Umbilical cord and bone marrow mesenchymal stem cell seeding on macroporous calcium phosphate for bone regeneration in rat cranial defects

Biomaterials

Volumn 34, Issue 38, 2013, Pages 9917-9925

  Chen, Wenchuan ^a,b   Liu, Jun ^a,b   Manuchehrabadi, Navid ^c   Weir, Michael D ^b   Zhu, Zhimin ^a   Xu, Hockin H K ^b,c,d  

^a SICHUAN UNIVERSITY   (China)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c Baltimore County   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Athymic rats; Bone regeneration; Calcium phosphate cement; Critical sized cranial defect; RGD; Stem cells

Indexed keywords

ATHYMIC; BONE REGENERATION; CALCIUM PHOSPHATE CEMENT; CRANIAL DEFECTS; RGD;

BLOOD VESSELS; BONE; CELL CULTURE; COMPUTERIZED TOMOGRAPHY; DEFECTS; PHOSPHATASES; RATS; SCAFFOLDS (BIOLOGY);

STEM CELLS;

ALKALINE PHOSPHATASE; CALCIUM PHOSPHATE; CALCIUM PHOSPHATE CEMENT; CEMENT; COLLAGEN TYPE 1; OSTEOCALCIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; BONE DENSITY; BONE MARROW; BONE MARROW MESENCHYMAL STEM CELL; BONE REGENERATION; CAPILLARY DENSITY; CELL ADHESION; CELL DENSITY; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFANT; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; PRIORITY JOURNAL; RAT; SKULL DEFECT; THICKNESS; TRABECULAR BONE; UMBILICAL CORD; UMBILICAL CORD MESENCHYMAL STEM CELL;

RATTUS;

ATHYMIC RATS; BONE REGENERATION; CALCIUM PHOSPHATE CEMENT; CRITICAL-SIZED CRANIAL DEFECT; RGD; STEM CELLS;

BONE MARROW CELLS; BONE REGENERATION; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELLS, CULTURED; COLLAGEN TYPE I; CORE BINDING FACTOR ALPHA 1 SUBUNIT; HUMANS; MESENCHYMAL STROMAL CELLS; MICROSCOPY, ELECTRON, SCANNING; OSTEOCALCIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKULL; STEM CELLS; TISSUE SCAFFOLDS; UMBILICAL CORD; X-RAY MICROTOMOGRAPHY;

EID: 84885390373     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.09.002     Document Type: Article

References (61)

