Matrix metalloproteinase-2 and -9 are associated with high stresses predicted using a nonlinear heterogeneous model of arteries

Journal of Biomechanical Engineering

Volumn 131, Issue 1, 2009, Pages

  Kim, Yu Shin ^a   Galis, Zorina S ^b   Rachev, Alexander ^a   Han, Hai Chao ^c   Vito, Raymond P ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c The University of Texas at San Antonio   (United States)

Author keywords

Blood vessels; Matrix metalloproteinase; Modeling; Vascular remodeling; Vascular smooth muscle cells

Indexed keywords

ARTERIAL WALL; CAROTID ARTERY; CIRCUMFERENTIAL STRESS; COLLAGEN FIBER; COMMON CAROTID ARTERY; EX-VIVO; FIBER STRAIN; HELICAL ANGLE; HETEROGENEOUS MODELS; HIGH STRESS; HOMOGENEOUS MODELS; IN-SITU; LOAD BEARING; LOCAL STRESS; LOWER STRESS; MATRIX METALLOPROTEINASE-2; MATRIX METALLOPROTEINASES; MECHANICAL ENVIRONMENT; MECHANICAL MODEL; MECHANICAL STRESS; MORPHOLOGICAL MEASUREMENTS; NON-LINEARITY; NON-UNIFORMITIES; ORGAN CULTURE SYSTEM; OUTER LAYER; PHYSIOLOGICAL CONDITION; PHYSIOLOGICAL LOADINGS; RESIDUAL STRAINS; STRUCTURAL HETEROGENEITY; TISSUE LEVELS; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELLS;

ANISOTROPY; BLOOD; BLOOD VESSEL PROSTHESES; BLOOD VESSELS; CELL CULTURE; CELLS; COLLAGEN; ELASTICITY; ENZYME INHIBITION; FIBERS; IMAGE SEGMENTATION; MUSCLE; STRAIN; STRESSES; WALLS (STRUCTURAL PARTITIONS);

PHYSIOLOGICAL MODELS;

COLLAGEN FIBER; ELASTIN; GELATINASE A; GELATINASE B;

ANIMAL TISSUE; ANISOTROPY; ARTERY; ARTERY MEDIA; ARTERY WALL; ARTICLE; BIOMECHANICS; CAROTID ARTERY; CELL CULTURE; CELL FUNCTION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; EX VIVO STUDY; MATHEMATICAL MODEL; MECHANICAL STRESS; NONHUMAN; NONLINEAR SYSTEM; PREDICTION; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; STRUCTURE ANALYSIS; SWINE; VASCULAR SMOOTH MUSCLE; ANIMAL; BIOLOGICAL MODEL; COMMON CAROTID ARTERY; COMPUTER SIMULATION; IN VITRO STUDY; MECHANOTRANSDUCTION; PHYSIOLOGY; YOUNG MODULUS;

SUS;

ANIMALS; CAROTID ARTERY, COMMON; COMPUTER SIMULATION; ELASTIC MODULUS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MECHANOTRANSDUCTION, CELLULAR; MODELS, CARDIOVASCULAR; NONLINEAR DYNAMICS; STRESS, MECHANICAL; SWINE;

EID: 64549156133     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.3005163     Document Type: Article

References (66)

