Stem Cell and Advanced Nano Bioceramic Interactions

  • Sevil Köse
  • Berna Kankilic
  • Merve Gizer
  • Eda Ciftci Dede
  • Erdal Bayramli
  • Petek Korkusuz
  • Feza Korkusuz
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1077)


Bioceramics are type of biomaterials generally used for orthopaedic applications due to their similar structure with bone. Especially regarding to their osteoinductivity and osteoconductivity, they are used as biodegradable scaffolds for bone regeneration along with mesenchymal stem cells. Since chemical properties of bioceramics are important for regeneration of tissue, physical properties are also important for cell proliferation. In this respect, several different manufacturing methods are used for manufacturing nano scale bioceramics. These nano scale bioceramics are used for regeneration of bone and cartilage both alone or with other types of biomaterials. They can also act as carrier for the delivery of drugs in musculoskeletal infections without causing any systemic toxicity.


Mesenchymal stem cells bioceramics hydroxyapatite tricalcium phosphate biphasic calcium phosphate nanotechnology osteogenic differentiation regeneration osteomyelitis 


  1. 1.
    Ammerman JM, Libricz J, Ammerman MD (2013) The role of Osteocel plus as a fusion substrate in minimally invasive instrumented transforaminal lumbar interbody fusion. Clin Neurol Neurosurg 115(7):991–994PubMedCrossRefGoogle Scholar
  2. 2.
    Arealis G, Nikolaou VS (2015) Bone printing: new frontiers in the treatment of bone defects. Injury 46(Suppl 8):S20–S22PubMedCrossRefGoogle Scholar
  3. 3.
    Asanuma H, Meldrum DR, Meldrum KK (2010) Therapeutic applications of mesenchymal stem cells to repair kidney injury. J Urol Jul 184(1):26–33CrossRefGoogle Scholar
  4. 4.
    Aubin JE (1998) Bone stem cells. J Cell Biochem Suppl 30–31:73PubMedCrossRefGoogle Scholar
  5. 5.
    Auffray I, Chevalier S, Froger J, Izac B, Vainchenker W, Gascan H, Coulombel L (1996) Nerve growth factor is involved in the supportive effect by bone marrow-derived stromal cells of the factor-dependent human cell line UT-7. Blood 88:1608–1618PubMedGoogle Scholar
  6. 6.
    Bai L, Caplan A, Lennon D, Miller RH (2007) Mesenchymal stem cell signals regulate neural stem cell fate. Neurochem Res 32:353–362PubMedCrossRefGoogle Scholar
  7. 7.
    Baino F, Tallia F, Novajra G, Minguella J, Montealegre MA, Korkusuz F, Vitale-Brovarone C (2015) Novel bone-like porous glass coatings on Al2O3 prosthetic substrates. In: Key engineering materials, vol 631. Trans Tech Publications, Pfäffikon, pp 236–240Google Scholar
  8. 8.
    Baino F, Minguella J, Kirk N, Montealegre MA, Fiaschi C, Korkusuz F, Orlygsson G, Vitale-Brovarone C (2016) Novel full-ceramic monoblock acetabular cup with a bioactive trabecular coating: design, fabrication and characterization. Ceram Int 42(6):6833–6845CrossRefGoogle Scholar
  9. 9.
    Bakhsheshi-Rad HR, Hamzah E, Ismail AF, Aziz M, Hadisi Z, Kashefian M, Najafinezhad A (2017) Novel nanostructured baghdadite-vancomycin scaffolds: in-vitro drug release, antibacterial activity and biocompatibility. Mater Lett 209:369–372CrossRefGoogle Scholar
  10. 10.
    Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characaterization. Int. J. Biochem Cell Biol 36:568–584CrossRefGoogle Scholar
  11. 11.
    Behnia H, Khojasteh A, Kiani MT, Khoshzaban A, Mashhadi Abbas F, Bashtar M, Dashti SG (2013) Bone regeneration with a combination of nanocrystalline hydroxyapa- tite silica gel, platelet-rich growth factor, and mesenchymal stem cells: a histologic study in rabbit calvaria. Oral Surg Oral Med Oral Pathol Oral Radiol 115(2):7–15CrossRefGoogle Scholar
  12. 12.
    Beier JP, Bitto FF, Lange C, Klumpp D, Arkudas A, Bleiziffer O, Boos A, Horch RE, Kneser U (2010) Myogenic differentiation of mesenchymal stem cells co-cultured with primary myoblasts. Cell Biol Int 35(4):397–406CrossRefGoogle Scholar
  13. 13.
