Extracellular matrix remodelling in response to venous hypertension: Proteomics of human varicose veins

Cardiovascular Research

Volumn 110, Issue 3, 2016, Pages 419-430

  Barallobre Barreiro, Javier ^a   Oklu, Rahmi ^b   Lynch, Marc ^a   Fava, Marika ^a,c   Baig, Ferheen ^a   Yin, Xiaoke ^a   Barwari, Temo ^a   Potier, David N ^a   Albadawi, Hassan ^d   Jahangiri, Marjan ^c   Porter, Karen E ^e   Watkins, Michael T ^d   Misra, Sanjay ^f   Stoughton, Julianne ^d   Mayr, Manuel ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b MAYO CLINIC   (United States)

^c ST GEORGE'S UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF LEEDS   (United Kingdom)

^f MAYO CLINIC   (United States)

Author keywords

Extracellular matrix; Protease; Smooth Muscle; Venous

Indexed keywords

AGGRECAN; AGGRECANASE; BIGLYCAN; CATHEPSIN D; CHYMASE; CLUSTERIN; COLLAGEN TYPE 1; DECORIN; ENTACTIN; FIBROMODULIN; FIBRONECTIN; GALECTIN 1; GALECTIN 3; GELSOLIN; LAMININ; LUMICAN; MIMECAN; NDOGEN 2; PROSAPOSIN; PROTEIN S 100; PROTEINASE; PROTEOGLYCAN; RECOMBINANT ENZYME; SCLEROPROTEIN; SERINE PROTEINASE; SERUM AMYLOID P; THROMBOSPONDIN 1; TRYPTASE; TRYPTASE BETA1; UNCLASSIFIED DRUG; VITRONECTIN;

ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CORONARY ARTERY BYPASS SURGERY; DOWN REGULATION; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROXYLATION; HYPERTENSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MEDICAL RECORD REVIEW; NEOINTIMA; PHLEBECTOMY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEOMICS; SAPHENOUS VEIN; TANDEM MASS SPECTROMETRY; UPREGULATION; VARICOSIS; VEIN DIAMETER; VEIN DISEASE; CASE CONTROL STUDY; CELL CULTURE; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; SMOOTH MUSCLE CELL; VARICOSE VEINS; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE; VENOUS PRESSURE;

CASE-CONTROL STUDIES; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PROTEOLYSIS; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SAPHENOUS VEIN; TANDEM MASS SPECTROMETRY; VARICOSE VEINS; VASCULAR REMODELING; VENOUS PRESSURE;

EID: 84973333027     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvw075     Document Type: Article

References (39)