1. Fung, Y. C., 1965, Foundations of Solid Mechanics, Prentice-Hall, Englewood Cliffs, NJ.
2. Humphrey, J. D., 1995, "Mechanics of the Arterial Wall: Review and Directions," Crit. Rev. Biomed. Eng., 23(1-2), pp. 1-162.
3. Vito, R. P., and Dixon, S. A., 2003, "Blood Vessel Constitutive Models - 1995-2002," Annu. Rev. Biomed. Eng., 5, pp. 413-439.
4. Brossollet, L. J., and Vito, R. P., 1996, "A New Approach to Mechanical Testing and Modeling of Biological Tissues, With Application to Blood Vessels," ASME J. Biomech. Eng., 118, pp. 433-439.
5. von Maltzahn, W. W., Besdo, D., and Wiemer, W., 1981, "Elastic Properties of Arteries: A Nonlinear Two-Layer Cylindrical Model," J. Biomech., 14(6), pp. 389-397.
6. von Maltzahn, W. W., Warriyar, R. G., and Keitzer, W. F., 1984, "Experimental Measurements of Elastic Properties of Media and Adventitia of Bovine Carotid Arteries," J. Biomech., 17(11), pp. 839-847.
7. Rachev, A., 1997, "Theoretical Study of the Effect of Stress-Dependent Remodeling on Arterial Geometry under Hypertensive Conditions," J. Biomech., 30(8), pp. 819-827.
8. Holzapfel, G. A., and Weizsäcker, H. W., 1998, "Biomechanical Behavior of the Arterial Wall and Its Numerical Characterization," Comput. Biol. Med., 28, pp. 377-392.
9. Holzapfel, G. A., Gasser, T. C., and Stadler, M., 2002, "A Structural Model for the Viscoelastic Behavior of Arterial Walls: Continuum Formulation and Finite Element Analysis," Eur. J. Mech. A/Solids, 21, pp. 441-463.
10. Wuyts, F. L., Vanhuyse, V. J., Langewouters, G. J., Decraemer, W. F., Raman, E. R., and Buyle, S., 1995, "Elastic Properties of Human Aortas in Relation to Age and Atherosclerosis: A Structural Model," Phys. Med. Biol., 40(10), pp. 1577-1597.
11. Zulliger, M. A., Fridez, P., Hayashi, K., and Stergiopulos, N., 2004, "A Strain Energy Function for Arteries Accounting for Wall Composition and Structure," J. Biomech., 37, pp. 989-1000. (Pubitemid 38686323)
12. Vito, R. P., and Hickey, J., 1980, "The Mechanical Properties of Soft Tissues-II: The Elastic Response of Arterial Segments," J. Biomech., 13, pp. 951-957. (Pubitemid 11226509)
13. Chuong, C. J., and Fung, Y. C., 1983, "Three-Dimensional Stress Distribution in Arteries," ASME J. Biomech. Eng., 105, pp. 268-274.
14. Vorp, D. A., Rajagopal, K. R., Smolinski, P. J., and Borovetz, H. S., 1995, "Identification of Elastic Properties of Homogeneous, Orthotropic Vascular Segments in Distension," J. Biomech., 28(5), pp. 501-512.
15. Chuong, C. J., and Fung, Y. C., 1986, "On Residual Stresses in Arteries," ASME J. Biomech. Eng., 108, pp. 189-192.
16. Matsumoto, T., and Hayashi, K., 1996, "Stress and Strain Distribution in Hypertensive and Normotensive Rat Aorta Considering Residual Strain," ASME J. Biomech. Eng., 118(1), pp. 62-73.
17. Rachev, A., Stergiopulos, N., and Meister, J.-J., 1996, "Theoretical Study of Dynamics of Arterial Wall Remodeling in Response to Changes in Blood Pressure," J. Biomech., 29(5), pp. 635-642. (Pubitemid 26093289)
18. Chaudhry, H. R., Bukiet, B., Davis, A., Ritter, A. B., and Findley, T., 1997, "Residual Stresses in Oscillating Thoracic Arteries Reduce Circumferential Stresses and Stress Gradients," J. Biomech., 30(1), pp. 57-62. (Pubitemid 27002982)
