Study of bilineage differentiation of human-bone-marrow-derived mesenchymal stem cells in oxidized sodium alginate/N-succinyl chitosan hydrogels and synergistic effects of RGD modification and low-intensity pulsed ultrasound

Acta Biomaterialia

Volumn 10, Issue 6, 2014, Pages 2518-2528

  Wang, Yingying ^a   Peng, Wenzhen ^b   Liu, Xia ^a   Zhu, Minghua ^c   Sun, Tao ^c   Peng, Qiang ^c   Zeng, Yi ^c   Feng, Bo ^a   Zhi, Wei ^a   Weng, Jie ^a   Wang, Jianxin ^a  

^a SOUTHWEST JIAOTONG UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

^c Sichuan Provincial Centre for Disease Control and Prevention   (China)

Author keywords

Bone tissue engineering; Endothelial differentiation; Hydrogel; LIPUS; Osteogenic differentiation

Indexed keywords

BONE; CELL CULTURE; CELL ENGINEERING; CHITOSAN; ENDOTHELIAL CELLS; PHOSPHATASES; SCAFFOLDS (BIOLOGY); SODIUM; SODIUM ALGINATE; STEM CELLS; ULTRASONICS;

BONE TISSUE ENGINEERING; CHITOSAN HYDROGEL; ENDOTHELIAL DIFFERENTIATION; HUMAN BONE MARROW DERIVED MESENCHYMAL STEM CELLS; LOW-INTENSITY PULSED ULTRASOUND; N-SUCCINYL-CHITOSAN; OSTEOGENIC DIFFERENTIATION; SYNERGISTIC EFFECT; TISSUE ENGINEERING SCAFFOLD; VASCULARIZATION;

HYDROGELS;

ALGINIC ACID; ALKALINE PHOSPHATASE; CD31 ANTIGEN; CD34 ANTIGEN; CHITOSAN DERIVATIVE; N SUCCINYL CHITOSAN; UNCLASSIFIED DRUG; ARGINYL-GLYCYL-ASPARTIC ACID; CHITOSAN; GLUCURONIC ACID; HEXURONIC ACID; HYDROGEL; OLIGOPEPTIDE;

ARTICLE; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MINERALIZATION; CELL ADHESION; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CHEMICAL MODIFICATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HYDROGEL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LOW INTENSITY PULSED ULTRASOUND; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; OSTEOBLAST; OXIDATION; PRIORITY JOURNAL; TISSUE ENGINEERING; ULTRASOUND; BONE MARROW CELL; CELL CULTURE; CELL LINEAGE; CHEMISTRY; CYTOLOGY; MESENCHYMAL STROMA CELL; OXIDATION REDUCTION REACTION;

ALGINATES; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHITOSAN; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; HYDROGELS; MESENCHYMAL STROMAL CELLS; OLIGOPEPTIDES; OXIDATION-REDUCTION; ULTRASONICS;

EID: 84899629059     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.12.052     Document Type: Article

References (56)

