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Stem cell research & therapy2018; 9(1); 60; doi: 10.1186/s13287-018-0790-8

Polymer-mineral scaffold augments in vivo equine multipotent stromal cell osteogenesis.

Abstract: Use of bioscaffolds to direct osteogenic differentiation of adult multipotent stromal cells (MSCs) without exogenous proteins is a contemporary approach to bone regeneration. Identification of in vivo osteogenic contributions of exogenous MSCs on bioscaffolds after long-term implantation is vital to understanding cell persistence and effect duration. This study was designed to quantify in vivo equine MSC osteogenesis on synthetic polymer scaffolds with distinct mineral combinations 9 weeks after implantation in a murine model. Cryopreserved, passage (P)1, equine bone marrow-derived MSCs (BMSC) and adipose tissue-derived MSCs (ASC) were culture expanded to P3 and immunophenotyped with flow cytometry. They were then loaded by spinner flask on to scaffolds composed of tricalcium phosphate (TCP)/hydroxyapatite (HA) (40:60; HT), polyethylene glycol (PEG)/poly-L-lactic acid (PLLA) (60:40; GA), or PEG/PLLA/TCP/HA (36:24:24:16; GT). Scaffolds with and without cells were maintained in static culture for up to 21 days or implanted subcutaneously in athymic mice that were radiographed every 3 weeks up to 9 weeks. In vitro cell viability and proliferation were determined. Explant composition (double-stranded (ds)DNA, collagen, sulfated glycosaminoglycan (sGAG), protein), equine and murine osteogenic target gene expression, microcomputed tomography (μCT) mineralization, and light microscopic structure were assessed. The ASC and BMSC number increased significantly in HT constructs between 7 and 21 days of culture, and BMSCs increased similarly in GT constructs. Radiographic opacity increased with time in GT-BMSC constructs. Extracellular matrix (ECM) components and dsDNA increased significantly in GT compared to HT constructs. Equine and murine osteogenic gene expression was highest in BMSC constructs with mineral-containing scaffolds. The HT constructs with either cell type had the highest mineral deposition based on μCT. Regardless of composition, scaffolds with cells had more ECM than those without, and osteoid was apparent in all BMSC constructs. In this study, both exogenous and host MSCs appear to contribute to in vivo osteogenesis. Addition of mineral to polymer scaffolds enhances equine MSC osteogenesis over polymer alone, but pure mineral scaffold provides superior osteogenic support. These results emphasize the need for bioscaffolds that provide customized osteogenic direction of both exo- and endogenous MSCs for the best regenerative potential.
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Publication Date: 2018-03-09 PubMed ID: 29523214PubMed Central: PMC5845133DOI: 10.1186/s13287-018-0790-8Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research study investigates the osteogenesis or bone development potential of horse-derived multipotent stromal cells (MSCs) when combined with synthetic polymer scaffolds. The study further explores the effects of different mineral combinations in the scaffolds on cell proliferation and bone formation.

Objectives and Setup of the Research

  • The study aimed to quantify the osteogenesis capability of equine MSCs after being implanted on bioscaffolds with different mineral combinations in a murine (mouse) model for a period of 9 weeks.
  • The researchers used cryopreserved, equine bone marrow-derived MSCs (BMSC) and adipose tissue-derived MSCs (ASC) and put them through culture expansion.
  • The cells were then loaded onto scaffolds composed of different proportions of tricalcium phosphate (TCP), hydroxyapatite (HA), polyethylene glycol (PEG), and poly-L-lactic acid (PLLA).
  • The scaffolds with and without the cells were maintained in static culture for up to 21 days or implanted subcutaneously in athymic mice for a period of 9 weeks.

Results of the Experiment

  • The study found that the number of ASC and BMSC cells significantly increased in constructs with TCP/HA mineral combination during the 21-day culture period.
  • The same increase in BMSCs was observed in constructs where PEG/PLLA/TCP/HA combination was used.
  • An increase in radiographic opacity was also observed over time in constructs with the latter mineral combination filled with BMSCs, suggesting an enhanced osteogenesis or bone formation.
  • Extracellular matrix (ECM) components and double-stranded DNA showed significant increases in polymer scaffolds combined with mineral than in pure mineral constructs (TCP/HA).
  • Highest gene expression indicating bone formation was found in BMSC constructs where the scaffolds included minerals.
  • The pure mineral scaffolds with either cell type had the highest mineral deposition according to microcomputed tomography.
  • Regardless of the composition of the scaffold, those with cells had more ECM than those without, and osteoid or new bone was evident in all BMSC constructs.

Implications of the Research

  • The study reveals that both exogenous (externally applied) and host MSCs contribute to bone formation when implanted on synthetic polymer scaffolds.
  • Adding mineral to polymer scaffolds improves the potential for bone development by the MSCs compared to polymer alone.
  • However, scaffolds composed purely of mineral exhibited the best support for fostering bone development.
  • The results highlight the need for bioscaffolds that cater to the osteogenic requirements of both externally applied and naturally occurring MSCs for optimal regenerative outcomes.

