Stress phase angle regulates differentiation of human adipose-derived stem cells toward endothelial phenotype
Tóm tắt
Endothelial cells are subjected to cyclic shear by pulsatile blood flow and pressures due to circumferential stresses. Although most of the researches on this topic have considered the effects of these two biomechanical forces separately or concurrently, few studies have noticed the interaction of these cyclic loadings on endothelial behavior. Negative temporal stress phase angle, defined by the phase lag between cyclic shear and tensile stresses, is an established parameter which is known to have substantial effects on blood vessel remodeling and progression of some serious cardiovascular diseases. In this research, intermittent shear and tensile stresses with different stress phase angle values were applied on human adipose stem cells (ASC). The expression level of three major endothelial-specific genes, elastic modulus of cells and cytoskeleton actin structure of cells were studied and compared among control and three test groups subjected to stress phase angle values at 0°, − 45°, and − 90°. Mechanical properties of ASCs were determined by atomic force microscopy and actin fiber structure was visualized by confocal imaging through Phalloidin staining. Results described a decrease in expression of FLK-1 and VE-cadherin and rise of vWF marker expression in case of higher negative stress phase angles. The Young’s moduli of cells were significantly higher and cytoskeletal actin structure was more organized with higher thickness for all test samples subjected to combined stresses; however, these features were less magnificent for applied stress phase angles with higher negative values. The results confirmed significant effects of SPA on endothelial differentiation of mesenchymal stem cells.
Tài liệu tham khảo
Alves da Silva ML, Martins A, Costa-Pinto A, Correlo V, Sol P, Bhattacharya M, Neves N (2011) Chondrogenic differentiation of human bone marrow mesenchymal stem cells in chitosan-based scaffolds using a flow-perfusion bioreactor. J Tissue Eng Regen Med 5(9):722–732
Barron V, Brougham C, Coghlan K, McLucas E, O’Mahoney D, Stenson-Cox C, McHugh PE (2007) The effect of physiological cyclic stretch on the cell morphology, cell orientation and protein expression of endothelial cells. J Mater Sci Mater Med 18(10):1973–1981
Bassiouny HS, White S, Glagov S, Choi E, Giddens DP, Zarins CK (1992) Anastomotic intimal hyperplasia: mechanical injury or flow induced. J Vasc Surg 15(4):708–717
Byfield FJ, Reen RK, Shentu T-P, Levitan I, Gooch KJ (2009) Endothelial actin and cell stiffness is modulated by substrate stiffness in 2D and 3D. J Biomech 42(8):1114–1119
Cevallos M, Riha GM, Wang X, Yang H, Yan S, Li M, Chen C (2006) Cyclic strain induces expression of specific smooth muscle cell markers in human endothelial cells. Differentiation 74(9):552–561
Charoenpanich A, Wall ME, Tucker CJ, Andrews DM, Lalush DS, Dirschl DR, Loboa EG (2014) Cyclic tensile strain enhances osteogenesis and angiogenesis in mesenchymal stem cells from osteoporotic donors. Tissue Eng Part A. 20(1–2):67–78. https://doi.org/10.1089/ten.TEA.2013.0006
Charrier EE, Pogoda K, Wells RG, Janmey PA (2018) Control of cell morphology and differentiation by substrates with independently tunable elasticity and viscous dissipation. Nat Commun 9(1):449
Dancu MB, Tarbell JM (2006) Large negative stress phase angle (SPA) attenuates nitric oxide production in bovine aortic endothelial cells. J Biomech Eng 128(3):329
Doggett TA, Girdhar G, Lawshé A, Schmidtke DW, Laurenzi IJ, Diamond SL, Diacovo TG (2002) Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIbα-vWF Tether bond. Biophys J 83(1):194–205
Dolan JM, Meng H, Singh S, Paluch R, Kolega J (2011) High fluid shear stress and spatial shear stress gradients affect endothelial proliferation, survival, and alignment. Ann Biomed Eng 39(6):1620–1631
Elhadj S, Akers RM, Forsten-Williams K (2003) Chronic pulsatile shear stress alters insulin-like growth factor-I (IGF-I) binding protein release in vitro. Ann Biomed Eng 31(2):163–170