1. Seidi A, Ramalingam M, Elloumi-Hannachi I, Ostrovidov S, Khademhosseini A. Gradient biomaterials for soft-to-hard interface tissue engineering. Acta Biomaterialia 2011;7:1441-51.
2. Thein-Han W, Misra R. Biomimetic chitosan-nanohydroxyapatite composite scaffolds for bone tissue engineering. Acta Biomaterialia 2009;5:1182-97.
3. Drury JL, Mooney DJ. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 2003;24:4337-51.
4. He FP, Ye JD. In vitro degradation, biocompatibility, and in vivo osteogenesis of poly(lactic-co-glycolic acid)/calcium phosphate cement scaffold with unidirectional lamellar pore structure. J Biol Mater Res 2012;100A:3239-50.
5. Boccaccini AR, Kneser U, Arkudas A. Scaffolds for vascularized bone regeneration: advances and challenges. Expert Rev Med Dev 2012;9:457-60.
6. Le Visage C, Gournay O, Benguirat N, Hamidi S, Chaussumier L, Mougenot N, et al. Mesenchymal stem cell delivery into rat infarcted myocardium using a porous polysaccharide-based scaffold: a quantitative comparison with endocardial injection. Tissue Eng part A 2012;18:35-44.
7. Urist MR. Bone: formation by autoinduction. Science 1965;150:893-9.
8. Dzau VJ, Gnecchi M, Pachori AS, Morello F, Melo LG. Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension 2005;46:7-18.
9. Griffon DJ, Sedighi MR, Schaeffer DV, Eurell JA, Johnson AL. Chitosan scaffolds: interconnective pore size and cartilage engineering. Acta Biomaterialia 2006;2:313-20.
10. Whang K, Healy KE, Elenz DR, Nam EK, Tsai DC, Thomas CH, et al. Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture. Tissue Eng 1999;5:35-51.
11. Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 2006;27:3413-31.
12. Li ZS, Ramay HR, Hauch KD, Xiao DM, Zhang MQ. Chitosan-alginate hybrid scaffolds for bone tissue engineering. Biomaterials 2005;26:3919-28.
13. Rogalsky AD, Kwon HJ, Lee-Sullivan P. Compressive stress-strain response of covalently crosslinked oxidized-alginate/N-succinyl-chitosan hydrogels. J Biomed Mater Res A 2011;99:367-75.
14. Köllmer M, Keskar V, Hauk TG, Collins JM, Russell B, Gemeinhart RA. Stem cellderived extracellular matrix enables survival and multilineage differentiation within superporous hydrogels. Biomacromolecules 2012;13:963-73.
15. Spadaro JA, Albanese SA. Application of low-intensity ultrasound to growing bone in rats. Ultrasound Med Biol 1998;24:567-73.
16. Warden SJ, Favaloro JM, Bennell KL, McMeeken JM, Ng KW, Zajac JD, et al. Lowintensity pulsed ultrasound stimulates a bone-forming response in UMR-106 cells. Biochem Biophys Res Commun 2001;286:443-50.
17. Naruse K, Mikuni-Takagaki Y, Azuma Y, Ito M, Oota T, Kameyama K, et al. Anabolic response of mouse bone-marrow-derived stromal cell clone ST2 cells to low-intensity pulsed ultrasound. Biochem Biophys Res Commun 2000;268:216-20.
18. Ito M, Azuma Y, Ohta T, Komoriya K. Effects of ultrasound and 1,25- dihydroxyvitamin D3 on growth factor secretion in co-cultures of osteoblasts and endothelial cells. Ultrasound Med. Biol 2000;26:161-6.
19. Sun S, Wang A. Adsorption properties of N-succinyl-chitosan and cross-linked N-succinyl-chitosan resin with Pb(II) as template ions. Sep Purif Technol 2006;51:409-15.
20. Yamaguchi R, Araj Y, Itoh T, Hirano S. Preparation of partially N-succinylated chitosans and their cross-linked gels. Carbohyd Res 1981;88:172-5.
21. Fan LH, Pan XR, Zhou Y, Chen LY, Xie WG, Long ZH, et al. Preparation and characterization of crosslinked carboxymethyl chitosan-oxidized sodium alginate hydrogels. J App Poly Sci 2011;122:2331-7.
22. Gao CM, Liu MZ, Chen J, Zhang X. Preparation and controlled degradation of oxidized sodium alginate hydrogel. Polym Degrad Stabil 2009;94:1405-10.
23. Liu X, Peng WZ, Wang YY, Zhu MH, Sun T, Peng Q, et al. Synthesis of an RGDgrafted oxidized sodium alginate-N-succinyl chitosan hydrogel and an in vitro study of endothelial and osteogenic differentiation. J Mater Chem B 2013;1: 4484-92.
24. Cao Y, Sun Z, Liao LM, Meng Y, Han Q, Zhao RCH. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun 2005;332:370-9.
25. Schneider RK, Puellen A, Kramann R, Raupach K, Bornemann J, Knuechel R, et al. The osteogenic differentiation of adult bone marrow and perinatal umbilical mesenchymal stem cells and matrix remodelling in threedimensional collagen scaffolds. Biomaterials 2010;31:467-80.
26. Wang MK, Su YP, Sun HQ, Wang T, Yan GH, Ran XZ, et al. Induced endothelial differentiation of cells from a murine embryonic mesenchymal cell line C3H/ 10T1/2 by angiogenic factors in vitro. Differentiation 2010;79:21-30.
27. Zhang W, Yang N, Shi XM. Regulation of mesenchymal stem cell osteogenic differentiation by glucocorticoid-induced leucine zipper (GILZ). J Biol Chem 2008;283:4723-9.
28. Takayama T, Suzuki N, Ikeda K, Shimada T, Suzuki A, Maeno M, et al. Lowintensity pulsed ultrasound stimulates osteogenic differentiation in ROS 17/ 2.8 cells. Life Sci 2007;80:965-71.
29. Zeng R, Wang LW, Hu ZB, Guo WT, Wei JS, Lin H, et al. Differentiation of human bone marrow mesenchymal stem cells into neuron-like cells in vitro. Spine 2011;36:997-1005.