Cite This Article

APA
Duan W, Chen C, Haque M, Hayes D, Lopez MJ. (2018). Polymer-mineral scaffold augments in vivo equine multipotent stromal cell osteogenesis. Stem Cell Res Ther, 9(1), 60. https://doi.org/10.1186/s13287-018-0790-8

Publication

Stem cell research & therapy
ISSN: 1757-6512
NlmUniqueID: 101527581
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 60
PII: 60

Researcher Affiliations

Duan, Wei
  • Laboratory for Equine and Comparative Orthopedic Research, Louisiana State University, Baton Rouge, LA, USA.
Chen, Cong
  • Department of Biomedical Engineering, Pennsylvania State University, University Park, PA, USA.
Haque, Masudul
  • Laboratory for Equine and Comparative Orthopedic Research, Louisiana State University, Baton Rouge, LA, USA.
Hayes, Daniel
  • Department of Biomedical Engineering, Pennsylvania State University, University Park, PA, USA.
Lopez, Mandi J
  • Laboratory for Equine and Comparative Orthopedic Research, Louisiana State University, Baton Rouge, LA, USA. mlopez@lsu.edu.

MeSH Terms

  • Adipose Tissue / cytology
  • Animals
  • Cells, Cultured
  • Horses
  • Hydroxyapatites / chemistry
  • Lactates / chemistry
  • Male
  • Mesenchymal Stem Cell Transplantation / methods
  • Mesenchymal Stem Cells / cytology
  • Mice
  • Osteogenesis
  • Pluripotent Stem Cells / cytology
  • Polyethylene Glycols / chemistry
  • Tissue Scaffolds / chemistry

Conflict of Interest Statement

ETHICS APPROVAL: All animal procedures were approved by the Louisiana State University Institutional Animal Care and Use Committee prior to study initiation (protocols #13-050 and 07-049). CONSENT FOR PUBLICATION: Not applicable. COMPETING INTERESTS: The authors declare that they have no competing interests. PUBLISHER’S NOTE: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

