Osteogenic differentiation of human mesenchymal stem cells in 3-D Zr-Si organic-inorganic scaffolds produced by two-photon polymerization technique

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Koroleva, Anastasia ^a   Deiwick, Andrea ^a   Nguyen, Alexander ^b   Schlie Wolter, Sabrina ^a   Narayan, Roger ^b   Timashev, Peter ^c   Popov, Vladimir ^c   Bagratashvili, Viktor ^c   Chichkov, Boris ^a  

^a LASER ZENTRUM HANNOVER E V   (Germany)

^b USA and North Carolina State University   (United States)

^c INSTITUTE ON LASER AND INFORMATION TECHNOLOGIES   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; ALKALINE PHOSPHATASE; CALCIUM ION; MOLECULAR SCAFFOLD; OSTEOCALCIN; POLYMER; SILICON; ZIRCONIUM; CALCIUM; INORGANIC COMPOUND; ORGANIC COMPOUND;

ADIPOSE DERIVED STEM CELL; AGING; AQUEOUS SOLUTION; ARTICLE; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MATRIX; BONE MINERALIZATION; BONE TISSUE; CALCIUM BONE LEVEL; CALCIUM CELL LEVEL; CELL DIFFERENTIATION; CELL LABELING; CELL LINEAGE; COMPOSITE MATERIAL; CONTROLLED STUDY; CULTURE MEDIUM; HARDNESS; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MICROTECHNOLOGY; OSSIFICATION; POLYMERIZATION; SCANNING ELECTRON MICROSCOPY; STAINING; STEM CELL CULTURE; SYNTHESIS; TISSUE ENGINEERING; TISSUE SCAFFOLD; TWO PHOTON POLYMERIZATION; YOUNG MODULUS; ADIPOSE TISSUE; CELL CULTURE; CELL CULTURE TECHNIQUE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES; REPRODUCIBILITY; STEM CELL; TIME FACTOR; ULTRASTRUCTURE;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE; CALCIUM; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHEMISTRY TECHNIQUES, SYNTHETIC; ELASTIC MODULUS; HARDNESS; HUMANS; INORGANIC CHEMICALS; MESENCHYMAL STROMAL CELLS; MICROSCOPY, ELECTRON, SCANNING; ORGANIC CHEMICALS; OSTEOCALCIN; OSTEOGENESIS; POLYMERIZATION; REPRODUCIBILITY OF RESULTS; SILICON; STEM CELLS; TIME FACTORS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; ZIRCONIUM;

EID: 84923270119     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118164     Document Type: Article

References (44)

