Shear stress induces osteogenic differentiation of human mesenchymal stem cells

Regenerative Medicine

Volumn 5, Issue 5, 2010, Pages 713-724

  Yourek, Gregory ^a   McCormick, Susan M ^b   Mao, Jeremy J ^c   Reilly, Gwendolen C ^d  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b University of Illinois at Chicago   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d NONE

Author keywords

alkaline phosphatase; bone repair; mesenchymal; osteogenesis; shear stress; stem cells

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; MESSENGER RNA; OSTEOPONTIN;

ADULT; ARTICLE; BONE CELL; CELL DIFFERENTIATION; CELL STIMULATION; CELL STRESS; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; MECHANICAL STRESS; MESENCHYMAL STEM CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS;

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CULTURE MEDIA; HUMANS; KINETICS; MESENCHYMAL STEM CELLS; OSTEOBLASTS; OSTEOGENESIS; OSTEOPONTIN; RHEOLOGY; RNA, MESSENGER; STRESS, MECHANICAL;

EID: 77957172424     PISSN: 17460751     EISSN: None     Source Type: Journal    
DOI: 10.2217/rme.10.60     Document Type: Article

References (60)

1. Bennett JH, Joyner CJ, Triffitt JT, Owen ME: Adipocytic cells cultured from marrow have osteogenic potential. J. Cell Sci. 99 (Pt 1), 131-139 (1991).
2. Young RG, Butler DL, Weber W: Use of mesenchymal stem cells in a collagen matrix for achilles tendon repair. J. Orthop. Res. 16, 406-413 (1998).
3. Azizi SA, Stokes D, Augelli BJ: Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats - similarities to astrocyte grafts. Proc. Natl Acad. Sci. USA 95, 3908-3913 (1998).
4. Ferrari G, Cusella-De Angelis G, Coletta M: Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528-1530 (1998).
5. Alhadlaq A, Elisseeff JH, Hong L et al.: Adult stem cell driven genesis of humanshaped articular condyle. Ann. Biomed. Eng. 32(7), 911-923 (2004).
6. Marion NW, Mao JJ: Mesenchymal stem cells and tissue engineering. Methods Enzymol. 420, 339-361 (2006).
7. Lee CH, Marion N W, Hollister S, Mao JJ: Tissue formation and vascularization in anatomically shaped human joint condyle ectopically in vivo. Tissue Eng. Part A 15(12), 3923-3930 (2009).
8. Caplan AI, Bruder SP: Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol. Med. 7, 259-264 (2001).
9. Alhadlaq A, Mao JJ: Mesenchymal stem cells: isolation and therapeutics. Stem Cells Dev. 13(4), 436-448 (2004).
10. Zuk PA, Zhu M, Mizuno H et al.: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7(2), 211-228 (2001).
11. Pittenger MF, Mackay AM, Beck SC et al.: Multilieneage potential of adult human mesenchymal stem cells. Science 284, 143-147 (1999).
12. Cooper JA, Hewison M, Stewart PM: Glucocorticoid activity, inactivity and the osteoblast. J. Endocrinol. 163, 159-164 (1999).
13. Maniatopoulos C, Sodek J, Melcher AH: Bone formation in vitro by stromal cells obtained from bone marrow of young adult rats. Cell Tissue Res. 254, 317-330 (1988).
14. Choong PF, Martin TJ, Ng KW: Effects of ascorbic acid, calcitriol, and retinoic acid on the differentiation of preosteoblasts. J. Orthop. Res. 11(5), 638-647 (1993).
15. Osyczka AM, Diefenderfer DL, Bhargave G, Leboy PS: Different effects of BMP-2 on marrow stromal cells from human and rat bone. Cells Tissues Organs 176 (1-3), 109-119 (2004).
16. Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M: Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders. J. Bone Miner. Res. 13(3), 371-382 (1998).
17. Reid IR: Glucocorticoid-induced osteoporosis. Baillieres Best. Pract. Res. Clin. Endocrinol. Metab. 14(2), 279-298 (2000).
18. Weinstein RS, Jilka RL, Parfitt AM, Manolagas SC: 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(2), 274-282 (1998).