This article includes 88 references
  1. Laurencin C, Khan Y, El-Amin SF. Bone graft substitutes.. Expert Rev Med Devices 2006 Jan;3(1):49-57.
    pubmed: 16359252doi: 10.1586/17434440.3.1.49google scholar: lookup
  2. Matsushima A, Kotobuki N, Tadokoro M, Kawate K, Yajima H, Takakura Y, Ohgushi H. In vivo osteogenic capability of human mesenchymal cells cultured on hydroxyapatite and on beta-tricalcium phosphate.. Artif Organs 2009 Jun;33(6):474-81.
    doi: 10.1111/j.1525-1594.2009.00749.xpubmed: 19473144google scholar: lookup
  3. Wu S, Liu X, Yeung KW, Liu C, Yang X. Biomimetic porous scaffolds for bone tissue engineering. Mater Sci Eng R Rep 2014;80:1–36.
    doi: 10.1016/j.mser.2014.04.001google scholar: lookup
  4. García-Gareta E, Coathup MJ, Blunn GW. Osteoinduction of bone grafting materials for bone repair and regeneration.. Bone 2015 Dec;81:112-121.
    doi: 10.1016/j.bone.2015.07.007pubmed: 26163110google scholar: lookup
  5. Vidal MA, Kilroy GE, Johnson JR, Lopez MJ, Moore RM, Gimble JM. Cell growth characteristics and differentiation frequency of adherent equine bone marrow-derived mesenchymal stromal cells: adipogenic and osteogenic capacity.. Vet Surg 2006 Oct;35(7):601-10.
    doi: 10.1111/j.1532-950X.2006.00197.xpubmed: 17026544google scholar: lookup
  6. Vidal MA, Kilroy GE, Lopez MJ, Johnson JR, Moore RM, Gimble JM. Characterization of equine adipose tissue-derived stromal cells: adipogenic and osteogenic capacity and comparison with bone marrow-derived mesenchymal stromal cells.. Vet Surg 2007 Oct;36(7):613-22.
    doi: 10.1111/j.1532-950X.2007.00313.xpubmed: 17894587google scholar: lookup
  7. Im GI, Shin YW, Lee KB. Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells?. Osteoarthritis Cartilage 2005 Oct;13(10):845-53.
    doi: 10.1016/j.joca.2005.05.005pubmed: 16129630google scholar: lookup
  8. Xie L, Zhang N, Marsano A, Vunjak-Novakovic G, Zhang Y, Lopez MJ. In vitro mesenchymal trilineage differentiation and extracellular matrix production by adipose and bone marrow derived adult equine multipotent stromal cells on a collagen scaffold.. Stem Cell Rev Rep 2013 Dec;9(6):858-72.
    doi: 10.1007/s12015-013-9456-1pmc: PMC3834181pubmed: 23892935google scholar: lookup
  9. Stevens MM. Biomaterials for bone tissue engineering. Mater Today 2008;11:18–25.
    doi: 10.1016/S1369-7021(08)70086-5google scholar: lookup
  10. Bose S, Roy M, Bandyopadhyay A. Recent advances in bone tissue engineering scaffolds.. Trends Biotechnol 2012 Oct;30(10):546-54.
    doi: 10.1016/j.tibtech.2012.07.005pmc: PMC3448860pubmed: 22939815google scholar: lookup
  11. Simmons CA, Alsberg E, Hsiong S, Kim WJ, Mooney DJ. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells.. Bone 2004 Aug;35(2):562-9.
    doi: 10.1016/j.bone.2004.02.027pubmed: 15268909google scholar: lookup
  12. LeGeros RZ. Calcium phosphate-based osteoinductive materials.. Chem Rev 2008 Nov;108(11):4742-53.
    doi: 10.1021/cr800427gpubmed: 19006399google scholar: lookup
  13. Gan Y, Dai K, Zhang P, Tang T, Zhu Z, Lu J. The clinical use of enriched bone marrow stem cells combined with porous beta-tricalcium phosphate in posterior spinal fusion.. Biomaterials 2008 Oct;29(29):3973-82.
    doi: 10.1016/j.biomaterials.2008.06.026pubmed: 18639333google scholar: lookup
  14. McCullen SD, Zhu Y, Bernacki SH, Narayan RJ, Pourdeyhimi B, Gorga RE, Loboa EG. Electrospun composite poly(L-lactic acid)/tricalcium phosphate scaffolds induce proliferation and osteogenic differentiation of human adipose-derived stem cells.. Biomed Mater 2009 Jun;4(3):035002.
    doi: 10.1088/1748-6041/4/3/035002pubmed: 19390143google scholar: lookup
  15. Dorozhkin SV. Calcium orthophosphate bioceramics. Ceram Int 2015;41:13913–13966.
    doi: 10.1016/j.ceramint.2015.08.004google scholar: lookup
  16. Hu Y, Zhang C, Zhang S, Xiong Z, Xu J. Development of a porous poly(L-lactic acid)/hydroxyapatite/collagen scaffold as a BMP delivery system and its use in healing canine segmental bone defect.. J Biomed Mater Res A 2003 Nov 1;67(2):591-8.
    doi: 10.1002/jbm.a.10070pubmed: 14566802google scholar: lookup
  17. Schellekens H, Hennink WE, Brinks V. The immunogenicity of polyethylene glycol: facts and fiction.. Pharm Res 2013 Jul;30(7):1729-34.
    doi: 10.1007/s11095-013-1067-7pubmed: 23673554google scholar: lookup
  18. Tong R, Gabrielson NP, Fan TM, Cheng J. Polymeric Nanomedicines Based on Poly(lactide) and Poly(lactide-co-glycolide).. Curr Opin Solid State Mater Sci 2012 Dec 1;16(6):323-332.
