Short bouts of mechanical loading are as effective as dexamethasone at inducing matrix production by human bone marrow mesenchymal stem cells

European Cells and Materials

Volumn 20, Issue , 2010, Pages 45-57

  Sittichokechaiwut, A ^a   Edwards, J H ^b   Scutt, A M ^c   Reilly, G C ^b  

^a NARESUAN UNIVERSITY   (Thailand)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Biomaterials scaffolds; Bioreactors; Bone; Bone mineralization; Collagen; Osteogenesis; Repair regeneration; Stem cells

Indexed keywords

ALKALINE PHOSPHATASE; COLLAGEN TYPE 1; DEXAMETHASONE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; OSTEOPONTIN; TRANSCRIPTION FACTOR RUNX2; GLUCOCORTICOID; TRANSCRIPTION FACTOR RUNX;

ADULT; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; CELL VIABILITY; COLORIMETRY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; LOADING TEST; MALE; MESENCHYMAL STEM CELL; MINERALIZATION; OSTEOBLAST; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR STRESS; UPREGULATION; BONE MINERALIZATION; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; EXTRACELLULAR MATRIX; GENETICS; MECHANICS; MESENCHYMAL STROMA CELL; METABOLISM; TISSUE ENGINEERING;

ALKALINE PHOSPHATASE; BONE MARROW CELLS; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; COLLAGEN TYPE I; CORE BINDING FACTOR ALPHA SUBUNITS; DEXAMETHASONE; EXTRACELLULAR MATRIX; GLUCOCORTICOIDS; HUMANS; MECHANICAL PHENOMENA; MESENCHYMAL STROMAL CELLS; OSTEOPONTIN; RNA, MESSENGER; TISSUE ENGINEERING;

EID: 77957158635     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v020a05     Document Type: Article

References (72)

