Effect of scaffold microarchitecture on osteogenic differentiation of human mesenchymal stem cells

European Cells and Materials

Volumn 25, Issue , 2012, Pages 114-129

  Phadke, Ameya ^a   Hwang, YongSung ^a   Hee Kim, Su ^b   Hyun Kim, Soo ^b   Yamaguchi, Tomonori ^c,d   Masuda, Koichi ^c   Varghese, Shyni ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Korea Institute of Science and Technology   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d DOSHISHA UNIVERSITY   (Japan)

Author keywords

Bone formation; Columnar cryogels; Mesenchymal stem cells; Osteoblastic genes; Spongy cryogels; Synthetic grafts

Indexed keywords

ALKALINE PHOSPHATASE; MOLECULAR SCAFFOLD; OSTEOCALCIN; OSTEOPONTIN; POLY(ETHYLENE GLYCOL)DIACRYLATE CO N ACRYLOYL 6 AMINOCAPROIC ACID; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; MACROGOL DERIVATIVE; RUNX2 PROTEIN, HUMAN; TISSUE SCAFFOLD;

ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; BONE GRAFT; CELL DIFFERENTIATION; CELL INFILTRATION; CELL PROLIFERATION; CELL VIABILITY; COLUMNAR CRYOGEL; CONTROLLED STUDY; CRYOGEL; ENZYME ACTIVITY; GENE EXPRESSION; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MICROTECHNOLOGY; MINERALIZATION; NONHUMAN; OCN GENE; OPN GENE; OSSIFICATION; POROSITY; RAT; RUNX2 GENE; SPONGY CRYOGEL; STRUCTURE ANALYSIS; VASCULARIZATION; ANIMAL; BONE PROSTHESIS; BONE REGENERATION; CELL CULTURE; CELL SURVIVAL; GENETICS; IMPLANT; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; NUDE RAT; PHYSIOLOGY; POLYMERIZATION; REGENERATIVE MEDICINE; SYNTHESIS;

ALKALINE PHOSPHATASE; ANIMALS; BONE REGENERATION; BONE SUBSTITUTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CRYOGELS; GENE EXPRESSION; HUMANS; IMPLANTS, EXPERIMENTAL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; OSTEOCALCIN; OSTEOGENESIS; OSTEOPONTIN; POLYETHYLENE GLYCOLS; POLYMERIZATION; POROSITY; RATS; RATS, NUDE; REGENERATIVE MEDICINE; TISSUE SCAFFOLDS;

MLCS; MLOWN;