19. Peterson, S. J., and Okamoto, R. J., 2000, "Effect of Residual Stress and Heterogeneity on Circumferential Stress in the Arterial Wall," ASME J. Biomech. Eng., 122(4), pp. 454-456.
20. Vito, R. P., Whang, M. C., Glagov, S., and Aoki, T., 1991, "The Distribution of Strains and Stresses in the Arterial Cross Section," Proceedings of the 1991 ASME Winter Annual Meeting, Atlanta, GA.
21. Greenwald, S. E., Moore, J. E., Rachev, A., Kane, T. P. C., and Meister, J.-J., 1997, "Experimental Investigation of the Distribution of Residual Strains in the Artery Wall," ASME J. Biomech. Eng., 119, pp. 438-444.
22. Matsumoto, T., Goto, T., and Sato, M., 2002, "Residual Stress and Strain in the Lamellar Unit of the Aorta: Experiment and Analysis," Proceedings of the Fouth World Congress Biomechanics, Calgary, Canada.
23. Feldman, S. A., and Glagov, S., 1971, "Transmedial Collagen and Elastin Gradients in Human Aortas: Reversal With Age," Atherosclerosis, 13, pp. 385-394.
24. Hasan, N., and Greenwald, S. E., 1995, "Variation in the Concentration of Scleroproteins across the Arterial Wall," J. Pathol., 176 (Suppl.), p. 26A.
25. 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, pp. 237-257.
26. Taber, L. A., and Humphrey, J. D., 2001, "Stress-Modulated Growth, Residual Stress, and Vascular Heterogeneity," ASME J. Biomech. Eng., 123(6), pp. 528-535.
27. Dollery, C. M., McEwan, J. R., and Henney, A. M., 1995, "Matrix Metalloproteinases and Cardiovascular Disease," Circ. Res., 77(5), pp. 863-868.
28. Johnson, C., and Galis, Z. S., 2004, "Matrix Metalloproteinase-2 and -9 Differentially Regulate Smooth Muscle Cell Migration and Cell-Mediated Collagen Organization," Arterioscler. Thromb., 24, pp. 54-60.
29. Defawe, O. D., Kenagy, R. D., Choi, C., Wan, S. Y. C., Deroanne, C., Nusgens, B., Sakalihasan, N., Colige, A., and Clowes, A. W., 2005, "MMP-9 Regulates Both Positively and Negatively Collagen Gel Contraction: A Nonproteolytic Function of MMP-9," Cardiovasc. Res., 66, pp. 402-409.
30. Asanuma, K., Magid, R., Johnson, C., Nerem, R. M., and Galis, Z. S., 2003, "Uniaxial Strain Upregulates Matrix-Degrading Enzymes Produced by Human Vascular Smooth Muscle Cells," Am. J. Physiol. Heart Circ. Physiol., 284, pp. H1778-H1784.
31. O'Callaghan, C. J., and Williams, B., 2000, "Mechanical Strain-Induced Extracellular Matrix Production by Human Vascular Smooth Muscle Cells: Role of TGF- β1," Hypertension, 36(3), pp. 319-324.
32. Chesler, N. C., Ku, D. N., and Galis, Z. S., 1999, "Transmural Pressure Induces Matrix-Degrading Activity in Porcine Arteries Ex Vivo," Am. J. Physiol., 277(5), pp. H2002-H2009.
33. Mavromatis, K., Fukai, T., Tate, M., Chesler, N., Ku, D. N., and Galis, Z. S., 2000, "Early Effects of Arterial Hemodynamic Conditions on Human Saphenous Veins Perfused Ex Vivo," Arterioscler. Thromb., 20, pp. 1889-1895.
34. Wilson, S. H., Herrmann, J., Lerman, L. O., Holmes, D. R., Napoli, C., Ritman, E. L., and Lerman, A., 2002, "Simvastatin Preserves the Structure of Coronary Adventitial Vasa Vasorum in Experimental Hypercholesterolemia Independent of Lipid Lowering," Circulation, 105(5), pp. 415-418.
