Guiding Chondrogenesis and Osteogenesis with Mineral-Coated Hydroxyapatite and BMP-2 Incorporated within High-Density hMSC Aggregates for Bone Regeneration

ACS Biomaterials Science and Engineering

Volumn 2, Issue 1, 2016, Pages 30-42

  Dang, Phuong N ^a   Dwivedi, Neha ^a   Yu, Xiaohua ^b   Phillips, Lauren ^a   Bowerman, Caitlin ^a   Murphy, William L ^b   Alsberg, Eben ^c  

^a Case Western Reserve University   (United States)

^b University of Wisconsin Health   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

bone tissue engineering; endochondral ossification; growth factor delivery; mineral coated microparticles

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; CALCIUM; COLLAGEN TYPE 2; HYDROXYAPATITE;

ARTICLE; BIOLOGICAL ACTIVITY; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MINERALIZATION; BONE REGENERATION; CHONDROGENESIS; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; ENCHONDRAL OSSIFICATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN SECRETION;

EID: 84969138618     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/acsbiomaterials.5b00277     Document Type: Article

References (56)

1. Hildebrand, F.; van Griensven, M.; Giannoudis, P.; Schreiber, T.; Frink, M.; Probst, C.; Grotz, M.; Krettek, C.; Pape, H. C. Impact of hypothermia on the immunologic response after trauma and elective surgery Surgical technology international 2005, 14, 41-50
2. Habal, M. B.; Reddi, A. H. Bone grafts and bone induction substitutes Clin. Plast. Surg. 1994, 21 (4) 525-42
3. Brinker, M. R.; O'Connor, D. P. Outcomes of tibial nonunion in older adults following treatment using the Ilizarov method Journal of orthopaedic trauma 2007, 21 (9) 634-42 10.1097/BOT.0b013e318156c2a2
4. Schmidmaier, G.; Capanna, R.; Wildemann, B.; Beque, T.; Lowenberg, D. Bone morphogenetic proteins in critical-size bone defects: what are the options? Injury 2009, 40 (Suppl 3) S39-S43 10.1016/S0020-1383(09)70010-5
5. Ronga, M.; Fagetti, A.; Canton, G.; Paiusco, E.; Surace, M. F.; Cherubino, P. Clinical applications of growth factors in bone injuries: experience with BMPs Injury 2013, 44 (Suppl 1) S34-S39 10.1016/S0020-1383(13)70008-1
6. Steinert, A. F.; Rackwitz, L.; Gilbert, F.; Noth, U.; Tuan, R. S. Concise review: the clinical application of mesenchymal stem cells for musculoskeletal regeneration: current status and perspectives Stem Cells Transl. Med. 2012, 1 (3) 237-47 10.5966/sctm.2011-0036
7. Johnstone, B.; Hering, T. M.; Caplan, A. I.; Goldberg, V. M.; Yoo, J. U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells Exp. Cell Res. 1998, 238 (1) 265-72 10.1006/excr.1997.3858
8. Tuan, R. S.; Boland, G.; Tuli, R. Adult mesenchymal stem cells and cell-based tissue engineering Arthritis research & therapy 2003, 5 (1) 32-45 10.1186/ar614
9. Welter, J. F.; Solchaga, L. A.; Penick, K. J. Simplification of aggregate culture of human mesenchymal stem cells as a chondrogenic screening assay BioTechniques 2007, 42 (6) 732 734-7 10.2144/000112451
