Heterogeneous transmural proteoglycan distribution provides a mechanism for regulating residual stresses in the aorta

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 3, 2008, Pages

  Azeloglu, Evren U ^a   Albro, Michael B ^a   Thimmappa, Vikrum A ^a   Ateshian, Gerard A ^a   Costa, Kevin D ^a  

^a Columbia University ^*  (United States)

Author keywords

Glycosaminoglycans; Vascular mechanics; Zero stress

Indexed keywords

GLYCOSAMINOGLYCAN; PROTEOGLYCAN; SODIUM CHLORIDE; SUCROSE;

ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTERY WALL; ARTICLE; CELL HETEROGENEITY; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; FINITE ELEMENT ANALYSIS; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HEART VENTRICLE WALL; IONIC STRENGTH; MALE; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; PROTEOGLYCAN SYNTHESIS; RAT; REGULATORY MECHANISM; SURFACE CHARGE; THREE DIMENSIONAL IMAGING; VASCULAR RING;

ALGORITHMS; ANIMALS; AORTA, THORACIC; FINITE ELEMENT ANALYSIS; GLYCOSAMINOGLYCANS; MALE; OSMOLAR CONCENTRATION; POISSON DISTRIBUTION; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; STRESS;

EID: 41549130765     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01027.2007     Document Type: Article

References (57)

