Arterial stiffening with ageing is associated with transforming growth factor-β1-related changes in adventitial collagen: Reversal by aerobic exercise

Journal of Physiology

Volumn 588, Issue 20, 2010, Pages 3971-3982

  Fleenor, Bradley S ^a   Marshall, Kurt D ^a   Durrant, Jessica R ^a   Lesniewski, Lisa A ^a   Seals, Douglas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; ELASTIN; GELATINASE A; PROTEIN LYSINE 6 OXIDASE; SUPEROXIDE; TEMPOL; TRANSFORMING GROWTH FACTOR BETA1;

ADVENTITIA; AEROBIC EXERCISE; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL STIFFNESS; ARTERY CALCIFICATION; ARTICLE; CAROTID ARTERY; CELL CULTURE; CONTROLLED STUDY; ENZYME DEGRADATION; EX VIVO STUDY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGING; ANALYSIS OF VARIANCE; ANIMALS; CAROTID ARTERY DISEASES; CELLS, CULTURED; COLLAGEN; CONNECTIVE TISSUE; CYCLIC N-OXIDES; ELASTIN; FIBROBLASTS; FIBRONECTINS; MALE; MATRIX METALLOPROTEINASE 2; MICE; MYOCYTES, SMOOTH MUSCLE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; SPIN LABELS; SUPEROXIDES; TRANSFORMING GROWTH FACTOR BETA1;

EID: 77958178612     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.194753     Document Type: Article

References (57)

