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Regulation of Vascular Smooth Muscle Cell Stiffness and Adhesion by [Ca2+]i: An Atomic Force Microscopy-Based Study

Published online by Cambridge University Press:  05 December 2018

Yi Zhu*
Affiliation:
Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA Department of Biomedical Engineering, University of Alabama at Birmingham, Birmingham, AL 35294, USA
Li He
Affiliation:
Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA
Jing Qu
Affiliation:
Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA
Yong Zhou*
Affiliation:
Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA Dalton Cardiovascular Research Center, University of Missouri, Columbia, MO 65211, USA Department of Ophthalmology, University of Alabama at Birmingham, Birmingham, AL 35294, USA
*
Author for correspondence: Yi Zhu, E-mail: [email protected]; Yong Zhou, E-mail: [email protected]
Author for correspondence: Yi Zhu, E-mail: [email protected]; Yong Zhou, E-mail: [email protected]
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Abstract

The intracellular concentration of calcium ion ([Ca2+]i) is a critical regulator of cell signaling and contractility of vascular smooth muscle cells (VSMCs). In this study, we employed an atomic force microscopy (AFM) nanoindentation-based approach to investigate the role of [Ca2+]i in regulating the cortical elasticity of rat cremaster VSMCs and the ability of rat VSMCs to adhere to fibronectin (Fn) matrix. Elevation of [Ca2+]i by ionomycin treatment increased rat VSMC stiffness and cell adhesion to Fn-biofunctionalized AFM probes, whereas attenuation of [Ca2+]i by 1,2-Bis (2-aminophenoxy)ethane-N,N,N’,N’-tetraacetic acid tetrakis (acetoxymethyl ester) (BAPTA-AM) treatment decreased the mechanical and matrix adhesive properties of VSMCs. Furthermore, we found that ionomycin/BAPTA-AM treatments altered expression of α5 integrin subunits and α smooth muscle actin in rat VSMCs. These data suggest that [Ca2+]i regulates VSMC elasticity and adhesion to the extracellular matrix by a potential mechanism involving changing dynamics of the integrin–actin cytoskeleton axis.

Type
Biological Science Applications
Copyright
© Microscopy Society of America 2018 

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Footnotes

Cite this article: Zhu Y, He L, Qu J and Zhou Y (2018) Regulation of Vascular Smooth Muscle Cell Stiffness and Adhesion by [Ca2+]i: An Atomic Force Microscopy-Based Study. Microsc Microanal. 24(6), 708–712. doi: 10.1017/S1431927618015519

References

Bootman, MD (2012) Calcium signaling. Cold Spring Harb Perspect Biol 4, a011171.Google Scholar
Hong, Z, Reeves, KJ, Sun, Z, Li, Z, Brown, NJ and Meininger, GA (2015) Vascular smooth muscle cell stiffness and adhesion to collagen I modified by vasoactive agonists. PLoS One 10, e0119533.Google Scholar
Hong, Z, Sun, Z, Li, M, Li, ZH, Bunyak, F, Ersoy, I, Trzeciakowski, JP, Staiculescu, MC, Jin, M, Martinez-Lemus, L, Hill, MA, Palaniappan, K and Meininger, GA (2014) Vasoactive agonists exert dynamic and coordinated effects on vascular smooth muscle cell elasticity, cytoskeletal remodelling and adhesion. J Physiol 592, 12491266.Google Scholar
Hong, Z, Sun, Z, Li, Z, Mesquitta, WT, Trzeciakowski, JP and Meininger, GA (2012) Coordination of fibronectin adhesion with contraction and relaxation in microvascular smooth muscle. Cardiovasc Res 96, 7380.Google Scholar
Jackson, TY, Sun, Z, Martinez-Lemus, LA, Hill, MA and Meininger, GA (2010) N-Cadherin and integrin blockade inhibit arteriolar myogenic reactivity but not pressure-induced increases in intracellular Ca2+ . Front Physiol 1, a165.Google Scholar
Metz, RP, Patterson, JL and Wilson, E (2012) Vascular smooth muscle cells: isolation, culture, and characterization. Methods Mol Biol 843, 169176.Google Scholar
Morgan, AJ and Jacob, R (1994) Ionomycin enhances Ca2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochem J 300, 665672.Google Scholar
Qiu, HY, Zhu, Y, Sun, Z, Trzeciakowski, JP, Gansner, M, Depre, C, Resuello Ranillo, RG, Natividad, FF, Hunter, WC, Genin, GM, Elson, EL, Vatner, DE, Meininger, GA and Vatner, SF (2010) Vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging. Circ Res 107, 615619.Google Scholar
Schillers, H, Walte, M, Urbanova, K and Oberleithner, H (2010) Real-time monitoring of cell elasticity reveals oscillating myosin activity. Biophys J 99, 36393646.Google Scholar
Sehgel, NL, Sun, Z, Hong, Z, Hunter, WC, Hill, MA, Vatner, DE, Vatner, SF and Meininger, GA (2015) Augmented vascular smooth muscle cell stiffness and adhesion when hypertension is superimposed on aging. Hypertension 65, 370377.Google Scholar
Sehgel, NL, Zhu, Y, Sun, Z, Trzeciakowski, JP, Hong, Z, Hunter, WC, Vatner, DE, Meininger, GA and Vatner, SF (2013) Increased vascular smooth muscle cell stiffness: a novel mechanism for aortic stiffness in hypertension. Am J Physiol Heart Circ Physiol 305, H1281H1287.Google Scholar
Sun, Z, Li, Z and Meininger, GA (2012) Mechanotransduction through fibronectin–integrin focal adhesion in microvascular smooth muscle cells: is calcium essential? Am J Physiol Heart Circ Physiol 302, H1965H1973.Google Scholar
Sun, Z, Martinez-Lemus, LA, Hill, MA and Meininger, GA (2008) Extracellular matrix-specific focal adhesions in vascular smooth muscle produce mechanically active adhesion sites. Am J Physiol Cell Physiol 295, C268C278.Google Scholar
Sun, Z, Martinez-Lemus, LA, Trache, A, Trzeciakowski, JP, Davis, GE, Pohl, U and Meininger, GA (2005) Mechanical properties of the interaction between fibronectin and α5β1-integrin on vascular smooth muscle cells studied using atomic force microscopy. Am J Physiol Heart Circ Physiol 289, H2526H2535.Google Scholar
Uehata, M, Ishizaki, T, Satoh, H, Ono, T, Kawahara, T, Morishita, T, Tamakawa, H, Yamagami, K, Inui, J, Maekawa, M and Narumiya, S (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990994.Google Scholar
Yamin, R and Morgan, KG (2012) Deciphering actin cytoskeletal function in the contractile vascular smooth muscle cell. J Physiol 590, 41454154.Google Scholar
Zhu, Y, Qiu, H, Trzeciakowski, JP, Sun, Z, Li, Z, Hong, Z, Hill, MA, Hunter, WC, Vatner, DE, Vatner, SF and Meininger, GA (2012) Temporal analysis of vascular smooth muscle cell elasticity and adhesion reveals oscillation waveforms that differ with aging. Aging Cell 11, 741750.Google Scholar