Macro and microfluidic flows for skeletal regenerative medicine

Cells

Volumn 1, Issue 4, 2012, Pages 1225-1245

  Riehl, Brandon D ^a   Yul Lim, Jung ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

2D and 3D; Bone; Fluid flow; Macroflow; Mechanotransduction; Microfluidics; Regenerative medicine

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALKALINE PHOSPHATASE; ALPHA ACTININ; BONE MORPHOGENETIC PROTEIN 2; CYCLOOXYGENASE 2; FOCAL ADHESION KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERSTITIAL COLLAGENASE; MATRIX EXTRACELLULAR PHOSPHOGLYCOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; OSTEOCALCIN; OSTEOPONTIN; PAXILLIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN E2; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STROMELYSIN; TALIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; VINCULIN;

BONE CELL; BONE REGENERATION; CALCIUM SIGNALING; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOSKELETON; EXTRACELLULAR MATRIX; FLOW RATE; FLUID FLOW; HUMAN; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCYTE; REGENERATIVE MEDICINE; REVIEW; SIGNAL TRANSDUCTION; SKELETON; STRESS FIBER; TEMPOROMANDIBULAR JOINT; TISSUE ENGINEERING;

EID: 84882268301     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells1041225     Document Type: Review

References (85)

1. Riddle, R.C.; Donahue, H.J. From streaming-potentials to shear stress: 25 years of bone cell mechanotransduction. J. Orthop. Res. 2009, 27, 143-149.
2. Wu, H.W.; Lin, C.C.; Lee, G.B. Stem cells in microfluidics. Biomicrofluidics 2011, 5, 13401.
3. Bennett, M.R.; Hasty, J. Microfluidic devices for measuring gene network dynamics in single cells. Nat. Rev. Genet. 2009, 10, 628-638.
4. Li, J.; Rose, E.; Frances, D.; Sun, Y.; You, L. Effect of oscillating fluid flow stimulation on osteocyte mRNA expression. J. Biomech. 2012, 45, 247-251.
5. Rumney, R.M.; Sunters, A.; Reilly, G.C.; Gartland, A. Application of multiple forms of mechanical loading to human osteoblasts reveals increased ATP release in response to fluid flow in 3D cultures and differential regulation of immediate early genes. J. Biomech. 2012, 45, 549-554.
6. Lu, X.L.; Huo, B.; Chiang, V.; Guo, X.E. Osteocytic network is more responsive in calcium signaling than osteoblastic network under fluid flow. J. Bone Miner. Res. 2012, 27, 563-574.
7. Ponik, S.M.; Triplett, J.W.; Pavalko, F.M. Osteoblasts and osteocytes respond differently to oscillatory and unidirectional fluid flow profiles. J. Cell. Biochem. 2007, 100, 794-807.
8. Genetos, D.C.; Kephart, C.J.; Zhang, Y.; Yellowley, C.E.; Donahue, H.J. Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J. Cell. Physiol. 2007, 212, 207-214.
9. Gardinier, J.D.; Majumdar, S.; Duncan, R.L.; Wang, L. Cyclic hydraulic pressure and fluid flow differentially modulate cytoskeleton re-organization in MC3T3 osteoblasts. Cell. Mol. Bioeng. 2009, 2, 133-143.
10. Jackson, W.M.; Jaasma, M.J.; Tang, R.Y.; Keaveny, T.M. Mechanical loading by fluid shear is sufficient to alter the cytoskeletal composition of osteoblastic cells. Am. J. Physiol. Cell. Physiol. 2008, 295, C1007-C1015.
11. Donahue, H.J. Gap junctions and biophysical regulation of bone cell differentiation. Bone 2000, 26, 417-422.
12. Hoey, D.A.; Kelly, D.J.; Jacobs, C.R. A role for the primary cilium in paracrine signaling between mechanically stimulated osteocytes and mesenchymal stem cells. Biochem. Biophys. Res. Commun. 2011, 412, 182-187.
13. Taylor, A.F.; Saunders, M.M.; Shingle, D.L.; Cimbala, J.M.; Zhou, Z.; Donahue, H.J. Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. Am. J. Physiol. Cell. Physiol. 2007, 292, C545-C552.
