Current advances for bone regeneration based on tissue engineering strategies

Rui Shi, Yuelong Huang, Chi Ma, Chengai Wu, Wei Tian

PDF(763 KB)
PDF(763 KB)
Front. Med. ›› 2019, Vol. 13 ›› Issue (2) : 160-188. DOI: 10.1007/s11684-018-0629-9
REVIEW
REVIEW

Current advances for bone regeneration based on tissue engineering strategies

Author information +
History +

Abstract

Bone tissue engineering (BTE) is a rapidly developing strategy for repairing critical-sized bone defects to address the unmet need for bone augmentation and skeletal repair. Effective therapies for bone regeneration primarily require the coordinated combination of innovative scaffolds, seed cells, and biological factors. However, current techniques in bone tissue engineering have not yet reached valid translation into clinical applications because of several limitations, such as weaker osteogenic differentiation, inadequate vascularization of scaffolds, and inefficient growth factor delivery. Therefore, further standardized protocols and innovative measures are required to overcome these shortcomings and facilitate the clinical application of these techniques to enhance bone regeneration. Given the deficiency of comprehensive studies in the development in BTE, our review systematically introduces the new types of biomimetic and bifunctional scaffolds. We describe the cell sources, biology of seed cells, growth factors, vascular development, and the interactions of relevant molecules. Furthermore, we discuss the challenges and perspectives that may propel the direction of future clinical delivery in bone regeneration.

Keywords

bone tissue engineering / stem cell / bone scaffold / growth factor / bone regeneration

Cite this article

Download citation ▾
Rui Shi, Yuelong Huang, Chi Ma, Chengai Wu, Wei Tian. Current advances for bone regeneration based on tissue engineering strategies. Front. Med., 2019, 13(2): 160‒188 https://doi.org/10.1007/s11684-018-0629-9

