Basement membrane stiffening promotes retinal endothelial activation associated with diabetes

FASEB Journal

Volumn 30, Issue 2, 2016, Pages 601-611

  Yang, Xiao ^a   Scott, Harry A ^a   Monickaraj, Finny ^c   Xu, Jun ^b   Ardekani, Soroush ^a   Nitta, Carolina F ^c,d   Cabrera, Andrea ^a   McGuire, Paul G ^c   Mohideen, Umar ^b   Das, Arup ^c,d   Ghosh, Kaustabh ^a  

^a University of California Riverside   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^d NEW MEXICO VA HEALTH CARE SYSTEM   (United States)

Author keywords

Diabetic retinopathy; Inflammation; Lysyl oxidase; Matrix stiffness; Nitric oxide

Indexed keywords

COLLAGEN TYPE 4; ENDOTHELIAL NITRIC OXIDE SYNTHASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; PROTEIN LYSINE 6 OXIDASE; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BASEMENT MEMBRANE STIFFNESS; CELL ACTIVATION; CELL ADHESION; CONTROLLED STUDY; CROSS LINKING; DIABETES MELLITUS; DISEASE ASSOCIATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MONOCYTE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RETINA CAPILLARY; RETINA CELL; RETINAL ENDOTHELIAL CELL; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED; COMPLICATION; DIABETIC RETINOPATHY; ENDOTHELIUM; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; HAPLORHINI; METABOLISM; PATHOLOGY; PHYSIOLOGY; RETINA;

ANIMALS; BASEMENT MEMBRANE; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOTHELIAL CELLS; ENDOTHELIUM; GENE EXPRESSION REGULATION; HAPLORHINI; HUMANS; MICE; MICE, INBRED C57BL; MONOCYTES; PROTEIN-LYSINE 6-OXIDASE; RETINA;

EID: 84958756262     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-277962     Document Type: Article

References (54)