10. Athanasiou, K. A.; Eswaramoorthy, R.; Hadidi, P.; Hu, J. C. Self-organization and the self-assembling process in tissue engineering Annu. Rev. Biomed. Eng. 2013, 15, 115-36 10.1146/annurev-bioeng-071812-152423
11. Lin, R. Z.; Chang, H. Y. Recent advances in three-dimensional multicellular spheroid culture for biomedical research Biotechnol. J. 2008, 3 (9-10) 1172-84 10.1002/biot.200700228
12. Langenbach, F.; Naujoks, C.; Smeets, R.; Berr, K.; Depprich, R.; Kubler, N.; Handschel, J. Scaffold-free microtissues: differences from monolayer cultures and their potential in bone tissue engineering Clinical oral investigations 2013, 17 (1) 9-17 10.1007/s00784-012-0763-8
13. Solorio, L. D.; Vieregge, E. L.; Dhami, C. D.; Alsberg, E. High-density cell systems incorporating polymer microspheres as microenvironmental regulators in engineered cartilage tissues Tissue Eng., Part B 2013, 19 (3) 209-20 10.1089/ten.teb.2012.0252
14. Hildebrandt, C.; Buth, H.; Thielecke, H. A scaffold-free in vitro model for osteogenesis of human mesenchymal stem cells Tissue Cell 2011, 43 (2) 91-100 10.1016/j.tice.2010.12.004
15. Ferro, F.; Falini, G.; Spelat, R.; D'Aurizio, F.; Puppato, E.; Pandolfi, M.; Beltrami, A. P.; Cesselli, D.; Beltrami, C. A.; Impiombato, F. S.; Curcio, F. Biochemical and biophysical analyses of tissue-engineered bone obtained from three-dimensional culture of a subset of bone marrow mesenchymal stem cells Tissue Eng., Part A 2010, 16 (12) 3657-67 10.1089/ten.tea.2009.0750
16. Burns, J. S.; Rasmussen, P. L.; Larsen, K. H.; Schroder, H. D.; Kassem, M. Parameters in three-dimensional osteospheroids of telomerized human mesenchymal (stromal) stem cells grown on osteoconductive scaffolds that predict in vivo bone-forming potential Tissue Eng., Part A 2010, 16 (7) 2331-42 10.1089/ten.tea.2009.0735
17. Wang, W.; Itaka, K.; Ohba, S.; Nishiyama, N.; Chung, U. I.; Yamasaki, Y.; Kataoka, K. 3D spheroid culture system on micropatterned substrates for improved differentiation efficiency of multipotent mesenchymal stem cells Biomaterials 2009, 30 (14) 2705-15 10.1016/j.biomaterials.2009.01.030
18. Muraglia, A.; Corsi, A.; Riminucci, M.; Mastrogiacomo, M.; Cancedda, R.; Bianco, P.; Quarto, R. Formation of a chondro-osseous rudiment in micromass cultures of human bone-marrow stromal cells J. Cell Sci. 2003, 116 (Pt 14) 2949-55 10.1242/jcs.00527
19. Farrell, E.; Both, S. K.; Odorfer, K. I.; Koevoet, W.; Kops, N.; O'Brien, F. J.; Baatenburg de Jong, R. J.; Verhaar, J. A.; Cuijpers, V.; Jansen, J.; Erben, R. G.; van Osch, G. J. In-vivo generation of bone via endochondral ossification by in-vitro chondrogenic priming of adult human and rat mesenchymal stem cells BMC Musculoskeletal Disord. 2011, 12, 31 10.1186/1471-2474-12-31
20. Scotti, C.; Tonnarelli, B.; Papadimitropoulos, A.; Scherberich, A.; Schaeren, S.; Schauerte, A.; Lopez-Rios, J.; Zeller, R.; Barbero, A.; Martin, I. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (16) 7251-6 10.1073/pnas.1000302107
