Advertisement

Elastin in Large Artery Stiffness and Hypertension

  • Jessica E. WagenseilEmail author
  • Robert P. Mecham
Article

Abstract

Large artery stiffness, as measured by pulse wave velocity, is correlated with high blood pressure and may be a causative factor in essential hypertension. The extracellular matrix components, specifically the mix of elastin and collagen in the vessel wall, determine the passive mechanical properties of the large arteries. Elastin is organized into elastic fibers in the wall during arterial development in a complex process that requires spatial and temporal coordination of numerous proteins. The elastic fibers last the lifetime of the organism but are subject to proteolytic degradation and chemical alterations that change their mechanical properties. This review discusses how alterations in the amount, assembly, organization, or chemical properties of the elastic fibers affect arterial stiffness and blood pressure. Strategies for encouraging or reversing alterations to the elastic fibers are addressed. Methods for determining the efficacy of these strategies, by measuring elastin amounts and arterial stiffness, are summarized. Therapies that have a direct effect on arterial stiffness through alterations to the elastic fibers in the wall may be an effective treatment for essential hypertension.

Keywords

Extracellular matrix Mechanics Pulse wave velocity Compliance 

Notes

Acknowledgments

This work was supported by the National Heart, Lung, and Blood Institute Grants HL-087653 (to J.E. Wagenseil), HL-74138 (to R.P. Mecham), and HL-105314 (to J.E. Wagenseil and R.P. Mecham).

References

  1. 1.
    Mulvany, M. J. (2008). Small artery remodelling in hypertension: Causes, consequences and therapeutic implications. Medical & Biological Engineering & Computing, 46(5), 461–467. doi: 10.1007/s11517-008-0305-3.CrossRefGoogle Scholar
  2. 2.
    Kearney, P. M., Whelton, M., Reynolds, K., Muntner, P., Whelton, P. K., & He, J. (2005). Global burden of hypertension: Analysis of worldwide data. Lancet, 365(9455), 217–223. doi: 10.1016/S0140-6736(05)17741-1.PubMedGoogle Scholar
  3. 3.
    Cecelja, M., & Chowienczyk, P. (2009). Dissociation of aortic pulse wave velocity with risk factors for cardiovascular disease other than hypertension: A systematic review. Hypertension, 54(6), 1328–1336. doi: 10.1161/HYPERTENSIONAHA.109.137653.PubMedCrossRefGoogle Scholar
  4. 4.
    Messerli, F. H., Frohlich, E. D., & Ventura, H. O. (1985). Arterial compliance in essential hypertension. Journal of Cardiovascular Pharmacology, 7(Suppl 2), S33–S35.PubMedCrossRefGoogle Scholar
  5. 5.
    Faury, G., Maher, G. M., Li, D. Y., Keating, M. T., Mecham, R. P., & Boyle, W. A. (1999). Relation between outer and luminal diameter in cannulated arteries. American Journal of Physiology, 277(5 Pt 2), H1745–H1753.PubMedGoogle Scholar
  6. 6.
    Mecham, R. P. (1998). Overview of extracellular matrix. In: Current protocols in cell biology. Wiley, New York, pp 10.11.11–10.11.14.Google Scholar
  7. 7.
    Fung, Y. C. (1993). Biomechanics: Mechanical properties of living tissues (2nd ed.). New York: Springer.Google Scholar
  8. 8.
    Greenwald, S. E. (2007). Ageing of the conduit arteries. The Journal of Pathology, 211(2), 157–172. doi: 10.1002/path.2101.PubMedCrossRefGoogle Scholar
  9. 9.
    McEniery, C. M., Wilkinson, I. B., & Avolio, A. P. (2007). Age, hypertension and arterial function. Clinical and Experimental Pharmacology & Physiology, 34(7), 665–671. doi: 10.1111/j.1440-1681.2007.04657.x.CrossRefGoogle Scholar
  10. 10.
    Wolinsky, H., & Glagov, S. (1967). A lamellar unit of aortic medial structure and function in mammals. Circulation Research, 20(1), 99–111.PubMedGoogle Scholar
  11. 11.
    Clark, J. M., & Glagov, S. (1985). Transmural organization of the arterial media. The lamellar unit revisited. Arteriosclerosis, 5(1), 19–34.PubMedCrossRefGoogle Scholar
  12. 12.
