Extracellular matrix-inspired growth factor delivery systems for bone regeneration

Advanced Drug Delivery Reviews

Volumn 94, Issue , 2015, Pages 41-52

  Martino, Mikaël M ^a   Briquez, Priscilla S ^b   Maruyama, Kenta ^a   Hubbell, Jeffrey A ^b,c,d  

^a OSAKA UNIVERSITY   (Japan)

^b EPFL   (Switzerland)

^c UNIVERSITY OF CHICAGO   (United States)

^d ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Bone morphogenetic protein; Clinical translation; Controlled delivery; Extracellular matrix; Fibroblast growth factor; Integrins; Platelet derived growth factor; Vascular endothelial growth factor

Indexed keywords

CELL CULTURE; COST EFFECTIVENESS;

BONE MORPHOGENETIC PROTEINS; CLINICAL TRANSLATION; CONTROLLED DELIVERY; EXTRACELLULAR MATRICES; FIBROBLAST GROWTH FACTOR; INTEGRINS; PLATELET-DERIVED GROWTH FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

TISSUE REGENERATION;

BIOMATERIAL; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN SPONGE; COLONY STIMULATING FACTOR 1; FIBRINOGEN; FIBROBLAST GROWTH FACTOR 2; GELATIN; GLYCOSAMINOGLYCAN; GROWTH DIFFERENTIATION FACTOR; GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR; MACROGOL; NANOPARTICLE; OSTEOGENIC PROTEIN 1; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR; TUMOR NECROSIS FACTOR; VASCULOTROPIN; VASCULOTROPIN A; BONE MORPHOGENETIC PROTEIN; DELAYED RELEASE FORMULATION; FIBROBLAST GROWTH FACTOR; INTEGRIN; PLATELET DERIVED GROWTH FACTOR; SIGNAL PEPTIDE;

ANGIOGENESIS; BINDING AFFINITY; BONE MINERALIZATION; BONE REGENERATION; BONE REMODELING; CALLUS; CELL FUNCTION; COST EFFECTIVENESS ANALYSIS; DIABETES MELLITUS; DRUG DELIVERY SYSTEM; DRUG MECHANISM; DRUG PROTEIN BINDING; EXTRACELLULAR MATRIX; FRACTURE HEALING; HUMAN; MICROENVIRONMENT; NONHUMAN; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; REVASCULARIZATION; REVIEW; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TISSUE INTERACTION; UNSPECIFIED SIDE EFFECT; DELAYED RELEASE FORMULATION; INFLAMMATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

BONE MORPHOGENETIC PROTEINS; BONE REGENERATION; DELAYED-ACTION PREPARATIONS; DRUG DELIVERY SYSTEMS; EXTRACELLULAR MATRIX; FIBROBLAST GROWTH FACTORS; HUMANS; INFLAMMATION; INTEGRINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PLATELET-DERIVED GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84947617350     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2015.04.007     Document Type: Review

References (167)