1. Atkinson J (2008). Age-related elastocalcinosis in arteries: mechanisms, animal models, and physiological consequences. J Appl Physiol 105, 1643-1651.
2. Bedell-Hogan D, Trackman P, Abrams W, Rosenbloom J & Kagan H (1993). Oxidation, cross-linking, and insolubilization of recombinant tropoelastin by purified lysyl oxidase. J Biol Chem 268, 10345-10350.
3. Blair S, Kohl H 3rd, Paffenbarger RS Jr, Clark D, Cooper K & Gibbons L (1989). Physical fitness and all-cause mortality. A prospective study of healthy men and women. J Am Med Assoc 262, 2395-2401.
4. Blobe GC, Schiemann WP & Lodish HF (2000). Role of transforming growth factor β in human disease. N Engl J Med 342, 1350-1358.
5. Boumaza S, Arribas SM, Osborne-Pellegrin M, McGrath JC, Laurent S, Lacolley P & Challande P (2001). Fenestrations of the carotid internal elastic lamina and structural adaptation in stroke-prone spontaneously hypertensive rats. Hypertension 37, 1101-1107.
6. Bradley RL, Jeon JY, Liu F-F & Maratos-Flier E (2008). Voluntary exercise improves insulin sensitivity and adipose tissue inflammation in diet-induced obese mice. Am J Physiol Endocrinol Metab 295, E586-594.
7. Brüel A & Oxlund H (1996). Changes in biomechanical properties, composition of collagen and elastin, and advanced glycation endproducts of the rat aorta in relation to age. Atherosclerosis 127, 155-165.
8. Cox RH (1983). Age-related changes in arterial wall mechanics and composition of NIA Fischer rats. Mech Ageing Dev 23, 21-36.
9. DeSouza CA, Shapiro LF, Clevenger CM, Dinenno FA, Monahan KD, Tanaka H & Seals DR (2000). Regular aerobic exercise prevents and restores age-related declines in endothelium-dependent vasodilation in healthy men. Circulation 102, 1351-1357.
10. Diez J (2007). Arterial stiffness and extracellular matrix. Adv Cardiol 44, 76-95.
11. Durrant JR, Seals DR, Connell ML, Russell MJ, Lawson BR, Folian BJ, Donato AJ & Lesniewski LA (2009). Voluntary wheel running restores endothelial function in conduit arteries of old mice: direct evidence for reduced oxidative stress, increased superoxide dismutase activity and down-regulation of NADPH oxidase. J Physiol 587, 3271-3285.
12. Emonard H & Hornebeck W (1997). Binding of 92 kDa and 72 kDa progelatineases to insoluble elastin modulates their proteolytic activation. Biol Chem 378, 265-271.
13. Hruska KA, Mathew S & Saab G (2005). Bone morphogenetic proteins in vascular calcification. Circ Res 97, 105-114.
14. Hynes RO & Yamada KM (1982). Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95, 369-377.
15. Kang YH, Jin JS, Yi DW & Son SM (2010). Bone morphogenetic protein-7 inhibits vascular calcification induced by high vitamin D in mice. Tohoku J Exp Med 221, 299-307.
16. Kass DA, Shapiro EP, Kawaguchi M, Capriotti AR, Scuteri A, DeGroof RC & Lakatta EG (2001). Improved arterial compliance by a novel advanced glycation end-product crosslink breaker. Circulation 104, 1464-1470.
17. Kawasaki T, Sasayama S, Yagi S-I, Asakawa T & Hirai T (1987). Non-invasive assessment of the age related changes in stiffness of major branches of the human arteries. Cardiovasc Res 21, 678-687.
18. Kieffer P, Robert A, Capdeville-Atkinson C, Atkinson J & Lartaud-Idjouadiene I (2000). Age-related arterial calcification in rats. Life Sci 66, 2371-2381.
19. Kothapalli CR & Ramamurthi A (2009). Lysyl oxidase enhances elastin synthesis and matrix formation by vascular smooth muscle cells. J Tissue Eng Regenerative Med 3, 655-661.
20. Koyanagi M, Egashira K, Kubo-Inoue M, Usui M, Kitamoto S, Tomita H, Shimokawa H & Takeshita A (2000). Role of transforming growth factor β1 in cardiovascular inflammatory changes induced by chronic inhibition of nitric oxide synthesis. Hypertension 35, 86-90.
21. Lakatta EG & Levy D (2003). Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part I: aging arteries: a "set up" for vascular disease. Circulation 107, 139-146.
22. Lesniewski LA, Connell ML, Durrant JR, Folian BJ, Anderson MC, Donato AJ & Seals DR (2009). B6D2F1 mice are a suitable model of oxidative stress-mediated impaired endothelium-dependent dilation with aging. J Gerontol A Biol Sci Med Sci 64A, 9-20.
23. Li Z, Froehlich J, Galis ZS & Lakatta EG (1999). Increased expression of matrix metalloproteinase-2 in the thickened intima of aged rats. Hypertension 33, 116-123.
24. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J &, on behalf of the American Heart Association Statistics Committee and Stroke Statistics S (2010). Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121, e46-215.
25. Matsuda M, Nosaka T, Sato M & Ohshima N (1993). Effects of physical exercise on the elasticity and elastic components of the rat aorta. Eur J Appl Physiol Occup Physiol 66, 122-126.
26. Maurel E, Shuttleworth CA & Bouissou H (1987). Interstitial collagens and ageing in human aorta. Virchows Archiv 410, 383-390.
27. Moreau KL, Donato AJ, Seals DR, DeSouza CA & Tanaka H (2003). Regular exercise, hormone replacement therapy and the age-related decline in carotid arterial compliance in healthy women. Cardiovasc Res 57, 861-868.
28. Muller-Delp J, Spier SA, Ramsey MW, Lesniewski LA, Papadopoulos A, Humphrey JD & Delp MD (2002). Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 282, H1843-1854.