Estes BT, Diekman BO, Gimble JM, Guilak F (2010) Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 5(7):1294–1311
Gavard J (2009) Breaking the VE-cadherin bonds. FEBS Lett 583(1):1–6
Guo W, Hamilton JA (1996) 13C MAS NMR studies of crystalline cholesterol and lipid mixtures modeling atherosclerotic plaques. Biophys J 71(5):2857–2868
Haga JH, Li Y-SJ, Chien S (2007) Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells. J Biomech 40(5):947–960
Haghighipour N, Tafazzoli-Shadpour M, Shokrgozar MA, Amini S (2010) Effects of cyclic stretch waveform on endothelial cell morphology using fractal analysis. Artif Org 34(6):481–490
Holmes K, Roberts OL, Thomas AM, Cross MJ (2007) Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell Signal 19(10):2003–2012
Huang Y, Jia X, Bai K, Gong X, Fan Y (2010) Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells. Arch Med Res 41(7):497–505
Huang Y, Zheng L, Gong X, Jia X, Song W, Liu M, Fan Y (2012) Effect of cyclic strain on cardiomyogenic differentiation of rat bone marrow derived mesenchymal stem cells. PLoS One 7(4):e34960
Hutter JL, Bechhoefer J (1993) Calibration of atomic-force microscope tips. Rev Sci Instrum 64(7):1868–1873
James N, Harrison D, Nerem R (1995) Effects of shear on endothelial cell calcium in the presence and absence of ATP. FASEB J 9(10):968–973
Jeon H, Simon CG, Kim G (2014) A mini-review: cell response to microscale, nanoscale, and hierarchical patterning of surface structure. J Biomed Mater Res B Appl Biomater 102(7):1580–1594
Joshi AK, Leask RL, Myers JG, Ojha M, Butany J, Ethier CR (2004) Intimal thickness is not associated with wall shear stress patterns in the human right coronary artery. Arterioscler Thromb Vasc Biol 24(12):2408–2413
Kang H, Cancel LM, Tarbell JM (2014) Effect of shear stress on water and LDL transport through cultured endothelial cell monolayers. Atherosclerosis 233(2):682–690
Ku DN, Giddens DP, Zarins CK, Glagov S (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arterioscler Thromb Vasc Biol 5(3):293–302
La A, Tranquillo RT (2018) Shear conditioning of adipose stem cells for reduced platelet binding to engineered vascular grafts. Tissue Eng Part A. https://doi.org/10.1089/ten.tea.2017.0475
Lekka M, Gil D, Pogoda K, Dulińska-Litewka J, Jach R, Gostek J, Klymenko O, Prauzner-Bechcicki S, Stachura Z, Wiltowska-Zuber J, Okoń K, Laidler P (2012) Cancer cell detection in tissue sections using AFM. Arch Biochem Biophys. 518(2):151–156. https://doi.org/10.1016/j.abb.2011.12.013
Li Y-SJ, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38(10):1949–1971
Lin DC, Dimitriadis EK, Horkay F (2007) Robust strategies for automated AFM force curve analysis—I. Non-adhesive indentation of soft, inhomogeneous materials. J Biomech Eng 129(3):430–440
Lip GY, Blann A (1997) von Willebrand factor: a marker of endothelial dysfunction in vascular disorders? Cardiovasc Res 34(2):255–265
Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA (2001) Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J Biomech 34(12):1545–1553
Maul TM, Chew DW, Nieponice A, Vorp DA (2011) Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech Model Mechanobiol 10(6):939–953
Nagel T, Resnick N, Atkinson WJ, Dewey CF Jr, Gimbrone MA Jr (1994) Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest 94(2):885
Obi S, Masuda H, Shizuno T, Sato A, Yamamoto K, Ando J, Asahara T (2012) Fluid shear stress induces differentiation of circulating phenotype endothelial progenitor cells. Am J Physiol Cell Physiol 303(6):C595–C606
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
Owatverot TB, Oswald SJ, Chen Y, Wille JJ, Yin FC (2005) Effect of combined cyclic stretch and fluid shear stress on endothelial cell morphological responses. J Biomech Eng 127(3):374
Paim A, Braghirolli D, Cardozo N, Pranke P, Tessaro I (2018) Human dental pulp stem cell adhesion and detachment in polycaprolactone electrospun scaffolds under direct perfusion. Braz J Med Biol Res 51(5):e6754