1. Antonetti, D. A., Klein, R., and Gardner, T. W. (2012) Diabetic retinopathy. N. Engl. J. Med. 366, 1227-1239
2. Rangasamy, S., McGuire, P. G., and Das, A. (2012) Diabetic retinopathy and inflammation: novel therapeutic targets. Middle East Afr. J Ophthalmol. 19, 52-59
3. Tang, J., and Kern, T. S. (2011) Inflammation in diabetic retinopathy. Prog. Retin. Eye Res. 30, 343-358
4. Miyamoto, K., Khosrof, S., Bursell, S. E., Rohan, R., Murata, T., Clermont, A. C., Aiello, L. P., Ogura, Y., and Adamis, A. P. (1999) Prevention of leukostasis and vascular leakage in streptozotocininduced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc. Natl. Acad. Sci. USA 96, 10836-10841
5. Lutty, G. A. (2013) Effects of diabetes on the eye. Invest. Ophthalmol. Vis. Sci. 54, ORSF81-7
6. Kowluru, R. A., Kowluru, A., Mishra, M., and Kumar, B. (2015) Oxidative stress and epigeneticmodifications in the pathogenesis of diabetic retinopathy. Prog. Retin. Eye Res. 48, 40-61
7. Chronopoulos, A., Tang, A., Beglova, E., Trackman, P. C., and Roy, S. (2010)High glucose increases lysyl oxidase expression and activity in retinal endothelial cells:mechanism for compromised extracellular matrix barrier function. Diabetes 59, 3159-3166
8. Kagan, H.M., and Li, W. (2003) Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J. Cell. Biochem. 88, 660-672
9. Mammoto, A., Mammoto, T., Kanapathipillai, M., Wing Yung, C., Jiang, E., Jiang, A., Lofgren, K., Gee, E. P., and Ingber, D. E. (2013) Control of lung vascular permeability and endotoxin-induced pulmonary oedema by changes in extracellular matrix mechanics. Nat. Commun. 4, 1759
10. Ghosh, K., and Ingber, D. E. (2007)Micromechanical control of cell and tissue development: implications for tissue engineering. Adv. Drug Deliv. Rev. 59, 1306-1318
11. Ghosh, K., Thodeti, C. K., Dudley, A. C., Mammoto, A., Klagsbrun, M., and Ingber, D.E. (2008)Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro. Proc. Natl. Acad. Sci. USA 105, 11305-11310
12. Scholl, Z. N., Yang, W., and Marszalek, P. E. (2014) Chaperones rescue luciferase folding by separating its domains. J. Biol. Chem. 289, 28607-28618
13. Kothapalli, D., Liu, S. L., Bae, Y. H., Monslow, J., Xu, T., Hawthorne, E. A., Byfield, F. J., Castagnino, P., Rao, S., Rader, D. J., Pure, E., Phillips, M.C., Lund-Katz, S., Janmey, P.A., and Assoian, R.K. (2012) Cardiovascular protection by ApoE and ApoE-HDL linked to suppression of ECM gene expression and arterial stiffening. Cell Reports 2, 1259-1271
14. Ito, H., Akiyama, H., Iguchi, H., Iyama, K., Miyamoto, M., Ohsawa, K., and Nakamura, T. (2001) Molecular cloning and biological activity of a novel lysyl oxidase-related gene expressed in cartilage. J. Biol. Chem. 276, 24023-24029
15. Bondareva, A., Downey, C. M., Ayres, F., Liu, W., Boyd, S. K., Hallgrimsson, B., and Jirik, F. R. (2009) The lysyl oxidase inhibitor, beta-aminopropionitrile, diminishes the metastatic colonization potential of circulating breast cancer cells. PLoS One 4, e5620
16. Beacham, D. A., Amatangelo, M. D., and Cukierman, E. (2007) Preparation of extracellular matrices produced by cultured and primary fibroblasts. Curr. Protoc. Cell Biol. Chapter 10, Unit 10.9 doi:10.1002/0471143030.cb1009s33
17. Wang, Y. L., and Pelham, R. J., Jr. (1998) Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol. 298, 489-496
18. 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, 24-34
19. Orr, A.W., Sanders, J.M., Bevard, M., Coleman, E., Sarembock, I. J., and Schwartz, M. A. (2005) The subendothelial extracellular matrix modulates NF-kappaB activation by flow: a potential role in atherosclerosis. J. Cell Biol. 169, 191-202
20. Pober, J. S., and Sessa, W.C. (2007) Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 7, 803-815
21. Palamakumbura, A. H., and Trackman, P. C. (2002) A fluorometric assay for detection of lysyl oxidase enzyme activity in biological samples. Anal. Biochem. 300, 245-251
22. Fogelgren, B., Polgar, N., Szauter, K. M., Ujfaludi, Z., Laczko, R., Fong, K. S., and Csiszar, K. (2005) Cellular fibronectin binds to lysyl oxidase with high affinity and is critical for its proteolytic activation. J. Biol. Chem. 280, 24690-24697
23. Lefer, D. J., Jones, S. P., Girod, W. G., Baines, A., Grisham, M. B., Cockrell, A. S., Huang, P. L., and Scalia, R. (1999) Leukocyteendothelial cell interactions in nitric oxide synthase-deficient mice. Am. J. Physiol. 276, H1943-H1950
24. Peng, H. B., Libby, P., and Liao, J. K. (1995) Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J. Biol. Chem. 270, 14214-14219
25. DeCaterina, R., Libby, P., Peng, H. B., Thannickal, V. J., Rajavashisth, T. B., Gimbrone, M. A., Jr., Shin, W. S., and Liao, J. K. (1995)Nitric oxidedecreases cytokine-induced endothelial activation;nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J. Clin. Invest. 96, 60-68
26. Hartge, M.M., Unger, T., and Kintscher, U. (2007)The endothelium and vascular inflammation in diabetes. Diab. Vasc. Dis. Res. 4, 84-88
27. Shirwany, N. A., and Zou, M. H. (2012) Vascular inflammation is a missing link for diabetes-enhanced atherosclerotic cardiovascular diseases. Front. Biosci. (Landmark Ed.) 17, 1140-1164
28. Chang, K. C., Tseng, C.D., Chou, T.F., Cho, Y. L., Chi, T.C., Su, M. J., and Tseng, Y.Z. (2006)Arterial stiffening andcardiachypertrophy in a new rat model of type 2 diabetes. Eur. J. Clin. Invest. 36, 1-7
