Novel osteoinductive photo-cross-linkable chitosan-lactide-fibrinogen hydrogels enhance bone regeneration in critical size segmental bone defects

Acta Biomaterialia

Volumn 10, Issue 12, 2014, Pages 5021-5033

  Kim, Sungwoo ^a   Bedigrew, Katherine ^b   Guda, Teja ^b   Maloney, William J ^a   Park, Sangwon ^c   Wenke, Joseph C ^b   Yang, Yunzhi Peter ^a,d  

^a STANFORD UNIVERSITY   (United States)

^b US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

^c Chonnam National University   (South Korea)

^d Stanford University   (United States)

Author keywords

BMP 2; Chitosan; Fibrinogen; Lactide; Photo cross linkable hydrogel

Indexed keywords

ALKALINITY; BONE; CELLS; COMPUTERIZED TOMOGRAPHY; CYTOLOGY; DEFECTS; DEGRADATION; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGELS; IMAGE ENHANCEMENT; MAMMALS; SCANNING ELECTRON MICROSCOPY;

BONE MORPHOGENETIC PROTEIN-2; BONE REGENERATION; CRITICAL SIZE; CROSS-LINKABLE; FIBRINOGEN; IN-VITRO; LACTIDES; OSTEOGENESIS; PHOTO-CROSS-LINKABLE HYDROGEL; SEGMENTAL BONE DEFECT;

CHITOSAN;

ALIZARIN RED S; ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; CHITOSAN; FIBRINOGEN; POLYLACTIDE; BMP2 PROTEIN, HUMAN; CROSS LINKING REAGENT; DELAYED RELEASE FORMULATION; DILACTIDE; DIOXANE DERIVATIVE; HYDROGEL;

ADULT; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; BONE DEFECT; BONE DEVELOPMENT; BONE MARROW STROMA CELL; BONE REGENERATION; CHEMICAL STRUCTURE; CROSS LINKING; CYTOTOXICITY TEST; DEGRADATION; ENZYME ACTIVITY; FRACTURE HEALING; HISTOPATHOLOGY; HYDROGEL; HYDROGEN BOND; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROSCOPY; MALE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; MTS ASSAY; MYOBLAST; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN SECRETION; RAT; SCANNING ELECTRON MICROSCOPY; SURFACE PROPERTY; SUSTAINED DRUG RELEASE; SYNTHESIS; ULTRAVIOLET IRRADIATION; ADMINISTRATION AND DOSAGE; ANIMAL; CHEMISTRY; COMPRESSIVE STRENGTH; DELAYED RELEASE FORMULATION; DIFFUSION; DOSE RESPONSE; DRUG EFFECTS; DRUG FORMULATION; FEMORAL FRACTURES; LIGHT; MATERIALS TESTING; PATHOLOGY; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; SPRAGUE DAWLEY RAT; TREATMENT OUTCOME; YOUNG MODULUS;

RATTUS;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CHITOSAN; COMPRESSIVE STRENGTH; CROSS-LINKING REAGENTS; DELAYED-ACTION PREPARATIONS; DIFFUSION; DIOXANES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMPOUNDING; ELASTIC MODULUS; FEMORAL FRACTURES; FIBRINOGEN; HYDROGELS; LIGHT; MALE; MATERIALS TESTING; OSTEOGENESIS; RATS; RATS, SPRAGUE-DAWLEY; TREATMENT OUTCOME;

EID: 84926390216     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.08.028     Document Type: Article

References (49)