19. Batson EL, Reilly GC, Currey JD, Balderson DS: Postexercise and positional variation in mechanical properties of the radius in young horses. Equine. Vet. J. 32, 95-100 (2000).
20. Kopher RA, Mao JJ: Suture growth modulated by the oscillatory component of micromechanical strain. J. Bone Miner. Res. 18, 521-528 (2003).
21. You J, Yellowley CE, Donahue HJ, Zhang Y, Chen Q, Jacobs CR: Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. J. Biomech. Eng. 122(4), 387-393 (2000).
22. McGarry JG, Klein-Nulend J, Mullender MG, Prendergast PJ: A comparison of strain and fluid shear stress in stimulating bone cell responses - a computational and experimental study. FASEB J. 19(3), 482-484 (2005).
23. Tami AE, Schaffler MB, Tate MLK: Probing the tissue to subcellular level structure underlying bone's molecular sieving function. Biorheology 40(6), 577-590 (2003).
24. Reich KM, Gay CV, Frangos JA: Fluid shear stress as a mediator of osteoblast cyclic adenosine monophosphate production. J. Cell Physiol. 143, 100-104 (1990).
25. Sittichockechaiwut A, Scutt AS, Reilly GC: Short bouts of mechanical loading are as effective as dexamethasone at inducing matrix production by human bone marrow mesenchymal stem cell. Eur. Cell Mater. 20, 45-57 (2010).
26. Friedl G, Schmidt H, Rehak I, Kostner G, Schauenstein K, Windhager R: Undifferentiated human mesenchymal stem cells (hMSCs) are highly sensitive to mechanical strain: transcriptionally controlled early osteo-chondrogenic response in vitro. Osteoarthritis Cartilage 15(11), 1293-1300 (2007).
27. Kreke MR, Huckle WR, Goldstein AS: Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. Bone 36(6), 1047-1055 (2005).
28. Datta N, Pham QP, Sharma U, Sikavitsas VI, Jansen JA, Mikos AG: In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc. Natl Acad. Sci. USA 103(8), 2488-2493 (2006).
29. Jungreuthmayer C, Donahue SW, Jaasma MJ et al.: A comparative study of shear stresses in collagen-glycosaminoglycan and calcium phosphate scaffolds in bone tissue-engineering bioreactors. Tissue Eng. Part A 15(5), 1141-1149 (2009).
30. Frangos JA, Eskin SG, McIntire LV, Ives CL: Flow effects on prostacyclin production by cultured human endothelial cells. Science 227, 1477-1479 (1985).
31. Allen FD, Hung CT, Pollack SR, Brighton CT: Serum modulates the intracellular calcium response of primary cultured bone cells to shear flow. J. Biomech. 33(12), 1585-1591 (2000).
32. Frank O, Heim M, Jakob M et al.: Real-time quantitative RT-PCR ana lysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J. Cell Biochem. 85(4), 737-746 (2002).
33. Kulterer B, Friedl G, Jandrositz A et al.: Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics 8, 70 (2007).
34. Sugawara Y, Suzuki K, Koshikawa M, Ando M, Iida J: Necessity of enzymatic activity of alkaline phosphatase for mineralization of osteoblastic cells. Jpn J. Pharmacol. 88(3), 262-269 (2002).
35. Grellier M, Bareille R, Bourget C, Amedee J: Responsiveness of human bone marrow stromal cells to shear stress. J. Tissue Eng. Regen. Med. 3(4), 302-309 (2009).
36. Li YJ, Batra NN, You L et al.: Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation. J. Orthop. Res. 22(6), 1283-1289 (2004).
37. Low MG, Saltiel AR: Structural and functional roles of glycosylphosphatidylinositol in membranes. Science 239(4837), 268-275 (1988).
38. Yoshikawa M, Suzuki K, Takashi K, Koshikawa M, Imai T, Matsumoto A: Quantitative ana lysis of alkaline phosphtase activity and mineralization of a clonal osteoblast-like cell mc3t3-e1. J. Hard Tis. Bio. 8(2), 37-42 (1999).
39. Diefenderfer DL, Osyczka AM, Reilly GC, Leboy PS: BMP responsiveness in human mesenchymal stem cells. Connect. Tissue Res. 44 (Suppl. 1), 305-311 (2003).
