Mechanisms of the inward remodeling process in resistance vessels: Is the actin cytoskeleton involved?

Microcirculation

Volumn 21, Issue 3, 2014, Pages 219-229

  Castorena Gonzalez, Jorge A ^a,b   Staiculescu, Marius C ^a   Foote, Christopher ^a   Martinez Lemus, Luis A ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c University of Missouri   (United States)

Author keywords

Actin polymerization; Elasticity; Hypertension; Matrix metalloproteinases; Rac; Rho; Stiffness; Strain; Stress; Transglutaminase

Indexed keywords

ACTIN; ACTIN DEPOLYMERIZING FACTOR; ALPHA ACTININ; COFILIN; COLLAGEN; ELASTIN; F ACTIN; G ACTIN; INTEGRIN; MATRIX METALLOPROTEINASE; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RAC PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTERIAL WALL THICKNESS; ARTERIOLE; ARTERY DIAMETER; ARTERY RESISTANCE; ARTICLE; BLOOD FLOW; BLOOD PRESSURE REGULATION; BLOOD VESSEL; BLOOD VESSEL DIAMETER; BLOOD VESSEL WALL; CELL MOTILITY; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ACTIVITY; ESSENTIAL HYPERTENSION; EXTRACELLULAR MATRIX; HUMAN; HYPERTENSION; MICROCIRCULATION; NONHUMAN; PRIORITY JOURNAL; RESISTANCE BLOOD VESSEL; SMOOTH MUSCLE FIBER; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION; YOUNG MODULUS; ANATOMY AND HISTOLOGY; ANIMAL; ARTERY; BIOLOGICAL MODEL; BIOMECHANICS; METABOLISM; MICROVASCULATURE; PHYSIOLOGY; VASCULAR REMODELING; VASCULAR RESISTANCE;

ACTIN CYTOSKELETON; ANIMALS; ARTERIES; BIOMECHANICAL PHENOMENA; ELASTIC MODULUS; GTP-BINDING PROTEINS; HUMANS; MATRIX METALLOPROTEINASES; MICROCIRCULATION; MICROVESSELS; MODELS, CARDIOVASCULAR; MYOCYTES, SMOOTH MUSCLE; RAC GTP-BINDING PROTEINS; RHO GTP-BINDING PROTEINS; TRANSGLUTAMINASES; VASCULAR REMODELING; VASCULAR RESISTANCE; VASOCONSTRICTION;

EID: 84898027418     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12105     Document Type: Article

References (85)