    Bennett SM, Arumugam M, Wilberforce S, Enea D, Rushton N, Zhang XC, Best SM, Cameron RE, Brooks RA (2016) The effect of particle size on the in vivo degradation of poly (d, l-lactide-co-glycolide)/α-tricalcium phosphate micro-and nanocomposites. Acta Biomater 45:340–348PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Best SM, Porter AE, Thian ES, Huang J (2008) Bioceramics: past, present and for the future. J Eur Ceram Soc 28(7):1319–1327CrossRefGoogle Scholar
  15. 15.
    Bhuiyan DB, Middleton JC, Tannenbaum R, Wick TM (2017) Bone regeneration from human mesenchymal stem cells on porous hydroxyapatite-PLGA-collagen bioactive polymer scaffolds. Biomed Mater Eng 28(6):671–685PubMedPubMedCentralGoogle Scholar
  16. 16.
    Bigi A, Boanini E, Capuccini C, Gazzano M (2007) Strontium-substituted hydroxyapatite nanocrystals. Inorg Chim Acta 360(3):1009–1016CrossRefGoogle Scholar
  17. 17.
    Bilousova G, Jun du H, King KB, De Langhe S, Chick WS, Torchia EC, Chow KS, Klemm DJ, Roop DR, Majka SM (2011) Osteoblasts derived from induced pluripotent stem cells form calcified structures in scaffolds both in vitro and in vivo. Stem Cells;29(2):206–216PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Birt MC, Anderson DW, Toby EB, Wang J (2017) Osteomyelitis: recent advances in pathophysiology and therapeutic strategies. J Orthop 14(1):45–52PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Blum C, Brückner T, Ewald A, Ignatius A, Gbureck U (2017) Mg: Ca ratio as regulating factor for osteoclastic in vitro resorption of struvite biocements. Mater Sci Eng C 73:111–119CrossRefGoogle Scholar
  20. 20.
    Bouler JM, Pilet P, Gauthier O, Verron E (2017) Biphasic calcium phosphate ceramics for bone reconstruction: a review of biological response. Acta Biomater 53:1–12PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Boyd NR, Boyd RL, Simo GP, Nisbet DR (2011) Synthetic multi-level matrices for bone regeneration. In: Tissue engineering in regenerative medicine. Humana Press, New York, pp 99–122CrossRefGoogle Scholar
  22. 22.
    Buyuksungur S, Tanir TE, Buyuksungur A, Bektas EI, Kose GT, Yucel D, Beyzadeoglu T, Cetinkaya E, Yenigun C, Tonuk E, Hasirci V, Hasirci N (2017) 3D printed poly (ε-caprolactone) scaffolds modified with hydroxyapatite and poly (propylene fumarate) and their effects on the healing of rabbit femur defects. Biomater Sci 5(10):2144–2158PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Cao Z, Jiang D, Yan L, Wu J (2017) In vitro and in vivo drug release and antibacterial properties of the novel vancomycin-loaded bone-like hydroxyapatite/poly amino acid scaffold. Int J Nanomedicine 12:1841–1851PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Centeno CJ, Schultz JR, Cheever M, Freeman M, Faulkner S, Robinson B, Hanson R (2011) Safety and compli- cations reporting update on the re-implantation of culture- expanded mesenchymal stem cells using autologous platelet lysate technique. Curr Stem Cell Res Ther 6(4):368–378PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Chen X, Li Y, Wang L, Katakowski M, Zhang L, Chen J, Xu Y, Gautam SC, Chopp M (2002) Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22:275–279PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Chopp M, Zhang XH, Li Y, Wang L, Chen J, Lu D (2000) Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation. Neuroreport 11(13):3001–3005PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Chou J, Hao J, Hatoyama H, Ben-Nissan B, Milthorpe B, Otsuka M (2015) Effect of biomimetic zinc-containing tricalcium phosphate (Zn–TCP) on the growth and osteogenic differentiation of mesenchymal stem cells. J Tissue Eng Regen Med 9(7):852–858PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Ciftci E, Köse S, Korkusuz P, Timucin M, Korkusuz F (2014) Boron containing Nano hydroxyapatites (Bn-HAp) stimulate mesenchymal stem cell adhesion, proliferation and differentiation. Key engineering materials (p 631)Google Scholar
  29. 29.