    doi: 10.1016/j.cossms.2013.01.001pmc: PMC3728009pubmed: 23914135google scholar: lookup
  19. Fitzgerald R, Vleggaar D. Using poly-L-lactic acid (PLLA) to mimic volume in multiple tissue layers.. J Drugs Dermatol 2009 Oct;8(10 Suppl):s5-14.
    pubmed: 19891116
  20. Liu X, Ma PX. Polymeric scaffolds for bone tissue engineering.. Ann Biomed Eng 2004 Mar;32(3):477-86.
    doi: 10.1023/B:ABME.0000017544.36001.8epubmed: 15095822google scholar: lookup
  21. Danoux CB, Barbieri D, Yuan H, de Bruijn JD, van Blitterswijk CA, Habibovic P. In vitro and in vivo bioactivity assessment of a polylactic acid/hydroxyapatite composite for bone regeneration.. Biomatter 2014;4:e27664.
    doi: 10.4161/biom.27664pmc: PMC3961484pubmed: 24441389google scholar: lookup
  22. Barbieri D, Yuan H, Luo X, Farè S, Grijpma DW, de Bruijn JD. Influence of polymer molecular weight in osteoinductive composites for bone tissue regeneration.. Acta Biomater 2013 Dec;9(12):9401-13.
    doi: 10.1016/j.actbio.2013.07.026pubmed: 23917043google scholar: lookup
  23. Shah SS, Zhu KJ, Pitt CG. Poly-DL-lactic acid: polyethylene glycol block copolymers. The influence of polyethylene glycol on the degradation of poly-DL-lactic acid.. J Biomater Sci Polym Ed 1994;5(5):421-31.
    doi: 10.1163/156856294X00121pubmed: 8038137google scholar: lookup
  24. Woo KM, Seo J, Zhang R, Ma PX. Suppression of apoptosis by enhanced protein adsorption on polymer/hydroxyapatite composite scaffolds.. Biomaterials 2007 Jun;28(16):2622-30.
    doi: 10.1016/j.biomaterials.2007.02.004pmc: PMC1934407pubmed: 17320948google scholar: lookup
  25. Ma PX, Zhang R, Xiao G, Franceschi R. Engineering new bone tissue in vitro on highly porous poly(alpha-hydroxyl acids)/hydroxyapatite composite scaffolds.. J Biomed Mater Res 2001 Feb;54(2):284-93.
    doi: 10.1002/1097-4636(200102)54:2<284::AID-JBM16>3.0.CO;2-Wpubmed: 11093189google scholar: lookup
  26. Milner PI, Clegg PD, Stewart MC. Stem cell-based therapies for bone repair.. Vet Clin North Am Equine Pract 2011 Aug;27(2):299-314.
    doi: 10.1016/j.cveq.2011.05.002pubmed: 21872760google scholar: lookup
  27. Sittinger M, Hutmacher DW, Risbud MV. Current strategies for cell delivery in cartilage and bone regeneration.. Curr Opin Biotechnol 2004 Oct;15(5):411-8.
    doi: 10.1016/j.copbio.2004.08.010pubmed: 15464370google scholar: lookup
  28. Martin I, Wendt D, Heberer M. The role of bioreactors in tissue engineering.. Trends Biotechnol 2004 Feb;22(2):80-6.
    doi: 10.1016/j.tibtech.2003.12.001pubmed: 14757042google scholar: lookup
  29. Grottkau BE, Lin Y. Osteogenesis of Adipose-Derived Stem Cells.. Bone Res 2013 Jun;1(2):133-45.
    doi: 10.4248/BR201302003pmc: PMC4472098pubmed: 26273498google scholar: lookup
  30. Plunkett N, O'Brien FJ. Bioreactors in tissue engineering.. Technol Health Care 2011;19(1):55-69.
    pubmed: 21248413doi: 10.3233/thc-2011-0605google scholar: lookup
  31. Sladkova M, de Peppo GM. Bioreactor systems for human bone tissue engineering. Processes 2014;2:494–525.
    doi: 10.3390/pr2020494google scholar: lookup
  32. Arnsdorf EJ, Tummala P, Kwon RY, Jacobs CR. Mechanically induced osteogenic differentiation--the role of RhoA, ROCKII and cytoskeletal dynamics.. J Cell Sci 2009 Feb 15;122(Pt 4):546-53.
    doi: 10.1242/jcs.036293pmc: PMC2714434pubmed: 19174467google scholar: lookup
  33. Arnsdorf EJ, Tummala P, Jacobs CR. Non-canonical Wnt signaling and N-cadherin related beta-catenin signaling play a role in mechanically induced osteogenic cell fate.. PLoS One 2009;4(4):e5388.
    doi: 10.1371/journal.pone.0005388pmc: PMC2670536pubmed: 19401766google scholar: lookup
  34. Bara JJ, McCarthy HE, Humphrey E, Johnson WE, Roberts S. Bone marrow-derived mesenchymal stem cells become antiangiogenic when chondrogenically or osteogenically differentiated: implications for bone and cartilage tissue engineering.. Tissue Eng Part A 2014 Jan;20(1-2):147-59.
    doi: 10.1089/ten.tea.2013.0196pubmed: 23895198google scholar: lookup
  35. Lopez MJ, Jarazo J. State of the art: stem cells in equine regenerative medicine.. Equine Vet J 2015 Mar;47(2):145-54.
    doi: 10.1111/evj.12311pubmed: 24957845google scholar: lookup
  36. Koch TG, Berg LC, Betts DH. Current and future regenerative medicine - principles, concepts, and therapeutic use of stem cell therapy and tissue engineering in equine medicine.. Can Vet J 2009 Feb;50(2):155-65.
    pmc: PMC2629419pubmed: 19412395
  37. Taylor SE, Smith RK, Clegg PD. Mesenchymal stem cell therapy in equine musculoskeletal disease: scientific fact or clinical fiction?. Equine Vet J 2007 Mar;39(2):172-80.