35. Han, H.-C., and Ku, D. N., 2001, "Contractile Responses in Arteries Subjected to Hypertensive Pressure in Seven-Day Organ Culture," Ann. Biomed. Eng., 29, pp. 467-475.
36. Davis, N. P., Han, H. C., Wayman, B., and Vito, R. P., 2005, "Sustained Axial Loading Lengthens Arteries in Organ Culture," Ann. Biomed. Eng., 33(7), pp. 867-877. (Pubitemid 40997673)
37. Ku, D. N., 1997, "Blood Flow in Arteries," Annu. Rev. Fluid Mech., 29, pp. 399-434.
38. Davis, N. P., 2002, "Axial Stretch as a Means of Lengthening Arteries: An Investigation in Organ Culture," Ph.D. thesis, Georgia Institute of Technology, Atlanta, GA.
39. Todd, M. E., Laye, C. G., and Osborne, D. N., 1983, "The Dimensional Characteristics of Smooth Muscle in Rat Blood Vessels: A Computer-Assisted Analysis," Circ. Res., 53, pp. 319-331.
40. Blomfield, J., and Farrar, J. F., 1967, "Fluorescence Spectra of Arterial Elastin," Biochem. Biophys. Res. Commun., 28(3), pp. 346-351.
41. Fitzmaurice, M., Bordagaray, J. O., Engelmann, G. L., Richards-Kortum, R., Kolubayev, T., Feld, M. S., Ratliff, N. B., and Kramer, J. R., 1989, "Argon Ion Laser-Excited Autofluorescence in Normal and Atherosclerotic Aorta and Coronary Arteries: Morphologic Studies," Am. Heart J., 118(5), pp. 1028-1038.
42. Baraga, J. J., Rava, R. P., Taroni, P., Kittrell, C., Fitzmaurice, M., and Feld, M. S., 1990, "Laser Induced Fluorescence Spectroscopy of Normal and Atherosclerotic Human Aorta Using 306-310 nm Excitation," Lasers Surg. Med., 10(3), pp. 245-261. (Pubitemid 20303831)
43. Junqueira, L. C. U., Bignolas, G., and Brentani, R. R., 1979, "Picrosirius Staining Plus Polarization Microscopy, A Specific Method for Collagen Detection in Tissue Sections," Histochem. J., 11, pp. 447-455. (Pubitemid 9238595)
44. Canham, P. B., Finlay, H. M., Kiernan, J. A., and Ferguson, G. G., 1999, "Layered Structure of Saccular Aneurysms Assessed by Collagen Birefringence," Neurol. Res., 21(7), pp. 618-626.
45. Junqueira, L. C. U., Montes, G. S., and Krisztan, R. M., 1979, "The Collagen of the Vertebrate Peripheral Nervous System," Cell Tissue Res., 202, pp. 453-460.
46. Junqueira, L. C. U., Montes, G. S., and Sanchez, E. M., 1982, "The Influence of Tissue Section Thickness on the Study of Collagen by the Picrosirius-Polarization Method," Histochemistry, 74(1), pp. 153-156.
47. Ehlers, E. G., 1987, Optical Mineralogy: Theory and Technique, Blackwell Scientific Publications, Palo Alto, CA, p. 29.
48. Whittaker, P., Kloner, R. A., Boughner, D. R., and Pickering, J. G., 1994, "Quantitative Assessment of Myocardial Collagen With Picrosirius Red Staining and Circularly Polarized Light," Basic Res. Cardiol., 89(5), pp. 397-410.
49. Szendroi, M., Vajta, G., Kovacs, L., Schaff, Z., and Lapis, K., 1984, "Polarization Colours of Collagen Fibres: A Sign of Collagen Production Activity in Fibrotic Processes," Acta Morphol. Hung., 32(1), pp. 47-55. (Pubitemid 14056782)
50. Wolman, M., and Kasten, F. H., 1986, "Polarized Light Microscopy in the Study of the Molecular Structure of Collagen and Reticulin," Histochemistry, 85(1), pp. 41-49.
51. Lee, R. T., Schoen, F. J., Loree, H. M., Lark, M. W., and Libby, P., 1996, "Circumferential Stress and Matrix Metalloproteinase 1 in Human Coronary Atherosclerosis: Implications for Plaque Rupture," Arterioscler. Thromb., 16(8), pp. 1070-1073.
