Glycated collagen decreased endothelial cell fibronectin alignment in response to cyclic stretch via interruption of actin alignment

Journal of Biomechanical Engineering

Volumn 136, Issue 10, 2014, Pages

  Figueroa, Dannielle S ^a   Kemeny, Steven F ^b   Clyne, Alisa Morss ^a,b  

^a DREXEL UNIVERSITY   (United States)

^b Drexel University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALIGNMENT; CELL CULTURE; COLLAGEN; ENZYME INHIBITION;

C-JUN N-TERMINAL KINASE; CARDIO-VASCULAR DISEASE; DEGRADATION ACTIVITY; EXTRACELLULAR MATRICES; FOCAL ADHESION KINASE; MATRIX METALLOPROTEINASE-2; MATRIX METALLOPROTEINASES; VASCULAR REMODELING;

ENDOTHELIAL CELLS;

ACTIN; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; CYTOCHALASIN; CYTOCHALASIN D; FIBRONECTIN; FOCAL ADHESION KINASE; GELATINASE A; GLYCATED COLLAGEN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MEMBRANE ASSOCIATED TYPE 1 MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG; VITRONECTIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; NONHUMAN; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN FUNCTION; WESTERN BLOTTING; ANIMAL; BIOMECHANICS; CYTOLOGY; CYTOSKELETON; DRUG EFFECTS; GLYCOSYLATION; MECHANICS; METABOLISM; PIG;

ACTINS; ANIMALS; BIOMECHANICAL PHENOMENA; COLLAGEN; CYTOCHALASINS; CYTOSKELETON; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FIBRONECTINS; GLYCOSYLATION; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MECHANICAL PROCESSES; MITOGEN-ACTIVATED PROTEIN KINASES; SWINE; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 84940252595     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4028037     Document Type: Article

References (71)

