Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation

Akimoto S, Mitsumata M, Sasaguri T, Yoshida Y (2000) Laminar shear stress inhibits vascular endothelial cell proliferation by inducing cyclin-dependent kinase inhibitor p21(sdi1/cip1/waf1). Circ Res 86(2): 185–190

Angele P, Yoo JU, Smith C, Mansour J, Jepsen KJ, Nerlich M, Johnstone B (2003) Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res 21(3): 451–457

Butler WT (1989) The nature and significance of osteopontin. Connect Tissue Res 23(2–3): 123–136

Cappadona C, Redmond EM, Theodorakis NG, McKillop IH, Hendrickson R, Chhabra A, Sitzmann JV, Cahill PA (1999) Phenotype dictates the growth response of vascular smooth muscle cells to pulse pressure in vitro. Exp Cell Res 250(1): 174–186

Chen J, Kitchen CM, Streb JW, Miano JM (2002) Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol 34(10): 1345–1356

Chien S (2006) Molecular basis of rheological modulation of endothelial functions: Importance of stress direction. Biorheology 43(2): 95–116

Chomczynski P, Sacchi N (1987) Single-step method of rna isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162(1): 156–159

Conklin BS, Zhong DS, Zhao W, Lin PH, Chen C (2002) Shear stress regulates occludin and vegf expression in porcine arterial endothelial cells. J Surg Res 102(1): 13–21

Conley BA, Smith JD, Guerrero-Esteo M, Bernabeu C, Vary CP (2000) Endoglin, a tgf-beta receptor-associated protein, is expressed by smooth muscle cells in human atherosclerotic plaques. Atherosclerosis 153(2): 323–335

De R, Zemel A, Safran SA (2007) Dynamics of cell orientation. Nat Phys 3(9): 655–659

Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751): 1139–1143

Du KL, Ip HS, Li J, Chen M, Dandre F, Yu W, Lu MM, Owens GK, Parmacek MS (2003) Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol Cell Biol 23(7): 2425–2437

Elder SH, Fulzele KS, McCulley WR (2005) Cyclic hydrostatic compression stimulates chondroinduction of c3h/10t1/2 cells. Biomech Model Mechanobiol 3(3): 141–146

Elder SH, Goldstein SA, Kimura JH, Soslowsky LJ, Spengler DM (2001) Chondrocyte differentiation is modulated by frequency and duration of cyclic compressive loading. Ann Biomed Eng 29(6): 476–482

Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D (2004) Substrate compliance versus ligand density in cell on gel responses. Biophys J 86(1): 617–628

Fernandes JMO, Mommens M, Hagen O, Babiak I, Solberg C (2008) Selection of suitable reference genes for real-time pcr studies of atlantic halibut development. Comp Biochem Physiol Part B: Biochem Mol Biol 150(1): 23–32

Fisher NI (1993) Statistical analysis of circular data. Cambridge, Melbourne

Fu J, Wang YK, Yang MT, Desai RA, Yu X, Liu Z, Chen CS (2010) Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 7(9): 733–736

Galmiche MC, Koteliansky VE, Briere J, Herve P, Charbord P (1993) Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 82(1): 66–76

Garcia-Cardena G, Comander J, Anderson KR, Blackman BR, Gimbrone MA (2001) Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci USA 98(8): 4478–4485

Hamilton DW, Maul TM, Vorp DA (2004) Characterization of the response of bone marrow derived progenitor cells to cyclic strain: Implications for vascular tissue engineering applications. Tissue Eng 10(3/4): 361–370

Hammond JP, Broadley MR, Craigon DJ, Higgins J, Emmerson ZF, Townsend HJ, White PJ, May ST (2005) Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. Plant Methods 1(1): 10

Hirschi KK, Majesky MW (2004) Smooth muscle stem cells. Anat Rec A Discov Mol Cell Evol Biol 276(1): 22–33

Intengan HD, Schiffrin EL (2001) Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension 38(3 Pt 2): 581–587

Isoda K, Nishikawa K, Kamezawa Y, Yoshida M, Kusuhara M, Moroi M, Tada N, Ohsuzu F (2002) Osteopontin plays an important role in the development of medial thickening and neointimal formation. Circ Res 91(1): 77–82

Ito M (2000) Factors controlling cyclin b expression. Plant Mol Biol 43(5–6): 677–690

Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP (1997) Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64(2): 295–312

Janes KA, Reinhardt HC, Yaffe MB (2008) Cytokine-induced signaling networks prioritize dynamic range over signal strength. Cell 135(2): 343–354

Javazon EH, Colter DC, Schwarz EJ, Prockop DJ (2001) Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 19(3): 219–225

Johnson EC, Jia L, Cepurna WO, Doser TA, Morrison JC (2007) Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Invest Ophthalmol Vis Sci 48(7): 3161–3177

Kataoka N, Ujita S, Sato M (1998) Effect of flow direction on the morphological responses of cultured bovine aortic endothelial cells. Med Biol Eng Comput 36(1): 122–128