    Armentano, R. L., Levenson, J., Barra, J. G., Fischer, E. I., Breitbart, G. J., Pichel, R. H., & Simon, A. (1991). Assessment of elastin and collagen contribution to aortic elasticity in conscious dogs. American Journal of Physiology, 260(6 Pt 2), H1870–H1877.PubMedGoogle Scholar
  13. 13.
    Wolinsky, H., & Glagov, S. (1964). Structural basis for the static mechanical properties of the aortic media. Circulation Research, 14, 400–413.PubMedGoogle Scholar
  14. 14.
    Wagenseil, J. E., & Mecham, R. P. (2009). Vascular extracellular matrix and arterial mechanics. Physiological Reviews, 89(3), 957–989. doi: 10.1152/physrev.00041.2008.PubMedCrossRefGoogle Scholar
  15. 15.
    Wagenseil, J. E., & Mecham, R. P. (2007). New insights into elastic fiber assembly. Birth Defects Research. Part C, Embryo Today, 81(4), 229–240.CrossRefGoogle Scholar
  16. 16.
    Kelleher, C. M., McLean, S. E., & Mecham, R. P. (2004). Vascular extracellular matrix and aortic development. Current Topics in Developmental Biology, 62, 153–188.PubMedCrossRefGoogle Scholar
  17. 17.
    Curran, M., Atkinson, D., Ewart, A., Morris, C., Leppert, M., & Keating, M. (1993). The elastin gene is disrupted by a translocation associated with supravalvular aortic stenosis. Cell, 73(1), 159–168.PubMedCrossRefGoogle Scholar
  18. 18.
    Li, D. Y., Toland, A. E., Boak, B. B., Atkinson, D. L., Ensing, G. J., Morris, C. A., & Keating, M. R. (1997). Elastin point mutations cause an obstructive vascular disease, supravalvular aortic stenosis. Human Molecular Genetics, 6, 1021–1028.PubMedCrossRefGoogle Scholar
  19. 19.
    Olson, T., Michels, V., Urban, Z., Csiszar, K., Christiano, A., Driscoll, D., Feldt, R., Boyd, C., & Thibodeau, S. (1995). A 30 kb deletion within the elastin gene results in familial supravalvular aortic stenosis. Human Molecular Genetics, 4(9), 1677–1679.PubMedCrossRefGoogle Scholar
  20. 20.
    Pober, B., Johnson, M., & Urban, Z. (2008). Mechanisms and treatment of cardiovascular disease in Williams-Beuren syndrome. The Journal of Clinical Investigation, 118(5), 1606–1615. doi: 10.1172/JCI35309.PubMedCrossRefGoogle Scholar
  21. 21.
    Urban, Z., Michels, V. V., Thibodeau, S. N., Davis, E. C., Bonnefont, J.-P., Munnich, A., Eyskens, B., Gewillig, M., Devriendt, K., & Boyd, C. D. (2000). Isolated supravalvular aortic stenosis: Functional haploinsufficiency of the elastin gene as a result of nonsense-mediated decay. Human Genetics, 106, 577–588.PubMedCrossRefGoogle Scholar
  22. 22.
    O’Connor, W. N., Davis, J. B., Jr., Geissler, R., Cottrill, C. M., Noonan, J. A., & Todd, E. P. (1985). Supravalvular aortic stenosis. Clinical and pathologic observations in six patients. Archives of Pathology & Laboratory Medicine, 109(2), 179–185.Google Scholar
  23. 23.
    Kozel, B. A., Wachi, H., Davis, E. C., & Mecham, R. P. (2003). Domains in tropoelastin that mediate elastin deposition in vitro and in vivo. Journal of Biological Chemistry, 278(20), 18491–18498.PubMedCrossRefGoogle Scholar
  24. 24.
    Graul-Neumann, L., Hausser, I., Essayie, M., Rauch, A., & Kraus, C. (2008). Highly variable cutis laxa resulting from a dominant splicing mutation of the elastin gene. American Journal of Medical Genetics. Part A, 146A(8), 977–983. doi: 10.1002/ajmg.a.32242.PubMedCrossRefGoogle Scholar
  25. 25.
    Rodriguez-Revenga, L., Iranzo, P., Badenas, C., Puig, S., Carrio, A., & Mila, M. (2004). A novel elastin gene mutation resulting in an autosomal dominant form of cutis laxa. Archives of Dermatology, 140(9), 1135–1139.PubMedCrossRefGoogle Scholar
  26. 26.
