Abnormal high-density lipoprotein induces endothelial dysfunction via activation of toll-like receptor-2

Immunity

Volumn 38, Issue 4, 2013, Pages 754-768

  Speer, Thimoteus ^a,b   Rohrer, Lucia ^c,d   Blyszczuk, Przemyslaw ^a   Shroff, Rukshana ^e,f   Kuschnerus, Kira ^a   Kränkel, Nicolle ^a   Kania, Gabriela ^a   Zewinger, Stephen ^b   Akhmedov, Alexander ^a   Shi, Yi ^a   Martin, Tina ^b   Perisa, Damir ^d   Winnik, Stephan ^a   Müller, Maja F ^a   Sester, Urban ^b   Wernicke, Gabriel ^b   Jung, Andreas ^b   Gutteck, Ursula ^d   Eriksson, Urs ^a,g   Geisel, Jürgen ^b   Deanfield, John ^f   von Eckardstein, Arnold ^c,d   Lüscher, Thomas F ^a,c   Fliser, Danilo ^b   Bahlmann, Ferdinand H ^b   Landmesser, Ulf ^a,c   more..

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b SAARLAND UNIVERSITY   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f Renal Unit   (United Kingdom)

^g GZO Spital Wetzikon ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; HIGH DENSITY LIPOPROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6;

ADULT; ARTERIAL PRESSURE; ARTICLE; BIOAVAILABILITY; BIOTRANSFORMATION; BLOOD PRESSURE MEASUREMENT; CARDIOVASCULAR RISK; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; FEMALE; HIGH RISK POPULATION; HUMAN; HYPERTENSION; INNATE IMMUNITY; MALE; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE; VASCULAR ENDOTHELIUM;

ADULT; ANIMALS; ARGININE; ARTERIAL PRESSURE; ATHEROSCLEROSIS; CHILD; ENDOTHELIUM; HUMANS; HYPERTENSION; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; KIDNEY DISEASES; LIPOPROTEINS, HDL; MICE; MICE, INBRED C57BL; NITRIC OXIDE; SIGNAL TRANSDUCTION; SUPEROXIDES; TOLL-LIKE RECEPTOR 2; WOUND HEALING;

EID: 84876780604     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.02.009     Document Type: Article

References (63)