1. Kalluri, R., 2003, "Basement Membranes: Structure, Assembly and Role in Tumour Angiogenesis," Nat. Rev. Cancer, 3(6), pp. 422-433. (Pubitemid 37328846)
2. Michiels, C., 2003, "Endothelial Cell Functions," J. Cell Physiol., 196(3), pp. 430-443. (Pubitemid 36927738)
3. LeBleu, V. S., Macdonald, B., and Kalluri, R., 2007, "Structure and Function of Basement Membranes," Exp. Biol. Med. (Maywood), 232(9), pp. 1121-1129. (Pubitemid 47503053)
4. Matthews, B. D., Overby, D. R., Mannix, R., and Ingber, D.E., 2006, "Cellular Adaptation to Mechanical Stress: Role of Integrins, Rho, Cytoskeletal Tension and Mechanosensitive Ion Channels," J. Cell Sci., 119(Pt 3), pp. 508-518.
5. Shyy, J. Y., and Chien, S., 2002, "Role of Integrins in Endothelial Mechanosensing of Shear Stress," Circ. Res., 91(9), pp. 769-775. (Pubitemid 35285073)
6. Jalali, S., del Pozo, M. A., Chen, K., Miao, H., Li, Y., Schwartz, M. A., Shyy, J. Y., and Chien, S., 2001, "Integrin-Mediated Mechanotransduction Requires Its Dynamic Interaction With Specific Extracellular Matrix (ECM) Ligands," Proc. Natl. Acad. Sci. U. S. A., 98(3), pp. 1042-1046. (Pubitemid 32121183)
7. Hirayama, Y., and Sumpio, B. E., 2007, "Role of Ligand-Specific Integrins in Endothelial Cell Alignment and Elongation Induced by Cyclic Strain," Endothelium, 14(6), pp. 275-283.
8. Thoumine, O., Nerem, R. M., and Girard, P. R., 1995, "Changes in Organization and Composition of the Extracellular Matrix Underlying Cultured Endothelial Cells Exposed to Laminar Steady Shear Stress," Lab Invest., 73(4), pp. 565-576.
9. Yamane, T., Mitsumata, M., Yamaguchi, N., Nakazawa, T., Mochizuki, K., Kondo, T., Kawasaki, T., Murata, S., Yoshida, Y., and Katoh, R., 2010, "Laminar High Shear Stress Up-Regulates Type IV Collagen Synthesis and Down-Regulates MMP-2 Secretion in Endothelium. A Quantitative Analysis," Cell Tissue Res., 340(3), pp. 471-479.
10. den Braber, E. T., de Ruijter, J. E., Ginsel, L. A., von Recum, A. F., and Jansen, J. A., 1998, "Orientation of ECM Protein Deposition, Fibroblast Cytoskeleton, and Attachment Complex Components on Silicone Microgrooved Surfaces," J. Biomed. Mater. Res., 40(2), pp. 291-300.
11. Nguyen, T. D., Liang, R., Woo, S. L., Burton, S. D., Wu, C., Almarza, A., Sacks, M. S., and Abramowitch, S., 2009, "Effects of Cell Seeding and Cyclic Stretch on the Fiber Remodeling in an Extracellular Matrix-Derived Bioscaffold," Tissue Eng. Part A, 15(4), pp. 957-963.
12. Wang, J. H., Jia, F., Gilbert, T. W., and Woo, S. L., 2003, "Cell Orientation Determines the Alignment of Cell-Produced Collagenous Matrix," J. Biomech., 36(1), pp. 97-102. (Pubitemid 35448098)
13. Kim, A., Lakshman, N., and Petroll, W. M., 2006, "Quantitative Assessment of Local Collagen Matrix Remodeling in 3-D Culture: The Role of Rho Kinase," Exp. Cell Res., 312(18), pp. 3683-3692. (Pubitemid 44470785)
14. Weidenhamer, N. K., and Tranquillo, R. T., 2013, "Influence of Cyclic Mechanical Stretch and Tissue Constraints on Cellular and Collagen Alignment in Fibroblast-Derived Cell Sheets," Tissue Eng. Part C Methods, 19(5), pp. 386-395.
15. Leung, D. Y., Glagov, S., and Mathews, M. B., 1976, "Cyclic Stretching Stimulates Synthesis of Matrix Components by Arterial Smooth Muscle Cells in vitro," Science, 191(4226), pp. 475-477.