21. Govender, S.; Csimma, C.; Genant, H. K.; Valentin-Opran, A.; Amit, Y.; Arbel, R.; Aro, H.; Atar, D.; Bishay, M.; Borner, M. G.; Chiron, P.; Choong, P.; Cinats, J.; Courtenay, B.; Feibel, R.; Geulette, B.; Gravel, C.; Haas, N.; Raschke, M.; Hammacher, E.; van der Velde, D.; Hardy, P.; Holt, M.; Josten, C.; Ketterl, R. L.; Lindeque, B.; Lob, G.; Mathevon, H.; McCoy, G.; Marsh, D.; Miller, R.; Munting, E.; Oevre, S.; Nordsletten, L.; Patel, A.; Pohl, A.; Rennie, W.; Reynders, P.; Rommens, P. M.; Rondia, J.; Rossouw, W. C.; Daneel, P. J.; Ruff, S.; Ruter, A.; Santavirta, S.; Schildhauer, T. A.; Gekle, C.; Schnettler, R.; Segal, D.; Seiler, H.; Snowdowne, R. B.; Stapert, J.; Taglang, G.; Verdonk, R.; Vogels, L.; Weckbach, A.; Wentzensen, A.; Wisniewski, T. Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients Journal of bone and joint surgery. American volume 2002, 84-A (12) 2123-34
22. Wozney, J. M.; Rosen, V.; Celeste, A. J.; Mitsock, L. M.; Whitters, M. J.; Kriz, R. W.; Hewick, R. M.; Wang, E. A. Novel regulators of bone formation: molecular clones and activities Science 1988, 242 (4885) 1528-34 10.1126/science.3201241
23. Wang, E. A.; Rosen, V.; D'Alessandro, J. S.; Bauduy, M.; Cordes, P.; Harada, T.; Israel, D. I.; Hewick, R. M.; Kerns, K. M.; LaPan, P. et al. Recombinant human bone morphogenetic protein induces bone formation Proc. Natl. Acad. Sci. U. S. A. 1990, 87 (6) 2220-4 10.1073/pnas.87.6.2220
24. Schmitt, B.; Ringe, J.; Haupl, T.; Notter, M.; Manz, R.; Burmester, G. R.; Sittinger, M.; Kaps, C. BMP2 initiates chondrogenic lineage development of adult human mesenchymal stem cells in high-density culture Differentiation 2003, 71 (9-10) 567-77 10.1111/j.1432-0436.2003.07109003.x
25. Leboy, P. S.; Sullivan, T. A.; Nooreyazdan, M.; Venezian, R. A. Rapid chondrocyte maturation by serum-free culture with BMP-2 and ascorbic acid J. Cell. Biochem. 1997, 66 (3) 394-403 10.1002/(SICI)1097-4644(19970901)66:3<394::AID-JCB11>3.0.CO;2-F
26. Soballe, K.; Overgaard, S.; Hansen, E. S.; Brokstedt-Rasmussen, H.; Lind, M.; Bunger, C. A review of ceramic coatings for implant fixation J. Long-Term Eff. Med. Implants 1999, 9 (1-2) 131-51
27. Dumbleton, J.; Manley, M. T. Hydroxyapatite-coated prostheses in total hip and knee arthroplasty Journal of bone and joint surgery. American volume 2004, 86-A (11) 2526-40
28. He, P.; Sahoo, S.; Ng, K. S.; Chen, K.; Toh, S. L.; Goh, J. C. Enhanced osteoinductivity and osteoconductivity through hydroxyapatite coating of silk-based tissue-engineered ligament scaffold J. Biomed. Mater. Res., Part A 2013, 101A (2) 555-66 10.1002/jbm.a.34333
29. Chiroff, R. T.; White, R. A.; White, E. W.; Weber, J. N.; Roy, D. The restoration of the articular surfaces overlying Replamineform porous biomaterials J. Biomed. Mater. Res. 1977, 11 (2) 165-78 10.1002/jbm.820110203
30. Suominen, E.; Aho, A. J.; Vedel, E.; Kangasniemi, I.; Uusipaikka, E.; Yli-Urpo, A. Subchondral bone and cartilage repair with bioactive glasses, hydroxyapatite, and hydroxyapatite-glass composite J. Biomed. Mater. Res. 1996, 32 (4) 543-51 10.1002/(SICI)1097-4636(199612)32:4<543::AID-JBM7>3.0.CO;2-R