    doi: 10.2746/042516407X180868pubmed: 17378447google scholar: lookup
  38. Smoak M, Hogan K, Kriegh L, Chen C, Terrell LB, Qureshi AT, Monroe WT, Gimble JM, Hayes DJ. Modulation of mesenchymal stem cell behavior by nano-and micro-sized β-tricalcium phosphate particles in suspension and composite structures. J Nanopart Res 2015;17:182.
    doi: 10.1007/s11051-015-2985-6google scholar: lookup
  39. Lee JE, Kim KE, Kwon IC, Ahn HJ, Lee SH, Cho H, Kim HJ, Seong SC, Lee MC. Effects of the controlled-released TGF-beta 1 from chitosan microspheres on chondrocytes cultured in a collagen/chitosan/glycosaminoglycan scaffold.. Biomaterials 2004 Aug;25(18):4163-73.
    doi: 10.1016/j.biomaterials.2003.10.057pubmed: 15046906google scholar: lookup
  40. Vidal MA, Robinson SO, Lopez MJ, Paulsen DB, Borkhsenious O, Johnson JR, Moore RM, Gimble JM. Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow.. Vet Surg 2008 Dec;37(8):713-24.
    doi: 10.1111/j.1532-950X.2008.00462.xpmc: PMC2746327pubmed: 19121166google scholar: lookup
  41. Spencer ND, Chun R, Vidal MA, Gimble JM, Lopez MJ. In vitro expansion and differentiation of fresh and revitalized adult canine bone marrow-derived and adipose tissue-derived stromal cells.. Vet J 2012 Feb;191(2):231-9.
    doi: 10.1016/j.tvjl.2010.12.030pmc: PMC3107397pubmed: 21315625google scholar: lookup
  42. Stegemann H, Stalder K. Determination of hydroxyproline.. Clin Chim Acta 1967 Nov;18(2):267-73.
    doi: 10.1016/0009-8981(67)90167-2pubmed: 4864804google scholar: lookup
  43. Enobakhare BO, Bader DL, Lee DA. Quantification of sulfated glycosaminoglycans in chondrocyte/alginate cultures, by use of 1,9-dimethylmethylene blue.. Anal Biochem 1996 Dec 1;243(1):189-91.
    doi: 10.1006/abio.1996.0502pubmed: 8954546google scholar: lookup
  44. Hartree EF. Determination of protein: a modification of the Lowry method that gives a linear photometric response.. Anal Biochem 1972 Aug;48(2):422-7.
    doi: 10.1016/0003-2697(72)90094-2pubmed: 4115981google scholar: lookup
  45. Zhang P, Hong Z, Yu T, Chen X, Jing X. In vivo mineralization and osteogenesis of nanocomposite scaffold of poly(lactide-co-glycolide) and hydroxyapatite surface-grafted with poly(L-lactide).. Biomaterials 2009 Jan;30(1):58-70.
    doi: 10.1016/j.biomaterials.2008.08.041pubmed: 18838160google scholar: lookup
  46. Suchanek W, Yoshimura M. Processing and properties of hydroxyapatite-based biomaterials for use as hard tissue replacement implants. J Mater Res 1998;13:94–117.
    doi: 10.1557/JMR.1998.0015google scholar: lookup
  47. Nunamaker D. On bone and fracture treatment in the horse, Proceedings of the 48th of the American Association of Equine Practitionners. 2002;9–101
  48. O'Malley MJ, Sayres SC, Saleem O, Levine D, Roberts M, Deland JT, Ellis S. Morbidity and complications following percutaneous calcaneal autograft bone harvest.. Foot Ankle Int 2014 Jan;35(1):30-7.
    pubmed: 24318626doi: 10.1177/1071100713511806google scholar: lookup
  49. Bohner M, Galea L, Doebelin N. Calcium phosphate bone graft substitutes: Failures and hopes. J Eur Ceram Soc 2012;32(11):2663–2671.
  50. Yuan H, de Bruijn JD, Zhang X, van Blitterswijk CA, de Groot K. Bone induction by porous glass ceramic made from Bioglass (45S5).. J Biomed Mater Res 2001 May 1;58(3):270-6.
    pubmed: 11319740doi: 10.1002/1097-4636(2001)58:3<270::aid-jbm1016>3.0.co;2-2google scholar: lookup
  51. Matassi F, Botti A, Sirleo L, Carulli C, Innocenti M. Porous metal for orthopedics implants.. Clin Cases Miner Bone Metab 2013 May;10(2):111-5.
    pmc: PMC3796997pubmed: 24133527
  52. Borjesson DL, Peroni JF. The regenerative medicine laboratory: facilitating stem cell therapy for equine disease.. Clin Lab Med 2011 Mar;31(1):109-23.
    pubmed: 21295725doi: 10.1016/j.cll.2010.12.001google scholar: lookup
  53. Oryan A, Alidadi S, Moshiri A, Maffulli N. Bone regenerative medicine: classic options, novel strategies, and future directions.. J Orthop Surg Res 2014 Mar 17;9(1):18.
    pmc: PMC3995444pubmed: 24628910doi: 10.1186/1749-799x-9-18google scholar: lookup
  54. Progatzky F, Dallman MJ, Lo Celso C. From seeing to believing: labelling strategies for in vivo cell-tracking experiments.. Interface Focus 2013 Jun 6;3(3):20130001.
    pmc: PMC3638420pubmed: 23853708doi: 10.1098/rsfs.2013.0001google scholar: lookup
  55. Pizzute T, Lynch K, Pei M. Impact of tissue-specific stem cells on lineage-specific differentiation: a focus on the musculoskeletal system.. Stem Cell Rev Rep 2015 Feb;11(1):119-32.