1. Ateshian GA, Chahine NO, Basalo IM, Hung CT. The correspondence between equilibrium biphasic and triphasic material properties in mixture models of articular cartilage. J Biomech 37: 391-400, 2004.
2. Ateshian GA, Ellis BJ, Weiss JA. Equivalence between short-time biphasic and incompressible elastic material responses. J Biomech Eng 129: 405, 2007.
3. Bonet J, Wood RD. Nonlinear Continuum Mechanics for Finite Element Analysis. Cambridge, UK: Cambridge Univ. Press, 1997, p. xvii, 248.
4. Chahine NO, Chen FH, Hung CT, Ateshian GA. Direct measurement of osmotic pressure of glycosaminoglycan solutions by membrane osmometry at room temperature. Biophys J 89: 1543-1550, 2005.
5. Chang Y, Yanagishita M, Hascall VC, Wight TN. Proteoglycans synthesized by smooth muscle cells derived from monkey (Macaca nemestrina) aorta. J Biol Chem 258: 5679-5688, 1983.
6. Chao PG, Tang Z, Angelini E, West AC, Costa KD, Hung CT. Dynamic osmotic loading of chondrocytes using a novel microfluidic device. J Biomech 38: 1273-1281, 2005.
7. Chen K, Wight TN. Proteoglycans in arterial smooth muscle cell cultures: an ultrastructural histochemical analysis. J Histochem Cytochem 32: 347-357, 1984.
8. Chuong CJ, Fung YC. On residual stresses in arteries. J Biomech Eng 108: 189-192, 1986.
9. Clowes AW, Clowes MM, Gown AM, Wight TN. Localization of proteoheparan sulfate in rat aorta. Histochemistry 80: 379-384, 1984.
10. Curnier A, He QC, Zysset P. Conewise linear elastic materials. J Elasticity 37: 1-38, 1995.
11. Deng SX, Tomioka J, Debes JC, Fung YC. New experiments on shear modulus of elasticity of arteries. Am J Physiol Heart Circ Physiol 266: H1-H10, 1994.
12. Ehrlich S, Wolff N, Schneiderman R, Maroudas A, Parker KH, Winlove CP. The osmotic pressure of chondroitin sulphate solutions: experimental measurements and theoretical analysis. Biorheology 35: 383-397, 1998.
13. Evanko SP, Johnson PY, Braun KR, Underhill CB, Dudhia J, Wight TN. Platelet-derived growth factor stimulates the formation of versican-hyaluronan aggregates and pericellular matrix expansion in arterial smooth muscle cells. Arch Biochem Biophys 394: 29-38, 2001.
14. Evanko SP, Raines EW, Ross R, Gold LI, Wight TN. Proteoglycan distribution in lesions of atherosclerosis depends on lesion severity, structural characteristics, and the proximity of platelet-derived growth factor and transforming growth factor-β. Am J Pathol 152: 533-546, 1998.
15. Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res 9: 247-248, 1982.
16. Fung YC. Biomechanics: Motion, Flow, Stress, Growth. New York: Springer-Verlag, 1990, p. xii, 569.
17. Greenwald SE, Moore JE Jr, Rachev A, Kane TP, Meister JJ. Experimental investigation of the distribution of residual strains in the artery wall. J Biomech Eng 119: 438-444, 1997.
18. Grodzinsky AJ. Electromechanical and physicochemical properties of connective tissue. Crit Rev Biomed Eng 9: 133-199, 1983.
19. Guo X, Kassab GS. Variation of mechanical properties along the length of the aorta in C57bl/6 mice. Am J Physiol Heart Circ Physiol 285: H2614-H2622, 2003.
20. Guo X, Lanir Y, Kassab GS. Effect of osmolarity on the zero-stress state and mechanical properties of aorta in various species. Am J Physiol Heart Circ Physiol 293: H2328-H2334, 2007.
21. Heegaard AM, Corsi A, Danielsen CC, Nielsen KL, Jorgensen HL, Riminucci M, Young MF, Bianco P. Biglycan deficiency causes spontaneous aortic dissection and rupture in mice. Circulation 115: 2731-2738, 2007.
22. Humphrey JD. Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. New York: Springer-Verlag, 2002, p. xvi, 757.
23. Kang T, Yin FC. The need to account for residual strains and composite nature of heart wall in mechanical analyses. Am J Physiol Heart Circ Physiol 271: H947-H961, 1996.
24. Kapoor R, Phelps CF, Wight TN. Physical properties of chondroitin sulphate/dermatan sulphate proteoglycans from bovine aorta. Biochem J 240: 575-583, 1986.
25. Kinsella MG, Wight TN. Formation of high molecular weight dermatan sulfate proteoglycan in bovine aortic endothelial cell cultures. Evidence for transglutaminase-catalyzed cross-linking to fibronectin. J Biol Chem 265: 17891-17898, 1990.
26. Kinsella MG, Wight TN. Modulation of sulfated proteoglycan synthesis by bovine aortic endothelial cells during migration. J Cell Biol 102: 679-687, 1986.
27. Kinsella MG, Wight TN. Structural characterization of heparan sulfate proteoglycan subclasses isolated from bovine aortic endothelial cell cultures. Biochemistry 27: 2136-2144, 1988.
28. Lai WM, Hou JS, Mow VC. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113: 245-258, 1991.