1. Marsell R., Einhorn T.A. The biology of fracture healing. Injury 2011, 42:551-555.
2. Schindeler A., McDonald M.M., Bokko P., Little D.G. Bone remodeling during fracture repair: The cellular picture. Semin. Cell Dev. Biol. 2008, 19:459-466.
3. Shapiro F. Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur. Cell Mater. 2008, 15:53-76.
4. Audige L., Griffin D., Bhandari M., Kellam J., Ruedi T.P. Path analysis of factors for delayed healing and nonunion in 416 operatively treated tibial shaft fractures. Clin. Orthop. Relat. Res. 2005, 438:221-232.
5. Gruber R., Koch H., Doll B.A., Tegtmeier F., Einhorn T.A., Hollinger J.O. Fracture healing in the elderly patient. Exp. Gerontol. 2006, 41:1080-1093.
6. Lu C., Hansen E., Sapozhnikova A., Hu D., Miclau T., Marcucio R.S. Effect of age on vascularization during fracture repair. J. Orthop. Res. 2008, 26:1384-1389.
7. Lynch J.R., Taitsman L.A., Barei D.P., Nork S.E. Femoral nonunion: risk factors and treatment options. J. Am. Acad. Orthop. Surg. 2008, 16:88-97.
8. Wukich D.K., Kline A.J. The management of ankle fractures in patients with diabetes. J. Bone Joint Surg. Am. Vol. 2008, 90:1570-1578.
9. Aronson J. Limb-lengthening, skeletal reconstruction, and bone transport with the Ilizarov method. J. Bone Joint Surg. Am. Vol. 1997, 79:1243-1258.
10. Perry C.R. Bone repair techniques, bone graft, and bone graft substitutes. Clin. Orthop. Relat. Res. 1999, 71-86.
11. Giannoudis P.V., Dinopoulos H., Tsiridis E. Bone substitutes: an update. Injury 2005, 36(Suppl. 3):S20-S27.
12. Laurencin C., Khan Y., El-Amin S.F. Bone graft substitutes. Expert Rev. Med. Devices 2006, 3:49-57.
13. Giannoudis P.V., Einhorn T.A., Marsh D. Fracture healing: the diamond concept. Injury 2007, 38(Suppl. 4):S3-S6.
14. Giannoudis P.V., Einhorn T.A., Schmidmaier G., Marsh D. The diamond concept - open questions. Injury 2008, 39(Suppl. 2):S5-S8.
15. Dawson J.I., Kanczler J., Tare R., Kassem M., Oreffo R.O. Concise review: bridging the gap: bone regeneration using skeletal stem cell-based strategies - where are we now?. Stem Cells 2014, 32:35-44.
16. Ratcliffe E., Glen K.E., Naing M.W., Williams D.J. Current status and perspectives on stem cell-based therapies undergoing clinical trials for regenerative medicine: case studies. Br. Med. Bull. 2013, 108:73-94.
17. Reichert J.C., Cipitria A., Epari D.R., Saifzadeh S., Krishnakanth P., Berner A., Woodruff M.A., Schell H., Mehta M., Schuetz M.A., Duda G.N., Hutmacher D.W. A tissue engineering solution for segmental defect regeneration in load-bearing long bones. Sci. Transl. Med. 2012, 4:141ra193.
18. Even J., Eskander M., Kang J. Bone morphogenetic protein in spine surgery: current and future uses. J. Am. Acad. Orthop. Surg. 2012, 20:547-552.
19. Axelrad T.W., Einhorn T.A. Bone morphogenetic proteins in orthopaedic surgery. Cytokine Growth Factor Rev. 2009, 20:481-488.
20. Kitamura M., Akamatsu M., Machigashira M., Hara Y., Sakagami R., Hirofuji T., Hamachi T., Maeda K., Yokota M., Kido J., Nagata T., Kurihara H., Takashiba S., Sibutani T., Fukuda M., Noguchi T., Yamazaki K., Yoshie H., Ioroi K., Arai T., Nakagawa T., Ito K., Oda S., Izumi Y., Ogata Y., Yamada S., Shimauchi H., Kunimatsu K., Kawanami M., Fujii T., Furuichi Y., Furuuchi T., Sasano T., Imai E., Omae M., Yamada S., Watanuki M., Murakami S. FGF-2 stimulates periodontal regeneration: results of a multi-center randomized clinical trial. J. Dent. Res. 2011, 90:35-40.
21. Nevins M., Kao R.T., McGuire M.K., McClain P.K., Hinrichs J.E., McAllister B.S., Reddy M.S., Nevins M.L., Genco R.J., Lynch S.E., Giannobile W.V. Platelet-derived growth factor promotes periodontal regeneration in localized osseous defects: 36-month extension results from a randomized, controlled, double-masked clinical trial. J. Periodontol. 2013, 84:456-464.
22. Yun Y.R., Jang J.H., Jeon E., Kang W., Lee S., Won J.E., Kim H.W., Wall I. Administration of growth factors for bone regeneration. Regen. Med. 2012, 7:369-385.
23. Claes L., Recknagel S., Ignatius A. Fracture healing under healthy and inflammatory conditions. Nat. Rev. Rheumatol. 2012, 8:133-143.
24. Ai-Aql Z.S., Alagl A.S., Graves D.T., Gerstenfeld L.C., Einhorn T.A. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J. Dent. Res. 2008, 87:107-118.
25. Cho T.J., Gerstenfeld L.C., Einhorn T.A. Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. J. Bone Miner. Res. 2002, 17:513-520.
26. Mountziaris P.M., Mikos A.G. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng. B Rev. 2008, 14:179-186.
27. Glass G.E., Chan J.K., Freidin A., Feldmann M., Horwood N.J., Nanchahal J. TNF-alpha promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1585-1590.
