Matrix ageing and vascular impacts: Focus on elastin fragmentation

Cardiovascular Research

Volumn 110, Issue 3, 2016, Pages 298-308

  Duca, Laurent ^a   Blaise, Sébastien ^a   Romier, Béatrice ^a   Laffargue, Muriel ^b   Gayral, Stéphanie ^b   El Btaouri, Hassan ^a   Kawecki, Charlotte ^a   Guillot, Alexandre ^a   Martiny, Laurent ^a   Debelle, Laurent ^a   Maurice, Pascal ^a  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^b Université de Toulouse   (France)

Author keywords

Ageing; Elastin fragmentation; Extracellular matrix remodelling; Vascular diseases

Indexed keywords

COLLAGEN; ELASTASE; ELASTIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; RECEPTOR PROTEIN; SIALIDASE; CARDIOVASCULAR AGENT; GLYCOSIDASE INHIBITOR; NEU1 PROTEIN, HUMAN; PANCREATIC ELASTASE; PEPTIDE FRAGMENT; SERINE PROTEINASE INHIBITOR;

AGING; BLOOD VESSEL WALL; BODY FLUID; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; VASCULAR DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTERY; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; SIGNAL TRANSDUCTION; VASCULAR DISEASES;

AGING; ANIMALS; ARTERIES; CARDIOVASCULAR AGENTS; ELASTIN; EXTRACELLULAR MATRIX; GLYCOSIDE HYDROLASE INHIBITORS; HUMANS; MOLECULAR TARGETED THERAPY; NEURAMINIDASE; PANCREATIC ELASTASE; PEPTIDE FRAGMENTS; PROTEOLYSIS; SERINE PROTEINASE INHIBITORS; SIGNAL TRANSDUCTION; VASCULAR DISEASES;

EID: 84973341518     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvw061     Document Type: Review

References (120)

1. Davidson JM, Hill KE, Mason ML, Giro MG. Longitudinal gradients of collagen and elastin gene expression in the porcine aorta. J Biol Chem 1985;260:1901-1908.
2. Brooke BS, Bayes-Genis A, LiDY. New insights into elastin and vascular disease. Trends Cardiovasc Med 2003;13:176-181.
3. Clark JM, Glagov S. Transmural organization of the arterial media. The lamellar unit revisited. Arteriosclerosis 1985;5:19-34.
4. Shapiro SD, Endicott SK, Province MA, Pierce JA, Campbell EJ. Marked longevity of human lung parenchymal elastic fibers deduced from prevalence of D-aspartate and nuclear weapons-related radiocarbon. J Clin Invest 1991;87:1828-1834.
5. Todorovich-Hunter L, Johnson DJ, Ranger P, Keeley FW, Rabinovitch M. Altered elastin and collagen synthesis associated with progressive pulmonary hypertension induced by monocrotaline. A biochemical and ultrastructural study. Lab Invest 1988; 58:184-195.
6. Yu BP. Aging and oxidative stress: modulation by dietary restriction. Free Radic Biol Med 1996;21:651-668.
7. Nilsson PM, Lurbe E, Laurent S. The early life origins of vascular ageing and cardiovascular risk: the EVA syndrome. J Hypertens 2008;26:1049-1057.
8. Greenwald SE. Ageing of the conduit arteries. J Pathol 2007;211:157-172.
9. Dobrin PB, Schwarcz TH, Baker WH. Mechanisms of arterial and aneurysmal tortuosity. Surgery 1988;104:568-571.
10. Dao HH, Essalihi R, Bouvet C, Moreau P. Evolution and modulation of age-related medial elastocalcinosis: impact on large artery stiffness and isolated systolic hypertension. Cardiovasc Res 2005;66:307-317.
11. Shao JS, Cai J, Towler DA. Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arterioscler Thromb Vasc Biol 2006;26:1423-1430.
12. Aronson D. Cross-linking of glycated collagen in the pathogenesis of arterial and myocardial stiffening of aging and diabetes. J Hypertens 2003;21:3-12.
13. Wang M, Kim SH, Monticone RE, Lakatta EG. Matrix metalloproteinases promote arterial remodeling in aging, hypertension, and atherosclerosis. Hypertension 2015;65: 698-703.
14. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F et al. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 2007;128:92-105.
15. Wang M, Jiang L, Monticone RE, Lakatta EG. Proinflammation: the key to arterial aging. Trends Endocrinol Metab 2014;25:72-79.
16. El Assar M, Angulo J, Rodriguez-Manas L. Oxidative stress and vascular inflammation in aging. Free Radic Biol Med 2013;65:380-401.
17. O'Rourke MF, Safar ME, Dzau V. The Cardiovascular Continuum extended: aging effects on the aorta and microvasculature. Vasc Med 2010;15:461-468.
18. Schiffmann E, Lavender DR, Miller EJ, Corcoran BA. Amino acids at the nucleating site in mineralizing elastic tissue. Calcif Tissue Res 1969;3:125-135.
19. Perrotta I, Russo E, Camastra C, Filice G, Di Mizio G, Colosimo F et al. New evidence for a critical role of elastin in calcification of native heart valves: immunohistochemical and ultrastructural study with literature review. Histopathology 2011;59:504-513.
20. Tanaka N, Tajima S, Ishibashi A, Uchida K, Shigematsu T. Immunohistochemical detection of lipid peroxidation products, protein-bound acrolein and 4-hydroxynonenal protein adducts, in actinic elastosis of photodamaged skin. Arch Dermatol Res 2001; 293:363-367.
21. Yamamoto Y, Sakata N, Meng J, Sakamoto M, Noma A, Maeda I et al. Possible involvement of increased glycoxidation and lipid peroxidation of elastin in atherogenesis in haemodialysis patients. Nephrol Dial Transplant 2002;17:630-636.
22. Zarkovic K, Larroque-Cardoso P, Pucelle M, Salvayre R, Waeg G, Negre-Salvayre A et al. Elastin aging and lipid oxidation products in human aorta. Redox Biol 2015;4: 109-117.
23. Konova E, Baydanoff S, Atanasova M, Velkova A. Age-related changes in the glycation of human aortic elastin. Exp Gerontol 2004;39:249-254.
24. Gorisse L, Pietrement C, Vuiblet V, Schmelzer CE, Kohler M, Duca L et al. Protein carbamylation is a hallmark of aging. Proc Natl Acad Sci USA 2016;113:1191-1196.
25. Gargiulo S, Gamba P, Poli G, Leonarduzzi G. Metalloproteinases and metalloproteinase inhibitors in age-related diseases. Curr Pharm Des 2014;20:2993-3018.
26. Maurice P, Blaise S, Gayral S, Debelle L, Laffargue M, HornebeckWet al. Elastin fragmentation and atherosclerosis progression: the elastokine concept. Trends Cardiovasc Med 2013;23:211-221.
27. Brassart B, Fuchs P, Huet E, Alix AJ, Wallach J, Tamburro AM et al. Conformational dependence of collagenase (matrix metalloproteinase-1) up-regulation by elastin peptides in cultured fibroblasts. J Biol Chem 2001;276:5222-5227.
28. Heinz A, Jung MC, Jahreis G, Rusciani A, Duca L, Debelle L et al. The action of neutrophil serine proteases on elastin and its precursor. Biochimie 2012;94:192-202.
29. Heinz A, Taddese S, Sippl W, Neubert RH, Schmelzer CE. Insights into the degradation of human elastin by matrilysin-1. Biochimie 2010;93:187-194.
30. Lee P, Bax DV, Bilek MM,Weiss AS. A novel cell adhesion region in tropoelastin mediates attachment to integrin alphaVbeta5. J Biol Chem 2014;289:1467-1477.
31. Rodgers UR,Weiss AS. Integrin alpha v beta 3 binds a unique non-RGD site near the C-terminus of human tropoelastin. Biochimie 2004;86:173-178.
32. Maeda I, Mizoiri N, Briones MP, Okamoto K. Induction of macrophage migration through lactose-insensitive receptor by elastin-derived nonapeptides and their analog. J Pept Sci 2007;13:263-268.
33. Pocza P, Suli-Vargha H, Darvas Z, Falus A. Locally generated VGVAPG and VAPG elastin-derived peptides amplify melanoma invasion via the galectin-3 receptor. Int J Cancer 2008;122:1972-1980.
