Human mesenchymal stem cell spheroids in fibrin hydrogels exhibit improved cell survival and potential for bone healing

Cell and Tissue Research

Volumn 357, Issue 1, 2014, Pages 91-99

  Murphy, Kaitlin C ^a   Fang, Sophia Y ^a,b   Leach, J Kent ^a,b  

^a University of California Davis   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell survival; Fibrin; Mesenchymal stem cell; Osteogenic potential; Spheroid

Indexed keywords

FIBRIN; OXYGEN; VASCULOTROPIN; HYDROGEL;

APOPTOSIS; ARTICLE; BONE REMODELING; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FRACTURE HEALING; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYMAL STEM CELL; MONOLAYER CULTURE; PRIORITY JOURNAL; SPHEROID CELL; BONE DEVELOPMENT; BONE REGENERATION; CELL CULTURE; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; MULTICELLULAR SPHEROID; PHYSIOLOGY;

BONE REGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; FIBRIN; HUMANS; HYDROGELS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; SPHEROIDS, CELLULAR;

EID: 84904676373     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1830-z     Document Type: Article

References (49)

1. Baraniak PR, McDevitt TC (2012) Scaffold-free culture of mesenchymal stem cell spheroids in suspension preserves multilineage potential. Cell Tissue Res 347:701-711
2. Barsotti MC, Magera A, Armani C, Chiellini F, Felice F, Dinucci D, Piras AM, Minnocci A, Solaro R, Soldani G, Balbarini A, Di Stefano R (2011) Fibrin acts as biomimetic niche inducing both differentiation and stem cell marker expression of early human endothelial progenitor cells. Cell Prolif 44:33-48
3. Bartosh TJ, Ylostalo JH, Mohammadipoor A, Bazhanov N, Coble K, Claypool K, Lee RH, Choi H, Prockop DJ (2010) Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties. Proc Natl Acad Sci U S A 107:13724-13729
4. Bhang SH, Cho SW, La WG, Lee TJ, Yang HS, Sun AY, Baek SH, Rhie JW, Kim BS (2011) Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells. Biomaterials 32:2734-2747
5. Bhang SH, Lee S, Lee TJ, La WG, Yang HS, Cho SW, Kim BS (2012a) Three-dimensional cell grafting enhances the angiogenic efficacy of human umbilical vein endothelial cells. Tissue Eng Part A 18:310-319
6. Bhang SH, Lee S, Shin JY, Lee TJ, Kim BS (2012b) Transplantation of cord blood mesenchymal stem cells as spheroids enhances vascularization. Tissue Eng A 18:2138-2147
7. Binder BY, Genetos DC, Leach JK (2014) Lysophosphatidic acid protects human mesenchymal stromal cells from differentiation-dependent vulnerability to apoptosis. Tissue Eng Part A (in press)
8. Caplan AI, Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98:1076-1084 (Pubitemid 44128350)
9. Correa de Sampaio P, Auslaender D, Krubasik D, Failla AV, Skepper JN, Murphy G, English WR (2012) A heterogeneous in vitro three dimensional model of tumour-stroma interactions regulating sprouting angiogenesis. PLoS One 7:e30753
10. Curcio E, Salerno S, Barbieri G, De Bartolo L, Drioli E, Bader A (2007) Mass transfer and metabolic reactions in hepatocyte spheroids cultured in rotating wall gas-permeable membrane system. Biomaterials 28:5487-5497 (Pubitemid 47599638)
11. Davis HE, Miller SL, Case EM, Leach JK (2011) Supplementation of fibrin gels with sodium chloride enhances physical properties and ensuing osteogenic response. Acta Biomater 7:691-699
12. Davis HE, Binder BY, Schaecher P, Yakoobinsky DD, Bhat A, Leach JK (2013) Enhancing osteoconductivity of fibrin gels with apatite-coated polymer microspheres. Tissue Eng A 19:1773-1782
13. Decaris ML, Binder BY, Soicher MA, Bhat A, Leach JK (2012) Cell-derived matrix coatings for polymeric scaffolds. Tissue Eng A 18:2148-2157
14. Del Duca D, Werbowetski T, Del Maestro RF (2004) Spheroid preparation from hanging drops: characterization of a model of brain tumor invasion. J Neurooncol 67:295-303 (Pubitemid 39137360)
15. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677-689 (Pubitemid 44233625)
16. Fey SJ, Wrzesinski K (2012) Determination of drug toxicity using 3D spheroids constructed from an immortal human hepatocyte cell line. Toxicol Sci 127:403-411
17. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4:309-324
18. Frith JE, Thomson B, Genever PG (2010) Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential. Tissue Eng C Methods 16:735-749
19. He J, Genetos DC, Leach JK (2010) Osteogenesis and trophic factor secretion are influenced by the composition of hydroxyapatite/poly(lactide-co- glycolide) composite scaffolds. Tissue Eng A 16:127-137
20. He J, Decaris ML, Leach JK (2012) Bioceramic-mediated trophic factor secretion by mesenchymal stem cells enhances in vitro endothelial cell persistence and in vivo angiogenesis. Tissue Eng A 18:1520-1528