40. Radomisli TE, Moore DC, Barrach HJ, Keeping HS, Ehrlich MG: Weight-bearing alters the expression of collagen types I and II, BMP 2/4 and osteocalcin in the early stages of distraction osteogenesis. J. Orthop. Res. 19(6), 1049-1056 (2001).
41. Sharp LA, Lee Y W, Goldstein AS: Effect of low-frequency pulsatile flow on expression of osteoblastic genes by bone marrow stromal cells. Ann. Biomed. Eng. 37(3), 445-453 (2009).
42. Diefenderfer DL, Osyczka AM, Garino JP, Leboy PS: Regulation of BMP-induced transcription in cultured human bone marrow stromal cells. J. Bone Joint Surg. Am. 85-A (Suppl. 3), 19-28 (2003).
43. You J, Reilly GC, Zhen X et al.: 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 (2001).
44. Harter LV, Hruska KA, Duncan RL: Human osteoblast-like cells respond to mechanical strain with increased bone matrix protein production independent of hormonal regulation. Endocrinology 136(2), 528-535 (1995).
45. Sittichockechaiwut A, Scutt AM, Ryan AJ, Bonewald LF, Reilly GC: Use of rapidly mineralising osteoblasts and short periods of mechanical loading to accelerate matrix maturation in 3D scaffolds. Bone 44(5), 822-829 (2009).
46. Klein-Nulend J, Roelofsen J, Semeins CM, Bronckers AL, Burger EH: Mechanical stimulation of osteopontin mrna expression and synthesis in bone cell cultures. J. Cell Physiol. 170(2), 174-181 (1997).
47. Miles RR, Turner CH, Santerre R et al.: Analysis of differential gene expression in rat tibia after an osteogenic stimulus in vivo: mechanical loading regulates osteopontin and myeloperoxidase. J. Cell Biochem. 68(3), 355-365 (1998).
48. Ganss B, Kim RH, Sodek J: Bone sialoprotein. Crit. Rev. Oral Biol. Med. 10(1), 79-98 (1999).
49. Ajubi NE, Klein-Nulend J, Nijweide PJ, Vrijheid-Lammers T, Alblas MJ, Burger EH: Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes - a cytoskeleton-dependent process. Biochem. Biophys. Res. Commun. 225(1), 62-68 (1996).
50. McGarry JG, Klein-Nulend J, Prendergast PJ: The effect of cytoskeletal disruption on pulsatile fluid flow-induced nitric oxide and prostaglandin E2 release in osteocytes and osteoblasts. Biochem. Biophys. Res. Commun. 330(1), 341-348 (2005).
51. Yourek G, Hussain MA, Mao JJ: Cytoskeletal changes of mesenchymal stem cells during differentiation. ASAIO J. 53(2), 219-228 (2007).
52. Yourek G, Alhadlaq A, Patel A et al.: Nanophysical properties of living cells: the cytoskeleton. In: Biological Nanostructures And Applications Of Nanostructures In Biology Electrical, Mechanical, And Optical Properties. Kluwer Academic Publishing, NY, USA 69-97 (2004).
53. Glossop JR, Cartmell SH: Effect of fluid flow-induced shear stress on human mesenchymal stem cells: differential gene expression of IL1B and MAP3K8 in MAPK signaling. Gene Expr. Patterns 9(5), 381-388 (2009).
54. Osyczka AM, Leboy PS: Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 146(8), 3428-3437 (2005).
55. Marie PJ, Fromigue O: Osteogenic differentiation of human marrow-derived mesenchymal stem cells. Regen. Med. 1(4), 539-548 (2006).
56. Altman GH, Horan RL, Martin I et al.: Cell differentiation by mechanical stress. FASEB J. 16(2), 270-272 (2002).
57. Reilly GC, Engler AJ: Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 43, 55-62 (2009).
58. Engler AJ, Sen S, Sweeney HL, Discher DE: Matrix elasticity directs stem cell lineage specification. Cell 126(4), 677-689 (2006).
59. Winer JP, Janmey PA, McCormick ME, Funaki M: Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng. Part A 15(1), 147-154 (2009).
60. Kopher RA: PhD thesis: Engineered osteogenesis of adult stem cells in polymeric scaffolds exposed to various mechanical stimuli. University of Illinois at Chicago College of Engineering, IL, USA (2006).