1. Adler KB, Krill J, Alberghini TV, Evans JN. Effect of cytochalasin D on smooth muscle contraction. Cell Motil 3: 545-551, 1983.
2. Andrianantoandro E, Pollard TD. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24: 13-23, 2006.
3. Anfinogenova Y, Wang R, Li QF, Spinelli AM, Tang DD. Abl silencing inhibits CAS-mediated process and constriction in resistance arteries. Circ Res 101: 420-428, 2007.
4. Bakker EN, Buus CL, Spaan JA, Perree J, Ganga A, Rolf TM, Sorop O, Bramsen LH, Mulvany MJ, Vanbavel E. Small artery remodeling depends on tissue-type transglutaminase. Circ Res 96: 119-126, 2005.
5. Bakker EN, Buus CL, VanBavel E, Mulvany MJ. Activation of resistance arteries with endothelin-1: from vasoconstriction to functional adaptation and remodeling. J Vasc Res 41: 174-182, 2004.
6. Bakker EN, Pistea A, Spaan JA, Rolf T, de Vries CJ, van Rooijen N, Candi E, VanBavel E. Flow-dependent remodeling of small arteries in mice deficient for tissue-type transglutaminase: possible compensation by macrophage-derived factor XIII. Circ Res 99: 86-92, 2006.
7. Bakker EN, Pistea A, VanBavel E. Transglutaminases in vascular biology: relevance for vascular remodeling and atherosclerosis. J Vasc Res 45: 271-278, 2008.
8. Baumbach GL, Dobrin PB, Hart MN, Heistad DD. Mechanics of cerebral arterioles in hypertensive rats. Circ Res 62: 56-64, 1988.
9. Baumbach GL, Hajdu MA. Mechanics and composition of cerebral arterioles in renal and spontaneously hypertensive rats. Hypertension 21: 816-826, 1993.
10. Baumbach GL, Walmsley JG, Hart MN. Composition and mechanics of cerebral arterioles in hypertensive rats. Am J Pathol 133: 464-471, 1988.
11. Bendeck MP, Conte M, Zhang M, Nili N, Strauss BH, Farwell SM. Doxycycline modulates smooth muscle cell growth, migration, and matrix remodeling after arterial injury. Am J Pathol 160: 1089-1095, 2002.
12. Blystone SD. Integrating an integrin: a direct route to actin. Biochim Biophys Acta 1692: 47-54, 2004.
13. Briones AM, Gonzalez JM, Somoza B, Giraldo J, Daly CJ, Vila E, Gonzalez MC, McGrath JC, Arribas SM. Role of elastin in spontaneously hypertensive rat small mesenteric artery remodelling. J Physiol 552: 185-195, 2003.
14. Briones AM, Rodriguez-Criado N, Hernanz R, Garcia-Redondo AB, Rodrigues-Diez RR, Alonso MJ, Egido J, Ruiz-Ortega M, Salaices M. Atorvastatin prevents angiotensin II-induced vascular remodeling and oxidative stress. Hypertension 54: 142-149, 2009.
15. Butler B, Gao C, Mersich AT, Blystone SD. Purified integrin adhesion complexes exhibit actin-polymerization activity. Curr Biol 16: 242-251, 2006.
16. Castro MM, Rizzi E, Ceron CS, Guimaraes DA, Rodrigues GJ, Bendhack LM, Gerlach RF, Tanus-Santos JE. Doxycycline ameliorates 2K-1C hypertension-induced vascular dysfunction in rats by attenuating oxidative stress and improving nitric oxide bioavailability. Nitric Oxide 26: 162-168, 2012.
17. Castro MM, Rizzi E, Rodrigues GJ, Ceron CS, Bendhack LM, Gerlach RF, Tanus-Santos JE. Antioxidant treatment reduces matrix metalloproteinase-2-induced vascular changes in renovascular hypertension. Free Radical Biol Med 46: 1298-1307, 2009.
18. Chen NX, O'Neill K, Chen X, Kiattisunthorn K, Gattone VH, Moe SM. Transglutaminase 2 accelerates vascular calcification in chronic kidney disease. Am J Nephrol 37: 191-198, 2013.
19. Chillon JM, Baumbach GL. Effects of chronic nitric oxide synthase inhibition on cerebral arterioles in Wistar-Kyoto rats. J Hypertens 22: 529-534, 2004.
20. Christensen KL, Mulvany MJ. Location of resistance arteries. J Vasc Res 38: 1-12, 2001.
