(2):155-162.
14. Wilusz R.E., Weinberg J.B., Guilak F., McNulty A.L. Inhibition of integrative repair of the meniscus following acute exposure to interleukin-1 invitro. JOrthop Res 2008, 26(4):504-512.
15. McNulty A.L., Moutos F.T., Weinberg J.B., Guilak F. Enhanced integrative repair of the porcine meniscus invitro by inhibition of interleukin-1 or tumor necrosis factor alpha. Arthritis Rheum 2007, 56(9):3033-3042.
16. Riera K.M., Rothfusz N.E., Wilusz R.E., Weinberg J.B., Guilak F., McNulty A.L. Interleukin-1, tumor necrosis factor-alpha, and transforming growth factor-beta 1 and integrative meniscal repair: influences on meniscal cell proliferation and migration. Arthritis Res Ther 2011, 13(6):R187.
17. Heldens G.T., Blaney Davidson E.N., Vitters E.L., Schreurs B.W., Piek E., van den Berg W.B., et al. Catabolic factors and osteoarthritis-conditioned medium inhibit chondrogenesis of human mesenchymal stem cells. Tissue Eng Part A 2012, 18(1-2):45-54.
18. Wehling N., Palmer G.D., Pilapil C., Liu F., Wells J.W., Muller P.E., et al. Interleukin-1beta and tumor necrosis factor alpha inhibit chondrogenesis by human mesenchymal stem cells through NF-kappaB-dependent pathways. Arthritis Rheum 2009, 60(3):801-812.
19. Rainbow R.S., Kwon H., Foote A.T., Preda R.C., Kaplan D.L., Zeng L. Muscle cell-derived factors inhibit inflammatory stimuli-induced damage in hMSC-derived chondrocytes. Osteoarthr Cartil 2013, 21(7):990-998.
20. Ousema P.H., Moutos F.T., Estes B.T., Caplan A.I., Lennon D.P., Guilak F., et al. The inhibition by interleukin 1 of MSC chondrogenesis and the development of biomechanical properties in biomimetic 3D woven PCL scaffolds. Biomaterials 2012, 33(35):8967-8974.
21. Scotti C., Piccinini E., Takizawa H., Todorov A., Bourgine P., Papadimitropoulos A., et al. Engineering of a functional bone organ through endochondral ossification. Proc Natl Acad Sci U S A 2013, 110(10):3997-4002.
22. Farrell E., Both S.K., Odorfer K.I., Koevoet W., Kops N., O'Brien F.J., et al. In-vivo generation of bone via endochondral ossification by in-vitro chondrogenic priming of adult human and rat mesenchymal stem cells. BMC Musculoskelet Disord 2011, 12:31.
23. Ferreira E., Porter R.M., Wehling N., O'Sullivan R.P., Liu F., Boskey A., et al. Inflammatory cytokines induce a unique mineralizing phenotype in mesenchymal stem cells derived from human bone marrow. JBiol Chem 2013, 288(41):29494-29505.
24. Mumme M., Scotti C., Papadimitropoulos A., Todorov A., Hoffmann W., Bocelli-Tyndall C., et al. Interleukin-1beta modulates endochondral ossification by human adult bone marrow stromal cells. Eur Cell Mater 2012, 24:224-236.
25. Seckinger P., Lowenthal J.W., Williamson K., Dayer J.M., MacDonald H.R. Aurine inhibitor of interleukin 1 activity that blocks ligand binding. JImmunol 1987, 139(5):1546-1549.
26. Chevalier X., Goupille P., Beaulieu A.D., Burch F.X., Bensen W.G., Conrozier T., et al. Intraarticular injection of anakinra in osteoarthritis of the knee: a multicenter, randomized, double-blind, placebo-controlled study. Arthritis Rheum 2009, 61(3):344-352.
27. Evans C.H., Ghivizzani S.C., Robbins P.D. Arthritis gene therapy and its tortuous path into the clinic. Transl Res 2013, 161(4):205-216.
28. Gerstenfeld L.C., Cullinane D.M., Barnes G.L., Graves D.T., Einhorn T.A. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. JCell Biochem 2003, 88(5):873-884.
29. Mangiapani D., Zeitler E., Furman B.D., Huebner J.L., Kraus V.B., Guilak F., et al. Inhibition of interleukin-1 prevents post-traumatic arthritisfollowing articular fracture in the mouse knee. ORS abstract 2012.
30. Barde I., Zanta-Boussif M.A., Paisant S., Leboeuf M., Rameau P., Delenda C., et al. Efficient control of gene expression in the hematopoietic system using a single tet-on inducible lentiviral vector. Mol Ther 2006, 13(2):382-390.
31. Urlinger S., Baron U., Thellmann M., Hasan M.T., Bujard H., Hillen W. Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity. Proc Natl Acad Sci U S A 2000, 97(14):7963-7968.
32. Watson R.S., Broome T.A., Levings P.P., Rice B.L., Kay J.D., Smith A.D., et al. scAAV-mediated gene transfer of interleukin-1-receptor antagonist to synovium and articular cartilage in large mammalian joints. Gene Ther 2013, 20(6):670-677.