28. Liu Y., Wang L., Kikuiri T., Akiyama K., Chen C., Xu X., Yang R., Chen W., Wang S., Shi S. Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-gamma and TNF-alpha. Nat. Med. 2011, 17:1594-1601.
29. Hankenson K.D., Dishowitz M., Gray C., Schenker M. Angiogenesis in bone regeneration. Injury 2011, 42:556-561.
30. Xie H., Cui Z., Wang L., Xia Z., Hu Y., Xian L., Li C., Xie L., Crane J., Wan M., Zhen G., Bian Q., Yu B., Chang W., Qiu T., Pickarski M., Duong le T., Windle J.J., Luo X., Liao E., Cao X. PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis. Nat. Med. 2014, 20:1270-1278.
31. Deckers M.M., van Bezooijen R.L., van der Horst G., Hoogendam J., van Der Bent C., Papapoulos S.E., Lowik C.W. Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 2002, 143:1545-1553.
32. Fei Y., Gronowicz G., Hurley M.M. Fibroblast growth factor-2, bone homeostasis and fracture repair. Curr. Pharm. Des. 2013, 19:3354-3363.
33. Maes C., Coenegrachts L., Stockmans I., Daci E., Luttun A., Petryk A., Gopalakrishnan R., Moermans K., Smets N., Verfaillie C.M., Carmeliet P., Bouillon R., Carmeliet G. Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J. Clin. Invest. 2006, 116:1230-1242.
34. Street J., Bao M., deGuzman L., Bunting S., Peale F.V., Ferrara N., Steinmetz H., Hoeffel J., Cleland J.L., Daugherty A., van Bruggen N., Redmond H.P., Carano R.A., Filvaroff E.H. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:9656-9661.
35. Keramaris N.C., Calori G.M., Nikolaou V.S., Schemitsch E.H., Giannoudis P.V. Fracture vascularity and bone healing: a systematic review of the role of VEGF. Injury 2008, 39(Suppl. 2):S45-S57.
36. Gerstenfeld L.C., Cullinane D.M., Barnes G.L., Graves D.T., Einhorn T.A. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J. Cell. Biochem. 2003, 88:873-884.
37. Uchida S., Sakai A., Kudo H., Otomo H., Watanuki M., Tanaka M., Nagashima M., Nakamura T. Vascular endothelial growth factor is expressed along with its receptors during the healing process of bone and bone marrow after drill-hole injury in rats. Bone 2003, 32:491-501.
38. Cramer T., Schipani E., Johnson R.S., Swoboda B., Pfander D. Expression of VEGF isoforms by epiphyseal chondrocytes during low-oxygen tension is HIF-1 alpha dependent. Osteoarthritis Cartilage 2004, 12:433-439.
39. Wang Y., Wan C., Deng L., Liu X., Cao X., Gilbert S.R., Bouxsein M.L., Faugere M.C., Guldberg R.E., Gerstenfeld L.C., Haase V.H., Johnson R.S., Schipani E., Clemens T.L. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J. Clin. Invest. 2007, 117:1616-1626.
40. Peng H., Wright V., Usas A., Gearhart B., Shen H.C., Cummins J., Huard J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J. Clin. Invest. 2002, 110:751-759.
41. Du X., Xie Y., Xian C.J., Chen L. Role of FGFs/FGFRs in skeletal development and bone regeneration. J. Cell. Physiol. 2012, 227:3731-3743.
42. Malizos K.N., Papatheodorou L.K. The healing potential of the periosteum molecular aspects. Injury 2005, 36(Suppl. 3):S13-S19.
43. Noth U., Osyczka A.M., Tuli R., Hickok N.J., Danielson K.G., Tuan R.S. Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J. Orthop. Res. 2002, 20:1060-1069.
44. Song L., Young N.J., Webb N.E., Tuan R.S. Origin and characterization of multipotential mesenchymal stem cells derived from adult human trabecular bone. Stem Cells Dev. 2005, 14:712-721.
45. Colnot C., Huang S., Helms J. Analyzing the cellular contribution of bone marrow to fracture healing using bone marrow transplantation in mice. Biochem. Biophys. Res. Commun. 2006, 350:557-561.
46. Eghbali-Fatourechi G.Z., Lamsam J., Fraser D., Nagel D., Riggs B.L., Khosla S. Circulating osteoblast-lineage cells in humans. N. Engl. J. Med. 2005, 352:1959-1966.
47. Kitaori T., Ito H., Schwarz E.M., Tsutsumi R., Yoshitomi H., Oishi S., Nakano M., Fujii N., Nagasawa T., Nakamura T. Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum. 2009, 60:813-823.
48. Ma J., Ge J., Zhang S., Sun A., Shen J., Chen L., Wang K., Zou Y. Time course of myocardial stromal cell-derived factor 1 expression and beneficial effects of intravenously administered bone marrow stem cells in rats with experimental myocardial infarction. Basic Res. Cardiol. 2005, 100:217-223.
49. Ceradini D.J., Kulkarni A.R., Callaghan M.J., Tepper O.M., Bastidas N., Kleinman M.E., Capla J.M., Galiano R.D., Levine J.P., Gurtner G.C. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 2004, 10:858-864.
50. Mackie E.J., Ahmed Y.A., Tatarczuch L., Chen K.S., Mirams M. Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int. J. Biochem. Cell Biol. 2008, 40:46-62.
