Bone regeneration using an alpha 2 beta 1 integrin-specific hydrogel as a BMP-2 delivery vehicle

Biomaterials

Volumn 35, Issue 21, 2014, Pages 5453-5461

  Shekaran, Asha ^a,b,d   García, José R ^b,c   Clark, Amy Y ^b,c   Kavanaugh, Taylor E ^a   Lin, Angela S ^b,c   Guldberg, Robert E ^b,c   García, Andrés J ^b,c  

^a Wallace H Coulter Department of Biomedical Engineering   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

BMP 2; Bone healing; Hydrogel; Integrin specific; Polyethylene glycol; Protein delivery

Indexed keywords

BONE; DEFECTS; POLYETHYLENE GLYCOLS; PROTEINS; REPAIR; STEM CELLS;

BMP-2; BONE HEALING; BONE MORPHOGENETIC PROTEINS; INTEGRIN-SPECIFIC; MECHANICALLY ROBUST; PROTEIN DELIVERY; PROTEIN THERAPEUTICS; STEM CELL DIFFERENTIATION;

HYDROGELS;

BMP2 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN; HYDROGEL; MACROGOL DERIVATIVE; PEPTIDE; RECOMBINANT PROTEIN; VERY LATE ACTIVATION ANTIGEN 2;

ANIMAL; BONE; BONE DEVELOPMENT; BONE REGENERATION; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE TRANSFER; GENETICS; HUMAN; HYDROGEL; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MOUSE; PHARMACOLOGY; PHYSIOLOGY; TISSUE ENGINEERING; WOUND HEALING;

ANIMALS; BONE AND BONES; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL DIFFERENTIATION; COLLAGEN; GENE TRANSFER TECHNIQUES; HUMANS; HYDROGELS; INTEGRIN ALPHA2BETA1; MALE; MESENCHYMAL STROMAL CELLS; MICE; OSTEOGENESIS; PEPTIDES; POLYETHYLENE GLYCOLS; RECOMBINANT PROTEINS; TISSUE ENGINEERING; WOUND HEALING;

EID: 84899489425     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.03.055     Document Type: Article

References (51)

