Mechanical stimulation by ultrasound enhances chondrogenic differentiation of mesenchymal stem cells in a fibrin-hyaluronic acid hydrogel

Artificial Organs

Volumn 37, Issue 7, 2013, Pages 648-655

  Choi, Jae Won ^a   Choi, Byung Hyune ^d   Park, Sang Hyug ^e   Pai, Ki Soo ^b   Li, Tian Zhu ^b   Min, Byoung Hyun ^a,b,c   Park, So Ra ^d  

^a Ajou University   (South Korea)

^b Ajou University School of Medicine   (South Korea)

^c Ajou University Medical Center   (South Korea)

^d Inha University School of Medicine   (South Korea)

^e Jungwon University   (South Korea)

Author keywords

Chondrogenesis; Fibrin hyaluronic acid; Low intensity ultrasound; Mesenchymal stem cells

Indexed keywords

CARTILAGE; CHEMICAL ANALYSIS; COLLAGEN; FLOWCHARTING; HYALURONIC ACID; HYDROGELS; STEM CELLS; TISSUE CULTURE; TISSUE ENGINEERING; ULTRASONICS;

CARTILAGE TISSUES; CELL-BE; CELL/B.E; CHONDROGENESIS; CHONDROGENIC DIFFERENTIATION; FIBRIN-HYALURONIC ACID; HYALURONIC ACID HYDROGELS; LOW INTENSITY ULTRASOUND; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL;

ORGANIC ACIDS;

ALGINIC ACID; COLLAGEN; FIBRIN; GLYCOSAMINOGLYCAN POLYSULFATE; HYALURONIC ACID; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CARTILAGE MATRIX; CELL DIFFERENTIATION; CHEMICAL ANALYSIS; CHONDROGENESIS; COMPRESSIVE STRENGTH; CONTROLLED STUDY; ECHOGRAPHY; FIBRIN HYALURONIC ACID HYDROGEL; HISTOLOGY; HYDROGEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LOW INTENSITY ULTRASOUND; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RABBIT; TISSUE CULTURE; TISSUE ENGINEERING;

ORYCTOLAGUS CUNICULUS;

EID: 84880317767     PISSN: 0160564X     EISSN: 15251594     Source Type: Journal    
DOI: 10.1111/aor.12041     Document Type: Article

References (43)

