Cell-mediated degradation regulates human mesenchymal stem cell chondrogenesis and hypertrophy in MMP-sensitive hyaluronic acid hydrogels

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Feng, Qian ^a   Zhu, Meiling ^a   Wei, Kongchang ^a   Bian, Liming ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; MALEIMIDE DERIVATIVE; MATRIX METALLOPROTEINASE; MOLECULAR SCAFFOLD; THIOL GROUP; BIOLOGICAL MARKER; HYDROGEL;

ARTICLE; BIODEGRADATION; BIOSYNTHESIS; CALCIFICATION; CARTILAGE MATRIX; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL STRUCTURE; CELL VIABILITY; CHEMICAL STRUCTURE; CHONDROGENESIS; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; HYDROLYSIS; HYPERTROPHY; MESENCHYMAL STEM CELL; MOLECULAR STABILITY; REGULATORY MECHANISM; BONE MINERALIZATION; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; MESENCHYMAL STROMA CELL; METABOLISM;

BIOLOGICAL MARKERS; CALCIFICATION, PHYSIOLOGIC; CELL CULTURE TECHNIQUES; CELL SURVIVAL; CELLS, CULTURED; CHONDROGENESIS; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HUMANS; HYALURONIC ACID; HYDROGEL; MATRIX METALLOPROTEINASES; MESENCHYMAL STROMAL CELLS;

EID: 84902590467     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099587     Document Type: Article

References (40)

