Emulating native periosteum cell population and subsequent paracrine factor production to promote tissue engineered periosteum-mediated allograft healing

Biomaterials

Volumn 52, Issue 1, 2015, Pages 426-440

  Hoffman, Michael D ^a,b   Benoit, Danielle S W ^a,b  

^a University of Rochester   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Bone allografts; Cell transplantation; Hydrogels; Mesenchymal stem cells; Periosteum; Poly(ethylene glycol)

Indexed keywords

BONE; CELL ENGINEERING; CELL PROLIFERATION; CELLS; CYTOLOGY; ENDOTHELIAL CELLS; FLOWCHARTING; GRAFTS; HYDROGELS; INTEGRATION; POLYETHYLENE GLYCOLS; POLYOLS; STEM CELLS; TISSUE;

BONE ALLOGRAFTS; BONE MORPHOGENETIC PROTEIN-2; CELL TRANSPLANTATION; CLINICAL APPLICATION; MESENCHYMAL STEM CELL; OSTEOPROGENITOR CELLS; PERIOSTEUM; VASCULAR ENDOTHELIAL GROWTH FACTOR;

CELL CULTURE;

BONE MORPHOGENETIC PROTEIN 2; MACROGOL; VASCULOTROPIN; BMP2 PROTEIN, MOUSE; HYDROGEL; MACROGOL DERIVATIVE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE ALLOGRAFT; CALLUS; CELL POPULATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HYDROGEL; IN VIVO STUDY; LASER CAPTURE MICRODISSECTION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSSIFICATION; OSTEOPROGENITOR CELL; PERIOSTEUM; PRIORITY JOURNAL; TISSUE ENGINEERING; TISSUE REGENERATION; ANIMAL; BAGG ALBINO MOUSE; BIOMECHANICS; BONE DEVELOPMENT; BONE TRANSPLANTATION; C57BL MOUSE; CHEMISTRY; CYTOLOGY; FEMUR; GRAFT SURVIVAL; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PROCEDURES; TRANSPLANTATION; WOUND HEALING;

ANIMALS; BIOMECHANICAL PHENOMENA; BONE MORPHOGENETIC PROTEIN 2; BONE TRANSPLANTATION; FEMALE; FEMUR; GRAFT SURVIVAL; HYDROGELS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OSTEOGENESIS; PERIOSTEUM; POLYETHYLENE GLYCOLS; TISSUE ENGINEERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 84932628240     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.064     Document Type: Article

References (89)

