Fibroblast response to interstitial flow: A state-of-the-art review

Biotechnology and Bioengineering

Volumn 107, Issue 1, 2010, Pages 1-10

  Dan, Liu ^a   Chua, Chee Kai ^a   Leong, Kah Fai ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Fibroblasts; Interstitial flow; Mechanotransduction; Tissue engineering

Indexed keywords

CALCIUM SIGNALING; FIBROBLAST GROWTH; FIBROBLAST RESPONSE; FLOW PROFILE; GROWTH CONDITIONS; INFLUENCING FACTOR; INTERSTITIAL FLOW; MECHANOTRANSDUCTION; NUTRIENT SUPPLY; SCAFFOLD PROPERTIES; SIGNALING MOLECULES; STATE-OF-THE-ART REVIEWS; THREE-DIMENSIONAL ENVIRONMENT;

CALCIUM; CELL CULTURE; FIBROBLASTS; GROWTH KINETICS; SIGNALING; TISSUE ENGINEERING;

TISSUE;

AUTOCRINE EFFECT; CALCIUM SIGNALING; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; ENZYME RELEASE; FIBROBLAST; FLUID FLOW; HUMAN; INTERSTITIAL FLUID; NONHUMAN; PARACRINE SIGNALING; PROTEIN SECRETION; REVIEW; TISSUE ENGINEERING;

ANIMALS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; EXTRACELLULAR FLUID; FIBROBLASTS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICROFLUIDICS; TISSUE ENGINEERING;

EID: 77956257482     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.22826     Document Type: Review

References (84)