1. Mikos A.G., Herring S.W., Ochareon P., Elisseeff J., Lu H.H., Kandel R., et al. Engineering complex tissues. Tissue Eng 2006, 12:3307-3339.
2. Kaigler D., Krebsbach P.H., Wang Z., West E.R., Horger K., Mooney D.J. Transplanted endothelial cells enhance orthotopic bone regeneration. JDent Res 2006, 85:633-637.
3. Deville S., Saiz E., Nalla R.K., Tomsia A.P. Freezing as a path to build complex composites. Science 2006, 311:515-518.
4. Johnson P.C., Mikos A.G., Fisher J.P., Jansen J.A. Strategic directions in tissue engineering. Tissue Eng 2007, 13:2827-2837.
5. Sundelacruz S., Kaplan D.L. Stem cell- and scaffold-based tissue engineering approaches to osteochondral regenerative medicine. Semin Cell Dev Biol 2009, 20:646-655.
6. Varghese S., Hwang N.S., Ferran A., Hillel A., Theprungsirikul P., Canver A.C., et al. Engineering musculoskeletal tissues with human embryonic germ cell derivatives. Stem Cells 2010, 28:765-774.
7. Mao J.J., Vunjak-Novakovic G., Mikos A.G., Atala A. Translational approaches in tissue engineering and regenerative medicine 2007, Chapters 1-3, Artech House, Boston, MA.
8. Quarto R., Thomas D., Liang C.T. Bone progenitor cell deficits and the age-associated decline in bone repair capacity. Calcif Tissue Int 1995, 56:123-129.
9. Mueller S.M., Glowacki J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. JCell Biochem 2001, 82:583-590.
10. Mendes S.C., Tibbe J.M., Veenhof M., Bakker K., Both S., Platenburg P.P., et al. Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age. Tissue Eng 2002, 8:911-920.
11. Stenderup K., Justesen J., Clausen C., Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003, 33:919-926.
12. Rodriguez J.P., Montecinos L., Rios S., Reyes P., Martinez J. Mesenchymal stem cells from osteoporotic patients produce a type I collagen-deficient extracellular matrix favoring adipogenic differentiation. JCell Biochem 2000, 79:557-565.
13. Suzuki Y., Kim K.J., Kotake S., Itoh T. Stromal cell activity in bone marrow from the tibia and iliac crest of patients with rheumatoid arthritis. JBone Miner Metab 2001, 19:56-60.
14. Wang H.S., Hung S.C., Peng S.T., Huang C.C., Wei H.M., Guo Y.J., et al. Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem Cells 2004, 22:1330-1337.
15. Zebardast N., Lickorish D., Davies J.E. Human umbilical cord perivascular cells (HUCPVC): a mesenchymal cell source for dermal wound healing. Organogenesis 2010, 6:197-203.
16. Baksh D., Yao R., Tuan R.S. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 2007, 25:1384-1392.
17. Bailey M.M., Wang L., Bode C.J., Mitchell K.E., Detamore M.S. Acomparison of human umbilical cord matrix stem cells and temporomandibular joint condylar chondrocytes for tissue engineering temporomandibular joint condylar cartilage. Tissue Eng 2007, 13:2003-2010.
18. Wang L., Singh M., Bonewald L.F., Detamore M.S. Signalling strategies for osteogenic differentiation of human umbilical cord mesenchymal stromal cells for 3D bone tissue engineering. JTissue Eng Regen Med 2009, 3:398-404.
19. Can A., Karahuseyinoglu S. Concise review: human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells 2007, 25:2886-2895.
20. Karahuseyinoglu S., Kocaefe C., Balci D., Erdemli E., Can A. Functional structure of adipocytes differentiated from human umbilical cord stroma-derived stem cells. Stem Cells 2008, 26:682-691.
21. Zhao L., Burguera E.F., Xu H.H.K., Amin N., Ryou H., Arola D.D. Fatigue and human umbilical cord stem cell seeding characteristics of calcium phosphate-chitosan-biodegradable fiber scaffolds. Biomaterials 2010, 31:840-847.
22. Wang L., Dormer N.H., Bonewald L.F., Detamore M.S. Osteogenic differentiation of human umbilical cord mesenchymal stromal cells in polyglycolic acid scaffolds. Tissue Eng Part A 2010, 16:1937-1948.
