Decreased Elastic Energy Storage, Not Increased Material Stiffness, Characterizes Central Artery Dysfunction in Fibulin-5 Deficiency Independent of Sex

Journal of Biomechanical Engineering

Volumn 137, Issue 3, 2015, Pages

  Ferruzzi, J ^a   Bersi, M R ^a   Uman, S ^a   Yanagisawa, H ^b   Humphrey, J D ^a,c  

^a Yale University   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

aorta; biaxial stiffness; carotid; energy dissipation; regional variations; stress

Indexed keywords

BLOOD VESSELS; ELASTICITY; ENERGY DISSIPATION; ENERGY STORAGE; GLYCOPROTEINS; MAMMALS; STIFFNESS; STRESSES;

AORTA; ARTERIAL WALL MECHANICS; BIAXIAL MECHANICAL PROPERTIES; CARDIOVASCULAR FUNCTION; CAROTID; COMMON CAROTID ARTERY; ELASTIC ENERGY STORAGE; REGIONAL VARIATION;

ELASTIN;

ELASTIN; FIBULIN 5; GLYCOPROTEIN; FBLN5 PROTEIN, MOUSE; RECOMBINANT PROTEIN; SCLEROPROTEIN;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ARTERIAL STIFFNESS; ARTICLE; ASCENDING AORTA; BIOMECHANICS; COMMON CAROTID ARTERY; CONTROLLED STUDY; DIASTOLE; ELASTIC FIBER; ENERGY; FEMALE; GENOTYPE; HEART FUNCTION; HEMODYNAMICS; MALE; MOUSE; NONHUMAN; STORAGE; SYSTOLE; THORACIC AORTA; ANIMAL; ARTERY; CYTOLOGY; DEFICIENCY; ELASTICITY; METABOLISM; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; ARTERIES; ELASTICITY; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENOTYPE; MALE; MICE; PHENOTYPE; RECOMBINANT PROTEINS; SEX CHARACTERISTICS; VASCULAR STIFFNESS;

EID: 84937633211     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4029431     Document Type: Article

References (60)