21. Clifford PS, Ella SR, Stupica AJ, Nourian Z, Li M, Martinez-Lemus LA, Dora KA, Yang Y, Davis MJ, Pohl U, Meininger GA, Hill MA. Spatial distribution and mechanical function of elastin in resistance arteries: a role in bearing longitudinal stress. Arterioscler Thromb Vasc Biol 31: 2889-2896, 2011.
22. Corteling RL, Brett SE, Yin H, Zheng X-L, Walsh MP, Welsh DG. The functional consequence of RhoA knockdown by RNA interference in rat cerebral arteries. Am J Physiol Heart Circ Physiol 293: H440-H447, 2007.
23. Coue M, Brenner SL, Spector I, Korn ED. Inhibition of actin polymerization by latrunculin A. FEBS Lett 213: 316-318, 1987.
24. DeMali KA, Barlow CA, Burridge K. Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J Cell Biol 159: 881-891, 2002.
25. Dobrin PB. Mechanical properties of arteries. Physiol Rev 58: 397-460, 1978.
26. Dumont O, Loufrani L, Henrion D. Key role of the NO-pathway and matrix metalloprotease-9 in high blood flow-induced remodeling of rat resistance arteries. Arterioscler Thromb Vasc Biol 27: 317-324, 2007.
27. Fernandez-Patron C, Radomski MW, Davidge ST. Vascular matrix metalloproteinase-2 cleaves big endothelin-1 yielding a novel vasoconstrictor. Circ Res 85: 906-911, 1999.
28. Gunst SJ, Zhang W. Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am J Physiol Cell Physiol 295: C576-C587, 2008.
29. Hall A. Rho GTPases and the actin cytoskeleton. Science 279: 509-514, 1998.
30. Heagerty AM, Aalkjaer C, Bund SJ, Korsgaard N, Mulvany MJ. Small artery structure in hypertension. Dual processes of remodeling and growth. Hypertension 21: 391-397, 1993.
31. Heerkens EH, Izzard AS, Heagerty AM. Integrins, vascular remodeling, and hypertension. Hypertension 49: 1-4, 2007.
32. Heerkens EH, Shaw L, Ryding A, Brooker G, Mullins JJ, Austin C, Ohanian V, Heagerty AM. alphaV integrins are necessary for eutrophic inward remodeling of small arteries in hypertension. Hypertension 47: 281-287, 2006.
33. 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 96: 73-80, 2012.
34. Intengan HD, Deng LY, Li JS, Schiffrin EL. Mechanics and composition of human subcutaneous resistance arteries in essential hypertension. Hypertension 33: 569-574, 1999.
35. Intengan HD, Schiffrin EL. Structure and mechanical properties of resistance arteries in hypertension: role of adhesion molecules and extracellular matrix determinants. Hypertension 36: 312-318, 2000.
36. Johnson JL, Dwivedi A, Somerville M, George SJ, Newby AC. Matrix metalloproteinase (MMP)-3 activates MMP-9 mediated vascular smooth muscle cell migration and neointima formation in mice. Arterioscler Thromb Vasc Biol 31: e35-e44, 2011.
37. Johnson KA, Polewski M, Terkeltaub RA. Transglutaminase 2 is central to induction of the arterial calcification program by smooth muscle cells. Circ Res 102: 529-537, 2008.
38. Kaibuchi K, Kuroda S, Amano M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu Rev Biochem 68: 459-486, 1999.
39. Kohno M, Ohmori K, Nozaki S, Mizushige K, Yasunari K, Kano H, Minami M, Yoshikawa J. Effects of valsartan on angiotensin II-induced migration of human coronary artery smooth muscle cells. Hypertens Res 23: 677-681, 2000.
40. Kozma R, Ahmed S, Best A, Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 15: 1942-1952, 1995.
41. Lagaud G, Gaudreault N, Moore EDW, Breemen Cv, Laher I. Pressure-dependent myogenic constriction of cerebral arteries occurs independently of voltage-dependent activation. Am J Physiol Heart Circ Physiol 283: H2187-H2195, 2002.
42. Liu Y, Li H, Bubolz AH, Zhang DX, Gutterman DD. Endothelial cytoskeletal elements are critical for flow-mediated dilation in human coronary arterioles. Med Biol Eng Compu 46: 469-478, 2008.
43. Loufrani L, Henrion D. Role of the cytoskeleton in flow (shear stress)-induced dilation and remodeling in resistance arteries. Med Biol Eng Compu 46: 451-460, 2008.