23. Zhao L., Weir M.D., Xu H.H.K. Human umbilical cord stem cell encapsulation in calcium phosphate scaffolds for bone engineering. Biomaterials 2010, 31:3848-3857.
24. Chen W.C., Zhou H.Z., Tang M.H., Weir M.D., Bao C.Y., Xu H.H.K. Gas-foaming calcium phosphate cement scaffold encapsulating human umbilical cord stem cells. Tissue Eng Part A 2012, 18:816-827.
25. Diao Y., Ma Q., Cui F., Zhong Y. Human umbilical cord mesenchymal stem cells: osteogenesis invivo as seed cells for bone tissue engineering. JBiomed Mater Res A 2009, 91:123-131.
26. Ruhe P.Q., Hedberg-Dirk E.L., Padron N.T., Spauwen P.H., Jansen J.A., Mikos A.G. Porous poly(DL-lactic-co-glycolic acid)/calcium phosphate cement composite for reconstruction of bone defects. Tissue Eng 2006, 12:789-800.
27. Ginebra M.P., Driessens F.C., Planell J.A. Effect of the particle size on the micro and nanostructural features of a calcium phosphate cement: a kinetic analysis. Biomaterials 2004, 25:3453-3462.
28. Habib M., Baroud G., Gitzhofer F., Bohner M. Mechanisms underlying the limited injectability of hydraulic calcium phosphate paste. Acta Biomater 2008, 4:1465-1471.
29. Zuo Y., Yang F., Wolke J.G., Li Y., Jansen J.A. Incorporation of biodegradable electrospun fibers into calcium phosphate cement for bone regeneration. Acta Biomater 2010, 6:1238-1247.
30. Friedman C.D., Costantino P.D., Takagi S., Chow L.C. BoneSource hydroxyapatite cement: a novel biomaterial for craniofacial skeletal tissue engineering and reconstruction. JBiomed Mater Res 1998, 43:428-432.
31. Jansen J.A., Vehof J.W., Ruhe P.Q., Kroeze-Deutman H., Kuboki Y., Takita H., et al. Growth factor-loaded scaffolds for bone engineering. JControl Release 2005, 101:127-136.
32. Kasten P., Beyen I., Niemeyer P., Luginbuhl R., Bohner M., Richter W. Porosity and pore size of beta-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: an invitro and invivo study. Acta Biomater 2008, 4:1904-1915.
33. Bohner M. Design of ceramic-based cements and putties for bone graft substitution. Eur Cell Mater 2010, 20:1-12.
34. Bohner M., Baroud G. Injectability of calcium phosphate pastes. Biomaterials 2005, 26:1553-1563.
35. Brown W.E., Chow L.C. Anew calcium phosphate water setting cement. Cements research progress 1986, 352-379. Am Ceram Soc, Westerville, OH. P.W. Brown (Ed.).
36. Schneiders W., Reinstorf A., Pompe W., Grass R., Biewener A., Holch M., et al. Effect of modification of hydroxyapatite/collagen composites with sodium citrate, phosphoserine, phosphoserine/RGD-peptide and calcium carbonate on bone remodelling. Bone 2007, 40:1048-1059.
37. Chen W.C., Zhou H.Z., Weir M.D., Tang M.H., Bao C.Y., Xu H.H.K. Human embryonic stem cell-derived mesenchymal stem cell seeding on calcium phosphate cement-chitosan-RGD scaffold for bone repair. Tissue Eng Part A 2013, 19:915-927.
38. Chen W.C., Zhou H.Z., Weir M.D., Bao C.Y., Xu H.H.K. Umbilical cord stem cells released from alginate-fibrin microbeads inside macroporous and biofunctionalized calcium phosphate cement for bone regeneration. Acta Biomater 2012, 8:2297-2306.
39. Park K.M., Joung K.J., Park K.D., Lee S.Y., Lee M.C. RGD-conjugated chitosan-pluronic hydrogels as a cell supported scaffold for articular cartilage regeneration. Macromol Res 2008, 16:517-523.
40. Zhou H.Z., Chen W.C., Weir M.D., Xu H.H.K. Biofunctionalized calcium phosphate cement to enhance the attachment and osteodifferentiation of stem cells released from fast-degradable alginate-fibrin microbeads. Tissue Eng Part A 2012, 18:1583-1595.
41. Hesaraki S., Zamanian A., Moztarzadeh F. The influence of the acidic component of the gas-foaming porogen used in preparing an injectable porous calcium phosphate cement on its properties: acetic acid versus citric acid. JBiomed Mater Res B Appl Biomater 2008, 86:208-216.
42. Cicuttini F.M., Begley C.G., Boyd A.W. The effect of recombinant stem cell factor (SCF) on purified CD34-positive human umbilical cord blood progenitor cells. Growth Factor 1992, 6:31-39.
