A fibrin/hyaluronic acid hydrogel for the delivery of mesenchymal stem cells and potential for articular cartilage repair

Journal of Biological Engineering

Volumn 8, Issue 1, 2014, Pages

  Snyder, Timothy N ^a,b   Madhavan, Krishna ^a   Intrator, Miranda ^a   Dregalla, Ryan C ^b   Park, Daewon ^a  

^a The University of Colorado Denver   (United States)

^b Regenerative Sciences LLC   (United States)

Author keywords

Cartilage; Fibrin; Hyaluronic acid; Hydrogel; Mesenchymal stem cell; Osteoarthritis; Regenerative medicine; Stem cell delivery; Tissue engineering

Indexed keywords

ACID ANHYDRIDE; COLLAGEN TYPE 1; FIBRIN; FIBRINOGEN; HYALURONIC ACID; METHACRYLIC ACID; AGGRECAN; COLLAGEN TYPE 1 ALPHA 1; COLLAGEN TYPE 2 ALPHA 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ARTICLE; ARTICULAR CARTILAGE; BIOLOGICAL ACTIVITY; CELL ADHESION; CELL PROLIFERATION; CHONDROGENESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; MESENCHYMAL STEM CELL; METABOLIC ACTIVITY ASSAY; OSTEOARTHRITIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; TISSUE REPAIR; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CARTILAGE; CARTILAGE CELL; CELL LYSATE; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROSS LINKING; HEMATOPOIETIC STEM CELL; NANOFABRICATION; PHENOTYPE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGENERATION; THROMBOCYTE;

EID: 84900034183     PISSN: None     EISSN: 17541611     Source Type: Journal    
DOI: 10.1186/1754-1611-8-10     Document Type: Article

References (63)