1. Karageorgiou V, Kaplan D (2005) Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26: 5474-5491. doi: 10.1016/j.biomaterials.2005.02.002 PMID: 15860204
2. Zollikofer Christoph P E, Ponce de Leon MS (1995) Tools for Rapid Prototyping in the Biosciences. IEEE Comput Graph Appl: 48-55.
3. Ovsianikov A, Ostendorf A, Chichkov BN (2007) Three-dimensional photofabrication with femtosecond lasers for applications in photonics and biomedicine. Appl Surf Sci 253: 6599-6602. doi: 10.1016/j.apsusc.2007.01.058
4. Nguyen A, Gittard SD, Koroleva A, Schlie S, Gaidukeviciute A, et al. (2013) Two-photon polymerization of polyethylene glycol diacrylate scaffolds with riboflavin and triethanolamine used as a water-soluble photoinitiator Aim: Regen Med 8: 51-64. doi: 10.2217/rme.13.60 PMID: 24147528
5. Ovsianikov A, Mironov V, Stampfl J, Liska R (2012) Engineering 3D cell-culture matrices: multiphoton processing technologies for biological and tissue engineering applications. Expert Rev Med Devices 9: 613-633. doi: 10.1586/erd.12.48 PMID: 22943308
6. Raimondi MT, Eaton SM, Nava MM, Laganà M, Cerullo G, et al. (2012) Two-photon laser polymerization: from fundamentals to biomedical application in tissue engineering and regenerative medicine. J Appl Biomater Biomech 10: 55-65. doi: 10.5301/JABB.2012.9249
7. Chevalier J, Gremillard L (2009) Ceramics for medical applications: A picture for the next 20 years. 29: 1245-1255. doi: 10.1016/j.jeurceramsoc.2008.08.025
8. Oubaha M, Copperwhite R, Boothman C, Ovsianikov A, Kiyan R, et al. (2010) Influence of hybrid organic-inorganic sol-gel matrices on the photophysics of amino-functionalized UV-sensitizers. J Mater Sci 46: 400-408. doi: 10.1007/s10853-010-4853-1
9. Miller P, Ovsianikov A, Koroleva A, Gittard SD, Chichkov B, et al. (2011) Medical applications of zirconium oxide hybrid materials. Am Ceram Soc Bull 90: 24-29.
10. Ovsianikov A, Gaidukeviciute A, Chichkov BN, Oubaha M, MacCraith BD, et al. (2008) Two-Photon Polymerization of Hybrid Sol-Gel Materials for Photonics Applications. Laser Chem 2008: 493059. doi: 10.1155/2008/493059
11. Ovsianikov A, Viertl J, Chichkov B, Oubaha M, MacCraith B, et al. (2008) Ultra-low shrinkage hybrid photosensitive material for two-photon polymerization microfabrication. ACS Nano 2: 2257-2262. doi: 10.1021/nn800451w PMID: 19206391
12. Psycharakis S, Tosca A, Melissinaki V, Giakoumaki A, Ranella A (2011) Tailor-made three-dimensional hybrid scaffolds for cell cultures. Biomed Mater 6: 045008. doi: 10.1088/1748-6041/6/4/045008 PMID: 21743121
13. Terzaki K, Kissamitaki M, Skarmoutsou A, Fotakis C, Charitidis C a, et al. (2013) Pre-osteoblastic cell response on three-dimensional, organic-inorganic hybrid material scaffolds for bone tissue engineering. J Biomed Mater Res A 101: 2283-2294. doi: 10.1002/jbm.a.34516 PMID: 23355483
14. Terzaki K, Kalloudi E, Mossou E, Mitchell EP, Forsyth VT, et al. (2013) Mineralized self-assembled peptides on 3D laser-made scaffolds: a new route toward "scaffold on scaffold" hard tissue engineering. Biofabrication 5: 045002. doi: 10.1088/1758-5082/5/4/045002 PMID: 23988557
15. Raimondi MT, Eaton SM, Laganà M, Aprile V, Nava MM, et al. (2013) Three-dimensional structural niches engineered via two-photon laser polymerization promote stem cell homing. Acta Biomater 9: 4579-4584. doi: 10.1016/j.actbio.2012.08.022 PMID: 22922332
16. Skoog S, Nguyen AK, Kumar G, Zheng J, Goering PL, et al. (2014) Two-photon polymerization of 3-D zirconium oxide hybrid scaffolds for long-term stem cell growth. Biointerphases 9: 029014. doi: 10.1116/1.4873688 PMID: 24985218
17. Pittenger MF (1999) Multilineage Potential of Adult Human Mesenchymal Stem Cells. Science (80-) 284: 143-147. doi: 10.1126/science.284.5411.143 PMID: 10102814
18. Zuk PA, Zhu M, Ashjian P, Ugarte DA De, Huang JI, et al. (2002) Human Adipose Tissue Is a Source of Multipotent Stem Cells. 13: 4279-4295. doi: 10.1091/mbc.E02 PMID: 12475952
19. Oliver WC, Pharr GM (2004) Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology. J Mater Res 19: 3-20. doi: 10.1557/jmr.2004.19.1.3
20. Gruene M, Pflaum M, Deiwick a, Koch L, Schlie S, et al. (2011) Adipogenic differentiation of laser-printed 3D tissue grafts consisting of human adipose-derived stem cells. Biofabrication 3: 015005. doi: 10.1088/1758-5082/3/1/015005 PMID: 21358040
21. Suga H, Shigeura T, Matsumoto D, Inoue K, Kato H, et al. (2007) Rapid expansion of human adipose-derived stromal cells preserving multipotency. Cytotherapy 9: 738-745. doi: 10.1080/14653240701679873 PMID: 18058361