51. Yu Y.Y., Lieu S., Lu C., Miclau T., Marcucio R.S., Colnot C. Immunolocalization of BMPs, BMP antagonists, receptors, and effectors during fracture repair. Bone 2010, 46:841-851.
52. Tsuji K., Cox K., Gamer L., Graf D., Economides A., Rosen V. Conditional deletion of BMP7 from the limb skeleton does not affect bone formation or fracture repair. J. Orthop. Res. 2010, 28:384-389.
53. Sampath T.K., Maliakal J.C., Hauschka P.V., Jones W.K., Sasak H., Tucker R.F., White K.H., Coughlin J.E., Tucker M.M., Pang R.H., et al. Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation in vitro. J. Biol. Chem. 1992, 267:20352-20362.
54. Tsuji K., Bandyopadhyay A., Harfe B.D., Cox K., Kakar S., Gerstenfeld L., Einhorn T., Tabin C.J., Rosen V. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat. Genet. 2006, 38:1424-1429.
55. Edgar C.M., Chakravarthy V., Barnes G., Kakar S., Gerstenfeld L.C., Einhorn T.A. Autogenous regulation of a network of bone morphogenetic proteins (BMPs) mediates the osteogenic differentiation in murine marrow stromal cells. Bone 2007, 40:1389-1398.
56. Long F. Building strong bones: molecular regulation of the osteoblast lineage. Nat. Rev. Mol. Cell Biol. 2012, 13:27-38.
57. Minear S., Leucht P., Jiang J., Liu B., Zeng A., Fuerer C., Nusse R., Helms J.A. Wnt proteins promote bone regeneration. Sci. Transl. Med. 2010, 2:29ra30.
58. Chen Y., Alman B.A. Wnt pathway, an essential role in bone regeneration. J. Cell. Biochem. 2009, 106:353-362.
59. Baron R., Kneissel M. WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat. Med. 2013, 19:179-192.
60. Crockett J.C., Rogers M.J., Coxon F.P., Hocking L.J., Helfrich M.H. Bone remodelling at a glance. J. Cell Sci. 2011, 124:991-998.
61. Lissenberg-Thunnissen S.N., de Gorter D.J., Sier C.F., Schipper I.B. Use and efficacy of bone morphogenetic proteins in fracture healing. Int. Orthop. 2011, 35:1271-1280.
62. Hollinger J.O., Hart C.E., Hirsch S.N., Lynch S., Friedlaender G.E. Recombinant human platelet-derived growth factor: biology and clinical applications. J. Bone Joint Surg. Am. Vol. 2008, 90(Suppl. 1):48-54.
63. Kempen D.H., Creemers L.B., Alblas J., Lu L., Verbout A.J., Yaszemski M.J., Dhert W.J. Growth factor interactions in bone regeneration. Tissue Eng. B Rev. 2010, 16:551-566.
64. Lieberman J.R., Daluiski A., Einhorn T.A. The role of growth factors in the repair of bone. Biology and clinical applications. J. Bone Joint Surg. Am. Vol. 2002, 84-A:1032-1044.
65. Wozney J.M. The bone morphogenetic protein family and osteogenesis. Mol. Reprod. Dev. 1992, 32:160-167.
66. Seeherman H., Wozney J.M. Delivery of bone morphogenetic proteins for orthopedic tissue regeneration. Cytokine Growth Factor Rev. 2005, 16:329-345.
67. Calori G.M., Tagliabue L., Gala L., d'Imporzano M., Peretti G., Albisetti W. Application of rhBMP-7 and platelet-rich plasma in the treatment of long bone non-unions: a prospective randomised clinical study on 120 patients. Injury 2008, 39:1391-1402.
68. Friedlaender G.E., Perry C.R., Cole J.D., Cook S.D., Cierny G., Muschler G.F., Zych G.A., Calhoun J.H., LaForte A.J., Yin S. Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J. Bone Joint Surg. Am. Vol. 2001, 83-A(Suppl. 1):S151-S158.
69. Giannoudis P.V., Tzioupis C. Clinical applications of BMP-7: the UK perspective. Injury 2005, 36(Suppl. 3):S47-S50.
70. 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., BMP-2 Evaluation in Surgery for Tibial Trauma (BESTT) Study Group Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients. J. Bone Joint Surg. Am. Vol. 2002, 84-A:2123-2134.
71. Katayama Y., Matsuyama Y., Yoshihara H., Sakai Y., Nakamura H., Imagama S., Ito Z., Wakao N., Kamiya M., Yukawa Y., Kanemura T., Sato K., Iwata H., Ishiguro N. Clinical and radiographic outcomes of posterolateral lumbar spine fusion in humans using recombinant human bone morphogenetic protein-2: an average five-year follow-up study. Int. Orthop. 2009, 33:1061-1067.
72. McKay W.F., Peckham S.M., Badura J.M. A comprehensive clinical review of recombinant human bone morphogenetic protein-2 (INFUSE Bone Graft). Int. Orthop. 2007, 31:729-734.
73. White A.P., Vaccaro A.R., Hall J.A., Whang P.G., Friel B.C., McKee M.D. Clinical applications of BMP-7/OP-1 in fractures, nonunions and spinal fusion. Int. Orthop. 2007, 31:735-741.
74. Epstein N.E. Complications due to the use of BMP/INFUSE in spine surgery: The evidence continues to mount. Surg. Neurol. Int. 2013, 4:S343-S352.
75. Mayr-Wohlfart U., Waltenberger J., Hausser H., Kessler S., Gunther K.P., Dehio C., Puhl W., Brenner R.E. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 2002, 30:472-477.