29. Oxlund, H., Rasmussen, L.M., and reassen, T. T., and Heickendorff, L. (1989) Increased aortic stiffness in patients with type 1 (insulindependent) diabetes mellitus. Diabetologia 32, 748-752
30. Huynh, J., Nishimura, N., Rana, K., Peloquin, J. M., Califano, J. P., Montague, C.R., King, M.R., Schaffer, C.B., andReinhart-King, C.A. (2011) Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci. Transl. Med. 3, 112ra122
31. Levental, K. R., Yu, H., Kass, L., Lakins, J.N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W., Yamauchi, M., Gasser, D. L., and Weaver, V. M. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906
32. Goldsbury, C. S., Scheuring, S., and Kreplak, L. (2009) Introduction to atomic force microscopy (AFM) in biology. Curr. Prot. Protein Sci. Chapter 17, Unit 17 17.11-19
33. Trache, A., and Meininger, G. A. (2008) Atomic force microscopy (AFM). Curr Prot. Microbiol. Chapter 2, Unit 2C.2
34. Lehenkari, P. P., Charras, G. T., Nesbitt, S. A., and Horton, M. A. (2000)New technologies in scanning probemicroscopy for studying molecular interactions in cells. Expert Rev. Mol. Med. 2, 1-19
35. Halfter, W., Oertle, P., Monnier, C.A., Camenzind, L., Reyes-Lua, M., Hu, H., Candiello, J., Labilloy, A., Balasubramani, M., Henrich, P. B., and Plodinec, M. (2015) New concepts in basement membrane biology. [E-pub ahead of print] FEBS J. 10.1111/febs.13495
36. Davis, G. E., and Senger, D. R. (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res. 97, 1093-1107
37. Roy, S., Maiello, M., and Lorenzi, M. (1994) Increased expression of basement membrane collagen in human diabetic retinopathy. J. Clin. Invest. 93, 438-442
38. Ljubimov, A. V., Burgeson, R. E., Butkowski, R. J., Couchman, J. R., Zardi, L., Ninomiya, Y., Sado, Y., Huang, Z. S., Nesburn, A. B., and Kenney, M. C. (1996)Basementmembraneabnormalities inhuman eyes with diabetic retinopathy. J. Histochem. Cytochem. 44, 1469-1479
39. Chronopoulos, A., Trudeau, K., Roy, S., Huang, H., Vinores, S. A., and Roy, S. (2011) High glucose-induced altered basement membrane composition and structure increases trans-endothelial permeability: implications for diabetic retinopathy. Curr. Eye Res. 36, 747-753
40. To, M., Goz, A., Camenzind, L., Oertle, P., Candiello, J., Sullivan, M., Henrich, P. B., Loparic, M., Safi, F., Eller, A., and Halfter, W. (2013) Diabetes-induced morphological, biomechanical, and compositional changes in ocular basement membranes. Exp. Eye Res. 116, 298-307
41. Shimizu, M., Minakuchi, K., Moon, M., and Koga, J. (1997) Difference in interaction of fibronectin with type I collagen and type IV collagen. Biochim. Biophys. Acta 1339, 53-61
42. Grant, M. B., Ellis, E. A., Caballero, S., and Mames, R. N. (1996) Plasminogenactivator inhibitor-1overexpressioninnonproliferative diabetic retinopathy. Exp. Eye Res. 63, 233-244
43. Azad, N., Agrawal, L., Emanuele, N. V., Klein, R., Bahn, G. D., McCarren, M., Reaven, P., Hayward, R., Duckworth, W., and Group, V. S.;VADTStudy Group. (2014)Associationof PAI-1 and fibrinogen with diabetic retinopathy in the Veterans Affairs Diabetes Trial (VADT). Diabetes Care 37, 501-506
44. Marchina, E., and Barlati, S. (1996) Degradation of human plasma and extracellular matrix fibronectin by tissue type plasminogen activator and urokinase. Int. J. Biochem. Cell Biol. 28, 1141-1150
45. Brownlee, M. (2005) The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54, 1615-1625
46. Mammoto, A., Connor, K. M., Mammoto, T., Yung, C. W., Huh, D., Aderman, C. M., Mostoslavsky, G., Smith, L. E., and Ingber, D. E. (2009) Amechanosensitive transcriptionalmechanismthat controls angiogenesis. Nature 457, 1103-1108
47. Zheng, L., Howell, S. J., Hatala, D. A., Huang, K., and Kern, T. S. (2007) Salicylate-based anti-inflammatory drugs inhibit the early lesion of diabetic retinopathy. Diabetes 56, 337-345
48. Iliaki, E., Poulaki, V., Mitsiades, N., Mitsiades, C. S., Miller, J.W., and Gragoudas, E. S. (2009) Role of alpha 4 integrin (CD49d) in the pathogenesis of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 50, 4898-4904
49. Palenski, T. L., Sorenson, C. M., and Sheibani, N. (2013) Inflammatory cytokine-specific alterations in retinal endothelial cell function. Microvasc. Res. 89, 57-69
50. Kolluru, G. K., Siamwala, J. H., and Chatterjee, S. (2010) eNOS phosphorylation in health and disease. Biochimie 92, 1186-1198
51. Li, Q., Verma, A., Han, P. Y., Nakagawa, T., Johnson, R. J., Grant, M. B., Campbell-Thompson, M., Jarajapu, Y. P., Lei, B., and Hauswirth, W. W. (2010) Diabetic eNOS-knockout mice develop accelerated retinopathy. Invest. Ophthalmol. Vis. Sci. 51, 5240-5246
52. Das, A., McGuire, P. G., and Rangasamy, S. (2015) Diabeticmacular edema: pathophysiology and novel therapeutic targets. Ophthalmology 122, 1375-1394
53. Bandello, F., Preziosa, C., Querques, G., and Lattanzio, R. (2014) Update of intravitreal steroids for the treatment of diabeticmacular edema. Ophthalmic Res. 52, 89-96
54. ODay, R. F., Barthelmes, D., Zhu, M., Wong, T. Y., McAllister, I. L., Arnold, J. J., and Gillies, M. C. (2014) Intraocular pressure rise is predictive of vision improvement after intravitreal triamcinolone acetonide for diabetic macular oedema: a retrospective analysis of data from a randomised controlled trial. BMC Ophthalmol. 14, 123