16. Sukmana, I., and Vermette, P., 2010, "Polymer Fibers as Contact Guidance to Orient Microvascularization in a 3D Environment," J. Biomed. Mater. Res. A, 92(4), pp. 1587-1597.
17. Gorfien, S. F., Winston, F. K., Thibault, L. E., and Macarak, E. J., 1989, "Effects of Biaxial Deformation on Pulmonary Artery Endothelial Cells," J. Cell Physiol., 139(3), pp. 492-500. (Pubitemid 19167820)
18. Sumpio, B. E., Banes, A. J., Link, G. W., and Iba, T., 1990, "Modulation of Endothelial Cell Phenotype by Cyclic Stretch: Inhibition of Collagen Production," J. Surg. Res., 48(5), pp. 415-420. (Pubitemid 20190687)
19. Chiquet, M., 1999, "Regulation of Extracellular Matrix Gene Expression by Mechanical Stress," Matrix Biol, 18(5), pp. 417-426.
20. Nagase, H., and Woessner, J. F., Jr., 1999, "Matrix Metalloproteinases," J. Biol. Chem., 274(31), pp. 21491-21494.
21. von Offenberg Sweeney, N., Cummins, P. M., Birney, Y. A., Cullen, J. P., Redmond, E. M., and Cahill, P. A., 2004, "Cyclic Strain-Mediated Regulation of Endothelial Matrix Metalloproteinase-2 Expression and Activity," Cardiovasc. Res., 63(4), pp. 625-634. (Pubitemid 39078676)
22. Wang, B. W., Chang, H., Lin, S., Kuan, P., and Shyu, K. G., 2003, "Induction of Matrix Metalloproteinases-14 and -2 by Cyclical Mechanical Stretch is Mediated by Tumor Necrosis Factor-Alpha in Cultured Human Umbilical Vein Endothelial Cells," Cardiovasc. Res., 59(2), pp. 460-469. (Pubitemid 37272040)
23. Yamaguchi, S., et al., 2002, "Cyclic Strain Stimulates Early Growth Response Gene Product 1-Mediated Expression of Membrane Type 1 Matrix Metalloproteinase in Endothelium," Lab Invest., 82(7), pp. 949-956. (Pubitemid 34761670)
24. Calles-Escandon, J., and Cipolla, M., 2001, "Diabetes and Endothelial Dysfunction: A Clinical Perspective," Endocr. Rev., 22(1), pp. 36-52. (Pubitemid 32187802)
25. Uusitupa, M. I., Niskanen, L. K., Siitonen, O., Voutilainen, E., and Pyorala, K., 1993, "Ten-Year Cardiovascular Mortality in Relation to Risk Factors and Abnormalities in Lipoprotein Composition in Type 2 (Non-Insulin-Dependent) Diabetic and Non-Diabetic Subjects," Diabetologia, 36(11), pp. 1175-1184. (Pubitemid 23314569)
26. Milicevic, Z., Raz, I., Beattie, S. D., Campaigne, B. N., Sarwat, S., Gromniak, E., Kowalska, I., Galic, E., Tan, M., and Hanefeld, M., 2008, "Natural History of Cardiovascular Disease in Patients With Diabetes: Role of Hyperglycemia," Diabetes Care, 31(Suppl 2), pp. S155-S160.
27. Avery, N. C., and Bailey, A. J., 2006, "The Effects of the Maillard Reaction on the Physical Properties and Cell Interactions of Collagen," Pathol. Biol. (Paris), 54(7), pp. 387-395. (Pubitemid 44442672)
28. Kuzuya, M., Asai, T., Kanda, S., Maeda, K., Cheng, X. W., and Iguchi, A., 2001 "Glycation Cross-Links Inhibit Matrix Metalloproteinase-2 Activation in Vascular Smooth Muscle Cells Cultured on Collagen Lattice," Diabetologia, 44(4), pp. 433-436. (Pubitemid 32324353)
29. Anderson, S. S., Wu, K., Nagase, H., Stettler-Stevenson, W. G., Kim, Y., and Tsilibary, E. C., 1996, "Effect of Matrix Glycation on Expression of Type IV Collagen, MMP-2, MMP-9, and TIMP-1 by Human Mesangial Cells," Cell Adhes. Commun., 4(2), pp. 89-101.
30. Portik-Dobos, V., Anstadt, M. P., Hutchinson, J., Bannan, M., and Ergul, A., 2002, "Evidence for a Matrix Metalloproteinase Induction/Activation System in Arterial Vasculature and Decreased Synthesis and Activity in Diabetes," Diabetes, 51(10), pp. 3063-3068.