    Dan Y, Liu O, Liu Y, Zhang YY, Li S, Feng XB, Shao XW, Yang C, Yang SH, Hong JB (2016) Development of novel biocomposite scaffold of chitosan-gelatin/Nanohydroxyapatite for potential bone tissue engineering applications. Nanoscale Res Lett 11(1):487PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Dard M, Larjava H (2017, December 20) Hydoxyapatite/beta-tricalcium phosphate biphasic ceramics as regenerative material for the repair of complex bone defects. J Biomed Mater Res Part B Appl Biomater. PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Diaz-Gomez L, García-González CA, Wang J, Yang F, Aznar-Cervantes S, Cenis JL, Reyes R, Degado A, Evora C, Concherio A, Alvarez-Lorenzo C (2017) Biodegradable PCL/fibroin/hydroxyapatite porous scaffolds prepared by supercritical foaming for bone regeneration. Int J Pharm 527(1–2):115–125PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Docheva D, Popov C, Mutschler W, Schieker M (2007) Human mesenchymal stem cells in contact with their environment: surface characteristics and the integrin system. J Cell Mol Med 11(1):21–38PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Dong Y, Chen X, Hong Y (2013) Tissue-engineered bone formation in vivo for artificial laminae of the vertebral arch using beta-tricalcium phosphate bioceramics seeded with mesenchymal stem cells. Spine 38(21):1300–1306CrossRefGoogle Scholar
  34. 34.
    Dziadek M, Stodolak-Zych E, Cholewa-Kowalska K (2017) Biodegradable ceramic-polymer composites for biomedical applications: a review. Mater Sci Eng C 71:1175–1191CrossRefGoogle Scholar
  35. 35.
    Esfahani H, Jose R, Ramakrishna S (2017) Electrospun ceramic nanofiber Mats today: synthesis, properties, and applications. Materials 10(11):1238PubMedCentralCrossRefGoogle Scholar
  36. 36.
    Farokhi M, Mottaghitalab F, Samani S, Shokrgozar MA, Kundu SC, Reis RL, Fatahi Y, Kaplan DL (2017) Silk fibroin/hydroxyapatite composites for bone tissue engineering. Biotechnol AdvGoogle Scholar
  37. 37.
    Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, Gully C, Gassner R, Lepperdinger G (2007) Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell 6(6):745–757PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Forero JC, Roa E, Reyes JG, Acevedo C, Osses N (2017) Development of useful biomaterial for bone tissue engineering by incorporating Nano-copper-zinc alloy (nCuZn) in chitosan/gelatin/Nano-hydroxyapatite (Ch/G/nHAp) scaffold. Materials 10(10):1177PubMedCentralCrossRefGoogle Scholar
  39. 39.
    Fox JM, Chamberlain G, Ashton BA, Middleton J (2007) Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 137(6):491–502PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Friedenstein AJ (1980) Stromal mechanisms of bone marrow: cloning in vitro and retransplantation in vivo. Immunology of bone marrow transplantation. Springer, Berlin/Heidelberg, pp 19–20Google Scholar
  41. 41.
    Gao J, Caplan AI (2003) Mesenchymal stem cells and tissue engineering for orthopaedic surgery. Chir Organi Mov 88(3):305–316PubMedPubMedCentralGoogle Scholar
  42. 42.
    Garrido CA, Lobo SE, Turibio FM, LeGeros RZ (2011) Biphasic calcium phosphate bioceramics for orthopaedic reconstructions: clinical outcomes. Int J Biomater 2011:1–9CrossRefGoogle Scholar
  43. 43.
    Geng Z, Cheng Y, Ma L, Li Z, Cui Z, Zhu S, Yanqin L, Liu Y, Bao H, Li X, Yang X (2017) Nanosized strontium substituted hydroxyapatite prepared from egg shell for enhanced biological properties. J Biomater Appl 32(7):896–905PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Hashemibeni B, Dehghani L, Sadeghi F, Esfandiari E, Gorbani M, Akhavan A, Tahani ST, Bahramian H, Goharian V (2016) Bone repair with differentiated osteoblasts from adipose-derived stem cells in hydroxyapatite/tricalcium phosphate in vivo. Int J Prevent Med 7:62CrossRefGoogle Scholar
  45. 45.
    Haynesworth SE, Baber MA, Caplan AI (1996) Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J Cell Physiol 166(3):585–592CrossRefGoogle Scholar
  46. 46.