    Tassabehji, M., Metcalfe, K., Hurst, J., Ashcroft, G. S., Kielty, C., Wilmot, C., Donnai, D., Read, A. P., & Jones, C. J. P. (1998). An elastin gene mutation producing abnormal tropoelastin and abnormal elastic fibres in a patient with autosomal dominant cutis laxa. Human Molecular Genetics, 7, 1021–1028.PubMedCrossRefGoogle Scholar
  27. 27.
    Zhang, M. C., Giro, M., Quaglino, D., Jr., & Davidson, J. M. (1995). Transforming growth factor-beta reverses a posttranscriptional defect in elastin synthesis in a cutis laxa skin fibroblast strain. The Journal of Clinical Investigation, 95, 986–994.PubMedCrossRefGoogle Scholar
  28. 28.
    Callewaert, B., Renard, M., Hucthagowder, V., Albrecht, B., Hausser, I., Blair, E., Dias, C., Albino, A., Wachi, H., Sato, F., Mecham, R., Loeys, B., Coucke, P., De Paepe, A., & Urban, Z. (2011). New insights into the pathogenesis of autosomal-dominant cutis laxa with report of five ELN mutations. Human Mutation, 32(4), 445–455. doi: 10.1002/humu.21462.PubMedCrossRefGoogle Scholar
  29. 29.
    Damkier, A., Brandrup, F., & Starklint, H. (1991). Cutis laxa: Autosomal dominant inheritance in five generations. Clinical Genetics, 39(5), 321–329.PubMedCrossRefGoogle Scholar
  30. 30.
    Szabo, Z., Crepeau, M. W., Mitchell, A. L., Stephan, M. J., Puntel, R. A., Yin Loke, K., Kirk, R. C., & Urban, Z. (2006). Aortic aneurysmal disease and cutis laxa caused by defects in the elastin gene. Journal of Medical Genetics, 43, 255–258.PubMedCrossRefGoogle Scholar
  31. 31.
    Urban, Z., Gao, J., Pope, F. M., & Davis, E. C. (2005). Autosomal dominant cutis laxa with severe lung disease: Synthesis and matrix deposition of mutant tropoelastin. The Journal of Investigative Dermatology, 124, 1193–1199.PubMedCrossRefGoogle Scholar
  32. 32.
    Iwai, N., Kajimoto, K., Kokubo, Y., & Tomoike, H. (2006). Extensive genetic analysis of 10 candidate genes for hypertension in Japanese. Hypertension, 48(5), 901–907. doi: 10.1161/01.HYP.0000242485.23148.bb.PubMedCrossRefGoogle Scholar
  33. 33.
    Milewicz, D. M., Urbán, Z., & Boyd, C. D. (2000). Genetic disorders of the elastic fiber system. Matrix Biology, 19, 471–480.PubMedCrossRefGoogle Scholar
  34. 34.
    Claus, S., Fischer, J., Megarbane, H., Megarbane, A., Jobard, F., Debret, R., Peyrol, S., Saker, S., Devillers, M., Sommer, P., & Damour, O. (2008). A p.C217R mutation in fibulin-5 from cutis laxa patients is associated with incomplete extracellular matrix formation in a skin equivalent model. The Journal of Investigative Dermatology, 128(6), 1442–1450. doi: 10.1038/sj.jid.5701211.PubMedCrossRefGoogle Scholar
  35. 35.
    Dasouki, M., Markova, D., Garola, R., Sasaki, T., Charbonneau, N., Sakai, L., & Chu, M. (2007). Compound heterozygous mutations in fibulin-4 causing neonatal lethal pulmonary artery occlusion, aortic aneurysm, arachnodactyly, and mild cutis laxa. American Journal of Medical Genetics. Part A, 143(22), 2635–2641. doi: 10.1002/ajmg.a.31980.CrossRefGoogle Scholar
  36. 36.
    Hu, Q., Loeys, B. L., Coucke, P. J., De Paepe, A., Mecham, R. P., Choi, J., Davis, E. C., & Urban, Z. (2006). Fibulin-5 mutations: Mechanisms of impaired elastic fiber formation in recessive cutis laxa. Human Molecular Genetics, 15(23), 3379–3386.PubMedCrossRefGoogle Scholar
  37. 37.
    Hucthagowder, V., Sausgruber, N., Kim, K., Angle, B., Marmorstein, L., & Urban, Z. (2006). Fibulin-4: A novel gene for an autosomal recessive cutis laxa syndrome. American Journal of Human Genetics, 78(6), 1075–1080. doi: 10.1086/504304.PubMedCrossRefGoogle Scholar
  38. 38.