1. Bucholz R.W. Nonallograft osteoconductive bone graft substitutes. Clin Orthop Relat Res 2002, 395:44-52.
2. Finkemeier C.G. Bone-grafting and bone-graft substitutes. JBone Joint Surg Am 2002, 84-A(3):454-464.
3. Giannoudis P.V., Dinopoulos H., Tsiridis E. Bone substitutes: an update. Injury 2005, 36(Suppl.3):S20-S27.
4. Kretlow J.D., Mikos A.G. Review: mineralization of synthetic polymer scaffolds for bone tissue engineering. Tissue Eng 2007, 13(5):927-938.
5. De Long W.G., Einhorn T.A., Koval K., McKee M., Smith W., Sanders R., et al. Bone grafts and bone graft substitutes in orthopaedic trauma surgery. A critical analysis. JBone Joint Surg Am 2007, 89(3):649-658.
6. Schmidmaier G., Schwabe P., Strobel C., Wildemann B. Carrier systems and application of growth factors in orthopaedics. Injury 2008, 39(Suppl.2):S37-S43.
7. Desai B.M. Osteobiologics. Am J Orthop (Belle Mead NJ) 2007, 36(4 Suppl.):8-11.
8. Carragee E.J., Hurwitz E.L., Weiner B.K. Acritical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned. Spine J 2011, 11(6):471-491.
9. Yoon S.T., Boden S.D. Osteoinductive molecules in orthopaedics: basic science and preclinical studies. Clin Orthop Relat Res 2002, 395:33-43.
10. Bishop G.B., Einhorn T.A. Current and future clinical applications of bone morphogenetic proteins in orthopaedic trauma surgery. Int Orthop 2007, 31(6):721-727.
11. Mikos A.G., Herring S.W., Ochareon P., Elisseeff J., Lu H.H., Kandel R., et al. Engineering complex tissues. Tissue Eng 2006, 12(12):3307-3339.
12. Salinas C.N., Anseth K.S. Mesenchymal stem cells for craniofacial tissue regeneration: designing hydrogel delivery vehicles. JDent Res 2009, 88(8):681-692.
13. Lutolf M.P., Hubbell J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005, 23(1):47-55.
14. Ratner B.D., Hoffman A.S. Non-fouling surfaces. Biomaterials science: an introduction to materials in medicine 2013, 241-247. Academic Press. D.R. Buddy, S.H. Allan, J.S. Frederick, E.L. Jack (Eds.).
15. Bailon P., Won C.Y. PEG-modified biopharmaceuticals. Expert Opin Drug Deliv 2009, 6(1):1-16.
16. Lutolf M.P., Weber F.E., Schmoekel H.G., Schense J.C., Kohler T., Muller R., et al. Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat Biotechnol 2003, 21(5):513-518.
17. Mariner P.D., Wudel J.M., Miller D.E., Genova E.E., Streubel S.O., Anseth K.S. Synthetic hydrogel scaffold is an effective vehicle for delivery of INFUSE (rhBMP2) to critical-sized calvaria bone defects in rats. JOrthop Res 2013, 31(3):401-406.
18. Reichert J.C., Cipitria A., Epari D.R., Saifzadeh S., Krishnakanth P., Berner A., et al. Atissue engineering solution for segmental defect regeneration in load-bearing long bones. Sci Transl Med 2012, 4(141):141ra93.
19. Boerckel J.D., Kolambkar Y.M., Dupont K.M., Uhrig B.A., Phelps E.A., Stevens H.Y., et al. Effects of protein dose and delivery system on BMP-mediated bone regeneration. Biomaterials 2011, 32(22):5241-5251.
20. Phelps E.A., Enemchukwu N.O., Fiore V.F., Sy J.C., Murthy N., Sulchek T.A., et al. Maleimide cross-linked bioactive PEG hydrogel exhibits improved reaction kinetics and cross-linking for cell encapsulation and in situ delivery. Adv Mater 2012, 24(1):64-70. 2.
21. Phelps E.A., Headen D.M., Taylor W.R., Thule P.M., Garcia A.J. Vasculogenic bio-synthetic hydrogel for enhancement of pancreatic islet engraftment and function in type 1 diabetes. Biomaterials 2013, 34(19):4602-4611.
22. Reyes C.D., Petrie T.A., Burns K.L., Schwartz Z., Garcia A.J. Biomolecular surface coating to enhance orthopaedic tissue healing and integration. Biomaterials 2007, 28(21):3228-3235.
23. Martino M.M., Tortelli F., Mochizuki M., Traub S., Ben-David D., Kuhn G.A., et al. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci Transl Med 2011, 3(100):100ra89.
24. Bourdoulous S., Orend G., MacKenna D.A., Pasqualini R., Ruoslahti E. Fibronectin matrix regulates activation of RHO and CDC42 GTPases and cell cycle progression. JCell Biol 1998, 143(1):267-276.
25. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276(5317):1425-1428.
26. Giancotti F.G., Ruoslahti E. Integrin signaling. Science 1999, 285(5430):1028-1032.
27. Mizuno M., Fujisawa R., Kuboki Y. Type I collagen-induced osteoblastic differentiation of bone-marrow cells mediated by collagen-alpha 2 beta 1 integrin interaction. JCell Physiol 2000, 184(2):207-213.
28. Jikko A., Harris S.E., Chen D., Mendrick D.L., Damsky C.H. Collagen integrin receptors regulate early osteoblast differentiation induced by BMP-2. JBone Min Res 1999, 14(7):1075-1083.