1. Harris JS, Bemenderfer TB, Wessel AR, Kacena MA. A review of mouse critical size defect models in weight bearing bones. Bone 2013; 55: 241-7.
2. Axelrad TW, Einhorn TA. Bone morphogenetic proteins in orthopaedic surgery. Cytokine Growth Factor Rev 2009; 20: 481-8.
3. Yu YY, Lieu S, Lu C, Colnot C. Bone morphogenetic protein 2 stimulates endochondral ossification by regulating periosteal cell fate during bone repair. Bone 2010; 47: 65-73.
4. Schützenberger S, Schultz A, Hausner T, Hopf R, Zanoni G, Redl H, et al. The optimal carrier for BMP-2: a comparison of collagen versus fibrin matrix. Arch Orthop Trauma Surg 2012; 132: 1363-70.
5. Zara JN, Siu RK, Zhang X, Shen J, Ngo R, Soo C, et al. High doses of bone morphogenetic protein 2 induce structurally abnormal bone and inflammation in vivo. Tissue Eng Part A 2011; 17: 1389-99.
6. Martino M, Tortelli F, Mochizuki M, Traub S, Ben-David D, Hubbell JA, et al. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci Transl Med 2011; 3 (100): 1-8.
7. Schmidmaier G, Schwabe P, Strobel C, Wildemann B. Carrier systems and application of growth factors in orthopaedics. Injury, Int J Care Injured 2008; 39S2: S37-43.
8. McKay WF, Peckham SM, Badura JM. A comprehensive clinical review of recombinant human bone morphogenetic protein-2 (INFUSE-Bone Graft). Int Orthop 2007; 31 (6): 729-34.
9. White AP, Vaccaro AR, Hall JA, Whang PG, Friel BC, McKee MD. Clinical applications of BMP-7/OP-1 in fractures, nonunions and spinal fusion. Int Orthop 2007; 31 (6): 735-41.
10. Bhakta G, Rai B, Lim ZXH, Hui JH, Stein GS, van Wijnen AJ, et al. Hyaluronic acid-based hydrogels functionalized with heparin that support controlled release of bioactive BMP-2. Biomaterials 2012; 33: 6113-22.
11. Ben-David D, Srouji S, Shapira-Schweitzer K, Kossover O, Ivanir E, Livne E, et al. Low dose BMP-2 treatment for bone repair using a PEGylated fibrinogen hydrogel matrix. Biomaterials 2013; 34: 2902-10.
12. Schmoekel HG, Weber FE, Schense JC, Grätz KW, Schawalder P, Hubbell JA. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol Bioeng 2005; 89 (3): 253-62.
13. Bhakta G, Lim ZX, Rai B, Lin T, Hui JH, Cool SM, et al. The influence of collagen and hyaluronan matrices on the delivery and bioactivity of bone morphogenetic protein-2 and ectopic bone formation. Acta Biomater 2013. http: //dx.doi.org/10.1016/j.actbio.2013.07.008.
14. Mariner PD, Wudel JM, Miller DE, Genova EE, Streubel SO, Anseth KS. Synthetic hydrogel scaffold is an effective vehicle for delivery of INFUSE (rhBMP2) to critical-sized calvaria bone defects in rats. J Orthop Res 2013; 31 (3): 401-6.
15. Vo TN, Kasper FK, Mikos AG. Strategies for controlled delivery of growth factors and cells for bone regeneration. Adv Drug Deliv Rev 2012; 64: 1292-309.
16. Jeon O, Powell C, Solorio LD, Krebs MD, Alsberg E. Affinity-based growth factor delivery using biodegradable, photocrosslinked heparin-alginate hydrogels. J Control Release 2011; 154 (3): 258-66.
17. Sakiyama-Elbert SE, Hubbell JA. Development of fibrin derivatives for controlled release of heparin-binding growth factors. J Control Release 2000; 65 (3): 389-402.
18. Gandhi NS, Mancera RL. Prediction of heparin binding sites in bone morphogenetic proteins (BMPs). Biochim Biophys Acta 2012; 1824 (12): 1374-81.
19. Ruppert R, Hoffmann E, Sebald W. Human bone morphogenetic protein 2 contains a heparin-binding site which modifies its biological activity. Eur J Biochem 1996; 237 (1): 295-302.
20. Odrljin TM, Shainoff JR, Lawrence SO, Simpson-Haidaris PJ. Thrombin cleavage enhances exposure of a heparin binding domain in the N-terminus of the fibrin beta chain. Blood 1996; 88 (6): 2050-61.
21. Martino MM, Briquez PS, Ranga A, Lutolf MP, Hubbell JA. Heparin-binding domain of fibrin (ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc Natl Acad Sci USA 2013; 110 (12): 4563-8.
22. Jiang B, Waller TM, Larson JC, Appel AA, Brey EM. Fibrin-loaded porous poly (ethylene glycol) hydrogels as scaffold materials for vascularized tissue formation. Tissue Eng Part A 2013; 19 (1-2): 224-34.
23. Shikanov A, Xu M, Woodruff TK, Shea LD. Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 2009; 30 (29): 5476-85.
24. Kim S, Kang Y, Mercado-Pag?n AE, Maloney WJ, Yang Y. In vitro evaluation of photo-crosslinkable chitosan-lactide hydrogels for bone tissue engineering. J Biomed Mater Res B Appl Biomater 2014. http: //dx.doi.org/10.1002/ jbm.b.33118.
25. Xu X, Jha AK, Duncan RL, Jia X. Heparin-decorated, hyaluronic acid-based hydrogel particles for the controlled release of bone morphogenetic protein 2. Acta Biomater 2011; 7 (8): 3050-9.