1. Bian L, Zhai DY, Mauck RL, Burdick JA (2011) Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage. Tissue Eng Part A 17: 1137-1145.
2. Khetan S, Guvendiren M, Legant WR, Cohen DM, Chen CS, et al. (2013) Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat Mater 12: 458-465.
3. Lutolf MP, Lauer-Fields JL, Schmoekel HG, Metters AT, Weber FE, et al. (2003) Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci U S A 100: 5413-5418. (Pubitemid 36542719)
4. Kim J, Kim IS, Cho TH, Kim HC, Yoon SJ, et al. (2010) In vivo evaluation of MMP sensitive high-molecular weight HA-based hydrogels for bone tissue engineering. J Biomed Mater Res A 95: 673-681.
5. Khetan S, Burdick JA (2010) Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials 31: 8228-8234.
6. Bahney CS, Hsu CW, Yoo JU, West JL, Johnstone B (2011) A bioresponsive hydrogel tuned to chondrogenesis of human mesenchymal stem cells. FASEB J 25: 1486-1496.
7. Bian L, Zhai DY, Tous E, Rai R, Mauck RL, et al. (2011) Enhanced MSC chondrogenesis following delivery of TGF-beta3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo. Biomaterials 32: 6425-6434.
8. Pelttari K, Winter A, Steck E, Goetzke K, Hennig T, et al. (2006) Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 54: 3254-3266. (Pubitemid 44622096)
9. Boskey AL (1991) The role of extracellular matrix components in dentin mineralization. Crit Rev Oral Biol Med 2: 369-387.
10. Anderson HC (1995) Molecular biology of matrix vesicles. Clin Orthop Relat Res: 266-280.
11. Jubeck B, Gohr C, Fahey M, Muth E, Matthews M, et al. (2008) Promotion of articular cartilage matrix vesicle mineralization by type I collagen. Arthritis Rheum 58: 2809-2817.
12. Ortega N, Behonick DJ, Werb Z (2004) Matrix remodeling during endochondral ossification. Trends Cell Biol 14: 86-93. (Pubitemid 38186642)
13. Erickson IE, Huang AH, Sengupta S, Kestle S, Burdick JA, et al. (2009) Macromer density influences mesenchymal stem cell chondrogenesis and maturation in photocrosslinked hyaluronic acid hydrogels. Osteoarthritis Cartilage 17: 1639-1648.
14. Bian L, Hou C, Tous E, Rai R, Mauck RL, et al. (2012) The influence of hyaluronic acid hydrogel crosslinking density and macromolecular diffusivity on human MSC chondrogenesis and hypertrophy. Biomaterials 34: 413-421.
15. Mueller MB, Tuan RS (2008) Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58: 1377-1388. (Pubitemid 351705927)
16. McGowan KB, Kurtis MS, Lottman LM, Watson D, Sah RL (2002) Biochemical quantification of DNA in human articular and septal cartilage using PicoGreen and Hoechst 33258. Osteoarthritis Cartilage 10: 580-587. (Pubitemid 34919074)
17. 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)
18. Hollander AP, Heathfield TF, Webber C, Iwata Y, Bourne R, et al. (1994) Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest 93: 1722-1732. (Pubitemid 24116414)
19. Scotti C, Tonnarelli B, Papadimitropoulos A, Scherberich A, Schaeren S, et al. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci U S A 107: 7251-7256.
20. Tous E, Ifkovits JL, Koomalsingh KJ, Shuto T, Soeda T, et al. (2011) Influence of injectable hyaluronic acid hydrogel degradation behavior on infarction-induced ventricular remodeling. Biomacromolecules 12: 4127-4135.
21. Park Y, Lutolf MP, Hubbell JA, Hunziker EB, Wong M (2004) Bovine primary chondrocyte culture in synthetic matrix metalloproteinase-sensitive poly(ethylene glycol)-based hydrogels as a scaffold for cartilage repair. Tissue Eng 10: 515-522. (Pubitemid 38580272)
22. Schwartz Z, Griffon DJ, Fredericks LP, Lee HB, Weng HY (2011) Hyaluronic acid and chondrogenesis of murine bone marrow mesenchymal stem cells in chitosan sponges. Am J Vet Res 72: 42-50.
23. Wu SC, Chang JK, Wang CK, Wang GJ, Ho ML (2010) Enhancement of chondrogenesis of human adipose derived stem cells in a hyaluronan-enriched microenvironment. Biomaterials 31: 631-640.
24. Bian L, Guvendiren M, Mauck RL, Burdick JA (2013) Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis. Proc Natl Acad Sci U S A 110: 10117-10122.
25. DeLise AM, Tuan RS (2002) Alterations in the spatiotemporal expression pattern and function of N-cadherin inhibit cellular condensation and chondrogenesis of limb mesenchymal cells in vitro. J Cell Biochem 87: 342-359. (Pubitemid 35231720)
26. Maleski MP, Knudson CB (1996) Hyaluronan-mediated aggregation of limb bud mesenchyme and mesenchymal condensation during chondrogenesis. Exp Cell Res 225: 55-66. (Pubitemid 26158455)
27. Nakamura M, Miyamoto S, Maeda H, Ishii G, Hasebe T, et al. (2005) Matrix metalloproteinase-7 degrades all insulin-like growth factor binding proteins and facilitates insulin-like growth factor bioavailability. Biochem Biophys Res Commun 333: 1011-1016. (Pubitemid 40854257)
28. Hermanson GT (2008) Bioconjugate Techniques: Elsevier.
29. Phelps EA, Enemchukwu NO, Fiore VF, Sy JC, Murthy N, et al. (2012) Maleimide cross-linked bioactive PEG hydrogel exhibits improved reaction kinetics and cross-linking for cell encapsulation and in situ delivery. Adv Mater 24: 64-70, 62.
30. Chen CC, Boskey AL, Rosenberg LC (1984) The inhibitory effect of cartilage proteoglycans on hydroxyapatite growth. Calcif Tissue Int 36: 285-290. (Pubitemid 14072396)
31. Jubeck B, Muth E, Gohr CM, Rosenthal AK (2009) Type II collagen levels correlate with mineralization by articular cartilage vesicles. Arthritis Rheum 60: 2741-2746.
32. Hubbell JA (2003) Materials as morphogenetic guides in tissue engineering. Curr Opin Biotechnol 14: 551-558.
33. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326: 1216-1219.
34. Mello MA, Tuan RS (2006) Effects of TGF-beta1 and triiodothyronine on cartilage maturation: in vitro analysis using long-term high-density micromass cultures of chick embryonic limb mesenchymal cells. J Orthop Res 24: 2095-2105. (Pubitemid 44717972)
35. Scotti C, Tonnarelli B, Papadimitropoulos A, Scherberich A, Schaeren S, et al. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proceedings of the National Academy of Sciences 107: 7251-7256.
36. Wang G, Woods A, Sabari S, Pagnotta L, Stanton L-A, et al. (2004) RhoA/ROCK Signaling Suppresses Hypertrophic Chondrocyte Differentiation. Journal of Biological Chemistry 279: 13205-13214. (Pubitemid 38445899)
37. Patterson J, Hubbell JA (2010) Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2. Biomaterials 31: 7836-7845.
38. Lim YB, Kang SS, An WG, Lee YS, Chun JS, et al. (2003) Chondrogenesis induced by actin cytoskeleton disruption is regulated via protein kinase C-dependent p38 mitogen-activated protein kinase signaling. J Cell Biochem 88: 713-718. (Pubitemid 36258821)
39. Zanetti NC, Solursh M (1984) Induction of chondrogenesis in limb mesenchymal cultures by disruption of the actin cytoskeleton. J Cell Biol 99: 115-123. (Pubitemid 14096874)
40. Gao L, McBeath R, Chen CS (2010) Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-cadherin. Stem Cells 28: 564-572.