31. Figueroa, D., Kemeny, S., and Clyne, A., 2011, "Glycated Collagen Impairs Endothelial Cell Response to Cyclic Stretch," Cell. Mol. Bioeng., 4(2), pp. 220-230.
32. Kemeny, S. F., Figueroa, D. S., Andrews, A. M., Barbee, K. A., and Clyne, A. M., 2011, "Glycated Collagen Alters Endothelial Cell Actin Alignment and Nitric Oxide Release in Response to Fluid Shear Stress," J. Biomech., 44(10), pp. 1927-1935.
33. Wong, M. K., and Gotlieb, A. I., 1984, "In Vitro Reendothelialization of a Single-Cell Wound. Role of Microfilament Bundles in Rapid Lamellipodia-Mediated Wound Closure," Lab Invest., 51(1), pp. 75-81. (Pubitemid 14053755)
34. Wipff, P. J., Majd, H., Acharya, C., Buscemi, L., Meister, J. J., and Hinz, B., 2009, "The Covalent Attachment of Adhesion Molecules to Silicone Membranes for Cell Stretching Applications," Biomaterials, 30(9), pp. 1781-1789.
35. Kemeny, S. F., and Clyne, A. M., 2011, "A Simplified Implementation of Edge Detection in Matlab Is Faster and More Sensitive Than Fast Fourier Transform for Actin Fiber Alignment Quantification," Microsc. Microanal., 17(2), pp. 156-166.
36. Kleiner, D. E., and Stetler-Stevenson, W. G., 1994, "Quantitative Zymography: Detection of Picogram Quantities of Gelatinases," Anal. Biochem., 218(2), pp. 325-329. (Pubitemid 24141631)
37. Cummins, P. M., von Offenberg Sweeney, N., Killeen, M. T., Birney, Y. A., Redmond, E. M., and Cahill, P. A., 2007, "Cyclic Strain-Mediated Matrix Metalloproteinase Regulation Within the Vascular Endothelium: A Force to be Reckoned With," Am J. Physiol. Heart Circ. Physiol., 292(1), pp. H28-H42. (Pubitemid 46105162)
38. Flanagan, M. D., and Lin, S., 1980, "Cytochalasins Block Actin Filament Elongation by Binding to High Affinity Sites Associated With F-actin," J. Biol. Chem., 255(3), pp. 835-838.
39. Dartsch, P. C., and Betz, E., 1989, "Response of Cultured Endothelial Cells to Mechanical Stimulation," Basic Res. Cardiol., 84(3), pp. 268-281. (Pubitemid 19166435)
40. Wang, J. H., Goldschmidt-Clermont, P., Wille, J., and Yin, F. C., 2001, "Specificity of Endothelial Cell Reorientation in Response to Cyclic Mechanical Stretching," J. Biomech., 34(12), pp. 1563-1572. (Pubitemid 33041372)
41. Moretti, M., Prina-Mello, A., Reid, A. J., Barron, V., and Prendergast, P. J., 2004, "Endothelial Cell Alignment on Cyclically-Stretched Silicone Surfaces," J Mater. Sci. Mater. Med., 15(10), pp. 1159-1164. (Pubitemid 39491723)
42. Bernardo, M. M., and Fridman, R., 2003, "TIMP-2 (Tissue Inhibitor of Metalloproteinase-2) Regulates MMP-2 (Matrix Metalloproteinase-2) Activity in the Extracellular Environment After Pro-MMP-2 Activation by MT1 (Membrane Type 1)-MMP," Biochem. J., 374(Pt 3), pp. 739-745. (Pubitemid 37163919)
43. Hernandez-Barrantes, S., Toth, M., Bernardo, M. M., Yurkova, M., Gervasi, D. C., Raz, Y., Sang, Q. A., and Fridman, R., 2000, "Binding of Active (57 kDa) Membrane Type 1-Matrix Metalloproteinase (MT1-MMP) to Tissue Inhibitor of Metalloproteinase (TIMP)-2 Regulates MT1-MMP Processing and Pro-MMP-2 Activation," J. Biol. Chem., 275(16), pp. 2080-2089.
44. Isenberg, B. C., Backman, D. E., Kinahan, M. E., Jesudason, R., Suki, B., Stone, P. J., Davis, E. C., and Wong, J. Y., 2012, "Micropatterned Cell Sheets With Defined Cell and Extracellular Matrix Orientation Exhibit Anisotropic Mechanical Properties," J. Biomech., 45(5), pp. 756-761.