26. Praveen G, Sreerekha PR, Menon D, Nair SV, Chennazhi KP. Fibrin nanoconstructs: a novel processing method and their use as controlled delivery agents. Nanotechnology 2012; 23 (9): 1-11.
27. Patel ZS, Young S, Tabata Y, Jansen JA, Wong ME, Mikos AG. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 2008; 43 (5): 931-40. http: //dx.doi.org/10.1016/ j.bone.2008.06.019.
28. Brown KV, Li B, Guda T, Perrien DS, Guelcher SA, Wenke JC. Improving bone formation in a rat femur segmental defect by controlling bone morphogenetic protein-2 release. Tissue Eng Part A 2011; 17 (13-14): 1735-46. http: // dx.doi.org/10.1089/ten.
29. Litvinov RI, Faizullin DA, Zuev YF, Weisel JW. The a-helix to b-sheet transition in stretched and compressed hydrated fibrin clots. Biophys J 2012; 103 (5): 1020-7.
30. Shrivastava S, Singh SK, Mukhopadhyay A, Sinha AS, Mandal RK, Dash D. Negative regulation of fibrin polymerization and clot formation by nanoparticles of silver. Colloids Surf B Biointerfaces 2011; 82 (1): 241-6.
31. Liu Y, Tian F, Hu KA. Synthesis and characterization of a brush-like copolymer of polylactide grafted onto chitosan. Carbohydr Res 2004; 339 (4): 845-51.
32. Wu Y, Zheng Y, Yang W, Wang C, Hu J, Fu S. Synthesis and characterization of a novel amphiphilic chitosan-polylactide graft copolymer. Carbohydr Polym 2005; 59: 165-71.
33. Falvo MR, Gorkun OV, Lord ST. The molecular origins of the mechanical properties of fibrin. Biophys Chem 2010; 152 (1-3): 15-20.
34. Barr?re F, van Blitterswijk CA, de Groot K. Bone regeneration: molecular and cellular interactions with calcium phosphate ceramics. Int J Nanomed 2006; 1 (3): 317-32.
35. Hiller O, Lichte A, Oberpichler A, Kocourek A, Tschesche H. Matrix metalloproteinases collagenase-2, macrophage elastase, collagenase-3, and membrane type 1-matrix metalloproteinase impair clotting by degradation of fibrinogen and factor XII. J Biol Chem 2000; 275 (42): 33008-13.
36. Freier T, Koh HS, Kazazian K, Shoichet MS. Controlling cell adhesion and degradation of chitosan films by N-acetylation. Biomaterials 2005; 26 (29): 5872-8.
37. An J, Yuan X, Luo Q, Wang D. Preparation of chitosan-graft- (methyl methacrylate)/Ag nanocomposite with antimicrobial activity. Polym Int 2010; 59: 62-70.
38. Pitarresi G, Casadei MA, Mandracchia D, Paolicelli P, Palumbo FS, Giammona G. Photocrosslinking of dextran and polyaspartamide derivatives: a combination suitable for colon-specific drug delivery. J Control Release 2007; 119 (3): 328-38.
39. Guo BL, Gao QY. Preparation and properties of a pH/temperature-responsive carboxymethyl chitosan/poly (N-isopropylacrylamide)semi-IPN hydrogel for oral delivery of drugs. Carbohydr Res 2007; 342 (16): 2416-22.
40. Hong Y, Song H, Gong Y, Mao Z, Gao C, Shen J. Covalently crosslinked chitosan hydrogel: properties of in vitro degradation and chondrocyte encapsulation. Acta Biomater 2007; 3 (1): 23-31.
41. Nguyen AH, Kim S, Maloney WJ, Wenke JC, Yang Y. Effect of coadministration of vancomycin and BMP-2 on cocultured Staphylococcus aureus and W-20-17 mouse bone marrow stromal cells in vitro. Antimicrob Agents Chemother 2012; 56 (7): 3776-84.
42. Kempen DH, Lu L, Hefferan TE, Creemers LB, Maran A, Yaszemski MJ, et al. Retention of in vitro and in vivo BMP-2 bioactivities in sustained delivery vehicles for bone tissue engineering. Biomaterials 2008; 29 (22): 3245-52.
43. Bramono DS, Murali S, Rai B, Ling L, Poh WT, Cool SM, et al. Bone marrowderived heparan sulfate potentiates the osteogenic activity of bone morphogenetic protein-2 (BMP-2). Bone 2012; 50 (4): 954-64.
44. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Suda T, et al. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 1994; 127 (6 Pt 1): 1755-66.
45. Mountziaris PM, Spicer PP, Kasper FK, Mikos AG. Harnessing and modulating inflammation in strategies for bone regeneration. Tissue Eng Part B Rev 2011; 17 (6): 393-402.
46. Barbosa JN, Amaral IF, Aguas AP, Barbosa MA. Evaluation of the effect of the degree of acetylation on the inflammatory response to 3D porous chitosan scaffolds. J Biomed Mater Res A 2010; 93 (1): 20-8.
47. Santos SG, Lamghari M, Almeida CR, Oliveira MI, Neves N, Barbosa MA, et al. Adsorbed fibrinogen leads to improved bone regeneration and correlates with differences in the systemic immune response. Acta Biomater 2013; 9 (7): 7209-17.
48. Peled E, Boss J, Bejar J, Zinman C, Seliktar D. A novel poly (ethylene glycol)- fibrinogen hydrogel for tibial segmental defect repair in a rat model. J Biomed Mater Res A 2007; 80 (4): 874-84.
49. Sciadini MF, Johnson KD. Evaluation of recombinant human bone morphogenetic protein-2 as a bone-graft substitute in a canine segmental defect model. J Orthop Res 2000; 18 (2): 289-302.