34. Hinek A, Pshezhetsky AV, von Itzstein M, Starcher B. Lysosomal sialidase (neuraminidase-1) is targeted to the cell surface in a multiprotein complex that facilitates elastic fiber assembly. J Biol Chem 2006;281:3698-3710.
35. Blanchevoye C, Floquet N, Scandolera A, Baud S, Maurice P, Bocquet O et al. Interaction between the elastin peptide VGVAPG and human elastin binding protein. J Biol Chem 2013;288:1317-1328.
36. Duca L, Blanchevoye C, Cantarelli B, Ghoneim C, Dedieu S, Delacoux F et al. The elastin receptor complex transduces signals through the catalytic activity of its Neu-1 subunit. J Biol Chem 2007;282:12484-12491.
37. Rusciani A, Duca L, Sartelet H, Chatron-Colliet A, Bobichon H, Ploton D et al. Elastin peptides signalling relies on neuraminidase-1-dependent lactosylceramide generation. PLoS One 2010;5:e14010.
38. Duca L, Lambert E, Debret R, Rothhut B, Blanchevoye C, Delacoux F et al. Elastin peptides activate extracellular signal-regulated kinase 1/2 via a Ras-independent mechanism requiring both p110gamma/Raf-1 and protein kinase A/B-Raf signalling in human skin fibroblasts. Mol Pharmacol 2005;67:1315-1324.
39. Mochizuki S, Brassart B, Hinek A. Signalling pathways transduced through the elastin receptor facilitate proliferation of arterial smooth muscle cells. J Biol Chem 2002;277: 44854-44863.
40. Fahem A, Robinet A, Cauchard JH, Duca L, Soula-Rothhut M, Rothhut B et al. Elastokine-mediated up-regulation of MT1-MMP is triggered by nitric oxide in endothelial cells. Int J Biochem Cell Biol 2008;40:1581-1596.
41. Varga Z, Jacob MP, Robert L, Csongor J, Fulop T Jr. Age-dependent changes of K-elastin stimulated effector functions of human phagocytic cells: relevance for atherogenesis. Exp Gerontol 1997;32:653-662.
42. Scandolera A, Rabenoelina F, Chaintreuil C, Rusciani A, Maurice P, Blaise S et al. Uncoupling of elastin complex receptor during in vitro aging is related to modifications in its intrinsic sialidase activity and the subsequent lactosylceramide production. PLoS One 2015;10:e0129994.
43. Bizbiz L, Alperovitch A, Robert L. Aging of the vascular wall: serum concentration of elastin peptides and elastase inhibitors in relation to cardiovascular risk factors. The EVA study. Atherosclerosis 1997;131:73-78.
44. Fulop T Jr,Wei SM, Robert L, Jacob MP. Determination of elastin peptides in normal and arteriosclerotic human sera by ELISA. Clin Physiol Biochem 1990;8:273-282.
45. Hong YJ, Kim J, Oh BR, Lee YJ, Lee EY, Lee EB et al. Serum elastin-derived peptides and anti-elastin antibody in patients with systemic sclerosis. J Korean Med Sci 2012;27: 484-488.
46. Shinohara T, Okada M, Suzuki K, Ohsuzu F, Katayama M. Quantitative analysis for soluble elastin in circulation and cell culture fluids using monoclonal antibody-based sandwich immunoassay. J Immunoassay Immunochem 2005;26:189-202.
47. Wei SM, Erdei J, Fulop T Jr, Robert L, Jacob MP. Elastin peptide concentration in human serum: variation with antibodies and elastin peptides used for the enzyme-linked immunosorbent assay. J Immunol Methods 1993;164:175-187.
48. Lamerz J, Friedlein A, Soder N, Cutler P, Dobeli H. Determination of free desmosine in human plasma and its application in two experimental medicine studies. Anal Biochem 2013;436:127-136.
49. Ma S, Turino GM, Hayashi T, Yanuma H, Usuki T, Lin YY. Stable deuterium internal standard for the isotope-dilution LC-MS/MS analysis of elastin degradation. Anal Biochem 2013;440:158-165.