    Hench LL (2013) An introduction to bioceramics. World Scientific Publishing Co Inc., SingaporeCrossRefGoogle Scholar
  47. 47.
    Homaeigohar S, Davoudpour Y, Habibi Y, Elbahri M (2017) The electrospun ceramic hollow nanofibers. Nanomaterials 7(11):383PubMedCentralCrossRefGoogle Scholar
  48. 48.
    Horwitz EM, Prockop DJ, Fitzpatrick LA (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nature Med 5:309–313PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Huang Y, Jia X, Bai K, Gong X, Fan Y (2010) Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells. Arch Med Res 41(7):497–505PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Jaiswal S, Kumar RM, Gupta P, Kumaraswamy M, Roy P, Lahiri D (2018) Mechanical, corrosion and biocompatibility behaviour of mg-3Zn-HA biodegradable composites for orthopaedic fixture accessories. J Mech Behav Biomed Mater 78:442–454PubMedCrossRefGoogle Scholar
  51. 51.
    Jaquet K, Krause KT, Denschel J, Faessler P, Nauerz M, Geidel S, Boczor S, Lange C, Stute N, Zander A, Kuck KH (2005) Reduction of myocardial scar size after implantation of mesenchymal stem cells in rats: what is the mechanism? Stem Cells Dev 14(3):299–309PubMedCrossRefGoogle Scholar
  52. 52.
    Jiang JL, Li YF, Fang TL, Zhou J, Li XL, Wang YC, Dong J (2012) Vancomycin-loaded nano-hydroxyapatite pellets to treat MRSA-induced chronic osteomyelitis with bone defect in rabbits. Inflamm Res 61(3):207–215PubMedCrossRefGoogle Scholar
  53. 53.
    Jones JR, Ehrenfried LM, Hench LL (2006) Optimising bioactive glass scaffolds for bone tissue engineering. Biomaterials 27(7):964–973PubMedCrossRefGoogle Scholar
  54. 54.
    Kankilic B, Bilgic E, Korkusuz P, Korkusuz F (2014) Vancomycin containing PLLA/β-TCP controls experimental osteomyelitis in vivo. J Orthopaedic Surg Res 9(1):114CrossRefGoogle Scholar
  55. 55.
    Kankilic B, Köse S, Korkusuz P, Timucin M, Korkusuz F (2016) Mesenchymal stem cells and nano-bioceramics for bone regeneration. Curr Stem Cell Res Ther 11(6):487–493PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Kankilic B, Ciftci Dede E, Korkusuz P, Timucin M, Korkusuz F (2017) Apatites for orthopedic applications. In: Kaur G (ed) Clinical applications of biomaterials. Springer, Cham, pp 65–90CrossRefGoogle Scholar
  57. 57.
    Khang G, Kim SH, Kim MS, Lee HB (2008) Hybrid, composite, and complex biomaterials for scaffolds. In: Principles of regenerative medicine. Elsevier – Academic Press, Amsterdam, pp 636–655CrossRefGoogle Scholar
  58. 58.
    Korkusuz F (2013) Editorial comment: Nanoscience in musculoskeletal medicine. Clin Orthop Relat Res 471:2530–2531PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Korkusuz P, Korkusuz F (2004) Hard tissue-biomaterial interactions. In: Yaszemski MJ, Trantolo DJ, Lewandrowski KU, Hasırcı V, Altobelli DE, Wise DL (eds) Biomaterials in orthopedics. Marcel Dekker, New York, pp 1–40Google Scholar
  60. 60.
    Korkusuz F, Timucin M, Korkusuz P (2014) Nanocrystalline apatite-based biomaterials and stem cells in orthopaedics. In: Ben-Nissan B (ed) Advances in calcium phosphate biomaterials, Springer series in biomaterials science and engineering. Springer, Heidelberg, pp 373–390CrossRefGoogle Scholar
  61. 61.
    Kose S, Aerts Kaya F, Denkbas EB, Korkusuz P, Cetinkaya FD (2016) Evaluation of biocompatibility of random or aligned electrospun polyhydroxybutyrate scaffolds combined with human mesenchymal stem cells. Turk J Biol 40:410–419CrossRefGoogle Scholar
  62. 62.
    Kumar S, Stokes JA III, Dean D, Rogers C, Nyairo E, Thomas V, Mishra MK (2017) Biphasic organo-bioceramic fibrous composite as a biomimetic extracellular matrix for bone tissue regeneration. Front Biosci (Elite Ed) 9:92Google Scholar
  63. 63.
