Vascularization and bone regeneration in a critical sized defect using 2-N,6-O-sulfated chitosan nanoparticles incorporating BMP-2

Biomaterials

Volumn 35, Issue 2, 2014, Pages 684-698

  Cao, Lingyan ^a,b,c   Wang, Jing ^a,c   Hou, Juan ^a,c   Xing, Wanli ^a,c   Liu, Changsheng ^a,b,c  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b East China University of Science and Technology   (China)

^c East China University of Science and Technology   (China)

Author keywords

Angiogenesis; BMP; Bone regeneration; Chitosan; Nanoparticle

Indexed keywords

ANGIOGENESIS; BIOMECHANICAL MEASUREMENT; BMP; BONE REGENERATION; BONE TISSUE ENGINEERING; CRITICAL SIZED DEFECTS; IMAGING , THREE DIMENSIONAL; MICROCOMPUTED TOMOGRAPHY;

BIOMATERIALS; BONE; CHITOSAN; COMPUTERIZED TOMOGRAPHY; NANOPARTICLES; REPAIR; TISSUE ENGINEERING;

DEFECTS;

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; CD31 ANTIGEN; CHITOSAN DERIVATIVE; GELATIN SPONGE; NANOPARTICLE; VON WILLEBRAND FACTOR;

ANGIOGENESIS; ARTICLE; BIOLOGICAL ACTIVITY; BIOMECHANICS; BONE MARROW; BONE MINERAL; BONE REGENERATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVITY; EXPERIMENTAL RABBIT; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; HYDRODYNAMICS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MICRO-COMPUTED TOMOGRAPHY; MICROVASCULATURE; MOLECULAR WEIGHT; NANOFABRICATION; OSSIFICATION; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RADIUS; SULFATION; SYNCHROTRON RADIATION; THREE DIMENSIONAL IMAGING; UPREGULATION; VASCULARIZATION;

ORYCTOLAGUS CUNICULUS;

ANGIOGENESIS; BMP; BONE REGENERATION; CHITOSAN; NANOPARTICLE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL SURVIVAL; CHITOSAN; GELATIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON, SCANNING; NANOPARTICLES; NEOVASCULARIZATION, PHYSIOLOGIC; RABBITS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84886752847     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.10.005     Document Type: Article

References (54)