14. Kulkarni, R.N.; Bakker, A.D.; Everts, V.; Klein-Nulend, J. Inhibition of osteoclastogenesis by mechanically loaded osteocytes: involvement of MEPE. Calcif. Tissue Int. 2010, 87, 461-468.
15. Kim, C.H.; You, L.; Yellowley, C.E.; Jacobs, C.R. Oscillatory fluid flow-induced shear stress decreases osteoclastogenesis through RANKL and OPG signaling. Bone 2006, 39, 1043-1047.
16. Malone, A.M.; Batra, N.N.; Shivaram, G.; Kwon, R.Y.; You, L.; Kim, C.H.; Rodriguez, J.; Jair, K.; Jacobs, C.R. The role of actin cytoskeleton in oscillatory fluid flow-induced signaling in MC3T3-E1 osteoblasts. Am. J. Physiol. Cell. Physiol. 2007, 292, C1830-C1836.
17. Pavalko, F.M.; Chen, N.X.; Turner, C.H.; Burr, D.B.; Atkinson, S.; Hsieh, Y.F.; Qiu, J.; Duncan, R.L. Fluid shear-induced mechanical signaling in MC3T3-E1 osteoblasts requires cytoskeleton-integrin interactions. Am. J. Physiol. 1998, 275, C1591-C1601.
18. Morris, H.L.; Reed, C.I.; Haycock, J.W.; Reilly, G.C. Mechanisms of fluid-flow-induced matrix production in bone tissue engineering. Proc. Inst. Mech. Eng. H 2010, 224, 1509-1521.
19. Kapur, S.; Baylink, D.J.; Lau, K.H. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 2003, 32, 241-251.
20. Li, P.; Ma, Y.C.; Sheng, X.Y.; Dong, H.T.; Han, H.; Wang, J.; Xia, Y.Y. Cyclic fluid shear stress promotes osteoblastic cells proliferation through ERK5 signaling pathway. Mol. Cell. Biochem. 2012, 364, 321-327.
21. Kreke, M.R.; Huckle, W.R.; Goldstein, A.S. Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. Bone 2005, 36, 1047-1055.
22. Scaglione, S.; Wendt, D.; Miggino, S.; Papadimitropoulos, A.; Fato, M.; Quarto, R.; Martin, I. Effects of fluid flow and calcium phosphate coating on human bone marrow stromal cells cultured in a defined 2D model system. J. Biomed. Mater. Res. A 2008, 86, 411-419.
23. Arnsdorf, E.J.; Tummala, P.; Kwon, R.Y.; Jacobs, C.R. Mechanically induced osteogenic differentiation-the role of RhoA, ROCKII and cytoskeletal dynamics. J. Cell. Sci. 2009, 122, 546-553.
24. Yourek, G.; McCormick, S.M.; Mao, J.J.; Reilly, G.C. Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen. Med. 2010, 5, 713-724.
25. Lim, J.Y.; Loiselle, A.E.; Lee, J.S.; Zhang, Y.; Salvi, J.D.; Donahue, H.J. Optimizing the osteogenic potential of adult stem cells for skeletal regeneration. J. Orthop. Res. 2011, 29, 1627-1633.
26. Poudel, I.; Menter, D.; Lim, J.Y. Directing cell function and fate via micropatterning: Role of cell patterning size, shape, and interconnectivity. Biomed. Eng. Lett. 2012, 2, 38-45.
27. Salvi, J.D.; Lim, J.Y.; Donahue, H.J. Increased mechanosensitivity of cells cultured on nanotopographies. J. Biomech. 2010, 43, 3058-3062.
28. Takai, E.; Landesberg, R.; Katz, R.W.; Hung, C.T.; Guo, X.E. Substrate modulation of osteoblast adhesion strength, focal adhesion kinase activation, and responsiveness to mechanical stimuli. Mol. Cell. Biomech. 2006, 3, 1-12.
29. Schwartz, Z.; Denison, T.A.; Bannister, S.R.; Cochran, D.L.; Liu, Y.H.; Lohmann, C.H.; Wieland, M.; Boyan, B.D. Osteoblast response to fluid induced shear depends on substrate microarchitecture and varies with time. J. Biomed. Mater. Res. A 2007, 83, 20-32.
30. Damsky, C.H.; Ilic, D. Integrin signaling: It's where the action is. Curr. Opin. Cell. Biol. 2002, 14, 594-602.
31. Lim, J.Y.; Taylor, A.F.; Li, Z.; Vogler, E.A.; Donahue, H.J. Integrin expression and osteopontin regulation in human fetal osteoblastic cells mediated by substratum surface characteristics. Tissue Eng. 2005, 11, 19-29.
