Niacin inhibits skin dendritic cell mobilization in a GPR109A independent manner but has no impact on monocyte trafficking in atherosclerosis

Immunobiology

Volumn 217, Issue 5, 2012, Pages 548-557

  Ingersoll, Molly A ^a   Potteaux, Stephane ^a,c   Alvarez, David ^a,d   Hutchison, Susan B ^a   van Rooijen, Nico ^b   Randolph, Gwendalyn J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Arteriosclerosis; Contact hypersensitivity; HM74A; Macrophage; Nicotinamide; Nicotinic acid; PUMA G

Indexed keywords

APOLIPOPROTEIN E; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 109A; HIGH DENSITY LIPOPROTEIN; LIPID; NICOTINIC ACID; PROSTAGLANDIN SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL MIGRATION; CELL MOTILITY; CELL TRANSPORT; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; FOOD INTAKE; GENE DELETION; HEART PROTECTION; IMMUNOCOMPETENT CELL; INHIBITION KINETICS; LIPID DIET; LYMPHATIC DRAINAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; SKIN DENDRITIC CELL; SKIN STIMULATION; WILD TYPE;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELL MOVEMENT; DENDRITIC CELLS; DERMATITIS, CONTACT; FEMALE; IMMUNOLOGIC FACTORS; LUNG; LYMPH NODES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NIACIN; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NICOTINIC; SKIN;

EID: 84858793548     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2011.05.014     Document Type: Article

References (58)