References

[1]
Khan SN, Cammisa FP Jr, Sandhu HS, Diwan AD, Girardi FP, Lane JM. The biology of bone grafting. J Am Acad Orthop Surg 2005; 13(1): 77–86
CrossRef Pubmed Google scholar
[2]
Oryan A, Alidadi S, Moshiri A, Maffulli N. Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 2014; 9(1): 18
CrossRef Pubmed Google scholar
[3]
Swetha M, Sahithi K, Moorthi A, Srinivasan N, Ramasamy K, Selvamurugan N. Biocomposites containing natural polymers and hydroxyapatite for bone tissue engineering. Int J Biol Macromol 2010; 47(1): 1–4
CrossRef Pubmed Google scholar
[4]
Hosseinkhani M, Mehrabani D, Karimfar MH, Bakhtiyari S, Manafi A, Shirazi R. Tissue engineered scaffolds in regenerative medicine. World J Plast Surg 2014; 3(1): 3–7
Pubmed
[5]
Gómez S, Vlad MD, López J, Fernández E. Design and properties of 3D scaffolds for bone tissue engineering. Acta Biomater 2016; 42: 341–350
CrossRef Pubmed Google scholar
[6]
D’souza N, Rossignoli F, Golinelli G, Grisendi G, Spano C, Candini O, Osturu S, Catani F, Paolucci P, Horwitz EM, Dominici M. Mesenchymal stem/stromal cells as a delivery platform in cell and gene therapies. BMC Med 2015; 13(1): 186
CrossRef Pubmed Google scholar
[7]
Pittenger MF. Mesenchymal stem cells from adult bone marrow. Methods Mol Biol 2008; 449: 27–44
Pubmed
[8]
Wang ZG, Wang Y, Huang Y, Lu Q, Zheng L, Hu D, Feng WK, Liu YL, Ji KT, Zhang HY, Fu XB, Li XK, Chu MP, Xiao J. bFGF regulates autophagy and ubiquitinated protein accumulation induced by myocardial ischemia/reperfusion via the activation of the PI3K/Akt/mTOR pathway. Sci Rep 2015; 5(1): 9287
CrossRef Pubmed Google scholar
[9]
Nguyen MK, Alsberg E. Bioactive factor delivery strategies from engineered polymer hydrogels for therapeutic medicine. Prog Polym Sci 2014; 39(7): 1235–1265
CrossRef Pubmed Google scholar
[10]
Polo-Corrales L, Latorre-Esteves M, Ramirez-Vick JE. Scaffold design for bone regeneration. J Nanosci Nanotechnol 2014; 14(1): 15–56
CrossRef Pubmed Google scholar
[11]
Porter JR, Ruckh TT, Popat KC. Bone tissue engineering: a review in bone biomimetics and drug delivery strategies. Biotechnol Prog 2009; 25(6): 1539–1560
Pubmed
[12]
Gong T, Xie J, Liao J, Zhang T, Lin S, Lin Y. Nanomaterials and bone regeneration. Bone Res 2015; 3(1): 15029
CrossRef Pubmed Google scholar
[13]
Tang D, Tare RS, Yang LY, Williams DF, Ou KL, Oreffo RO. Biofabrication of bone tissue: approaches, challenges and translation for bone regeneration. Biomaterials 2016; 83: 363–382
CrossRef Pubmed Google scholar
[14]
Harris GM, Rutledge K, Cheng Q, Blanchette J, Jabbarzadeh E. Strategies to direct angiogenesis within scaffolds for bone tissue engineering. Curr Pharm Des 2013; 19(19): 3456–3465
CrossRef Pubmed Google scholar
[15]
Fernandez-Yague MA, Abbah SA, McNamara L, Zeugolis DI, Pandit A, Biggs MJ. Biomimetic approaches in bone tissue engineering: Integrating biological and physicomechanical strategies. Adv Drug Deliv Rev 2015; 84: 1–29
CrossRef Pubmed Google scholar
[16]
Li Y, Thula TT, Jee S, Perkins SL, Aparicio C, Douglas EP, Gower LB. Biomimetic mineralization of woven bone-like nanocomposites: role of collagen cross-links. Biomacromolecules 2012; 13(1): 49–59
CrossRef Pubmed Google scholar
[17]
Venkatesan J, Kim SK. Nano-hydroxyapatite composite biomaterials for bone tissue engineering—a review. J Biomed Nanotechnol 2014; 10(10): 3124–3140
CrossRef Pubmed Google scholar
[18]
Sang L, Huang J, Luo D, Chen Z, Li X. Bone-like nanocomposites based on self-assembled protein-based matrices with Ca2+ capturing capability. J Mater Sci Mater Med 2010; 21(9): 2561–2568
CrossRef Pubmed Google scholar
[19]
Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000; 21(24): 2529–2543
CrossRef Pubmed Google scholar
[20]
Osathanon T, Linnes ML, Rajachar RM, Ratner BD, Somerman MJ, Giachelli CM. Microporous nanofibrous fibrin-based scaffolds for bone tissue engineering. Biomaterials 2008; 29(30): 4091–4099
CrossRef Pubmed Google scholar
[21]
Lin KF, He S, Song Y, Wang CM, Gao Y, Li JQ, Tang P, Wang Z, Bi L, Pei GX. Low-temperature additive manufacturing of biomimic three-dimensional hydroxyapatite/collagen scaffolds for bone regeneration. ACS Appl Mater Interfaces 2016; 8(11): 6905–6916
CrossRef Pubmed Google scholar
[22]
Ryan GE, Pandit AS, Apatsidis DP. Porous titanium scaffolds fabricated using a rapid prototyping and powder metallurgy technique. Biomaterials 2008; 29(27): 3625–3635
CrossRef Pubmed Google scholar
[23]
Patra S, Young V. A review of 3D printing techniques and the future in biofabrication of bioprinted tissue. Cell Biochem Biophys 2016; 74(2): 93–98
CrossRef Pubmed Google scholar
[24]
Brunello G, Sivolella S, Meneghello R, Ferroni L, Gardin C, Piattelli A, Zavan B, Bressan E. Powder-based 3D printing for bone tissue engineering. Biotechnol Adv 2016; 34(5): 740–753
CrossRef Pubmed Google scholar
[25]
Warnke PH, Seitz H, Warnke F, Becker ST, Sivananthan S, Sherry E, Liu Q, Wiltfang J, Douglas T. Ceramic scaffolds produced by computer-assisted 3D printing and sintering: characterization and biocompatibility investigations. J Biomed Mater Res B Appl Biomater 2010; 93(1): 212–217
Pubmed
[26]
Xia Y, Zhou P, Cheng X, Xie Y, Liang C, Li C, Xu S. Selective laser sintering fabrication of nano-hydroxyapatite/poly-e-caprolactone scaffolds for bone tissue engineering applications. Int J Nanomedicine 2013; 8: 4197–4213
Pubmed
[27]
Chia HN, Wu BM. Recent advances in 3D printing of biomaterials. J Biol Eng 2015; 9(1): 4
CrossRef Pubmed Google scholar
[28]
Mota C, Puppi D, Chiellini F, Chiellini E. Additive manufacturing techniques for the production of tissue engineering constructs. J Tissue Eng Regen Med 2015; 9(3): 174–190
CrossRef Pubmed Google scholar
[29]
Zhang LC, Attar H, Calin M, Eckert J. Review on manufacture by selective laser melting and properties of titanium based materials for biomedical applications. Mater Technol 2016; 31(2): 66-76
CrossRef Google scholar
[30]
Körner C. Additive manufacturing of metallic components by selective electron beam melting—a review. Int Mater Rev 2016; 61(5): 361–367
CrossRef Google scholar
[31]
Bose S, Tarafder S, Bandyopadhyay A. Effect of chemistry on osteogenesis and angiogenesis towards bone tissue engineering using 3D printed scaffolds. Ann Biomed Eng 2017; 45(1): 261–272
Pubmed
[32]
Torres J, Tamimi F, Alkhraisat MH, Prados-Frutos JC, Rastikerdar E, Gbureck U, Barralet JE, López-Cabarcos E. Vertical bone augmentation with 3D-synthetic monetite blocks in the rabbit calvaria. J Clin Periodontol 2011; 38(12): 1147–1153
CrossRef Pubmed Google scholar
[33]
Tarafder S, Davies NM, Bandyopadhyay A, Bose S. 3D printed tricalcium phosphate scaffolds: effect of SrO and MgO doping on in vivo osteogenesis in a rat distal femoral defect model. Biomater Sci 2013; 1(12): 1250–1259
CrossRef Pubmed Google scholar
[34]
Tamimi F, Torres J, Al-Abedalla K, Lopez-Cabarcos E, Alkhraisat MH, Bassett DC, Gbureck U, Barralet JE. Osseointegration of dental implants in 3D-printed synthetic onlay grafts customized according to bone metabolic activity in recipient site. Biomaterials 2014; 35(21): 5436–5445
CrossRef Pubmed Google scholar
[35]
Castilho M, Dias M, Vorndran E, Gbureck U, Fernandes P, Pires I, Gouveia B, Armés H, Pires E, Rodrigues J. Application of a 3D printed customized implant for canine cruciate ligament treatment by tibial tuberosity advancement. Biofabrication 2014; 6(2): 025005
CrossRef Pubmed Google scholar
[36]
Ronca A, Ambrosio L, Grijpma DW. Design of porous three-dimensional PDLLA/nano-hap composite scaffolds using stereolithography. J Appl Biomater Funct Mater 2012; 10(3): 249–258
CrossRef Pubmed Google scholar
[37]
Lan PX, Lee JW, Seol YJ, Cho DW. Development of 3D PPF/DEF scaffolds using micro-stereolithography and surface modification. J Mater Sci Mater Med 2009; 20(1): 271–279