EID: 84877746831     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Ayala R, Zhang C, Yang D, Hwang Y, Aung A, Shroff SS, Arce FT, Lal R, Arya G, Varghese S (2011) Engineering the cell-material interface for controlling stem cell adhesion, migration, and differentiation. Biomaterials 32: 3700-3711.
2. Barradas A, Yuan H, van der Stok J, Le Quang B, Fernandes H, Chaterjea A, Hogenes MCH, Shultz K, Donahue LR, van Blitterswijk C, de Boer J (2012) The influence of genetic factors on the osteoinductive potential of calcium phosphate ceramics in mice. Biomaterials 33: 5696-5705.
3. Benoit DSW, Schwartz MP, Durney AR, Anseth KS (2008) Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater 7: 816-823.
4. Birmingham E, Niebur GL, McHugh PE, Shaw G, Barry FP, McNamara LM (2012) Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur Cells Mater 23: 13-27.
5. Bruder SP, Jaiswal N, Ricalton NS, Mosca JD, Kraus KH, Kadiyala S (1998) Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orth Relat Res 355: S247.
6. Chai YC, Roberts SJ, Schrooten J, Luyten FP (2010) Probing the osteoinductive effect of calcium phosphate by using an in vitro biomimetic model. Tissue Eng Part A 17: 1083-1097.
7. Chai YC, Carlier A, Bolander J, Roberts SJ, Geris L, Schrooten J, Van Oosterwyck H, Luyten FP (2012) Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies. Acta Biomater 8: 3876-3887.
8. Cheng L, Duan X, Xiang Z, Shi Y, Lu X, Ye F, Bu H (2012) Ectopic bone formation cannot occur by hydroxyapatite/β-tricalcium phosphate bioceramics in green fluorescent protein chimeric mice. Appl Surf Sci 262: 200-206.
9. Chiu Y-C, Cheng M-H, Engel H, Kao S-W, Larson JC, Gupta S, Brey EM (2011) The role of pore size on vascularization and tissue remodeling in PEG hydrogels. Biomaterials 32: 6045-6051.
10. Cowan CM, Shi YY, Aalami OO, Chou YF, Mari C, Thomas R, Quarto N, Contag CH, Wu B, Longaker MT (2004) Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22: 560-567.
11. Curran JM, Chen R, Hunt JA (2006) The guidance of human mesenchymal stem cell differentiation in vitro by controlled modifications to the cell substrate. Biomaterials 27: 4783-4793.
12. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CDW, Oreffo ROC (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6: 997-1003.
13. Deville S (2008) Freeze-casting of porous ceramics: A review of current achievements and issues. Adv Eng Mater 10: 155-169.
14. Deville S, Saiz E, Tomsia AP (2006) Freeze casting of hydroxyapatite scaffolds for bone tissue engineering. Biomaterials 27: 5480-5489.
15. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
16. Fu Q, Rahaman MN, Bal BS, Brown RF (2009) In vitro cellular response to hydroxyapatite scaffolds with oriented pore architectures. Mater Sci Eng C 29: 2147-2153.
17. Galante J, Rostoker W, Ray RD (1970) Physical properties of trabecular bone. Calcif Tissue Int 5: 236-246.
18. Gauthier O, Bouler J-M, Aguado E, Pilet P, Daculsi G (1998) Macroporous biphasic calcium phosphate ceramics: influence of macropore diameter and macroporosity percentage on bone ingrowth. Biomaterials 19: 133-139.
19. Gerhardt L-C, Widdows KL, Erol MM, Burch CW, Sanz-Herrera J, Ochoa I, Stämpfli R, Roqan IS, Gabe S, Ansari T, Boccaccini AR (2011) The pro-angiogenic properties of multi-functional bioactive glass composite scaffolds. Biomaterials 32: 4096-4108.
20. Gomes M, Holtorf H, Reis R, Mikos A (2006) Influence of the porosity of starch-based fiber mesh scaffolds on the proliferation and osteogenic differentiation of bone marrow stromal cells cultured in a flow perfusion bioreactor. Tissue Eng 12: 801-809.
21. Gorustovich A, Roether J, Boccaccini A (2010) Effect of bioactive glasses on angiogenesis: a review of in vitro and in vivo evidences. Tissue Eng Part B Rev 16: 199-207.
22. Hutmacher DW, Schantz JT, Lam CXF, Tan KC, Lim TC (2007) State of the art and future directions of scaffold-based bone engineering from a biomaterials perspective. J Tissue Eng Regen Med 1: 245-260.
23. Hwang NS, Varghese S, Puleo C, Zhang Z, Elisseeff J (2007) Morphogenetic signals from chondrocytes promote chondrogenic and osteogenic differentiation of mesenchymal stem cells. J Cell Physiol 212: 281-284.
24. Hwang NS, Zhang C, Hwang Y, Varghese S (2009a) Mesenchymal stem cell differentiation and roles in regenerative medicine. Wiley Interdisc Rev Syst Biol Med 1: 97-106.
25. Hwang Y, Zhang C, Varghese S (2009b) Poly (ethylene glycol) cryogels as potential cell scaffolds: effect of polymerization conditions on cryogel microstructure and properties. J Mater Chem 20: 345-351.
26. Hwang Y, Sangaj N, Varghese S (2010) Interconnected macroporous poly(ethylene glycol) cryogels as a cell scaffold for cartilage tissue engineering. Tissue Eng Part A 16: 3033-3041.
27. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP (1997) Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64: 295-312.
28. Kadiyala S, Jaiswal N, Bruder SP (1997) Culture-expanded, bone marrow-derived mesenchymal stem cells can regenerate a critical-sized segmental bone defect. Tissue Eng 3: 173-185.
29. Karageorgiou V, Kaplan D (2005) Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26: 5474-5491.
30. Kasten P, Beyen I, Niemeyer P, Luginbühl R, Bohner M, Richter W (2008) Porosity and pore size of β-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: An in vitro and in vivo study. Acta Biomater 4: 1904-1915.