1. Allan R.S., Waithman J., Bedoui S., Jones C.M., Villadangos J.A., Zhan Y., Lew A.M., Shortman K., Heath W.R., Carbone F.R. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006, 25:153-162.
2. Altschul R., Hoffer A., Stephen J.D. Influence of nicotinic acid on serum cholesterol in man. Arch. Biochem. 1955, 54:558-559.
3. Angeli V., Faveeuw C., Roye O., Fontaine J., Teissier E., Capron A., Wolowczuk I., Capron M., Trottein F. Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J. Exp. Med. 2001, 193:1135-1147.
4. Angeli V., Llodra J., Rong J.X., Satoh K., Ishii S., Shimizu T., Fisher E.A., Randolph G.J. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity 2004, 21:561-574.
5. Askenase P.W. Yes T cells, but three different T cells (αβ, γδ and NK T cells), and also B-1 cells mediate contact sensitivity. Clin. Exp. Immunol. 2001, 125:345-350.
6. Benyo Z., Gille A., Bennett C.L., Clausen B.E., Offermanns S. Nicotinic acid-induced flushing is mediated by activation of epidermal langerhans cells. Mol. Pharmacol. 2006, 70:1844-1849.
7. Benyo Z., Gille A., Kero J., Csiky M., Suchankova M.C., Nusing R.M., Moers A., Pfeffer K., Offermanns S. GPR109A (PUMA-G/HM74A) mediates nicotinic acid-induced flushing. J. Clin. Invest. 2005, 115:3634-3640.
8. Blankenhorn D.H., Azen S.P., Crawford D.W., Nessim S.A., Sanmarco M.E., Selzer R.H., Shircore A.M., Wickham E.C. Effects of colestipol-niacin therapy on human femoral atherosclerosis. Circulation 1991, 83:438-447.
9. Blankenhorn D.H., Nessim S.A., Johnson R.L., Sanmarco M.E., Azen S.P., Cashin-Hemphill L. Beneficial effects of combined colestipol-niacin therapy on coronary atherosclerosis and coronary venous bypass grafts. JAMA 1987, 257:3233-3240.
10. Brown B.G., Zhao X.Q., Chait A., Fisher L.D., Cheung M.C., Morse J.S., Dowdy A.A., Marino E.K., Bolson E.L., Alaupovic P., et al. Simvastatin and niacin, antioxidant vitamins, or the combination for the prevention of coronary disease. N. Engl. J. Med. 2001, 345:1583-1592.
11. Brown G., Albers J.J., Fisher L.D., Schaefer S.M., Lin J.T., Kaplan C., Zhao X.Q., Bisson B.D., Fitzpatrick V.F., Dodge H.T. Regression of coronary artery disease as a result of intensive lipid-lowering therapy in men with high levels of apolipoprotein B. N. Engl. J. Med. 1990, 323:1289-1298.
12. Canner P.L., Berge K.G., Wenger N.K., Stamler J., Friedman L., Prineas R.J., Friedewald W. Fifteen year mortality in Coronary Drug Project patients: long-term benefit with niacin. J. Am. Coll. Cardiol. 1986, 8:1245-1255.
13. Carlson L.A. Studies on the effect of nicotinic acid on catecholamine stimulated lipolysis in adipose tissue in vitro. Acta Med. Scand. 1963, 173:719-722.
14. Carlson L.A. Nicotinic acid: the broad-spectrum lipid drug. A 50th anniversary review. J. Intern. Med. 2005, 258:94-114.
15. Carlson L.A., Rosenhamer G. Reduction of mortality in the Stockholm Ischaemic Heart Disease Secondary Prevention Study by combined treatment with clofibrate and nicotinic acid. Acta Med. Scand. 1988, 223:405-418.
16. Declercq V., Yeganeh B., Moshtaghi-Kashanian G.R., Khademi H., Bahadori B., Moghadasian M.H. Paradoxical effects of fenofibrate and nicotinic acid in apo E-deficient mice. J. Cardiovasc. Pharmacol. 2005, 46:18-24.
17. Digby J.E., McNeill E., Dyar O.J., Lam V., Greaves D.R., Choudhury R.P. Anti-inflammatory effects of nicotinic acid in adipocytes demonstrated by suppression of fractalkine, RANTES, and MCP-1 and upregulation of adiponectin. Atherosclerosis 2010, 209:89-95.
18. Dunbar R.L., Gelfand J.M. Seeing red: flushing out instigators of niacin-associated skin toxicity. J. Clin. Invest. 2010, 120:2651-2655.
19. Feig J.E., Pineda-Torra I., Sanson M., Bradley M.N., Vengrenyuk Y., Bogunovic D., Gautier E.L., Rubinstein D., Hong C., Liu J., et al. LXR promotes the maximal egress of monocyte-derived cells from mouse aortic plaques during atherosclerosis regression. J. Clin. Invest. 2010, 120:4415-4424.