43. Xu H.H.K., Zhao L., Weir M.D. Stem cell-calcium phosphate constructs for bone engineering. JDent Res 2010, 89:1482-1488.
44. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
45. Zou D., Zhang Z., He J., Zhu S., Wang S., Zhang W., et al. Repairing critical-sized calvarial defects with BMSCs modified by a constitutively active form of hypoxia-inducible factor-1alpha and a phosphate cement scaffold. Biomaterials 2011, 32:9707-9718.
46. Xu H.H.K., Simon C.G. Fast setting calcium phosphate-chitosan scaffold: mechanical properties and biocompatibility. Biomaterials 2005, 26:1337-1348.
47. Weir M.D., Xu H.H.K. Culture human mesenchymal stem cells with calcium phosphate cement scaffolds for bone repair. JBiomed Mater Res B Appl Biomater 2010, 93:93-105.
48. El-Ghannam A.R., Ducheyne P., Risbud M., Adams C.S., Shapiro I.M., Castner D., et al. Model surfaces engineered with nanoscale roughness and RGD tripeptides promote osteoblast activity. JBiomed Mater Res A 2004, 68:615-627.
49. Secchi A.G., Grigoriou V., Shapiro I.M., Cavalcanti-Adam E.A., Composto R.J., Ducheyne P., et al. RGDS peptides immobilized on titanium alloy stimulate bone cell attachment, differentiation and confer resistance to apoptosis. JBiomed Mater Res A 2007, 83:577-584.
50. Kim K., Dean D., Mikos A.G., Fisher J.P. Effect of initial cell seeding density on early osteogenic signal expression of rat bone marrow stromal cells cultured on cross-linked poly(propylene fumarate) disks. Biomacromolecules 2009, 10:1810-1817.
51. Reilly G.C., Radin S., Chen A.T., Ducheyne P. Differential alkaline phosphatase responses of rat and human bone marrow derived mesenchymal stem cells to 45S5 bioactive glass. Biomaterials 2007, 28:4091-4097.
52. Benoit D.S., Collins S.D., Anseth K.S. Multifunctional hydrogels that promote osteogenic hMSC differentiation through stimulation and sequestering of BMP2. Adv Funct Mater 2007, 17:2085-2093.
53. Zhu C., Chang Q., Zou D., Zhang W., Wang S., Zhao J., et al. LvBMP-2 gene-modified BMSCs combined with calcium phosphate cement scaffolds for the repair of calvarial defects in rats. JMater Sci Mater Med 2011, 22:1965-1973.
54. Carter D.R., Loboa P.E.G., Beaupre G.S. Mechanical influences on skeletal regeneration and bone resorption. Bone engineering 2000, 358-368. Em Squared Inc, Toronto. J.E. Davies (Ed.).
55. Lakey L.A., Akella R., Ranieri J.P. Angiogenesis: implications for tissue repair. Bone engineering 2000, 137-142. Em Squared Inc, Toronto, Canada. J.E. Davies (Ed.).
56. Yao Z., Lafage-Proust M.H., Plouet J., Bloomfield S., Alexandre C., Vico L. Increase of both angiogenesis and bone mass in response to exercise depends on VEGF. JBone Miner Res 2004, 19:1471-1480.
57. Veillette C.J., von Schroeder H.P. Endothelin-1 down-regulates the expression of vascular endothelial growth factor-A associated with osteoprogenitor proliferation and differentiation. Bone 2004, 34:288-296.
58. Kleinheinz J., Stratmann U., Joos U., Wiesmann H.P. VEGF-activated angiogenesis during bone regeneration. JOral Maxillofac Surg 2005, 63:1310-1316.
59. Piattelli A., Degidi M., Di Stefano D.A., Rubini C., Fioroni M., Strocchi R. Microvessel density in alveolar ridge regeneration with autologous and alloplastic bone. Implant Dent 2002, 11:370-375.
60. Degidi M., Artese L., Rubini C., Perrotti V., Iezzi G., Piattelli A. Microvessel density and vascular endothelial growth factor expression in sinus augmentation using Bio-Oss. Oral Dis 2006, 12:469-475.
61. Hsieh J.Y., Fu Y.S., Chang S.J., Tsuang Y.H., Wang H.W. Functional module analysis reveals differential osteogenic and stemness potentials in human mesenchymal stem cells from bone marrow and Wharton's jelly of umbilical cord. Stem Cells Dev 2010, 19:1895-1910.