50. Miliotis T, Lindberg C, Semb KF, van Geest M, Kjellstrom S. Quantitative highperformance liquid chromatography-tandem mass spectrometry method for the analysis of free desmosines in plasma and urine. J Chromatogr A 2013;1308:73-78.
51. Schrader CU, Heinz A, Majovsky P, Schmelzer CE. Fingerprinting desmosinecontaining elastin peptides. J Am Soc Mass Spectrom 2015;26:762-773.
52. Yamanaka H, Osaka M, Takayama M, Munakata K, Nejima J, Katayama M. Age-adjusted level of circulating elastin as a cardiovascular risk factor in medical check-up individuals. J Cardiovasc Med (Hagerstown) 2014;15:364-370.
53. Smith ER, Tomlinson LA, Ford ML, McMahon LP, Rajkumar C, Holt SG. Elastin degradation is associated with progressive aortic stiffening and all-cause mortality in predialysis chronic kidney disease. Hypertension 2012;59:973-978.
54. Sun Z. Aging, arterial stiffness, and hypertension. Hypertension 2015;65:252-256.
55. Wagenseil JE, Mecham RP. Elastin in large artery stiffness and hypertension. J Cardiovasc Transl Res 2012;5:264-273.
56. Wagenseil JE, Ciliberto CH, Knutsen RH, Levy MA, Kovacs A, Mecham RP. Reduced vessel elasticity alters cardiovascular structure and function in newborn mice. Circ Res 2009;104:1217-1224.
57. Faury G, Pezet M, Knutsen RH, BoyleWA, Heximer SP, McLean SE et al. Developmental adaptation of the mouse cardiovascular system to elastin haploinsufficiency. J Clin Invest 2003;112:1419-1428.
58. Le VP, Knutsen RH, Mecham RP, Wagenseil JE. Decreased aortic diameter and compliance precedes blood pressure increases in postnatal development of elastininsufficient mice. Am J Physiol Heart Circ Physiol 2011;301:H221-H229.
59. Hirano E, Knutsen RH, Sugitani H, Ciliberto CH, Mecham RP. Functional rescue of elastin insufficiency in mice by the human elastin gene: implications for mouse models of human disease. Circ Res 2007;101:523-531.
60. Aggoun Y, Sidi D, Levy BI, Lyonnet S, Kachaner J, Bonnet D. Mechanical properties of the common carotid artery in Williams syndrome. Heart 2000;84:290-293.
61. Lacolley P, Boutouyrie P, Glukhova M, Daniel Lamaziere JM, Plouin PF, Bruneval P et al. Disruption of the elastin gene in adult Williams syndrome is accompanied by a paradoxical reduction in arterial stiffness. Clin Sci (Lond) 2002;103:21-29.
62. Urban Z, Riazi S, Seidl TL, Katahira J, Smoot LB, Chitayat D et al. Connection between elastin haploinsufficiency and increased cell proliferation in patients with supravalvular aortic stenosis and Williams-Beuren syndrome. Am J Hum Genet 2002;71:30-44.
63. Khavandgar Z, Roman H, Li J, Lee S, Vali H, Brinckmann J et al. Elastin haploinsufficiency impedes the progression of arterial calcification in MGP-deficient mice. J Bone Miner Res 2014;29:327-337.
64. Nikolov A, Tsinlikov I, Nicoloff G, Tsinlikova I, Blazhev A, Garev A. Abnormal levels of age-elastin derived peptides in sera of diabetic patients with arterial hypertension. Cent Eur J Immunol 2014;39:345-351.
65. Newby AC. Matrix metalloproteinase inhibition therapy for vascular diseases. Vascul Pharmacol 2012;56:232-244.
66. Lafarge JC, Naour N, Clement K, Guerre-Millo M. Cathepsins and cystatin C in atherosclerosis and obesity. Biochimie 2010;92:1580-1586.
67. Van der Donckt C, Van Herck JL, Schrijvers DM, Vanhoutte G, Verhoye M, Blockx I et al. Elastin fragmentation in atherosclerotic mice leads to intraplaque neovascularization, plaque rupture, myocardial infarction, stroke, and sudden death. Eur Heart J 2015; 36:1049-1058.