20. Ganji S.H., Qin S., Zhang L., Kamanna V.S., Kashyap M.L. Niacin inhibits vascular oxidative stress, redox-sensitive genes, and monocyte adhesion to human aortic endothelial cells. Atherosclerosis 2009, 202:68-75.
21. Garrigue J.L., Nicolas J.F., Fraginals R., Benezra C., Bour H., Schmitt D. Optimization of the mouse ear swelling test for in vivo and in vitro studies of weak contact sensitizers. Contact Dermatitis 1994, 30:231-237.
22. Gautier E.L., Jakubzick C., Randolph G.J. Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1412-1418.
23. Glass C.K., Witztum J.L. Atherosclerosis. The road ahead. Cell 2001, 104:503-516.
24. Grange P.A., Raingeaud J., Calvez V., Dupin N. Nicotinamide inhibits propionibacterium acnes-induced IL-8 production in keratinocytes through the NF-kappaB and MAPK pathways. J. Dermatol. Sci. 2009, 56:106-112.
25. Hanson J., Gille A., Zwykiel S., Lukasova M., Clausen B.E., Ahmed K., Tunaru S., Wirth A., Offermanns S. Nicotinic acid- and monomethyl fumarate-induced flushing involves GPR109A expressed by keratinocytes and COX-2-dependent prostanoid formation in mice. J. Clin. Invest. 2010, 120:2910-2919.
26. Jakubzick C., Helft J., Kaplan T.J., Randolph G.J. Optimization of methods to study pulmonary dendritic cell migration reveals distinct capacities of DC subsets to acquire soluble versus particulate antigen. J. Immunol. Methods 2008, 337:121-131.
27. Langenbach R., Morham S.G., Tiano H.F., Loftin C.D., Ghanayem B.I., Chulada P.C., Mahler J.F., Lee C.A., Goulding E.H., Kluckman K.D., et al. Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell 1995, 83:483-492.
28. Lee J.M., Robson M.D., Yu L.M., Shirodaria C.C., Cunnington C., Kylintireas I., Digby J.E., Bannister T., Handa A., Wiesmann F., et al. Effects of high-dose modified-release nicotinic acid on atherosclerosis and vascular function: a randomized, placebo-controlled, magnetic resonance imaging study. J. Am. Coll. Cardiol. 2009, 54:1787-1794.
29. Lee J.M.S., Robson M.D., Yu L.-M., Shirodaria C.C., Cunnington C., Kylintireas I., Digby J.E., Bannister T., Handa A., Wiesmann F., et al. Effects of high-dose modified-release nicotinic acid on atherosclerosis and vascular function: a randomized, placebo-controlled, magnetic resonance imaging study. J. Am. Coll. Cardiol. 2009, 54:1787-1794.
30. Llodra J., Angeli V., Liu J., Trogan E., Fisher E.A., Randolph G.J. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11779-11784.
31. Lukasova M., Malaval C., Gille A., Kero J., Offermanns S. Nicotinic acid inhibits progression of atherosclerosis in mice through its receptor GPR109A expressed by immune cells. J. Clin. Invest. 2011, 121:1163-1173.
32. Maciejewski-Lenoir D., Richman J.G., Hakak Y., Gaidarov I., Behan D.P., Connolly D.T. Langerhans cells release prostaglandin D2 in response to nicotinic acid. J. Invest. Dermatol. 2006, 126:2637-2646.
33. Martin-Fontecha A., Sebastiani S., Hopken U.E., Uguccioni M., Lipp M., Lanzavecchia A., Sallusto F. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 2003, 198:615-621.
34. Montecucco F., Quercioli A., Dallegri F., Viviani G.L., Mach F.X. New evidence for nicotinic acid treatment to reduce atherosclerosis. Expert Rev. Cardiovasc. Ther. 2010, 8:1457-1467.
35. Morrow J.D., Awad J.A., Oates J.A., Roberts L.J. Identification of skin as a major site of prostaglandin D2 release following oral administration of niacin in humans. J. Invest. Dermatol. 1992, 98:812-815.
36. Morrow J.D., Parsons W.G., Roberts L.J. Release of markedly increased quantities of prostaglandin D2 in vivo in humans following the administration of nicotinic acid. Prostaglandins 1989, 38:263-274.
37. O'Leary J.G., Goodarzi M., Drayton D.L., von Andrian U.H. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 2006, 7:507-516.
38. Offermanns S. The nicotinic acid receptor GPR109A (HM74A or PUMA-G) as a new therapeutic target. Trends Pharmacol. Sci. 2006, 27:384-390.