32. Lim, J.Y.; Dreiss, A.D.; Zhou, Z.; Hansen, J.C.; Siedlecki, C.A.; Hengstebeck, R.W.; Cheng, J.; Winograd, N.; Donahue, H.J. The regulation of integrin-mediated osteoblast focal adhesion and focal adhesion kinase expression by nanoscale topography. Biomaterials 2007, 28, 1787-1797.
33. Young, S.R.; Gerard-O'Riley, R.; Kim, J.B.; Pavalko, F.M. Focal adhesion kinase is important for fluid shear stress-induced mechanotransduction in osteoblasts. J. Bone Miner. Res. 2009, 24, 411-424.
34. Young, S.R.; Hum, J.M.; Rodenberg, E.; Turner, C.H.; Pavalko, F.M. Non-overlapping functions for Pyk2 and FAK in osteoblasts during fluid shear stress-induced mechanotransduction. PLoS One 2011, 6, e16026.
35. Myers, K.A.; Rattner, J.B.; Shrive, N.G.; Hart, D.A. Osteoblast-like cells and fluid flow: cytoskeleton-dependent shear sensitivity. Biochem. Biophys. Res. Commun. 2007, 364, 214-219.
36. Sterck, J.G.; Klein-Nulend, J.; Lips, P.; Burger, E.H. Response of normal and osteoporotic human bone cells to mechanical stress in vitro. Am. J. Physiol. 1998, 274, E1113-E1120.
37. Bakker, A.D.; Klein-Nulend, J.; Tanck, E.; Heyligers, I.C.; Albers, G.H.; Lips, P.; Burger, E.H. Different responsiveness to mechanical stress of bone cells from osteoporotic versus osteoarthritic donors. Osteoporos. Int. 2006, 17, 827-833.
38. Zhao, F.; Chella, R.; Ma, T. Effects of shear stress on 3-D human mesenchymal stem cell construct development in a perfusion bioreactor system: Experiments and hydrodynamic modeling. Biotechnol. Bioeng. 2007, 96, 584-595.
39. Barron, M.J.; Tsai, C.J.; Donahue, S.W. Mechanical stimulation mediates gene expression in MC3T3 osteoblastic cells differently in 2D and 3D environments. J. Biomech. Eng. 2010, 132, 041005.
40. Meinel, L.; Karageorgiou, V.; Fajardo, R.; Snyder, B.; Shinde-Patil, V.; Zichner, L.; Kaplan, D.; Langer, R.; Vunjak-Novakovic, G. Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann. Biomed. Eng. 2004, 32, 112-122.
41. Riehl, B.D.; Park, J.H.; Kwon, I.K.; Lim, J.Y. Mechanical stretching for tissue engineering: Two-dimensional and three-dimensional constructs. Tissue Eng. Part. B Rev. 2012, 18, 288-300.
42. Bjerre, L.; Bunger, C.; Baatrup, A.; Kassem, M.; Mygind, T. Flow perfusion culture of human mesenchymal stem cells on coralline hydroxyapatite scaffolds with various pore sizes. J. Biomed. Mater. Res. A 2011, 97, 251-263.
43. Sikavitsas, V.I.; Bancroft, G.N.; Holtorf, H.L.; Jansen, J.A.; Mikos, A.G. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc. Natl. Acad. Sci. USA 2003, 100, 14683-14688.
44. Kim, J.; Ma, T. Bioreactor strategy in bone tissue engineering: pre-culture and osteogenic differentiation under two flow configurations. Tissue Eng. Part. A 2012, 18, 2354-2364.
45. Liu, L.; Yu, B.; Chen, J.; Tang, Z.; Zong, C.; Shen, D.; Zheng, Q.; Tong, X.; Gao, C.; Wang, J. Different effects of intermittent and continuous fluid shear stresses on osteogenic differentiation of human mesenchymal stem cells. Biomech. Model. Mechanobiol. 2012, 11, 391-401.
46. McCoy, R.J.; Jungreuthmayer, C.; O'Brien, F.J. Influence of flow rate and scaffold pore size on cell behavior during mechanical stimulation in a flow perfusion bioreactor. Biotechnol. Bioeng. 2012, 109, 1583-1594.
47. Jungreuthmayer, C.; Donahue, S.W.; Jaasma, M.J.; Al-Munajjed, A.A.; Zanghellini, J.; Kelly, D.J.; O'Brien, F.J. A comparative study of shear stresses in collagen-glycosaminoglycan and calcium phosphate scaffolds in bone tissue-engineering bioreactors. Tissue Eng. Part. A 2009, 15, 1141-1149.
48. Fritton, S.P.; Weinbaum, S. Fluid and solute transport in bone: flow-induced mechanotransduction. Annu. Rev. Fluid Mech. 2009, 41, 347-374.
49. Price, C.; Zhou, X.; Li, W.; Wang, L. Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J. Bone Miner. Res. 2011, 26, 277-285.