33. Goodrich L.R., Phillips J.N., McIlwraith C.W., Foti S.B., Grieger J.C., Gray S.J., et al. Optimization of scAAV IL-1ra invitro and invivo to deliver high levels of therapeutic protein for treatment of osteoarthritis. Mol Ther Nucleic Acids 2013, 2:e70.
34. Kay J.D., Gouze E., Oligino T.J., Gouze J.N., Watson R.S., Levings P.P., et al. Intra-articular gene delivery and expression of interleukin-1Ra mediated by self-complementary adeno-associated virus. JGene Med 2009, 11(7):605-614.
35. Madry H., Cucchiarini M., Terwilliger E.F., Trippel S.B. Recombinant adeno-associated virus vectors efficiently and persistently transduce chondrocytes in normal and osteoarthritic human articular cartilage. Hum Gene Ther 2003, 14(4):393-402.
36. Cucchiarini M., Madry H., Ma C., Thurn T., Zurakowski D., Menger M.D., et al. Improved tissue repair in articular cartilage defects invivo by rAAV-mediated overexpression of human fibroblast growth factor 2. Mol Ther 2005, 12(2):229-238.
37. Brunger J.M., Huynh N.P.T., Guenther C.M., Perez-Pinera P., Moutos F.T., Sanchez-Adams J., et al. Scaffold-mediated lentiviral transduction for functional tissue engineering of cartilage. Proc Natl Acad Sci U S A 2014, 111(9):E798-E806.
38. Gossen M., Freundlieb S., Bender G., Muller G., Hillen W., Bujard H. Transcriptional activation by tetracyclines in mammalian cells. Science 1995, 268(5218):1766-1769.
39. Wiznerowicz M., Szulc J., Trono D. Tuning silence: conditional systems for RNA interference. Nat Methods 2006, 3(9):682-688.
40. Salmon P., Trono D. Production and titration of lentiviral vectors. Curr Protoc Hum Genet 2007, [Chapter 12]: Unit 12 0, 12.10.1--12.10.24.
41. Phillips J.E., Burns K.L., Le Doux J.M., Guldberg R.E., Garcia A.J. Engineering graded tissue interfaces. Proc Natl Acad Sci U S A 2008, 105(34):12170-12175.
42. Gersbach C.A., Coyer S.R., Le Doux J.M., Garcia A.J. Biomaterial-mediated retroviral gene transfer using self-assembled monolayers. Biomaterials 2007, 28(34):5121-5127.
43. Mow V.C., Kuei S.C., Lai W.M., Armstrong C.G. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. JBiomech Eng 1980, 102(1):73-84.
44. Farndale R.W., Buttle D.J., Barrett A.J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986, 883(2):173-177.
45. Reddy G.K., Enwemeka C.S. Asimplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem 1996, 29(3):225-229.
46. McNulty A.L., Rothfusz N.E., Leddy H.A., Guilak F. Synovial fluid concentrations and relative potency of interleukin-1 alpha and beta in cartilage and meniscus degradation. JOrthop Res 2013, 31(7):1039-1045.
47. Bouffi C., Bony C., Courties G., Jorgensen C., Noel D. IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One 2010, 5(12):e14247.
48. Bernardo M.E., Fibbe W.E. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell 2013, 13(4):392-402.
49. Egg D. Concentrations of prostaglandins D2, E2, F2 alpha, 6-keto-F1 alpha and thromboxane B2 in synovial fluid from patients with inflammatory joint disorders and osteoarthritis. ZRheumatol 1984, 43(2):89-96.
50. Johnstone B., Hering T.M., Caplan A.I., Goldberg V.M., Yoo J.U. Invitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998, 238(1):265-272.
51. Diekman B.O., Rowland C.R., Lennon D.P., Caplan A.I., Guilak F. Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage-derived matrix. Tissue Eng Part A 2010, 16(2):523-533.
52. Lima E.G., Tan A.R., Tai T., Bian L., Stoker A.M., Ateshian G.A., et al. Differences in interleukin-1 response between engineered and native cartilage. Tissue Eng Part A 2008, 14(10):1721-1730.
53. Ramachandran M., Achan P., Salter D.M., Bader D.L., Chowdhury T.T. Biomechanical signals and the C-type natriuretic peptide counteract catabolic activities induced by IL-1beta in chondrocyte/agarose constructs. Arthritis Res Ther 2011, 13(5):R145.
54. Athanasiou K.A., Agarwal A., Dzida F.J. Comparative study of the intrinsic mechanical properties of the human acetabular and femoral head cartilage. JOrthop Res 1994, 12(3):340-349.
55. Mow V.C., Guo X.E. Mechano-electrochemical properties of articular cartilage: their inhomogeneities and anisotropies. Annu Rev Biomed Eng 2002, 4:175-209.
56. Mais A., Klein T., Ullrich V., Schudt C., Lauer G. Prostanoid pattern and iNOS expression during chondrogenic differentiation of human mesenchymal stem cells. JCell Biochem 2006, 98(4):798-809.