30. Choi CB, Cho YK, Prakash KVB, Jee BK, Han CW, Paik YK, et al. Analysis of neuron-like differentiation of human bone marrow mesenchymal stem cells. Biochem Biophys Res Commun 2006;350:138-46.
31. Gade N, Pratheesh M, Nath A, Dubey P, Sharma B, Saikumar G, et al. Molecular and cellular characterization of buffalo bone marrow-derived mesenchymal stem cells. Reprod Domestic Animals 2012;48:358-67.
32. Zheng HZ, Liu C, Ou YF, Zhang YJ, Fu XK. Total saponins of Panax notoginseng enhance VEGF and relative receptors signals and promote angiogenesis derived from rat bone marrow mesenchymal stem cells. J Ethnopharmacol 2013;147:595-602.
33. Kim BS, Kim JS, Chung YS, Sin YW, Ryu KH, Lee J, et al. Growth and osteogenic differentiation of alveolar human bone marrow-derived mesenchymal stem cells on chitosan/hydroxyapatite composite fabric. J Biol Mater Res 2013;101:1550-8.
34. Ehrlich PJ, Lanyon LE. Mechanical strain and bone cell function: a review. Osteoporos Int 2002;13:688-700.
35. Magnusson P, Larsson L, Magnusson M, Davie MW, Sharp CA. Isoforms of bone alkaline phosphatase: characterization and origin in human trabecular and cortical bone. Bone Miner Res 1999;14:1926-33.
36. Anderson H. Mechanism of mineral formation in bone. J technical methods and pathology. 1989;60:320-30.
37. Gerstenfeld LC, Chipman SD, Glowacki J, Lian JB. Expression of differentiated function by mineralizing cultures of chicken osteoblasts. Dev Biol 1987;122: 49-60.
38. Sugawara Y, Suzuki K, Koshikawa M, Ando M, Iida J. Necessity of enzymatic activity of alkaline phosphatase for mineralization of osteoblastic cells. Japanese J Pharmacol 2002;88:262-9.
39. Aubin J, Liu F, Malaval L, Gupta A. Osteoblast and chondroblast differentiation. Bone 1995;17:S77-83.
40. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 1997;64:295-312.
41. Wang D, Haile A, Jones LC. Dexamethasone-induced lipolysis increases the adverse effect of adipocytes on osteoblasts using cells derived from human mesenchymal stem cells. Bone 2013;53:520-30.
42. Moreira SM, Andrade FK, Domingues L, Gama M. Development of a strategy to functionalize a dextrin-based hydrogel for animal cell cultures using a starchbinding module fused to RGD sequence. BMC Biotechnol 2008;8:78.
43. Wang L, Dormer NH, Bonewald LF, Detamore MS. Osteogenic differentiation of human umbilical cord mesenchymal stromal cells in polyglycolic acid scaffolds. Tissue Eng 2010;16:1937-48.
44. Parvizi J, Wu CC, Lewallen DG, Greenleaf JF, Bolander ME. Low-intensity ultrasound stimulates proteoglycan synthesis in rat chondrocytes by increasing aggrecan gene expression. J Orthop Res 1999;17:488-94.
45. Zhang ZJ, Huckle J, Francomano CA, Spencer RG. The effects of pulsed lowintensity ultrasound on chondrocyte viability, proliferation, gene expression and matrix production. Ultrasound Med Biol 2003;29:1645-51.
46. Li L, Yang Z, Zhang H, Chen W, Chen M, Zhu Z. Low-intensity pulsed ultrasound regulates proliferation and differentiation of osteoblasts through osteocytes. Biochem Biophys Res Commun 2012;418:296-300.
47. Reher P, Harris M, Whiteman M, Hai H, Meghji S. Ultrasound stimulates nitric oxide and prostaglandin E2 production by human osteoblasts. Bone 2002;31:236-41.
48. Korstjens C, Nolte P, Burger E, Albers G, Semeins C, Aartman I, et al. Stimulation of bone cell differentiation by low-intensity ultrasound - a histomorphometric in vitro study. J Orthop Res 2004;22:495-500.
49. Chen YJ, Wang CJ, Yang KD, Chang PR, Huang HC, Huang YT, et al. Pertussis toxin-sensitive GKi protein and ERK-dependent pathways mediate ultrasound promotion of osteogenic transcription in human osteoblasts. FEBS Lett 2003;554:154-8.
50. Jiang T, Xu T, Gu F, Chen A, Xiao Z, Zhang D. Osteogenic effect of low intensity pulsed ultrasound on rat adipose-derived stem cells in vitro. J Huazhong Univ Sci Technol-Med Sci 2012;32:75.
51. Chen SH, Chiu CY, Yeh JM, Wang SH, Effect of low intensity ultrasounds on the growth of osteoblasts, Engineering in Medicine and Biology Society, 2007. EMBS 2007. 29th Annual International Conference of the IEEE. IEEE, 2007, 5833-5836.
52. Doan N, Reher P, Meghji S, Harris M. In vitro effects of therapeutic ultrasound on cell proliferation, protein synthesis, and cytokine production by human fibroblasts, osteoblasts, and monocytes. J Oral Maxillofac Surg 1999;57: 409-19.
53. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 2007;292:H1209-24.
54. Chun C, Lim HJ, Hong K-Y, Park K-H, Song S-C. The use of injectable, thermosensitive poly (organophosphazene)-RGD conjugates for the enhancement of mesenchymal stem cell osteogenic differentiation. Biomaterials 2009;30:6295-308.
55. Taubenberger AV, Woodruff MA, Bai H, Muller DJ, Hutmacher DW. The effect of unlocking RGD-motifs in collagen I on pre-osteoblast adhesion and differentiation. Biomaterials 2010;31:2827-35.
56. Dinno M, Dyson M, Young S, Mortimer A, Hart J, Crum L. The significance of membrane changes in the safe and effective use of therapeutic and diagnostic ultrasound. Phys Med Biol 1989;34:1543.