1. Yanagisawa, H., and Davis, E. C., 2010, "Unraveling the Mechanism of Elastic Fiber Assembly: The Roles of Short Fibulins," Int. J. Biochem. Cell Biol., 42(7), pp. 1084-1093.
2. Ramirez, F., and Dietz, H. C., 2007, "Fibrillin-Rich Microfibrils: Structural Determinants of Morphogenetic and Homeostatic Events," J. Cell. Physiol., 213(2), pp. 326-330.
3. Huang, J., Davis, E. C., Chapman, S. L., Budatha, M., Marmorstein, L. Y., Word, R. A., and Yanagisawa, H., 2010, "Fibulin-4 Deficiency Results in Ascending Aortic Aneurysms: A Potential Link Between Abnormal Smooth Muscle Cell Phenotype and Aneurysm Progression," Circ. Res., 106(3), pp. 583-592.
4. Nakamura, T., Lozano, P. R., Ikeda, Y., Iwanaga, Y., Hinek, A., Minamisawa, S., Cheng, C.-F., Kobuke, K., Dalton, N., Takada, Y., Tashiro, K., Ross, J., Jr., Honjo, T., and Chien, K. R., 2002, "Fibulin-5/DANCE is Essential for Elastogenesis In Vivo," Nature, 415(6868), pp. 171-175.
5. Yanagisawa, H., Davis, E. C., Starcher, B. C., Ouchi, T., Yanagisawa, M., Richardson, J. A., and Olson, E. N., 2002, "Fibulin-5 is an Elastin-Binding Protein Essential for Elastic Fibre Development In Vivo," Nature, 415(6868), pp. 168-171.
6. Yanagisawa, H., Schluterman, M. K., and Brekken, R. A., 2009, "Fibulin-5, an Integrin-Binding Matricellular Protein: Its Function in Development and Disease," J. Cell Commun. Signalling, 3(3-4), pp. 337-347.
7. Spencer, J. A., Hacker, S. L., Davis, E. C., Mecham, R. P., Knutsen, R. H., Li, D. Y., Gerard, R. D., Richardson, J. A., Olson, E. N., and Yanagisawa, H., 2005, "Altered Vascular Remodeling in Fibulin-5-Deficient Mice Reveals a Role of Fibulin-5 in Smooth Muscle Cell Proliferation and Migration," Proc. Natl. Acad. Sci. USA, 102(8), pp. 2946-2951.
8. Wan, W., Yanagisawa, H., and Gleason, R. L., Jr., 2010, "Biomechanical and Microstructural Properties of Common Carotid Arteries From Fibulin-5 Null Mice," Ann. Biomed. Eng., 38(12), pp. 3605-3617.
9. Wan, W., and Gleason, R. L., 2013, "Dysfunction in Elastic Fiber Formation in Fibulin-5 Null Mice Abrogates the Evolution in Mechanical Response of Carotid Arteries During Maturation," Am. J. Physiol.: Heart Circ. Physiol., 304(5), pp. H674-H686.
10. Boutouyrie, P., Laurent, S., and Briet, M., 2008, "Importance of Arterial Stiffness as Cardiovascular Risk Factor for Future Development of New Type of Drugs," Fundam. Clin. Pharmacol., 22(3), pp. 241-246.
11. Adji, A., O'Rourke, M. F., and Namasivayam, M., 2011, "Arterial Stiffness, Its Assessment, Prognostic Value, and Implications for Treatment," Am. J. Hypertens., 24(1), pp. 5-17.
12. Najjar, S. S., Scuteri, A., Shetty, V., Wright, J. G., Muller, D. C., Fleg, J. L., Spurgeon, H. P., Ferrucci, L., and Lakatta, E. G., 2008, "Pulse Wave Velocity is an Independent Predictor of the Longitudinal Increase in Systolic Blood Pressure and of Incident Hypertension in the Baltimore Longitudinal Study of Aging," J. Am. Coll. Cardiol., 51(14), pp. 1377-1383.
13. Wang, K.-L., Cheng, H.-M., Sung, S.-H., Chuang, S.-Y., Li, C.-H., Spurgeon, H. A., Ting, C.-T., Najjar, S. S., Lakatta, E. G., Yin, F. C. P., Chou, P., and Chen, C.-H., 2010, "Wave Reflection and Arterial Stiffness in the Prediction of 15-Year All-Cause and Cardiovascular Mortalities: A Community-Based Study," Hypertension, 55(3), pp. 799-805.
14. Agabiti-Rosei, E., Mancia, G., O'Rourke, M. F., Roman, M. J., Safar, M. E., Smulyan, H., Wang, J.-G., Wilkinson, I. B., Williams, B., and Vlachopoulos, C., 2007, "Central Blood Pressure Measurements and Antihypertensive Therapy: A Consensus Document," Hypertension, 50(1), pp. 154-160.
15. Lakatta, E. G., Wang, M., and Najjar, S. S., 2009, "Arterial Aging and Subclinical Arterial Disease are Fundamentally Intertwined at Macroscopic and Molecular Levels," Med. Clin. N. Am., 93(3), pp. 583-604.
16. Safar, M. E., 2010, "Arterial Aging - Hemodynamic Changes and Therapeutic Options," Nat. Rev. Cardiol., 7(8), pp. 442-449.
17. Sugawara, J., Hayashi, K., Yokoi, T., and Tanaka, H., 2008, "Age-Associated Elongation of the Ascending Aorta in Adults," JACC Cardiovasc. Imaging, 1(6), pp. 739-748.
18. Hickson, S. S., Butlin, M., Graves, M., Taviani, V., Avolio, A. P., McEniery, C. M., and Wilkinson, I. B., 2010, "The Relationship of Age With Regional Aortic Stiffness and Diameter," JACC Cardiovasc. Imaging, 3(12), pp. 1247-1255.