CrossRef Pubmed Google scholar
[38]
Guo R, Lu S, Page JM, Merkel AR, Basu S, Sterling JA, Guelcher SA. Fabrication of 3D scaffolds with precisely controlled substrate modulus and pore size by templated-fused deposition modeling to direct osteogenic differentiation. Adv Healthc Mater 2015; 4(12): 1826–1832
CrossRef Pubmed Google scholar
[39]
Nowicki MA, Castro NJ, Plesniak MW, Zhang LG. 3D printing of novel osteochondral scaffolds with graded microstructure. Nanotechnology 2016; 27(41): 414001
CrossRef Pubmed Google scholar
[40]
Ostrowska B, Di Luca A, Szlazak K, Moroni L, Swieszkowski W. Influence of internal pore architecture on biological and mechanical properties of three-dimensional fiber deposited scaffolds for bone regeneration. J Biomed Mater Res A 2016; 104(4): 991–1001
CrossRef Pubmed Google scholar
[41]
Xu N, Ye X, Wei D, Zhong J, Chen Y, Xu G, He D. 3D artificial bones for bone repair prepared by computed tomography-guided fused deposition modeling for bone repair. ACS Appl Mater Interfaces 2014; 6(17): 14952–14963
CrossRef Pubmed Google scholar
[42]
Xuan Y, Tang H, Wu B, Ding X, Lu Z, Li W, Xu Z. A specific groove design for individualized healing in a canine partial sternal defect model by a polycaprolactone/hydroxyapatite scaffold coated with bone marrow stromal cells. J Biomed Mater Res A 2014; 102(10): 3401–3408
CrossRef Pubmed Google scholar
[43]
Mehta M, Schmidt-Bleek K, Duda GN, Mooney DJ. Biomaterial delivery of morphogens to mimic the natural healing cascade in bone. Adv Drug Deliv Rev 2012; 64(12): 1257–1276
CrossRef Pubmed Google scholar
[44]
Farokhi M, Mottaghitalab F, Shokrgozar MA, Ou KL, Mao C, Hosseinkhani H. Importance of dual delivery systems for bone tissue engineering. J Control Release 2016; 225: 152–169
CrossRef Pubmed Google scholar
[45]
McFadden TM, Duffy GP, Allen AB, Stevens HY, Schwarzmaier SM, Plesnila N, Murphy JM, Barry FP, Guldberg RE, O’Brien FJ. The delayed addition of human mesenchymal stem cells to pre-formed endothelial cell networks results in functional vascularization of a collagen-glycosaminoglycan scaffold in vivo. Acta Biomater 2013; 9(12): 9303–9316
CrossRef Pubmed Google scholar
[46]
Bayer EA, Gottardi R, Fedorchak MV, Little SR. The scope and sequence of growth factor delivery for vascularized bone tissue regeneration. J Control Release 2015; 219: 129–140
CrossRef Pubmed Google scholar
[47]
Basmanav FB, Kose GT, Hasirci V. Sequential growth factor delivery from complexed microspheres for bone tissue engineering. Biomaterials 2008; 29(31): 4195–4204
CrossRef Pubmed Google scholar
[48]
Kim S, Kang Y, Krueger CA, Sen M, Holcomb JB, Chen D, Wenke JC, Yang Y. Sequential delivery of BMP-2 and IGF-1 using a chitosan gel with gelatin microspheres enhances early osteoblastic differentiation. Acta Biomater 2012; 8(5): 1768–1777
CrossRef Pubmed Google scholar
[49]
Rothstein SN, Huber KD, Sluis-Cremer N, Little SR. In vitro characterization of a sustained-release formulation for enfuvirtide. Antimicrob Agents Chemother 2014; 58(3): 1797–1799
CrossRef Pubmed Google scholar
[50]
Perez RA, Kim HW. Core-shell designed scaffolds for drug delivery and tissue engineering. Acta Biomater 2015; 21: 2–19
CrossRef Pubmed Google scholar
[51]
Kempen DH, Lu L, Heijink A, Hefferan TE, Creemers LB, Maran A, Yaszemski MJ, Dhert WJ. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 2009; 30(14): 2816–2825
CrossRef Pubmed Google scholar
[52]
Wu C, Fan W, Gelinsky M, Xiao Y, Chang J, Friis T, Cuniberti G. In situ preparation and protein delivery of silicate-alginate composite microspheres with core-shell structure. J R Soc Interface 2011; 8(65): 1804–1814
CrossRef Pubmed Google scholar
[53]
Bai Y, Leng Y, Yin G, Pu X, Huang Z, Liao X, Chen X, Yao Y. Effects of combinations of BMP-2 with FGF-2 and/or VEGF on HUVECs angiogenesis in vitro and CAM angiogenesis in vivo. Cell Tissue Res 2014; 356(1): 109–121
CrossRef Pubmed Google scholar
[54]
Boanini E, Bigi A. Biomimetic gelatin-octacalcium phosphate core–shell microspheres. J Colloid Interface Sci 2011; 362(2):594–599
[55]
Kim K, Lam J, Lu S, Spicer PP, Lueckgen A, Tabata Y, Wong ME, Jansen JA, Mikos AG, Kasper FK. Osteochondral tissue regeneration using a bilayered composite hydrogel with modulating dual growth factor release kinetics in a rabbit model. J Control Release 2013; 168(2): 166–178
CrossRef Pubmed Google scholar
[56]
Lu S, Lam J, Trachtenberg JE, Lee EJ, Seyednejad H, van den Beucken JJJP, Tabata Y, Wong ME, Jansen JA, Mikos AG, Kasper FK. Dual growth factor delivery from bilayered, biodegradable hydrogel composites for spatially-guided osteochondral tissue repair. Biomaterials 2014; 35(31): 8829–8839
CrossRef Pubmed Google scholar
[57]
Shah NJ, Hyder MN, Quadir MA, Dorval Courchesne NM, Seeherman HJ, Nevins M, Spector M, Hammond PT. Adaptive growth factor delivery from a polyelectrolyte coating promotes synergistic bone tissue repair and reconstruction. Proc Natl Acad Sci U S A 2014; 111(35): 12847–12852
CrossRef Pubmed Google scholar
[58]
DeMuth PC, Moon JJ, Suh H, Hammond PT, Irvine DJ. Releasable layer-by-layer assembly of stabilized lipid nanocapsules on microneedles for enhanced transcutaneous vaccine delivery. ACS Nano 2012; 6(9): 8041–8051
CrossRef Pubmed Google scholar
[59]
Min J, Braatz RD, Hammond PT. Tunable staged release of therapeutics from layer-by-layer coatings with clay interlayer barrier. Biomaterials 2014; 35(8): 2507–2517
CrossRef Pubmed Google scholar
[60]
Derby B. Printing and prototyping of tissues and scaffolds. Science 2012; 338(6109): 921–926
CrossRef Pubmed Google scholar
[61]
Li J, Chen M, Fan X, Zhou H. Recent advances in bioprinting techniques: approaches, applications and future prospects. J Transl Med 2016; 14(1): 271
CrossRef Pubmed Google scholar
[62]
Kang HW, Lee SJ, Ko IK, Kengla C, Yoo JJ, Atala A. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol 2016; 34(3): 312–319
CrossRef Pubmed Google scholar
[63]
Gudapati H, Dey M, Ozbolat I. A comprehensive review on droplet-based bioprinting: past, present and future. Biomaterials 2016; 102: 20–42
CrossRef Pubmed Google scholar
[64]
Cui X, Breitenkamp K, Finn MG, Lotz M, D’Lima DD. Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Eng Part A 2012; 18(11-12): 1304–1312
CrossRef Pubmed Google scholar
[65]
Cui X, Breitenkamp K, Lotz M, D’Lima D. Synergistic action of fibroblast growth factor-2 and transforming growth factor-β1 enhances bioprinted human neocartilage formation. Biotechnol Bioeng 2012; 109(9): 2357–2368
CrossRef Pubmed Google scholar
[66]
Cui X, Gao G, Qiu Y. Accelerated myotube formation using bioprinting technology for biosensor applications. Biotechnol Lett 2013; 35(3): 315–321
CrossRef Pubmed Google scholar
[67]
Gao G, Schilling AF, Yonezawa T, Wang J, Dai G, Cui X. Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol J 2014; 9(10): 1304–1311
CrossRef Pubmed Google scholar
[68]
Gao G, Yonezawa T, Hubbell K, Dai G, Cui X. Inkjet-bioprinted acrylated peptides and PEG hydrogel with human mesenchymal stem cells promote robust bone and cartilage formation with minimal printhead clogging. Biotechnol J 2015; 10(10): 1568–1577
CrossRef Pubmed Google scholar
[69]
Gao G, Schilling AF, Hubbell K, Yonezawa T, Truong D, Hong Y, Dai G, Cui X. Improved properties of bone and cartilage tissue from 3D inkjet-bioprinted human mesenchymal stem cells by simultaneous deposition and photocrosslinking in PEG-GelMA. Biotechnol Lett 2015; 37(11): 2349–2355
CrossRef Pubmed Google scholar
[70]
Mandrycky C, Wang Z, Kim K, Kim DH. 3D bioprinting for engineering complex tissues. Biotechnol Adv 2016; 34(4): 422–434
CrossRef Pubmed Google scholar
[71]
Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials 2016; 76: 321–343
CrossRef Pubmed Google scholar
[72]
Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol 2014; 32(8): 773–785