1. Archambault JM, Elfervig-Wall MK, Tsuzaki M, Herzog W, Banes AJ. 2002. Rabbit tendon cells produce MMP-3 in response to fluid flow without significant calcium transients. J Biomech 35(3):303-309.
2. Balcells M, Suarez MF, Vazquez M, Edelman ER. 2005. Cells in fluidic environments are sensitive to flow frequency. J Cell Physiol 204(1):329-335.
3. Bartolo P, Chua CK, Almeida HA, Chou SM, Lim ASC. 2009. Biomanufacturing for tissue engineering: Present and future trends. Virtual Phys Prototyping 4(4):203-216.
4. Berridge MJ, Lipp P, Bootman MD. 2000. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11-21.
5. Bilgen B, Uygun K, Bueno EM, Sucosky P, Barabino GA. 2009. Tissue growth modeling in a wavy-walled bioreactor. Tissue Eng 15(4):761-771.
6. Butler PJ, Norwich G, Weinbaum S, Chien S. 2001. Shear stress induces a time- and position-dependent increase in endothelial cell membrane fluidity. Am J Physiol 280(4):C962-C969.
7. Chachisvilis M, Zhang YL, Frangos JA. 2006. G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci USA 103(42):15463-15468.
8. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, Brown PO. 2002. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 99(20):12877-12882.
9. Chiquet M, Gelman L, Lutz R, Maier S. 2009. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim Biophys Acta 1793(5):911-920.
10. Chotard-Ghodsnia R, Drochon A, Faucheux N, Nagel MD, Grebe R. 2002. Effect of shear stress and of transmural pressure on cAMP-dependent responses of cells adhering to a biomaterial. Eur Phys J 17(2):155-162. (Pubitemid 34156391)
11. Chung CA, Chen CP, Lin TH, Tseng CS. 2008. A compact computational model for cell construct development in perfusion culture. Biotechnol Bioeng 99(6):1535-1541.
12. Cioffi M, Boschetti F, Raimondi MT, Dubini G. 2006. Modeling evaluation of the fluid-dynamic microenvironment in tissue-engineered constructs: A micro-CT based model. Biotechnol Bioeng 93(3):500-510.
13. Curran SJ, Black RA. 2005. Oxygen transport and cell viability in an annular flow bioreactor: Comparison of laminar couette and Taylor-vortex flow regimes. Biotechnol Bioeng 89(7):766-774.
14. Das T, Maiti TK, Chakraborty S. 2008. Traction force microscopy on-chip: Shear deformation of fibroblast cells. Lab Chip 8(8):1308-1318.
15. del Rio A, Perez-Jimenez R, Liu RC, Roca-Cusachs P, Fernandez JM, Sheetz MP. 2009. Stretching single talin rod molecules activates vinculin binding. Science 323(5914):638-641.
16. Desrosiers EA, Methot S, Yahia LH, Rivard CH. 1995. Response of ligamentous fibroblasts to mechanical stimulation. Ann Chir 49(8):768-774.
17. Domeij H, Modeer T, Yucel-Lindberg T. 2004. Matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 production in human gingival fibroblasts: The role of protein kinase C. J Periodontal Res 39(5):308-314.
18. Friedl P, Brocker EB. 2000. The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol Life Sci 57(1):41-64.
19. Friedrichs J, Taubenberger A, Franz CM, Muller DJ. 2007. Cellular remodelling of individual collagen fibrils visualized by time-lapse AFM. J Mol Biol 372(3):594-607.
20. Garanich JS, Mathura RA, Shi ZD, Tarbell JM. 2007. Effects of fluid shear stress on adventitial fibroblast migration: Implications for flow-mediated mechanisms of arterialization and intimal hyperplasia. Am J Physiol 292(6):H3128-H3135.
21. Garcia AJ, Ducheyne P, Boettiger D. 1997. Cell adhesion strength increases linearly with adsorbed fibronectin surface density. Tissue Eng 3(2):197-206.
22. Goldstein AS, DiMilla PA. 1997. Application of fluid mechanic and kinetic models to characterize mammalian cell detachment in a radial-flow chamber. Biotechnol Bioeng 55(4):616-629.
23. Goldstein AS, DiMilla PA. 2002. Effect of adsorbed fibronectin concentration on cell adhesion and deformation under shear on hydrophobic surfaces. J Biomed Mater Res 59(4):665-675.
24. Grierson JP, Meldolesi J. 1995. Shear stress-induced [Ca2+]i transients and oscillations in mouse fibroblasts are mediated by endogenously released ATP. J Biol Chem 270(9):4451-4456.
25. Gudi S, Nolan JP, Frangos JA. 1998. Modulation of GTPase activity of G proteins by fluid shear stress and phospholipid composition. Proc Natl Acad Sci USA 95(5):2515-2519.
26. Gumbiner BM. 1996. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84(3):345-357.
27. Haidekker MA, L'Heureux N, Frangos JA. 2000. Fluid shear stress increases membrane fluidity in endothelial cells: A study with DCVJ fluorescence. Am J Physiol 278(4):H1401-H1406.
28. Hung CT, Allen FD, Pollack SR, Attia ET, Hannafin JA, Torzilli PA. 1997. Intracellular calcium response of ACL and MCL ligament fibroblasts to fluid-induced shear stress. San Francisco, CA. Elsevier Science Inc. p 587-594.
29. Ingber DE, Jamieson JD. 1985. Cells as tensegrity structures- architectural regulation of histodifferentiation by physical forces transduced over basement membrane. In: Andersson Leif C, Gahmberg CG, Ekblom P, editors. Gene expression during normal and malignant differentiation. 1st edition. New York: Academic Press. p 13-32.