1. Arnsdorf EJ, Tummala P, Kwon RY, Jacobs CR (2009) Mechanically induced osteogenic differentiation-the role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sci 122: 546-553.
2. Aubin JE (1999) Osteoprogenitor cell frequency in rat bone marrow stromal populations: role for heterotypic cellcell interactions in osteoblast differentiation. J Cell Biochem 72: 396-410.
3. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME (1992) Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102: 341-351.
4. Bianco P, Kuznetsov SA, Riminucci M, Gehron Robey P (2006) Postnatal skeletal stem cells. Methods Enzymol 419: 117-148.
5. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S (1998) The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am, 80:985-996.
6. Byrne EM, Farrell E, McMahon LA, Haugh MG, O'Brien FJ, Campbell VA, Prendergast PJ, O'Connell BC (2008) Gene expression by marrow stromal cells in a porous collagen-glycosaminoglycan scaffold is affected by pore size and mechanical stimulation. J Mater Sci Mater Med 19: 3455-3463.
7. Cartmell SH, Porter BD, Garcia AJ, Guldberg RE (2003) Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng 9: 1197-1203.
8. Canalis E, Economides AN, Gazzerro E (2003) Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24: 218-235.
9. Cowie R, Walker RD, Scutt A (2006) The use of highfrequency, low-intensity vibration to stimulate the proliferation and differentiation of primary rat bone marrow cells. Cytotherapy 8: 63-63.
10. Datta N, Holtorf HL, Sikavitsas VI, Jansen JA, Mikos AG (2005) Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials 26: 971-977.
11. Diederichs S, Freiberger F, van Griensven M (2009) Effects of repetitive and short time strain in human bone marrow stromal cells. J Biomed Mater Res A 88: 907-915.
12. Diefenderfer DL, Osyczka AM, Garino JP, Leboy PS (2003) Regulation of BMP-induced transcription in cultured human bone marrow stromal cells. J Bone Joint Surg Am, 85-A Suppl 3: 19-28.
13. Dieudonne SC, Kerr JM, Xu T, Sommer B, DeRubeis AR, Kuznetsov SA, Kim IS, Gehron Robey P, Young MF (1999) Differential display of human marrow stromal cells reveals unique mRNA expression patterns in response to dexamethasone. J Cell Biochem, 76:231-243.
14. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
15. Donahue TLH, Haut TR, Yellowley CE, Donahue HJ, Jacobs CR (2003) Mechanosensitivity of bone cells to oscillating fluid flow induced shear stress may be modulated by chemotransport. J Biomech 36: 1363-1371.
16. Duty AO, Oest ME, Guldberg RE (2007) Cyclic mechanical compression increases mineralization of cellseeded polymer scaffolds in vivo. J Biomech Eng 129: 531-539.
17. Friedl G, Schmidt H, Rehak I, Kostner G, Schauenstein K, Windhager R (2007) Undifferentiated human mesenchymal stem cells (hMSCs) are highly sensitive to mechanical strain: transcriptionally controlled early osteochondrogenic response in vitro. Osteoarthritis Cartilage, 15:1293-1300.
18. Grayson WL, Bhumiratana S, Cannizzaro C, Chao PH, Lennon DP, Caplan AI, Vunjak-Novakovic G (2008) Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng Part A 14: 1809-1820.
19. Gregory CA, Gunn WG, Peister A, Prockop DJ (2004) An alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 329: 77-84.
20. Grellier M, Bareille R, Bourget C, Amedee J (2009) Responsiveness of human bone marrow stromal cells to shear stress. J Tissue Eng Regen Med 3: 302-309.
21. Guelcher SA, Patel V, Gallagher KM, Connolly S, Didier JE, Doctor JS, Hollinger JO (2006) Synthesis and in vitro biocompatibility of injectable polyurethane foam scaffolds. Tissue Eng 12: 1247-1259.
22. Heath CA (2000) Cells for tissue engineering. Trends Biotechnol 18: 17-19.
23. Heng BC, Cao T, Stanton LW, Robson P, Olsen B (2004) Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J Bone Miner Res 19: 1379-1394.
24. Holtorf HL, Jansen JA, Mikos AG (2005) Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexamethasone. J Biomed Mater Res A 72: 326-334.
25. Huang CY, Hagar KL, Frost LE, Sun Y, Cheung HS (2004) Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 22: 313-323.
26. Jagodzinski M, Drescher M, Zeichen J, Hankemeier S, Krettek C, Bosch U, van Griensven M (2004) Effects of cyclic longitudinal mechanical strain and dexamethasone on osteogenic differentiation of human bone marrow stromal cells. Eur Cell Mater 7: 35-41.