76. Orlandini M., Spreafico A., Bardelli M., Rocchigiani M., Salameh A., Nucciotti S., Capperucci C., Frediani B., Oliviero S. Vascular endothelial growth factor-D activates VEGFR-3 expressed in osteoblasts inducing their differentiation. J. Biol. Chem. 2006, 281:17961-17967.
77. Eckardt H., Ding M., Lind M., Hansen E.S., Christensen K.S., Hvid I. Recombinant human vascular endothelial growth factor enhances bone healing in an experimental nonunion model. J. Bone Joint Surg. Br. Vol. 2005, 87:1434-1438.
78. Leach J.K., Kaigler D., Wang Z., Krebsbach P.H., Mooney D.J. Coating of VEGF-releasing scaffolds with bioactive glass for angiogenesis and bone regeneration. Biomaterials 2006, 27:3249-3255.
79. Kaigler D., Silva E.A., Mooney D.J. Guided bone regeneration using injectable vascular endothelial growth factor delivery gel. J. Periodontol. 2013, 84:230-238.
80. Young S., Patel Z.S., Kretlow J.D., Murphy M.B., Mountziaris P.M., Baggett L.S., Ueda H., Tabata Y., Jansen J.A., Wong M., Mikos A.G. Dose effect of dual delivery of vascular endothelial growth factor and bone morphogenetic protein-2 on bone regeneration in a rat critical-size defect model. Tissue Eng. A 2009, 15:2347-2362.
81. Patel Z.S., Young S., Tabata Y., Jansen J.A., Wong M.E., Mikos A.G. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 2008, 43:931-940.
82. Andrae J., Gallini R., Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 2008, 22:1276-1312.
83. Caplan A.I., Correa D. PDGF in bone formation and regeneration: new insights into a novel mechanism involving MSCs. J. Orthop. Res. 2011, 29:1795-1803.
84. Hollinger J.O., Onikepe A.O., MacKrell J., Einhorn T., Bradica G., Lynch S., Hart C.E. Accelerated fracture healing in the geriatric, osteoporotic rat with recombinant human platelet-derived growth factor-BB and an injectable beta-tricalcium phosphate/collagen matrix. J. Orthop. Res. 2008, 26:83-90.
85. Nash T.J., Howlett C.R., Martin C., Steele J., Johnson K.A., Hicklin D.J. Effect of platelet-derived growth factor on tibial osteotomies in rabbits. Bone 1994, 15:203-208.
86. Kaipel M., Schutzenberger S., Schultz A., Ferguson J., Slezak P., Morton T.J., Van Griensven M., Redl H. BMP-2 but not VEGF or PDGF in fibrin matrix supports bone healing in a delayed-union rat model. J. Orthop. Res. 2012, 30:1563-1569.
87. Kubota K., Sakikawa C., Katsumata M., Nakamura T., Wakabayashi K. Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor. J. Bone Miner. Res. 2002, 17:257-265.
88. Marden L.J., Fan R.S., Pierce G.F., Reddi A.H., Hollinger J.O. Platelet-derived growth factor inhibits bone regeneration induced by osteogenin, a bone morphogenetic protein, in rat craniotomy defects. J. Clin. Invest. 1993, 92:2897-2905.
89. Ranly D.M., McMillan J., Keller T., Lohmann C.H., Meunch T., Cochran D.L., Schwartz Z., Boyan B.D. Platelet-derived growth factor inhibits demineralized bone matrix-induced intramuscular cartilage and bone formation. A study of immunocompromised mice. J. Bone Joint Surg. Am. Vol. 2005, 87:2052-2064.
90. Friedlaender G.E., Lin S., Solchaga L.A., Snel L.B., Lynch S.E. The role of recombinant human platelet-derived growth factor-BB (rhPDGF-BB) in orthopaedic bone repair and regeneration. Curr. Pharm. Des. 2013, 19:3384-3390.
91. Schmid G.J., Kobayashi C., Sandell L.J., Ornitz D.M. Fibroblast growth factor expression during skeletal fracture healing in mice. Dev. Dyn. 2009, 238:766-774.
92. Nakamura T., Hara Y., Tagawa M., Tamura M., Yuge T., Fukuda H., Nigi H. Recombinant human basic fibroblast growth factor accelerates fracture healing by enhancing callus remodeling in experimental dog tibial fracture. J. Bone Miner. Res. 1998, 13:942-949.
93. Radomsky M.L., Aufdemorte T.B., Swain L.D., Fox W.C., Spiro R.C., Poser J.W. Novel formulation of fibroblast growth factor-2 in a hyaluronan gel accelerates fracture healing in nonhuman primates. J. Orthop. Res. 1999, 17:607-614.
94. Pun S., Florio C.L., Wronski T.J. Anabolic effects of basic fibroblast growth factor in the tibial diaphysis of ovariectomized rats. Bone 2000, 27:197-202.
95. Tabata Y., Yamada K., Miyamoto S., Nagata I., Kikuchi H., Aoyama I., Tamura M., Ikada Y. Bone regeneration by basic fibroblast growth factor complexed with biodegradable hydrogels. Biomaterials 1998, 19:807-815.
96. Kawaguchi H., Jingushi S., Izumi T., Fukunaga M., Matsushita T., Nakamura T., Mizuno K., Nakamura T., Nakamura K. Local application of recombinant human fibroblast growth factor-2 on bone repair: a dose-escalation prospective trial on patients with osteotomy. J. Orthop. Res. 2007, 25:480-487.