30. Janmey PA, McCulloch CA. 2007. Cell mechanics: Integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng 9:1-34.
31. Jarman-Smith M, Bodamyali T, Stevens C, Howell JA, Horrocks M, Chaudhuri JB. 2004. Human fibroblast culture on a crosslinked dermal porcine collagen matrix. Biochem Eng J 20(2-3):217-222.
32. Kalyanaraman B, Supp DM, Boyce ST. 2008. Medium flow rate regulates viability and barrier function of engineered skin substitutes in perfusion culture. Tissue Eng Part A 14(5):583-593.
33. Karamichos D, Lakshman N, Petroll WM. 2009. An experimental model for assessing fibroblast migration in 3-D collagen matrices. Cell Motil Cytoskeleton 66(1):1-9.
34. Katsumi A, Naoe T, Matsushita T, Kaibuchi K, Schwartz MA. 2005. Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J Biol Chem 280(17):16546-16549.
35. Kilarski WW, Samolov B, Petersson L, Kvanta A, Gerwins P. 2009. Biomechanical regulation of blood vessel growth during tissue vascularization. Nat Med 15(6):657-664.
36. Ko KS, Arora PD, McCulloch CAG. 2001. Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium-permeable channels. J Biol Chem 276(38):35967-35977.
37. Kohyama T, Yamauchi Y, Takizawa H, Itakura S, Kamitani S, Desaki M, Kawasaki S, Nagase T. 2009. Procaterol inhibits lung fibroblast migration. Inflammation 32(6):387-392.
38. Kong QJ, Vazquez M. 2006. Internal fluid flow increases cellular interconnects between medial collateral ligament fibroblasts and cellular extensions within three-dimensional collagen matrixes. Cell Commun Adhes 13(3):139-149.
39. Korin N, Bransky A, Dinnar U, Levenberg S. 2007. A parametric study of human fibroblasts culture in a microchannel bioreactor. Lab Chip 7(5):611-617.
40. Kulangara K, Leong KW. 2009. Substrate topography shapes cell function. Soft Matter 5(21):4072-4076.
41. Leong KF, Cheah CM, Chua CK. 2003. Solid freeform fabrication of three-dimensional scaffolds for engineering replacement tissues and organs. Biomaterials 24(13):2363-2378.
42. Levick J. 2000. Circulation of fluid between plasma, interstitium and lymph. An introduction to cardiovascular physiology. 3rd edition. London: Hodder Arnold.
43. Li S, Guan JL, Chien S. 2005. Biochemistry and biomechanics of cell motility. Annu Rev Biomed Eng 7:105-150.
44. Martines E, McGhee K, Wilkinson C, Curtis A. 2004. A parallel-plate flow chamber to study initial cell adhesion on a nanofeatured surface. IEEE Trans Nanobiosci 3(2):90-95.
45. McAnulty RJ. 2007. Fibroblasts and myofibroblasts: Their source, function and role in disease. Int J Biochem Cell Biol 39(4):666-671.
46. McFetridge PS, Abe K, Horrocks M, Chaudhuri JB. 2007. Vascular tissue engineering: Bioreactor design considerations for extended culture of primary human vascular smooth muscle cells. ASAIO J 53:623-630.
47. Millar NL, Wei AQ, Molloy TJ, Bonar F, Murrell GAC. 2009. Cytokines and apoptosis in supraspinatus tendinopathy. J Bone Joint Surg (Br) 91(3):417-424.
48. Mizuno S, Watanabe S, Takagi T. 2004. Hydrostatic fluid pressure promotes cellularity and proliferation of human dermal fibroblasts in a three-dimensional collagen gel/sponge. Biochem Eng J 20(2-3):203-208.
49. Mol A, Driessen NJB, Rutten MCM, Hoerstrup SP, Bouten CVC, Baaijens FPT. 2005. Tissue engineering of human heart valve leaflets: A novel bioreactor for a strain-based conditioning approach. Ann Biomed Eng 33(12):1778-1788.
50. Ng CP, Swartz MA. 2003. Fibroblast alignment under interstitial fluid flow using a novel 3D tissue culture model. Am J Physiol 284:H1771-H1777.
51. Ng CP, Swartz MA. 2006. Mechanisms of interstitial flow-induced remodeling of fibroblast-collagen cultures. Ann Biomed Eng 34(3):446-454.
52. Ng CP, Hinz B, Swartz MA. 2005. Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118(20):4731-4739.
53. Nolte SV, Xu W, Rennekampff HO, Rodemann HP. 2008. Diversity of fibroblasts - A review on implications for skin tissue engineering. Cells Tissues Organs 187(3):165-176.
54. Park JY, Yoo SJ, Hwang CM, Lee SH. 2009. Simultaneous generation of chemical concentration and mechanical shear stress gradients using microfluidic osmotic flow comparable to interstitial flow. Lab Chip 9(15):2194-2202.
55. Pedersen JA, Boschetti F, Swartz MA. 2007. Effects of extracellular fiber architecture on cell membrane shear stress in a 3D fibrous matrix. J Biomech 40(7):1484-1492.
56. Reyes CD, Petrie TA, Garcia AJ. 2008. Mixed extracellular matrix ligands synergistically modulate integrin adhesion and signaling. J Cell Physiol 217(2):450-458.
57. Rose, F, Grimminger, F, Appel, J, Heller, M, Pies, V, Weissmann, N, Fink, L, Schmidt, S, Krick, S, Camenisch, G, Gassmann, M, Seeger, W, Hanze, J, 2002. Hypoxic pulmonary artery fibroblasts trigger proliferation of vascular smooth muscle cells: Role of hypoxia-inducible transcription factors. FASEB J 16(12):1660-1661.
58. Rutkowski JM, Swartz MA. 2007. A driving force for change: Interstitial flow as a morphoregulator. Trends Cell Biol 17(1):44-50.