27. Jagodzinski M, Breitbart A, Wehmeier M, Hesse E, Haasper C, Krettek C, Zeichen J, Hankemeier S (2008) Influence of perfusion and cyclic compression on proliferation and differentiation of bone marrow stromal cells in 3-dimensional culture. J Biomech 41: 1885-1891.
28. Karsenty G (2001) Minireview: transcriptional control of osteoblast differentiation. Endocrinology 142: 2731-2733.
29. Klein-Nulend J, Bacabac RG, Mullender MG (2005) Mechanobiology of bone tissue. Pathol Biol (Paris) 53: 576-580.
30. Kreke MR, Sharp LA, Lee YW, Goldstein AS (2008) Effect of intermittent shear stress on mechanotransductive signaling and osteoblastic differentiation of bone marrow stromal cells. Tissue Eng Part A 14: 529-537.
31. Lacroix D, Chateau A, Ginebra MP, Planell JA (2006) Micro-finite element models of bone tissue engineering scaffolds. Biomaterials 27: 5326-5334.
32. Lecoeur L, Ouhayoun JP (1997) In vitro induction of osteogenic differentiation from non-osteogenic mesenchymal cells. Biomaterials 18: 989-993.
33. Lian JB, Stein GS, Stein JL, van Wijnen AJ (1998) Transcriptional control of osteoblast differentiation. Biochem Soc Trans 26: 14-21.
34. Maniatopoulos C, Sodek J, Melcher AH (1988) Bone formation in vitro by stromal cells obtained from bone marrow of young adult rats. Cell Tissue Res 254: 317-330.
35. Mauney JR, Blumberg J, Pirun M, Volloch V, Vunjak-Novakovic G, Kaplan DL (2004a) Osteogenic differentiation of human bone marrow stromal cells on partially demineralized bone scaffolds in vitro. Tissue Eng 10: 81-92.
36. Mauney JR, Sjostorm S, Blumberg J, Horan R, O'Leary JP, Vunjak-Novakovic G, Volloch V, Kaplan DL (2004b) Mechanical stimulation promotes osteogenic differentiation of human bone marrow stromal cells on 3-D partially demineralized bone scaffolds in vitro. Calcif Tissue Int 74: 458-468.
37. Mauth C, Bono E, Haas S, Paesold G, Wiese H, Maier G, Boos N, Graf-Hausner U (2009) Cell-seeded polyurethane-fibrin structures - a possible system for intervertebral disc regeneration. Eur Cell Mater 18: 27-38.
38. Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, Zichner L, Kaplan D, Langer R, Vunjak-Novakovic G (2004) Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann Biomed Eng 32: 112-122.
39. Ng KW, Leong DT, Hutmacher DW (2005) The challenge to measure cell proliferation in two and three dimensions. Tissue Eng 11: 182-191.
40. O'Brien FJ, Harley BA, Waller MA, Yannas IV, Gibson LJ, Prendergast PJ (2007) The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol Health Care 15: 3-17.
41. Osyczka AM, Noth U, O'Connor J, Caterson EJ, Yoon K, Danielson KG, Tuan RS (2002) Multilineage differentiation of adult human bone marrow progenitor cells transduced with human papilloma virus type 16 E6/ E7 genes. Calcif Tissue Int 71: 447-458.
42. Peter SJ, Liang CR, Kim DJ, Widmer MS, Mikos AG (1998) Osteoblastic phenotype of rat marrow stromal cells cultured in the presence of dexamethasone, betaglycerolphosphate, and L-ascorbic acid. J Cell Biochem 71: 55-62.
43. Porter RM, Huckle WR, Goldstein AS (2003) Effect of dexamethasone withdrawal on osteoblastic differentiation of bone marrow stromal cells. J Cell Biochem 90: 13-22.
44. Reilly GC, Engler AJ (2009) Intrinsic extracellular matrix properties regulate stem cell differentiation. J Biomech 1: 1.
45. Reilly GC, Radin S, Chen AT, Ducheyne P (2007) Differential alkaline phosphatase responses of rat and human bone marrow derived mesenchymal stem cells to 45S5 bioactive glass. Biomaterials 28: 4091-4097.
46. Robey PG, Bianco P (2006) The use of adult stem cells in rebuilding the human face. J Am Dent Assoc, 137:961-972.
47. Roshan-Ghias A, Terrier A, Bourban PE, Pioletti DP (2010) In vivo cyclic loading as a potent stimulatory signal for bone formation inside tissue engineering scaffold. Eur Cell Mater 19: 41-49.
48. Rubin J, Rubin C, Jacobs CR (2006) Molecular pathways mediating mechanical signaling in bone. Gene 367: 1-16.
49. Schliephake H, Knebel JW, Aufderheide M, Tauscher M (2001) Use of cultivated osteoprogenitor cells to increase bone formation in segmental mandibular defects: an experimental pilot study in sheep. Int J Oral Maxillofac Surg 30: 531-537.
50. Sharp LA, Lee YW, Goldstein AS (2009) Effect of lowfrequency pulsatile flow on expression of osteoblastic genes by bone marrow stromal cells. Ann Biomed Eng 37: 445-453.