45. Yan, J., Qiang, L., Gao, Y., Cui, X., Zhou, H., Zhong, S., Wang, Q., and Wang, H., 2012, "Effect of Fiber Alignment in Electrospun Scaffolds on Keratocytes and Corneal Epithelial Cells Behavior," J. Biomed. Mater. Res. A, 100A(2), pp. 527-535.
46. Yeh, Y. T., Hur, S. S., Chang, J., Wang, K. C., Chiu, J. J., Li, Y. S., and Chien, S., 2012, "Matrix Stiffness Regulates Endothelial Cell Proliferation Through Septin 9," PLoS One, 7(10), p. e46889.
47. Yeung, T., Georges, P. C., Flanagan, L. A., Marg, B., Ortiz, M., Funaki, M., Zahir, N., Ming, W., Weaver, V., and Janmey, P. A., 2005, "Effects of Substrate Stiffness on Cell Morphology, Cytoskeletal Structure, and Adhesion," Cell Motil. Cytoskeleton, 60(1), pp. 24-34. (Pubitemid 40066224)
48. Petrie, R. J., Doyle, A. D., and Yamada, K. M., 2009, "Random Versus Directionally Persistent Cell Migration," Nat. Rev. Mol. Cell Biol., 10(8), pp. 538-549.
49. Doyle, A. D., Wang, F. W., Matsumoto, K., and Yamada, K. M., 2009, "One-Dimensional Topography Underlies Three-Dimensional Fibrillar Cell Migration," J. Cell Biol., 184(4), pp. 481-490.
50. Nakatsuji, N., and Johnson, K. E., 1984, "Experimental Manipulation of a Contact Guidance System in Amphibian Gastrulation by Mechanical Tension," Nature, 307(5950), pp. 453-455. (Pubitemid 14132058)
51. Sidani, M., Wyckoff, J., Xue, C., Segall, J. E., and Condeelis, J., 2006, "Probing the Microenvironment of Mammary Tumors Using Multiphoton Microscopy," J. Mammary Gland Biol. Neoplasia, 11(2), pp. 151-163. (Pubitemid 46111262)
52. Foolen, J., Deshpande, V. S., Kanters, F. M., and Baaijens, F. P., 2012, "The Influence of Matrix Integrity on Stress-Fiber Remodeling in 3D," Biomaterials, 33(30), pp. 7508-7518.
53. McGinn, S., Poronnik, P., Gallery, E. D., and Pollock, C. A., 2004, "The Effects of High Glucose and Atorvastatin on Endothelial Cell Matrix Production," Diabet Med., 21(10), pp. 1102-1107. (Pubitemid 39389222)
54. Kemeny, S. F., Cicalese, S., Figueroa, D. S., and Clyne, A. M., 2013, "Glycated Collagen and Altered Glucose Increase Endothelial Cell Adhesion Strength," J. Cell Physiol., 228(8), pp. 1727-1736.
55. Rittie, L., Berton, A., Monboisse, J. C., Hornebeck, W., and Gillery, P., 1999, "Decreased Contraction of Glycated Collagen Lattices Coincides With Impaired Matrix Metalloproteinase Production," Biochem. Biophys. Res. Commun., 264(2), pp. 488-492. (Pubitemid 29516113)
56. Hsu, H. J., Lee, C. F., Locke, A., Vanderzyl, S. Q., and Kaunas, R., 2010, "Stretch-Induced Stress Fiber Remodeling and the Activations of JNK and ERK Depend on Mechanical Strain Rate, but Not FAK," PLoS One, 5(8), pp. e12470.
57. Kito, H., Chen, E. L., Wang, X., Ikeda, M., Azuma, N., Nakajima, N., Gahtan, V., and Sumpio, B. E., 2000, "Role of Mitogen-Activated Protein Kinases in Pulmonary Endothelial Cells Exposed to Cyclic Strain," J. Appl. Physiol., 89(6), pp. 2391-2400.
58. Grote, K., Flach, I., Luchtefeld, M., Akin, E., Holland, S. M., Drexler, H., and Schieffer, B., 2003, "Mechanical Stretch Enhances mRNA Expression and Proenzyme Release of Matrix Metalloproteinase-2 (MMP-2) Via NAD(P)H Oxidase-Derived Reactive Oxygen Species," Circ. Res., 92(11), pp. e80-e86.