59. Scallan J, Huxley VH, Korthuis RJ. 2010. Capillary fluid exchange: Regulation, functions, and pathology. Colloquium Series on Integrated Systems Physiology: From Molecule to Function, In: Neil Granger, Granger J, editors. San Rafael Morgan & Claypool Publishers. p 1-94.
60. Shi ZD, Mathura RA, Garanich JS, Abraham G, Tarbell JM. 2007. Shear stress plays a role in differentiation and migration of adventitial fibroblasts. Annual IEEE Northeast Bioengineering Conference New York: IEEE. p 205-206.
61. Shi ZD, Ji XY, Qazi H, Tarbell JM. 2009. Interstitial flow promotes vascular fibroblast, myofibroblast, and smooth muscle cell motility in 3-D collagen I via upregulation of MMP-1. Am J Physiol 297(4):H1225-H1234.
62. Shi ZD, Ji XY, Berardi DE, Qazi H, Tarbell JM. 2010. Interstitial flow induces MMP-1 expression and vascular SMC migration in collagen I gels via an ERK1/2-dependent and c-Jun-mediated mechanism. Am J Physiol 298(1):H127-H135.
63. Shimizu M, Takakuwa Y, Nitta S. 1995. Study of stimulation-secretion coupling in a flow culture system: Periodic secretion of hepatocyte growth factor by interleukin-1 alpha-stimulated human embryonic lung fibroblasts. Biochim Biophys Acta 1244(2-3):357-362.
64. Sodian R, Lueders C, Kraemer L, Kuebler W, Shakibaei M, Reichart B, Daebritz S, Hetzer R. 2006. Tissue engineering of autologous human heart valves using cryopreserved vascular umbilical cord cells. Ann Thoracic Surg 81(6):2207-2216.
65. Starly B, Choubey A. 2008. Enabling sensor technologies for the quantitative evaluation of engineered tissue. Ann Biomed Eng 36(1):30-40.
66. Stolberg S, McCloskey KE. 2009. Can shear stress direct stem cell fate? Biotechnol Prog 25(1):10-19.
67. Sun T, Jackson S, Haycock JW, MacNeil S. 2006. Culture of skin cells in 3D rather than 2D improves their ability to survive exposure to cytotoxic agents. J Biotechnol 122(3):372-381.
68. Swartz MA, Fleury ME. 2007. Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng 9:229-256.
69. Tiede S, Ernst N, Bayat A, Paus R, Tronnier V, Zechel C. 2009. Basic fibroblast growth factor: A potential new therapeutic tool for the treatment of hypertrophic and keloid scars. Ann Anat 191(1):33-44.
70. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. 2002. Myofi- broblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5):349-363.
71. Tranquillo RT, Durrani MA, Moon AG. 1992. Tissue engineering science: Consequences of cell traction force. Cytotechnology 10(3):225-250.
72. van der Pauw MTM, Klein-Nulend J, van den Bos T, Burger EH, Everts V, Beertsen W. 2000. Response of periodontal ligament fibroblasts and gingival fibroblasts to pulsating fluid flow: Nitric oxide and prostaglandin E-2 release and expression of tissue non-specific alkaline phosphatase activity. J Periodontal Res 35(6):335-343.
73. Vankooten TG, Schakenraad JM, Vandermei HC, Busscher HJ. 1992. Development and use of a parallel-plate flow chamber for studying cellular adhesion to solid surfaces. J Biomed Mater Res 26(6):725-738.
74. Vankooten TG, Schakenraad JM, Vandermei HC, Busscher HJ. 1993. Influence of pulsatile flow on the behaviour of human fibroblasts adhered to glass. J Biomater Sci (Polymer Ed) 4(6):601-614.
75. Hutmacher DW, Singh H. 2008. Computational fluid dynamics for improved bioreactor design and 3D culture. Trends Biotechnol 26(4):166-172.
76. Wang N, Butler JP, Ingber DE. 1993. Mechanotransduction across the cell surface and through the cytoskeleton Science. 260(5111):1124-1127.
77. Wang HJ, Bertrand-De Haas M, Riesle J, Lamme E, Van Blitterswijk CA. 2003. Tissue engineering of dermal substitutes based on porous PEGT/PBT copolymer scaffolds: Comparison of culture conditions. J Mater Sci 14(3):235-240.
78. Weston MW, Yoganathan AP. 2001. Biosynthetic activity in heart valve leaflets in response to in vitro flow environments. Ann Biomed Eng 29(9):752-763.
79. White CR, Frangos JA. 2007. The shear stress of it all: The cell membrane and mechanochemical transduction. Philos Trans R Soc Lond B Biol Sci 362(1484):1459-1467.
80. Wiria FE, Chua CK, Leong KF, Quah ZY, Chandrasekaran M, Lee MW. 2008. Improved biocomposite development of poly(vinyl alcohol) and hydroxyapatite for tissue engineering scaffold fabrication using selective laser sintering. J Mater Sci Mater Med 19(3):989-996.
81. Xu ZC, Zhang WJ, Li H, Cui L, Cen L, Zhou GD, Liu W, Cao YL. 2008. Engineering of an elastic large muscular vessel wall with pulsatile stimulation in bioreactor. Biomaterials 29(10):1464-1472.
82. Yang SF, Leong KF, Du ZH, Chua CK. 2002. The design of scaffolds for use in tissue engineering. Part II. Rapid prototyping techniques. Tissue Eng 8(1):1-11.
83. Yeong WY, Chua CK, Leong KF, Chandrasekaran M. 2004. Rapid prototyping in tissue engineering: Challenges and potential. Trends Biotechnol 22(12):643-652.
84. Zhang J, Yang L, Tang ZY, Xue RY, Wang YQ, Luo ZW, Huang W, Sung KLP. 2009. Expression of MMPs and TIMPs family in human ACL and MCL fibroblasts. Connect Tissue Res 50(1):7-13.