19. Redheuil, A., Yu, W.-C., Wu, C. O., Mousseaux, E., Cesare, A., de, Yan, R., Kachenoura, N., Bluemke, D., and Lima, J. A. C., 2010, "Reduced Ascending Aortic Strain and Distensibility: Earliest Manifestations of Vascular Aging in Humans," Hypertension, 55(2), pp. 319-326.
20. O'Rourke, M. F., and Hashimoto, J., 2007, "Mechanical Factors in Arterial Aging: A Clinical Perspective," J. Am. Coll. Cardiol., 50(1), pp. 1-13.
21. Lacolley, P., Challande, P., Osborne-Pellegrin, M., and Regnault, V., 2009, "Genetics and Pathophysiology of Arterial Stiffness," Cardiovasc. Res., 81(4), pp. 637-648.
22. Wagenseil, J. E., and Mecham, R. P., 2012, "Elastin in Large Artery Stiffness and Hypertension," J. Cardiovasc. Transl. Res., 5(3), pp. 264-273.
23. Rachev, A., Greenwald, S., and Shazly, T., 2013, "Are Geometrical and Structural Variations Along the Length of the Aorta Governed by a Principle of 'Optimal Mechanical Operation'?," ASME J. Biomech. Eng., 135(8), p. 081006.
24. Roccabianca, S., Figueroa, C. A., Tellides, G., and Humphrey, J. D., 2014, "Quantification of Regional Differences in Aortic Stiffness in the Aging Human," J. Mech. Behav. Biomed. Mater., 29(1), pp. 618-634.
25. Daugherty, A., Rateri, D., Hong, L., and Balakrishnan, A., 2009, "Measuring Blood Pressure in Mice Using Volume Pressure Recording, a Tail-Cuff Method," J. Vis. Exp., (27).
26. Gleason, R. L., Wilson, E., Humphrey, J. D., and Gray, S. P., 2005, "A Multiaxial Computer-Controlled Organ Culture and Biomechanical Device for Mouse Carotid Arteries," ASME J. Biomech. Eng., 126(6), pp. 787-795.
27. Ferruzzi, J., Bersi, M. R., and Humphrey, J. D., 2013, "Biomechanical Phenotyping of Central Arteries in Health and Disease: Advantages of and Methods for Murine Models," Ann. Biomed. Eng., 41(7), pp. 1311-1330.
28. Bersi, M. R., Ferruzzi, J., Eberth, J. F., Gleason, R. L., and Humphrey, J. D., 2014, "Consistent Biomechanical Phenotyping of Common Carotid Arteries From Seven Genetic, Pharmacological, and Surgical Mouse Models," Ann. Biomed. Eng., 42(6), pp. 1207-1223.
29. Gleason, R. L., Dye, W. W., Wilson, E., and Humphrey, J. D., 2008, "Quantification of the Mechanical Behavior of Carotid Arteries From Wild-Type, Dystrophin-Deficient, and Sarcoglycan-d Knockout Mice," J. Biomech., 41(15), pp. 3213-3218.
30. Eberth, J. F., Taucer, A. I., Wilson, E., and Humphrey, J. D., 2009, "Mechanics of Carotid Arteries in a Mouse Model of Marfan Syndrome," Ann. Biomed. Eng., 37(6), pp. 1093-1104.
31. Ferruzzi, J., Collins, M. J., Yeh, A. T., and Humphrey, J. D., 2011, "Mechanical Assessment of Elastin Integrity in Fibrillin-1-Deficient Carotid Arteries: Implications for Marfan Syndrome," Cardiovasc. Res., 92(2), pp. 287-295.
32. Bersi, M. R., Collins, M. J., Wilson, E., and Humphrey, J. D., 2012, "Disparate Changes in the Mechanical Properties of Murine Carotid Arteries and Aorta in Response to Chronic Infusion of Angiotensin-II," Int. J. Adv. Eng. Sci. Appl. Math., 4(4), pp. 228-240.
33. Humphrey, J. D., 2002, Cardiovascular Solid Mechanics: Cells, Tissues, and Organs, Springer, New York.
34. Ferruzzi, J., Vorp, D. A., and Humphrey, J. D., 2011, "On Constitutive Descriptors of the Biaxial Mechanical Behaviour of Human Abdominal Aorta and Aneurysms," J. R. Soc. Interface, 8(56), pp. 435-450.
35. Baek, S., Gleason, R. L., Rajagopal, K. R., and Humphrey, J. D., 2007, "Theory of Small on Large: Potential Utility in Computations of Fluid-Solid Interactions in Arteries," Comput. Methods Appl. Mech. Eng., 196(31-32), pp. 3070-3078.
36. Warriner, R. K., Johnston, K. W., and Cobbold, R. S. C., 2008, "A Viscoelastic Model of Arterial Wall Motion in Pulsatile Flow: Implications for Doppler Ultrasound Clutter Assessment," Physiol. Meas., 29(2), pp. 157-159.
37. Wight, T. N., 1989, "Cell Biology of Arterial Proteoglycans," Arterioscler. Thromb. Vasc. Biol., 9(1), pp. 1-20.
38. Merrilees, M. J., Tiang, K. M., and Scott, L., 1987, "Changes in Collagen Fibril Diameters Across Artery Walls Including a Correlation With Glycosaminoglycan Content," Connect. Tissue Res., 16(3), pp. 237-257.