    Loeys, B., Van Maldergem, L., Mortier, G., Coucke, P., Gerniers, S., Naeyaert, J. M., & De Paepe, A. (2002). Homozygosity for a missense mutation in fibulin-5 (FBLN5) results in a severe form of cutis laxa. Human Molecular Genetics, 11(18), 2113–2118.PubMedCrossRefGoogle Scholar
  39. 39.
    Lotery, A., Baas, D., Ridley, C., Jones, R., Klaver, C., Stone, E., Nakamura, T., Luff, A., Griffiths, H., Wang, T., Bergen, A., & Trump, D. (2006). Reduced secretion of fibulin 5 in age-related macular degeneration and cutis laxa. Human Mutation, 27(6), 568–574. doi: 10.1002/humu.20344.PubMedCrossRefGoogle Scholar
  40. 40.
    Li, D. Y., Brooke, B., Davis, E. C., Mecham, R. P., Sorensen, L. K., Boak, B. B., Eichwald, E., & Keating, M. T. (1998). Elastin is an essential determinant of arterial morphogenesis. Nature, 393(6682), 276–280.PubMedCrossRefGoogle Scholar
  41. 41.
    Wagenseil, J. E., Ciliberto, C. H., Knutsen, R. H., Levy, M. A., Kovacs, A., & Mecham, R. P. (2010). The importance of elastin to aortic development in mice. American Journal of Physiology - Heart and Circulatory Physiology, 299(2), H257–H264. doi: 10.1152/ajpheart.00194.2010.PubMedCrossRefGoogle Scholar
  42. 42.
    Wagenseil, J. E., Ciliberto, C. H., Knutsen, R. H., Levy, M. A., Kovacs, A., & Mecham, R. P. (2009). Reduced vessel elasticity alters cardiovascular structure and function in newborn mice. Circulation Research, 104(10), 1217–1224. doi: 10.1161/CIRCRESAHA.108.192054.PubMedCrossRefGoogle Scholar
  43. 43.
    Karnik, S. K., Brooke, B. S., Bayes-Genis, A., Sorensen, L., Wythe, J. D., Schwartz, R. S., Keating, M. T., & Li, D. Y. (2003). A critical role for elastin signaling in vascular morphogenesis and disease. Development, 130(2), 411–423.PubMedCrossRefGoogle Scholar
  44. 44.
    Faury, G., Pezet, M., Knutsen, R. H., Boyle, W. A., Heximer, S. P., McLean, S. E., Minkes, R. K., Blumer, K. J., Kovacs, A., Kelly, D. P., Li, D. Y., Starcher, B., & Mecham, R. P. (2003). Developmental adaptation of the mouse cardiovascular system to elastin haploinsufficiency. The Journal of Clinical Investigation, 112(9), 1419–1428.PubMedGoogle Scholar
  45. 45.
    Li, D. Y., Faury, G., Taylor, D. G., Davis, E. C., Boyle, W. A., Mecham, R. P., Stenzel, P., Boak, B., & Keating, M. T. (1998). Novel arterial pathology in mice and humans hemizygous for elastin. The Journal of Clinical Investigation, 102(10), 1783–1787.PubMedCrossRefGoogle Scholar
  46. 46.
    Wagenseil, J. E., Nerurkar, N. L., Knutsen, R. H., Okamoto, R. J., Li, D. Y., & Mecham, R. P. (2005). Effects of elastin haploinsufficiency on the mechanical behavior of mouse arteries. American Journal of Physiology - Heart and Circulatory Physiology, 289(3), H1209–H1217.PubMedCrossRefGoogle Scholar
  47. 47.
    Wagenseil, J. E., Knutsen, R. H., Li, D., & Mecham, R. P. (2007). Elastin-insufficient mice show normal cardiovascular remodeling in 2K1C hypertension, despite higher baseline pressure and unique cardiovascular architecture. American Journal Physiology - Heart and Circulatory Physiology, 293(1), H574–H582.CrossRefGoogle Scholar
  48. 48.
    Le, V. P., Knutsen, R. H., Mecham, R. P., & Wagenseil, J. E. (2011). Decreased aortic diameter and compliance precedes blood pressure increases in postnatal development of elastin-insufficient mice. American Journal of Physiology - Heart and Circulatory Physiology. doi: 10.1152/ajpheart.00119.2011.
