Functional Remodeling of the Contractile Smooth Muscle Cell Cortex, a Provocative Concept, Supported by Direct Visualization of Cortical Remodeling
Considerable controversy has surrounded the functional anatomy of the cytoskeleton of the contractile vascular smooth muscle cell. Recent studies have suggested a dynamic nature of the cortical cytoskeleton of these cells, but direct proof has been lacking. Here, we review past studies in this area...
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Published in | Biology (Basel, Switzerland) Vol. 11; no. 5; p. 662 |
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Abstract | Considerable controversy has surrounded the functional anatomy of the cytoskeleton of the contractile vascular smooth muscle cell. Recent studies have suggested a dynamic nature of the cortical cytoskeleton of these cells, but direct proof has been lacking. Here, we review past studies in this area suggesting a plasticity of smooth muscle cells. We also present images testing these suggestions by using the technique of immunoelectron microscopy of metal replicas to directly visualize the cortical actin cytoskeleton of the contractile smooth muscle cell along with interactions by representative cytoskeletal binding proteins. We find the cortical cytoskeletal matrix to be a branched, interconnected network of linear actin bundles. Here, the focal adhesion proteins talin and zyxin were localized with nanometer accuracy. Talin is reported in past studies to span the integrin-cytoplasm distance in fibroblasts and zyxin is known to be an adaptor protein between alpha-actinin and VASP. In response to activation of signal transduction with the alpha-agonist phenylephrine, we found that no movement of talin was detectable but that the zyxin-zyxin spacing was statistically significantly decreased in the smooth muscle cells examined. Contractile smooth muscle is often assumed to have a fixed cytoskeletal structure. Thus, the results included here are important in that they directly support the concept at the electron microscopic level that the focal adhesion of the contractile smooth muscle cell has a dynamic nature and that the protein-protein interfaces showing plasticity are protein-specific. |
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AbstractList | Considerable controversy has surrounded the functional anatomy of the cytoskeleton of the contractile vascular smooth muscle cell. Recent studies have suggested a dynamic nature of the cortical cytoskeleton of these cells, but direct proof has been lacking. Here, we review past studies in this area suggesting a plasticity of smooth muscle cells. We also present images testing these suggestions by using the technique of immunoelectron microscopy of metal replicas to directly visualize the cortical actin cytoskeleton of the contractile smooth muscle cell along with interactions by representative cytoskeletal binding proteins. We find the cortical cytoskeletal matrix to be a branched, interconnected network of linear actin bundles. Here, the focal adhesion proteins talin and zyxin were localized with nanometer accuracy. Talin is reported in past studies to span the integrin-cytoplasm distance in fibroblasts and zyxin is known to be an adaptor protein between alpha-actinin and VASP. In response to activation of signal transduction with the alpha-agonist phenylephrine, we found that no movement of talin was detectable but that the zyxin-zyxin spacing was statistically significantly decreased in the smooth muscle cells examined. Contractile smooth muscle is often assumed to have a fixed cytoskeletal structure. Thus, the results included here are important in that they directly support the concept at the electron microscopic level that the focal adhesion of the contractile smooth muscle cell has a dynamic nature and that the protein-protein interfaces showing plasticity are protein-specific. Simple SummaryAs a key element of the smooth muscle cell contractile apparatus, the actin cytoskeleton participates in the development of force by acting as a molecular track for the myosin cross bridge motor. At the same time, the actin cytoskeleton must transmit the force developed during contraction to the extracellular matrix and, thus, to neighboring cells. This propagation of force to the cell periphery and beyond is initiated in part on specifically localized cellular cortical actin filaments also involved in mechano-chemical transduction. During the contractile process itself and in response to extracellular structural and chemical alterations, the smooth muscle actin cytoskeletal remodels. This indicates that the cytoskeleton is a dynamic cellular organelle that adapts to the changes in cell shape and chemical cues. Current evidence connecting contractile function and mechano-transduction