1. Malizos K.N., Papatheodorou L.K. The healing potential of the periosteum molecular aspects. Injury 2005, 36(Suppl.3):S13-S19.
2. Dwek J.R. The periosteum: what is it, where is it, and what mimics it in its absence?. Skelet Radiol 2010, 39(4):319-323.
3. Ham A.W. Ahistological study of the early phases of bone repair. JBone Jt Surg 1930, 12:827-844.
4. Hoffman M.D., Benoit D.S. Emerging ideas: engineering the periosteum: revitalizing allografts by mimicking autograft healing. Clin Orthop Relat Res 2013, 471(3):721-726.
5. Hutmacher D.W., Sittinger M. Periosteal cells in bone tissue engineering. Tissue Eng 2003, 9(Suppl.1):S45-S64.
6. Squier C.A., Ghoneim S., Kremenak C.R. Ultrastructure of the periosteum from membrane bone. JAnat 1990, 171:233-239.
7. Ellender G., Feik S.A., Carach B.J. Periosteal structure and development in a rat caudal vertebra. JAnat 1988, 158:173-187.
8. Gnecchi M., Zhang Z., Ni A., Dzau V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008, 103(11):1204-1219.
9. Chen L., Tredget E.E., Wu P.Y., Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3(4):e1886.
10. Zhang X., Xie C., Lin A.S., Ito H., Awad H., Lieberman J.R., et al. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. JBone Miner Res 2005, 20(12):2124-2137.
11. Xie C., Reynolds D., Awad H., Rubery P.T., Pelled G., Gazit D., et al. Structural bone allograft combined with genetically engineered mesenchymal stem cells as a novel platform for bone tissue engineering. Tissue Eng 2007, 13(3):435-445.
12. Hoffman M.D., Xie C., Zhang X., Benoit D.S. The effect of mesenchymal stem cells delivered via hydrogel-based tissue engineered periosteum on bone allograft healing. Biomaterials 2013, 34(35):8887-8898.
13. Devescovi V., Leonardi E., Ciapetti G., Cenni E. Growth factors in bone repair. Chir Organi Mov 2008, 92(3):161-168.
14. Burchardt H. The biology of bone graft repair. Clin Orthop Relat Res 1983, 174:28-42.
15. Burchardt H., Enneking W.F. Transplantation of bone. Surg Clin N Am 1978, 58(2):403-427.
16. Burchardt H., Jones H., Glowczewskie F., Rudner C., Enneking W.F. Freeze-dried allogeneic segmental cortical-bone grafts in dogs. JBone Jt Surg Am 1978, 60(8):1082-1090.
17. Stevenson S., Shaffer J.W., Goldberg V.M. The humoral response to vascular and nonvascular allografts of bone. Clin Orthop Relat Res 1996, 326:86-95.
18. Stevenson S., Li X.Q., Davy D.T., Klein L., Goldberg V.M. Critical biological determinants of incorporation of non-vascularized cortical bone grafts. Quantification of a complex process and structure. JBone Jt Surg Am 1997, 79(1):1-16.
19. Mankin H.J., Gebhardt M.C., Jennings L.C., Springfield D.S., Tomford W.W. Long-term results of allograft replacement in the management of bone tumors. Clin Orthop Relat Res 1996, 324:86-97.
20. Granero-Molto F., Weis J.A., Miga M.I., Landis B., Myers T.J., O'Rear L., et al. Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells 2009, 27(8):1887-1898.
21. Bielby R., Jones E., McGonagle D. The role of mesenchymal stem cells in maintenance and repair of bone. Injury 2007, 38(Suppl.1):S26-S32.
22. Chappuis V., Gamer L., Cox K., Lowery J.W., Bosshardt D.D., Rosen V. Periosteal BMP2 activity drives bone graft healing. Bone 2012, 51(4):800-809.
23. Derner R., Anderson A.C. The bone morphogenic protein. Clin Podiatr Med Surg 2005, 22(4):607-618. vii.
24. Mattar T., Friedrich P.F., Bishop A.T. Effect of rhBMP-2 and VEGF in a vascularized bone allotransplant experimental model based on surgical neoangiogenesis. JOrthop Res 2013, 31(4):561-566.
25. Deckers M.M., van Bezooijen R.L., van der Horst G., Hoogendam J., van Der Bent C., Papapoulos S.E., et al. Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 2002, 143(4):1545-1553.
26. Kempen D.H., Creemers L.B., Alblas J., Lu L., Verbout A.J., Yaszemski M.J., et al. Growth factor interactions in bone regeneration. Tissue Eng Part B Rev 2010, 16(6):551-566.
