Vascular smooth muscle cell stiffness and adhesion to collagen I modified by vasoactive agonists

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Hong, Zhongkui ^a,c   Reeves, Kimberley J ^a,d   Sun, Zhe ^a,c   Li, Zhaohui ^a   Brown, Nicola J ^b   Meininger, Gerald A ^a,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF MISSOURI   (United States)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ANGIOTENSIN II; COLLAGEN TYPE 1; INTEGRIN; NITRIC OXIDE DONOR;

ANIMAL CELL; ARTERIOLE; ARTICLE; CELL ADHESION; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; CREMASTER MUSCLE; MALE; NONHUMAN; RAT; RIGIDITY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTILITY; SMOOTH MUSCLE FIBER; SMOOTH MUSCLE RELAXATION; VASCULAR SMOOTH MUSCLE; YOUNG MODULUS; ANIMAL; ATOMIC FORCE MICROSCOPY; CYTOLOGY; DRUG EFFECTS; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS;

ANGIOTENSIN II; ANIMALS; CELL ADHESION; COLLAGEN TYPE I; MALE; MICROSCOPY, ATOMIC FORCE; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE DONORS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84924145277     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119533     Document Type: Article

References (40)

1. Balasubramanian L, Ahmed A, Lo CM, Sham JS, Yip KP. Integrin-mediated mechanotransduction in renal vascular smooth muscle cells: activation of calcium sparks. Am J Physiol Regul Integr Comp Physiol. 2007; 293: R1586-1594. PMID: 17699564
2. Delon I, Brown NH. Integrins and the actin cytoskeleton. Curr Opin Cell Biol. 2007; 19: 43-50. PMID: 17184985
3. Goldschmidt ME, McLeod KJ, Taylor WR. Integrin-mediated mechanotransduction in vascular smooth muscle cells: frequency and force response characteristics. Circ Res. 2001; 88: 674-680. PMID: 11304489
4. Hong Z, Sun Z, Li Z, Mesquitta WT, Trzeciakowski JP, Meininger GA. Coordination of fibronectin adhesion with contraction and relaxation in microvascular smooth muscle. Cardiovasc Res. 2012; 96: 73-80. doi: 10.1093/cvr/cvs239 PMID: 22802110
5. Wilson E, Sudhir K, Ives HE. Mechanical strain of rat vascular smooth muscle cells is sensed by specific extracellular matrix/integrin interactions. J Clin Invest. 1995; 96: 2364-2372. PMID: 7593624
6. Liddington RC, Ginsberg MH. Integrin activation takes shape. J Cell Biol. 2002; 158: 833-839. PMID: 12213832
7. Calderwood DA. Integrin activation. J Cell Sci. 2004; 117: 657-666. PMID: 14754902
8. Dean DC, Iademarco MF, Rosen GD, Sheppard AM. The Integrin α4β1 and Its Counter Receptor VCAM-1 in Development and Immune Function. American Review of Respiratory Disease. 1993; 148: S43-S46. PMID: 7504895
9. Takada Y, Hemler ME. The primary structure of the VLA-2/collagen receptor alpha 2 subunit (platelet GPIa): homology to other integrins and the presence of a possible collagen-binding domain. J Cell Biol. 1989; 109: 397-407. PMID: 2545729
10. Briesewitz R, Epstein MR, Marcantonio EE. Expression of native and truncated forms of the human integrin alpha 1 subunit. J Biol Chem. 1993; 268: 2989-2996. PMID: 8428973
11. Camper L, Hellman U, Lundgren-Akerlund E. Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem. 1998; 273: 20383-20389. PMID: 9685391
12. Velling T, Kusche-Gullberg M, Sejersen T, Gullberg D. cDNA cloning and chromosomal localization of human alpha(11) integrin. A collagen-binding, I domain-containing, beta(1)-associated integrin alphachain present in muscle tissues. J Biol Chem. 1999; 274: 25735-25742. PMID: 10464311
13. Hillis GS, Mlynski RA, Simpson JG, MacLeod AM. The expression of beta 1 integrins in human coronary artery. Basic Res Cardiol. 1998; 93: 295-302. PMID: 9782372
14. Prockop JD. Collagens: Molecular Biology, Diseases, and Potentials for Therapy. Annual Review of Biochemistry. 1995; 64: 403-434. PMID: 7574488
15. Harburger DS, Calderwood DA. Integrin signalling at a glance. J Cell Sci. 2009; 122: 159-163. doi: 10.1242/jcs.018093 PMID: 19118207
16. Martinez-Lemus LA, Crow T, Davis MJ, Meininger GA. alphavbeta3- and alpha5beta1-integrin blockade inhibits myogenic constriction of skeletal muscle resistance arterioles. Am J Physiol Heart Circ Physiol. 2005; 289: H322-329. PMID: 15722407
17. Heerkens EH, Shaw L, Ryding A, Brooker G, Mullins JJ, Austin C, et al. alphaV integrins are necessary for eutrophic inward remodeling of small arteries in hypertension. Hypertension. 2006; 47: 281-287. PMID: 16380536
18. Zhu Y, Qiu H, Trzeciakowski JP, Sun Z, Li Z, Hong Z, et al. Temporal analysis of vascular smooth muscle cell elasticity and adhesion reveals oscillation waveforms that differ with aging. Aging Cell. 2012; 11: 741-750. doi: 10.1111/j.1474-9726.2012.00840.x PMID: 22639979