1. Oklu R, Habito R, Mayr M, Deipolyi AR, Albadawi H, Hesketh R, Walker TG, Linskey KR, Long CA, Wicky S, Stoughton J, Watkins MT. Pathogenesis of varicose veins. J Vasc Interv Radiol 2012;23:33-39.
2. Hamdan A. Management of varicose veins and venous insufficiency. JAMA 2012;308: 2612-2621.
3. Bharath V, Kahn SR, Lazo-Langner A. Genetic polymorphisms of vein wall remodeling in chronic venous disease: a narrative and systematic review. Blood 2014;124:1242-1250.
4. Barallobre-Barreiro J, Didangelos A, Yin X, Doménech N, Mayr M. A sequential extraction methodology for cardiac extracellular matrix prior to proteomics analysis. Methods Mol Biol 2013;1005:215-223.
5. Barallobre-Barreiro J, Didangelos A, Schoendube FA, Drozdov I, Yin X, Fernández-Caggiano M, Willeit P, Puntmann VO, Aldama-López G, Shah AM, Doménech N, Mayr M. Proteomics analysis of cardiac extracellular matrix remodeling in a porcine model of ischemia/reperfusion injury. Circulation 2012;125:789-802.
6. Didangelos A, Yin X, Mandal K, Saje A, Smith A, Xu Q, JahangiriM, Mayr M. Extracellular matrix composition and remodeling in human abdominal aortic aneurysms: a proteomics approach. Mol Cell Proteomics 2011;10:M111. 008128.
7. Didangelos A, Yin X, Mandal K, Baumert M, Jahangiri M, Mayr M. Proteomics characterization of extracellular space components in the human aorta. Mol Cell Proteomics 2010; 9:2048-2062.
8. Stegemann C, Didangelos A, Barallobre-Barreiro J, Langley S, Mandal K, Jahangiri M, Mayr M. Proteomic identification of matrix metalloproteinase substrates in the human vasculature. Circ Cardiovasc Genet 2013;6:106-117.
9. Pokidysheva E, Boudko S, Vranka J, Zientek K, Maddox K, Moser M, Fässler R, Ware J, Bächinger HP. Biological role of prolyl 3-hydroxylation in type IV collagen. Proc Natl Acad Sci USA 2014;111:161-166.
10. Yamauchi M, Sricholpech M. Lysine post-translational modifications of collagen. Essays Biochem 2012;52:113-133.
11. Beebe-Dimmer JL, Pfeifer JR, Engle JS, Schottenfeld D. The epidemiology of chronic venous insufficiency and varicose veins. Ann Epidemiol 2005;15:175-184.
12. McGuckin M, Waterman R, Brooks J, Cherry G, Porten L, Hurley S, Kerstein MD. Validation of venous leg ulcer guidelines in the United States and United Kingdom. Am J Surg 2002;183:132-137.
13. Drozdov I, Didangelos A, Yin X, Zampetaki A, Abonnenc M, Murdoch C, Zhang M, Ouzounis CA, Mayr M, Tsoka S, Shah AM. Gene network and proteomic analyses of cardiac responses to pathological and physiological stress. Circ Cardiovasc Genet 2013; 6:588-597.
14. Wilson R, Norris EL, Brachvogel B, Angelucci C, Zivkovic S, Gordon L, Bernardo BC, Stermann J, Sekiguchi K, Gorman JJ, Bateman JF. Changes in the chondrocyte and extracellular matrix proteome during post-natal mouse cartilage development. Mol Cell Proteomics 2012;11:M111. 014159.
15. Wu YJ, La Pierre DP,Wu J, Yee AJ, Yang BB. The interaction of versican with its binding partners. Cell Res 2005;15:483-494.
16. Higley H, Ksander G, Gerhardt C, Falanga V. Extravasation of macromolecules and possible trapping of transforming growth factor-b in venous ulceration. Br J Dermatol 1995; 132:79-85.
17. Badier-Commander C, Couvelard A, Henin D, Verbeuren T, Michel JB, Jacob MP. Smooth muscle cell modulation and cytokine overproduction in varicose veins. An in situ study. J Pathol 2001;193:398-407.
18. Merline R, Schaefer RM, Schaefer L. The matricellular functions of small leucine-rich proteoglycans (SLRPs). J Cell Commun Signal 2009;3:323-335.
19. Chen S, Birk DE. The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS J 2013;280:2120-2137.
20. Murphy MA, Joyce WP, Condron C, Bouchier-Hayes D. A reduction in serum cytokine levels parallels healing of venous ulcers in patients undergoing compression therapy. Eur J Vasc Endovasc Surg 2002;23:349-352.
21. Kucukguven A, Khalil RA. Matrix metalloproteinases as potential targets in the venous dilation associated with varicose veins. Curr Drug Targets 2013;14:287.
22. Basu R, Lee J, Morton JS, Takawale A, Fan D, Kandalam V, Wang X, Davidge ST, Kassiri Z. TIMP3 is the primary TIMP to regulate agonist-induced vascular remodelling and hypertension. Cardiovasc Res 2013;98:360-371.
23. Kelwick R, Desanlis I, Wheeler GN, Edwards DR. The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family. Genome Biol 2015;16:113.
24. Kinoshita M, Okada M, Hara M, Furukawa Y, Matsumori A. Mast cell tryptase in mast cell granules enhances MCP-1 and interleukin-8 production in human endothelial cells. Arterioscler Thromb Vasc Biol 2005;25:1858-1863.
25. Leskinen M, Wang Y, Leszczynski D, Lindstedt KA, Kovanen PT. Mast cell chymase induces apoptosis of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2001; 21:516-522.
26. Haviarová Z, Weismann P, Pavlíková D, Durdík Š, Kováč P,ŠtvrtinováV, Mráz P. Mast cell infiltration in the wall of varicose veins. Acta Histochem 2002;104:357-360.
27. Sayer G, Smith P. Immunocytochemical characterisation of the inflammatory cell infiltrate of varicose veins. Eur J Vasc Endovasc Surg 2004;28:479-483.
28. Guo C, Ju H, Leung D, Massaeli H, Shi M, Rabinovitch M. A novel vascular smooth muscle chymase is upregulated in hypertensive rats. J Clin Invest 2001;107:703.
29. Ju H, Gros R, You X, Tsang S, Husain M, Rabinovitch M. Conditional and targeted overexpression of vascular chymase causes hypertension in transgenic mice. Proc Natl Acad Sci USA 2001;98:7469-7474.
30. Shankman LS, Gomez D, Cherepanova OA, Salmon M, Alencar GF, Haskins RM, Swiatlowska P, Newman AA, Greene ES, Straub AC, Isakson B, Randolph GJ, Owens GK. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med 2015;21:628-637.
31. Miyazaki M, Takai S, Jin D, Muramatsu M. Pathological roles of angiotensin II produced by mast cell chymase and the effects of chymase inhibition in animal models. Pharmacol Ther 2006;112:668-676.
32. Waern I, Jonasson S, Hjoberg J, Bucht A, A brink M, Pejler G, Wernersson S. Mouse mast cell protease 4 is the major chymase in murine airways and has a protective role in allergic airway inflammation. J Immunol 2009;183:6369-6376.
33. Leskinen MJ, HeikkiläHM, Speer MY, Hakala JK, Laine M, Kovanen PT, Lindstedt KA. Mast cell chymase induces smooth muscle cell apoptosis by disrupting NF-kB-mediated survival signaling. Exp Cell Res 2006;312:1289-1298.
34. Leskinen MJ, Lindstedt KA, Wang Y, Kovanen PT, Lindstedt KA. Mast cell chymase induces smooth muscle cell apoptosis by a mechanism involving fibronectin degradation and disruption of focal adhesions. Arterioscler Thromb Vasc Biol 2003;23:238-243.
35. Kokkonen JO, Lindstedt KA, Kovanen PT. Role for chymase in heart failure angiotensin II-dependent or-independent mechanisms? Circulation 2003;107:2522-2524.
36. Pfisterer L, Meyer R, Feldner A, Drews O, Hecker M, Korff T. Bortezomib protects from varicose-like venous remodeling. FASEB J 2014;28:3518-3527.
37. Metzler B, Xu Q. The role of mast cells in atherosclerosis. Int Arch Allergy Immunol 1997; 114:10-14.
38. Sun J, Zhang J, Lindholt JS, Sukhova GK, Liu J, He A, A brink M, Pejler G, Stevens RL, ThompsonRW, Ennis TL, Gurish MF, Libby P, Shi G-P. Critical role of mast cell chymase in mouse abdominal aortic aneurysm formation. Circulation 2009;120:973-982.
39. Xu N, Zhang Y-Y, Lin Y, Bao B, Zheng L, Shi G-P, Liu J. Increased levels of lysosomal cysteinyl cathepsins in human varicose veins: a histology study. Thromb Haemost 2014;111:333-344.