29. Lanir Y, Hayam G, Abovsky M, Zlotnick AY, Uretzky G, Nevo E, Ben-Haim SA. Effect of myocardial swelling on residual strain in the left ventricle of the rat. Am J Physiol Heart Circ Physiol 270: H1736-H1743, 1996.
30. Liu SQ, Fung YC. Changes in the structure and mechanical properties of pulmonary arteries of rats exposed to cigarette smoke. Am Rev Respir Dis 148: 768-777, 1993.
31. Liu SQ, Fung YC. Relationship between hypertension, hypertrophy, and opening angle of zero-stress state of arteries following aortic constriction. J Biomech Eng 111: 325-335, 1989.
32. Lu X, Zhao JB, Wang GR, Gregersen H, Kassab GS. Remodeling of the zero-stress state of femoral arteries in response to flow overload. Am J Physiol Heart Circ Physiol 280: H1547-H1559, 2001.
33. Maroudas AI. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 260: 808-809, 1976.
34. Matsumoto T, Hayashi K. Stress and strain distribution in hypertensive and normotensive rat aorta considering residual strain. J Biomech Eng 118: 62-73, 1996.
35. Mow VC, Ratcliffe A. Structure and function of articular cartilage and meniscus. In: Basic Orthopaedic Biomechanics, edited by Mow VC, Hayes WC. Philadelphia, PA: Lippincott-Raven, 1997, p. 113-177.
36. Overbeek JT. The Donnan equilibrium. Prog Biophys Biophys Chem 6: 57-84, 1956.
37. Porterfield SP, Calhoon TB, Weiss HS. Changes in connective tissue colloidal charge density with atherosclerosis and age. J Physiol 215: 324-329, 1968.
38. Rachev A, Greenwald SE. Residual strains in conduit arteries. J Biomech 36: 661-670, 2003.
39. Reynertson RH, Parmley RT, Roden L, Oparil S. Proteoglycans and hypertension. I. A biochemical and ultrastructural study of aorta glycosaminoglycans in spontaneously hypertensive rats. Coll Relat Res 6: 77-101, 1986.
40. Riessen R, Isner JM, Blessing E, Loushin C, Nikol S, Wight TN. Regional differences in the distribution of the proteoglycans biglycan and decorin in the extracellular matrix of atherosclerotic and restenotic human coronary arteries. Am J Pathol 144: 962-974, 1994.
41. Rodriguez EK, Hoger A, McCulloch AD. Stress-dependent finite growth in soft elastic tissues. J Biomech 27: 455-467, 1994.
42. Ruigrok YM, Rinkel GJ, Wijmenga C. The versican gene and the risk of intracranial aneurysms. Stroke 37: 2372-2374, 2006.
43. Saini A, Berry C, Greenwald S. Effect of age and sex on residual stress in the aorta. J Vasc Res 32: 398-405, 1995.
44. Seibel MJ, Macaulay W, Jelsma R, Saed-Nejad F, Ratcliffe A. Antigenic properties of keratan sulfate: influence of antigen structure, monoclonal antibodies, and antibody valency. Arch Biochem Biophys 296: 410-418, 1992.
45. Setton LA, Tohyama H, Mow VC. Swelling and curling behaviors of articular cartilage. J Biomech Eng 120: 355-361, 1998.
46. Skalak R, Dasgupta G, Moss M, Otten E, Dullumeijer P, Vilmann H. Analytical description of growth. J Theor Biol 94: 555-577, 1982.
47. Taber LA. Biomechanics of growth, remodeling, and morphogenesis. Appl Mech Rev 48: 487, 1995.
48. Taber LA, Humphrey JD. Stress-modulated growth, residual stress, and vascular heterogeneity. J Biomech Eng 123: 528-535, 2001.
49. Takamizawa K, Hayashi K. Strain energy density function and uniform strain hypothesis for arterial mechanics. J Biomech 20: 7-17, 1987.
50. Tong P, Fung YC. The stress-strain relationship for the skin. J Biomech 9: 649-657, 1976.
51. Velleman SG, Bacon W, Whitmoyer R, Hosso SJ. Changes in distribution of glycosaminoglycans during the progression of cholesterol induced atherosclerosis in Japanese quail. Atherosclerosis 137: 63-70, 1998.
52. Vijayagopal P, Figueroa JE, Fontenot JD, Glancy DL. Isolation and characterization of a proteoglycan variant from human aorta exhibiting a marked affinity for low density lipoprotein and demonstration of its enhanced expression in atherosclerotic plaques. Atherosclerosis 127: 195-203, 1996.
53. Volker W, Schmidt A, Oortmann W, Broszey T, Faber V, Buddecke E. Mapping of proteoglycans in atherosclerotic lesions. Eur Heart J 11, Suppl E: 29-40, 1990.
54. Wagenseil JE, Nerurkar NL, Knutsen RH, Okamoto RJ, Li DY, Mecham RP. Effects of elastin haploinsufficiency on the mechanical behavior of mouse arteries. Am J Physiol Heart Circ Physiol 289: H1209-H1217, 2005.
55. Weiss TF. Cellular Biophysics. Cambridge, MA: MIT, 1996, p. v.
56. Wight TN. Vessel proteoglycans and thrombogenesis. Prog Hemost Thromb 5: 1-39, 1980.
57. Yao LY, Moody C, Schonherr E, Wight TN, Sandell LJ. Identification of the proteoglycan versican in aorta and smooth muscle cells by DNA sequence analysis, in situ hybridization and immunohistochemistry. Matrix Biol 14: 213-225, 1994.