1. Acton S., Rigotti A., Landschulz K.T., Xu S., Hobbs H.H., Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 1996, 271:518-520.
2. Alexopoulou L., Thomas V., Schnare M., Lobet Y., Anguita J., Schoen R.T., Medzhitov R., Fikrig E., Flavell R.A. Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1- and TLR2-deficient mice. Nat. Med. 2002, 8:878-884.
3. Assanasen C., Mineo C., Seetharam D., Yuhanna I.S., Marcel Y.L., Connelly M.A., Williams D.L., de la Llera-Moya M., Shaul P.W., Silver D.L. Cholesterol binding, efflux, and a PDZ-interacting domain of scavenger receptor-BI mediate HDL-initiated signaling. J. Clin. Invest. 2005, 115:969-977.
4. Barter P.J., Caulfield M., Eriksson M., Grundy S.M., Kastelein J.J., Komajda M., Lopez-Sendon J., Mosca L., Tardif J.C., Waters D.D., et al. Effects of torcetrapib in patients at high risk for coronary events. N. Engl. J. Med. 2007, 357:2109-2122. ILLUMINATE Investigators.
5. Beaulieu L.M., Lin E., Morin K.M., Tanriverdi K., Freedman J.E. Regulatory effects of TLR2 on megakaryocytic cell function. Blood 2011, 117:5963-5974.
6. Berenson G.S., Srinivasan S.R., Bao W., Newman W.P., Tracy R.E., Wattigney W.A. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N. Engl. J. Med. 1998, 338:1650-1656.
7. Beutler B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 2004, 430:257-263.
8. Bisoendial R.J., Hovingh G.K., Levels J.H., Lerch P.G., Andresen I., Hayden M.R., Kastelein J.J., Stroes E.S. Restoration of endothelial function by increasing high-density lipoprotein in subjects with isolated low high-density lipoprotein. Circulation 2003, 107:2944-2948.
9. Bode-Böger S.M., Scalera F., Kielstein J.T., Martens-Lobenhoffer J., Breithardt G., Fobker M., Reinecke H. Symmetrical dimethylarginine: a new combined parameter for renal function and extent of coronary artery disease. J. Am. Soc. Nephrol. 2006, 17:1128-1134.
10. Boden W.E., Probstfield J.L., Anderson T., Chaitman B.R., Desvignes-Nickens P., Koprowicz K., McBride R., Teo K., Weintraub W. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N. Engl. J. Med. 2011, 365:2255-2267. AIM-HIGH Investigators.
11. Böger R.H., Bode-Böger S.M., Szuba A., Tsao P.S., Chan J.R., Tangphao O., Blaschke T.F., Cooke J.P. Asymmetric dimethylarginine (ADMA): a novel risk factor for endothelial dysfunction: its role in hypercholesterolemia. Circulation 1998, 98:1842-1847.
12. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R.B., Belisle J.T., Bleharski J.R., Maitland M., Norgard M.V., Plevy S.E., Smale S.T., et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 1999, 285:732-736.
13. Cabanski M., Steinmüller M., Marsh L.M., Surdziel E., Seeger W., Lohmeyer J. PKR regulates TLR2/TLR4-dependent signaling in murine alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 2008, 38:26-31.
14. Charakida M., Besler C., Batuca J.R., Sangle S., Marques S., Sousa M., Wang G., Tousoulis D., Delgado Alves J., Loukogeorgakis S.P., et al. Vascular abnormalities, paraoxonase activity, and dysfunctional HDL in primary antiphospholipid syndrome. JAMA 2009, 302:1210-1217.
15. Di Gangi I.M., Chiandetti L., Gucciardi A., Moret V., Naturale M., Giordano G. Simultaneous quantitative determination of N(G),N(G)-dimethyl-L-arginine or asymmetric dimethylarginine and related pathway's metabolites in biological fluids by ultrahigh-performance liquid chromatography/electrospray ionization-tandem mass spectrometry. Anal. Chim. Acta 2010, 677:140-148.
16. Edfeldt K., Swedenborg J., Hansson G.K., Yan Z.Q. Expression of toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation. Circulation 2002, 105:1158-1161.
17. Favre J., Musette P., Douin-Echinard V., Laude K., Henry J.P., Arnal J.F., Thuillez C., Richard V. Toll-like receptors 2-deficient mice are protected against postischemic coronary endothelial dysfunction. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1064-1071.
18. Fliser D., Kronenberg F., Kielstein J.T., Morath C., Bode-Böger S.M., Haller H., Ritz E. Asymmetric dimethylarginine and progression of chronic kidney disease: the mild to moderate kidney disease study. J. Am. Soc. Nephrol. 2005, 16:2456-2461.
19. Fujita M., Into T., Yasuda M., Okusawa T., Hamahira S., Kuroki Y., Eto A., Nisizawa T., Morita M., Shibata K. Involvement of leucine residues at positions 107, 112, and 115 in a leucine-rich repeat motif of human Toll-like receptor 2 in the recognition of diacylated lipoproteins and lipopeptides and Staphylococcus aureus peptidoglycans. J. Immunol. 2003, 171:3675-3683.
20. Go A.S., Chertow G.M., Fan D., McCulloch C.E., Hsu C.Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 2004, 351:1296-1305.