1. Pittenger MF, Mackay AM, Beck SC, etal. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
2. Diekman BO, Rowland CR, Caplan AI, Lennon D, 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 2009;16:523-533.
3. Oshina H, Sotome S, Yoshii T, etal. Effects of continuous dexamethasone treatment on differentiation capabilities of bone marrow-derived mesenchymal cells. Bone 2007;41:575-583.
4. Indrawattana N, Chen G, Tadokoro M, etal. Growth factor combination for chondrogenic induction from human mesenchymal stem cell. Biochem Biophys Res Commun 2004;320:914-919.
5. Mastrogiacomo M, Cancedda R, Quarto R. Effect of different growth factors on the chondrogenic potential of human bone marrow stromal cells. Osteoarthritis Cartilage 2001;9(Suppl. A):S36-40.
6. Kurth T, Hedbom E, Shintani N, etal. Chondrogenic potential of human synovial mesenchymal stem cells in alginate. Osteoarthritis Cartilage 2007;15:1178-1189.
7. Wang Y, Kim UJ, Blasioli DJ, Kim HJ, Kaplan DL. In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 2005;26:7082-7094.
8. Jin CZ, Park SR, Choi BH, Park K, Min BH. In vivo cartilage tissue engineering using a cell-derived extracellular matrix scaffold. Artif Organs 2007;31:183-192.
9. Wegener B, Schrimpf FM, Bergschmidt P, etal. Cartilage regeneration by bone marrow cells-seeded scaffolds. J Biomed Mater Res A 2010;95:735-740.
10. Uematsu K, Hattori K, Ishimoto Y, etal. Cartilage regeneration using mesenchymal stem cells and a three-dimensional poly-lactic-glycolic acid (PLGA) scaffold. Biomaterials 2005;26:4273-4279.
11. Kuo CK, Li WJ, Mauck RL, Tuan RS. Cartilage tissue engineering: its potential and uses. Curr Opin Rheumatol 2006;18:64-73.
12. Sundelacruz S, Kaplan DL. Stem cell- and scaffold-based tissue engineering approaches to osteochondral regenerative medicine. Semin Cell Dev Biol 2009;20:646-655.
13. Choi KH, Choi BH, Park SR, Kim BJ, Min BH. The chondrogenic differentiation of mesenchymal stem cells on an extracellular matrix scaffold derived from porcine chondrocytes. Biomaterials 2010;31:5355-5365.
14. Kubo M, Imai S, Fujimiya M, etal. Exogenous collagen-enhanced recruitment of mesenchymal stem cells during rabbit articular cartilage repair. Acta Orthop 2007;78:845-855.
15. Sittinger M, Hutmacher DW, Risbud MV. Current strategies for cell delivery in cartilage and bone regeneration. Curr Opin Biotechnol 2004;15:411-418.
16. Noth U, Rackwitz L, Steinert AF, Tuan RS. Cell delivery therapeutics for musculoskeletal regeneration. Adv Drug Deliv Rev 2010;62:765-783.
17. Park SH, Park SR, Chung SI, Pai KS, Min BH. Tissue-engineered cartilage using fibrin/hyaluronan composite gel and its in vivo implantation. Artif Organs 2005;29:838-845.
18. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T. Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol Bioeng 2006;93:1152-1163.
19. 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.
20. Angele P, Yoo JU, Smith C, etal. Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res 2003;21:451-457.
21. Huang CY, Hagar KL, Frost LE, Sun Y, Cheung HS. Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 2004;22:313-323.
22. Lee HJ, Choi BH, Min BH, Son YS, Park SR. Low-intensity ultrasound stimulation enhances chondrogenic differentiation in alginate culture of mesenchymal stem cells. Artif Organs 2006;30:707-715.
23. Cui JH, Park K, Park SR, Min BH. Effects of low-intensity ultrasound on chondrogenic differentiation of mesenchymal stem cells embedded in polyglycolic acid: an in vivo study. Tissue Eng 2006;12:75-82.
24. Cui JH, Park SR, Park K, Choi BH, Min BH. Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation in vivo. Tissue Eng 2007;13:351-360.
25. Danisovic L, Varga I, Zamborsky R, Bohmer D. The tissue engineering of articular cartilage: cells, scaffolds and stimulating factors. Exp Biol Med 2012;237:10-17.
26. Reddy GK, Enwemeka CS. A simplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem 1996;29:225-229.
27. Edwards CA, O'Brien WD Jr. Modified assay for determination of hydroxyproline in a tissue hydrolyzate. Clin Chim Acta 1980;104:161-167.
28. Farndale RW, Buttle DJ, Barrett AJ. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986;883:173-177.
29. Chen G, Liu D, Tadokoro M, etal. Chondrogenic differentiation of human mesenchymal stem cells cultured in a cobweb-like biodegradable scaffold. Biochem Biophys Res Commun 2004;322:50-55.
30. Huang GS, Dai LG, Yen BL, Hsu SH. Spheroid formation of mesenchymal stem cells on chitosan and chitosan-hyaluronan membranes. Biomaterials 2011;32:6929-6945.
31. Fan H, Hu Y, Zhang C, etal. Cartilage regeneration using mesenchymal stem cells and a PLGA-gelatin/chondroitin/hyaluronate hybrid scaffold. Biomaterials 2006;27:4573-4580.
32. Ahmed TA, Dare EV, Hincke M. Fibrin: a versatile scaffold for tissue engineering applications. Tissue Eng Part B Rev 2008;14:199-215.
33. Janmey PA, Winer JP, Weisel JW. Fibrin gels and their clinical and bioengineering applications. J R Soc Interface 2009;6:1-10.
34. Sechler JL, Corbett SA, Wenk MB, Schwarzbauer JE. Modulation of cell-extracellular matrix interactions. Ann N Y Acad Sci 1998;857:143-154.
35. Toole BP. Hyaluronan in morphogenesis. Semin Cell Dev Biol 2001;12:79-87.
36. Schumann D, Kujat R, Zellner J, etal. Treatment of human mesenchymal stem cells with pulsed low intensity ultrasound enhances the chondrogenic phenotype in vitro. Biorheology 2006;43:431-443.
37. Mosesson MW. Fibrinogen and fibrin structure and functions. J Thromb Haemost 2005;3:1894-1904.
38. Salinas CN, Anseth KS. The enhancement of chondrogenic differentiation of human mesenchymal stem cells by enzymatically regulated RGD functionalities. Biomaterials 2008;29:2370-2377.
39. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 2004;4:528-539.
40. Wright MO, Nishida K, Bavington C, etal. Hyperpolarisation of cultured human chondrocytes following cyclical pressure-induced strain: evidence of a role for alpha 5 beta 1 integrin as a chondrocyte mechanoreceptor. J Orthop Res 1997;15:742-747.
41. Grandolfo M, Calabrese A, D'Andrea P. Mechanism of mechanically induced intercellular calcium waves in rabbit articular chondrocytes and in HIG-82 synovial cells. J Bone Miner Res 1998;13:443-453.
42. Salter DM, Millward-Sadler SJ, Nuki G, Wright MO. Integrin-interleukin-4 mechanotransduction pathways in human chondrocytes. Clin Orthop Relat Res 2001;391(Suppl.):S49-60.
43. Choi BH, Choi MH, Kwak MG, Min BH, Woo ZH, Park SR. Mechanotransduction pathways of low-intensity ultrasound in C-28/I2 human chondrocyte cell line. Proc Inst Mech Eng H 2007;221:527-535.