    pmc: PMC4326629pubmed: 25113801doi: 10.1007/s12015-014-9546-8google scholar: lookup
  56. Monaco E, Bionaz M, Rodriguez-Zas S, Hurley WL, Wheeler MB. Transcriptomics comparison between porcine adipose and bone marrow mesenchymal stem cells during in vitro osteogenic and adipogenic differentiation.. PLoS One 2012;7(3):e32481.
    pmc: PMC3296722pubmed: 22412878doi: 10.1371/journal.pone.0032481google scholar: lookup
  57. Zhang X, Guo J, Zhou Y, Wu G. The roles of bone morphogenetic proteins and their signaling in the osteogenesis of adipose-derived stem cells.. Tissue Eng Part B Rev 2014 Feb;20(1):84-92.
    pmc: PMC3922312pubmed: 23758605doi: 10.1089/ten.teb.2013.0204google scholar: lookup
  58. Zuk P. Adipose-derived stem cells in tissue regeneration: a review. ISRN Stem Cells 2013.
  59. David Roodman G. Role of stromal-derived cytokines and growth factors in bone metastasis.. Cancer 2003 Feb 1;97(3 Suppl):733-8.
    pubmed: 12548570doi: 10.1002/cncr.11148google scholar: lookup
  60. Festuccia C, Bologna M, Gravina GL, Guerra F, Angelucci A, Villanova I, Millimaggi D, Teti A. Osteoblast conditioned media contain TGF-beta1 and modulate the migration of prostate tumor cells and their interactions with extracellular matrix components.. Int J Cancer 1999 May 5;81(3):395-403.
    pubmed: 10209954doi: 10.1002/(sici)1097-0215(19990505)81:3<395::aid-ijc13>3.0.co;2-vgoogle scholar: lookup
  61. Kim KI, Park S, Im GI. Osteogenic differentiation and angiogenesis with cocultured adipose-derived stromal cells and bone marrow stromal cells.. Biomaterials 2014 Jun;35(17):4792-804.
    pubmed: 24655782doi: 10.1016/j.biomaterials.2014.02.048google scholar: lookup
  62. Roohani-Esfahani SI, Nouri-Khorasani S, Lu Z, Appleyard R, Zreiqat H. The influence hydroxyapatite nanoparticle shape and size on the properties of biphasic calcium phosphate scaffolds coated with hydroxyapatite-PCL composites.. Biomaterials 2010 Jul;31(21):5498-509.
    pubmed: 20398935doi: 10.1016/j.biomaterials.2010.03.058google scholar: lookup
  63. Samavedi S, Whittington AR, Goldstein AS. Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior.. Acta Biomater 2013 Sep;9(9):8037-45.
    pubmed: 23791671doi: 10.1016/j.actbio.2013.06.014google scholar: lookup
  64. Polini A, Pisignano D, Parodi M, Quarto R, Scaglione S. Osteoinduction of human mesenchymal stem cells by bioactive composite scaffolds without supplemental osteogenic growth factors.. PLoS One 2011;6(10):e26211.
    pmc: PMC3192176pubmed: 22022571doi: 10.1371/journal.pone.0026211google scholar: lookup
  65. Fathi M, Hanifi A, Mortazavi V. Preparation and bioactivity evaluation of bone-like hydroxyapatite nanopowder. J Mater Process Technol 2008;202(1):536-542.
  66. Inzana JA, Olvera D, Fuller SM, Kelly JP, Graeve OA, Schwarz EM, Kates SL, Awad HA. 3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration.. Biomaterials 2014 Apr;35(13):4026-34.
    pmc: PMC4065717pubmed: 24529628doi: 10.1016/j.biomaterials.2014.01.064google scholar: lookup
  67. Sikavitsas VI, Bancroft GN, Mikos AG. Formation of three-dimensional cell/polymer constructs for bone tissue engineering in a spinner flask and a rotating wall vessel bioreactor.. J Biomed Mater Res 2002 Oct;62(1):136-48.
    pubmed: 12124795doi: 10.1002/jbm.10150google scholar: lookup
  68. Stiehler M, Bünger C, Baatrup A, Lind M, Kassem M, Mygind T. Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells.. J Biomed Mater Res A 2009 Apr;89(1):96-107.
    pubmed: 18431785doi: 10.1002/jbm.a.31967google scholar: lookup
  69. Hutmacher DW. Scaffolds in tissue engineering bone and cartilage.. Biomaterials 2000 Dec;21(24):2529-43.
    pubmed: 11071603doi: 10.1016/s0142-9612(00)00121-6google scholar: lookup
  70. Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges.. Crit Rev Biomed Eng 2012;40(5):363-408.
    pmc: PMC3766369pubmed: 23339648doi: 10.1615/critrevbiomedeng.v40.i5.10google scholar: lookup
  71. Laschke MW, Harder Y, Amon M, Martin I, Farhadi J, Ring A, Torio-Padron N, Schramm R, Rücker M, Junker D, Häufel JM, Carvalho C, Heberer M, Germann G, Vollmar B, Menger MD. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes.. Tissue Eng 2006 Aug;12(8):2093-104.
    pubmed: 16968151doi: 10.1089/ten.2006.12.2093google scholar: lookup
  72. Deligianni DD, Katsala ND, Koutsoukos PG, Missirlis YF. Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength.. Biomaterials 2001 Jan;22(1):87-96.
    pubmed: 11085388doi: 10.1016/s0142-9612(00)00174-5google scholar: lookup