CrossRef Pubmed Google scholar
[73]
Lu CH, Chang YH, Lin SY, Li KC, Hu YC. Recent progresses in gene delivery-based bone tissue engineering. Biotechnol Adv 2013; 31(8): 1695–1706
CrossRef Pubmed Google scholar
[74]
Carlier A, Skvortsov GA, Hafezi F, Ferraris E, Patterson J, Koç B, Van Oosterwyck H. Computational model-informed design and bioprinting of cell-patterned constructs for bone tissue engineering. Biofabrication 2016; 8(2): 025009
CrossRef Pubmed Google scholar
[75]
Koch L, Gruene M, Unger C, Chichkov B. Laser assisted cell printing. Curr Pharm Biotechnol 2013; 14(1): 91–97
Pubmed
[76]
Jana S, Lerman A. Bioprinting a cardiac valve. Biotechnol Adv 2015; 33(8): 1503–1521
CrossRef Pubmed Google scholar
[77]
Catros S, Fricain JC, Guillotin B, Pippenger B, Bareille R, Remy M, Lebraud E, Desbat B, Amédée J, Guillemot F. Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication 2011; 3(2): 025001
CrossRef Pubmed Google scholar
[78]
Ali M, Pages E, Ducom A, Fontaine A, Guillemot F. Controlling laser-induced jet formation for bioprinting mesenchymal stem cells with high viability and high resolution. Biofabrication 2014; 6(4): 045001
CrossRef Pubmed Google scholar
[79]
Yao Q, Wei B, Guo Y, Jin C, Du X, Yan C, Yan J, Hu W, Xu Y, Zhou Z, Wang Y, Wang L. Design, construction and mechanical testing of digital 3D anatomical data-based PCL-HA bone tissue engineering scaffold. J Mater Sci Mater Med 2015; 26(1): 51
CrossRef Pubmed Google scholar
[80]
Pati F, Song TH, Rijal G, Jang J, Kim SW, Cho DW. Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials 2015; 37: 230–241
CrossRef Pubmed Google scholar
[81]
Baranski JD, Chaturvedi RR, Stevens KR, Eyckmans J, Carvalho B, Solorzano RD, Yang MT, Miller JS, Bhatia SN, Chen CS. Geometric control of vascular networks to enhance engineered tissue integration and function. Proc Natl Acad Sci U S A 2013; 110(19): 7586–7591
CrossRef Pubmed Google scholar
[82]
Barabaschi GD, Manoharan V, Li Q, Bertassoni LE. Engineering pre-vascularized scaffolds for bone regeneration. Adv Exp Med Biol 2015; 881: 79–94
CrossRef Pubmed Google scholar
[83]
Qin D, Xia Y, Whitesides GM. Soft lithography for micro- and nanoscale patterning. Nat Protoc 2010; 5(3): 491–502
CrossRef Pubmed Google scholar
[84]
Nikkhah M, Eshak N, Zorlutuna P, Annabi N, Castello M, Kim K, Dolatshahi-Pirouz A, Edalat F, Bae H, Yang Y, Khademhosseini A. Directed endothelial cell morphogenesis in micropatterned gelatin methacrylate hydrogels. Biomaterials 2012; 33(35): 9009–9018
CrossRef Pubmed Google scholar
[85]
Raghavan S, Nelson CM, Baranski JD, Lim E, Chen CS. Geometrically controlled endothelial tubulogenesis in micropatterned gels. Tissue Eng Part A 2010; 16(7): 2255–2263
CrossRef Pubmed Google scholar
[86]
Zheng Y, Chen J, Craven M, Choi NW, Totorica S, Diaz-Santana A, Kermani P, Hempstead B, Fischbach-Teschl C, López JA, Stroock AD. In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci U S A 2012; 109(24): 9342–9347
CrossRef Pubmed Google scholar
[87]
Wray LS, Tsioris K, Gi ES, Omenetto FG, Kaplan DL. Slowly degradable porous silk microfabricated scaffolds for vascularized tissue formation. Adv Funct Mater 2013; 23(27): 3404–3412
CrossRef Pubmed Google scholar
[88]
Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen DH, Cohen DM, Toro E, Chen AA, Galie PA, Yu X, Chaturvedi R, Bhatia SN, Chen CS. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 2012; 11(9): 768–774
CrossRef Pubmed Google scholar
[89]
Bertassoni LE, Cardoso JC, Manoharan V, Cristino AL, Bhise NS, Araujo WA, Zorlutuna P, Vrana NE, Ghaemmaghami AM, Dokmeci MR, Khademhosseini A. Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 2014; 6(2): 024105
CrossRef Pubmed Google scholar
[90]
Kinstlinger IS, Yalacki DR, Miller JS. Engineered tissues with perfusable vascular networks created by sacrificial templating of laser sintered carbohydrates. Front Bioeng Biotechnol 2016; Conference Abstract: 10th World Biomaterials Congress. https://doi.org/10.3389/conf.FBIOE.2016.01.00491
[91]
Kolesky DB, Truby RL, Gladman AS, Busbee TA, Homan KA, Lewis JA. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 2014; 26(19): 3124–3130
CrossRef Pubmed Google scholar
[92]
Radtke CL, Nino-Fong R, Esparza Gonzalez BP, Stryhn H, McDuffee LA. Characterization and osteogenic potential of equine muscle tissue- and periosteal tissue-derived mesenchymal stem cells in comparison with bone marrow- and adipose tissue-derived mesenchymal stem cells. Am J Vet Res 2013; 74(5): 790–800
CrossRef Pubmed Google scholar
[93]
Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006; 24(5): 1294–1301
CrossRef Pubmed Google scholar
[94]
Pantalone A, Antonucci I, Guelfi M, Pantalone P, Usuelli FG, Stuppia L, Salini V. Amniotic fluid stem cells: an ideal resource for therapeutic application in bone tissue engineering. Eur Rev Med Pharmacol Sci 2016; 20(13): 2884–2890
Pubmed
[95]
Petridis X, Diamanti E, Trigas GCh, Kalyvas D, Kitraki E. Bone regeneration in critical-size calvarial defects using human dental pulp cells in an extracellular matrix-based scaffold. J Craniomaxillofac Surg 2015; 43(4): 483–490
CrossRef Pubmed Google scholar
[96]
Guan J, Zhang J, Li H, Zhu Z, Guo S, Niu X, Wang Y, Zhang C. Human urine derived stem cells in combination with b-TCP can be applied for bone regeneration. PLoS One 2015; 10(5): e0125253
CrossRef Pubmed Google scholar
[97]
Illich DJ, Demir N, Stojkovic M, Scheer M, Rothamel D, Neugebauer J, Hescheler J, Zoller JE. Induced pluripotent stem (iPS) cells and lineage reprogramming: prospects for bone regeneration. Stem Cells 2011; 29(4): 555–563
CrossRef Pubmed Google scholar
[98]
Chan CK, Seo EY, Chen JY, Lo D, McArdle A, Sinha R, Tevlin R, Seita J, Vincent-Tompkins J, Wearda T, Lu WJ, Senarath-Yapa K, Chung MT, Marecic O, Tran M, Yan KS, Upton R, Walmsley GG, Lee AS, Sahoo D, Kuo CJ, Weissman IL, Longaker MT. Identification and specification of the mouse skeletal stem cell. Cell 2015; 160(1-2): 285–298
CrossRef Pubmed Google scholar
[99]
Aicher WK, Bühring HJ, Hart M, Rolauffs B, Badke A, Klein G. Regeneration of cartilage and bone by defined subsets of mesenchymal stromal cells—potential and pitfalls. Adv Drug Deliv Rev 2011; 63(4-5): 342–351
CrossRef Pubmed Google scholar
[100]
Beane OS, Fonseca VC, Cooper LL, Koren G, Darling EM. Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells. PLoS One 2014; 9(12): e115963
CrossRef Pubmed Google scholar
[101]
Li YY, Cheng HW, Cheung KM, Chan D, Chan BP. Mesenchymal stem cell-collagen microspheres for articular cartilage repair: cell density and differentiation status. Acta Biomater 2014; 10(5): 1919–1929
CrossRef Pubmed Google scholar
[102]
Mizuno H. Adipose-derived stem cells for tissue repair and regeneration: ten years of research and a literature review. J Nippon Med Sch 2009; 76(2): 56–66
CrossRef Pubmed Google scholar
[103]
Levi B, Longaker MT. Concise review: adipose-derived stromal cells for skeletal regenerative medicine. Stem Cells 2011; 29(4): 576–582
CrossRef Pubmed Google scholar
[104]
Markarian CF, Frey GZ, Silveira MD, Chem EM, Milani AR, Ely PB, Horn AP, Nardi NB, Camassola M. Isolation of adipose-derived stem cells: a comparison among different methods. Biotechnol Lett 2014; 36(4): 693–702
CrossRef Pubmed Google scholar
[105]
Baer PC, Geiger H. Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int 2012; 2012: 81
[106]
Lindroos B, Suuronen R, Miettinen S. The potential of adipose stem cells in regenerative medicine. Stem Cell Rev 2011; 7(2): 269–291
CrossRef Pubmed Google scholar
[107]
Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M, Péault B, Cummins J, Huard J. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc 2008; 3(9): 1501–1509
CrossRef Pubmed Google scholar
[108]
