|
|
|
|
|
|
|
|
|||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | |||||
Journal of Cell Science, Vol 112, Issue 4 435-445, Copyright © 1999 by Company of Biologists
JOURNAL ARTICLES |
PL Jones, FS Jones, B Zhou and M Rabinovitch
Division of Cardiovascular Research, Research Institute, The Hospital for Sick Children, Department of Pediatrics, University of Toronto, Ontario, Canada M5G 1X8. mr@sickkids.on.ca
Tenascin-C is an extracellular matrix glycoprotein, the expression of which is upregulated in remodeling arteries. In previous studies we showed that the presence of tenascin-C alters vascular smooth muscle cell shape and amplifies their proliferative response by promoting growth factor receptor clustering and phosphorylation. Moreover, we demonstrated that denatured type I collagen induces smooth muscle cell tenascin-C protein production via beta3 integrins. In the present study, we examine the pathway by which beta3 integrins stimulate expression of tenascin-C, and define a promoter sequence that is critical for its induction. On native collagen, A10 smooth muscle cells adopt a stellate morphology and produce low levels of tenascin-C mRNA and protein, whereas on denatured collagen they spread extensively and produce high levels of tenascin-C mRNA and protein, which is incorporated into an elaborate extracellular matrix. Increased tenascin-C synthesis on denatured collagen is associated with elevated protein tyrosine phosphorylation, including activation of extracellular signal-regulated kinases 1 and 2 (ERK1 and ERK2). beta3 integrin function-blocking antibodies attenuate ERK1/2 activation and tenascin-C protein synthesis. Consistent with these findings, treatment with the specific MEK inhibitor, PD 98059, results in suppression of tenascin-C protein synthesis. To investigate whether beta3 integrin-dependent activation of ERK1/2 regulates the tenascin-C promoter, we transfected A10 cells with a full-length (approx. 4 kb) mouse tenascin-C gene promoter-chloramphenicol acetyltransferse reporter construct and showed that, relative to native collagen, its activity is increased on denatured collagen. Next, to identify regions of the promoter involved, we examined a series of tenascin-C promoter constructs with 5' deletions and showed that denatured collagen-dependent promoter activity was retained by a 122-base pair element, located -43 to -165 bp upstream of the RNA start site. Activation of this element was suppressed either by blocking beta3 integrins, or by preventing ERK1/2 activation. These observations demonstrate that smooth muscle cell binding to beta3 integrins activates the mitogen activated protein kinase pathway, which is required for the induction of tenascin-C gene expression via a potential extracellular matrix response element in the tenascin-C gene promoter. Our data suggest a mechanism by which remodeling of type I collagen modulates tenascin-C gene expression via a beta3 integrin-mediated signaling pathway, and as such represents a paradigm for vascular development and disease whereby smooth muscle cells respond to perturbations in extracellular matrix composition by altering their phenotype and patterns of gene expression.
This article has been cited by other articles:
|
|
 |
|
  A. Della Corte, C. Quarto, C. Bancone, C. Castaldo, F. Di Meglio, D. Nurzynska, L. S. De Santo, M. De Feo, M. Scardone, S. Montagnani, et al. Spatiotemporal patterns of smooth muscle cell changes in ascending aortic dilatation with bicuspid and tricuspid aortic valve stenosis: Focus on cell matrix signaling J. Thorac. Cardiovasc. Surg., January 1, 2008; 135(1): 8 - 18. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Y. Sung, H. Guan, A. Czibula, A. R. King, K. Eder, E. Heath, S. K. Suvarna, S. K. Dower, A. G. Wilson, S. E. Francis, et al. Human Tribbles-1 Controls Proliferation and Chemotaxis of Smooth Muscle Cells via MAPK Signaling Pathways J. Biol. Chem., June 22, 2007; 282(25): 18379 - 18387. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. L. Jones Move On!: Smooth Muscle Cell Motility Paired Down Circ. Res., March 30, 2007; 100(6): 757 - 760. [Full Text] [PDF]
|
|
|
|
|
|
A. Umesh, M. A. Thompson, E. N. Chini, K.-P. Yip, and J. S. K. Sham Integrin Ligands Mobilize Ca2+ from Ryanodine Receptor-gated Stores and Lysosome-related Acidic Organelles in Pulmonary Arterial Smooth Muscle Cells J. Biol. Chem., November 10, 2006; 281(45): 34312 - 34323. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Chapados, K. Abe, K. Ihida-Stansbury, D. McKean, A. T. Gates, M. Kern, S. Merklinger, J. Elliott, A. Plant, H. Shimokawa, et al. ROCK Controls Matrix Synthesis in Vascular Smooth Muscle Cells: Coupling Vasoconstriction to Vascular Remodeling Circ. Res., October 13, 2006; 99(8): 837 - 844. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Ihida-Stansbury, D. M. McKean, K. B. Lane, J. E. Loyd, L. A. Wheeler, N. W. Morrell, and P. L. Jones Tenascin-C is induced by mutated BMP type II receptors in familial forms of pulmonary arterial hypertension Am J Physiol Lung Cell Mol Physiol, October 1, 2006; 291(4): L694 - L702. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. J. Aitken, G. Block, A. Lorenzo, D. Herz, N. Sabha, O. Dessouki, F. Fung, M. Szybowska, L. Craig, and D. J. Bagli Mechanotransduction of Extracellular Signal-Regulated Kinases 1 and 2 Mitogen-Activated Protein Kinase Activity in Smooth Muscle Is Dependent on the Extracellular Matrix and Regulated by Matrix Metalloproteinases Am. J. Pathol., August 1, 2006; 169(2): 459 - 470. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. von Wnuck Lipinski, P. Keul, N. Ferri, S. Lucke, G. Heusch, J. W. Fischer, and B. Levkau Integrin-Mediated Transcriptional Activation of Inhibitor of Apoptosis Proteins Protects Smooth Muscle Cells Against Apoptosis Induced by Degraded Collagen Circ. Res., June 23, 2006; 98(12): 1490 - 1497. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. von Wnuck Lipinski, P. Keul, S. Lucke, G. Heusch, J. Wohlschlaeger, H. A. Baba, and B. Levkau Degraded collagen induces calpain-mediated apoptosis and destruction of the X-chromosome-linked inhibitor of apoptosis (xIAP) in human vascular smooth muscle cells Cardiovasc Res, February 15, 2006; 69(3): 697 - 705. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L. Merklinger, P. L. Jones, E. C. Martinez, and M. Rabinovitch Epidermal Growth Factor Receptor Blockade Mediates Smooth Muscle Cell Apoptosis and Improves Survival in Rats With Pulmonary Hypertension Circulation, July 19, 2005; 112(3): 423 - 431. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Greenway, R. J. van Suylen, G. Du Marchie Sarvaas, E. Kwan, N. Ambartsumian, E. Lukanidin, and M. Rabinovitch S100A4/Mts1 Produces Murine Pulmonary Artery Changes Resembling Plexogenic Arteriopathy and Is Increased in Human Plexogenic Arteriopathy Am. J. Pathol., January 1, 2004; 164(1): 253 - 262. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Manes, D.-Q. Zheng, S. Tognin, A. S. Woodard, P. C. Marchisio, and L. R. Languino {alpha}v{beta}3 integrin expression up-regulates cdc2, which modulates cell migration J. Cell Biol., May 26, 2003; 161(4): 817 - 826. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. M. McKean, L. Sisbarro, D. Ilic, N. Kaplan-Alburquerque, R. Nemenoff, M. Weiser-Evans, M. J. Kern, and P. L. Jones FAK induces expression of Prx1 to promote tenascin-C-dependent fibroblast migration J. Cell Biol., April 28, 2003; 161(2): 393 - 402. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Castellon, S. Caballero, H. K. Hamdi, S. R. Atilano, A. M. Aoki, R. W. Tarnuzzer, M. C. Kenney, M. B. Grant, and A. V. Ljubimov Effects of Tenascin-C on Normal and Diabetic Retinal Endothelial Cells in Culture Invest. Ophthalmol. Vis. Sci., August 1, 2002; 43(8): 2758 - 2766. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Wang and E. G. Lakatta Altered Regulation of Matrix Metalloproteinase-2 in Aortic Remodeling During Aging Hypertension, April 1, 2002; 39(4): 865 - 873. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. Jones, R. Chapados, H. S. Baldwin, G. W. Raff, E. V. Vitvitsky, T. L. Spray, and J. W. Gaynor Altered hemodynamics controls matrix metalloproteinase activity and tenascin-C expression in neonatal pig lung Am J Physiol Lung Cell Mol Physiol, January 1, 2002; 282(1): L26 - L35. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Jian, P. L. Jones, Q. Li, E. R. Mohler III, F. J. Schoen, and R. J. Levy Matrix Metalloproteinase-2 Is Associated with Tenascin-C in Calcific Aortic Stenosis Am. J. Pathol., July 1, 2001; 159(1): 321 - 327. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Rescan, A. Coutant, H. Talarmin, N. Theret, D. Glaise, C. Guguen-Guillouzo, and G. Baffet Mechanism in the Sequential Control of Cell Morphology and S Phase Entry by Epidermal Growth Factor Involves Distinct MEK/ERK Activations Mol. Biol. Cell, March 1, 2001; 12(3): 725 - 738. [Abstract] [Full Text]
|
|
|
|
|
|
N. Vyavahare, P. L. Jones, S. Tallapragada, and R. J. Levy Inhibition of Matrix Metalloproteinase Activity Attenuates Tenascin-C Production and Calcification of Implanted Purified Elastin in Rats Am. J. Pathol., September 1, 2000; 157(3): 885 - 893. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Babal, S. M. Manuel, J. W. Olson, and M. N. Gillespie Cellular disposition of transported polyamines in hypoxic rat lung and pulmonary arteries Am J Physiol Lung Cell Mol Physiol, March 1, 2000; 278(3): L610 - L617. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E Stringa, V Knauper, G Murphy, and J Gavrilovic Collagen degradation and platelet-derived growth factor stimulate the migration of vascular smooth muscle cells J. Cell Sci., January 6, 2000; 113(11): 2055 - 2064. [Abstract] [PDF]
|
|
|
|
|
|
K. N. Cowan, P. L. Jones, and M. Rabinovitch Regression of Hypertrophied Rat Pulmonary Arteries in Organ Culture Is Associated With Suppression of Proteolytic Activity, Inhibition of Tenascin-C, and Smooth Muscle Cell Apoptosis Circ. Res., May 28, 1999; 84(10): 1223 - 1233. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. S. Jones, R. Meech, D. B. Edelman, R. J. Oakey, and P. L. Jones Prx1 Controls Vascular Smooth Muscle Cell Proliferation and Tenascin-C Expression and Is Upregulated With Prx2 in Pulmonary Vascular Disease Circ. Res., July 20, 2001; 89(2): 131 - 138. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. W. Galt, S. Lindemann, D. Medd, L. L. Allen, L. W. Kraiss, E. S. Harris, S. M. Prescott, T. M. McIntyre, A. S. Weyrich, and G. A. Zimmerman Differential Regulation of Matrix Metalloproteinase-9 by Monocytes Adherent to Collagen and Platelets Circ. Res., September 14, 2001; 89(6): 509 - 516. [Abstract] [Full Text] [PDF]
|
|
