Mechanism of stretch-induced activation of the mechanotransducer zyxin in vascular cells

Science Signaling

Volumn 5, Issue 254, 2012, Pages

  Babu, Sahana Suresh ^a,c   Wojtowicz, Agnieszka ^a,d   Freichel, Marc ^a   Birnbaumer, Lutz ^b   Hecker, Markus ^a   Cattaruzza, Marco ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; ENDOTHELIN 1; GUANYLATE CYCLASE ACTIVATOR; SMALL INTERFERING RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; ZYXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CELL GROWTH; CELL NUCLEUS; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; FEMORAL ARTERY; GENE EXPRESSION; GENE INACTIVATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; STRETCH RECEPTOR;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ARTERIES; ATRIAL NATRIURETIC FACTOR; CELL NUCLEUS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIN-1; GENE EXPRESSION REGULATION; GUANYLATE CYCLASE; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; STRESS, MECHANICAL; TRANSIENT RECEPTOR POTENTIAL CHANNELS; ZYXIN;

EID: 84871153587     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003173     Document Type: Article

References (45)

1. P. F. Davies, Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc. Med. 6, 16-26 (2009).
2. N. Frey, E. N. Olson, Cardiac hypertrophy: The good, the bad, and the ugly. Annu. Rev. Physiol. 65, 45-79 (2003).
3. T. Macalma, J. Otte, M. E. Hensler, S. M. Bockholt, H. A. Louis, M. Kalff-Suske, K. H. Grzeschik, D. von der Ahe, M. C. Beckerle, Molecular characterization of human zyxin. J. Biol. Chem. 271, 31470-31478 (1996).
4. L. M. Hoffman, D. A. Nix, B. Benson, R. Boot-Hanford, E. Gustafsson, C. Jamora, A. S. Menzies, K. L. Goh, C. C. Jensen, F. B. Gertler, E. Fuchs, R. Fässler, M. C. Beckerle, Targeted disruption of the murine zyxin gene. Mol. Cell. Biol. 23, 70-79 (2003).
5. M. Cattaruzza, C. Lattrich, M. Hecker, The focal adhesion protein zyxin is a mechanosensitive modulator of gene expression in vascular smooth muscle cells. Hypertension 43, 726-730 (2004).
6. A. Wójtowicz, S. S. Babu, L. Li, N. Gretz, M. Hecker, M. Cattaruzza, Zyxin mediation of stretch-induced gene expression in human endothelial cells. Circ. Res. 107, 898-902 (2010).
7. M. Yoshigi, L. M. Hoffman, C. C. Jensen, H. J. Yost, M. C. Beckerle, Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J. Cell Biol. 171, 209-215 (2005).
8. T. Kato, J. Muraski, Y. Chen, Y. Tsujita, J. Wall, C. C. Glembotski, E. Schaefer, M. Beckerle, M. A. Sussman, Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and Akt. J. Clin. Invest. 115, 2716-2730 (2005).
9. A receptors. Am. J. Physiol. Renal Physiol. 286, F660-F668 (2004).
10. 2/ω-hydroxylase/20-HETE pathways. Circ. Res. 104, 1399-1409 (2009).
11. R. Sharif-Naeini, A. Dedman, J. H. Folgering, F. Duprat, A. Patel, B. Nilius, E. Honoré, TRP channels and mechanosensory transduction: Insights into the arterial myogenic response. Pflugers Arch. 456, 529-540 (2008).
12. I. Kishimoto, S. K. Dubois, D. L. Garbers, The heart communicates with the kidney exclusively through the guanylyl cyclase-A receptor: Acute handling of sodium and water in response to volume expansion. Proc. Natl. Acad. Sci. U.S.A. 93, 6215-6219 (1996).
13. B. Schreier, S. Börner, K. Völker, S. Gambaryan, S. C. Schäfer, P. Kuhlencordt, B. Gassner, M. Kuhn, The heart communicates with the endothelium through the guanylyl cyclase-A receptor: Acute handling of intravascular volume in response to volume expansion. Endocrinology 149, 4193-4199 (2008).