    Labouyrie E, Dubus P, Groppi A, Mahon FX, Ferrer J, Parrens M, Reiffers J, De Mascarel A, Merlio JP (1999) Expression of neurotrophins and their receptors in human bone marrow. Am J Pathol 154:405–415PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Lee DS, Pai Y, Chang S, Kim DH (2016) Microstructure, physical properties, and bone regeneration effect of the nano-sized β-tricalcium phosphate granules. Mater Sci Eng C 58:971–976CrossRefGoogle Scholar
  65. 65.
    Lei Y, Xu Z, Ke Q, Yin W, Chen Y, Zhang C, Guo Y (2017) Strontium hydroxyapatite/chitosan nanohybrid scaffolds with enhanced osteoinductivity for bone tissue engineering. Mater Sci Eng C 72:134–142CrossRefGoogle Scholar
  66. 66.
    Levengood SKL, Zhang M (2014) Chitosan-based scaffolds for bone tissue engineering. J Mater Chem B 2(21):3161–3184PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Li J, Yang L, Guo X, Cui W, Yang S, Wang J, Yanzhen Q, Shao Z, Xu S. (2017) Osteogenesis effects of strontium-substituted hydroxyapatite coatings on true bone ceramic surfaces in vitro and in vivo. Biomedical materials;13(1):015018Google Scholar
  68. 68.
    Liu B, Lun DX (2012) Current application of β-tricalcium phosphate composites in Orthopaedics. Orthop Surg 4(3):139–144PubMedCrossRefGoogle Scholar
  69. 69.
    Lu M, Liao J, Dong J, Wu J, Qiu H, Zhou X, Li J, Jiang D, He TC, Quan Z (2016) An effective treatment of experimental osteomyelitis using the antimicrobial titanium/silver-containing nHP66 (nano-hydroxyapatite/polyamide-66) nanoscaffold biomaterials. Sci Rep 6:39174PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Marques CF, Perera FH, Marote A, Ferreira S, Vieira SI, Olhero S, Miranda P, Ferreira JM (2017) Biphasic calcium phosphate scaffolds fabricated by direct write assembly: mechanical, anti-microbial and osteoblastic properties. J Eur Ceram Soc 37(1):359–368CrossRefGoogle Scholar
  71. 71.
    Melichercik P, Cerovsky V, Nesuta O, Jahoda D, Landor I, Ballay R, Fulin P (2018) Testing the efficacy of antimicrobial peptides in the topical treatment of induced osteomyelitis in rats. Folia Microbiol 63(1):97–104CrossRefGoogle Scholar
  72. 72.
    Mistry S, Roy S, Maitra NJ, Kundu B, Chanda A, Datta S, Joy M (2016) A novel, multi-barrier, drug eluting calcium sulfate/biphasic calcium phosphate biodegradable composite bone cement for treatment of experimental MRSA osteomyelitis in rabbit model. J Control Release 239:169–181PubMedCrossRefGoogle Scholar
  73. 73.
    Modglin VC, Brown RF, Jung SB, Day DE (2013) Cytotoxicity assessment of modified bioactive glasses with MLO-A5 osteogenic cells in vitro. J Mater Sci Mater Med 24(5):1191–1199PubMedCrossRefGoogle Scholar
  74. 74.
    Mohamadyar-Toupkanlou F, Vasheghani-Farahani E, Hanaee-Ahvaz H, Soleimani M, Dodel M, Havasi P, Abdolreza A, Taherzadeh ES (2017) Osteogenic differentiation of MSCs on fibronectin-coated and nHA-modified scaffolds. ASAIO J 63(5):684–691PubMedCrossRefGoogle Scholar
  75. 75.
    Mohsin S, Shams S, Ali Nasir G, Khan M, Javaid Awan S, Khan SN, Riazuddin S (2011) Enhanced hepatic differentiation of mesenchymal stem cells after pretreatment with injured liver tissue. Differentiation 81(1):42–48PubMedCrossRefGoogle Scholar
  76. 76.
    Mondal S, Dorozhkin SV, Pal U. (2017) Recent progress on fabrication and drug delivery applications of nanostructured hydroxyapatite. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology. e1504Google Scholar
  77. 77.
