10.1007/s40204-018-0090-5

Stress phase angle regulates differentiation of human adipose-derived stem cells toward endothelial phenotype

HTML PDF
  • Shahrokh Shojaei1,
  • Mohammad Tafazzoli-Shadpour*2,
  • Mohammad Ali Shokrgozar3,
  • Nooshin Haghighipour3,
  • Fatemeh Hejazi Jahromi4,
  1. Faculty of Biomedical Engineering, Central Tehran Branch, Islamic Azad University, Tehran, IR
  2. Cardiovascular Engineering Lab., Faculty of Biomedical Engineering, Amirkabir University of Technology, Tehran, 158754413, IR
  3. National Cell Bank of Iran, Pasteur Institute of Iran, Tehran, 1316943551, IR
  4. Hard Tissue Engineering Research Center, Tissue Engineering and Regenerative Medicine Institute, Central Tehran Branch, Islamic Azad University, Tehran, IR
Cover Image

Published in Issue 2018-05-21

How to Cite

Shojaei, S., Tafazzoli-Shadpour, M., Shokrgozar, M. A., Haghighipour, N., & Jahromi, F. H. (2018). Stress phase angle regulates differentiation of human adipose-derived stem cells toward endothelial phenotype. Progress in Biomaterials, 7(2 (June 2018). https://doi.org/10.1007/s40204-018-0090-5
Crossref
Scopus
Google Scholar
Europe PMC

Abstract

Abstract 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.

Keywords

  • Stress phase angel,
  • Shear stress,
  • Cyclic stretch,
  • Adipose mesenchymal stem cells,
  • Cell behavior
HTML PDF