27. Bostrom M.P., Lane J.M., Berberian W.S., Missri A.A., Tomin E., Weiland A., et al. Immunolocalization and expression of bone morphogenetic proteins 2 and 4 in fracture healing. JOrthop Res 1995, 13(3):357-367.
28. Hanada K., Solchaga L.A., Caplan A.I., Hering T.M., Goldberg V.M., Yoo J.U., et al. BMP-2 induction and TGF-beta 1 modulation of rat periosteal cell chondrogenesis. JCell Biochem 2001, 81(2):284-294.
29. Bouletreau P.J., Warren S.M., Spector J.A., Peled Z.M., Gerrets R.P., Greenwald J.A., et al. Hypoxia and VEGF up-regulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plast Reconstr Surg 2002, 109(7):2384-2397.
30. Mayr-Wohlfart U., Waltenberger J., Hausser H., Kessler S., Gunther K.P., Dehio C., et al. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 2002, 30(3):472-477.
31. Fiedler J., Leucht F., Waltenberger J., Dehio C., Brenner R.E. VEGF-A and PlGF-1 stimulate chemotactic migration of human mesenchymal progenitor cells. Biochem Biophys Res Commun 2005, 334(2):561-568.
32. Ito H., Koefoed M., Tiyapatanaputi P., Gromov K., Goater J.J., Carmouche J., et al. Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nat Med 2005, 11(3):291-297.
33. Ma D., Yao H., Tian W., Chen F., Liu Y., Mao T., et al. Enhancing bone formation by transplantation of a scaffold-free tissue-engineered periosteum in a rabbit model. Clin Oral Implants Res 2011, 22(10):1193-1199.
34. Schonmeyr B., Clavin N., Avraham T., Longo V., Mehrara B.J. Synthesis of a tissue-engineered periosteum with acellular dermal matrix and cultured mesenchymal stem cells. Tissue Eng Part A 2009, 15(7):1833-1841.
35. Yu Y.Y., Lieu S., Lu C.Y., Colnot C. Bone morphogenetic protein 2 stimulates endochondral ossification by regulating periosteal cell fate during bone repair. Bone 2010, 47(1):65-73.
36. Long T., Zhu Z., Awad H.A., Schwarz E.M., Hilton M.J., Dong Y. The effect of mesenchymal stem cell sheets on structural allograft healing of critical sized femoral defects in mice. Biomaterials 2013, 35(9):2752-2759.
37. Huang C., Tang M., Yehling E., Zhang X. Overexpressing sonic hedgehog peptide restores periosteal bone formation in a murine bone allograft transplantation model. Mol Ther 2014, 22(2):430-439.
38. Huang Y.C., Kaigler D., Rice K.G., Krebsbach P.H., Mooney D.J. Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. JBone Miner Res 2005, 20(5):848-857.
39. Peng H., Wright V., Usas A., Gearhart B., Shen H.C., Cummins J., et al. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. JClin Invest 2002, 110(6):751-759.
40. Samee M., Kasugai S., Kondo H., Ohya K., Shimokawa H., Kuroda S. Bone morphogenetic protein-2 (BMP-2) and vascular endothelial growth factor (VEGF) transfection to human periosteal cells enhances osteoblast differentiation and bone formation. JPharmacol Sci 2008, 108(1):18-31.
41. Awad H.A., Zhang X., Reynolds D.G., Guldberg R.E., O'Keefe R.J., Schwarz E.M. Recent advances in gene delivery for structural bone allografts. Tissue Eng 2007, 13(8):1973-1985.
42. Takahata M., Awad H.A., O'Keefe R.J., Bukata S.V., Schwarz E.M. Endogenous tissue engineering: PTH therapy for skeletal repair. Cell Tissue Res 2012, 347(3):545-552.
43. Cao L., Liu X., Liu S., Jiang Y., Zhang X., Zhang C., et al. Experimental repair of segmental bone defects in rabbits by angiopoietin-1 gene transfected MSCs seeded on porous beta-TCP scaffolds. JBiomed Mater Res B Appl Biomater 2012, 100(5):1229-1236.
44. Han S.K., Yoon T.H., Lee D.G., Lee M.A., Kim W.K. Potential of human bone marrow stromal cells to accelerate wound healing invitro. Ann Plast Surg 2005, 55(4):414-419.
45. Allen M.R., Hock J.M., Burr D.B. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone 2004, 35(5):1003-1012.
46. Hsiao S.T., Asgari A., Lokmic Z., Sinclair R., Dusting G.J., Lim S.Y., et al. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem Cells Dev 2012, 21(12):2189-2203.
47. Brudno Y., Ennett-Shepard A.B., Chen R.R., Aizenberg M., Mooney D.J. Enhancing microvascular formation and vessel maturation through temporal control over multiple pro-angiogenic and pro-maturation factors. Biomaterials 2013, 34(36):9201-9209.