    Moormeier DE, Bayles KW (2017) Staphylococcus aureus biofilm: a complex developmental organism. Mol Microbiol 104(3):365–376PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Murakami S, Miyaji H, Nishida E, Kawamoto K, Miyata S, Takita H, Akasaka T, Fugetsu B, Iwanaga T, Hongo H, Amizuka N (2017) Dose effects of beta-tricalcium phosphate nanoparticles on biocompatibility and bone conductive ability of three-dimensional collagen scaffolds. Dent Mater J 36(5):573–583PubMedCrossRefGoogle Scholar
  79. 79.
    Nandi SK, Bandyopadhyay S, Da P, Samanta I, Mukherjee P, Roy S, Kundu B (2016) Understanding osteomyelitis and its treatment through local drug delivery system. Biotechnol Adv 34(8):1305–1317PubMedCrossRefGoogle Scholar
  80. 80.
    Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE (2006) Mesenchymal stem cells inhibit generation and function of both CD34+−derived and monocyte-derived dendritic cells. J Immunol 177(4):2080–2087PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Nejadnik H, Hui JH, Feng Choong EP, Tai BC, Lee EH (2010) Autologous bone marrow-derived mesenchymal stem cells versus autologous chondrocyte implantation: an observational cohort study. Am J Sports Med 38(6):1110–1116PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    O’Donoghue K, Fisk NM (2004) Fetal stem cells. Best Pract Res Clin Obstet Gynaecol 18(6):853–857PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Ogawa K, Miyaji H, Kato A, Kosen Y, Momose T, Yoshida T, Fugetsu B (2016) Periodontal tissue engineering by nano beta-tricalcium phosphate scaffold and fibroblast growth factor-2 in one-wall infrabony defects of dogs. J Periodontal Res 51(6):758–767PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Pan HB, Zhao XL, Zhang X, Zhang KB, Li LC, Li ZY, Lin KL (2009) Strontium borate glass: potential biomaterial for bone regeneration. J R Soc InterfaceGoogle Scholar
  85. 85.
    Parent M, Magnaudeix A, Delebassée S, Sarre E, Champion E, Viana Trecant M, Damia C (2016) Hydroxyapatite microporous bioceramics as vancomycin reservoir: antibacterial efficiency and biocompatibility investigation. J Biomater Appl 31(4):488–498PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Pittenger MF, Mackay AM, Beck SC (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147CrossRefGoogle Scholar
  87. 87.
    Pizzorno L (2015) Nothing boring about boron. Integr Med Clin J 14(4):35Google Scholar
  88. 88.
    Prabha RD, Kraft DCE, Harkness L, Melsen B, Varma H, Nair PD, Kassem M (2017) Bioactive Nano-fibrous scaffold for vascularized craniofacial bone regeneration. J Tissue Eng Regen Med 12(3):1537–1548CrossRefGoogle Scholar
  89. 89.
    Predoi D, Iconaru SL, Deniaud A, Chevallet M, Michaud-Soret I, Buton N, Prodan AM (2017) Textural, structural and biological evaluation of hydroxyapatite doped with zinc at low concentrations. Materials 10(3):229PubMedCentralCrossRefPubMedGoogle Scholar
  90. 90.
    Quarto R, Mastrogiacom M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M (2001) Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344(5):385–386PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Rabiee SM, Nazparvar N, Azizian M, Vashaee D, Tayebi L (2015) Effect of ion substitution on properties of bioactive glasses: a review. Ceram Int 41(6):7241–7251CrossRefGoogle Scholar
  92. 92.
    Ratnayake JT, Mucalo M, Dias GJ (2017) Substituted hydroxyapatites for bone regeneration: a review of current trends. J Biomed Mater Res B Appl Biomater 105(5):1285–1299PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Ravaglioli A, Krajewski A (2012) Bioceramics: materials properties applications. Springer, ChamGoogle Scholar
  94. 94.
    Ravi ND, Balu R, Sampath Kumar TS (2012) Strontium-substituted calcium deficient hydroxyapatite nanoparticles: synthesis, characterization, and antibacterial properties. J Am Ceram Soc 95(9):2700–2708CrossRefGoogle Scholar
  95. 95.