68. Van Herck JL, De Meyer GR, MartinetW, Van Hove CE, Foubert K, Theunis MH et al. Impaired fibrillin-1 function promotes features of plaque instability in apolipoprotein E-deficient mice. Circulation 2009;120:2478-2487.
69. Gayral S, Garnotel R, Castaing-Berthou A, Blaise S, Fougerat A, Berge E et al. Elastinderived peptides potentiate atherosclerosis through the immune Neu1-PI3Kgamma pathway. Cardiovasc Res 2014;102:118-127.
70. Seyrantepe V, Hinek A, Peng J, Fedjaev M, Ernest S, Kadota Y et al. Enzymatic activity of lysosomal carboxypeptidase (cathepsin) A is required for proper elastic fiber formation and inactivation of endothelin-1. Circulation 2008;117:1973-1981.
71. Seyrantepe V, Iannello A, Liang F, Kanshin E, Jayanth P, Samarani S et al. Regulation of phagocytosis in macrophages by neuraminidase 1. J Biol Chem 2010;285:206-215.
72. Johnson JL. Emerging regulators of vascular smooth muscle cell function in the development and progression of atherosclerosis. Cardiovasc Res 2014;103:452-460.
73. Ooyama T, Fukuda K, Oda H, Nakamura H, Hikita Y. Substratum-bound elastin peptide inhibits aortic smooth muscle cell migration in vitro. Arteriosclerosis 1987;7: 593-598.
74. Simionescu A, Philips K, Vyavahare N. Elastin-derived peptides and TGF-beta1 induce osteogenic responses in smooth muscle cells. Biochem Biophys Res Commun 2005;334: 524-532.
75. Simionescu A, Simionescu DT, Vyavahare NR. Osteogenic responses in fibroblasts activated by elastin degradation products and transforming growth factor-beta1: role of myofibroblasts in vascular calcification. Am J Pathol 2007;171:116-123.
76. Kent KC. Clinical practice. Abdominal aortic aneurysms. N Engl J Med 2014;371: 2101-2108.
77. Qin Y, Cao X, Guo J, Zhang Y, Pan L, Zhang H et al. Deficiency of cathepsin S attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Cardiovasc Res 2012;96:401-410.
78. Sun J, Sukhova GK, Zhang J, Chen H, Sjoberg S, Libby P et al. Cathepsin K deficiency reduces elastase perfusion-induced abdominal aortic aneurysms in mice. Arterioscler Thromb Vasc Biol 2012;32:15-23.
79. Sun J, Sukhova GK, Zhang J, Chen H, Sjoberg S, Libby P et al. Cathepsin L activity is essential to elastase perfusion-induced abdominal aortic aneurysms in mice. Arterioscler Thromb Vasc Biol 2011;31:2500-2508.
80. Hellenthal FA, BuurmanWA, WodzigWK, Schurink GW. Biomarkers of AAA progression. Part 1: extracellular matrix degeneration. Nat Rev Cardiol 2009;6: 464-474.
81. Hance KA, Tataria M, Ziporin SJ, Lee JK, Thompson RW. Monocyte chemotactic activity in human abdominal aortic aneurysms: role of elastin degradation peptides and the 67-kD cell surface elastin receptor. J Vasc Surg 2002;35:254-261.
82. Guo G, Booms P, Halushka M, Dietz HC, Ney A, Stricker S et al. Induction of macrophage chemotaxis by aortic extracts of the mgR Marfan mouse model and a GxxPG-containing fibrillin-1 fragment. Circulation 2006;114:1855-1862.
83. Guo G, Munoz-Garcia B, Ott CE, Grunhagen J, Mousa SA, Pletschacher A et al. Antagonism of GxxPG fragments ameliorates manifestations of aortic disease in Marfan syndrome mice. Hum Mol Genet 2013;22:433-443.
84. Smyth S, Heron A. Diabetes and obesity: the twin epidemics. Nat Med 2006;12: 75-80.
85. Hopps E, Caimi G. Matrix metalloproteinases in metabolic syndrome. Eur J Intern Med 2012;23:99-104.
86. Nicoloff G, Nikolov A, Dekov D. Serum AGE-elastin derived peptides among diabetic children. Vascul Pharmacol 2005;43:193-197.