29. Niederhoffer N, Kieffer P, Desplanches D, Lartaud-Idjouadiene I, Sornay M-H & Atkinson J (2000). Physical exercise, aortic blood pressure, and aortic wall elasticity and composition in rats. Hypertension 35, 919-924.
30. Nosaka H, Tanaka H, Watanabe I, Sato M & Matsuda M (2003). Influence of regular exercise on age-related changes in arterial elasticity: mechanistic insights from wall compositions in rat aorta. Can J Appl Physiol 28, 204-212.
31. Pagano P, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM & Quinn MT (1997). Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: Enhancement by angiotensin II. Proc Natl Acad Sci U S A 94, 14483-14488.
32. Patel S, Shi Y, Niculescu R, Chung EH, Martin JL & Zalewski A (2000). Characteristics of coronary smooth muscle cells and adventitial fibroblasts. Circulation 101, 524-532.
33. Qiu H, Depre C, Ghosh K, Resuello RG, Natividad FF, Rossi F, Peppas A, Shen Y-T, Vatner DE & Vatner SF (2007a). Mechanism of gender-specific differences in aortic stiffness with aging in nonhuman primates. Circulation 116, 669-676.
34. Qiu H, Tian B, Resuello RG, Natividad FF, Peppas A, Shen Y-T, Vatner DE, Vatner SF & Depre C (2007b). Sex-specific regulation of gene expression in the aging monkey aorta. Physiol Genomics 29, 169-180.
35. Rippe C, Lesniewski L, Connell M, LaRocca T, Donato A & Seals D (2010). Short-term calorie restriction reverses vascular endothelial dysfunction in old mice by increasing nitric oxide and reducing oxidative stress. Aging Cell 9, 304-312.
36. Ruckman JL, Luvalle PA, Hill KE, Giro MG & Davidson JM (1994). Phenotypic stability and variation in cells of the porcine aorta: collagen and elastin production. Matrix Biol 14, 135-145.
37. Ruiz-Ortega M, Rodriguez-Vita J, Sanchez-Lopez E, Carvajal G & Egido J (2007). TGF-β signaling in vascular fibrosis. Cardiovasc Res 74, 196-206.
38. Sauvage M, Hinglais N, Mandet C, Badier C, Deslandes F, Michel JB & Jacob MP (1998). Localization of elastin mRNA and TGF-β1 in rat aorta and caudal artery as a function of age. Cell Tissue Res 291, 305-314.
39. Schulze-Bauer CAJ, Regitnig P & Holzapfel GA (2002). Mechanics of the human femoral adventitia including the high-pressure response. Am J Physiol Heart Circ Physiol 282, H2427-2440.
40. Seals DR, DeSouza CA, Donato AJ & Tanaka H (2008). Habitual exercise and arterial aging. J Appl Physiol 105, 1323-1332.
41. Seals DR, Walker AE, Pierce GL & Lesniewski LA (2009). Habitual exercise and vascular ageing. J Physiol 587, 5541-5549.
42. Semba RD, Najjar SS, Sun K, Lakatta EG & Ferrucci L (2009). Serum carboxymethyl-lysine, an advanced glycation end product, is associated with increased aortic pulse wave velocity in adults. Am J Hypertens 22, 74-79.
43. Simionescu A, Philips K & Vyavahare N (2005). Elastin-derived peptides and TGF β1 induce osteogenic responses in smooth muscle cells. Biochem Biophys Res Commun 334, 524-532.
44. Simionescu A, Simionescu D & Vyavahare N (2007). Osteogenic responses in fibroblasts activated by elastin degradation products and transforming growth factor β1. Am J Pathol 171, 116-123.
45. Simon G & Danneman KJ (2005). Dilation and reduced distensibility of rat carotid artery with aging. Clin Exp Hypertens 6, 459-466.
46. Siow RCM & Churchman AT (2007). Adventitial growth factor signalling and vascular remodelling: Potential of perivascular gene transfer from the outside-in. Cardiovasc Res 75, 659-668.
47. Sommer G, Regitnig P, Koltringer L & Holzapfel GA (2010). Biaxial mechanical properties of intact and layer-dissected human carotid arteries at physiological and supraphysiological loadings. Am J Physiol Heart Circ Physiol 298, H898-912.
48. Sternlicht MD & Werb Z (2001). How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17, 463-516.
49. Tanaka H, DeSouza CA & Seals DR (1998). Absence of age-related increase in central arterial stiffness in physically active women. Arterioscler Thromb Vasc Biol 18, 127-132.
50. Tanaka H, Dinenno FA, Monahan KD, Clevenger CM, DeSouza CA & Seals DR (2000). Aging, habitual exercise, and dynamic arterial compliance. Circulation 102, 1270-1275.
51. Vaitkevicius PV, Fleg JL, Engel JH, O'Connor FC, Wright JG, Lakatta LE, Yin FC & Lakatta EG (1993). Effects of age and aerobic capacity on arterial stiffness in healthy adults. Circulation 88, 1456-1462.
52. Wang M & Lakatta EG (2002). Altered regulation of matrix metalloproteinase-2 in arotic remodeling during aging. Hypertension 39, 865-873.
53. Wang M & Lakatta EG (2002). Altered regulation of matrix metalloproteinase-2 in aortic remodeling during aging. Hypertension 39, 865-873.
54. Wang M, Zhang J, Jiang L-Q, Spinetti G, Pintus G, Monticone R, Kolodgie FD, Virmani R & Lakatta EG (2007). Proinflammatory profile within the grossly normal aged human aortic wall. Hypertension 50, 219-227.
55. Wang M, Zhang J, Spinetti G, Jiang L-Q, Monticone R, Zhao D, Cheng L, Krawczyk M, Talan M, Pintus G & Lakatta EG (2005). Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats. Am J Pathol 167, 1429-1442.
56. Wang M, Zhao D, Spinetti G, Zhang J, Jiang L-Q, Pintus G, Monticone R & Lakatta EG (2006). Matrix metalloproteinase 2 activation of transforming growth factor-β1 (TGF-β1) and TGF-β1-type II receptor signaling within the aged arterial wall. Arterioscler Thromb Vasc Biol 26, 1503-1509.
57. Zieman SJ, Melenovsky V & Kass DA (2005). Mechanisms, pathophysiology, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol 25, 932-943.