    Reddy S, Wasnik S, Guha A, Kumar JM, Sinha A, Singh S (2013) Evaluation of nano-biphasic calcium phosphate ceramics for bone tissue engineering applications: in vitro and preliminary in vivo studies. J Biomater Appl 27(5):565–575PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Saidykhan L, Baka MZBA, Rukayadi Y, Kura AU, Latifah SY (2016) Development of nanoantibiotic delivery system using cockle shell-derived aragonite nanoparticles for treatment of osteomyelitis. Int J Nanomedicine 11:661PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Sakar M, Korkusuz P, Demirbilek M, Cetinkaya DU, Arslan S, Denkbas EB, Temucin CM, Bilgic E, Hazer DB, Bozkurt G (2014) The effect of poly(3-hydroxybutyrate-co-3- hydroxyhexanoate) (PHBHHx) and human mesenchymal stem cell (hMSC) on axonal regeneration in experimental sciatic nerve damage. Int J Neurosci 124(9):685–696PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Santos C, Gomes P, Duarte JA, Almeida MM, Costa ME, Fernandes MH (2017) Development of hydroxyapatite nanoparticles loaded with folic acid to induce osteoblastic differentiation. Int J Pharm 516(1):185–195PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Seyfoori A, Imani Fooladi AA, Mahmoodzadeh HH (2017) Calcium phosphate-based nanocomposite carriers for local antibiotic delivery against an osteomyelitis agent. Adv Appl Ceram 116(6):316–324CrossRefGoogle Scholar
  100. 100.
    Shahbazarab Z, Teimouri A, Chermahini AN, Azadi M (2017) Fabrication and characterization of nanobiocomposite scaffold of zein/chitosan/nanohydroxyapatite prepared by freeze-drying method for bone tissue engineering. Int J Biol MacromolGoogle Scholar
  101. 101.
    Song S, Song S, Zhang H, Cuevas J, Sanchez-Ramos J (2007) Comparison of neuron-like cells derived from bone marrow stem cells to those differentiated from adult brain neural stem cells. Stem Cells Dev 16(5):747–756PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Stappenbeck TS, Miyoshi H (2009) The role of stromal stem cells in tissue regeneration and wound repair. Science 324(5935):1666–1669PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Supova M (2015) Substituted hydroxyapatites for biomedical applications: a review. Ceram Int 41(8):9203–9231CrossRefGoogle Scholar
  104. 104.
    Szymonowicz M, Korczynski M, Dobrzynski M, Zawisza K, Mikulewicz M, Karuga-Kuzniewska E, Wiglusz RJ (2017) Cytotoxicity evaluation of high-temperature annealed nanohydroxyapatite in contact with fibroblast cells. Materials 10(6):590PubMedCentralCrossRefGoogle Scholar
  105. 105.
    Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Temenoff JS, Mikos AG (2008) Biomaterials: the intersection of biology and materials science. Pearson/Prentice Hall, Upper Saddle RiverGoogle Scholar
  107. 107.
    Thi Hiep N, Chan Khon H, Dai Hai N, Byong-Taek L, Van Toi V, Thanh HL (2017) Biocompatibility of PCL/PLGA-BCP porous scaffold for bone tissue engineering applications. J Biomater Sci Poly 28(9):864–878CrossRefGoogle Scholar
  108. 108.
    Thomson JA, Itskovitx-Eldor J, Shapiro SS (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147Google Scholar
  109. 109.
    Tong SY, Wang Z, Lim PN, Wang W, San TE (2017) Uniformly-dispersed nanohydroxapatite-reinforced poly (ε-caprolactone) composite films for tendon tissue engineering application. Mater Sci Eng C 70:1149–1155CrossRefGoogle Scholar
  110. 110.
    Tuncay EO, Demirtas TT, Gumusderelioglu M (2017) Microwave-induced production of boron-doped HAp (B-HAp) and B-HAp coated composite scaffolds. J Trace Elem Med Biol 40:72–81PubMedCrossRefGoogle Scholar
  111. 111.
    Uzeda MJ, de Brito Resende RF, Sartoretto SC, Alves ATNN, Granjeiro JM, Calasans-Maia MD (2017) Randomized clinical trial for the biological evaluation of two nanostructured biphasic calcium phosphate biomaterials as a bone substitute. Clin Implant Dent Relat Res 19(5):802–811PubMedCrossRefGoogle Scholar
  112. 112.
    Vallet-Regi M (2001) Ceramics for medical applications. J Chem Soc Dalton Trans 2:97–108CrossRefGoogle Scholar
  113. 113.
    Venkatesan J, Kim SK (2014) Nano-hydroxyapatite composite biomaterials for bone tissue engineering—a review. J Biomed Nanotechnol 10(10):3124–3140PubMedCrossRefGoogle Scholar
  114. 114.