1. Lawrence RC, Felson DT, Helmick CG, Arnold LM, Choi H, Deyo RA, Gabriel S, Hirsch R, Hochberg MC, Hunder GG, Jordan JM, Katz JN, Kremers HM, Wolfe F. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum 2008, 58:26-35. 10.1002/art.23176, 3266664, 18163497.
2. CDC Prevalence of disabilities and associated health conditions among adults - United States, 1999. JAMA 2001, 285:1571-1572. CDC.
3. Spiller KL, Maher SA, Lowman AM. Hydrogels for the repair of articular cartilage defects. Tissue Eng Part B Rev 2011, 17:281-299. 10.1089/ten.teb.2011.0077, 3171151, 21510824.
4. Stockwell RA. Chondrocytes. J Clin Pathol Suppl (R Coll Pathol) 1978, 12:7-13. 1347119, 365896.
5. Hubbard MJS. Articular debridement versus washout for degeneration of the medial femoral condyle - A five-year study. J Bone Joint Surg (Br) 1996, 78B:217-219.
6. Steadman JR, Rodkey WG, Rodrigo JJ. Microfracture: Surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res 2001, (391 Suppl):S362-S369.
7. Steadman JR, Briggs KK, Rodrigo JJ, Kocher MS, Gill TJ, Rodkey WG. Outcomes of microfracture for traumatic chondral defects of the knee: Average 11-year follow-up. Arthroscopy 2003, 19:477-484. 10.1053/jars.2003.50112, 12724676.
8. Steadman JR, Rodkey WG, Briggs KK. Microfracture chondroplasty: indications, techniques, and outcomes. Sports Med Arthrosc 2003, 11:236-244.
9. Matsusue Y, Yamamuro T, Hama H. Arthroscopic multiple osteochondral transplantation to the chondral defect in the knee associated with anterior cruciate ligament disruption. Arthroscopy 1993, 9:318-321. 10.1016/S0749-8063(05)80428-1, 8323618.
10. Homminga GN, Bulstra SK, Bouwmeester PS, van der Linden AJ. Perichondral grafting for cartilage lesions of the knee. J Bone Joint Surg (Br) 1990, 72:1003-1007.
11. Bouwmeester SJ, Beckers JM, Kuijer R, van der Linden AJ, Bulstra SK. Longterm results of rib perichondrial grafts for repair of cartilage defects in the human knee. Int Orthop 1997, 21:313-317. 10.1007/s002640050175, 3617805, 9476161.
12. Hoikka VEJ, Jaroma HJ, Ritsila VA. Reconstruction of the patellar articulation with periosteal grafts: 4-year follow-up of 13 cases. Acta Orthop Scand 1990, 61:36-39. 10.3109/17453679008993062, 2336949.
13. Ritsila VA, Santavirta S, Alhopuro S, Poussa M, Jaroma H, Rubak JM, Eskola A, Hoikka V, Snellman O, Osterman K. Periosteal and perichondral grafting in reconstructive surgery. Clin Orthop Relat Res 1994, 302:259-265.
14. Messner K, Gillquist J. Synthetic implants for the repair of osteochondral defects of the medial femoral condyle - a biomechanical and histological-evaluation in the rabbit knee. Biomaterials 1993, 14:513-521. 10.1016/0142-9612(93)90240-3, 8329524.
15. Hunziker EB. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 2002, 10:432-463. 10.1053/joca.2002.0801, 12056848.
16. Ahmed N, Stanford WL, Kandel RA. Mesenchymal stem and progenitor cells for cartilage repair. Skeletal Radiol 2007, 36:909-912. 10.1007/s00256-007-0333-3, 17558504.
17. Kalunian K. Patient Information: Osteoarthritis treatment (Beyond the Basics) [http://www.uptodate.com/contents/osteoarthritis-treatment-beyond-the-basics].
18. Peterson L, Vasiliadis HS, Brittberg M, Lindahl A. Autologous chondrocyte implantation: A long-term follow-up. Am J Sports Med 2010, 38:1117-1124. 10.1177/0363546509357915, 20181804.
19. Vasiliadis HS, Danielson B, Ljungberg M, McKeon B, Lindahl A, Peterson L. Autologous chondrocyte implantation in cartilage lesions of the knee. Long-term evaluation with magnetic resonance imaging and delayed gadolinium-enhanced magnetic resonance imaging technique. Am J Sports Med 2010, 38:943-949. 10.1177/0363546509358266, 20185841.
20. Vasiliadis HS, Lindahl A, Georgoulis AD, Peterson L. Malalignment and cartilage lesions in the patellofemoral joint treated with autologous chondrocyte implantation. Knee Surg Sports Traumatol Arthrosc 2011, 19:452-457. 10.1007/s00167-010-1267-1, 20845030.
21. Minas T, Peterson L. Autologous chondrocyte transplantation. Oper Techn Sport Med 2012, 20:72-86.
22. Galle J, Bader A, Hepp P, Grill W, Fuchs B, Kas JA, Krinner A, Marquass B, Muller K, Schiller J, Schulz RM, von Buttlar M, von der Burg E, Zscharnack M, Loffler M. Mesenchymal stem cells in cartilage repair: State of the art and methods to monitor cell growth, differentiation and cartilage regeneration. Curr Med Chem 2010, 17:2274-2291. 10.2174/092986710791331095, 20459378.