21. Herrmann JL, Wang Y, Abarbanell AM, Weil BR, Tan J, Meldrum DR (2010) Preconditioning mesenchymal stem cells with transforming growth factor-alpha improves mesenchymal stem cell-mediated cardioprotection. Shock 33:24-30
22. Hoch AI, Binder BY, Genetos DC, Leach JK (2012) Differentiation-dependent secretion of proangiogenic factors by mesenchymal stem cells. PLoS One 7:e35579
23. Holzwarth C, Vaegler M, Gieseke F, Pfister SM, Handgretinger R, Kerst G, Muller I (2010) Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol 11:11
24. Janmey PA, Winer JP, Weisel JW (2009) Fibrin gels and their clinical and bioengineering applications. J R Soc Interface 6:1-10
25. Kaigler D, Wang Z, Horger K, Mooney DJ, Krebsbach PH (2006) VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. J Bone Miner Res 21:735-744
26. Kneser U, Schaefer DJ, Polykandriotis E, Horch RE (2006) Tissue engineering of bone: the reconstructive surgeon's point of view. J Cell Mol Med 10:7-19 (Pubitemid 44882940)
27. Korff T, Augustin HG (1998) Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J Cell Biol 143:1341-1352 (Pubitemid 28559834)
28. Kunz-Schughart LA, Kreutz M, Knuechel R (1998) Multicellular spheroids: a three-dimensional in vitro culture system to study tumour biology. Int J Exp Pathol 79:1-23 (Pubitemid 28137705)
29. Lai Y, Kisaalita WS (2012) Performance evaluation of 3D polystyrene 96-well plates with human neural stem cells in a calcium assay. J Lab Autom 17:284-292
30. Laschke MW, Schank TE, Scheuer C, Kleer S, Schuler S, Metzger W, Eglin D, Alini M, Menger MD (2013) Three-dimensional spheroids of adipose-derived mesenchymal stem cells are potent initiators of blood vessel formation in porous polyurethane scaffolds. Acta Biomater 9:6876-6884
31. Laurencin C, Khan Y, El-Amin SF (2006) Bone graft substitutes. Expert Rev Med Devices 3:49-57
32. Lee EJ, Park SJ, Kang SK, Kim GH, Kang HJ, Lee SW, Jeon HB, Kim HS (2012) Spherical bullet formation via E-cadherin promotes therapeutic potency of mesenchymal stem cells derived from human umbilical cord blood for myocardial infarction. Mol Ther 20:1424-1433
33. Leu A, Stieger SM, Dayton P, Ferrara KW, Leach JK (2009) Angiogenic response to bioactive glass promotes bone healing in an irradiated calvarial defect. Tissue Eng A 15:877-885
34. Mehta M, Schmidt-Bleek K, Duda GN, Mooney DJ (2012) Biomaterial delivery of morphogens to mimic the natural healing cascade in bone. Adv Drug Deliv Rev 64:1257-1276
35. Mueller-Klieser W (1997) Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am J Physiol 273:C1109-C1123
36. Murphy KC, Leach JK (2012) A reproducible, high throughput method for fabricating fibrin gels. BMC Res Notes 5:423
37. O'Keefe RJ, Mao J (2011) Bone tissue engineering and regeneration: from discovery to the clinic-an overview. Tissue Eng B Rev 17:389-392
38. Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 77:134-142 (Pubitemid 351195153)
39. Potier E, Ferreira E, Meunier A, Sedel L, Logeart-Avramoglou D, Petite H (2007) Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death. Tissue Eng 13:1325-1331 (Pubitemid 46986732)
40. Shaikh FM, Callanan A, Kavanagh EG, Burke PE, Grace PA, McGloughlin TM (2008) Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs 188:333-346
41. Shimizu T, Yamato M, Isoi Y, Akutsu T, Setomaru T, Abe K, Kikuchi A, Umezu M, Okano T (2002) Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheetmanipulation technique and temperature-responsive cell culture surfaces. Circ Res 90:e40
42. Shweiki D, Neeman M, Itin A, Keshet E (1995) Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc Natl Acad Sci U S A 92:768-772
43. Siddappa R, Licht R, van Blitterswijk C, de Boer J (2007) Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J Orthop Res 25:1029-1041 (Pubitemid 47233079)
44. Titushkin I, Cho M (2007) Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophys J 93:3693-3702 (Pubitemid 350190831)
45. Wang CC, Chen CH, Hwang SM, Lin WW, Huang CH, Lee WY, Chang Y, Sung HW (2009) Spherically symmetric mesenchymal stromal cell bodies inherent with endogenous extracellular matrices for cellular cardiomyoplasty. Stem Cells 27:724-732
46. Wenger A, Stahl A, Weber H, Finkenzeller G, Augustin HG, Stark GB, Kneser U (2004) Modulation of in vitro angiogenesis in a three-dimensional spheroidal coculture model for bone tissue engineering. Tissue Eng 10:1536-1547 (Pubitemid 39557857)
47. Winer JP, Janmey PA, McCormick ME, Funaki M (2009) Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng A 15:147-154
48. Yang J, Yamato M, Kohno C, Nishimoto A, Sekine H, Fukai F, Okano T (2005) Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials 26:6415-6422 (Pubitemid 41021737)
49. Zhang M, Methot D, Poppa V, Fujio Y, Walsh K, Murry CE (2001) Cardiomyocyte grafting for cardiac repair: graft cell death and antideath strategies. J Mol Cell Cardiol 33:907-921 (Pubitemid 32545326)