50. Schmidt, S.M.; McCready, M.J.; Ostafin, A.E. Effect of oscillating fluid shear on solute transport in cortical bone. J. Biomech. 2005, 38, 2337-2343.
51. Porter, B.; Zauel, R.; Stockman, H.; Guldberg, R.; Fyhrie, D. 3-D computational modeling of media flow through scaffolds in a perfusion bioreactor. J. Biomech. 2005, 38, 543-549.
52. Kim, J.; Ma, T. Perfusion regulation of hMSC microenvironment and osteogenic differentiation in 3D scaffold. Biotechnol. Bioeng. 2012, 109, 252-261.
53. Li, D.; Tang, T.; Lu, J.; Dai, K. Effects of flow shear stress and mass transport on the construction of a large-scale tissue-engineered bone in a perfusion bioreactor. Tissue Eng. Part. A 2009, 15, 2773-2783.
54. Riddle, R.C.; Hippe, K.R.; Donahue, H.J. Chemotransport contributes to the effect of oscillatory fluid flow on human bone marrow stromal cell proliferation. J. Orthop. Res. 2008, 26, 918-924.
55. Cukierman, E.; Pankov, R.; Stevens, D.R.; Yamada, K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294, 1708-1712.
56. Stiehler, M.; Bunger, C.; Baatrup, A.; Lind, M.; Kassem, M.; Mygind, T. Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. J. Biomed. Mater. Res. A 2009, 89, 96-107.
57. Fröhlich, M.; Grayson, W.L.; Marolt, D.; Gimble, J.M.; Kregar-Velikonja, N.; Vunjak-Novakovic, G. Bone grafts engineered from human adipose-derived stem cells in perfusion bioreactor culture. Tissue Eng. Part. A 2010, 16, 179-189.
58. Grayson, W.L.; Marolt, D.; Bhumiratana, S.; Frohlich, M.; Guo, X.E.; Vunjak-Novakovic, G. Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol. Bioeng. 2011, 108, 1159-1170.
59. Janssen, F.W.; van Dijkhuizen-Radersma, R.; Van Oorschot, A.; Oostra, J.; de Bruijn, J.D.; Van Blitterswijk, C.A. Human tissue-engineered bone produced in clinically relevant amounts using a semi-automated perfusion bioreactor system: a preliminary study. J. Tissue Eng. Regen. Med. 2010, 4, 12-24.
60. Grayson, W.L.; Frohlich, M.; Yeager, K.; Bhumiratana, S.; Chan, M.E.; Cannizzaro, C.; Wan, L.Q.; Liu, X.S.; Guo, X.E.; Vunjak-Novakovic, G. Engineering anatomically shaped human bone grafts. Proc. Natl. Acad. Sci. USA 2010, 107, 3299-3304.
61. Nakamura, M.; Iwanaga, S.; Henmi, C.; Arai, K.; Nishiyama, Y. Biomatrices and biomaterials for future developments of bioprinting and biofabrication. Biofabrication. 2010, 2, 014110.
62. Liao, J.; Guo, X.; Nelson, D.; Kasper, F.K.; Mikos, A.G. Modulation of osteogenic properties of biodegradable polymer/extracellular matrix scaffolds generated with a flow perfusion bioreactor. Acta. Biomater. 2010, 6, 2386-2393.
63. Pham, Q.P.; Kasper, F.K.; Mistry, A.S.; Sharma, U.; Yasko, A.W.; Jansen, J.A.; Mikos, A.G. Analysis of the osteoinductive capacity and angiogenicity of an in vitro generated extracellular matrix. J. Biomed. Mater. Res. A 2009, 88, 295-303.
64. Wheeler, A.R.; Throndset, W.R.; Whelan, R.J.; Leach, A.M.; Zare, R.N.; Liao, Y.H.; Farrell, K.; Manger, I.D.; Daridon, A. microfluidic device for single-cell analysis. Anal. Chem. 2003, 75, 3581-3586.
65. Thomas, R.S.; Mitchell, P.D.; Oreffo, R.O.; Morgan, H. Trapping single human osteoblast-like cells from a heterogeneous population using a dielectrophoretic microfluidic device. Biomicrofluidics 2010, 4, 022806.
66. Kou, S.; Pan, L.; van Noort, D.; Meng, G.; Wu, X.; Sun, H.; Xu, J.; Lee, I. A multishear microfluidic device for quantitative analysis of calcium dynamics in osteoblasts. Biochem. Biophys. Res. Commun. 2011, 408, 350-355.
67. Leclerc, E.; David, B.; Griscom, L.; Lepioufle, B.; Fujii, T.; Layrolle, P.; Legallaisa, C. Study of osteoblastic cells in a microfluidic environment. Biomaterials 2006, 27, 586-595.