Wu X, Wang S, Chen B, An X. Muscle-derived stem cells: isolation, characterization, differentiation, and application in cell and gene therapy. Cell Tissue Res 2010; 340(3): 549–567
CrossRef Pubmed Google scholar
[109]
Nimura A, Muneta T, Koga H, Mochizuki T, Suzuki K, Makino H, Umezawa A, Sekiya I. Increased proliferation of human synovial mesenchymal stem cells with autologous human serum: comparisons with bone marrow mesenchymal stem cells and with fetal bovine serum. Arthritis Rheum 2008; 58(2): 501–510
CrossRef Pubmed Google scholar
[110]
Fan J, Varshney RR, Ren L, Cai D, Wang DA. Synovium-derived mesenchymal stem cells: a new cell source for musculoskeletal regeneration. Tissue Eng Part B Rev 2009; 15(1): 75–86
CrossRef Pubmed Google scholar
[111]
Yamazaki H, Tsuneto M, Yoshino M, Yamamura K, Hayashi S. Potential of dental mesenchymal cells in developing teeth. Stem Cells 2007; 25(1): 78–87
CrossRef Pubmed Google scholar
[112]
Guan JJ, Niu X, Gong FX, Hu B, Guo SC, Lou YL, Zhang CQ, Deng ZF, Wang Y. Biological characteristics of human-urine-derived stem cells: potential for cell-based therapy in neurology. Tissue Eng Part A 2014; 20(13-14): 1794–1806
CrossRef Pubmed Google scholar
[113]
Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391): 1145–1147
CrossRef Pubmed Google scholar
[114]
Hwang YS, Polak JM, Mantalaris A. In vitro direct osteogenesis of murine embryonic stem cells without embryoid body formation. Stem Cells Dev 2008; 17(5): 963–970
CrossRef Pubmed Google scholar
[115]
Ström S, Inzunza J, Grinnemo KH, Holmberg K, Matilainen E, Strömberg AM, Blennow E, Hovatta O. Mechanical isolation of the inner cell mass is effective in derivation of new human embryonic stem cell lines. Hum Reprod 2007; 22(12): 3051–3058
CrossRef Pubmed Google scholar
[116]
Bielec B, Stojko R. Stem cells of umbilical blood cord — therapeutic use. Postepy Hig Med Dosw (Online) 2015; 69: 853–863 (in Polish)
CrossRef Pubmed Google scholar
[117]
Fong CY, Chak LL, Biswas A, Tan JH, Gauthaman K, Chan WK, Bongso A. Human Wharton’s jelly stem cells have unique transcriptome profiles compared to human embryonic stem cells and other mesenchymal stem cells. Stem Cell Rev 2011; 7(1): 1–16
CrossRef Pubmed Google scholar
[118]
Huang P, Lin LM, Wu XY, Tang QL, Feng XY, Lin GY, Lin X, Wang HW, Huang TH, Ma L. Differentiation of human umbilical cord Wharton’s jelly-derived mesenchymal stem cells into germ-like cells in vitro. J Cell Biochem 2010; 109(4): 747–754
Pubmed
[119]
De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 2007; 25(1): 100–106
CrossRef Pubmed Google scholar
[120]
Roubelakis MG, Pappa KI, Bitsika V, Zagoura D, Vlahou A, Papadaki HA, Antsaklis A, Anagnou NP. Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cells. Stem Cells Dev 2007; 16(6): 931–952
CrossRef Pubmed Google scholar
[121]
Trohatou O, Anagnou NP, Roubelakis MG. Human amniotic fluid stem cells as an attractive tool for clinical applications. Curr Stem Cell Res Ther 2013; 8(2): 125–132
CrossRef Pubmed Google scholar
[122]
Gholizadeh-Ghaleh Aziz S, Pashaei-Asl F, Fardyazar Z, Pashaiasl M. Isolation, characterization, cryopreservation of human amniotic stem cells and differentiation to osteogenic and adipogenic cells. PLoS One 2016; 11(7): e0158281
Pubmed
[123]
Lee JM, Jung J, Lee HJ, Jeong SJ, Cho KJ, Hwang SG, Kim GJ. Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells. Int Immunopharmacol 2012; 13(2): 219–224
CrossRef Pubmed Google scholar
[124]
Fazekasova H, Lechler R, Langford K, Lombardi G. Placenta-derived MSCs are partially immunogenic and less immunomodulatory than bone marrow-derived MSCs. J Tissue Eng Regen Med 2011; 5(9): 684–694
CrossRef Pubmed Google scholar
[125]
Zhong ZN, Zhu SF, Yuan AD, Lu GH, He ZY, Fa ZQ, Li WH. Potential of placenta-derived mesenchymal stem cells as seed cells for bone tissue engineering: preliminary study of osteoblastic differentiation and immunogenicity. Orthopedics 2012; 35(9): 779–788
CrossRef Pubmed Google scholar
[126]
Semenov OV, Koestenbauer S, Riegel M, Zech N, Zimmermann R, Zisch AH, Malek A. Multipotent mesenchymal stem cells from human placenta: critical parameters for isolation and maintenance of stemness after isolation. Am J Obstet Gynecol 2010; 202(2): 193.e1–193.e13
CrossRef Pubmed Google scholar
[127]
Lange-Consiglio A, Corradetti B, Meucci A, Perego R, Bizzaro D, Cremonesi F. Characteristics of equine mesenchymal stem cells derived from amnion and bone marrow: in vitro proliferative and multilineage potential assessment. Equine Vet J 2013; 45(6): 737–744
CrossRef Pubmed Google scholar
[128]
Violini S, Gorni C, Pisani LF, Ramelli P, Caniatti M, Mariani P. Isolation and differentiation potential of an equine amnion-derived stromal cell line. Cytotechnology 2012; 64(1): 1–7
CrossRef Pubmed Google scholar
[129]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663–676
CrossRef Pubmed Google scholar
[130]
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131(5): 861–872
CrossRef Pubmed Google scholar
[131]
Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318(5858): 1917–1920
CrossRef Pubmed Google scholar
[132]
Jung Y, Bauer G, Nolta JA. Concise review: Induced pluripotent stem cell-derived mesenchymal stem cells: progress toward safe clinical products. Stem Cells 2012; 30(1): 42–47
CrossRef Pubmed Google scholar
[133]
Grellier M, Bordenave L, Amédée J. Cell-to-cell communication between osteogenic and endothelial lineages: implications for tissue engineering. Trends Biotechnol 2009; 27(10): 562–571
CrossRef Pubmed Google scholar
[134]
Nakasa T, Ishida O, Sunagawa T, Nakamae A, Yasunaga Y, Agung M, Ochi M. Prefabrication of vascularized bone graft using a combination of fibroblast growth factor-2 and vascular bundle implantation into a novel interconnected porous calcium hydroxyapatite ceramic. J Biomed Mater Res A 2005; 75(2): 350–355
CrossRef Pubmed Google scholar
[135]
Kawamura K, Yajima H, Ohgushi H, Tomita Y, Kobata Y, Shigematsu K, Takakura Y. Experimental study of vascularized tissue-engineered bone grafts. Plast Reconstr Surg 2006; 117(5): 1471–1479
CrossRef Pubmed Google scholar
[136]
Sun H, Qu Z, Guo Y, Zang G, Yang B. In vitro and in vivo effects of rat kidney vascular endothelial cells on osteogenesis of rat bone marrow mesenchymal stem cells growing on polylactide-glycoli acid (PLGA) scaffolds. Biomed Eng Online 2007; 6: 41
Pubmed
[137]
Xue Y, Xing Z, Bolstad AI, Van Dyke TE, Mustafa K. Co-culture of human bone marrow stromal cells with endothelial cells alters gene expression profiles. Int J Artif Organs 2013; 36(9): 650–662
CrossRef Pubmed Google scholar
[138]
Nesti LJ, Caterson EJ, Li WJ, Chang R, McCann TD, Hoek JB, Tuan RS. TGF-β1 calcium signaling in osteoblasts. J Cell Biochem 2007; 101(2): 348–359
CrossRef Pubmed Google scholar
[139]
Stahl A, Wenger A, Weber H, Stark GB, Augustin HG, Finkenzeller G. Bi-directional cell contact-dependent regulation of gene expression between endothelial cells and osteoblasts in a three-dimensional spheroidal coculture model. Biochem Biophys Res Commun 2004; 322(2): 684–692
CrossRef Pubmed Google scholar
[140]
Santos MI, Unger RE, Sousa RA, Reis RL, Kirkpatrick CJ. Crosstalk between osteoblasts and endothelial cells co-cultured on a polycaprolactone-starch scaffold and the in vitro development of vascularization. Biomaterials 2009; 30(26): 4407–4415
CrossRef Pubmed Google scholar
[141]
Dohle E, Fuchs S, Kolbe M, Hofmann A, Schmidt H, Kirkpatrick CJ. Sonic hedgehog promotes angiogenesis and osteogenesis in a coculture system consisting of primary osteoblasts and outgrowth endothelial cells. Tissue Eng Part A 2010; 16(4): 1235–1237
CrossRef Pubmed Google scholar
[142]
Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 2009; 24(2): 274–282
CrossRef Pubmed Google scholar
[143]