  73. Dawson E, Mapili G, Erickson K, Taqvi S, Roy K. Biomaterials for stem cell differentiation.. Adv Drug Deliv Rev 2008 Jan 14;60(2):215-28.
    pubmed: 17997187doi: 10.1016/j.addr.2007.08.037google scholar: lookup
  74. Bonjour JP. Calcium and phosphate: a duet of ions playing for bone health.. J Am Coll Nutr 2011 Oct;30(5 Suppl 1):438S-48S.
    pubmed: 22081690doi: 10.1080/07315724.2011.10719988google scholar: lookup
  75. Kruyt MC, Dhert WJ, Oner FC, van Blitterswijk CA, Verbout AJ, de Bruijn JD. Analysis of ectopic and orthotopic bone formation in cell-based tissue-engineered constructs in goats.. Biomaterials 2007 Apr;28(10):1798-805.
    pubmed: 17182096doi: 10.1016/j.biomaterials.2006.11.038google scholar: lookup
  76. Scott MA, Levi B, Askarinam A, Nguyen A, Rackohn T, Ting K, Soo C, James AW. Brief review of models of ectopic bone formation.. Stem Cells Dev 2012 Mar 20;21(5):655-67.
    pmc: PMC3295855pubmed: 22085228doi: 10.1089/scd.2011.0517google scholar: lookup
  77. Zhang Y, Li X, Chihara T, Mizoguchi T, Hori A, Udagawa N, Nakamura H, Hasegawa H, Taguchi A, Shinohara A, Kagami H. Comparing immunocompetent and immunodeficient mice as animal models for bone tissue engineering.. Oral Dis 2015 Jul;21(5):583-92.
    pubmed: 25648203doi: 10.1111/odi.12319google scholar: lookup
  78. Higuera GA, Hendriks JA, van Dalum J, Wu L, Schotel R, Moreira-Teixeira L, van den Doel M, Leijten JC, Riesle J, Karperien M, van Blitterswijk CA, Moroni L. In vivo screening of extracellular matrix components produced under multiple experimental conditions implanted in one animal.. Integr Biol (Camb) 2013 Jun;5(6):889-98.
    pubmed: 23652478doi: 10.1039/c3ib40023agoogle scholar: lookup
  79. Thompson EM, Matsiko A, Farrell E, Kelly DJ, O'Brien FJ. Recapitulating endochondral ossification: a promising route to in vivo bone regeneration.. J Tissue Eng Regen Med 2015 Aug;9(8):889-902.
    pubmed: 24916192doi: 10.1002/term.1918google scholar: lookup
  80. Cornell CN, Lane JM. Newest factors in fracture healing.. Clin Orthop Relat Res 1992 Apr;(277):297-311.
    pubmed: 1555354
  81. Rizzi SC, Heath DJ, Coombes AG, Bock N, Textor M, Downes S. Biodegradable polymer/hydroxyapatite composites: surface analysis and initial attachment of human osteoblasts.. J Biomed Mater Res 2001 Jun 15;55(4):475-86.
    pubmed: 11288075doi: 10.1002/1097-4636(20010615)55:4<475::aid-jbm1039>3.0.co;2-qgoogle scholar: lookup
  82. Peng F, Yu X, Wei M. In vitro cell performance on hydroxyapatite particles/poly(L-lactic acid) nanofibrous scaffolds with an excellent particle along nanofiber orientation.. Acta Biomater 2011 Jun;7(6):2585-92.
    pubmed: 21333762doi: 10.1016/j.actbio.2011.02.021google scholar: lookup
  83. Montjovent MO, Mathieu L, Schmoekel H, Mark S, Bourban PE, Zambelli PY, Laurent-Applegate LA, Pioletti DP. Repair of critical size defects in the rat cranium using ceramic-reinforced PLA scaffolds obtained by supercritical gas foaming.. J Biomed Mater Res A 2007 Oct;83(1):41-51.
    pubmed: 17377968doi: 10.1002/jbm.a.31208google scholar: lookup
  84. Montjovent MO, Mathieu L, Hinz B, Applegate LL, Bourban PE, Zambelli PY, Månson JA, Pioletti DP. Biocompatibility of bioresorbable poly(L-lactic acid) composite scaffolds obtained by supercritical gas foaming with human fetal bone cells.. Tissue Eng 2005 Nov-Dec;11(11-12):1640-9.
    pubmed: 16411809doi: 10.1089/ten.2005.11.1640google scholar: lookup
  85. James AW, Levi B, Nelson ER, Peng M, Commons GW, Lee M, Wu B, Longaker MT. Deleterious effects of freezing on osteogenic differentiation of human adipose-derived stromal cells in vitro and in vivo.. Stem Cells Dev 2011 Mar;20(3):427-39.
    pmc: PMC3128779pubmed: 20536327doi: 10.1089/scd.2010.0082google scholar: lookup
  86. Duan W, Lopez MJ. Effects of Cryopreservation on Canine Multipotent Stromal Cells from Subcutaneous and Infrapatellar Adipose Tissue.. Stem Cell Rev Rep 2016 Apr;12(2):257-68.
    pmc: PMC4841859pubmed: 26537238doi: 10.1007/s12015-015-9634-4google scholar: lookup
  87. Duan W, Zhang N, Lopez MJ. Canine Adipose Tissue Derived Multipotent Stromal Cells Harvested from Infrapatellar and Subcutaneous Adipose Tissue Have Similarin Vitrobehavior. Vet Sur 2014;43(6):E163.
  88. Mitchell JB, McIntosh K, Zvonic S, Garrett S, Floyd ZE, Kloster A, Di Halvorsen Y, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM. Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers.. Stem Cells 2006 Feb;24(2):376-85.
    pubmed: 16322640doi: 10.1634/stemcells.2005-0234google scholar: lookup