51. Simmons CA, Matlis S, Thornton AJ, Chen S, Wang CY, Mooney DJ (2003) Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J Biomech 36: 1087-1096.
52. Sittichokechaiwut A, Reilly GC (2009). Development of a culture system to modulate tissue engineered bone formation by varying loading conditions. Proc 7th IntConf Manufact Res (ICMR 09), pp 443-448.
53. Sittichockechaiwut A, Scutt AM, Ryan AJ, Bonewald L, Reilly GC (2009) Use of rapidly mineralizing osteoblasts and short periods of mechanical loading to accelerate matrix maturation in 3D scaffolds. Bone 44: 822-829.
54. Sumanasinghe RD, Bernacki SH, Loboa EG (2006) Osteogenic differentiation of human mesenchymal stem cells in collagen matrices: effect of uniaxial cyclic tensile strain on bone morphogenetic protein (BMP-2) mRNA expression. Tissue Eng 12: 3459-3465.
55. Taguchi Y, Yamamoto M, Yamate T, Lin SC, Mocharla H, DeTogni P, Nakayama N, Boyce BF, Abe E, Manolagas SC (1998) Interleukin-6-type cytokines stimulate mesenchymal progenitor differentiation toward the osteoblastic lineage. Proc Assoc Am Physicians 110: 559-574.
56. Tullberg-Reinert H, Jundt G (1999) In situ measurement of collagen synthesis by human bone cells with a Sirius red-based colorimetric microassay: effects of transforming growth factor beta2 and ascorbic acid 2- phosphate. Histochem Cell Biol 112: 271-276.
57. Turner CH, Owan I, Alvey T, Hulman J, Hock JM (1998) Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone 22: 463-469.
58. Vaccaro AR, Chiba K, Heller JG, Patel T, Thalgott JS, Truumees E, Fischgrund JS, Craig MR, Berta SC, Wang JC (2002) Bone grafting alternatives in spinal surgery. Spine J 2: 206-215.
59. Van Leeuwen JP, Van Driel M, Van den Bemd GJ, Pols HA (2001) Vitamin D control of osteoblast function and bone extracellular matrix mineralization. Crit Rev Eukaryot Gene Expr 11: 199-226.
60. Weinstein RS, Jilka RL, Parfitt AM, Manolagas SC (1998) Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids - Potential mechanisms of their deleterious effects on bone. J Clin Invest 102: 274-282.
61. Weissman IL (2000) Translating stem and progenitor cell biology to the clinic: barriers and opportunities. Science 287: 1442-1446.
62. Wozniak M, Fausto A, Carron CP, Meyer DM, Hruska KA (2000) Mechanically strained cells of the osteoblast lineage organize their extracellular matrix through unique sites of alphavbeta3-integrin expression. J Bone Miner Res 15: 1731-1745.
63. Yoshikawa T, Ohgushi H, Tamai S (1996) Immediate bone forming capability of prefabricated osteogenic hydroxyapatite. J Biomed Mater Res 32: 481-492.
64. You J, Reilly GC, Zhen X, Yellowley CE, Chen Q, Donahue HJ, Jacobs CR (2001) Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen activated protein kinase in MC3T3-E1 osteoblasts. J Biol Chem 276: 13365-13371.
65. Yourek G, McCormick SM, Mao JJ, Reilly GC (2010) Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regenerative Medicine, in press.
66. Zanetta M, Quirici N, Demarosi F, Tanzi MC, Rimondini L, Fare S (2009) Ability of polyurethane foams to support cell proliferation and the differentiation of MSCs into osteoblasts. Acta Biomater 5: 1126-1136.
67. Farrell E, O'Brien FJ, Doyle P, Fischer J, Yannas I, Harley BA, O'Connell B, Prendergast PJ, Campbell VA (2006) A collagen-glycosaminoglycan scaffold supports adult rat mesenchymal stem cell differentiation along osteogenic and chondrogenic routes. Tissue Eng 12: 459-468.
68. Glossop JR, Cartmell SH (2009) Effect of fluid flowinduced shear stress on human mesenchymal stem cells: Differential gene expression of IL1B and MAP3K8 in MAPK signaling. Gene Expr Patt 9: 381-388.
69. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger MF (2000) Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen activated protein kinase. J Biol Chem 275: 9645-9652.
70. Kim SH, Choi YR, Park MS, Shin JW, Park KD, Kim SJ, Lee JW (2007) Erk 1/2 activation in enhanced osteogenesis of human mesenchymal stem cells in poly(lactic-glycolic acid) by cyclic hydrostatic pressure. J Biomed Mater Res 80A: 826-836.
71. Lund AW, Stegemann JP, Plopper GE (2009) Inhibition of ERK promotes collagen gel compaction and fibrillogenesis to amplify the osteogenesis of human mesenchymal stem cells in three-dimensional collagen I culture. Stem Cells Dev 18: 331-41.
72. Osyczka AM, Leboy PS (2005) Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signalregulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 146: 3428-3437.