Chen D, Zhang X, He Y, Lu J, Shen H, Jiang Y, Zhang C, Zeng B. Co-culturing mesenchymal stem cells from bone marrow and periosteum enhances osteogenesis and neovascularization of tissue-engineered bone. J Tissue Eng Regen Med 2012; 6(10): 822–832
CrossRef Pubmed Google scholar
[144]
Chen D, Shen H, He Y, Chen Y, Wang Q, Lu J, Jiang Y. Synergetic effects of hBMSCs and hPCs in osteogenic differentiation and their capacity in the repair of critical-sized femoral condyle defects. Mol Med Rep 2015; 11(2): 1111–1119
CrossRef Pubmed Google scholar
[145]
Park JS, Park KH. Light enhanced bone regeneration in an athymic nude mouse implanted with mesenchymal stem cells embedded in PLGA microspheres. Biomater Res 2016; 20(1): 4
CrossRef Pubmed Google scholar
[146]
Wu L, Zhao X, He B, Jiang J, Xie XJ, Liu L. The possible roles of biological bone constructed with peripheral blood derived EPCs and BMSCs in osteogenesis and angiogenesis. Biomed Res Int. 2016; 2016:8168943
[147]
Fisher JN, Peretti GM, Scotti C. Stem cells for bone regeneration: from cell-based therapies to decellularised engineered extracellular matrices. Stem Cells Int 2016; 2016:9352598
[148]
Dmitrieva RI, Minullina IR, Bilibina AA, Tarasova OV, Anisimov SV, Zaritskey AY. Bone marrow- and subcutaneous adipose tissue-derived mesenchymal stem cells: differences and similarities. Cell Cycle 2012; 11(2): 377–383
CrossRef Pubmed Google scholar
[149]
Brocher J, Janicki P, Voltz P, Seebach E, Neumann E, Mueller-Ladner U, Richter W. Inferior ectopic bone formation of mesenchymal stromal cells from adipose tissue compared to bone marrow: rescue by chondrogenic pre-induction. Stem Cell Res 2013; 11(3): 1393–1406
CrossRef Pubmed Google scholar
[150]
Sándor GK, Numminen J, Wolff J, Thesleff T, Miettinen A, Tuovinen VJ, Mannerström B, Patrikoski M, Seppänen R, Miettinen S, Rautiainen M, Öhman J. Adipose stem cells used to reconstruct 13 cases with cranio-maxillofacial hard-tissue defects. Stem Cells Transl Med 2014; 3(4): 530–540
CrossRef Pubmed Google scholar
[151]
Kuhn LT, Liu Y, Boyd NL, Dennis JE, Jiang X, Xin X, Charles LF, Wang L, Aguila HL, Rowe DW, Lichtler AC, Goldberg AJ. Developmental-like bone regeneration by human embryonic stem cell-derived mesenchymal cells. Tissue Eng Part A 2014; 20(1-2): 365–377
CrossRef Pubmed Google scholar
[152]
Levi B, Hyun JS, Montoro DT, Lo DD, Chan CK, Hu S, Sun N, Lee M, Grova M, Connolly AJ, Wu JC, Gurtner GC, Weissman IL, Wan DC, Longaker MT. In vivo directed differentiation of pluripotent stem cells for skeletal regeneration. Proc Natl Acad Sci U S A 2012; 109(50): 20379–20384
CrossRef Pubmed Google scholar
[153]
Mathieu M, Rigutto S, Ingels A, Spruyt D, Stricwant N, Kharroubi I, Albarani V, Jayankura M, Rasschaert J, Bastianelli E, Gangji V. Decreased pool of mesenchymal stem cells is associated with altered chemokines serum levels in atrophic nonunion fractures. Bone 2013; 53(2): 391–398
CrossRef Pubmed Google scholar
[154]
Yamada Y, Nakamura S, Ito K, Sugito T, Yoshimi R, Nagasaka T, Ueda M. A feasibility of useful cell-based therapy by bone regeneration with deciduous tooth stem cells, dental pulp stem cells, or bone-marrow-derived mesenchymal stem cells for clinical study using tissue engineering technology. Tissue Eng Part A 2010; 16(6): 1891–1900
CrossRef Pubmed Google scholar
[155]
Balmayor ER. Targeted delivery as key for the success of small osteoinductive molecules. Adv Drug Deliv Rev 2015; 94: 13–27
CrossRef Pubmed Google scholar
[156]
Massagué J, Wotton D. Transcriptional control by the TGF-β/Smad signaling system. EMBO J 2000; 19(8): 1745–1754PMID:10775259
CrossRef Google scholar
[157]
Joyce ME, Jingushi S, Bolander ME. Transforming growth factor-β in the regulation of fracture repair. Orthop Clin North Am 1990; 21(1): 199–209
Pubmed
[158]
Lind M, Schumacker B, Søballe K, Keller J, Melsen F, Bünger C. Transforming growth factor-β enhances fracture healing in rabbit tibiae. Acta Orthop Scand 1993; 64(5): 553–556
CrossRef Pubmed Google scholar
[159]
Critchlow MA, Bland YS, Ashhurst DE. The effect of exogenous transforming growth factor-β 2 on healing fractures in the rabbit. Bone 1995; 16(5): 521–527
CrossRef Pubmed Google scholar
[160]
Tamai N, Myoui A, Hirao M, Kaito T, Ochi T, Tanaka J, Takaoka K, Yoshikawa H. A new biotechnology for articular cartilage repair: subchondral implantation of a composite of interconnected porous hydroxyapatite, synthetic polymer (PLA-PEG), and bone morphogenetic protein-2 (rhBMP-2). Osteoarthritis Cartilage 2005; 13(5): 405–417
CrossRef Pubmed Google scholar
[161]
Vrijens K, Lin W, Cui J, Farmer D, Low J, Pronier E, Zeng FY, Shelat AA, Guy K, Taylor MR, Chen T, Roussel MF. Identification of small molecule activators of BMP signaling. PLoS One 2013; 8(3): e59045
CrossRef Pubmed Google scholar
[162]
Bandyopadhyay A, Yadav PS, Prashar P. BMP signaling in development and diseases: a pharmacological perspective. Biochem Pharmacol 2013; 85(7): 857–864
CrossRef Pubmed Google scholar
[163]
Bergeron E, Leblanc E, Drevelle O, Giguère R, Beauvais S, Grenier G, Faucheux N. The evaluation of ectopic bone formation induced by delivery systems for bone morphogenetic protein-9 or its derived peptide. Tissue Eng Part A 2012; 18(3-4): 342–352
CrossRef Pubmed Google scholar
[164]
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(2): 293–300
CrossRef Pubmed Google scholar
[165]
Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13(12): 4279–4295
CrossRef Pubmed Google scholar
[166]
Wang J, Zheng Y, Zhao J, Liu T, Gao L, Gu Z, Wu G. Low-dose rhBMP2/7 heterodimer to reconstruct peri-implant bone defects: a micro-CT evaluation. J Clin Periodontol 2012; 39(1): 98–105
CrossRef Pubmed Google scholar
[167]
He X, Liu Y, Yuan X, Lu L. Enhanced healing of rat calvarial defects with MSCs loaded on BMP-2 releasing chitosan/alginate/hydroxyapatite scaffolds. PLoS One 2014; 9(8): e104061
CrossRef Pubmed Google scholar
[168]
Li J, Hong J, Zheng Q, Guo X, Lan S, Cui F, Pan H, Zou Z, Chen C. Repair of rat cranial bone defects with nHAC/PLLA and BMP-2-related peptide or rhBMP-2. J Orthop Res 2011; 29(11): 1745–1752
CrossRef Pubmed Google scholar
[169]
Lind M. Growth factor stimulation of bone healing. Effects on osteoblasts, osteomies, and implants fixation. Acta Orthop Scand Suppl 1998; 283: 2–37
Pubmed
[170]
Kato T, Kawaguchi H, Hanada K, Aoyama L, Hiyama Y, Nakamura T, Ku-zutani K, Tamura M, Kurokawa T, Nakamura K. Single local injection of re-combinant fibroblast growth factor-2 stimulates healing of segmental bone defects in rabbits. J Orthop Res 1998; 16: 654–659
CrossRef Pubmed Google scholar
[171]
Liu Z, Lavine KJ, Hung IH, Ornitz DM. FGF18 is required for early chondrocyte proliferation, hypertrophy and vascular invasion of the growth plate. Dev Biol 2007; 302(1): 80–91
CrossRef Pubmed Google scholar
[172]
Schmid GJ, Kobayashi C, Sandell LJ, Ornitz DM. Fibroblast growth factor expression during skeletal fracture healing in mice. Dev Dyn 2009; 238(3): 766–774
CrossRef Pubmed Google scholar
[173]
Behr B, Leucht P, Longaker MT, Quarto N. Fgf-9 is required for angiogenesis and osteogenesis in long bone repair. Proc Natl Acad Sci U S A 2010; 107(26): 11853–11858
CrossRef Pubmed Google scholar
[174]
Bak B, Jørgensen PH, Andreassen TT. Dose response of growth hormone on fracture healing in the rat. Acta Orthop Scand 1990; 61(1): 54–57
CrossRef Pubmed Google scholar
[175]
Thaller SR, Dart A, Tesluk H. The effects of insulin-like growth factor-1 on critical-size calvarial defects in Sprague-Dawley rats. Ann Plast Surg 1993; 31(5): 429–433
CrossRef Pubmed Google scholar
[176]
Segar CE, Ogle ME, Botchwey EA. Regulation of angiogenesis and bone regeneration with natural and synthetic small molecules. Curr Pharm Des 2013; 19(19): 3403–3419
CrossRef Pubmed Google scholar
[177]
Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, Ferrara N, Steinmetz H, Hoeffel J, Cleland JL, Daugherty A, van Bruggen N, Redmond HP, Carano RA, Filvaroff EH. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A 2002; 99(15): 9656–9661
CrossRef Pubmed Google scholar
[178]
Bouletreau PJ, Warren SM, Spector JA, Peled ZM, Gerrets RP, Greenwald JA, Longaker MT. 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
CrossRef Pubmed Google scholar
[179]
Zelzer E, McLean W, Ng YS, Fukai N, Reginato AM, Lovejoy S, D’Amore PA, Olsen BR. Skeletal defects in VEGF(120/120) mice reveal multiple roles for VEGF in skeletogenesis. Development 2002; 129(8): 1893–1904
Pubmed
[180]
Cui F, Wang X, Liu X, Dighe AS, Balian G, Cui Q. VEGF and BMP-6 enhance bone formation mediated by cloned mouse osteoprogenitor cells. Growth Factors 2010; 28(5): 306–317
CrossRef Pubmed Google scholar
[181]
Bab I, Gazit D, Chorev M, Muhlrad A, Shteyer A, Greenberg Z, Namdar M, Kahn A. Histone H4-related osteogenic growth peptide (OGP): a novel circulating stimulator of osteoblastic activity. EMBO J 1992; 11(5): 1867–1873
Pubmed
[182]
Gabarin N, Gavish H, Muhlrad A, Chen YC, Namdar-Attar M, Nissenson RA, Chorev M, Bab I. Mitogenic G(i) protein-MAP kinase signaling cascade in MC3T3-E1 osteogenic cells: activation by C-terminal pentapeptide of osteogenic growth peptide [OGP(10-14)] and attenuation of activation by cAMP. J Cell Biochem 2001; 81(4): 594–603
CrossRef Pubmed Google scholar
[183]
An G, Xue Z, Zhang B, Deng QK, Wang YS, Lv SC. Expressing osteogenic growth peptide in the rabbit bone mesenchymal stem cells increased alkaline phosphatase activity and enhanced the collagen accumulation. Eur Rev Med Pharmacol Sci 2014; 18(11): 1618–1624
Pubmed
[184]
Brager MA, Patterson MJ, Connolly JF, Nevo Z. Osteogenic growth peptide normally stimulated by blood loss and marrow ablation has local and systemic effects on fracture healing in rats. J Orthop Res 2000; 18(1): 133–139
CrossRef Pubmed Google scholar
[185]
Shuqiang M, Kunzheng W, Xiaoqiang D, Wei W, Mingyu Z, Daocheng W. Osteogenic growth peptide incorporated into PLGA scaffolds accelerates healing of segmental long bone defects in rabbits. J Plast Reconstr Aesthet Surg 2008; 61(12): 1558–1560
CrossRef Pubmed Google scholar
[186]
Jilka RL. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 2007; 40(6): 1434–1446
CrossRef Pubmed Google scholar
[187]
Manabe T, Mori S, Mashiba T, Kaji Y, Iwata K, Komatsubara S, Seki A, Sun YX, Yamamoto T. Human parathyroid hormone (1-34) accelerates natural fracture healing process in the femoral osteotomy model of cynomolgus monkeys. Bone 2007; 40(6): 1475–1482
CrossRef Pubmed Google scholar
[188]
Komatsu DE, Brune KA, Liu H, Schmidt AL, Han B, Zeng QQ, Yang X, Nunes JS, Lu Y, Geiser AG, Ma YL, Wolos JA, Westmore MS, Sato M. Longitudinal in vivo analysis of the region-specific efficacy of parathyroid hormone in a rat cortical defect model. Endocrinology 2009; 150(4): 1570–1579
CrossRef Pubmed Google scholar
[189]
Jung RE, Cochran DL, Domken O, Seibl R, Jones AA, Buser D, Hammerle CH. The effect of matrix bound parathyroid hormone on bone regeneration. Clin Oral Implants Res 2007; 18(3): 319–325
CrossRef Pubmed Google scholar
[190]
Kaback LA, Soung Y, Naik A, Geneau G, Schwarz EM, Rosier RN, O’Keefe RJ, Drissi H. Teriparatide (1-34 human PTH) regulation of osterix during fracture repair. J Cell Biochem 2008; 105(1): 219–226
CrossRef Pubmed Google scholar
[191]
Aspenberg P, Genant HK, Johansson T, Nino AJ, See K, Krohn K, García-Hernández PA, Recknor CP, Einhorn TA, Dalsky GP, Mitlak BH, Fierlinger A, Lakshmanan MC. Teriparatide for acceleration of fracture repair in humans: a prospective, randomized, double-blind study of 102 postmenopausal women with distal radial fractures. J Bone Miner Res 2010; 25(2): 404–414
CrossRef Pubmed Google scholar
[192]
Reynolds DG, Shaikh S, Papuga MO, Lerner AL, O’Keefe RJ, Schwarz EM, Awad HA. muCT-based measurement of cortical bone graft-to-host union. J Bone Miner Res 2009; 24(5): 899–907
CrossRef Pubmed Google scholar
[193]
Manton KJ, Leong DFM, Cool SM, Nurcombe V. Disruption of heparan and chondroitin sulfate signaling enhances mesenchymal stem cell-derived osteogenic differentiation via bone morphogenetic protein signaling pathways. Stem Cells 2007; 25(11): 2845–2854
CrossRef Pubmed Google scholar
[194]
Choi YJ, Lee JY, Park JH, Park JB, Suh JS, Choi YS, Lee SJ, Chung CP, Park YJ. The identification of a heparin binding domain peptide from bone morphogenetic protein-4 and its role on osteogenesis. Biomaterials 2010; 31(28): 7226–7238
CrossRef Pubmed Google scholar
[195]
Lee JY, Choo JE, Park HJ, Park JB, Lee SC, Jo I, Lee SJ, Chung CP, Park YJ. Injectable gel with synthetic collagen-binding peptide for enhanced osteogenesis in vitro and in vivo. Biochem Biophys Res Commun 2007; 357(1): 68–74
CrossRef Pubmed Google scholar
[196]
Yewle JN, Puleo DA, Bachas LG. Bifunctional bisphosphonates for delivering PTH (1-34) to bone mineral with enhanced bioactivity. Biomaterials 2013; 34(12): 3141–3149
CrossRef Pubmed Google scholar
[197]
Rezania A, Healy KE. Biomimetic peptide surfaces that regulate adhesion, spreading, cytoskeletal organization, and mineralization of the matrix deposited by osteoblast-like cells. Biotechnol Prog 1999; 15(1): 19–32
CrossRef Pubmed Google scholar
[198]
Lo KW, Ashe KM, Kan HM, Laurencin CT. The role of small molecules in musculoskeletal regeneration. Regen Med 2012; 7(4): 535–549
CrossRef Pubmed Google scholar
[199]
Tai IC, Wang YH, Chen CH, Chuang SC, Chang JK, Ho ML. Simvastatin enhances Rho/actin/cell rigidity pathway contributing to mesenchymal stem cells’ osteogenic differentiation. Int J Nanomedicine 2015; 10: 5881–5894
Pubmed
[200]
Ruiz-Gaspa S, Nogues X, Enjuanes A, Monllau JC, Blanch J, Carreras R, Mellibovsky L, Grinberg D, Balcells S, Díez-Perez A, Pedro-Botet J. Simvastatin and atorvastatin enhance gene expression of collagen type 1 and osteocalcin in primary human osteoblasts and MG-63 cultures. J Cell Biochem 2007; 101(6): 1430–1438
CrossRef Pubmed Google scholar
[201]
Moriyama Y, Ayukawa Y, Ogino Y, Atsuta I, Todo M, Takao Y, Koyano K. Local application of fluvastatin improves peri-implant bone quantity and mechanical properties: a rodent study. Acta Biomater 2010; 6(4): 1610–1618
CrossRef Pubmed Google scholar
[202]
Lo KW, Ulery BD, Kan HM, Ashe KM, Laurencin CT. Evaluating the feasibility of utilizing the small molecule phenamil as a novel biofactor for bone regenerative engineering. J Tissue Eng Regen Med 2014; 8(9): 728–736
CrossRef Pubmed Google scholar
[203]
Balmayor ER. Targeted delivery as key for the success of small osteoinductive molecules. Adv Drug Deliv Rev 2015; 94: 13–27
CrossRef Pubmed Google scholar
[204]
Park KW, Waki H, Kim WK, Davies BS, Young SG, Parhami F, Tontonoz P. The small molecule phenamil induces osteoblast differentiation and mineralization. Mol Cell Biol 2009; 29(14): 3905–3914
CrossRef Pubmed Google scholar
[205]
Zhao J, Ohba S, Shinkai M, Chung UI, Nagamune T. Icariin induces osteogenic differentiation in vitro in a BMP- and Runx2-dependent manner. Biochem Biophys Res Commun 2008; 369(2): 444–448
CrossRef Pubmed Google scholar
[206]
Nakajima K, Komiyama Y, Hojo H, Ohba S, Yano F, Nishikawa N, Ihara S, Aburatani H, Takato T, Chung UI. Enhancement of bone formation ex vivo and in vivo by a helioxanthin-derivative. Biochem Biophys Res Commun 2010; 395(4): 502–508
CrossRef Pubmed Google scholar
[207]
Salazar VS, Gamer LW, Rosen V. BMP signalling in skeletal development, disease and repair. Nat Rev Endocrinol 2016; 12(4): 203–221
CrossRef Pubmed Google scholar
[208]
Wu X, Ding S, Ding Q, Gray NS, Schultz PG. A small molecule with osteogenesis-inducing activity in multipotent mesenchymal progenitor cells. J Am Chem Soc 2002; 124(49): 14520–14521
CrossRef Pubmed Google scholar
[209]