29. Mizuno M., Kuboki Y. Osteoblast-related gene expression of bone marrow cells during the osteoblastic differentiation induced by type I collagen. JBiochem 2001, 129(1):133-138.
30. Suzawa M., Tamura Y., Fukumoto S., Miyazono K., Fujita T., Kato S., et al. Stimulation of Smad1 transcriptional activity by Ras-extracellular signal-regulated kinase pathway: a possible mechanism for collagen-dependent osteoblastic differentiation. JBone Min Res 2002, 17(2):240-248.
31. Takeuchi Y., Suzawa M., Kikuchi T., Nishida E., Fujita T., Matsumoto T. Differentiation and transforming growth factor-beta receptor down-regulation by collagen-alpha2beta1 integrin interaction is mediated by focal adhesion kinase and its downstream signals in murine osteoblastic cells. JBiol Chem 1997, 272(46):29309-29316.
32. Xiao G., Wang D., Benson M.D., Karsenty G., Franceschi R.T. Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. JBiol Chem 1998, 273(49):32988-32994.
33. Morton L.F., Peachey A.R., Zijenah L.S., Goodall A.H., Humphries M.J., Barnes M.J. Conformation-dependent platelet adhesion to collagen involving integrin alpha 2 beta 1-mediated and other mechanisms: multiple alpha 2 beta 1-recognition sites in collagen type I. Biochem J 1994, 299(Pt 3):791-797.
34. Knight C.G., Morton L.F., Peachey A.R., Tuckwell D.S., Farndale R.W., Barnes M.J. The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. JBiol Chem 2000, 275(1):35-40.
35. Knight C.G., Morton L.F., Onley D.J., Peachey A.R., Messent A.J., Smethurst P.A., et al. Identification in collagen type I of an integrin alpha2 beta1-binding site containing an essential GER sequence. JBiol Chem 1998, 273(50):33287-33294.
36. Reyes C.D., Garcia A.J. Engineering integrin-specific surfaces with a triple-helical collagen-mimetic peptide. JBiomed Mater Res A 2003, 65(4):511-523.
37. Reyes C.D., Garcia A.J. Alpha2beta1 integrin-specific collagen-mimetic surfaces supporting osteoblastic differentiation. JBiomed Mater Res A 2004, 69(4):591-600.
38. Wojtowicz A.M., Shekaran A., Oest M.E., Dupont K.M., Templeman K.L., Hutmacher D.W., et al. Coating of biomaterial scaffolds with the collagen-mimetic peptide GFOGER for bone defect repair. Biomaterials 2010, 31(9):2574-2582.
39. Miljkovic N.D., Cooper G.M., Hott S.L., Disalle B.F., Gawalt E.S., Smith D.M., et al. Calcium aluminate, RGD-modified calcium aluminate, and beta-tricalcium phosphate implants in a calvarial defect. JCraniofac Surg 2009, 20(5):1538-1543.
40. Hennessy K.M., Clem W.C., Phipps M.C., Sawyer A.A., Shaikh F.M., Bellis S.L. The effect of RGD peptides on osseointegration of hydroxyapatite biomaterials. Biomaterials 2008, 29(21):3075-3083.
41. Jager M., Boge C., Janissen R., Rohrbeck D., Hulsen T., Lensing-Hohn S., et al. Osteoblastic potency of bone marrow cells cultivated on functionalized biometals with cyclic RGD-peptide. JBiomed Mater Res A 2013, 101(10):2905-2914.
42. Duvall C.L., Taylor W.R., Weiss D., Wojtowicz A.M., Guldberg R.E. Impaired angiogenesis, early callus formation, and late stage remodeling in fracture healing of osteopontin-deficient mice. JBone Min Res 2007, 22(2):286-297.
43. Patterson J., Hubbell J.A. SPARC-derived protease substrates to enhance the plasmin sensitivity of molecularly engineered PEG hydrogels. Biomaterials 2011, 32(5):1301-1310.
44. Patterson J., Hubbell J.A. Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2. Biomaterials 2010, 31(30):7836-7845.
45. Kimelman-Bleich N., Pelled G., Zilberman Y., Kallai I., Mizrahi O., Tawackoli W., et al. Targeted gene-and-host progenitor cell therapy for nonunion bone fracture repair. Mol Ther 2011, 19(1):53-59.
46. Kolambkar Y.M., Boerckel J.D., Dupont K.M., Bajin M., Huebsch N., Mooney D.J., et al. Spatiotemporal delivery of bone morphogenetic protein enhances functional repair of segmental bone defects. Bone 2011, 49(3):485-492.
47. Lehman R.A., Kang D.G. Symptomatic ectopic intracanal ossification after transforaminal lumbar interbody fusion with rhBMP-2. Spine J 2012, 12(6):530-531.
48. Fiedler J., Roderer G., Gunther K.P., Brenner R.E. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. JCell Biochem 2002, 87(3):305-312.
49. Sorger J.I., Hornicek F.J., Zavatta M., Menzner J.P., Gebhardt M.C., Tomford W.W., et al. Allograft fractures revisited. Clin Orthop Relat Res 2001, 382:66-74.
50. Mankin H.J., Hornicek F.J., Raskin K.A. Infection in massive bone allografts. Clin Orthop Relat Res 2005, 432:210-216.
51. Azad V., Breitbart E., Al-Zube L., Yeh S., O'Connor J.P., Lin S.S. rhBMP-2 enhances the bone healing response in a diabetic rat segmental defect model. JOrthop Trauma 2009, 23(4):267-276.