Reducing macrophage proteoglycan sulfation increases atherosclerosis and obesity through enhanced type i interferon signaling

Cell Metabolism

Volumn 20, Issue 5, 2014, Pages 813-826

  Gordts, Philip L S M ^a   Foley, Erin M ^a,b   Lawrence, Roger ^a   Sinha, Risha ^a   Lameda Diaz, Carlos ^a   Deng, Liwen ^a   Nock, Ryan ^a   Glass, Christopher K ^a,c   Erbilgin, Ayca ^d   Lusis, Aldons J ^d   Witztum, Joseph L ^c   Esko, Jeffrey D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; HEPARAN SULFATE; INTERFERON; PROTEOGLYCAN; STAT1 PROTEIN; HEPARITIN SULFOTRANSFERASE; PROTEOHEPARAN SULFATE; SULFOTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; GENE; GENE CONTROL; MACROPHAGE; MOUSE; N ACETYLGLUCOSAMINE N DEACETYLASE N SULFOTRANSFERASE 1 GENE; NONHUMAN; OBESITY; PROTEIN PHOSPHORYLATION; SULFATION; ADVERSE EFFECTS; ANIMAL; ATHEROGENIC DIET; CHEMICAL STRUCTURE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MALE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ATHEROSCLEROSIS; DIET, ATHEROGENIC; FEMALE; GENE EXPRESSION REGULATION; HEPARAN SULFATE PROTEOGLYCANS; INTERFERON TYPE I; MACROPHAGES; MALE; MICE; MODELS, MOLECULAR; OBESITY; SIGNAL TRANSDUCTION; SULFOTRANSFERASES;

EID: 84910156813     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.09.016     Document Type: Article

References (38)