14. D. R. Pimentel, J. K. Amin, L. Xiao, T. Miller, J. Viereck, J. Oliver-Krasinski, R. Baliga, J. Wang, D. A. Siwik, K. Singh, P. Pagano, W. S. Colucci, D. B. Sawyer, Reactive oxygen species mediate amplitude-dependent hypertrophic and apoptotic responses to mechanical stretch in cardiac myocytes. Circ. Res. 89, 453-460 (2001).
15. R. Inoue, Z. Jian, Y. Kawarabayashi, Mechanosensitive TRP channels in cardiovascular pathophysiology. Pharmacol. Ther. 123, 371-385 (2009).
16. A. Dietrich, H. Kalwa, U. Storch, M. Mederos y Schnitzler, B. Salanova, O. Pinkenburg, G. Dubrovska, K. Essin, M. Gollasch, L. Birnbaumer, T. Gudermann, Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch. 455, 465-477 (2007).
17. M. Freichel, S. H. Suh, A. Pfeifer, U. Schweig, C. Trost, P. Weissgerber, M. Biel, S. Philipp, D. Freise, G. Droogmans, F. Hofmann, V. Flockerzi, B. Nilius, Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4-/- mice. Nat. Cell Biol. 3, 121-127 (2001).
18. A. Dietrich, M. Mederos Y Schnitzler, M. Gollasch, V. Gross, U. Storch, G. Dubrovska, M. Obst, E. Yildirim, B. Salanova, H. Kalwa, K. Essin, O. Pinkenburg, F. C. Luft, T. Gudermann, L. Birnbaumer, Increased vascular smooth muscle contractility in TRPC6-/- mice. Mol. Cell. Biol. 25, 6980-6989 (2005).
19. J. Hartmann, E. Dragicevic, H. Adelsberger, H. A. Henning, M. Sumser, J. Abramowitz, R. Blum, A. Dietrich, M. Freichel, V. Flockerzi, L. Birnbaumer, A. Konnerth, TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 59, 392-398 (2008).
20. 2+-dependent toxicity. Gastroenterology 140, 2107-2115 (2011).
21. M. J. Lopez, S. K. Wong, I. Kishimoto, S. Dubois, V. Mach, J. Friesen, D. L. Garbers, A. Beuve, Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature 378, 65-68 (1995).
22. K. Sabrane, M. N. Kruse, L. Fabritz, B. Zetsche, D. Mitko, B. V. Skryabin, M. Zwiener, H. A. Baba, M. Yanagisawa, M. Kuhn, Vascular endothelium is critically involved in the hypotensive and hypovolemic actions of atrial natriuretic peptide. J. Clin. Invest. 115, 1666-1674 (2005).
23. N. Blom, T. Sicheritz-Pontén, R. Gupta, S. Gammeltoft, S. Brunak, Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649 (2004).
24. K. Quick, J. Zhao, N. Eijkelkamp, J. E. Linley, F. Rugiero, J. J. Cox, R. Raouf, M. Gringhuis, J. E. Sexton, J. Abramowitz, R. Taylor, A. Forge, J. Ashmore, N. Kirkwood, C. J. Kros, G. P. Richardson, M. Freichel, V. Flockerzi, L. Birnbaumer, J. N. Wood, TRPC3 and TRPC6 are essential for normal mechanotransduction in subsets of sensory neurons and cochlear hair cells. Open Biol. 2, 120068 (2012).
25. D. J. Beech, Emerging functions of 10 types of TRP cationic channel in vascular smooth muscle. Clin. Exp. Pharmacol. Physiol. 32, 597-603 (2005).
26. F. Thilo, C. Loddenkemper, E. Berg, W. Zidek, M. Tepel, Increased TRPC3 expression in vascular endothelium of patients with malignant hypertension. Mod. Pathol. 22, 426-430 (2009).
27. Z. Zhao, Y. Ni, J. Chen, J. Zhong, H. Yu, X. Xu, H. He, Z. Yan, A. Scholze, D. Liu, Z. Zhu, M. Tepel, Increased migration of monocytes in essential hypertension is associated with increased transient receptor potential channel canonical type 3 channels. PLoS One 7, e32628 (2012).
28. D. Liu, D. Yang, H. He, X. Chen, T. Cao, X. Feng, L. Ma, Z. Luo, L. Wang, Z. Yan, Z. Zhu, M. Tepel, Increased transient receptor potential canonical type 3 channels in vasculature from hypertensive rats. Hypertension 53, 70-76 (2009).
29. H. Macarthur, T. D. Warner, E. G. Wood, R. Corder, J. R. Vane, Endothelin-1 release from endothelial cells in culture is elevated both acutely and chronically by short periods of mechanical stretch. Biochem. Biophys. Res. Commun. 200, 395-400 (1994).