97. Kawaguchi H., Oka H., Jingushi S., Izumi T., Fukunaga M., Sato K., Matsushita T., Nakamura K., Group T. A local application of recombinant human fibroblast growth factor 2 for tibial shaft fractures: A randomized, placebo-controlled trial. J. Bone Miner. Res. 2010, 25:2735-2743.
98. Kitamura M., Nakashima K., Kowashi Y., Fujii T., Shimauchi H., Sasano T., Furuuchi T., Fukuda M., Noguchi T., Shibutani T., Iwayama Y., Takashiba S., Kurihara H., Ninomiya M., Kido J., Nagata T., Hamachi T., Maeda K., Hara Y., Izumi Y., Hirofuji T., Imai E., Omae M., Watanuki M., Murakami S. Periodontal tissue regeneration using fibroblast growth factor-2: randomized controlled phase II clinical trial. PLoS One 2008, 3:e2611.
99. Bland Y.S., Critchlow M.A., Ashhurst D.E. Exogenous fibroblast growth factors-1 and -2 do not accelerate fracture healing in the rabbit. Acta Orthop. Scand. 1995, 66:543-548.
100. Nakajima F., Ogasawara A., Goto K., Moriya H., Ninomiya Y., Einhorn T.A., Yamazaki M. Spatial and temporal gene expression in chondrogenesis during fracture healing and the effects of basic fibroblast growth factor. J. Orthop. Res. 2001, 19:935-944.
101. Nakajima F., Nakajima A., Ogasawara A., Moriya H., Yamazaki M. Effects of a single percutaneous injection of basic fibroblast growth factor on the healing of a closed femoral shaft fracture in the rat. Calcif. Tissue Int. 2007, 81:132-138.
102. Kimoto T., Hosokawa R., Kubo T., Maeda M., Sano A., Akagawa Y. Continuous administration of basic fibroblast growth factor (FGF-2) accelerates bone induction on rat calvaria - an application of a new drug delivery system. J. Dent. Res. 1998, 77:1965-1969.
103. Nakamura Y., Tensho K., Nakaya H., Nawata M., Okabe T., Wakitani S. Low dose fibroblast growth factor-2 (FGF-2) enhances bone morphogenetic protein-2 (BMP-2)-induced ectopic bone formation in mice. Bone 2005, 36:399-407.
104. Sakano S., Hasegawa Y., Murata Y., Ito T., Genda E., Iwata H., Ishiguro N., Seo H. Inhibitory effect of bFGF on endochondral heterotopic ossification. Biochem. Biophys. Res. Commun. 2002, 293:680-685.
105. Zellin G., Linde A. Effects of recombinant human fibroblast growth factor-2 on osteogenic cell populations during orthopic osteogenesis in vivo. Bone 2000, 26:161-168.
106. Woo E.J. Recombinant human bone morphogenetic protein-2: adverse events reported to the Manufacturer and User Facility Device Experience database. Spine J. 2012, 12:894-899.
107. Grabowski G., Cornett C.A. Bone graft and bone graft substitutes in spine surgery: current concepts and controversies. J. Am. Acad. Orthop. Surg. 2013, 21:51-60.
108. 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.
109. Carragee E.J., Chu G., Rohatgi R., Hurwitz E.L., Weiner B.K., Yoon S.T., Comer G., Kopjar B. Cancer risk after use of recombinant bone morphogenetic protein-2 for spinal arthrodesis. J. Bone Joint Surg. Am. Vol. 2013, 95:1537-1545.
110. Devine J.G., Dettori J.R., France J.C., Brodt E., McGuire R.A. The use of rhBMP in spine surgery: is there a cancer risk?. Evid. Based Spine Care J. 2012, 3:35-41.
111. Simons M., Ware J.A. Therapeutic angiogenesis in cardiovascular disease. Nat. Rev. Drug Discov. 2003, 2:863-871.
112. Dahabreh Z., Calori G.M., Kanakaris N.K., Nikolaou V.S., Giannoudis P.V. A cost analysis of treatment of tibial fracture nonunion by bone grafting or bone morphogenetic protein-7. Int. Orthop. 2009, 33:1407-1414.
113. Garrison K.R., Donell S., Ryder J., Shemilt I., Mugford M., Harvey I., Song F. Clinical effectiveness and cost-effectiveness of bone morphogenetic proteins in the non-healing of fractures and spinal fusion: a systematic review. Health Technol. Assess. 2007, 11:1-150. (iii-iv).
114. Bishop G.B., Einhorn T.A. Current and future clinical applications of bone morphogenetic proteins in orthopaedic trauma surgery. Int. Orthop. 2007, 31:721-727.
115. Lee K., Silva E.A., Mooney D.J. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J. R. Soc. Interface 2011, 8:153-170.
116. Rice J.J., Martino M.M., De Laporte L., Tortelli F., Briquez P.S., Hubbell J.A. Engineering the regenerative microenvironment with biomaterials. Adv. Healthc. Mater. 2013, 2:57-71.
117. Vo T.N., Kasper F.K., Mikos A.G. Strategies for controlled delivery of growth factors and cells for bone regeneration. Adv. Drug Deliv. Rev. 2012, 64:1292-1309.
118. Humphries J.D., Byron A., Humphries M.J. Integrin ligands at a glance. J. Cell Sci. 2006, 119:3901-3903.
119. Schonherr E., Hausser H.J. Extracellular matrix and cytokines: a functional unit. Dev. Immunol. 2000, 7:89-101.
120. Schultz G.S., Wysocki A. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen. 2009, 17:153-162.