44. Martinez-Lemus LA. Persistent agonist-induced vasoconstriction is not required for angiotensin II to mediate inward remodeling of isolated arterioles with myogenic tone. J Vasc Res 45: 211-221, 2008.
45. Martinez-Lemus LA. The dynamic structure of arterioles. Basic Clin Pharmacol Toxicol 110: 5-11, 2012.
46. Martinez-Lemus LA, Hill MA, Bolz SS, Pohl U, Meininger GA. Acute mechanoadaptation of vascular smooth muscle cells in response to continuous arteriolar vasoconstriction: implications for functional remodeling. FASEB J 18: 708-710, 2004.
47. Martinez-Lemus LA, Hill MA, Meininger GA. The plastic nature of the vascular wall: a continuum of remodeling events contributing to control of arteriolar diameter and structure. Physiology (Bethesda) 24: 45-57, 2009.
48. Martinez-Lemus LA, Wu X, Wilson E, Hill MA, Davis GE, Davis MJ, Meininger GA. Integrins as unique receptors for vascular control. J Vasc Res 40: 211-233, 2003.
49. Martinez-Lemus LA, Zhao G, Galinanes EL, Boone M. Inward remodeling of resistance arteries requires reactive oxygen species-dependent activation of matrix metalloproteinases. Am J Physiol Heart Circ Physiol 300: H2005-H2015, 2011.
50. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3: e442, 2006.
51. Mathiassen ON, Buus NH, Larsen ML, Mulvany MJ, Christensen KL. Small artery structure adapts to vasodilatation rather than to blood pressure during antihypertensive treatment. J Hypertens 25: 1027-1034, 2007.
52. Mathiassen ON, Buus NH, Sihm I, Thybo NK, Morn B, Schroeder AP, Thygesen K, Aalkjaer C, Lederballe O, Mulvany MJ, Christensen KL. Small artery structure is an independent predictor of cardiovascular events in essential hypertension. J Hypertens 25: 1021-1026, 2007.
53. Mehta D, Gunst SJ. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol 519(Pt 3): 829-840, 1999.
54. Moriyama K, Yahara I. Two activities of cofilin, severing and accelerating directional depolymerization of actin filaments, are affected differentially by mutations around the actin-binding helix. EMBO J 18: 6752-6761, 1999.
55. Nagareddy PR, Chow FL, Hao L, Wang X, Nishimura T, MacLeod KM, McNeill JH, Fernandez-Patron C. Maintenance of adrenergic vascular tone by MMP transactivation of the EGFR requires PI3K and mitochondrial ATP synthesis. Cardiovasc Res 84: 368-377, 2009.
56. Nobes CD, Hall A. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81: 53-62, 1995.
57. Nobes CD, Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144: 1235-1244, 1999.
58. Nurminskaya MV, Belkin AM. Cellular functions of tissue transglutaminase. Int Rev Cell Mol Biol 294: 1-97, 2012.
59. Obara K, Yabu H. Effect of cytochalasin B on intestinal smooth muscle cells. Eur J Pharmacol 255: 139-147, 1994.
60. Ohanian V, Gatfield K, Ohanian J. Role of the actin cytoskeleton in G-protein-coupled receptor activation of PYK2 and paxillin in vascular smooth muscle. Hypertension 46: 93-99, 2005.
61. Ohashi K, Nagata K, Maekawa M, Ishizaki T, Narumiya S, Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem 275: 3577-3582, 2000.
62. Rembold CM, Tejani AD, Ripley ML, Han S. Paxillin phosphorylation, actin polymerization, noise temperature, and the sustained phase of swine carotid artery contraction. Am J Physiol Cell Physiol 293: C993-C1002, 2007.
63. Rhodin JAG. Architecture of the vessel wall. In: Compr Physiol 2011, Supplement 7: Handbook of Physiology, The Cardiovascular System, Vascular Smooth Muscle, edited by Bohr DF, Somlyo AP, Sparks HV. Washington, DC: American Physiological Society, 1980, pp. 1-31.
64. Rhodin JAG. The ultrastructure of mammalian arterioles and precapillary sphincters. J Ultrasruct Res 18: 181-223, 1967.