39. Rezakhaniha, R., Agianniotis, A., Schrauwen, J. T. C., Griffa, A., Sage, D., Bouten, C. V. C., van de Vosse, F. N., Unser, M., and Stergiopulos, N., 2012, "Experimental Investigation of Collagen Waviness and Orientation in the Arterial Adventitia Using Confocal Laser Scanning Microscopy," Biomech. Model. Mechanobiol., 11(3-4), pp. 461-473.
40. Crawley, M. J., 2012, The R Book, Wiley, Chichester, UK.
41. Arribas, S. M., Hinek, A., and González, M. C., 2006, "Elastic Fibres and Vascular Structure in Hypertension," Pharmacol. Ther., 111(3), pp. 771-791.
42. Karnik, S. K., Brooke, B. S., Bayes-Genis, A., Sorensen, L., Wythe, J. D., Schwartz, R. S., Keating, M. T., and Li, D. Y., 2003, "A Critical Role for Elastin Signaling in Vascular Morphogenesis and Disease," Development, 130(2), pp. 411-423.
43. Carta, L., Wagenseil, J. E., Knutsen, R. H., Mariko, B., Faury, G., Davis, E. C., Starcher, B., Mecham, R. P., and Ramirez, F., 2009, "Discrete Contributions of Elastic Fiber Components to Arterial Development and Mechanical Compliance," Arterioscler. Thromb. Vasc. Biol., 29(12), pp. 2083-2089.
44. Wagenseil, J. E., Nerurkar, N. L., Knutsen, R. H., Okamoto, R. J., Li, D. Y., and Mecham, R. P., 2005, "Effects of Elastin Haploinsufficiency on the Mechanical Behavior of Mouse Arteries," Am. J. Physiol.: Heart Circ. Physiol., 289(3), pp. H1209-H1217.
45. Eberth, J. F., Gresham, V. C., Reddy, A. K., Popovic, N., Wilson, E., and Humphrey, J. D., 2009, "Importance of Pulsatility in Hypertensive Carotid Artery Growth and Remodeling," J. Hypertens., 27(10), pp. 2010-2021.
46. Humphrey, J. D., Eberth, J. F., Dye, W. W., and Gleason, R. L., 2009, "Fundamental Role of Axial Stress in Compensatory Adaptations by Arteries," J. Biomech., 42(1), pp. 1-8.
47. Truesdell, C., and Noll, W., 2004, The Non-Linear Field Theories of Mechanics, Springer, Berlin, Germany.
48. Eberth, J. F., Cardamone, L., and Humphrey, J. D., 2011, "Evolving Biaxial Mechanical Properties of Mouse Carotid Arteries in Hypertension," J. Biomech., 44(14), pp. 2532-2537.
49. Humphrey, J. D., 2008, "Vascular Adaptation and Mechanical Homeostasis at Tissue, Cellular, and Sub-Cellular Levels," Cell Biochem. Biophys., 50(2), pp. 53-78.
50. Tanaka, T. T., and Fung, Y.-C., 1974, "Elastic and Inelastic Properties of the Canine Aorta and Their Variation Along the Aortic Tree," J. Biomech., 7(4), pp. 357-370.
51. Sokolis, D. P., 2007, "Passive Mechanical Properties and Structure of the Aorta: Segmental Analysis," Acta Physiol., 190(4), pp. 277-289.
52. Sokolis, D. P., Boudoulas, H., and Karayannacos, P. E., 2008, "Segmental Differences of Aortic Function and Composition: Clinical Implications," Hell. J. Cardiol., 49(3), pp. 145-154, available at: http://www.hellenicjcardiol.com/archive/full-text/2008/3/2008-3-145.pdf
53. Zhao, J., Day, J., Yuan, Z. F., and Gregersen, H., 2002, "Regional Arterial Stress-Strain Distributions Referenced to the Zero-Stress State in the Rat," Am. J. Physiol.: Heart Circ. Physiol., 282(2), pp. H622-H629.
54. Guo, X., and Kassab, G. S., 2003, "Variation of Mechanical Properties Along the Length of the Aorta in C57bl/6 Mice," Am. J. Physiol.: Heart Circ. Physiol., 285(6), pp. H2614-H2622.
55. 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., and Mecham, R. P., 2003, "Developmental Adaptation of the Mouse Cardiovascular System to Elastin Haploinsufficiency," J. Clin. Invest., 112(9), pp. 1419-1428.
56. Wagenseil, J. E., and Mecham, R. P., 2009, "Vascular Extracellular Matrix and Arterial Mechanics," Physiol. Rev., 89(3), pp. 957-989.
57. Han, H.-C., and Fung, Y.-C., 1995, "Longitudinal Strain of Canine and Porcine Aortas," J. Biomech., 28(5), pp. 637-641.
58. Beller, C. J., Labrosse, M. R., Thubrikar, M. J., and Robicsek, F., 2004, "Role of Aortic Root Motion in the Pathogenesis of Aortic Dissection," Circulation, 109(6), pp. 763-769.
59. Jin, S., Oshinski, J., and Giddens, D. P., 2003, "Effects of Wall Motion and Compliance on Flow Patterns in the Ascending Aorta," ASME J. Biomech. Eng., 125(3), pp. 347-354.
60. Labrosse, M. R., Gerson, E. R., Veinot, J. P., and Beller, C. J., 2013, "Mechanical Characterization of Human Aortas From Pressurization Testing and a Paradigm Shift for Circumferential Residual Stress," J. Mech. Behav. Biomed. Mater., 17, pp. 44-55.