68. Jang, K.; Sato, K.; Igawa, K.; Chung, U.I.; Kitamori, T. Development of an osteoblast-based 3D continuous-perfusion microfluidic system for drug screening. Anal. Bioanal. Chem. 2008, 390, 825-832.
69. Song, S.H.; Choi, J.; Jung, H.I. A microfluidic magnetic bead impact generator for physical stimulation of osteoblast cell. Electrophoresis 2010, 31, 2762-2770.
70. Kirchhof, K.; Andar, A.; Yin, H.B.; Gadegaard, N.; Riehle, M.O.; Groth, T. Polyelectrolyte multilayers generated in a microfluidic device with pH gradients direct adhesion and movement of cells. Lab. Chip 2011, 11, 3326-3335.
71. Zhang, Y.; Gazit, Z.; Pelled, G.; Gazit, D.; Vunjak-Novakovic, G. Patterning osteogenesis by inducible gene expression in microfluidic culture systems. Integr. Biol. 2011, 3, 39-47.
72. Numthuam, S.; Ginoza, T.; Zhu, M.; Suzuki, H.; Fukuda, J. Gold-black micropillar electrodes for microfluidic ELISA of bone metabolic markers. Analyst 2011, 136, 456-458.
73. Chen, J.; Zheng, Y.; Tan, Q.; Shojaei-Baghini, E.; Zhang, Y.L.; Li, J.; Prasad, P.; You, L.; Wu, X.Y.; Sun, Y. Classification of cell types using a microfluidic device for mechanical and electrical measurement on single cells. Lab. Chip 2011, 11, 3174-3181.
74. Lee, J.H.; Gu, Y.; Wang, H.; Lee, W.Y. Microfluidic 3D bone tissue model for high-throughput evaluation of wound-healing and infection-preventing biomaterials. Biomaterials 2012, 33, 999-1006.
75. Lee, J.H.; Wang, H.; Kaplan, J.B.; Lee, W.Y. Effects of Staphylococcus epidermidis on osteoblast cell adhesion and viability on a Ti alloy surface in a microfluidic co-culture environment. Acta. Biomater. 2010, 6, 4422-4429.
76. Wei, C.W.; Cheng, J.Y.; Young, T.H. Elucidating in vitro cell-cell interaction using a microfluidic coculture system. Biomed. Microdevices. 2006, 8, 65-71.
77. Scherberich, A.; Galli, R.; Jaquiery, C.; Farhadi, J.; Martin, I. Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 2007, 25, 1823-1829.
78. Yuan, L.; Sakamoto, N.; Song, G.; Sato, M. Migration of human mesenchymal stem cells under low shear stress mediated by mitogen-activated protein kinase signaling. Stem Cells Dev. 2012, 21, 2520-2530.
79. Gurkan, U.A.; Akkus, O. The mechanical environment of bone marrow: A review. Ann. Biomed. Eng. 2008, 36, 1978-1991.
80. Kshitiz; Park, J.; Kim, P.; Helen, W.; Engler, A.J.; Levchenko, A.; Kim, D.H. Control of stem cell fate and function by engineering physical microenvironments. Integr. Biol. 2012, 4, 1008-1018.
81. Gonçalves, A.; Costa, P.; Rodrigues, M.T.; Dias, I.R.; Reis, R.L.; Gomes, M.E. Effect of flow perfusion conditions in the chondrogenic differentiation of bone marrow stromal cells cultured onto starch based biodegradable scaffolds. Acta. Biomater. 2011, 7, 1644-1652.
82. Alves da Silva, M.L.; Martins, A.; Costa-Pinto, A.R.; Correlo, V.M.; Sol, P.; Bhattacharya, M.; Faria, S.; Reis, R.L.; Neves, N.M. Chondrogenic differentiation of human bone marrow mesenchymal stem cells in chitosan-based scaffolds using a flow-perfusion bioreactor. J. Tissue Eng. Regen. Med. 2011, 5, 722-732.
83. Kinney, M.A.; Sargent, C.Y.; McDevitt, T.C. The multiparametric effects of hydrodynamic environments on stem cell culture. Tissue Eng. Part. B Rev. 2011, 17, 249-262.
84. Patwari, P.; Lee, R.T. Mechanical control of tissue morphogenesis. Circ. Res. 2008, 103, 234-243.
85. Barron, M.J.; Goldman, J.; Tsai, C.J.; Donahue, S.W. Perfusion flow enhances osteogenic gene expression and the infiltration of osteoblasts and endothelial cells into three-dimensional calcium phosphate scaffolds. Int. J. Biomater. 2012, 2012, 915620.