59. von Offenberg Sweeney, N., Cummins, P. M., Birney, Y. A., Redmond, E. M., and Cahill, P. A., 2004, "Cyclic Strain-Induced Endothelial MMP-2: Role in Vascular Smooth Muscle Cell Migration," Biochem. Biophys. Res. Commun., 320(2), pp. 325-333. (Pubitemid 38798869)
60. Takino, T., Nakada, M., Miyamori, H., Watanabe, Y., Sato, T., Gantulga, D., Yoshioka, K., Yamada, K. M., and Sato, H., 2005, "JSAP1/JIP3 Cooperates With Focal Adhesion Kinase to Regulate c-Jun N-Terminal Kinase and Cell Migration," J. Biol. Chem., 280(45), pp. 37772-37781. (Pubitemid 41642387)
61. Takino, T., Yoshioka, K., Miyamori, H., Yamada, K. M., and Sato, H., 2002, "A Scaffold Protein in the c-Jun N-Terminal Kinase Signaling Pathway Is Associated With Focal Adhesion Kinase and Tyrosine-Phosphorylated," Oncogene, 21(42), pp. 6488-6497. (Pubitemid 35155453)
62. Desai, L. P., White, S. R., and Waters, C. M., 2009, "Mechanical Stretch Decreases FAK Phosphorylation and Reduces Cell Migration Through Loss of JIP3-Induced JNK Phosphorylation in Airway Epithelial Cells," Am. J. Physiol. Lung Cell Mol. Physiol., 297(3), pp. L520-L529.
63. Azuma, N., Akasaka, N., Kito, H., Ikeda, M., Gahtan, V., Sasajima, T., and Sumpio, B. E., 2001, "Role of p38 MAP Kinase in Endothelial Cell Alignment Induced by Fluid Shear Stress," Am. J. Physiol. Heart Circ. Physiol., 280(1), pp. H189-H197.
64. Reunanen, N., Li, S. P., Ahonen, M., Foschi, M., Han, J. H., and Kahari, V. M., 2002, "Activation of p38 Alpha MAPK Enhances Collagenase-1 (Matrix Metalloproteinase (MMP)-1) and Stromelysin-1 (MMP-3) Expression by mRNA Stabilization," J. Biol. Chem., 277(35), pp. 32360-32368. (Pubitemid 34969054)
65. Markovic, D. S., Vinnakota, K., Chirasani, S., Synowitz, M., Raguet, H., Stock, K., Sliwa, M., Lehmann, S., Kalin, R., van Rooijeng, N., Holmbeck, K., Heppner, F. L., Kiwit, J., Matyash, V., Lehnardt, S., Kaminska, B., Glass, R., and Kettenmann, H., 2009, "Gliomas Induce and Exploit Microglial MT1-MMP Expression for Tumor Expansion," Proc. Natl. Acad. Sci. U. S. A., 106(30), pp. 12530-12535.
66. Ikeda, M., Taki, T., Mills, I., Kito, H., and Sumpio, B. E., 1999, "Extracellular Signal-Regulated Kinases 1 and 2 Activation in Endothelial Cells Exposed to Cyclic Strain," Am. J. Physiol. Heart Circ. Physiol., 276(2), pp. H614-H622. (Pubitemid 29100630)
67. Kuzuya, M., Satake, S., Ai, S., Asai, T., Kanda, S., Ramos, M. A., Miura, H., Ueda, M., and Iguchi, A., 1998, "Inhibition of Angiogenesis on Glycated Collagen Lattices," Diabetologia, 41(5), pp. 491-499. (Pubitemid 28206817)
68. Chen, J., Brodsky, S. V., Goligorsky, D. M., Hampel, D. J., Li, H., Gross, S. S., and Goligorsky, M. S., 2002, "Glycated Collagen I Induces Premature Senescence-Like Phenotypic Changes in Endothelial Cells," Circ. Res., 90(12), pp. 1290-1298. (Pubitemid 34787411)
69. Ross, R., 1999, "Atherosclerosis-An Inflammatory Disease," N. Engl. J. Med., 340(2), pp. 115-126.
70. Libby, P., Ridker, P. M., and Maseri, A., 2002, "Inflammation and Atherosclerosis," Circulation, 105(9), pp. 1135-1143. (Pubitemid 34212626)
71. Palinski, W., Chen, J., Brodsky, S., Li, H., Hampel, D. J., Miyata, T., Weinstein, T., Gafter, U., Norman, J. T., Fine, L. G., and Goligorsky, M. S., 1989, "Low Density Lipoprotein Undergoes Oxidative Modification in Vivo," Proc. Natl. Acad. Sci. U. S. A., 86(4), pp. 1372-1376. (Pubitemid 19061548)