57. Pountos I., Giannoudis P.V., Jones E., English A., Churchman S., Field S., et al. NSAIDS inhibit invitro MSC chondrogenesis but not osteogenesis: implications for mechanism of bone formation inhibition in man. JCell Mol Med 2011, 15(3):525-534.
58. Goldring M.B., Suen L.F., Yamin R., Lai W.F. Regulation of collagen gene expression by prostaglandins and interleukin-1beta in cultured chondrocytes and fibroblasts. Am J Ther 1996, 3(1):9-16.
59. Fermor B., Weinberg J.B., Pisetsky D.S., Misukonis M.A., Fink C., Guilak F. Induction of cyclooxygenase-2 by mechanical stress through a nitric oxide-regulated pathway. Osteoarthr Cartil 2002, 10(10):792-798.
60. Clark C.A., Schwarz E.M., Zhang X., Ziran N.M., Drissi H., O'Keefe R.J., et al. Differential regulation of EP receptor isoforms during chondrogenesis and chondrocyte maturation. Biochem Biophys Res Commun 2005, 328(3):764-776.
61. Nemeth K., Leelahavanichkul A., Yuen P.S., Mayer B., Parmelee A., Doi K., et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009, 15(1):42-49.
62. Leddy H.A., Awad H.A., Guilak F. Molecular diffusion in tissue-engineered cartilage constructs: effects of scaffold material, time, and culture conditions. JBiomed Mater Res B Appl Biomater 2004, 70(2):397-406.
63. Shamji M.F., Betre H., Kraus V.B., Chen J., Chilkoti A., Pichika R., et al. Development and characterization of a fusion protein between thermally responsive elastin-like polypeptide and interleukin-1 receptor antagonist: sustained release of a local antiinflammatory therapeutic. Arthritis Rheum 2007, 56(11):3650-3661.
64. Gorth D.J., Mauck R.L., Chiaro J.A., Mohanraj B., Hebela N.M., Dodge G.R., et al. IL-1ra delivered from poly(lactic-co-glycolic acid) microspheres attenuates IL-1beta-mediated degradation of nucleus pulposus invitro. Arthritis Res Ther 2012, 14(4):R179.
65. Whitmire R.E., Wilson D.S., Singh A., Levenston M.E., Murthy N., Garcia A.J. Self-assembling nanoparticles for intra-articular delivery of anti-inflammatory proteins. Biomaterials 2012, 33(30):7665-7675.
66. Buhrmann C., Mobasheri A., Matis U., Shakibaei M. Curcumin mediated suppression of nuclear factor-kappaB promotes chondrogenic differentiation of mesenchymal stem cells in a high-density co-culture microenvironment. Arthritis Res Ther 2010, 12(4):R127.
67. Willard V.P., Diekman B.O., Sanchez-Adams J., O'Connor S.K., Christoforou N., Leong K.W., Guilak F. Osteoarthritis in a dish: the effects of pro-inflammatory cytokines on cartilage derived from induced pluripotent stem cells. Osteoarthr Cartil 2013, 21(Suppl.):S281-S282.
68. Hu W.W., Wang Z., Hollister S.J., Krebsbach P.H. Localized viral vector delivery to enhance in situ regenerative gene therapy. Gene Ther 2007, 14(11):891-901.
69. Gersbach C.A., Phillips J.E., Garcia A.J. Genetic engineering for skeletal regenerative medicine. Annu Rev Biomed Eng 2007, 9:87-119.
70. Basile P., Dadali T., Jacobson J., Hasslund S., Ulrich-Vinther M., Soballe K., et al. Freeze-dried tendon allografts as tissue-engineering scaffolds for Gdf5 gene delivery. Mol Ther 2008, 16(3):466-473.
71. Liao I.C., Chen S., Liu J.B., Leong K.W. Sustained viral gene delivery through core-shell fibers. JControl Release 2009, 139(1):48-55.
72. Holladay C., Power K., Sefton M., O'Brien T., Gallagher W.M., Pandit A. Functionalized scaffold-mediated interleukin 10 gene delivery significantly improves survival rates of stem cells invivo. Mol Ther 2011, 19(5):969-978.
73. Shea L.D., Smiley E., Bonadio J., Mooney D.J. DNA delivery from polymer matrices for tissue engineering. Nat Biotechnol 1999, 17(6):551-554.
74. Neumann A.J., Schroeder J., Alini M., Archer C.W., Stoddart M.J. Enhanced adenovirus transduction of hMSCs using 3D hydrogel cell carriers. Mol Biotechnol 2013, 53(2):207-216.
75. Lee H.H., O'Malley M.J., Friel N.A., Chu C.R. Effects of doxycycline on mesenchymal stem cell chondrogenesis and cartilage repair. Osteoarthr Cartil 2013, 21(2):385-393.
76. Brandt K.D., Mazzuca S.A., Katz B.P., Lane K.A., Buckwalter K.A., Yocum D.E., et al. Effects of doxycycline on progression of osteoarthritis: results of a randomized, placebo-controlled, double-blind trial. Arthritis Rheum 2005, 52(7):2015-2025.