1. Bolland B.J., Tilley S., New A.M., Dunlop D.G., Oreffo R.O. Adult mesenchymal stem cells and impaction grafting: a new clinical paradigm shift. Expert Rev Med Devices 2007, 4:393-404.
2. Kneser U., Schaefer D.J., Polykandriotis E., Horch R.E. Tissue engineering of bone: the reconstructive surgeon's point of view. JCell Mol Med 2006, 10:7-19.
3. Brey E.M., King T.W., Johnston C., McIntire L.V., Reece G.P., Patrick C.W. Atechnique for quantitative three-dimensional analysis of microvascular structure. Microvasc Res 2002, 63:279-294.
4. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003, 9:653-660.
5. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000, 6:389-395.
6. Li J., Zhang Y.P., Kirsner R.S. Angiogenesis in wound repair: angiogenic growth factors and the extracellular matrix. Microsc Res Tech 2003, 60:107-114.
7. Nomi M., Miyake H., Sugita Y., Fujisawa M., Soker S. Role of growth factors and endothelial cells in therapeutic angiogenesis and tissue engineering. Curr Stem Cell Res Ther 2006, 1:333-343.
8. Lovett M., Lee K., Edwards A., Kaplan D.L. Vascularization strategies for tissue engineering. Tissue Eng Part B Rev 2009, 15:353-370.
9. Yang J., Zhou W., Zheng W., Ma Y., Lin L., Tang T., et al. Effects of myocardial transplantation of marrow mesenchymal stem cells transfected with vascular endothelial growth factor for the improvement of heart function and angiogenesis after myocardial infarction. Cardiology 2007, 107:17-29.
10. Conconi M.T., Ghezzo F., Dettin M., Urbani L., Grandi C., Guidolin D., et al. Effects on invitro and invivo angiogenesis induced by small peptides carrying adhesion sequences. JPept Sci 2010, 16:349-357.
11. von der Mark K., Park J., Bauer S., Schmuki P. Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix. Cell Tissue Res 2010, 339:131-153.
12. Zisch A.H., Lutolf M.P., Hubbell J.A. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol 2003, 12:295-310.
13. Santos M.I., Reis R.L. Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges. Macromol Biosci 2010, 10:12-27.
14. Smorenburg S.M., Van Noorden C.J. The complex effects of heparins on cancer progression and metastasis in experimental studies. Pharmacol Rev 2001, 53:93-105.
15. Zhang W., Chuang Y.J., Swanson R., Li J., Seo K., Leung L., et al. Antiangiogenic antithrombin down-regulates the expression of the proangiogenic heparan sulfate proteoglycan, perlecan, in endothelial cells. Blood 2004, 103:1185-1191.
16. Sasaki T., Larsson H., Kreuger J., Salmivirta M., Claesson-Welsh L., Lindahl U., et al. Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin. EMBO J 1999, 18:6240-6248.
17. Street J.T., McGrath M., O'Regan K., Wakai A., McGuinness A., Redmond H.P. Thromboprophylaxis using a low molecular weight heparin delays fracture repair. Clin Orthop Relat Res 2000, 381:278-289.
18. Le Templier G., Rodger M.A. Heparin-induced osteoporosis and pregnancy. Curr Opin Pulm Med 2008, 14:403-407.
19. Nishimura S.I., Kai H., Shinada K., Yoshida T., Tokura S., Kurita K., et al. Regioselective syntheses of sulfated polysaccharides: specific anti-HIV-1 activity of novel chitin sulfates. Carbohydr Res 1998, 306:427-433.
20. Yang J., Luo K., Li D., Yu S., Cai J., Chen L., et al. Preparation, characterization and invitro anticoagulant activity of highly sulfated chitosan. Int J Biol Macromol 2013, 52:25-31.
21. Matassi F., Nistri L., Chicon Paez D., Innocenti M. New biomaterials for bone regeneration. Clin Cases Miner Bone Metab 2011, 8:21-24.
22. 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.
23. Kaneko H., Arakawa T., Mano H., Kaneda T., Ogasawara A., Nakagawa M., et al. Direct stimulation of osteoclastic bone resorption by bone morphogenetic protein (BMP)-2 and expression of BMP receptors in mature osteoclasts. Bone 2000, 27:479-486.
24. Raida M., Heymann A.C., Gunther C., Niederwieser D. Role of bone morphogenetic protein 2 in the crosstalk between endothelial progenitor cells and mesenchymal stem cells. Int J Mol Med 2006, 18:735-739.
25. 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, 32:5241-5251.
26. Lee K., Silva E.A., Mooney D.J. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. JR Soc Interface 2011, 8:153-170.
27. Issa J.P., Bentley M.V., Iyomasa M.M., Sebald W., De Albuquerque R.F. Sustained release carriers used to delivery bone morphogenetic proteins in the bone healing process. Anat Histol Embryol 2008, 37:181-187.