  49. 49.
    Passman, J. N., Dong, X. R., Wu, S. P., Maguire, C. T., Hogan, K. A., Bautch, V. L., & Majesky, M. W. (2008). A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proceedings of the National Academy of Sciences of the United States of America, 105(27), 9349–9354.PubMedCrossRefGoogle Scholar
  50. 50.
    Hirano, E., Knutsen, R. H., Sugitani, H., Ciliberto, C. H., & Mecham, R. P. (2007). Functional rescue of elastin insufficiency in mice by the human elastin gene: Implications for mouse models of human disease. Circulation Research, 101(5), 523–531.PubMedCrossRefGoogle Scholar
  51. 51.
    Li, Z., Froehlich, J., Galis, Z. S., & Lakatta, E. G. (1999). Increased expression of matrix metalloproteinase-2 in the thickened intima of aged rats. Hypertension, 33(1), 116–123.PubMedGoogle Scholar
  52. 52.
    Tamarina, N. A., McMillan, W. D., Shively, V. P., & Pearce, W. H. (1997). Expression of matrix metalloproteinases and their inhibitors in aneurysms and normal aorta. Surgery, 122(2), 264–271. discussion 271–262.PubMedCrossRefGoogle Scholar
  53. 53.
    Yasmin, Mc. Eniery. C. M., O’Shaughnessy, K. M., Harnett, P., Arshad, A., Wallace, S., Maki-Petaja, K., McDonnell, B., Ashby, M. J., Brown, J., Cockcroft, J. R., & Wilkinson, I. B. (2006). Variation in the human matrix metalloproteinase-9 gene is associated with arterial stiffness in healthy individuals. Arteriosclerosis, Thrombosis, and Vascular Biology, 26(8), 1799–1805. doi: 10.1161/01.ATV.0000227717.46157.32.PubMedCrossRefGoogle Scholar
  54. 54.
    Wolinsky, H. (1970). Response of the rat aortic media to hypertension. Morphological and chemical studies. Circulation Research, 26(4), 507–522.PubMedGoogle Scholar
  55. 55.
    Todorovich-Hunter, L., Johnson, D., Ranger, P., Keeley, F., & Rabinovitch, M. (1988). Altered elastin and collagen synthesis associated with progressive pulmonary hypertension induced by monocrotaline. A biochemical and ultrastructural study. Laboratory Investigation, 58(2), 184–195.PubMedGoogle Scholar
  56. 56.
    Keeley, F. W., Elmoselhi, A., & Leenen, F. H. (1991). Effects of antihypertensive drug classes on regression of connective tissue components of hypertension. Journal of Cardiovascular Pharmacology, 17(Suppl 2), S64–S69.PubMedGoogle Scholar
  57. 57.
    Dao, H. H., Essalihi, R., Bouvet, C., & Moreau, P. (2005). Evolution and modulation of age-related medial elastocalcinosis: Impact on large artery stiffness and isolated systolic hypertension. Cardiovascular Research, 66(2), 307–317. doi: 10.1016/j.cardiores.2005.01.012.PubMedCrossRefGoogle Scholar
  58. 58.
    Aronson, D. (2003). Cross-linking of glycated collagen in the pathogenesis of arterial and myocardial stiffening of aging and diabetes. Journal of Hypertension, 21(1), 3–12. doi: 10.1097/01.hjh.0000042892.24999.92.PubMedCrossRefGoogle Scholar
  59. 59.
    Konova, E., Baydanoff, S., Atanasova, M., & Velkova, A. (2004). Age-related changes in the glycation of human aortic elastin. Experimental Gerontology, 39(2), 249–254. doi: 10.1016/j.exger.2003.10.003.PubMedCrossRefGoogle Scholar
  60. 60.
    Milewicz, D. M., Urban, Z., & Boyd, C. (2000). Genetic disorders of the elastic fiber system. Matrix Biology, 19(6), 471–480.PubMedCrossRefGoogle Scholar
  61. 61.
    Allaire, E., Forough, R., Clowes, M., Starcher, B., & Clowes, A. W. (1998). Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. The Journal of Clinical Investigation, 102(7), 1413–1420. doi: 10.1172/JCI2909.PubMedCrossRefGoogle Scholar
  62. 62.