22. Folkman J, Moscona A (1978) Role of cell shape in growth control. Nature 273: 345-349. PMID: 661946
23. Kufelt O, El-Tamer A, Sehring C, Schlie-Wolter S, Chichkov BN (2014) Hyaluronic Acid Based Materials for Scaffolding via Two-Photon Polymerization. Biomacromolecules 15: 650-659. doi: 10.1021/bm401712q PMID: 24432740
24. Haslam G, Wyatt D, Kitos P a (2000) Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology 32: 63-75. doi: 10.1023/A:1008121125755 PMID: 19002967
25. Bernhardt A, Despang F, Lode A, Demmler A, Hanke T, et al. (2009) Proliferation and osteogenic differentiation of human bone marrow stromal cells on alginate - gelatine - hydroxyapatite scaffolds with anisotropic pore structure: 54-62. doi: 10.1002/term PMID: 24607421
26. Moravec R, Corporation P (2002) CytoTox-ONE™ Homogeneous Membrane Integrity Assay: 15-18.
27. Ovsianikov A, Malinauskas M, Schlie S, Chichkov B, Gittard S, et al. (2011) Three-dimensional laser micro- and nano-structuring of acrylated poly(ethylene glycol) materials and evaluation of their cytoxicity for tissue engineering applications. Acta Biomater 7: 967-974. doi: 10.1016/j.actbio.2010.10.023 PMID: 20977947
28. Owen T, Aronow M, Shalhoub V, Barone LM, Wilming L, et al. (1990) Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143: 420-430. doi: 10.1002/jcp.1041430304 PMID: 1694181
29. Li T, Ebert K, Vogel J, Groth T (2013) Comparative studies on osteogenic potential of micro- and nanofibre scaffolds prepared by electrospinning of poly (å-caprolactone): 1-13.
30. Bernhardt A, Lode A, Peters F, Gelinsky M (2013) Comparative evaluation of different calcium phosphate-based bone graft granules - an in vitro study with osteoblast-like cells. Clin Oral Implants Res 24: 441-449. doi: 10.1111/j.1600-0501.2011.02350.x PMID: 22092911
31. Mizuno M, Kuboki Y (2001) Osteoblast-related gene expression of bone marrow cells during the osteoblastic differentiation induced by type I collagen. J Biochem 129: 133-138. PMID: 11134967
32. Golub EE, Harrison G, Taylor a G, Camper S, Shapiro IM (1992) The role of alkaline phosphatase in cartilage mineralization. Bone Miner 17: 273-278. PMID: 1611320
33. Tang J, Peng R, Ding J (2010) The regulation of stem cell differentiation by cell-cell contact on micropatterned material surfaces. Biomaterials 31: 2470-2476. doi: 10.1016/j.biomaterials.2009.12.006 PMID: 20022630
34. Fagotto F, Gumbiner BM (1996) Cell Contact-Dependent Signaling. Dev Biol 180: 445-454. PMID: 8954717
35. Dorshkind K, Green L, Godwin a, FletcherWH (1993) Connexin-43-type gap junctions mediate communication between bone marrow stromal cells. Blood 82: 38-45. PMID: 8391877
36. Huebsch N, Arany PR, Mao AS, Shvartsman D, Ali O a, et al. (2010) Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 9: 518-526. doi: 10.1038/nmat2732 PMID: 20418863
37. Correia C, Bhumiratana S, Yan L-P, Oliveira AL, Gimble JM, et al. (2012) Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater 8: 2483-2492. doi: 10.1016/j.actbio.2012.03.019 PMID: 22421311
38. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689. doi: 10.1016/j.cell.2006.06.044 PMID: 16923388
39. Shih Y-R V, Tseng K-F, Lai H-Y, Lin C-H, Lee OK (2011) Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells. J Bone Miner Res 26: 730-738. doi: 10.1002/jbmr.278 PMID: 20939067
40. Rho JY, Tsui TY, Pharr GM (1997) Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials 18: 1325-1330. PMID: 9363331
41. Skarmoutsou A, Lolas G, Charitidis C a, Chatzinikolaidou M, Vamvakaki M, et al. (2013) Nanomechanical properties of hybrid coatings for bone tissue engineering. J Mech Behav Biomed Mater 25: 48-62. doi: 10.1016/j.jmbbm.2013.05.003 PMID: 23726922
42. Lewandrowski K-U, Gresser JD, P.Bondre S, Silva AE, Wise DL, et al. (2000) Developing porosity of poly(propylene glycol-co-fumaric acid) bone graft substitutes and the effect on osteointegration: A preliminary histology study in rats. J Biomater Sci Polym Ed 11: 879-889. doi: 10.1163/156856200744075 PMID: 11211098
43. Kuboki Y, Jin Q, Kikuchi M, Mamood J, Takita H (2002) Geometry of Artificial ECM: Sizes of Pores Controlling Phenotype Expression in BMP-Induced Osteogenesis and Chondrogenesis. Connect Tissue Res 43: 529-534. doi: 10.1080/03008200290001104 PMID: 12489210
44. Zuk PA, Ph D, Zhu MIN, Mizuno H, Benhaim P, et al. (2001) Multilineage Cells from Human Adipose Tissue: Implications for Cell-Based Therapies. Tissue Eng 7: 211-228. PMID: 11304456