    Viateau V, Manassero M, Sensebe L, Langonne A, Marchat D, Logeart-Avramoglou D, Petite H, Bensidhoum M (2013) Comparative study of the osteogenic ability of four different ceramic constructs in an ectopic large animal model. J Tissue Eng Regen Med 10(3):177–187CrossRefGoogle Scholar
  115. 115.
    Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M (2002) Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthr Cartil 10(3):199–206PubMedCrossRefGoogle Scholar
  116. 116.
    Wakitani S, Nawata M, Tensho K, Okabe T, Machida H, Ohgushi H (2007) Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mes- enchymal cell transplantation: three case reports involving nine defects in five knees. J Tissue Eng Regen Med 1(1):74–79PubMedCrossRefGoogle Scholar
  117. 117.
    Wang B, Liu W, Xing D, Li R, Lv C, Li Y, Lin J (2017a) Injectable nanohydroxyapatite-chitosan-gelatin micro-scaffolds induce regeneration of knee subchondral bone lesions. Sci Rep 7(1):16709PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Wang Q, Chen C, Liu W, He X, Zhou N, Zhang D, Huang W (2017b) Levofloxacin loaded mesoporous silica microspheres/nano-hydroxyapatite/polyurethane composite scaffold for the treatment of chronic osteomyelitis with bone defects. Sci Rep 7:41808PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Weissman IL (2007) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100(1):157–168CrossRefGoogle Scholar
  120. 120.
    Xu F, Shi J, Yu B, Ni W, Wu X, Gu Z (2010) Chemokines mediate mesenchymal stem cell migration toward gliomas in vitro. Oncol Rep 23(6):1561–1567PubMedPubMedCentralGoogle Scholar
  121. 121.
    Xue J, Xie J, Liu W, Xia Y (2017) Electrospun nanofibers: new concepts, materials, and applications. Acc Chem Res 50(8):1976–1987PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Yamanaka S (2012) Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10(6):678–684PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Zhang P, Gan YK, Tang J, Hao YQ, Wang Y, Sun YH, Zhu ZA, Dai KR (2008) Clinical study of lumbar fusion by hybrid construct of stem cells technique and bio- degradable material. Zhonghua Wai Ke Za Zhi (Chinese J Surg) 46(7):493–496Google Scholar
  124. 124.
    Zhang B, Zhang PB, Wang ZL, Lyu ZW, Wu H (2017a) Tissue-engineered composite scaffold of poly (lactide-co-glycolide) and hydroxyapatite nanoparticles seeded with autologous mesenchymal stem cells for bone regeneration. J Zhejiang Univ Sci B 18(11):963–976PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Zhang CL, Huang T, Wu BL, He WX, Liu D (2017b) Stem cells in cancer therapy: opportunities and challenges. Oncotarget 8(43):75756–75766PubMedPubMedCentralGoogle Scholar
  126. 126.
    Zhang S, Jiang G, Prabhakaran MP, Qin X, Ramakrishna S (2017c) Evaluation of electrospun biomimetic substrate surface-decorated with nanohydroxyapatite precipitation for osteoblasts behavior. Mater Sci Eng C 79:687–696CrossRefGoogle Scholar
  127. 127.
    Zhu H, Guo D, Qi W, Xu K (2017) Development of Sr-incorporated biphasic calcium phosphate bone cement. Biomed Mater 12(1):015016PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Zurita M, Vaquero J (2006) Bone marrow stromal cells can achieve cure of chronic paraplegic rats: functional and morphological outcome one year after transplantation. Neurosci Lett 402(1–2):51–56PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Sevil Köse
    • 1
  • Berna Kankilic
    • 2
  • Merve Gizer
    • 3
  • Eda Ciftci Dede
    • 3
  • Erdal Bayramli
    • 4
  • Petek Korkusuz
    • 5
  • Feza Korkusuz
    • 6
  1. 1.Faculty of Health Sciences, Department of Nutrition and DieteticsAtilim UniversityAnkaraTurkey
  2. 2.Head of Certification, Directorate of DirectivesTurkish Standards InstitutionAnkaraTurkey
  3. 3.Department of BioengineeringHacettepe UniversityAnkaraTurkey
  4. 4.Department of ChemistryMiddle East Technical UniversityAnkaraTurkey
  5. 5.Department of Histology and EmbryologyFaculty of Medicine, Hacettepe UniversityAnkaraTurkey
  6. 6.Department of Sports MedicineFaculty of Medicine, Hacettepe UniversityAnkaraTurkey

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