39. Ost C.R., Stenson S. Regression of peripheral atherosclerosis during therapy with high doses of nicotinic acid. Scand. J. Clin. Lab. Invest. Suppl. 1967, 99:241-245.
40. Paust S., Gill H.S., Wang B.-Z., Flynn M.P., Moseman E.A., Senman B., Szczepanik M., Telenti A., Askenase P.W., Compans R.W., von Andrian U.H. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat. Immunol. 2010, 11:1127-1135.
41. -/- mice during disease regression. J. Clin. Invest. 2011, 121:2025-2036.
42. Randolph G.J. Emigration of monocyte-derived cells to lymph nodes during resolution of inflammation and its failure in atherosclerosis. Curr. Opin. Lipidol. 2008, 19:462-468.
43. Randolph G.J. The fate of monocytes in atherosclerosis. J. Thromb. Haemost. 2009, 7(Suppl. 1):28-30.
44. Robbiani D.F., Finch R.A., Jager D., Muller W.A., Sartorelli A.C., Randolph G.J. The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 2000, 103:757-768.
45. Robertson A.K., Hansson G.K. T cells in atherogenesis: for better or for worse?. Arterioscler. Thromb. Vasc. Biol. 2006, 26:2421-2432.
46. Schaub A., Futterer A., Pfeffer K. PUMA-G, an IFN-gamma-inducible gene in macrophages is a novel member of the seven transmembrane spanning receptor superfamily. Eur. J. Immunol. 2001, 31:3714-3725.
47. Soga T., Kamohara M., Takasaki J., Matsumoto S., Saito T., Ohishi T., Hiyama H., Matsuo A., Matsushime H., Furuichi K. Molecular identification of nicotinic acid receptor. Biochem. Biophys. Res. Commun. 2003, 303:364-369.
48. Tacke F., Alvarez D., Kaplan T.J., Jakubzick C., Spanbroek R., Llodra J., Garin A., Liu J., Mack M., van Rooijen N., et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 2007, 117:185-194.
49. Tacke F., Ginhoux F., Jakubzick C., van Rooijen N., Merad M., Randolph G.J. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J. Exp. Med. 2006, 203:583-597.
50. Taylor A.J., Villines T.C., Stanek E.J., Devine P.J., Griffen L., Miller M., Weissman N.J., Turco M. Extended-release niacin or ezetimibe and carotid intima-media thickness. N. Engl. J. Med. 2009, 361:2113-2122.
51. Clofibrate and niacin in coronary heart disease. JAMA 1975, 231:360-381. The Coronary Drug Project Research Group.
52. Tunaru S., Kero J., Schaub A., Wufka C., Blaukat A., Pfeffer K., Offermanns S. PUMA-G and HM74 are receptors for nicotinic acid and mediate its anti-lipolytic effect. Nat. Med. 2003, 9:352-355.
53. Wahlberg G., Walldius G. Effects of nicotinic acid treatment on glyceride formation and lipolysis in adipose tissue of hyperlipidemic patients. Int. J. Clin. Lab. Res. 1993, 23:88-94.
54. Walters R.W., Shukla A.K., Kovacs J.J., Violin J.D., DeWire S.M., Lam C.M., Chen J.R., Muehlbauer M.J., Whalen E.J., Lefkowitz R.J. beta-Arrestin1 mediates nicotinic acid-induced flushing, but not its antilipolytic effect, in mice. J. Clin. Invest. 2009, 119:1312-1321.
55. Whitney E.J., Krasuski R.A., Personius B.E., Michalek J.E., Maranian A.M., Kolasa M.W., Monick E., Brown B.G., Gotto A.M. A randomized trial of a strategy for increasing high-density lipoprotein cholesterol levels: effects on progression of coronary heart disease and clinical events. Ann. Intern. Med. 2005, 142:95-104.
56. Wise A., Foord S.M., Fraser N.J., Barnes A.A., Elshourbagy N., Eilert M., Ignar D.M., Murdock P.R., Steplewski K., Green A., et al. Molecular identification of high and low affinity receptors for nicotinic acid. J. Biol. Chem. 2003, 278:9869-9874.
57. Wu B.J., Yan L., Charlton F., Witting P., Barter P.J., Rye K.A. Evidence that niacin inhibits acute vascular inflammation and improves endothelial dysfunction independent of changes in plasma lipids. Arterioscler. Thromb. Vasc. Biol. 2010, 30:968-975.
58. Zhang Y., Schmidt R.J., Foxworthy P., Emkey R., Oler J.K., Large T.H., Wang H., Su E.W., Mosior M.K., Eacho P.I., Cao G. Niacin mediates lipolysis in adipose tissue through its G-protein coupled receptor HM74A. Biochem. Biophys. Res. Commun. 2005, 334:729-732.