31. Kawai T, Anada T, Honda Y, Kamakura S, Matsui K, Matsui A, Sasaki K, Morimoto S, Echigo S, Suzuki O (2009) Synthetic octacalcium phosphate augments bone regeneration correlated with its content in collagen scaffold. Tissue Eng Part A 15: 23-32.
32. Kim K, Yeatts A, Dean D, Fisher J (2010) Stereolithographic bone scaffold design parameters: osteogenic differentiation and signal expression. Tissue Eng Part B Rev 16: 523-539.
33. Kühne JH, Bartl R, Frisch B, Hammer C, Jansson V, Zimmer M (1994) Bone formation in coralline hydroxyapatite: effects of pore size studied in rabbits. Acta Orthopaedica 65: 246-252.
34. Lee JS, Suarez-Gonzalez D, Murphy WL (2011) Mineral coatings for temporally controlled delivery of multiple proteins. Adv Mater 23: 4279-4284.
35. Le Nihouannen D, Daculsi G, Saffarzadeh A, Gauthier O, Delplace Sv, Pilet P, Layrolle P (2005) Ectopic bone formation by microporous calcium phosphate ceramic particles in sheep muscles. Bone 36: 1086-1093.
36. Mastrogiacomo M, Scaglione S, Martinetti R, Dolcini L, Beltrame F, Cancedda R, Quarto R (2006) Role of scaffold internal structure on in vivo bone formation in macroporous calcium phosphate bioceramics. Biomaterials 27: 3230-3237.
37. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
38. Müller P, Bulnheim U, Diener A, Lüthen F, Teller M, Klinkenberg ED, Neumann HG, Nebe B, Liebold A, Steinhoff G (2008) Calcium phosphate surfaces promote osteogenic differentiation of mesenchymal stem cells. J Cell Mol Med 12: 281-291.
39. Osathanon T, Linnes ML, Rajachar RM, Ratner BD, Somerman MJ, Giachelli CM (2008) Microporous nanofibrous fibrin-based scaffolds for bone tissue engineering. Biomaterials 29: 4091-4099.
40. Oyane A, Kim HM, Furuya T, Kokubo T, Miyazaki T, Nakamura T (2003) Preparation and assessment of revised simulated body fluids. J Biomed Mater Res Part A 65: 188-195.
41. Pek YS, Gao S, Arshad MSM, Leck KJ, Ying JY (2008) Porous collagen-apatite nanocomposite foams as bone regeneration scaffolds. Biomaterials 29: 4300-4305.
42. Phadke A, Chang CW, Varghese S (2010a) Functional Biomaterials for Controlling Stem Cell Differentiation. In: Biomaterials as Stem Cell Niche (Roy K, ed), Springer, Berlin Heidelberg, pp 19-44.
43. Phadke A, Zhang C, Hwang YS, Vecchio K, Varghese S (2010b) Templated mineralization of synthetic hydrogels for bone-like composite materials: role of matrix hydrophobicity. Biomacromolecules 12: 2060-2068.
44. Phadke A, Shih Y, Varghese S (2012) Mineralized synthetic matrices as an instructive microenvironment for osteogenic differentiation of human mesenchymal stem cells. Macromol Biosci 12: 1022-1032.
45. Schaffler MB, Burr DB (1988) Stiffness of compact bone: effects of porosity and density. J Biomech 21: 13-16.
46. Selye H, Lemire Y, Bajusz E (1960) Induction of bone, cartilage and hemopoietic tissue by subcutaneously implanted tissue diaphragms. Dev Genes Evol 151: 572-585.
47. Seyedjafari E, Soleimani M, Ghaemi N, Shabani I (2010) Nanohydroxyapatite-coated electrospin poly(L-lactide) nanofibers enhance osteogenic differneitation of stem cells and induce ectopic bone formation. Biomacromolecules 11: 3118-3125.
48. Tsuruga E, Takita H, Itoh H, Wakisaka Y, Kuboki Y (1997) Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. J Biochem 121: 317-324.
49. Uebersax L, Hagenmüller H, Hofmann S, Gruenblatt E, Müller R, Vunjak-Novokovic G, Kaplan D, Merkle HP, Meinel L (2006) Effect of scaffold design on bone morphology in vitro. Tissue Eng 12: 3417-3429.
50. Varghese S, Hwang NS, Ferran A, Hillel A, Theprungsirikul P, Canver AC, Zhang Z, Gearhart J, Elisseeff J (2010) Engineering musculoskeletal tissues with human embryonic germ cell derivatives. Stem Cells 28: 765-774.
51. Von Doernberg M-C, von Rechenberg B, Bohner M, Grünenfelder S, van Lenthe GH, Müller R, Gasser B, Mathys R, Baroud G, Auer J (2006) In vivo behavior of calcium phosphate scaffolds with four different pore sizes. Biomaterials 27: 5186-5198.
52. Wang X, Ni Q (2003) Determination of cortical bone porosity and pore size distribution using a low field pulsed NMR approach. J Orth Res 21: 312-319.
53. Wegst U, Schechter M, Donius A, Hunger P (2010) Biomaterials by freeze casting. Phil Trans R Soc A 368: 2099-2121.
54. Yang Z, Yuan H, Tong W, Zou P, Chen W, Zhang X (1996) Osteogenesis in extraskeletally implanted porous calcium phosphate ceramics: variability among different kinds of animals. Biomaterials 17: 2131-2137.
55. Yuan H, van Blitterswijk CA, de Groot K, de Bruijn JD (2006) Cross-species comparison of ectopic bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) scaffolds. Tissue Eng 12: 1607-1615.
56. Yuan H, Fernandes H, Habibovic P, De Boer J, Barradas A, De Ruiter A, Walsh WR, Van Blitterswijk CA, De Bruijn JD (2010) Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci USA 107: 13614-13619.
57. Yunoki S, Ikoma T, Monkawa A, Ohta K, Kikuchi M, Sotome S, Shinomiya K, Tanaka J (2006) Control of pore structure and mechanical property in hydroxyapatite/collagen composite using unidirectional ice growth. Mater Letters 60: 999-1002.
58. Zeltinger J, Sherwood J, Graham D, Müeller R, Griffith L (2001) Effect of pore size and void fraction on cellular adhesion, proliferation and matrix deposition. Tissue Eng 7: 557-572.
59. Zhang C, Aung A, Liao L, Varghese S (2009) A novel single precursor-based biodegradable hydrogel with enhanced mechanical properties. Soft Matter 5: 3831-3834.
60. Zhang H, Hussain I, Brust M, Butler MF, Rannard SP, Cooper AI (2005) Aligned two-and three-dimensional structures by directional freezing of polymers and nanoparticles. Nat Mater 4: 787-793.