65. Ridley AJ. Rho family proteins and regulation of the actin cytoskeleton. Prog Mol Subcell Biol 22: 1-22, 1999.
66. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399, 1992.
67. Rizzoni D, Porteri E, Boari GE, De Ciuceis C, Sleiman I, Muiesan ML, Castellano M, Miclini M, Agabiti-Rosei E. Prognostic significance of small-artery structure in hypertension. Circulation 108: 2230-2235, 2003.
68. Saito SY, Hori M, Ozaki H, Karaki H. Cytochalasin D inhibits smooth muscle contraction by directly inhibiting contractile apparatus. J Smooth Muscle Res 32: 51-60, 1996.
69. Schiffrin EL. Remodeling of resistance arteries in essential hypertension and effects of antihypertensive treatment. Am J Hypertens 17: 1192-1200, 2004.
70. Schnittler HJ, Schneider SW, Raifer H, Luo F, Dieterich P, Just I, Aktories K. Role of actin filaments in endothelial cell-cell adhesion and membrane stability under fluid shear stress. Pflugers Arch 442: 675-687, 2001.
71. Schubert R, Kalentchuk VU, Krien U. Rho kinase inhibition partly weakens myogenic reactivity in rat small arteries by changing calcium sensitivity. Am J Physiol Heart Circ Physiol 283: H2288-H2295, 2002.
72. Sept D, McCammon JA. Thermodynamics and kinetics of actin filament nucleation. Biophys J 81: 667-674, 2001.
73. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
74. Staiculescu MC, Galinanes EL, Zhao G, Ulloa U, Jin M, Beig MI, Meininger GA, Martinez-Lemus LA. Prolonged vasoconstriction of resistance arteries involves vascular smooth muscle actin polymerization leading to inward remodelling. Cardiovasc Res 98: 428-436, 2013.
75. Su Y, Edwards-Bennett S, Bubb MR, Block ER. Regulation of endothelial nitric oxide synthase by the actin cytoskeleton. Am J Physiol Cell Physiol 284: C1542-C1549, 2003.
76. Su Y, Zharikov SI, Block ER. Microtubule-active agents modify nitric oxide production in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 282: L1183-L1189, 2002.
77. Tseng S, Kim R, Kim T, Morgan KG, Hai CM. F-actin disruption attenuates agonist-induced [Ca2+], myosin phosphorylation, and force in smooth muscle. Am J Physiol 272: C1960-C1967, 1997.
78. Ueki Y, Uda Y, Sakamoto N, Sato M. Measurements of strain on single stress fibers in living endothelial cells induced by fluid shear stress. Biochem Biophys Res Commun 395: 441-446, 2010.
79. Van Den Akker J, Schoorl MJC, Bakker ENTP, Vanbavel E. Small artery remodeling: current concepts and questions. J Vasc Res 47: 183-202, 2010.
80. van den Akker J, VanBavel E, vanGeel R, Matlung HL, Guvenc Tuna B, Janssen GM, vanVeelen PA, Boelens WC, De Mey JG, Bakker EN. The redox state of transglutaminase 2 controls arterial remodeling. PLoS One 6: e23067, 2011.
81. VanBavel E, van der Meulen E, Spaan J. Role of Rho-associated protein kinase in tone and calcium sensitivity of cannulated rat mesenteric small arteries. Exp Physiol 86: 585-592, 2001.
82. Wang X, Chow FL, Oka T, Hao L, Lopez-Campistrous A, Kelly S, Cooper S, Odenbach J, Finegan BA, Schulz R, Kassiri Z, Lopaschuk GD, Fernandez-Patron C. Matrix metalloproteinase-7 and ADAM-12 (a disintegrin and metalloproteinase-12) define a signaling axis in agonist-induced hypertension and cardiac hypertrophy. Circulation 119: 2480-2489, 2009.
83. Yamin R, Morgan KG. Deciphering actin cytoskeletal function in the contractile vascular smooth muscle cell. J Physiol 590: 4145-4154, 2012.
84. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393: 809-812, 1998.
85. Zhou MS, Jaimes EA, Raij L. Vascular but not cardiac remodeling is associated with superoxide production in angiotensin II hypertension. J Hypertens 23: 1737-1743, 2005.