    Jiang, L., Wang, M., Zhang, J., Monticone, R. E., Telljohann, R., Spinetti, G., Pintus, G., & Lakatta, E. G. (2008). Increased aortic calpain-1 activity mediates age-associated angiotensin II signaling of vascular smooth muscle cells. PLoS One, 3(5), e2231. doi: 10.1371/journal.pone.0002231.PubMedCrossRefGoogle Scholar
  63. 63.
    Castro, M. M., Rizzi, E., Figueiredo-Lopes, L., Fernandes, K., Bendhack, L. M., Pitol, D. L., Gerlach, R. F., & Tanus-Santos, J. E. (2008). Metalloproteinase inhibition ameliorates hypertension and prevents vascular dysfunction and remodeling in renovascular hypertensive rats. Atherosclerosis, 198(2), 320–331. doi: 10.1016/j.atherosclerosis.2007.10.011.PubMedCrossRefGoogle Scholar
  64. 64.
    Tatchum-Talom, R., Niederhoffer, N., Amin, F., Makki, T., Tankosic, P., & Atkinson, J. (1995). Aortic stiffness and left ventricular mass in a rat model of isolated systolic hypertension. Hypertension, 26(6 Pt 1), 963–970.PubMedGoogle Scholar
  65. 65.
    Ng, K., Hildreth, C. M., Avolio, A. P., & Phillips, J. K. (2011). Angiotensin-converting enzyme inhibitor limits pulse-wave velocity and aortic calcification in a rat model of cystic renal disease. American Journal of Physiology. Renal Physiology, 301(5), F959–F966. doi: 10.1152/ajprenal.00393.2011.PubMedCrossRefGoogle Scholar
  66. 66.
    Schurgers, L. J., Spronk, H. M., Soute, B. A., Schiffers, P. M., DeMey, J. G., & Vermeer, C. (2007). Regression of warfarin-induced medial elastocalcinosis by high intake of vitamin K in rats. Blood, 109(7), 2823–2831. doi: 10.1182/blood-2006-07-035345.PubMedGoogle Scholar
  67. 67.
    Gaillard, V., Casellas, D., Seguin-Devaux, C., Schohn, H., Dauca, M., Atkinson, J., & Lartaud, I. (2005). Pioglitazone improves aortic wall elasticity in a rat model of elastocalcinotic arteriosclerosis. Hypertension, 46(2), 372–379. doi: 10.1161/01.HYP.0000171472.24422.33.PubMedCrossRefGoogle Scholar
  68. 68.
    Bouvet, C., Moreau, S., Blanchette, J., de Blois, D., & Moreau, P. (2008). Sequential activation of matrix metalloproteinase 9 and transforming growth factor beta in arterial elastocalcinosis. Arteriosclerosis, Thrombosis, and Vascular Biology, 28(5), 856–862. doi: 10.1161/ATVBAHA.107.153056.PubMedCrossRefGoogle Scholar
  69. 69.
    Tang, S. S., Trackman, P. C., & Kagan, H. M. (1983). Reaction of aortic lysyl oxidase with beta-aminopropionitrile. Journal of Biological Chemistry, 258(7), 4331–4338.PubMedGoogle Scholar
  70. 70.
    Mercier, N., Kakou, A., Challande, P., Lacolley, P., & Osborne-Pellegrin, M. (2009). Comparison of the effects of semicarbazide and beta-aminopropionitrile on the arterial extracellular matrix in the Brown Norway rat. Toxicology and Applied Pharmacology, 239(3), 258–267. doi: 10.1016/j.taap.2009.06.005.PubMedCrossRefGoogle Scholar
  71. 71.
    Ooshima, A., & Midorikawa, O. (1977). Increased lysyl oxidase activity in blood vessels of hypertensive rats and effect of beta-aminopropionitrile on arteriosclerosis. Japanese Circulation Journal, 41(12), 1337–1340.PubMedCrossRefGoogle Scholar
  72. 72.
    Corman, B., Duriez, M., Poitevin, P., Heudes, D., Bruneval, P., Tedgui, A., & Levy, B. I. (1998). Aminoguanidine prevents age-related arterial stiffening and cardiac hypertrophy. Proceedings of the National Academy of Sciences of the United States of America, 95(3), 1301–1306.PubMedCrossRefGoogle Scholar
  73. 73.
    Lansing, A. I., Rosenthal, T. B., Alex, M., & Dempsey, E. W. (1952). The structure and chemical characterization of elastic fibers as revealed by elastase and by electron microscopy. The Anatomical Record, 114(4), 555–575.PubMedCrossRefGoogle Scholar
  74. 74.