21. Grote K., Schuett H., Salguero G., Grothusen C., Jagielska J., Drexler H., Mühlradt P.F., Schieffer B. Toll-like receptor 2/6 stimulation promotes angiogenesis via GM-CSF as a potential strategy for immune defense and tissue regeneration. Blood 2010, 115:2543-2552.
22. Hansson G.K., Hermansson A. The immune system in atherosclerosis. Nat. Immunol. 2011, 12:204-212.
23. Harrison D.G., Guzik T.J., Lob H.E., Madhur M.S., Marvar P.J., Thabet S.R., Vinh A., Weyand C.M. Inflammation, immunity, and hypertension. Hypertension 2011, 57:132-140.
24. Huang P.L., Huang Z., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., Fishman M.C. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995, 377:239-242.
25. Jin M.S., Kim S.E., Heo J.Y., Lee M.E., Kim H.M., Paik S.G., Lee H., Lee J.O. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007, 130:1071-1082.
26. Kania G., Blyszczuk P., Stein S., Valaperti A., Germano D., Dirnhofer S., Hunziker L., Matter C.M., Eriksson U. Heart-infiltrating prominin-1+/CD133+ progenitor cells represent the cellular source of transforming growth factor beta-mediated cardiac fibrosis in experimental autoimmune myocarditis. Circ. Res. 2009, 105:462-470.
27. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650.
28. Kielstein J.T., Böger R.H., Bode-Böger S.M., Frölich J.C., Haller H., Ritz E., Fliser D. Marked increase of asymmetric dimethylarginine in patients with incipient primary chronic renal disease. J. Am. Soc. Nephrol. 2002, 13:170-176.
29. Klag M.J., Whelton P.K., Randall B.L., Neaton J.D., Brancati F.L., Ford C.E., Shulman N.B., Stamler J. Blood pressure and end-stage renal disease in men. N. Engl. J. Med. 1996, 334:13-18.
30. Kleschyov A.L., Mollnau H., Oelze M., Meinertz T., Huang Y., Harrison D.G., Munzel T. Spin trapping of vascular nitric oxide using colloid Fe(II)-diethyldithiocarbamate. Biochem. Biophys. Res. Commun. 2000, 275:672-677.
31. Kubes P., Suzuki M., Granger D.N. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA 1991, 88:4651-4655.
32. Landmesser U., Cai H., Dikalov S., McCann L., Hwang J., Jo H., Holland S.M., Harrison D.G. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 2002, 40:511-515.
33. Landmesser U., Hornig B., Drexler H. Endothelial function: a critical determinant in atherosclerosis?. Circulation 2004, 109(21, Suppl 1):II27-II33.
34. Libby P., Ridker P.M., Hansson G.K. Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473:317-325.
35. Lloyd-Jones D., Adams R.J., Brown T.M., Carnethon M., Dai S., De Simone G., Ferguson T.B., Ford E., Furie K., Gillespie C., et al. Executive summary: heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010, 121:948-954. American Heart Association Statistics Committee and Stroke Statistics Subcommittee.
36. Meinitzer A., Kielstein J.T., Pilz S., Drechsler C., Ritz E., Boehm B.O., Winkelmann B.R., März W. Symmetrical and asymmetrical dimethylarginine as predictors for mortality in patients referred for coronary angiography: the Ludwigshafen Risk and Cardiovascular Health study. Clin. Chem. 2011, 57:112-121.
37. Miller N.E., Thelle D.S., Forde O.H., Mjos O.D. The Tromsø heart-study. High-density lipoprotein and coronary heart-disease: a prospective case-control study. Lancet 1977, 1:965-968.
38. Mullick A.E., Tobias P.S., Curtiss L.K. Modulation of atherosclerosis in mice by Toll-like receptor 2. J. Clin. Invest. 2005, 115:3149-3156.
39. Mullick A.E., Soldau K., Kiosses W.B., Bell T.A., Tobias P.S., Curtiss L.K. Increased endothelial expression of Toll-like receptor 2 at sites of disturbed blood flow exacerbates early atherogenic events. J. Exp. Med. 2008, 205:373-383.
40. Nofer J.R., van der Giet M., Tölle M., Wolinska I., von Wnuck Lipinski K., Baba H.A., Tietge U.J., Gödecke A., Ishii I., Kleuser B., et al. HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J. Clin. Invest. 2004, 113:569-581.
41. Osto E., Matter C.M., Kouroedov A., Malinski T., Bachschmid M., Camici G.G., Kilic U., Stallmach T., Boren J., Iliceto S., et al. c-Jun N-terminal kinase 2 deficiency protects against hypercholesterolemia-induced endothelial dysfunction and oxidative stress. Circulation 2008, 118:2073-2080.
42. Peterson J.C., Adler S., Burkart J.M., Greene T., Hebert L.A., Hunsicker L.G., King A.J., Klahr S., Massry S.G., Seifter J.L. Blood pressure control, proteinuria, and the progression of renal disease. The Modification of Diet in Renal Disease Study. Ann. Intern. Med. 1995, 123:754-762.
43. Pober J.S., Sessa W.C. Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 2007, 7:803-815.
