Treatment with sulphated galactan inhibits macrophage chemotaxis and reduces intraplaque macrophage content in atherosclerotic mice

Vascular Pharmacology

Volumn 71, Issue , 2015, Pages 84-92

  Gomes Quinderé, Ana Luíza ^a,b   Barros Benevides, Norma Maria ^c   Pelli, Graziano ^d   Lenglet, Sébastien ^d   Burger, Fabienne ^d   Carbone, Federico ^d,e   Fraga Silva, Rodrigo A ^c   Stergiopulos, Nikolaos ^c   Pagano, Sabrina ^f   Bertolotto, Maria ^e   Dallegri, Franco ^e   Vuilleumier, Nicolas ^f   Mach, François ^d   Montecucco, Fabrizio ^d,e,f  

^a MINISTRY OF EDUCATION OF BRAZIL   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c EPFL   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e UNIVERSITY OF GENOA   (Italy)

^f GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Antithrombotic drug; Atherosclerosis; Inflammation; Red alga

Indexed keywords

ANTICOAGULANT AGENT; APOLIPOPROTEIN E; COLLAGEN; FATTY ACID; GELATINASE B; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; SULPHATED GALACTAN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; GALACTAN; GALACTAN POLYSULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICOAGULATION; AORTA ARCH; AORTA ROOT; AORTA SINUS; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MACROPHAGE MIGRATION; MOUSE; NEUTROPHIL; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMOTAXIS; DRUG EFFECTS; KNOCKOUT MOUSE; MACROPHAGE; MONONUCLEAR CELL; PATHOLOGY; PHYSIOLOGY; PLAQUE, ATHEROSCLEROTIC; RED ALGA;

ANIMALS; CELLS, CULTURED; CHEMOTAXIS; GALACTANS; HUMANS; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLAQUE, ATHEROSCLEROTIC; RHODOPHYTA;

EID: 84937970043     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2015.02.015     Document Type: Article

References (37)