mechanisms to the plasticity of the vascular smooth muscle actin cytoskeleton is reviewed; we then describe new evidence for cytoskeletal remodeling in vascular smooth muscle cells. Here, using immunoelectron microscopy, we visualize the actin binding proteins filamin A, zyxin and talin in these cells and show that they participate in the cortical cell cytoskeletal alteration, thus supporting the premise that smooth muscle cell remodeling occurs during contraction.AbstractConsiderable controversy has surrounded the functional anatomy of the cytoskeleton of the contractile vascular smooth muscle cell. Recent studies have suggested a dynamic nature of the cortical cytoskeleton of these cells, but direct proof has been lacking. Here, we review past studies in this area suggesting a plasticity of smooth muscle cells. We also present images testing these suggestions by using the technique of immunoelectron microscopy of metal replicas to directly visualize the cortical actin cytoskeleton of the contractile smooth muscle cell along with interactions by representative cytoskeletal binding proteins. We find the cortical cytoskeletal matrix to be a branched, interconnected network of linear actin bundles. Here, the focal adhesion proteins talin and zyxin were localized with nanometer accuracy. Talin is reported in past studies to span the integrin–cytoplasm distance in fibroblasts and zyxin is known to be an adaptor protein between alpha-actinin and VASP. In response to activation of signal transduction with the alpha-agonist phenylephrine, we found that no movement of talin was detectable but that the zyxin-zyxin spacing was statistically significantly decreased in the smooth muscle cells examined. Contractile smooth muscle is often assumed to have a fixed cytoskeletal structure. Thus, the results included here are important in that they directly support the concept at the electron microscopic level that the focal adhesion of the contractile smooth muscle cell has a dynamic nature and that the protein–protein interfaces showing plasticity are protein-specific. |
Author | Lehman, William Suphamungmee, Worawit Morgan, Kathleen G |
AuthorAffiliation | 2 Department of Health Sciences, Boston University Sargent College, 635 Commonwealth Ave., Boston, MA 02215, USA 3 Department of Physiology & Biophysics, Boston University School of Medicine, 700 Albany Street, Boston, MA 02118, USA 1 Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand; worawit.sup@mahidol.ac.th |
AuthorAffiliation_xml | – name: 2 Department of Health Sciences, Boston University Sargent College, 635 Commonwealth Ave., Boston, MA 02215, USA – name: 1 Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok 10400, Thailand; worawit.sup@mahidol.ac.th – name: 3 Department of Physiology & Biophysics, Boston University School of Medicine, 700 Albany Street, Boston, MA 02118, USA |
Author_xml | – sequence: 1 givenname: Worawit orcidid: 0000-0002-1576-8608 surname: Suphamungmee fullname: Suphamungmee, Worawit organization: Department of Physiology & Biophysics, Boston University School of Medicine, 700 Albany Street, Boston, MA 02118, USA – sequence: 2 givenname: William surname: Lehman fullname: Lehman, William organization: Department of Physiology & Biophysics, Boston University School of Medicine, 700 Albany Street, Boston, MA 02118, USA – sequence: 3 givenname: Kathleen G orcidid: 0000-0003-3300-3630 surname: Morgan fullname: Morgan, Kathleen G organization: Department of Health Sciences, Boston University Sargent College, 635 Commonwealth Ave., Boston, MA 02215, USA |
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Keywords | actin immunoelectron microscopy vascular smooth muscle talin zyxin |
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Snippet | Considerable controversy has surrounded the functional anatomy of the cytoskeleton of the contractile vascular smooth muscle cell. Recent studies have... Simple SummaryAs a key element of the smooth muscle cell contractile apparatus, the actin cytoskeleton participates in the development of force by acting as a... |
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SubjectTerms | Actin Actinin Adaptor proteins Adhesion Cardiovascular disease Cell size Chemical stimuli Cytoplasm Cytoskeleton Extracellular matrix Fibroblasts Filaments Functional anatomy Immunoelectron microscopy Interfaces Kinases Mechanotransduction Microscopy Muscle contraction Myosin Phenylephrine Polymerization Proteins Review Signal transduction Smooth muscle Talin vascular smooth muscle zyxin |
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Title | Functional Remodeling of the Contractile Smooth Muscle Cell Cortex, a Provocative Concept, Supported by Direct Visualization of Cortical Remodeling |
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