23. Park JS, Yang HN, Woo DG, Jeon SY, Park KH. Chondrogenesis of human mesenchymal stem cells in fibrin constructs evaluated in vitro and in nude mouse and rabbit defects models. Biomaterials 2011, 32:1495-1507. 10.1016/j.biomaterials.2010.11.003, 21122912.
24. Park SH, Choi BH, Park SR, Min BH. Chondrogenesis of rabbit mesenchymal stem cells in fibrin/hyaluronan composite scaffold in vitro. Tissue Eng Part A 2011, 17:1277-1286. 10.1089/ten.tea.2010.0337, 21189070.
25. Danisovic L, Varga I, Polak S. Growth factors and chondrogenic differentiation of mesenchymal stem cells. Tissue Cell 2012, 44:69-73. 10.1016/j.tice.2011.11.005, 22185680.
26. Mauck RL, Yuan X, Tuan RS. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 2006, 14:179-189. 10.1016/j.joca.2005.09.002, 16257243.
27. Richter W. Mesenchymal stem cells and cartilage in situ regeneration. J Intern Med 2009, 266:390-405. 10.1111/j.1365-2796.2009.02153.x, 19765182.
28. Pelttari K, Lorenz H, Boeuf S, Templin MF, Bischel O, Goetzke K, Hsu HY, Steck E, Richter W. Secretion of matrix metalloproteinase 3 by expanded articular chondrocytes as a predictor of ectopic cartilage formation capacity in vivo. Arthritis Rheum 2008, 58:467-474. 10.1002/art.23302, 18240244.
29. Schante CE, Zubera G, Herlinb C, Vandammea TF. Chemical modifications of hyaluronic acid for the synthesis of derivatives for a broad range of biomedical applications. Carbohydr Polym 2011, 85:469-489.
30. Bian L, Hou C, Tous E, Rai R, Mauck RL, Burdick JA. The influence of hyaluronic acid hydrogel crosslinking density and macromolecular diffusivity on human MSC chondrogenesis and hypertrophy. Biomaterials 2013, 34:413-421. 10.1016/j.biomaterials.2012.09.052, 3578381, 23084553.
31. Jha AK, Xu X, Duncan RL, Jia X. Controlling the adhesion and differentiation of mesenchymal stem cells using hyaluronic acid-based, doubly crosslinked networks. Biomaterials 2011, 32:2466-2478. 10.1016/j.biomaterials.2010.12.024, 3032013, 21216457.
32. Espandar L, Bunnell B, Wang GY, Gregory P, McBride C, Moshirfar M. Adipose-derived stem cells on hyaluronic acid-derived scaffold a new horizon in bioengineered cornea. Arch Ophthalmol 2012, 130:202-208. 10.1001/archopthalmol.2011.1398, 22332213.
33. Chung C, Burdick JA. Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. Tissue Eng Part A 2009, 15:243-254. 2678568, 19193129.
34. LeBoeuf RD, Raja RH, Fuller GM, Weigel PH. Human fibrinogen specifically binds hyaluronic acid. J Biol Chem 1986, 261:12586-12592.
35. Nehls V, Drenckhahn D. A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc Res 1995, 50:311-322. 10.1006/mvre.1995.1061, 8583947.
36. Dozza B, Di Bella C, Lucarelli E, Giavaresi G, Fini M, Tazzari PL, Giannini S, Donati D. Mesenchymal stem cells and platelet lysate in fibrin or collagen scaffold promote non-cemented hip prosthesis integration. J Orthop Res 2011, 29:961-968. 10.1002/jor.21333, 21284031.
37. Anitua E, Sanchez M, Nurden AT, Nurden P, Orive G, Andia I. New insights into and novel applications for platelet-rich fibrin therapies. Trends Biotechnol 2006, 24:227-234. 10.1016/j.tibtech.2006.02.010, 16540193.
38. Hale BW, Goodrich LR, Frisbie DD, McIlwraith CW, Kisiday JD. Effect of scaffold dilution on migration of mesenchymal stem cells from fibrin hydrogels. Am J Vet Res 2012, 73:313-318. 10.2460/ajvr.73.2.313, 22280396.
39. Choi JW, Choi BH, Park SH, Pai KS, Li TZ, Min BH, Park SR. Mechanical stimulation by ultrasound enhances chondrogenic differentiation of mesenchymal stem cells in a fibrin-hyaluronic acid hydrogel. Artif Organs 2013, 37:648-655. 10.1111/aor.12041, 23495957.
40. Seo S, Na K. Mesenchymal stem cell-based tissue engineering for chondrogenesis. J Biomed Biotechnol 2011, 2011:806891. 3191858, 22007146.
41. Kim IL, Khetan S, Baker BM, Chen CS, Burdick JA. Fibrous hyaluronic acid hydrogels that direct MSC chondrogenesis through mechanical and adhesive cues. Biomaterials 2013, 34:5571-5580. 10.1016/j.biomaterials.2013.04.004, 23623322.
42. Hunter CJ, Mouw JK, Levenston ME. Dynamic compression of chondrocyte-seeded fibrin gels: effects on matrix accumulation and mechanical stiffness. Osteoarthritis Cartilage 2004, 12:117-130. 10.1016/j.joca.2003.08.009, 14723871.
43. Hokugo A, Takamoto T, Tabata Y. Preparation of hybrid scaffold from fibrin and biodegradable polymer fiber. Biomaterials 2006, 27:61-67. 10.1016/j.biomaterials.2005.05.030, 16000222.