Paul NE, Denecke B, Kim BS, Dreser A, Bernhagen J, Pallua N (2018) The effect of mechanical stress on the proliferation, adipogenic differentiation and gene expression of human adipose-derived stem cells. J Tissue Eng Regen Med 12(1):276–284
Peng X, Recchia FA, Byrne BJ, Wittstein IS, Ziegelstein RC, Kass DA (2000) In vitro system to study realistic pulsatile flow and stretch signaling in cultured vascular cells. Am J Physiol Cell Physiol 279(3):C797–C805
Qi M-C, Hu J, Zou SJ, Chen HQ, Zhou HX, Han LC (2008) Mechanical strain induces osteogenic differentiation: Cbfa1 and Ets-1 expression in stretched rat mesenchymal stem cells. Int J Oral Maxillofac Surg 37(5):453–458
Qiu Y, Tarbell JM (2000a) Interaction between wall shear stress and circumferential strain affects endothelial cell biochemical production. J Vasc Res 37(3):147–157
Qiu Y, Tarbell JM (2000b) Numerical simulation of pulsatile flow in a compliant curved tube model of a coronary artery. J Biomech Eng 122(1):77–85
Sachs F (2010) Stretch-activated ion channels: what are they? Physiology 25(1):50–56
Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 67(1):395–424
Shoajei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N (2014) Alteration of human umbilical vein endothelial cell gene expression in different biomechanical environments. Cell Biol Int 38(5):577–581. https://doi.org/10.1002/cbin.10237
Shojaei S, Farokhi M, Omidvar R, Mottaghitalab F, Haghighipour N, Shokrgozar M, Ai J (2013a) Essential functionality of endometrial and adipose stem cells in normal and mechanically motivated conditions. J Biomater Tissue Eng 3(5):581–588
Shojaei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N (2013b) Effects of mechanical and chemical stimuli on differentiation of human adipose-derived stem cells into endothelial cells. Int J Artif Org 36(9):663–673
Shojaei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N (2013c) Effects of mechanical and chemical stimuli on differentiation of human adipose-derived stem cells into endothelial cells. Int J Artif Org 36(9):663–673
Shojaei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N (2015) Comparative analysis of effects of cyclic uniaxial and equiaxial stretches on gene expression of human umbilical vein endothelial cells. Cell Biol Int 39(6):741–749
Simoneau B, Houle F, Huot J (2012) Regulation of endothelial permeability and transendothelial migration of cancer cells by tropomyosin-1 phosphorylation. Vasc Cell 4(1):18
Steinman DA, Thomas JB, Ladak HM, Milner JS, Rutt BK, Spence JD (2002) Reconstruction of carotid bifurcation hemodynamics and wall thickness using computational fluid dynamics and MRI. Magn Reson Med 47(1):149–159
Suhalim JL, Chung C-Y, Lilledahl MB, Lim RS, Levi M, Tromberg BJ, Potma EO (2012) Characterization of cholesterol crystals in atherosclerotic plaques using stimulated Raman scattering and second-harmonic generation microscopy. Biophys J 102(8):1988–1995
Tada S, Tarbell J (2005) A computational study of flow in a compliant carotid bifurcation–stress phase angle correlation with shear stress. Ann Biomed Eng 33(9):1202–1212
Tada S, Dong C, Tarbell JM (2007) Effect of the stress phase angle on the strain energy density of the endothelial plasma membrane. Biophys J 93(9):3026–3033
Vining KH, Mooney DJ (2017) Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol 18(12):728
Vischer U (2006) von Willebrand factor, endothelial dysfunction, and cardiovascular disease. J Thromb Haemost 4(6):1186–1193
Wang JH-C, Goldschmidt-Clermont P, Wille J, Yin FC-P (2001) Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J Biomech 34(12):1563–1572
Wu C-C, Chao Y-C, Chen C-N, Chien S, Chen Y-C, Chien C-C, Linju BL (2008) Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells. J Biomech 41(4):813–821
Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A, Ando J (2003) Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 95(5):2081–2088
Yourek G, McCormick SM, Mao JJ, Reilly GC (2010) Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen Med 5(5):713–724