References

  1. Alves da Silva et al. (2011) Chondrogenic differentiation of human bone marrow mesenchymal stem cells in chitosan-based scaffolds using a flow-perfusion bioreactor 5(9) (pp. 722-732) https://doi.org/10.1002/term.372
  2. Barron et al. (2007) The effect of physiological cyclic stretch on the cell morphology, cell orientation and protein expression of endothelial cells 18(10) (pp. 1973-1981) https://doi.org/10.1007/s10856-007-3125-3
  3. Bassiouny et al. (1992) Anastomotic intimal hyperplasia: mechanical injury or flow induced 15(4) (pp. 708-717) https://doi.org/10.1016/0741-5214(92)90019-5
  4. Byfield et al. (2009) Endothelial actin and cell stiffness is modulated by substrate stiffness in 2D and 3D 42(8) (pp. 1114-1119) https://doi.org/10.1016/j.jbiomech.2009.02.012
  5. Cevallos et al. (2006) Cyclic strain induces expression of specific smooth muscle cell markers in human endothelial cells 74(9) (pp. 552-561) https://doi.org/10.1111/j.1432-0436.2006.00089.x
  6. Charoenpanich et al. (2014) Cyclic tensile strain enhances osteogenesis and angiogenesis in mesenchymal stem cells from osteoporotic donors 20(1–2) (pp. 67-78) https://doi.org/10.1089/ten.tea.2013.0006
  7. Charrier et al. (2018) Control of cell morphology and differentiation by substrates with independently tunable elasticity and viscous dissipation 9(1) https://doi.org/10.1038/s41467-018-02906-9
  8. Dancu and Tarbell (2006) Large negative stress phase angle (SPA) attenuates nitric oxide production in bovine aortic endothelial cells 128(3) https://doi.org/10.1115/1.1824120
  9. Doggett et al. (2002) Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIbα-vWF Tether bond 83(1) (pp. 194-205) https://doi.org/10.1016/S0006-3495(02)75161-8
  10. Dolan et al. (2011) High fluid shear stress and spatial shear stress gradients affect endothelial proliferation, survival, and alignment 39(6) (pp. 1620-1631) https://doi.org/10.1007/s10439-011-0267-8
  11. Elhadj et al. (2003) Chronic pulsatile shear stress alters insulin-like growth factor-I (IGF-I) binding protein release in vitro 31(2) (pp. 163-170) https://doi.org/10.1114/1.1540637
  12. Estes et al. (2010) Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype 5(7) (pp. 1294-1311) https://doi.org/10.1038/nprot.2010.81
  13. Gavard (2009) Breaking the VE-cadherin bonds 583(1) (pp. 1-6) https://doi.org/10.1016/j.febslet.2008.11.032
  14. Guo and Hamilton (1996) 13C MAS NMR studies of crystalline cholesterol and lipid mixtures modeling atherosclerotic plaques 71(5) (pp. 2857-2868) https://doi.org/10.1016/S0006-3495(96)79482-1
  15. Haga et al. (2007) Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells 40(5) (pp. 947-960) https://doi.org/10.1016/j.jbiomech.2006.04.011
  16. Haghighipour et al. (2010) Effects of cyclic stretch waveform on endothelial cell morphology using fractal analysis 34(6) (pp. 481-490) https://doi.org/10.1111/j.1525-1594.2010.01003.x
  17. Holmes et al. (2007) Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition 19(10) (pp. 2003-2012) https://doi.org/10.1016/j.cellsig.2007.05.013
  18. Huang et al. (2010) Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells 41(7) (pp. 497-505) https://doi.org/10.1016/j.arcmed.2010.10.002
  19. Huang et al. (2012) Effect of cyclic strain on cardiomyogenic differentiation of rat bone marrow derived mesenchymal stem cells 7(4) https://doi.org/10.1371/journal.pone.0034960
  20. Hutter and Bechhoefer (1993) Calibration of atomic-force microscope tips 64(7) (pp. 1868-1873) https://doi.org/10.1063/1.1143970
  21. James et al. (1995) Effects of shear on endothelial cell calcium in the presence and absence of ATP 9(10) (pp. 968-973) https://doi.org/10.1096/fasebj.9.10.7615166
  22. Jeon et al. (2014) A mini-review: cell response to microscale, nanoscale, and hierarchical patterning of surface structure 102(7) (pp. 1580-1594) https://doi.org/10.1002/jbm.b.33158
  23. Joshi et al. (2004) Intimal thickness is not associated with wall shear stress patterns in the human right coronary artery 24(12) (pp. 2408-2413) https://doi.org/10.1161/01.ATV.0000147118.97474.4b
  24. Kang et al. (2014) Effect of shear stress on water and LDL transport through cultured endothelial cell monolayers 233(2) (pp. 682-690) https://doi.org/10.1016/j.atherosclerosis.2014.01.056
  25. Ku et al. (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress 5(3) (pp. 293-302) https://doi.org/10.1161/01.ATV.5.3.293
  26. La and Tranquillo (2018) Shear conditioning of adipose stem cells for reduced platelet binding to engineered vascular grafts https://doi.org/10.1089/ten.tea.2017.0475
  27. Lekka et al. (2012) Cancer cell detection in tissue sections using AFM 518(2) (pp. 151-156) https://doi.org/10.1016/j.abb.2011.12.013
  28. Li et al. (2005) Molecular basis of the effects of shear stress on vascular endothelial cells 38(10) (pp. 1949-1971) https://doi.org/10.1016/j.jbiomech.2004.09.030
  29. Lin et al. (2007) Robust strategies for automated AFM force curve analysis—I. Non-adhesive indentation of soft, inhomogeneous materials 129(3) (pp. 430-440) https://doi.org/10.1115/1.2720924
  30. Lip and Blann (1997) von Willebrand factor: a marker of endothelial dysfunction in vascular disorders? 34(2) (pp. 255-265) https://doi.org/10.1016/S0008-6363(97)00039-4