44. Haugh MG, Thorpe SD, Vinardell T, Buckley CT, Kelly DJ. The application of plastic compression to modulate fibrin hydrogel mechanical properties. J Mech Behav Biomed Mater 2012, 16:66-72.
45. Ahearne M, Kelly DJ. A comparison of fibrin, agarose and gellan gum hydrogels as carriers of stem cells and growth factor delivery microspheres for cartilage regeneration. Biomed Mater 2013, 8:035004. 10.1088/1748-6041/8/3/035004, 23532058.
46. Camci-Unal G, Cuttica D, Annabi N, Demarchi D, Khademhosseini A. Synthesis and characterization of hybrid hyaluronic acid-gelatin hydrogels. Biomacromolecules 2013, 14:1085-1092. 10.1021/bm3019856, 3643200, 23419055.
47. Seidlits SK, Khaing ZZ, Petersen RR, Nickels JD, Vanscoy JE, Shear JB, Schmidt CE. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials 2010, 31:3930-3940. 10.1016/j.biomaterials.2010.01.125, 20171731.
48. Fernandez P, Bausch AR. The compaction of gels by cells: a case of collective mechanical activity. Integr Biol (Camb) 2009, 1:252-259. 10.1039/b822897c, 20023736.
49. Bian W, Liau B, Badie N, Bursac N. Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues. Nat Protoc 2009, 4:1522-1534. 10.1038/nprot.2009.155, 2924624, 19798085.
50. Schutte SC, Chen Z, Brockbank KG, Nerem RM. Tissue engineering of a collagen-based vascular media Demonstration of functionality. Organogenesis 2010, 6:204-211. 10.4161/org.6.4.12651, 3055645, 21220958.
51. Lee F, Kurisawa M. Formation and stability of interpenetrating polymer network hydrogels consisting of fibrin and hyaluronic acid for tissue engineering. Acta Biomater 2013, 9:5143-5152. 10.1016/j.actbio.2012.08.036, 22943886.
52. LeBoeuf RD, Gregg RR, Weigel PH, Fuller GM. Effects of hyaluronic acid and other glycosaminoglycans on fibrin polymer formation. Biochemistry 1987, 26:6052-6057. 10.1021/bi00393a016, 3689758.
53. Worster AA, Brower-Toland BD, Fortier LA, Bent SJ, Williams J, Nixon AJ. Chondrocytic differentiation of mesenchymal stem cells sequentially exposed to transforming growth factor-beta 1 in monolayer and insulin-like growth factor-I in a three-dimensional matrix. J Orthop Res 2001, 19:738-749. 10.1016/S0736-0266(00)00054-1, 11518286.
54. Lisignolia G, Cristino S, Piacentini A, Toneguzzi S, Grassi F, Cavallo C, Zini N, Solimando L, Maraldi NM, Facchini A. Cellular and molecular events during chondrogenesis of human mesenchymal stromal cells grown in a three-dimensional hyaluronan based scaffold. Biomaterials 2005, 26:5677-5686. 10.1016/j.biomaterials.2005.02.031, 15878373.
55. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumur M, Fujinag T. Gene expression profile of bovine bone marrow mesenchymal stem cell during spontaneous chondrogenic differentiation in pellet culture system. Jpn J Vet Res 2006, 53:127-139.
56. Jakobsen RB, Shahdadfar A, Reinholt FP, Brinchmann JE. Chondrogenesis in a hyaluronic acid scaffold: comparison between chondrocytes and MSC from bone marrow and adipose tissue. Knee Surg Sports Traumatol Arthrosc 2010, 18:1407-1416. 10.1007/s00167-009-1017-4, 20020100.
57. Ho ST, Cool SM, Hui JH, Hutmacher DW. The influence of fibrin based hydrogels on the chondrogenic differentiation of human bone marrow stromal cells. Biomaterials 2010, 31:38-47. 10.1016/j.biomaterials.2009.09.021, 19800683.
58. Patrascu JM, Kruger JP, Boss HG, Ketzmar AK, Freymann U, Sittinger M, Notter M, Endres M, Kaps C. Polyglycolic acid-hyaluronan scaffolds loaded with bone marrow-derived mesenchymal stem cells show chondrogenic differentiation in vitro and cartilage repair in the rabbit model. J Biomed Mater Res B Appl Biomater 2013, 101:1310-1320. 10.1002/jbm.b.32944, 23661546.
59. Akiyama H. Control of chondrogenesis by the transcription factor Sox9. Mod Rheumatol 2008, 18:213-219. 10.3109/s10165-008-0048-x, 18351289.
60. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop DJ, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 2006, 8:315-317. 10.1080/14653240600855905, 16923606.
61. Ning J, Li C, Li H, Chang J. Bone marrow mesenchymal stem cells differentiate into urothelial cells and the implications for reconstructing urinary bladder mucosa. Cytotechnology 2011, 63:531-539. 10.1007/s10616-011-9376-3, 3176931, 21915725.
62. Boxall SA, Jones E. Markers for Characterization of Bone Marrow Multipotential Stromal Cells. Stem Cells Intern 2012, 2012:975871.
63. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997, 275:964-966. 10.1126/science.275.5302.964, 9020076.