87. Nicoloff G, Petrova C, Christova P, Nikolov A. Detection of free elastin-derived peptides among diabetic children. Atherosclerosis 2007;192:342-347.
88. Nicoloff G, Baydanoff S, Stanimirova N, Petrova C, Christova P. An association of antielastin IgA antibodies with development of retinopathy in diabetic children. Gen Pharmacol 2000;35:83-87.
89. Nicoloff G, Blazhev A, Petrova C, Christova P, Jordanova-Laleva P, Dekov D et al. Detection of free antielastin antibodies among diabetic children. J Investig Med 2005;53: 128-134.
90. Lafarge JC, Pini M, Pelloux V, Orasanu G, Hartmann G, Venteclef N et al. Cathepsin S inhibition lowers blood glucose levels in mice. Diabetologia 2014;57:1674-1683.
91. Talukdar S, Oh da Y, Bandyopadhyay G, LiD, Xu J, McNelis J et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012; 18:1407-1412.
92. Mansuy-Aubert V, Zhou QL, Xie X, Gong Z, Huang JY, Khan AR et al. Imbalance between neutrophil elastase and its inhibitor alpha1-antitrypsin in obesity alters insulin sensitivity, inflammation, and energy expenditure. Cell Metab 2013;17: 534-548.
93. Blaise S, Romier B, Kawecki C, Ghirardi M, Rabenoelina F, Baud S et al. Elastin-derived peptides are new regulators of insulin resistance development in mice. Diabetes 2013; 62:3807-3816.
94. Kawecki C, Hezard N, Bocquet O, Poitevin G, Rabenoelina F, Kauskot A et al. Elastinderived peptides are new regulators of thrombosis. Arterioscler Thromb Vasc Biol 2014; 34:2570-2578.
95. Esmon CT, Esmon NL. The link between vascular features and thrombosis. Annu Rev Physiol 2011;73:503-514.
96. Alam SR, Newby DE, Henriksen PA. Role of the endogenous elastase inhibitor, elafin, in cardiovascular injury: from epithelium to endothelium. Biochem Pharmacol 2012;83: 695-704.
97. Ohta K, Nakajima T, Cheah AY, Zaidi SH, Kaviani N, Dawood F et al. Elafin-overexpressing mice have improved cardiac function after myocardial infarction. Am J Physiol Heart Circ Physiol 2004;287:H286-H292.
98. Zaidi SH, You XM, Ciura S, O'Blenes S, Husain M, Rabinovitch M. Suppressed smooth muscle proliferation and inflammatory cell invasion after arterial injury in elafin-overexpressing mice. J Clin Invest 2000;105:1687-1695.
99. Alam SR, Lewis SC, Zamvar V, Pessotto R, Dweck MR, Krishan A et al. Perioperative elafin for ischaemia-reperfusion injury during coronary artery bypass graft surgery: a randomised-controlled trial. Heart 2015;101:1639-1645.
100. Fields GB. New strategies for targeting matrix metalloproteinases. Matrix Biol 2015; 44-46:239-246.
101. Wijkmans J, Gossen J. Inhibitors of cathepsin K: a patent review (2004-2010). Expert Opin Ther Pat 2011;21:1611-1629.
102. Fonovic M, Turk B. Cysteine cathepsins and extracellular matrix degradation. Biochim Biophys Acta 2014;1840:2560-2570.
103. Samokhin AO, Wilson S, Nho B, Lizame ML, Musenden OE, Bromme D. Cholatecontaining high-fat diet induces the formation of multinucleated giant cells in atherosclerotic plaques of apolipoprotein E2/2 mice. Arterioscler Thromb Vasc Biol 2010;30: 1166-1173.
104. Robinet A, Millart H, Oszust F, HornebeckW, Bellon G. Binding of elastin peptides to S-Gal protects the heart against ischaemia/reperfusion injury by triggering the RISK pathway. FASEB J 2007;21:1968-1978.
105. Toupance S, Brassart B, Rabenoelina F, Ghoneim C, Vallar L, Polette M et al. Elastin-derived peptides increase invasive capacities of lung cancer cells by posttranscriptional regulation of MMP-2 and uPA. Clin Exp Metastasis 2012;29: 511-522.
