Excessive adventitial remodeling leads to early aortic maladaptation in angiotensin-induced hypertension

Hypertension

Volumn 67, Issue 5, 2016, Pages 890-896

  Bersi, Matthew R ^a   Bellini, Chiara ^a   Wu, Jing ^b   Montaniel, Kim R C ^b   Harrison, David G ^b   Humphrey, Jay D ^a,c  

^a Yale University   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

arterial stiffness; collagen; elastic energy; hypertension; wall stress

Indexed keywords

ANGIOTENSIN II;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL STIFFNESS; ARTERIAL WALL THICKNESS; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL WALL; CLINICAL ASSESSMENT; CONTROLLED STUDY; HYPERTENSION; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PULSE WAVE; THORACIC AORTA; VASCULAR REMODELING; WALL STRESS; ADVENTITIA; ANALYSIS OF VARIANCE; ANIMAL; AORTA; C57BL MOUSE; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RANDOMIZATION;

ADVENTITIA; ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; AORTA; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; HYPERTENSION; MALE; MICE; MICE, INBRED C57BL; RANDOM ALLOCATION; STRESS, PHYSIOLOGICAL; VASCULAR REMODELING; VASCULAR STIFFNESS;

EID: 84961392963     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.06262     Document Type: Article

References (47)

1. O'Rourke MF, Hashimoto J, Mechanical factors in arterial aging: a clinical perspective. J Am Coll Cardiol 2007 50 1 13. doi: 10.1016/j.jacc.2006.12.050
2. Lakatta EG, Wang M, Najjar SS, Arterial aging and subclinical arterial disease are fundamentally intertwined at macroscopic and molecular levels. Med Clin North Am 2009 93 583 604, Table of Contents. doi: 10.1016/j.mcna.2009.02.008
3. Safar ME, Arterial aging-hemodynamic changes and therapeutic options. Nat Rev Cardiol 2010 7 442 449. doi: 10.1038/nrcardio.2010.96
4. Avolio AP, Van Bortel LM, Boutouyrie P, Cockcroft JR, McEniery CM, Protogerou AD, Roman MJ, Safar ME, Segers P, Smulyan H, Role of pulse pressure amplification in arterial hypertension: experts' opinion and review of the data. Hypertension 2009 54 375 383. doi: 10.1161/HYPERTENSIONAHA.109.134379
5. Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, Pannier B, Vlachopoulos C, Wilkinson I, Struijker-Boudier H, European Network for Non-invasive Investigation of Large Arteries Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 2006 27 2588 2605. doi: 10.1093/eurheartj/ehl254
6. Wolinsky H, Comparison of medial growth of human thoracic and abdominal aortas. Circ Res 1970 27 531 538
7. Xu C, Zarins CK, Bassiouny HS, Briggs WH, Reardon C, Glagov S, Differential transmural distribution of gene expression for collagen types I and III proximal to aortic coarctation in the rabbit. J Vasc Res 2000 37 170 182. 25728
8. Hayashi K, Naiki T, Adaptation and remodeling of vascular wall; biomechanical response to hypertension. J Mech Behav Biomed Mater 2009 2 3 19. doi: 10.1016/j.jmbbm.2008.05.002
9. Vogt M, Kühn A, Baumgartner D, Baumgartner C, Busch R, Kostolny M, Hess J, Impaired elastic properties of the ascending aorta in newborns before and early after successful coarctation repair: proof of a systemic vascular disease of the prestenotic arteries? Circulation 2005 111 3269 3273. doi: 10.1161/CIRCULATIONAHA.104.529792
10. McMaster WG, Kirabo A, Madhur MS, Harrison DG, Inflammation, immunity, and hypertensive end-organ damage. Circ Res 2015 116 1022 1033. doi: 10.1161/CIRCRESAHA.116.303697
11. McEniery CM, Wilkinson IB, Large artery stiffness and inflammation. J Hum Hypertens 2005 19 507 509. doi: 10.1038/sj.jhh.1001814