Corcoran RB, Scott MP. Oxysterols stimulate Sonic hedgehog signal transduction and proliferation of medulloblastoma cells. Proc Natl Acad Sci USA 2006; 103(22): 8408–8413
CrossRef Pubmed Google scholar
[210]
James AW. Review of signaling pathways governing MSC osteogenic and adipogenic differentiation. Scientifica (Cairo) 2013; 2013: 684736
[211]
Sinha S, Chen JK. Purmorphamine activates the Hedgehog pathway by targeting Smoothened. Nat Chem Biol 2006; 2(1): 29–30
CrossRef Pubmed Google scholar
[212]
Gellynck K, Shah R, Parkar M, Young A, Buxton P, Brett P. Small molecule stimulation enhances bone regeneration but not titanium implant osseointegration. Bone 2013; 57(2): 405–412
CrossRef Pubmed Google scholar
[213]
Amantea CM, Kim WK, Meliton V, Tetradis S, Parhami F. Oxysterol-induced osteogenic differentiation of marrow stromal cells is regulated by Dkk-1 inhibitable and PI3-kinase mediated signaling. J Cell Biochem 2008; 105(2): 424–436
CrossRef Pubmed Google scholar
[214]
Aghaloo TL, Amantea CM, Cowan CM, Richardson JA, Wu BM, Parhami F, Tetradis S. Oxysterols enhance osteoblast differentiation in vitro and bone healing in vivo. J Orthop Res 2007; 25(11): 1488–1497
CrossRef Pubmed Google scholar
[215]
Stappenbeck F, Xiao W, Epperson M, Riley M, Priest A, Huang D, Nguyen K, Jung ME, Thies RS, Farouz F. Novel oxysterols activate the Hedgehog pathway and induce osteogenesis. Bioorg Med Chem Lett 2012; 22(18): 5893–5897
CrossRef Pubmed Google scholar
[216]
Siddappa R, Martens A, Doorn J, Leusink A, Olivo C, Licht R, van Rijn L, Gaspar C, Fodde R, Janssen F, van Blitterswijk C, de Boer J. cAMP/PKA pathway activation in human mesenchymal stem cells in vitro results in robust bone formation in vivo. Proc Natl Acad Sci U S A 2008; 105(20): 7281–7286
CrossRef Pubmed Google scholar
[217]
Lo KWH, Kan HM, Ashe KM, Laurencin CT. The small molecule PKA-specific cyclic AMP analogue as an inducer of osteoblast-like cells differentiation and mineralization. J Tissue Eng Regen Med 2012; 6(1): 40–48
CrossRef Pubmed Google scholar
[218]
Lo KW, Kan HM, Gagnon KA, Laurencin CT. One-day treatment of small molecule 8-bromo-cyclic AMP analogue induces cell-based VEGF production for in vitro angiogenesis and osteoblastic differentiation. J Tissue Eng Regen Med 2016; 10(10): 867–875
CrossRef Pubmed Google scholar
[219]
Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, Vacher J, Proia RL, Germain RN. Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 2009; 458(7237): 524–528
CrossRef Pubmed Google scholar
[220]
Petrie Aronin CE, Sefcik LS, Tholpady SS, Tholpady A, Sadik KW, Macdonald TL, Peirce SM, Wamhoff BR, Lynch KR, Ogle RC, Botchwey EA. FTY720 promotes local microvascular network formation and regeneration of cranial bone defects. Tissue Eng Part A 2010; 16(6): 1801–1809
CrossRef Pubmed Google scholar
[221]
Petrie Aronin CE, Shin SJ, Naden KB, Rios PD Jr, Sefcik LS, Zawodny SR, Bagayoko ND, Cui Q, Khan Y, Botchwey EA. The enhancement of bone allograft incorporation by the local delivery of the sphingosine 1-phosphate receptor targeted drug FTY720. Biomaterials 2010; 31(25): 6417–6424
CrossRef Pubmed Google scholar
[222]
Gellynck K, Neel EA, Li H, Mardas N, Donos N, Buxton P, Young AM. Cell attachment and response to photocured, degradable bone adhesives containing tricalcium phosphate and purmorphamine. Acta Biomater 2011; 7(6): 2672–2677
CrossRef Pubmed Google scholar
[223]
Qi Y, Zhao T, Yan W, Xu K, Shi Z, Wang J. Mesenchymal stem cell sheet transplantation combined with locally released simvastatin enhances bone formation in a rat tibia osteotomy model. Cytotherapy 2013; 15(1): 44–56
CrossRef Pubmed Google scholar
[224]
Maeda Y, Hojo H, Shimohata N, Choi S, Yamamoto K, Takato T, Chung UI, Ohba S. Bone healing by sterilizable calcium phosphate tetrapods eluting osteogenic molecules. Biomaterials 2013; 34(22): 5530–5537
CrossRef Pubmed Google scholar
[225]
Ohba S, Nakajima K, Komiyama Y, Kugimiya F, Igawa K, Itaka K, Moro T, Nakamura K, Kawaguchi H, Takato T, Chung UI. A novel osteogenic helioxanthin-derivative acts in a BMP-dependent manner. Biochem Biophys Res Commun 2007; 357(4): 854–860
CrossRef Pubmed Google scholar
[226]
Chatterjea A, LaPointe VL, Alblas J, Chatterjea S, van Blitterswijk CA, de Boer J. Suppression of the immune system as a critical step for bone formation from allogeneic osteoprogenitors implanted in rats. J Cell Mol Med 2014; 18(1): 134–142
CrossRef Pubmed Google scholar
[227]
Ghadakzadeh S, Mekhail M, Aoude A, Hamdy R, Tabrizian M. Small players ruling the hard game: siRNA in bone regeneration. J Bone Miner Res 2016; 31(3): 475–487
CrossRef Pubmed Google scholar
[228]
Hong L, Wei N, Joshi V, Yu Y, Kim N, Krishnamachari Y, Zhang Q, Salem AK. Effects of glucocorticoid receptor small interfering RNA delivered using poly lactic-co-glycolic acid microparticles on proliferation and differentiation capabilities of human mesenchymal stromal cells. Tissue Eng Part A 2012; 18(7-8): 775–784
CrossRef Pubmed Google scholar
[229]
Wang Y, Tran KK, Shen H, Grainger DW. Selective local delivery of RANK siRNA to bone phagocytes using bone augmentation biomaterials. Biomaterials 2012; 33(33): 8540–8547
CrossRef Pubmed Google scholar
[230]
Zhang Y, Wei L, Miron RJ, Shi B, Bian Z. Anabolic bone formation via a site-specific bone-targeting delivery system by interfering with semaphorin 4D expression. J Bone Miner Res 2015; 30(2): 286–296
CrossRef Pubmed Google scholar
[231]
Zhang Y, Wei L, Miron RJ, Zhang Q, Bian Z. Prevention of alveolar bone loss in an osteoporotic animal model via interference of semaphorin 4d. J Dent Res 2014; 93(11): 1095–1100
CrossRef Pubmed Google scholar
[232]
Jackson AL, Linsley PS. Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat Rev Drug Discov 2010; 9(1): 57–67
CrossRef Pubmed Google scholar
[233]
Hankenson KD, Dishowitz M, Gray C, Schenker M. Angiogenesis in bone regeneration. Injury 2011; 42(6): 556–561
CrossRef Pubmed Google scholar
[234]
Ozdemir T, Higgins AM, Brown JL. Osteoinductive biomaterial geometries for bone regenerative engineering. Curr Pharm Des 2013; 19(19): 3446–3455
CrossRef Pubmed Google scholar
[235]
Mandal BB, Grinberg A, Gil ES, Panilaitis B, Kaplan DL. High-strength silk protein scaffolds for bone repair. Proc Natl Acad Sci USA 2012; 109(20): 7699–7704
CrossRef Pubmed Google scholar
[236]
O’Brien FJ, Harley BA, Yannas IV, Gibson LJ. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005; 26(4): 433–441
CrossRef Pubmed Google scholar
[237]
Sicchieri LG, Crippa GE, de Oliveira PT, Beloti MM, Rosa AL. Pore size regulates cell and tissue interactions with PLGA-CaP scaffolds used for bone engineering. J Tissue Eng Regen Med 2012; 6(2): 155–162
CrossRef Pubmed Google scholar
[238]
Zajac AL, Discher DE. Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling. Curr Opin Cell Biol 2008; 20(6): 609–615
CrossRef Pubmed Google scholar
[239]
Yousefi AM, Hoque ME, Prasad RG, Uth N. Current strategies in multiphasic scaffold design for osteochondral tissue engineering: a review. J Biomed Mater Res A 2015; 103(7): 2460–2481
CrossRef Pubmed Google scholar
[240]
Chapanian R, Amsden BG. Combined and sequential delivery of bioactive VEGF165 and HGF from poly(trimethylene carbonate) based photo-cross-linked elastomers. J Control Release 2010; 143(1): 53–63
CrossRef Pubmed Google scholar

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 51673029, 81330043, and 81071499), Beijing Talent Fund (No. 2016000021223ZK34), and another fund (No. PXM2018_026275_000001).

Compliance with ethics guidelines

Rui Shi, Yuelong Huang, Chi Ma, Chengai Wu, and Wei Tian declare that they have no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

RIGHTS & PERMISSIONS

2018 Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature
AI Summary AI Mindmap
PDF(763 KB)

Accesses

Citations

Detail

Sections
Recommended

/