121. Capila I., Linhardt R.J. Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 2002, 41:391-412.
122. Macri L., Silverstein D., Clark R.A. Growth factor binding to the pericellular matrix and its importance in tissue engineering. Adv. Drug Deliv. Rev. 2007, 59:1366-1381.
123. Martino M.M., Hubbell J.A. The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J. 2010, 24:4711-4721.
124. Martino M.M., Briquez P.S., Ranga A., Lutolf M.P., Hubbell J.A. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4563-4568.
125. De Laporte L., Rice J.J., Tortelli F., Hubbell J.A. Tenascin C promiscuously binds growth factors via its fifth fibronectin type III-like domain. PLoS One 2013, 8:e62076.
126. Upton Z., Cuttle L., Noble A., Kempf M., Topping G., Malda J., Xie Y., Mill J., Harkin D.G., Kravchuk O., Leavesley D.I., Kimble R.M. Vitronectin: growth factor complexes hold potential as a wound therapy approach. J. Invest. Dermatol. 2008, 128:1535-1544.
127. Martino M.M., Briquez P.S., Guc E., Tortelli F., Kilarski W.W., Metzger S., Rice J.J., Kuhn G.A., Muller R., Swartz M.A., Hubbell J.A. Growth factors engineered for super-affinity to the extracellular matrix enhance tissue healing. Science 2014, 343:885-888.
128. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219.
129. Schultz G.S., Davidson J.M., Kirsner R.S., Bornstein P., Herman I.M. Dynamic reciprocity in the wound microenvironment. Wound Repair Regen. 2011, 19:134-148.
130. Giancotti F.G., Tarone G. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu. Rev. Cell Dev. Biol. 2003, 19:173-206.
131. Kim S.H., Turnbull J., Guimond S. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J. Endocrinol. 2011, 209:139-151.
132. Zhu J., Clark R.A. Fibronectin at select sites binds multiple growth factors and enhances their activity: expansion of the collaborative ECM-GF paradigm. J. Invest. Dermatol. 2014, 134:895-901.
133. Meinel L., Kaplan D.L. Silk constructs for delivery of musculoskeletal therapeutics. Adv. Drug Deliv. Rev. 2012, 64:1111-1122.
134. Yamamoto M., Takahashi Y., Tabata Y. Enhanced bone regeneration at a segmental bone defect by controlled release of bone morphogenetic protein-2 from a biodegradable hydrogel. Tissue Eng. 2006, 12:1305-1311.
135. Furuya H., Tabata Y., Kaneko K. Bone regeneration for murine femur fracture by gelatin hydrogels incorporating basic fibroblast growth factor with different release profiles. Tissue Eng. A 2014, 20:1531-1541.
136. Takahashi Y., Yamamoto M., Tabata Y. Enhanced osteoinduction by controlled release of bone morphogenetic protein-2 from biodegradable sponge composed of gelatin and beta-tricalcium phosphate. Biomaterials 2005, 26:4856-4865.
137. Takahashi Y., Yamamoto M., Yamada K., Kawakami O., Tabata Y. Skull bone regeneration in nonhuman primates by controlled release of bone morphogenetic protein-2 from a biodegradable hydrogel. Tissue Eng. 2007, 13:293-300.
138. Kawaguchi H., Nakamura K., Tabata Y., Ikada Y., Aoyama I., Anzai J., Nakamura T., Hiyama Y., Tamura M. Acceleration of fracture healing in nonhuman primates by fibroblast growth factor-2. J. Clin. Endocrinol. Metab. 2001, 86:875-880.
139. Macri L., Clark R.A. Tissue engineering for cutaneous wounds: selecting the proper time and space for growth factors, cells and the extracellular matrix. Skin Pharmacol Physiol 2009, 22:83-93.
140. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
141. Chung Y.I., Ahn K.M., Jeon S.H., Lee S.Y., Lee J.H., Tae G. Enhanced bone regeneration with BMP-2 loaded functional nanoparticle-hydrogel complex. J. Control. Release 2007, 121:91-99.
142. Koo K.H., Lee J.M., Ahn J.M., Kim B.S., La W.G., Kim C.S., Im G.I. Controlled delivery of low-dose bone morphogenetic protein-2 using heparin-conjugated fibrin in the posterolateral lumbar fusion of rabbits. Artif. Organs 2013, 37:487-494.
143. Lee S.S., Huang B.J., Kaltz S.R., Sur S., Newcomb C.J., Stock S.R., Shah R.N., Stupp S.I. Bone regeneration with low dose BMP-2 amplified by biomimetic supramolecular nanofibers within collagen scaffolds. Biomaterials 2013, 34:452-459.
144. Yang H.S., La W.G., Cho Y.M., Shin W., Yeo G.D., Kim B.S. Comparison between heparin-conjugated fibrin and collagen sponge as bone morphogenetic protein-2 carriers for bone regeneration. Exp. Mol. Med. 2012, 44:350-355.
145. Zhao B., Katagiri T., Toyoda H., Takada T., Yanai T., Fukuda T., Chung U.I., Koike T., Takaoka K., Kamijo R. Heparin potentiates the in vivo ectopic bone formation induced by bone morphogenetic protein-2. J. Biol. Chem. 2006, 281:23246-23253.