31. Sotoudeh, A.; Jahanshahi, A.; Takhtfooladi, M. A.; Bazazan, A.; Ganjali, A.; Harati, M. P. Study on nano-structured hydroxyapatite/zirconia stabilized yttria on healing of articular cartilage defect in rabbit Acta cirurgica brasileira/Sociedade Brasileira para Desenvolvimento Pesquisa em Cirurgia 2013, 28 (5) 340-5 10.1590/S0102-86502013000500004
32. Sumner, D. R.; Turner, T. M.; Urban, R. M.; Virdi, A. S.; Inoue, N. Additive enhancement of implant fixation following combined treatment with rhTGF-beta2 and rhBMP-2 in a canine model Journal of bone and joint surgery. American volume 2006, 88 (4) 806-17 10.2106/JBJS.E.00846
33. Alt, V.; Pfefferle, H. J.; Kreuter, J.; Stahl, J. P.; Pavlidis, T.; Meyer, C.; Mockwitz, J.; Wenisch, S.; Schnettler, R. Effect of glycerol-L-lactide coating polymer on bone ingrowth of bFGF-coated hydroxyapatite implants J. Controlled Release 2004, 99 (1) 103-11 10.1016/j.jconrel.2004.06.017
34. Hossain, M.; Irwin, R.; Baumann, M. J.; McCabe, L. R. Hepatocyte growth factor (HGF) adsorption kinetics and enhancement of osteoblast differentiation on hydroxyapatite surfaces Biomaterials 2005, 26 (15) 2595-602 10.1016/j.biomaterials.2004.07.051
35. Yu, X.; Khalil, A.; Dang, P. N.; Alsberg, E.; Murphy, W. L. Multilayered Inorganic Microparticles for Tunable Dual Growth Factor Delivery Adv. Funct. Mater. 2014, 24 (20) 3082-3093 10.1002/adfm.201302859
36. Jongpaiboonkit, L.; Franklin-Ford, T.; Murphy, W. L. Growth of hydroxyapatite coatings on biodegradable polymer microspheres ACS Appl. Mater. Interfaces 2009, 1 (7) 1504-11 10.1021/am9001716
37. Ishaug-Riley, S. L.; Crane, G. M.; Gurlek, A.; Miller, M. J.; Yasko, A. W.; Yaszemski, M. J.; Mikos, A. G. Ectopic bone formation by marrow stromal osteoblast transplantation using poly(DL-lactic-co-glycolic acid) foams implanted into the rat mesentery J. Biomed. Mater. Res. 1997, 36 (1) 1-8 10.1002/(SICI)1097-4636(199707)36:1<1::AID-JBM1>3.0.CO;2-P
38. Ishaug, S. L.; Crane, G. M.; Miller, M. J.; Yasko, A. W.; Yaszemski, M. J.; Mikos, A. G. Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds J. Biomed. Mater. Res. 1997, 36 (1) 17-28 10.1002/(SICI)1097-4636(199707)36:1<17::AID-JBM3>3.3.CO;2-D
39. Coyle, C. H.; Izzo, N. J.; Chu, C. R. Sustained hypoxia enhances chondrocyte matrix synthesis J. Orthop. Res. 2009, 27 (6) 793-9 10.1002/jor.20816
40. Schipani, E. Hypoxia and HIF-1alpha in chondrogenesis Ann. N. Y. Acad. Sci. 2006, 1068, 66-73 10.1196/annals.1346.009
41. Petersen, W.; Tsokos, M.; Pufe, T. Expression of VEGF121 and VEGF165 in hypertrophic chondrocytes of the human growth plate and epiphyseal cartilage J. Anat. 2002, 201 (2) 153-7 10.1046/j.1469-7580.2002.00085.x
42. Haynesworth, S. E.; Goshima, J.; Goldberg, V. M.; Caplan, A. I. Characterization of cells with osteogenic potential from human marrow Bone 1992, 13 (1) 81-8 10.1016/8756-3282(92)90364-3
43. Solorio, L. D.; Dhami, C. D.; Dang, P. N.; Vieregge, E. L.; Alsberg, E. Spatiotemporal regulation of chondrogenic differentiation with controlled delivery of transforming growth factor-beta1 from gelatin microspheres in mesenchymal stem cell aggregates Stem Cells Transl. Med. 2012, 1 (8) 632-9 10.5966/sctm.2012-0039