106. Antonicelli F, Bellon G, Debelle L, HornebeckW. Elastin-elastases and inflamm-aging. Curr Top Dev Biol 2007;79:99-155.
107. Magesh S, Savita V, Moriya S, Suzuki T, Miyagi T, Ishida H et al. Human sialidase inhibitors: design, synthesis, and biological evaluation of 4-acetamido-5-acylamido-2-fluoro benzoic acids. Bioorg Med Chem 2009;17:4595-4603.
108. O'Shea LK, Abdulkhalek S, Allison S, Neufeld RJ, Szewczuk MR. Therapeutic targeting of Neu1 sialidase with oseltamivir phosphate (Tamiflu(R)) disables cancer cell survival in human pancreatic cancer with acquired chemoresistance. Onco Targets Ther 2014;7: 117-134.
109. Fougerat A, Gayral S, Malet N, Briand-Mesange F, Breton-Douillon M, Laffargue M. Phosphoinositide 3-kinases and their role in inflammation: potential clinical targets in atherosclerosis? Clin Sci (Lond) 2009;116:791-804.
110. Puri KD, Doggett TA, Huang CY, Douangpanya J, Hayflick JS, Turner M et al. The role of endothelial PI3Kgamma activity in neutrophil trafficking. Blood 2005;106: 150-157.
111. Fougerat A, Smirnova NF, Gayral S, Malet N, Hirsch E, Wymann MP et al. Key role of PI3Kgamma in monocyte chemotactic protein-1-mediated amplification of PDGF-induced aortic smooth muscle cell migration. Br J Pharmacol 2012;166: 1643-1653.
112. Lupieri A, Smirnova N, Malet N, Gayral S, Laffargue M. PI3K signalling in arterial diseases: non redundant functions of the PI3K isoforms. Adv Biol Regul 2015;59: 4-18.
113. Fougerat A, Gayral S, Gourdy P, Schambourg A, Ruckle T, Schwarz MK et al. Genetic and pharmacological targeting of phosphoinositide 3-kinase-gamma reduces atherosclerosis and favors plaque stability by modulating inflammatory processes. Circulation 2008;117:1310-1317.
114. Smirnova NF, Gayral S, Pedros C, Loirand G, Vaillant N, Malet N et al. Targeting PI3Kgamma activity decreases vascular trauma-induced intimal hyperplasia through modulation of the Th1 response. J Exp Med 2014;211:1779-1792.
115. Amith SR, Jayanth P, Franchuk S, Finlay T, Seyrantepe V, Beyaert R et al. Neu1 desialylation of sialyl alpha-2,3-linked beta-galactosyl residues of TOLL-like receptor 4 is essential for receptor activation and cellular signalling. Cell Signal 2010;22: 314-324.
116. Jayanth P, Amith SR, Gee K, Szewczuk MR. Neu1 sialidase and matrix metalloproteinase-9 cross-talk is essential for neurotrophin activation of Trk receptors and cellular signalling. Cell Signal 2010;22:1193-1205.
117. Hinek A, Bodnaruk TD, Bunda S,Wang Y, Liu K. Neuraminidase-1, a subunit of the cell surface elastin receptor, desialylates and functionally inactivates adjacent receptors interacting with the mitogenic growth factors PDGF-BB and IGF-2. Am J Pathol 2008; 173:1042-1056.
118. Lillehoj EP, Hyun SW, Feng C, Zhang L, Liu A, Guang W et al. NEU1 sialidase expressed in human airway epithelia regulates epidermal growth factor receptor (EGFR) and MUC1 protein signalling. J Biol Chem 2012;287:8214-8231.
119. Lee C, Liu A, Miranda-Ribera A, Hyun SW, Lillehoj EP, Cross AS et al. NEU1 sialidase regulates the sialylation state of CD31 and disrupts CD31-driven capillary-like tube formation in human lung microvascular endothelia. J Biol Chem 2014;289: 9121-9135.
120. Pshezhetsky AV, Hinek A. Where catabolism meets signalling: neuraminidase 1 as a modulator of cell receptors. Glycoconj J 2011;28:441-452.