1. Murray C.J.L., Vos T., Lozano R., Naghavi M., Flaxman A.D., Michaud C., et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012, 380:2197-2223.
2. Libby P., Lichtman A.H., Hansson G.K. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 2013, 38:1092-1104.
3. Moore K.J., Sheedy F.J., Fisher E.A. Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol 2013, 13:709-721.
4. Garrido-Urbani S., Meguenani M., Montecucco F., Imhof B.A. Immunological aspects of atherosclerosis. Semin Immunopathol 2014, 36:73-91.
5. Sakakura K., Nakano M., Otsuka F., Ladich E., Kolodgie F.D., Virmani R. Pathophysiology of atherosclerosis plaque progression. Heart Lung Circ 2013, 22:399-411.
6. Robbins C.S., Hilgendorf I., Weber G.F., Theurl I., Iwamoto Y., Figueiredo J.L., et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 2013, 19:1166-1172.
7. Steffel J., Luscher T.F., Tanner F.C. Tissue factor in cardiovascular diseases: molecular mechanisms and clinical implications. Circulation 2006, 113:722-731.
8. Morange P., Blankenberg S., Alessi M., Bickel C., Rupprecht H., Schnabel R., et al. Prognostic value of plasma tissue factor and tissue factor pathway inhibitor for cardiovascular death in patients with coronary artery disease: the AtheroGene study. J Thromb Haemost 2007, 5:475-482.
9. Wilcox J., Smith K., Schwartz S., Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci U S A 1989, 86:2839-2843.
10. Thiruvikraman S., Guha A., Roboz J., Taubman M., Nemerson Y., Fallon J. In situ localization of tissue factor in human atherosclerotic plaques by binding of digoxigenin-labeled factors VIIa and X. Lab Invest 1996, 75:451-461.
11. Borissoff J.I., Heeneman S., Kilinc E., Kassak P., Van Oerle R., Winckers K., et al. Early atherosclerosis exhibits an enhanced procoagulant state. Circulation 2010, 122:821-830.
12. Quindere A.L., Fontes B.P., Vanderlei EdSO, Queiroz INLd, Rodrigues JAG, de Araújo IWFd, et al. Peripheral antinociception and anti-edematogenic effect of a sulfated polysaccharide from Acanthophora muscoides. Pharmacol Rep 2013, 65:600-613.
13. Quindere A.L., Santos G.R., Oliveira S.N., Glauser B.F., Fontes B.P., Queiroz I.N., et al. Is the antithrombotic effect of sulfated galactans independent of serpin?. J Thromb Haemost 2014, 12:43-53.
14. Braunersreuther V., Zernecke A., Arnaud C., Liehn E.A., Steffens S., Shagdarsuren E., et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2007, 27:373-379.
15. Montecucco F., Di Marzo V., da Silva R.F., Vuilleumier N., Capettini L., Lenglet S., et al. The activation of the cannabinoid receptor type 2 reduces neutrophilic protease-mediated vulnerability in atherosclerotic plaques. Eur Heart J 2012, 33:846-856.
16. Gao Q., Jiang Y., Ma T., Zhu F., Gao F., Zhang P., et al. A critical function of Th17 proinflammatory cells in the development of atherosclerotic plaque in mice. J Immunol 2010, 185:5820-5827.
17. Montecucco F., Mach F., Lenglet S., Vonlaufen A., Quindere A.L., Pelli G., et al. Treatment with Evasin-3 abrogates neutrophil-mediated inflammation in mouse acute pancreatitis. Eur J Clin Invest 2014, 10.1111/eci.12327.
18. Montecucco F., Vuilleumier N., Pagano S., Lenglet S., Bertolotto M., Braunersreuther V., et al. Anti-Apolipoprotein A-1 auto-antibodies are active mediators of atherosclerotic plaque vulnerability. Eur Heart J 2011, 32:412-421.
19. Satta N., Toti F., Feugeas O., Bohbot A., Dachary-Prigent J., Eschwège V., et al. Monocyte vesiculation is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide. J Immunol 1994, 153:3245-3255.
20. Riches A.C., Sharp J.G., Thomas D.B., Smith S.V. Blood volume determination in the mouse. J Physiol 1973, 228:279-284.
21. Zeini M., Través P.G., López-Fontal R., Pantoja C., Matheu A., Serrano M., et al. Specific contribution of p19(ARF) to nitric oxide-dependent apoptosis. J Immunol 2006, 177:3327-3336.
22. Iqbal A.J., Regan-Komito D., Christou I., White G.E., McNeill E., Kenyon A., et al. A real time chemotaxis assay unveils unique migratory profiles amongst different primary murine macrophages. PLoS One 2013, 8:e58744.
23. Nencioni A., da Silva R.F., Fraga-Silva R.A., Steffens S., Fabre M., Bauer I., et al. Nicotinamide phosphoribosyltransferase inhibition reduces intraplaque CXCL1 production and associated neutrophil infiltration in atherosclerotic mice. Thromb Haemost 2014, 111:308-322.
24. Braunersreuther V., Steffens S., Arnaud C., Pelli G., Burger F., Proudfoot A., et al. A novel RANTES antagonist prevents progression of established atherosclerotic lesions in mice. Arterioscler Thromb Vasc Biol 2008, 28:1090-1096.
25. Montecucco F., Lenglet S., Gayet-Ageron A., Bertolotto M., Pelli G., Palombo D., et al. Systemic and intraplaque mediators of inflammation are increased in patients symptomatic for ischemic stroke. Stroke 2010, 41:1394-1404.
26. Engelberg H. Heparin and atherosclerosis. A review of old and recent findings. Am Heart J 1980, 99:359-372.
27. Elsayed E., Becker R. The impact of heparin compounds on cellular inflammatory responses: a construct for future investigation and pharmaceutical development. J Thromb Thrombolysis 2003, 15:11-18.
28. Guo H., Xu F., Sun A., Liu L., Shi Y. Heparin inhibits the production of matrix metalloproteinase-2 and improves atherosclerosis in LDL receptor-deficient mice. Coron Artery Dis 2010, 21:39-45.
29. Rao N., Argyle B., Xu X., Reynolds P., Walenga J., Prechel M., et al. Low anticoagulant heparin targets multiple sites of inflammation, suppresses heparin-induced thrombocytopenia, and inhibits interaction of RAGE with its ligands. Am J Physiol Cell Physiol 2010, 299:C97-C110.
30. Yla-Herttuala S., Bentzon J.F., Daemen M., Falk E., Garcia-Garcia H.M., Herrmann J., et al. Stabilisation of atherosclerotic plaques. Position paper of the European Society of Cardiology (ESC) Working Group on atherosclerosis and vascular biology. Thromb Haemost 2011, 106:1-19.
31. Mantovani A., Vecchi A., Allavena P. Pharmacological modulation of monocytes and macrophages. Curr Opin Pharmacol 2014, 17C:38-44.
32. Gleissner C.A. Macrophage phenotype modulation by CXCL4 in atherosclerosis. Front Physiol 2012, 3:1.
33. Leitinger N., Schulman I.G. Phenotypic polarization of macrophages in atherosclerosis. Arterioscler Thromb Vasc Biol 2013, 33:1120-1126.
34. Pepe G., Giusti B., Attanasio, Gori A, Comeglio P, Martini F, et al. Tissue factor and plasminogen activator inhibitor type 2 expression in human stimulated monocytes is inhibited by heparin. Semin Thromb Hemost 1997, 23:135-141.
35. Chu A.J. Tissue factor, blood coagulation, and beyond: an overview. Int J Inflamm 2011, 2011:367284.
36. Aberg M., Siegbahn A. Tissue factor non-coagulant signaling - molecular mechanisms and biological consequences with a focus on cell migration and apoptosis. J Thromb Haemost 2013, 11:817-825.
37. Alberelli M.A., De Candia E. Functional role of protease activated receptors in vascular biology. Vascul Pharmacol 2014, 62:72-81.