44. Honda, Y.; Ding, X.; Mussano, F.; Wiberg, A.; Ho, C. M.; Nishimura, I. Guiding the osteogenic fate of mouse and human mesenchymal stem cells through feedback system control Sci. Rep. 2013, 3, 3420 10.1038/srep03420
45. Farndale, R. W.; Buttle, D. J.; Barrett, A. J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue Biochim. Biophys. Acta, Gen. Subj. 1986, 883 (2) 173-7 10.1016/0304-4165(86)90306-5
46. Estes, B. T.; Diekman, B. O.; Gimble, J. M.; Guilak, F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype Nat. Protoc. 2010, 5 (7) 1294-311 10.1038/nprot.2010.81
47. Egan, K. P.; Brennan, T. A.; Pignolo, R. J. Bone histomorphometry using free and commonly available software Histopathology 2012, 61 (6) 1168-73 10.1111/j.1365-2559.2012.04333.x
48. Miao, D.; Scutt, A. Histochemical localization of alkaline phosphatase activity in decalcified bone and cartilage J. Histochem. Cytochem. 2002, 50 (3) 333-40 10.1177/002215540205000305
49. van der Stok, J.; Koolen, M. K.; Jahr, H.; Kops, N.; Waarsing, J. H.; Weinans, H.; van der Jagt, O. P. Chondrogenically differentiated mesenchymal stromal cell pellets stimulate endochondral bone regeneration in critical-sized bone defects Eur. Cell. Mater. 2014, 27, 137-48 discussion 148
50. Liu, K.; Zhou, G. D.; Liu, W.; Zhang, W. J.; Cui, L.; Liu, X.; Liu, T. Y.; Cao, Y. The dependence of in vivo stable ectopic chondrogenesis by human mesenchymal stem cells on chondrogenic differentiation in vitro Biomaterials 2008, 29 (14) 2183-92 10.1016/j.biomaterials.2008.01.021
51. Kim, Y. J.; Sah, R. L.; Doong, J. Y.; Grodzinsky, A. J. Fluorometric assay of DNA in cartilage explants using Hoechst 33258 Anal. Biochem. 1988, 174 (1) 168-76 10.1016/0003-2697(88)90532-5
52. Awad, H. A.; Halvorsen, Y. D.; Gimble, J. M.; Guilak, F. Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells Tissue Eng. 2003, 9 (6) 1301-12 10.1089/10763270360728215
53. Mueller, M. B.; Fischer, M.; Zellner, J.; Berner, A.; Dienstknecht, T.; Prantl, L.; Kujat, R.; Nerlich, M.; Tuan, R. S.; Angele, P. Hypertrophy in mesenchymal stem cell chondrogenesis: effect of TGF-beta isoforms and chondrogenic conditioning Cells Tissues Organs 2010, 192 (3) 158-66 10.1159/000313399
54. Siddappa, R.; Licht, R.; van Blitterswijk, C.; de Boer, J. Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering J. Orthop. Res. 2007, 25 (8) 1029-41 10.1002/jor.20402
55. Mentink, A.; Hulsman, M.; Groen, N.; Licht, R.; Dechering, K. J.; van der Stok, J.; Alves, H. A.; Dhert, W. J.; van Someren, E. P.; Reinders, M. J.; van Blitterswijk, C. A.; de Boer, J. Predicting the therapeutic efficacy of MSC in bone tissue engineering using the molecular marker CADM1 Biomaterials 2013, 34 (19) 4592-601 10.1016/j.biomaterials.2013.03.001
56. Phinney, D. G.; Kopen, G.; Righter, W.; Webster, S.; Tremain, N.; Prockop, D. J. Donor variation in the growth properties and osteogenic potential of human marrow stromal cells J. Cell. Biochem. 1999, 75 (3) 424-36 10.1002/(SICI)1097-4644(19991201)75:3<424::AID-JCB8>3.3.CO;2-#