28. Zhou H., Qian J., Wang J., Yao W., Liu C., Chen J., et al. Enhanced bioactivity of bone morphogenetic protein-2 with low dose of 2-N, 6-O-sulfated chitosan invitro and invivo. Biomaterials 2009, 30:1715-1724.
29. Tan M.L., Friedhuber A.M., Dunstan D.E., Choong P.F., Dass C.R. The performance of doxorubicin encapsulated in chitosan-dextran sulphate microparticles in an osteosarcoma model. Biomaterials 2010, 31:541-551.
30. Salgado A.J., Gomes M.E., Chou A., Coutinho O.P., Reis R.L., Hutmacher D.W. Preliminary study on the adhesion and proliferation of human osteoblasts on starch-based scaffolds. Mat Sci Eng C 2002, 20:27-33.
31. Dal Monte M., Martini D., Ristori C., Azara D., Armani C., Balbarini A., et al. Hypoxia effects on proangiogenic factors in human umbilical vein endothelial cells: functional role of the peptide somatostatin. Naunyn Schmiedebergs Arch Pharmacol 2011, 383:593-612.
32. Arnaoutova I., Kleinman H.K. Invitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc 2010, 5:628-635.
33. ®) as a scaffold for osteoblasts. JMat Sci Mat Med 2008, 19:1173-1182.
34. Zou D., Zhang Z., He J., Zhu S., Wang S., Zhang W., et al. Repairing critical-sized calvarial defects with BMSCs modified by a constitutively active form of hypoxia-inducible factor-1alpha and a phosphate cement scaffold. Biomaterials 2011, 32:9707-9718.
35. Au C., Mutkus L., Dobson A., Riffle J., Lalli J., Aschner M. Effects of nanoparticles on the adhesion and cell viability on astrocytes. Biol Trace Elem Res 2007, 120:248-256.
36. Renghini C., Komlev V., Fiori F., Verne E., Baino F., Vitale-Brovarone C. Micro-CT studies on 3-D bioactive glass-ceramic scaffolds for bone regeneration. Acta Biomater 2009, 5:1328-1337.
37. Kempen D.H., Lu L., Heijink A., Hefferan T.E., Creemers L.B., Maran A., et al. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 2009, 30:2816-2825.
38. van Hinsbergh V.W., Koolwijk P. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res 2008, 78:203-212.
39. Daub J.T., Merks R.M. Acell-based model of extracellular-matrix-guided endothelial cell migration during angiogenesis. Bull Math Biol 2013, 75:1377-1399.
40. Zieris A., Chwalek K., Prokoph S., Levental K.R., Welzel P.B., Freudenberg U., et al. Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels. JControl Release 2011, 156:28-36.
41. Kidoya H., Takakura N. Biology of the apelin-APJ axis in vascular formation. JBiochem 2012, 152:125-131.
42. Du F., Wang H., Zhao W., Li D., Kong D., Yang J., et al. Gradient nanofibrous chitosan/poly varepsilon-caprolactone scaffolds as extracellular microenvironments for vascular tissue engineering. Biomaterials 2012, 33:762-770.
43. Janairo R.R., Henry J.J., Lee B.L., Hashi C.K., Derugin N., Lee R., et al. Heparin-modified small-diameter nanofibrous vascular grafts. IEEE Trans Nanobioscience 2012, 11:22-27.
44. Browning M.B., Dempsey D., Guiza V., Becerra S., Rivera J., Russell B., et al. Multilayer vascular grafts based on collagen-mimetic proteins. Acta Biomater 2012, 8:1010-1021.
45. Rema R.B., Rajendran K., Ragunathan M. Angiogenic efficacy of Heparin on chick chorioallantoic membrane. Vasc Cell 2012, 4:8.
46. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
47. Piali L., Hammel P., Uherek C., Bachmann F., Gisler R.H., Dunon D., et al. CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. JCell Biol 1995, 130:451-460.
48. Sadler J.E. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 1998, 67:395-424.
49. Visser R., Arrabal P.M., Becerra J., Rinas U., Cifuentes M. The effect of an rhBMP-2 absorbable collagen sponge-targeted system on bone formation invivo. Biomaterials 2009, 30:2032-2037.
50. Li B., Yoshii T., Hafeman A.E., Nyman J.S., Wenke J.C., Guelcher S.A. The effects of rhBMP-2 released from biodegradable polyurethane/microsphere composite scaffolds on new bone formation in rat femora. Biomaterials 2009, 30:6768-6779.
51. Jha A.K., Yang W., Kirn-Safran C.B., Farach-Carson M.C., Jia X. Perlecan domain I-conjugated, hyaluronic acid-based hydrogel particles for enhanced chondrogenic differentiation via BMP-2 release. Biomaterials 2009, 30:6964-6975.
52. Johnson M.R., Lee H.J., Bellamkonda R.V., Guldberg R.E. Sustained release of BMP-2 in a lipid-based microtube vehicle. Acta Biomater 2009, 5:23-28.
53. Carano R.A., Filvaroff E.H. Angiogenesis and bone repair. Drug Discov Today 2003, 8:980-989.
54. Street J., Lenehan B. Vascular endothelial growth factor regulates osteoblast survival - evidence for an autocrine feedback mechanism. JOrthop Surg Res 2009, 4:19.