48. Hou H., Zhang X., Tang T., Dai K., Ge R. Enhancement of bone formation by genetically-engineered bone marrow stromal cells expressing BMP-2, VEGF and angiopoietin-1. Biotechnol Lett 2009, 31(8):1183-1189.
49. Xiao Y., Haase H., Young W.G., Bartold P.M. Development and transplantation of a mineralized matrix formed by osteoblasts invitro for bone regeneration. Cell Transpl 2004, 13(1):15-25.
50. Sawhney A.S., Pathak C.P., Hubbell J.A. Bioerodible hydrogels based on photopolymerized poly(ethylene glycol)-co-poly(alpha-hydroxy acid) diacrylate macromers. Macromolecules 1993, 26(4):581-587.
51. Hoffman M.D., Benoit D.S. Agonism of Wnt-beta-catenin signalling promotes mesenchymal stem cell (MSC) expansion. JTissue Eng Regen Med 2015, [in press].
52. Lin-Gibson S., Bencherif S., Cooper J.A., Wetzel S.J., Antonucci J.M., Vogel B.M., et al. Synthesis and characterization of PEG dimethacrylates and their hydrogels. Biomacromolecules 2004, 5(4):1280-1287.
53. Van Hove A.H., Wilson B.D., Benoit D.S.W. Microwave-assisted functionalization of poly(ethylene glycol) and on-resin peptides for use in chain polymerizations and hydrogel formation. JOVE 2013, 80(e50890):1-16.
54. Benoit D.S., Boutin M.E. Controlling mesenchymal stem cell gene expression using polymer-mediated delivery of siRNA. Biomacromolecules 2012, 13(11):3841-3849.
55. Jaiswal N., Haynesworth S.E., Caplan A.I., Bruder S.P. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells invitro. JCell Biochem 1997, 64(2):295-312.
56. Tiyapatanaputi P., Rubery P.T., Carmouche J., Schwarz E.M., O'Keefe R.J., Zhang X. Anovel murine segmental femoral graft model. JOrthop Res 2004, 22(6):1254-1260.
57. Benoit D.S., Tripodi M.C., Blanchette J.O., Langer S.J., Leinwand L.A., Anseth K.S. Integrin-linked kinase production prevents anoikis in human mesenchymal stem cells. JBiomed Mater Res A 2007, 81(2):259-268.
58. Benoit D.S.W., Collins S.D., Anseth K.S. Multifunctional hydrogels that promote osteogenic human mesenchymal stem cell differentiation through stimulation and sequestering of bone morphogenic protein 2. Adv Funct Mater 2007, 17(13):2085-2093.
59. Benoit D.S.W., Schwartz M.P., Durney A.R., Anseth K.S. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater 2008, 7(10):816-823.
60. Fairbanks B.D., Schwartz M.P., Bowman C.N., Anseth K.S. Photoinitiated polymerization of PEG-diacrylate with lithium phenyl-2,4,6-trimethylbenzoylphosphinate: polymerization rate and cytocompatibility. Biomaterials 2009, 30(35):6702-6707.
61. Nuttelman C.R., Tripodi M.C., Anseth K.S. Synthetic hydrogel niches that promote hMSC viability. Matrix Biol 2005, 24(3):208-218.
62. Duvall C.L., Taylor W.R., Weiss D., Guldberg R.E. Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury. Am J Physiol Heart Circ Physiol 2004, 287(1):H302-H310.
63. Jiang X., Kalajzic Z., Maye P., Braut A., Bellizzi J., Mina M., et al. Histological analysis of GFP expression in murine bone. JHistochem Cytochem 2005, 53(5):593-602.
64. Hassan M.Q., Tare R.S., Lee S.H., Mandeville M., Morasso M.I., Javed A., et al. BMP2 commitment to the osteogenic lineage involves activation of Runx2 by DLX3 and a homeodomain transcriptional network. JBiol Chem 2006, 281(52):40515-40526.
65. Hattori T., Muller C., Gebhard S., Bauer E., Pausch F., Schlund B., et al. SOX9 is a major negative regulator of cartilage vascularization, bone marrow formation and endochondral ossification. Development 2010, 137(6):901-911.
66. Kenyon N.J., Ward R.W., McGrew G., Last J.A. TGF-beta1 causes airway fibrosis and increased collagen I and III mRNA in mice. Thorax 2003, 58(9):772-777.
67. Park G.T., Morasso M.I. Bone morphogenetic protein-2 (BMP-2) transactivates Dlx3 through Smad1 and Smad4: alternative mode for Dlx3 induction in mouse keratinocytes. Nucleic Acids Res 2002, 30(2):515-522.
68. Pfaffl M.W. Anew mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