  31. Mathur et al. (2001) Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy 34(12) (pp. 1545-1553) https://doi.org/10.1016/S0021-9290(01)00149-X
  32. Maul et al. (2011) Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation 10(6) (pp. 939-953) https://doi.org/10.1007/s10237-010-0285-8
  33. Nagel et al. (1994) Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells 94(2) https://doi.org/10.1172/JCI117410
  34. Obi et al. (2012) Fluid shear stress induces differentiation of circulating phenotype endothelial progenitor cells 303(6) (pp. C595-C606) https://doi.org/10.1152/ajpcell.00133.2012
  35. Ohashi et al. (2007) Hydrostatic pressure influences morphology and expression of VE-cadherin of vascular endothelial cells 40(11) (pp. 2399-2405) https://doi.org/10.1016/j.jbiomech.2006.11.023
  36. Owatverot et al. (2005) Effect of combined cyclic stretch and fluid shear stress on endothelial cell morphological responses 127(3) https://doi.org/10.1115/1.1894180
  37. Paim et al. (2018) Human dental pulp stem cell adhesion and detachment in polycaprolactone electrospun scaffolds under direct perfusion 51(5) https://doi.org/10.1590/1414-431x20186754
  38. Paul et al. (2018) The effect of mechanical stress on the proliferation, adipogenic differentiation and gene expression of human adipose-derived stem cells 12(1) (pp. 276-284) https://doi.org/10.1002/term.2411
  39. Peng et al. (2000) In vitro system to study realistic pulsatile flow and stretch signaling in cultured vascular cells 279(3) (pp. C797-C805) https://doi.org/10.1152/ajpcell.2000.279.3.C797
  40. Qi et al. (2008) Mechanical strain induces osteogenic differentiation: Cbfa1 and Ets-1 expression in stretched rat mesenchymal stem cells 37(5) (pp. 453-458) https://doi.org/10.1016/j.ijom.2007.12.008
  41. Qiu and Tarbell (2000) Interaction between wall shear stress and circumferential strain affects endothelial cell biochemical production 37(3) (pp. 147-157) https://doi.org/10.1159/000025726
  42. Qiu and Tarbell (2000) Numerical simulation of pulsatile flow in a compliant curved tube model of a coronary artery 122(1) (pp. 77-85) https://doi.org/10.1115/1.429629
  43. Sachs (2010) Stretch-activated ion channels: what are they? 25(1) (pp. 50-56) https://doi.org/10.1152/physiol.00042.2009
  44. Sadler (1998) Biochemistry and genetics of von Willebrand factor 67(1) (pp. 395-424) https://doi.org/10.1146/annurev.biochem.67.1.395
  45. Shoajei et al. (2014) Alteration of human umbilical vein endothelial cell gene expression in different biomechanical environments 38(5) (pp. 577-581) https://doi.org/10.1002/cbin.10237
  46. Shojaei et al. (2013) Essential functionality of endometrial and adipose stem cells in normal and mechanically motivated conditions 3(5) (pp. 581-588) https://doi.org/10.1166/jbt.2013.1115
  47. Shojaei et al. (2013) Effects of mechanical and chemical stimuli on differentiation of human adipose-derived stem cells into endothelial cells 36(9) (pp. 663-673) https://doi.org/10.5301/ijao.5000242
  48. Shojaei et al. (2013) Effects of mechanical and chemical stimuli on differentiation of human adipose-derived stem cells into endothelial cells 36(9) (pp. 663-673) https://doi.org/10.5301/ijao.5000242
  49. Shojaei et al. (2015) Comparative analysis of effects of cyclic uniaxial and equiaxial stretches on gene expression of human umbilical vein endothelial cells 39(6) (pp. 741-749) https://doi.org/10.1002/cbin.10443
  50. Simoneau et al. (2012) Regulation of endothelial permeability and transendothelial migration of cancer cells by tropomyosin-1 phosphorylation 4(1) https://doi.org/10.1186/2045-824X-4-18
  51. Steinman et al. (2002) Reconstruction of carotid bifurcation hemodynamics and wall thickness using computational fluid dynamics and MRI 47(1) (pp. 149-159) https://doi.org/10.1002/mrm.10025
  52. Suhalim et al. (2012) Characterization of cholesterol crystals in atherosclerotic plaques using stimulated Raman scattering and second-harmonic generation microscopy 102(8) (pp. 1988-1995) https://doi.org/10.1016/j.bpj.2012.03.016
  53. Tada and Tarbell (2005) A computational study of flow in a compliant carotid bifurcation–stress phase angle correlation with shear stress 33(9) (pp. 1202-1212) https://doi.org/10.1007/s10439-005-5630-1
  54. Tada et al. (2007) Effect of the stress phase angle on the strain energy density of the endothelial plasma membrane 93(9) (pp. 3026-3033) https://doi.org/10.1529/biophysj.106.100685
  55. Vining and Mooney (2017) Mechanical forces direct stem cell behaviour in development and regeneration 18(12) https://doi.org/10.1038/nrm.2017.108
  56. Vischer (2006) von Willebrand factor, endothelial dysfunction, and cardiovascular disease 4(6) (pp. 1186-1193) https://doi.org/10.1111/j.1538-7836.2006.01949.x
  57. Wang et al. (2001) Specificity of endothelial cell reorientation in response to cyclic mechanical stretching 34(12) (pp. 1563-1572) https://doi.org/10.1016/S0021-9290(01)00150-6
  58. Wu et al. (2008) Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells 41(4) (pp. 813-821) https://doi.org/10.1016/j.jbiomech.2007.11.008
  59. Yamamoto et al. (2003) Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress 95(5) (pp. 2081-2088) https://doi.org/10.1152/japplphysiol.00232.2003
  60. Yourek et al. (2010) Shear stress induces osteogenic differentiation of human mesenchymal stem cells 5(5) (pp. 713-724) https://doi.org/10.2217/rme.10.60