Citations

This article has been cited 8 times.
  1. Urzì O, Gasparro R, Costanzo E, De Luca A, Giavaresi G, Fontana S, Alessandro R. Three-Dimensional Cell Cultures: The Bridge between In Vitro and In Vivo Models. Int J Mol Sci 2023 Jul 27;24(15).
    doi: 10.3390/ijms241512046pubmed: 37569426google scholar: lookup
  2. Merlo B, Baldassarro VA, Flagelli A, Marcoccia R, Giraldi V, Focarete ML, Giacomini D, Iacono E. Peptide Mediated Adhesion to Beta-Lactam Ring of Equine Mesenchymal Stem Cells: A Pilot Study. Animals (Basel) 2022 Mar 15;12(6).
    doi: 10.3390/ani12060734pubmed: 35327131google scholar: lookup
  3. Lipreri MV, Baldini N, Graziani G, Avnet S. Perfused Platforms to Mimic Bone Microenvironment at the Macro/Milli/Microscale: Pros and Cons. Front Cell Dev Biol 2021;9:760667.
    doi: 10.3389/fcell.2021.760667pubmed: 35047495google scholar: lookup
  4. Long Y, Bundkirchen K, Gräff P, Krettek C, Noack S, Neunaber C. Cytological Effects of Serum Isolated from Polytraumatized Patients on Human Bone Marrow-Derived Mesenchymal Stem Cells. Stem Cells Int 2021;2021:2612480.
    doi: 10.1155/2021/2612480pubmed: 34876907google scholar: lookup
  5. Li Z, Xiang S, Li EN, Fritch MR, Alexander PG, Lin H, Tuan RS. Tissue Engineering for Musculoskeletal Regeneration and Disease Modeling. Handb Exp Pharmacol 2021;265:235-268.
    doi: 10.1007/164_2020_377pubmed: 33471201google scholar: lookup
  6. Storti G, Scioli MG, Kim BS, Orlandi A, Cervelli V. Adipose-Derived Stem Cells in Bone Tissue Engineering: Useful Tools with New Applications. Stem Cells Int 2019;2019:3673857.
    doi: 10.1155/2019/3673857pubmed: 31781238google scholar: lookup
  7. Yang Q, Pinto VMR, Duan W, Paxton EE, Dessauer JH, Ryan W, Lopez MJ. In vitro Characteristics of Heterogeneous Equine Hoof Progenitor Cell Isolates. Front Bioeng Biotechnol 2019;7:155.
    doi: 10.3389/fbioe.2019.00155pubmed: 31355191google scholar: lookup
  8. Ferraro W, Civilleri A, Gögele C, Carbone C, Vitrano I, Carfi Pavia F, Brucato V, La Carrubba V, Werner C, Schäfer-Eckart K, Schulze-Tanzil G. The Phenotype of Mesenchymal Stromal Cell and Articular Chondrocyte Cocultures on Highly Porous Bilayer Poly-L-Lactic Acid Scaffolds Produced by Thermally Induced Phase Separation and Supplemented with Hydroxyapatite. Polymers (Basel) 2024 Jan 25;16(3).
    doi: 10.3390/polym16030331pubmed: 38337220google scholar: lookup
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