19. Sehgel NL, Zhu Y, Sun Z, Trzeciakowski JP, Hong Z, Hunter WC, et al. Increased vascular smooth muscle cell stiffness: a novel mechanism for aortic stiffness in hypertension. Am J Physiol Heart Circ Physiol. 2013; 305: H1281-1287. doi: 10.1152/ajpheart.00232.2013 PMID: 23709594
20. Sun Z, Martinez-Lemus LA, Hill MA, Meininger GA. Extracellular matrix-specific focal adhesions in vascular smooth muscle produce mechanically active adhesion sites. Am J Physiol Cell Physiol. 2008; 295: C268-278. doi: 10.1152/ajpcell.00516.2007 PMID: 18495809
21. Lehenkari PP, Horton MA. Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy. Biochem Biophys Res Commun. 1999; 259: 645-650. PMID: 10364472
22. Qiu H, Zhu Y, Sun Z, Trzeciakowski JP, Gansner M, Depre C, et al. Short communication: vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging. Circ Res. 2010; 107: 615-619. doi: 10.1161/CIRCRESAHA.110.221846 PMID: 20634486
23. Sun Z, Martinez-Lemus LA, Trache A, Trzeciakowski JP, Davis GE, Pohl U, et al. Mechanical properties of the interaction between fibronectin and alpha5beta1-integrin on vascular smooth muscle cells studied using atomic force microscopy. Am J Physiol Heart Circ Physiol. 2005; 289: H2526-2535. PMID: 16100245
24. Butt H-J, Jaschke M. Calculation of thermal noise in atomic forcemicroscopy. Nanotechnology. 1995; 6 7.
25. Hutter JL, Bechhoefer J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 1993; 64: 6.
26. Costa KD. Single-cell elastography: probing for disease with the atomic force microscope. Dis Markers. 2003; 19: 139-154. PMID: 15096710
27. Li QS, Lee GY, Ong CN, Lim CT. AFM indentation study of breast cancer cells. Biochem Biophys Res Commun. 2008; 374: 609-613. doi: 10.1016/j.bbrc.2008.07.078 PMID: 18656442
28. Hong Z, Sun Z, Li M, Li Z, Bunyak F, Ersoy I, et al. Vasoactive agonists exert dynamic and coordinated effects on vascular smooth muscle cell elasticity, cytoskeletal remodelling and adhesion. J Physiol. 2014; 592: 1249-1266. doi: 10.1113/jphysiol.2013.264929 PMID: 24445320
29. Kuznetsova TG, Starodubtseva MN, Yegorenkov NI, Chizhik SA, Zhdanov RI. Atomic force microscopy probing of cell elasticity. Micron. 2007; 38: 824-833. PMID: 17709250
30. Vargas-Pinto R, Gong H, Vahabikashi A, Johnson M. The Effect of the Endothelial Cell Cortex on Atomic Force Microscopy Measurements. Biophysical Journal. 2013; 105: 300-309. doi: 10.1016/j.bpj.2013.05.034 PMID: 23870251
31. Choi CK, Vicente-Manzanares M, Zareno J, Whitmore LA, Mogilner A, Horwitz AR. Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat Cell Biol. 2008; 10: 1039-1050. doi: 10.1038/ncb1763 PMID: 19160484
32. Kucik DF, O'Toole TE, Zheleznyak A, Busettini DK, Brown EJ. Activation-enhanced alpha(IIb)beta(3)- integrin-cytoskeleton interactions outside of focal contacts require the alpha-subunit. Mol Biol Cell. 2001; 12: 1509-1518. PMID: 11359939
33. Min J, Reznichenko M, Poythress RH, Gallant CM, Vetterkind S, Li Y, et al. Src modulates contractile vascular smooth muscle function via regulation of focal adhesions. J Cell Physiol. 2012.
34. Zhang W, Gunst SJ. Interactions of airway smooth muscle cells with their tissue matrix: implications for contraction. Proc Am Thorac Soc. 2008; 5: 32-39. PMID: 18094082
35. Zhang W, Wu Y, Wu C, Gunst SJ. Integrin-linked kinase regulates N-WASp-mediated actin polymerization and tension development in tracheal smooth muscle. J Biol Chem. 2007; 282: 34568-34580. PMID: 17897939
36. Zhang W, Wu Y, Du L, Tang DD, Gunst SJ. Activation of the Arp2/3 complex by N-WASp is required for actin polymerization and contraction in smooth muscle. Am J Physiol Cell Physiol. 2005; 288: C1145-1160. PMID: 15625304
37. Kim HR, Gallant C, Leavis PC, Gunst SJ, Morgan KG. Cytoskeletal remodeling in differentiated vascular smooth muscle is actin isoform dependent and stimulus dependent. Am J Physiol Cell Physiol. 2008; 295: C768-778. doi: 10.1152/ajpcell.00174.2008 PMID: 18596213
38. Poythress RH, Gallant C, Vetterkind S, Morgan KG. Vasoconstrictor-induced endocytic recycling regulates focal adhesion protein localization and function in vascular smooth muscle. Am J Physiol Cell Physiol. 2013; 305: C215-227. doi: 10.1152/ajpcell.00103.2013 PMID: 23703522
39. Gangopadhyay SS, Takizawa N, Gallant C, Barber AL, Je HD, Smith TC, et al. Smooth muscle archvillin: a novel regulator of signaling and contractility in vascular smooth muscle. J Cell Sci. 2004; 117: 5043-5057. PMID: 15383618
40. Moreno-Dominguez A, El-Yazbi AF, Zhu H-L, Colinas O, Zhong XZ, Walsh EJ, et al. Cytoskeletal Reorganization Evoked by Rho-associated kinase- and Protein Kinase C-Catalyzed Phosphorylation of Cofilin and Heat Shock Protein 27, Respectively, Contributes to Myogenic Constriction of Rat Cerebral Arteries. Journal of Biological Chemistry. 2014.