146. Sakiyama-Elbert S.E. Incorporation of heparin into biomaterials. Acta Biomater. 2014, 10:1581-1587.
147. Yang H.S., La W.G., Bhang S.H., Jeon J.Y., Lee J.H., Kim B.S. Heparin-conjugated fibrin as an injectable system for sustained delivery of bone morphogenetic protein-2. Tissue Eng. A 2010, 16:1225-1233.
148. Lin F., Ren X.D., Pan Z., Macri L., Zong W.X., Tonnesen M.G., Rafailovich M., Bar-Sagi D., Clark R.A. Fibronectin growth factor-binding domains are required for fibroblast survival. J. Invest. Dermatol. 2011, 131:84-98.
149. Wijelath E.S., Rahman S., Namekata M., Murray J., Nishimura T., Mostafavi-Pour Z., Patel Y., Suda Y., Humphries M.J., Sobel M. Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain: enhancement of VEGF biological activity by a singular growth factor/matrix protein synergism. Circ. Res. 2006, 99:853-860.
150. Upton Z., Wallace H.J., Shooter G.K., van Lonkhuyzen D.R., Yeoh-Ellerton S., Rayment E.A., Fleming J.M., Broszczak D., Queen D., Sibbald R.G., Leavesley D.I., Stacey M.C. Human pilot studies reveal the potential of a vitronectin: growth factor complex as a treatment for chronic wounds. Int. Wound J. 2011, 8:522-532.
151. Alam N., Goel H.L., Zarif M.J., Butterfield J.E., Perkins H.M., Sansoucy B.G., Sawyer T.K., Languino L.R. The integrin-growth factor receptor duet. J. Cell. Physiol. 2007, 213:649-653.
152. Comoglio P.M., Boccaccio C., Trusolino L. Interactions between growth factor receptors and adhesion molecules: breaking the rules. Curr. Opin. Cell Biol. 2003, 15:565-571.
153. Kisiel M., Martino M.M., Ventura M., Hubbell J.A., Hilborn J., Ossipov D.A. Improving the osteogenic potential of BMP-2 with hyaluronic acid hydrogel modified with integrin-specific fibronectin fragment. Biomaterials 2013, 34:704-712.
154. Martino M.M., Tortelli F., Mochizuki M., Traub S., Ben-David D., Kuhn G.A., Müller R., Livne E., Eming S.A., Hubbell J.A. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci. Transl. Med. 2011, 3:100ra189.
155. Shekaran A., Garcia J.R., Clark A.Y., Kavanaugh T.E., Lin A.S., Guldberg R.E., Garcia A.J. Bone regeneration using an alpha 2 beta 1 integrin-specific hydrogel as a BMP-2 delivery vehicle. Biomaterials 2014, 35:5453-5461.
156. Schense J.C., Hubbell J.A. Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug. Chem. 1999, 10:75-81.
157. Schmoekel H.G., Weber F.E., Schense J.C., Gratz K.W., Schawalder P., Hubbell J.A. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol. Bioeng. 2005, 89:253-262.
158. Ehrbar M., Djonov V.G., Schnell C., Tschanz S.A., Martiny-Baron G., Schenk U., Wood J., Burri P.H., Hubbell J.A., Zisch A.H. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ. Res. 2004, 94:1124-1132.
159. Traub S., Morgner J., Martino M.M., Honing S., Swartz M.A., Wickstrom S.A., Hubbell J.A., Eming S.A. The promotion of endothelial cell attachment and spreading using FNIII10 fused to VEGF-A165. Biomaterials 2013, 34:5958-5968.
160. Arrighi I., Mark S., Alvisi M., von Rechenberg B., Hubbell J.A., Schense J.C. Bone healing induced by local delivery of an engineered parathyroid hormone prodrug. Biomaterials 2009, 30:1763-1771.
161. Chen B., Lin H., Wang J., Zhao Y., Wang B., Zhao W., Sun W., Dai J. Homogeneous osteogenesis and bone regeneration by demineralized bone matrix loading with collagen-targeting bone morphogenetic protein-2. Biomaterials 2007, 28:1027-1035.
162. Han X., Zhang W., Gu J., Zhao H., Ni L., Han J., Zhou Y., Gu Y., Zhu X., Sun J., Hou X., Yang H., Dai J., Shi Q. Accelerated postero-lateral spinal fusion by collagen scaffolds modified with engineered collagen-binding human bone morphogenetic protein-2 in rats. PLoS One 2014, 9:e98480.
163. Tokunou T., Miller R., Patwari P., Davis M.E., Segers V.F., Grodzinsky A.J., Lee R.T. Engineering insulin-like growth factor-1 for local delivery. FASEB J. 2008, 22:1886-1893.
164. Kim Y.H., Furuya H., Tabata Y. Enhancement of bone regeneration by dual release of a macrophage recruitment agent and platelet-rich plasma from gelatin hydrogels. Biomaterials 2014, 35:214-224.
165. Chang J., Liu F., Lee M., Wu B., Ting K., Zara J.N., Soo C., Al Hezaimi K., Zou W., Chen X., Mooney D.J., Wang C.Y. NF-kappaB inhibits osteogenic differentiation of mesenchymal stem cells by promoting beta-catenin degradation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:9469-9474.
166. Ratanavaraporn J., Furuya H., Tabata Y. Local suppression of pro-inflammatory cytokines and the effects in BMP-2-induced bone regeneration. Biomaterials 2012, 33:304-316.
167. Thomas M.V., Puleo D.A. Infection, inflammation, and bone regeneration: a paradoxical relationship. J. Dent. Res. 2011, 90:1052-1061.