30. M. Cattaruzza, C. Dimigen, H. Ehrenreich, M. Hecker, Stretch-induced endothelin B receptor-mediated apoptosis in vascular smooth muscle cells. FASEB J. 14, 991-998 (2000).
31. A receptor blockade prevents increased tissue endothelin-1, vascular hypertrophy, and endothelial dysfunction in salt-sensitive hypertension. Hypertension 31, 499-504 (1998).
32. F. Amiri, A. Virdis, M. F. Neves, M. Iglarz, N. G. Seidah, R. M. Touyz, T. L. Reudelhuber, E. L. Schiffrin, Endothelium-restricted overexpression of human endothelin-1 causes vascular remodeling and endothelial dysfunction. Circulation 110, 2233-2240 (2004).
33. C. Delli Gatti, E. Osto, A. Kouroedov, M. Eto, S. Shaw, M. Volpe, T. F. Lüscher, F. Cosentino, Pulsatile stretch induces release of angiotensin II and oxidative stress in human endothelial cells: Effects of ACE inhibition and AT1 receptor antagonism. Clin. Exp. Hypertens 30, 616-627 (2008).
34. S. Hammerschmidt, H. Kuhn, C. Gessner, H. J. Seyfarth, H. Wirtz, Stretch-induced alveolar type II cell apoptosis: Role of endogenous bradykinin and PI3K-Akt signaling. Am. J. Respir. Cell Mol. Biol. 37, 699-705 (2007).
35. G. S. Call, J. Y. Chung, J. A. Davis, B. D. Price, T. S. Primavera, N. C. Thomson, M. V. Wagner, M. D. Hansen, Zyxin phosphorylation at serine 142 modulates the zyxin head-tail interaction to alter cell-cell adhesion. Biochem. Biophys. Res. Commun. 404, 780-784 (2011).
36. C. J. Ramnanan, D. C. McMullen, A. G. Groom, K. B. Storey, The regulation of AMPK signaling in a natural state of profound metabolic rate depression. Mol. Cell. Biochem. 335, 91-105 (2010).
37. H. Y. Kwan, Y. Huang, X. Yao, Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G. Proc. Natl. Acad. Sci. U.S.A. 101, 2625-2630 (2004).
38. M. Cattaruzza, I. Eberhardt, M. Hecker, Mechanosensitive transcription factors involved in endothelin B receptor expression. J. Biol. Chem. 276, 36999-37003 (2001).
39. W. Du, I. Mills, B. E. Sumpio, Cyclic strain causes heterogeneous induction of transcription factors, AP-1, CRE binding protein and NF-kB, in endothelial cells: Species and vascular bed diversity. J. Biomech. 28, 1485-1491 (1995).
40. A. Koller, Signaling pathways of mechanotransduction in arteriolar endothelium and smooth muscle cells in hypertension. Microcirculation 9, 277-294 (2002).
41. B. Suki, S. Ito, D. Stamenovic, K. R. Lutchen, E. P. Ingenito, Biomechanics of the lung parenchyma: Critical roles of collagen and mechanical forces. J. Appl. Physiol. 98, 1892-1899 (2005).
42. H. J. Novaira, D. S. Ornellas, T. M. Ortiga-Carvalho, X. M. Zhang, J. Souza-Menezes, S. E. Guggino, W. B. Guggino, M. M. Morales, Atrial natriuretic peptide modulates cystic fibrosis transmembrane conductance regulator chloride channel expression in rat proximal colon and human intestinal epithelial cells. J. Endocrinol. 189, 155-165 (2006).
43. J. H. Han, M. Y. Lee, S. C. Myung, The effect of endothelin-1 on the production of interleukin-6 in cultured human detrusor smooth muscle cells, and the effect of interleukin-6 on the contractile response of bladder smooth muscle strips from rats. BJU Int. 104, 707-712 (2009).
44. A. R. Asif, M. Hecker, M. Cattaruzza, Disinhibition of SOD-2 expression to compensate for a genetically determined NO deficit in endothelial cells - Brief report. Arterioscler. Thromb. Vasc. Biol. 29, 1890-1893 (2009).
45. M. Cattaruzza, T. J. Guzik, W. Słodowski, A. Pelvan, J. Becker, M. Halle, A. B. Buchwald, K. M. Channon, M. Hecker, Shear stress insensitivity of endothelial nitric oxide synthase expression as a genetic risk factor for coronary heart disease. Circ. Res. 95, 841-847 (2004).