12. Wu J, Thabet SR, Kirabo A, Trott DW, Saleh MA, Xiao L, Madhur MS, Chen W, Harrison DG, Inflammation and mechanical stretch promote aortic stiffening in hypertension through activation of p38 mitogen-Activated protein kinase. Circ Res 2014 114 616 625. doi: 10.1161/CIRCRESAHA.114.302157
13. Bellini C, Ferruzzi J, Roccabianca S, Di Martino ES, Humphrey JD, A microstructurally motivated model of arterial wall mechanics with mechanobiological implications. Ann Biomed Eng 2014 42 488 502. doi: 10.1007/s10439-013-0928-x
14. Ferruzzi J, Bersi MR, Uman S, Yanagisawa H, Humphrey JD, Decreased elastic energy storage, not increased material stiffness, characterizes central artery dysfunction in fibulin-5 deficiency independent of sex. J Biomech Eng 2015 137. doi: 10.1115/1.4029431
15. Shadwick RE, Mechanical design in arteries. J Exp Biol 1999 202 pt 23 3305 3313
16. Bersi MR, Ferruzzi J, Eberth JF, Gleason RL Jr, Humphrey JD, Consistent biomechanical phenotyping of common carotid arteries from seven genetic, pharmacological, and surgical mouse models. Ann Biomed Eng 2014 42 1207 1223. doi: 10.1007/s10439-014-0988-6
17. Wagenseil JE, Mecham RP, Vascular extracellular matrix and arterial mechanics. Physiol Rev 2009 89 957 989. doi: 10.1152/physrev.00041.2008
18. Dajnowiec D, Sabatini PJ, Van Rossum TC, Lam JT, Zhang M, Kapus A, Langille BL, Force-induced polarized mitosis of endothelial and smooth muscle cells in arterial remodeling. Hypertension 2007 50 255 260. doi: 10.1161/HYPERTENSIONAHA.107.089730
19. Cyron CJ, Humphrey JD, Preferred fiber orientations in healthy arteries and veins understood from netting analysis. Math Mech Solids 2014 1 17
20. Demiray H, Wave propagation through a viscous fluid contained in a prestressed thin elastic tube. Int J Eng Sci 1992 30 1607 1620
21. Jackson ZS, Gotlieb AI, Langille BL, Wall tissue remodeling regulates longitudinal tension in arteries. Circ Res 2002 90 918 925
22. Humphrey JD, Eberth JF, Dye WW, Gleason RL, Fundamental role of axial stress in compensatory adaptations by arteries. J Biomech 2009 42 1 8. doi: 10.1016/j.jbiomech.2008.11.011
23. Humphrey JD, Cardiovascular Solid Mechanics: Cells, Tissues and Organs 2002 New York Springer
24. Wolinsky H, Glagov S, A lamellar unit of aortic medial structure and function in mammals. Circ Res 1967 20 99 111
25. Humphrey JD, Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress. Hypertension 2008 52 195 200. doi: 10.1161/HYPERTENSIONAHA.107.103440
26. Dajnowiec D, Langille BL, Arterial adaptations to chronic changes in haemodynamic function: coupling vasomotor tone to structural remodelling. Clin Sci (Lond) 2007 113 15 23. doi: 10.1042/CS20060337
27. Wolinsky H, Long-Term effects of hypertension on the rat aortic wall and their relation to concurrent aging changes. Morphological and chemical studies. Circ Res 1972 30 301 309
28. Eberth JF, Popovic N, Gresham VC, Wilson E, Humphrey JD, Time course of carotid artery growth and remodeling in response to altered pulsatility. Am J Physiol Heart Circ Physiol 2010 299 H1875 H1883. doi: 10.1152/ajpheart.00872.2009
29. Kuang SQ, Geng L, Prakash SK, Cao JM, Guo S, Villamizar C, Kwartler CS, Peters AM, Brasier AR, Milewicz DM, Aortic remodeling after transverse aortic constriction in mice is attenuated with AT1 receptor blockade. Arterioscler Thromb Vasc Biol 2013 33 2172 2179. doi: 10.1161/ATVBAHA.113.301624
30. Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB, The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 2012 95 194 204. doi: 10.1093/cvr/cvs135
31. Goel SA, Guo LW, Shi XD, Kundi R, Sovinski G, Seedial S, Liu B, Kent KC, Preferential secretion of collagen type 3 versus type 1 from adventitial fibroblasts stimulated by TGF-β/Smad3-Treated medial smooth muscle cells. Cell Signal 2013 25 955 960. doi: 10.1016/j.cellsig.2012.12.021