    Starcher, B. (2001). A ninhydrin-based assay to quantitate the total protein content of tissue samples. Analytical Biochemistry, 292(1), 125–129. doi: 10.1006/abio.2001.5050.PubMedCrossRefGoogle Scholar
  75. 75.
    Long, J. L., & Tranquillo, R. T. (2003). Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biology, 22(4), 339–350.PubMedCrossRefGoogle Scholar
  76. 76.
    Starcher, B. C. (1977). Determination of the elastin content of tissues by measuring desmosine and isodesmosine. Analytical Biochemistry, 79(1–2), 11–15.PubMedCrossRefGoogle Scholar
  77. 77.
    Starcher, B. C., & Mecham, R. P. (1981). Desmosine radioimmunoassay as a means of studying elastogenesis in cell culture. Connective Tissue Research, 8(3–4), 255–258.PubMedCrossRefGoogle Scholar
  78. 78.
    Nonaka, R., Onoue, S., Wachi, H., Sato, F., Urban, Z., Starcher, B. C., & Seyama, Y. (2009). DANCE/fibulin-5 promotes elastic fiber formation in a tropoelastin isoform-dependent manner. Clinical Biochemistry, 42(7–8), 713–721. doi: 10.1016/j.clinbiochem.2008.12.020.PubMedCrossRefGoogle Scholar
  79. 79.
    Mecham, R. P. (2008). Methods in elastic tissue biology: Elastin isolation and purification. Methods, 45(1), 32–41. doi: 10.1016/j.ymeth.2008.01.007.PubMedCrossRefGoogle Scholar
  80. 80.
    Cox, R. H. (1983). Comparison of arterial wall mechanics using ring and cylindrical segments. American Journal of Physiology, 244(2), H298–H303.PubMedGoogle Scholar
  81. 81.
    Okamoto, R. J., Wagenseil, J. E., DeLong, W. R., Peterson, S. J., Kouchoukos, N. T., & Sundt, T. M., 3rd. (2002). Mechanical properties of dilated human ascending aorta. Annals of Biomedical Engineering, 30(5), 624–635.PubMedCrossRefGoogle Scholar
  82. 82.
    Gleason, R. L., Gray, S. P., Wilson, E., & Humphrey, J. D. (2004). A multiaxial computer-controlled organ culture and biomechanical device for mouse carotid arteries. Journal of Biomechanical Engineering, 126(6), 787–795.PubMedCrossRefGoogle Scholar
  83. 83.
    Jackson, Z. S., Gotlieb, A. I., & Langille, B. L. (2002). Wall tissue remodeling regulates longitudinal tension in arteries. Circulation Research, 90(8), 918–925.PubMedCrossRefGoogle Scholar
  84. 84.
    Eberth, J. F., Taucer, A. I., Wilson, E., & Humphrey, J. D. (2009). Mechanics of carotid arteries in a mouse model of Marfan Syndrome. Annals of Biomedical Engineering, 37(6), 1093–1104. doi: 10.1007/s10439-009-9686-1.PubMedCrossRefGoogle Scholar
  85. 85.
    Oliver, J. J., & Webb, D. J. (2003). Noninvasive assessment of arterial stiffness and risk of atherosclerotic events. Arteriosclerosis, Thrombosis, and Vascular Biology, 23(4), 554–566. doi: 10.1161/01.ATV.0000060460.52916.D6.PubMedCrossRefGoogle Scholar
  86. 86.
    Hartley, C. J., Reddy, A. K., Madala, S., Entman, M. L., Michael, L. H., & Taffet, G. E. (2011). Doppler velocity measurements from large and small arteries of mice. American Journal of Physiology - Heart and Circulatory Physiology, 301(2), H269–H278. doi: 10.1152/ajpheart.00320.2011.PubMedCrossRefGoogle Scholar
  87. 87.
    Carta, L., Wagenseil, J. E., Knutsen, R. H., Mariko, B., Faury, G., Davis, E. C., Starcher, B., Mecham, R. P., & Ramirez, F. (2009). Discrete contributions of elastic fiber components to arterial development and mechanical compliance. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(12), 2083–2089. doi: 10.1161/ATVBAHA.109.193227.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringSaint Louis UniversitySt. LouisUSA
  2. 2.Department of Cell Biology and PhysiologyWashington UniversitySt. LouisUSA

Personalised recommendations