Keppel G, Wickens TD (2004) Design and analysis: a researchers handbook, 4th edn. Pearson, Upper Saddle River

Kim DH, Yoo KH, Choi KS, Choi J, Choi SY, Yang SE, Yang YS, Im HJ, Kim KH, Jung HL, Sung KW, Koo HH (2005) Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 31(2): 119–126

Kobayashi N, Yasu T, Ueba H, Sata M, Hashimoto S, Kuroki M, Saito M, Kawakami M (2004) Mechanical stress promotes the expression of smooth muscle-like properties in marrow stromal cells. Exp Hematol 32(12): 1238–1245

Kreke MR, Huckle WR, Goldstein AS (2005) Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. Bone 36(6): 1047–1055

Kuhn NZ, Tuan RS (2010) Regulation of stemness and stem cell niche of mesenchymal stem cells: Implications in tumorigenesis and metastasis. J Cell Physiol 222(2): 268–277

Kurpinski K, Chu J, Hashi C, Li S (2006) Anisotropic mechanosensing by mesenchymal stem cells. Proc Natl Acad Sci USA 103(44): 16095–16100

Kurpinski K, Park J, Thakar RG, Li S (2006) Regulation of vascular smooth muscle cells and mesenchymal stem cells by mechanical strain. Mol Cell Biomech 3(1): 21–34

Lee WC, Rubin JP, Marra KG (2006) Regulation of alpha-smooth muscle actin protein expression in adipose-derived stem cells. Cells Tissues Organs 183(2): 80–86

Li YJ, Batra NN, You L, Meier SC, Coe IA, Yellowley CE, Jacobs CR (2004) Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation. J Orthop Res 22(6): 1283–1289

Liao XD, Wang XH, Jin HJ, Chen LY, Chen Q (2004) Mechanical stretch induces mitochondria-dependent apoptosis in neonatal rat cardiomyocytes and g2/m accumulation in cardiac fibroblasts. Cell Res 14(1): 16–26

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2-[delta][delta]ct method. Methods 25(4): 402–408

Lu J, Landerholm TE, Wei JS, Dong X-R, Wu S-P, Liu X, Nagata K-i, Inagaki M, Majesky MW (2001) Coronary smooth muscle differentiation from proepicardial cells requires rhoa-mediated actin reorganization and p160 rho-kinase activity. Dev Biol 240(2): 404–418

Maul TM, Hamilton DW, Nieponice A, Soletti L, Vorp DA (2007) A new experimental system for the extended application of cyclic hydrostatic pressure to cell culture. J Biomech Eng 129(1): 110–116

McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and rhoa regulate stem cell lineage commitment. Dev Cell 6(4): 483–495

Millgard J, Lind L (1998) Acute hypertension impairs endothelium-dependent vasodilation. Clin Sci (Colch) 94(6): 601–607

Mills I, Cohen CR, Kamal K, Li G, Shin T, Du W, Sumpio BE (1997) Strain activation of bovine aortic smooth muscle cell proliferation and alignment: Study of strain dependency and the role of protein kinase a and c signaling pathways. J Cell Physiol 170(3): 228–234

Moore BR (1980) A modification of the rayleigh test for vector data. Biometrika 67(1): 175–180

Nagatomi J, Arulanandam BP, Metzger DW, Meunier A, Bizios R (2001) Frequency- and duration-dependent effects of cyclic pressure on select bone cell functions. Tissue Eng 7(6): 717–728

Nerem RM, Levesque MJ, Cornhill JF (1981) Vascular endothelial morphology as an indicator of the pattern of blood flow. J Biomech Eng 103(3): 172–176

Nieponice A, Maul TM, Cumer JM, Soletti L, Vorp DA (2006) Mechanical stimulation induces morphological and phenotypic changes in bone marrow-derived progenitor cells within a three-dimensional fibrin matrix. J Biomed Mater Res A 81A(3): 523–530

O’Cearbhaill ED, Punchard MA, Murphy M, Barry FP, McHugh PE, Barron V (2008) Response of mesenchymal stem cells to the biomechanical environment of the endothelium on a flexible tubular silicone substrate. Biomaterials 29(11): 1610–1619

Ohashi T, Sugaya Y, Sakamoto N, Sato M (2007) Hydrostatic pressure influences morphology and expression of ve-cadherin of vascular endothelial cells. J Biomech 40(11): 2399–2405

Oluwole BO, Du W, Mills I, Sumpio BE (1997) Gene regulation by mechanical forces. Endothel: J Endothel Cell Res 5(2): 85–93

Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84(3): 767–801

Park JS, Chu JS, Cheng C, Chen F, Chen D, Li S (2004) Differential effects of equiaxial and uniaxial strain on mesenchymal stem cells. Biotechnol Bioeng 88(3): 359–368

Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411): 143–147

Quesenberry PJ, Aliotta JM (2008) The paradoxical dynamism of marrow stem cells: Considerations of stem cells, niches, and microvesicles. Stem Cell Rev 4(3): 137–147

Resnick N, Gimbrone MA (1995) Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J 9(10): 874–882

Riha GM, Lin PH, Lumsden AB, Yao Q, Chen C (2005) Roles of hemodynamic forces in vascular cell differentiation. Ann Biomed Eng 33(6): 772–779

Riha GM, Wang X, Wang H, Chai H, Mu H, Lin PH, Lumsden AB, Yao Q, Chen C (2007) Cyclic strain induces vascular smooth muscle cell differentiation from murine embryonic mesenchymal progenitor cells. Surgery 141(3): 394–402

Rodriguez-Barbero A, Obreo J, Eleno N, Rodriguez-Pena A, Duwel A, Jerkic M, Sanchez-Rodriguez A, Bernabeu C, Lopez-Novoa JM (2001) Endoglin expression in human and rat mesangial cells and its upregulation by tgf-beta1. Biochem Biophys Res Commun 282(1): 142–147

Ruoslahti E (1988) Fibronectin and its receptors. Annu Rev Biochem 57: 375–413

Sato M, Ohashi T (2005) Biorheological views of endothelial cell responses to mechanical stimuli. Biorheology 42(6): 421–441

Scaglione S, Wendt D, Miggino S, Papadimitropoulos A, Fato M, Quarto R, Martin I (2007) 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 86(2): 411–419

Schwartz EA, Bizios R, Medow MS, Gerritsen ME (1999) Exposure of human vascular endothelial cells to sustained hydrostatic pressure stimulates proliferation. Involvement of the alphaV integrins. Circ Res 84(3): 315–322

Seliktar D, Black RA, Vito RP, Nerem RM (2000) Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann Biomed Eng 28(4): 351–362

Shin HY, Smith ML, Toy KJ, Williams PM, Bizios R, Gerritsen ME (2002) Vegf-c mediates cyclic pressure-induced endothelial cell proliferation. Physiol Genomics 11(3): 245–251

Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM (2002) Smooth muscle progenitor cells in human blood. Circulation 106(10): 1199–1204

Skalak TC, Price RJ, Zeller PJ (1998) Where do new arterioles come from? Mechanical forces and microvessel adaptation. Microcirculation 5(2–3): 91–94

Stegemann JP, Nerem RM (2003) Phenotype modulation in vascular tissue engineering using biochemical and mechanical stimulation. Ann Biomed Eng 31(4): 391–402

Stover J, Nagatomi J (2007) Cyclic pressure stimulates DNA synthesis through the pi3k/akt signaling pathway in rat bladder smooth muscle cells. Ann Biomed Eng 35(9): 1585–1594

Sumpio BE, Widmann MD, Ricotta J, Awolesi MA, Watase M (1994) Increased ambient pressure stimulates proliferation and morphologic changes in cultured endothelial cells. J Cell Physiol 158(1): 133–139

Vande Geest JP, Di Martino ES, Vorp DA (2004) An analysis of the complete strain field within flexercell membranes. J Biomech 37(12): 1923–1928

Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C (2005) Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25(9): 1817–1823

Wasserman SM, Mehraban F, Komuves LG, Yang RB, Tomlinson JE, Zhang Y, Spriggs F, Topper JN (2002) Gene expression profile of human endothelial cells exposed to sustained fluid shear stress. Physiol Genomics 12(1): 13–23

Wasserman SM, Topper JN (2004) Adaptation of the endothelium to fluid flow: in vitro analyses of gene expression and in vivo implications. Vasc Med 9(1): 35–45

Watase M, Awolesi MA, Ricotta J, Sumpio BE (1997) Effect of pressure on cultured smooth muscle cells. Life Sci 61(10): 987–996

Whaley L, Wong D (1999) Nursing care of infants and children, 5th edn. Mosby, St. Louis

Wolinsky H (1970) Response of the rat aortic media to hypertension. Morphological and chemical studies. Circ Res 26(4): 507–522

Xie Z, Pimental DR, Lohan S, Vasertriger A, Pligavko C, Colucci WS, Singh K (2001) Regulation of angiotensin ii-stimulated osteopontin expression in cardiac microvascular endothelial cells: role of p42/44 mitogen-activated protein kinase and reactive oxygen species. J Cell Physiol 188(1): 132–138

Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J (2005) Fluid shear stress induces differentiation of flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol 288(4): H1915–1924

Yamashita JK (2004) Differentiation and diversification of vascular cells from embryonic stem cells. Int J Hematol 80(1): 1–6

Yoshida T, Kawai-Kowase K, Owens GK (2004) Forced expression of myocardin is not sufficient for induction of smooth muscle differentiation in multipotential embryonic cells. Arterioscler Thromb Vasc Biol 24(9): 1596–1601