32. Humphrey JD, Dufresne ER, Schwartz MA, Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 2014 1 11
33. Eberth JF, Gresham VC, Reddy AK, Popovic N, Wilson E, Humphrey JD, Importance of pulsatility in hypertensive carotid artery growth and remodeling. J Hypertens 2009 27 2010 2021. doi: 10.1097/HJH.0b013e32832e8dc8
34. Capers Q IV, Alexander RW, Lou P, De Leon H, Wilcox JN, Ishizaka N, Howard AB, Taylor WR, Monocyte chemoattractant protein-1 expression in aortic tissues of hypertensive rats. Hypertension 1997 30 1397 1402
35. Fleenor BS, Marshall KD, Durrant JR, Lesniewski LA, Seals DR, Arterial stiffening with ageing is associated with transforming growth factor-β1-related changes in adventitial collagen: reversal by aerobic exercise. J Physiol 2010 588 pt 20 3971 3982. doi: 10.1113/jphysiol.2010.194753
36. Lesniewski LA, Durrant JR, Connell ML, Henson GD, Black AD, Donato AJ, Seals DR, Aerobic exercise reverses arterial inflammation with aging in mice. Am J Physiol Heart Circ Physiol 2011 301 H1025 H1032. doi: 10.1152/ajpheart.01276.2010
37. Maiellaro K, Taylor WR, The role of the adventitia in vascular inflammation. Cardiovasc Res 2007 75 640 648. doi: 10.1016/j.cardiores.2007.06.023
38. Gingras M, Farand P, Safar ME, Plante GE, Adventitia: the vital wall of conduit arteries. J Am Soc Hypertens 2009 3 166 183. doi: 10.1016/j.jash.2009.03.002
39. Majesky MW, Dong XR, Hoglund V, Mahoney WM Jr, Daum G, The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol 2011 31 1530 1539. doi: 10.1161/ATVBAHA.110.221549
40. Li Q, Muragaki Y, Hatamura I, Ueno H, Ooshima A, Stretch-induced collagen synthesis in cultured smooth muscle cells from rabbit aortic media and a possible involvement of angiotensin II and transforming growth factor-beta. J Vasc Res 1998 35 93 103
41. Stanley AG, Patel H, Knight AL, Williams B, Mechanical strain-induced human vascular matrix synthesis: the role of angiotensin II. J Renin Angiotensin Aldosterone Syst 2000 1 32 35. doi: 10.3317/jraas.2000.007
42. Ford CM, Li S, Pickering JG, Angiotensin II stimulates collagen synthesis in human vascular smooth muscle cells. Involvement of the AT(1) receptor, transforming growth factor-beta, and tyrosine phosphorylation. Arterioscler Thromb Vasc Biol 1999 19 1843 1851
43. Browatzki M, Larsen D, Pfeiffer CA, Gehrke SG, Schmidt J, Kranzhofer A, Katus HA, Kranzhofer R, Angiotensin II stimulates matrix metalloproteinase secretion in human vascular smooth muscle cells via nuclear factor-kappaB and activator protein 1 in a redox-sensitive manner. J Vasc Res 2005 42 415 423. doi: 10.1159/000087451
44. Tieu BC, Ju X, Lee C, Sun H, Lejeune W, Recinos A III, Brasier AR, Tilton RG, Aortic adventitial fibroblasts participate in angiotensin-induced vascular wall inflammation and remodeling. J Vasc Res 2011 48 261 272. doi: 10.1159/000320358
45. Marvar PJ, Thabet SR, Guzik TJ, Lob HE, McCann LA, Weyand C, Gordon FJ, Harrison DG, Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res 2010 107 263 270. doi: 10.1161/CIRCRESAHA.110.217299
46. Bardy N, Merval R, Benessiano J, Samuel JL, Tedgui A, Pressure and angiotensin II synergistically induce aortic fibronectin expression in organ culture model of rabbit aorta. Evidence for a pressure-induced tissue renin-Angiotensin system. Circ Res 1996 79 70 78
47. Lehoux S, Lemarié CA, Esposito B, Lijnen HR, Tedgui A, Pressure-induced matrix metalloproteinase-9 contributes to early hypertensive remodeling. Circulation 2004 109 1041 1047. doi: 10.1161/01.CIR.0000115521.95662.7A.