44. Pullamsetti S., Kiss L., Ghofrani H.A., Voswinckel R., Haredza P., Klepetko W., Aigner C., Fink L., Muyal J.P., Weissmann N., et al. Increased levels and reduced catabolism of asymmetric and symmetric dimethylarginines in pulmonary hypertension. FASEB J. 2005, 19:1175-1177.
45. Ramos H.C., Rumbo M., Sirard J.C. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 2004, 12:509-517.
46. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 1999, 340:115-126.
47. Roux A.L., Ray A., Pawlik A., Medjahed H., Etienne G., Rottman M., Catherinot E., Coppée J.Y., Chaoui K., Monsarrat B., et al. Overexpression of proinflammatory TLR-2-signalling lipoproteins in hypervirulent mycobacterial variants. Cell. Microbiol. 2011, 13:692-704.
48. Sandor F., Latz E., Re F., Mandell L., Repik G., Golenbock D.T., Espevik T., Kurt-Jones E.A., Finberg R.W. Importance of extra- and intracellular domains of TLR1 and TLR2 in NFkappa B signaling. J. Cell Biol. 2003, 162:1099-1110.
49. Schepers E., Barreto D.V., Liabeuf S., Glorieux G., Eloot S., Barreto F.C., Massy Z., Vanholder R. Symmetric dimethylarginine as a proinflammatory agent in chronic kidney disease. Clin. J. Am. Soc. Nephrol. 2011, 6:2374-2383. European Uremic Toxin Work Group (EUTox).
50. Schwartz G.G., Olsson A.G., Abt M., Ballantyne C.M., Barter P.J., Brumm J., Chaitman B.R., Holme I.M., Kallend D., Leiter L.A., et al. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N. Engl. J. Med. 2012, 367:2089-2099. dal-OUTCOMES Investigators.
51. Seimon T.A., Nadolski M.J., Liao X., Magallon J., Nguyen M., Feric N.T., Koschinsky M.L., Harkewicz R., Witztum J.L., Tsimikas S., et al. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab. 2010, 12:467-482.
52. Shi Y., Cosentino F., Camici G.G., Akhmedov A., Vanhoutte P.M., Tanner F.C., Lüscher T.F. Oxidized low-density lipoprotein activates p66Shc via lectin-like oxidized low-density lipoprotein receptor-1, protein kinase C-beta, and c-Jun N-terminal kinase kinase in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2090-2097.
53. Sorrentino S.A., Bahlmann F.H., Besler C., Müller M., Schulz S., Kirchhoff N., Doerries C., Horváth T., Limbourg A., Limbourg F., et al. Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. Circulation 2007, 116:163-173.
54. Sorrentino S.A., Besler C., Rohrer L., Meyer M., Heinrich K., Bahlmann F.H., Mueller M., Horváth T., Doerries C., Heinemann M., et al. Endothelial-vasoprotective effects of high-density lipoprotein are impaired in patients with type 2 diabetes mellitus but are improved after extended-release niacin therapy. Circulation 2010, 121:110-122.
55. Spieker L.E., Sudano I., Hürlimann D., Lerch P.G., Lang M.G., Binggeli C., Corti R., Ruschitzka F., Lüscher T.F., Noll G. High-density lipoprotein restores endothelial function in hypercholesterolemic men. Circulation 2002, 105:1399-1402.
56. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
57. Terasaka N., Yu S., Yvan-Charvet L., Wang N., Mzhavia N., Langlois R., Pagler T., Li R., Welch C.L., Goldberg I.J., Tall A.R. ABCG1 and HDL protect against endothelial dysfunction in mice fed a high-cholesterol diet. J. Clin. Invest. 2008, 118:3701-3713.
58. Van Biesen W., De Bacquer D., Verbeke F., Delanghe J., Lameire N., Vanholder R. The glomerular filtration rate in an apparently healthy population and its relation with cardiovascular mortality during 10 years. Eur. Heart J. 2007, 28:478-483.
59. Voight B.F., Peloso G.M., Orho-Melander M., Frikke-Schmidt R., Barbalic M., Jensen M.K., Hindy G., Hólm H., Ding E.L., Johnson T., et al. Plasma HDL cholesterol and risk of myocardial infarction: a mendelian randomisation study. Lancet 2012, 380:572-580.
60. West X.Z., Malinin N.L., Merkulova A.A., Tischenko M., Kerr B.A., Borden E.C., Podrez E.A., Salomon R.G., Byzova T.V. Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature 2010, 467:972-976.
61. West A.P., Brodsky I.E., Rahner C., Woo D.K., Erdjument-Bromage H., Tempst P., Walsh M.C., Choi Y., Shadel G.S., Ghosh S. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011, 472:476-480.
62. Yuhanna I.S., Zhu Y., Cox B.E., Hahner L.D., Osborne-Lawrence S., Lu P., Marcel Y.L., Anderson R.G., Mendelsohn M.E., Hobbs H.H., Shaul P.W. High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat. Med. 2001, 7:853-857.
63. Zoccali C., Bode-Böger S., Mallamaci F., Benedetto F., Tripepi G., Malatino L., Cataliotti A., Bellanuova I., Fermo I., Frölich J., Böger R. Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: a prospective study. Lancet 2001, 358:2113-2117.