69. Reynolds D.G., Hock C., Shaikh S., Jacobson J., Zhang X., Rubery P.T., et al. Micro-computed tomography prediction of biomechanical strength in murine structural bone grafts. JBiomech 2007, 40(14):3178-3186.
70. Brodt M.D., Ellis C.B., Silva M.J. Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. JBone Miner Res 1999, 14(12):2159-2166.
71. Reynolds D.G., Shaikh S., Papuga M.O., Lerner A.L., O'Keefe R.J., Schwarz E.M., et al. muCT-based measurement of cortical bone graft-to-host union. JBone Miner Res 2009, 24(5):899-907.
72. Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration (vol. 24, pg 274, 2009). JBone Miner Res 2009, 24(4):758.
73. Nie H., Ho M.L., Wang C.K., Wang C.H., Fu Y.C. BMP-2 plasmid loaded PLGA/HAp composite scaffolds for treatment of bone defects in nude mice. Biomaterials 2009, 30(5):892-901.
74. Henriksen K., Karsdal M., Delaisse J.M., Engsig M.T. RANKL and vascular endothelial growth factor (VEGF) induce osteoclast chemotaxis through an ERK1/2-dependent mechanism. JBiol Chem 2003, 278(49):48745-48753.
75. Dhillon R.S., Xie C., Tyler W., Calvi L.M., Awad H.A., Zuscik M.J., et al. PTH-enhanced structural allograft healing is associated with decreased angiopoietin-2-mediated arteriogenesis, mast cell accumulation, and fibrosis. JBone Miner Res 2013, 28(3):586-597.
76. Udani V., Santarelli J., Yung Y., Cheshier S., Andrews A., Kasad Z., et al. Differential expression of angiopoietin-1 and angiopoietin-2 may enhance recruitment of bone-marrow-derived endothelial precursor cells into brain tumors. Neurol Res 2005, 27(8):801-806.
77. Lienau J., Schmidt-Bleek K., Peters A., Haschke F., Duda G.N., Perka C., et al. Differential regulation of blood vessel formation between standard and delayed bone healing. JOrthop Res 2009, 27(9):1133-1140.
78. 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(5):931-940.
79. Peng H., Usas A., Olshanski A., Ho A.M., Gearhart B., Cooper G.M., et al. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. JBone Miner Res 2005, 20(11):2017-2027.
80. Zhang W.J., Wang X.L., Wang S.Y., Zhao J., Xu L.Y., Zhu C., et al. The use of injectable sonication-induced silk hydrogel for VEGF(165) and BMP-2 delivery for elevation of the maxillary sinus floor. Biomaterials 2011, 32(35):9415-9424.
81. Taguchi K., Ogawa R., Migita M., Hanawa H., Ito H., Orimo H. The role of bone marrow-derived cells in bone fracture repair in a green fluorescent protein chimeric mouse model. Biochem Biophys Res Commun 2005, 331(1):31-36.
82. Tsuji K., Bandyopadhyay A., Harfe B.D., Cox K., Kakar S., Gerstenfeld L., et al. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet 2006, 38(12):1424-1429.
83. Yazici C., Takahata M., Reynolds D.G., Xie C., Samulski R.J., Samulski J., et al. Self-complementary AAV2.5-BMP2-coated femoral allografts mediated superior bone healing versus live autografts in mice with equivalent biomechanics to unfractured femur. Mol Ther 2011, 19(8):1416-1425.
84. Mountziaris P.M., Mikos A.G. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev 2008, 14(2):179-186.
85. Suzuki T., Miyamoto T., Fujita N., Ninomiya K., Iwasaki R., Toyama Y., et al. Osteoblast-specific angiopoietin 1 overexpression increases bone mass. Biochem Biophys Res Commun 2007, 362(4):1019-1025.
86. Van Hove A.H., Beltejar M.J.G., Benoit D.S.W. Development and invitro assessment of enzymatically-responsive poly(ethylene glycol) hydrogels for the delivery of therapeutic peptides. Biomaterials 2014, 35(36):9719-9730.
87. Benoit D.S.W., Anseth K.S. Heparin functionalized PEG gels that modulate protein adsorption for hMSC adhesion and differentiation. Acta Biomater 2005, 1(4):461-470.
88. Benoit D.S.W., Durney A.R., Anseth K.S. The effect of heparin-functionalized PEG hydrogels on three-dimensional human mesenchymal stem cell osteogenic differentiation. Biomaterials 2007, 28(1):66-77.
89. Benoit D.S.W., Nuttelman C.R., Collins S.D., Anseth K.S. Synthesis and characterization of a fluvastatin-releasing hydrogel delivery system to modulate hMSC differentiation and function for bone regeneration. Biomaterials 2006, 27(36):6102-6110.