52. Galis, Z. S., Sukhova, G. K., and Libby, P., 1995, "Microscopic Localization of Active Proteases by In Situ Zymography: Detection of Matrix Metalloproteinase Activity in Vascular Tissue," FASEB J., 9(10), pp. 974-980.
53. Torrance, H. B., and Shwatz, S., 1961, "The Elastic Behaviour of the Arterial Wall," J. R. Coll. Surg. Edinb., 7, pp. 55-60.
54. Conklin, B. S., Richter, E. R., Kreutziger, K. L., Zhong, D.-S., and Chen, C., 2002, "Development and Evaluation of a Novel Decellularized Vascular Xenograft," Med. Eng. Phys., 24, pp. 173-183. (Pubitemid 34327597)
55. Fung, Y. C., 1984, Biodynamics: Circulation, Springer-Verlag, New York, NY, pp. 64-65.
56. Kim, Y., 2007, "Correlation Between MMP-2 and -9 Levels and Local Stresses in Arteries Using a Heterogeneous Mechanical Model," Ph. D. thesis, Georgia Institute of Technology, Atlanta, GA.
57. Canham, P. B., Finlay, H. M., Whittaker, P., and Starkey, J., 1986, "The Tunica Muscularis of Human Brain Arteries: Three-Dimensional Measurements of Alignment of the Smooth Muscle Mechanical Axis, by Polarized Light and the Universal Stage," Neurol. Res., 8(2), pp. 66-74. (Pubitemid 16098554)
58. Finlay, H. M., Dixon, J. G., and Canham, P. B., 1991, "Fabric Organization of the Subendothelium of the Human Brain Artery by Polarized-Light Microscopy," Arterioscler., Thromb., Vasc. Biol., 11, pp. 681-690.
59. Wilson, E., Sudhir, K., and Ives, H. E., 1995, "Mechanical Strain of Rat Vascular Smooth Muscle Cells is Sensed by Specific Extracellular Matrix/ Integrin Interactions," J. Clin. Invest., 96(5), pp. 2364-2372.
60. Koyama, H., Raines, E. W., Bornfeldt, K. E., Roberts, J. M., and Ross, R., 1996, "Fibrillar Collagen Inhibits Arterial Smooth Muscle Proliferation Through Regulation of Cdk2 Inhibitors," Cell, 87, pp. 1069-1078. (Pubitemid 26427990)
61. Carey, D. J., 1991, "Control of Growth and Differentiation of Vascular Cells by Extracellular Matrix Proteins," Annu. Rev. Physiol., 53, pp. 161-177.
62. Capers, Q., Alexander, R. W., Lou, P., De Leon, H., Wilcox, J. N., Ishizaka, N., Howard, A. B., and Taylor, W. R., 1997, "Monocyte Chemoattractant Protein-1 Expression in Aortic Tissues of Hypertensive Rats," Hypertension, 30(6), pp. 1397-1402.
63. Liu, S. Q., and Fung, Y. C., 1989, "Relationship Between Hypertension, Hypertrophy, and Opening Angle of Zero-Stress State of Arteries Following Aortic Constriction," ASME J. Biomech. Eng., 111, pp. 325-335.
64. Matsumoto, T., and Hayashi, K., 1994, "Mechanical and Dimensional Adaptation of Rat Aorta to Hypertension," ASME J. Biomech. Eng., 116, pp. 278-283.
65. Fridez, P., Zulliger, M., Bobard, F., Montorzi, G., Miyazaki, H., Hayashi, K., and Stergiopulos, N., 2003, "Geometrical, Functional, and Histomorphometric Adaptation of Rat Carotid Artery in Induced Hypertension," J. Biomech., 36, pp. 671-680.
66. Xu, C., Zarins, C. K., Bassiouny, H. S., Briggs, W. H., Reardon, C., and Glagov, S., 2000, "Differential Transmural Distribution of Gene Expression for Collagen Types I and III Proximal to Aortic Coarctation in the Rabbit," J. Vasc. Res., 37(3), pp. 170-182. (Pubitemid 30350885)