1. M. Abe, M. Matsuda, H. Kobayashi, Y. Miyata, Y. Nakayama, R. Komuro, A. Fukuhara, and I. Shimomura Effects of statins on adipose tissue inflammation: their inhibitory effect on MyD88-independent IRF3/IFN-beta pathway in macrophages Arterioscler. Thromb. Vasc. Biol. 28 2008 871 877
2. M. Blich, A. Golan, G. Arvatz, A. Sebbag, I. Shafat, E. Sabo, V. Cohen-Kaplan, S. Petcherski, S. Avniel-Polak, and A. Eitan Macrophage activation by heparanase is mediated by TLR-2 and TLR-4 and associates with plaque progression Arterioscler. Thromb. Vasc. Biol. 33 2013 e56 e65
3. B.B. Boyanovsky, P. Shridas, M. Simons, D.R. van der Westhuyzen, and N.R. Webb Syndecan-4 mediates macrophage uptake of group V secretory phospholipase A2-modified LDL J. Lipid Res. 50 2009 641 650
4. B.E. Clausen, C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster Conditional gene targeting in macrophages and granulocytes using LysMcre mice Transgenic Res. 8 1999 265 277
5. N.A. de Weerd, J.P. Vivian, T.K. Nguyen, N.E. Mangan, J.A. Gould, S.J. Braniff, L. Zaker-Tabrizi, K.Y. Fung, S.C. Forster, and T. Beddoe Structural basis of a unique interferon-β signaling axis mediated via the receptor IFNAR1 Nat. Immunol. 14 2013 901 907
6. G.K. Dhoot, M.K. Gustafsson, X.B. Ai, W.T. Sun, D.M. Standiford, and C.P. Emerson Jr. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase Science 293 2001 1663 1666
7. J.S. Frank, and A.M. Fogelman Ultrastructure of the intima in WHHL and cholesterol-fed rabbit aortas prepared by ultra-rapid freezing and freeze-etching J. Lipid Res. 30 1989 967 978
8. P. Goossens, M.J. Gijbels, A. Zernecke, W. Eijgelaar, M.N. Vergouwe, I. van der Made, J. Vanderlocht, L. Beckers, W.A. Buurman, and M.J. Daemen Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions Cell Metab. 12 2010 142 153
9. D.J. Gough, N.L. Messina, C.J. Clarke, R.W. Johnstone, and D.E. Levy Constitutive type I interferon modulates homeostatic balance through tonic signaling Immunity 36 2012 166 174
10. A.S. Haka, I. Grosheva, E. Chiang, A.R. Buxbaum, B.A. Baird, L.M. Pierini, and F.R. Maxfield Macrophages create an acidic extracellular hydrolytic compartment to digest aggregated lipoproteins Mol. Biol. Cell 20 2009 4932 4940
11. W. Hollmann Endurance training and the prevention of coronary heart disease Bol. Asoc. Med. P. R. 81 1989 30 31
12. C. Jin, J. Henao-Mejia, and R.A. Flavell Innate immune receptors: key regulators of metabolic disease progression Cell Metab. 17 2013 873 882
13. R. Lawrence, S.K. Olson, R.E. Steele, L. Wang, R. Warrior, R.D. Cummings, and J.D. Esko Evolutionary differences in glycosaminoglycan fine structure detected by quantitative glycan reductive isotope labeling J. Biol. Chem. 283 2008 33674 33684
14. J.M. MacArthur, J.R. Bishop, K.I. Stanford, L. Wang, A. Bensadoun, J.L. Witztum, and J.D. Esko Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members J. Clin. Invest. 117 2007 153 164
15. I. Maor, T. Hayek, M. Hirsh, T.C. Iancu, and M. Aviram Macrophage-released proteoglycans enhance LDL aggregation: studies in aorta from apolipoprotein E-deficient mice Atherosclerosis 150 2000 91 101
16. K.J. Moore, F.J. Sheedy, and E.A. Fisher Macrophages in atherosclerosis: a dynamic balance Nat. Rev. Immunol. 13 2013 709 721
17. K. Murata, A. Murata, and K. Yoshida Heparan sulfate isomers in cerebral arteries of Japanese women with aging and with atherosclerosis - heparitinase and high-performance liquid chromatography determinations Atherosclerosis 132 1997 9 17
18. A.J. Murphy, M. Akhtari, S. Tolani, T. Pagler, N. Bijl, C.L. Kuo, M. Wang, M. Sanson, S. Abramowicz, and C. Welch ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice J. Clin. Invest. 121 2011 4138 4149
19. K. Nakaya, J. Tohyama, S.U. Naik, H. Tanigawa, C. MacPhee, J.T. Billheimer, and D.J. Rader Peroxisome proliferator-activated receptor-α activation promotes macrophage reverse cholesterol transport through a liver X receptor-dependent pathway Arterioscler. Thromb. Vasc. Biol. 31 2011 1276 1282
20. B. Nardelli, L. Zaritskaya, M. Semenuk, Y.H. Cho, D.W. LaFleur, D. Shah, S. Ullrich, G. Girolomoni, C. Albanesi, and P.A. Moore Regulatory effect of IFN-kappa, a novel type I IFN, on cytokine production by cells of the innate immune system J. Immunol. 169 2002 4822 4830
21. C. Osterholm, L. Folkersen, M. Lengquist, F. Pontén, T. Renné, J. Li, and U. Hedin Increased expression of heparanase in symptomatic carotid atherosclerosis Atherosclerosis 226 2013 67 73
22. F. Re, and J.L. Strominger IL-10 released by concomitant TLR2 stimulation blocks the induction of a subset of Th1 cytokines that are specifically induced by TLR4 or TLR3 in human dendritic cells J. Immunol. 173 2004 7548 7555
23. C.S. Robbins, I. Hilgendorf, G.F. Weber, I. Theurl, Y. Iwamoto, J.L. Figueiredo, R. Gorbatov, G.K. Sukhova, L.M. Gerhardt, and D. Smyth Local proliferation dominates lesional macrophage accumulation in atherosclerosis Nat. Med. 19 2013 1166 1172
24. S. Sarrazin, W.C. Lamanna, and J.D. Esko Heparan sulfate proteoglycans Cold Spring Harb. Perspect. Biol. 3 2011 a004952
25. T.A. Seimon, A. Obstfeld, K.J. Moore, D.T. Golenbock, and I. Tabas Combinatorial pattern recognition receptor signaling alters the balance of life and death in macrophages Proc. Natl. Acad. Sci. USA 103 2006 19794 19799
26. T. Senda, S. Saitoh, and Y. Mitsui Refined crystal structure of recombinant murine interferon-beta at 2.15 A resolution J. Mol. Biol. 253 1995 187 207
27. C. Shao, X. Shi, M. White, Y. Huang, K. Hartshorn, and J. Zaia Comparative glycomics of leukocyte glycosaminoglycans FEBS J. 280 2013 2447 2461
28. K.I. Stanford, J.R. Bishop, E.M. Foley, J.C. Gonzales, I.R. Niesman, J.L. Witztum, and J.D. Esko Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice J. Clin. Invest. 119 2009 3236 3245
29. F.K. Swirski, and M. Nahrendorf Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure Science 339 2013 161 166
30. I. Tabas, K.J. Williams, and J. Borén Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications Circulation 116 2007 1832 1844
31. F. Tacke, D. Alvarez, T.J. Kaplan, C. Jakubzick, R. Spanbroek, J. Llodra, A. Garin, J. Liu, M. Mack, and N. van Rooijen Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques J. Clin. Invest. 117 2007 185 194
32. K. Tran-Lundmark, P.K. Tran, G. Paulsson-Berne, V. Fridén, R. Soininen, K. Tryggvason, T.N. Wight, M.G. Kinsella, J. Borén, and U. Hedin Heparan sulfate in perlecan promotes mouse atherosclerosis: roles in lipid permeability, lipid retention, and smooth muscle cell proliferation Circ. Res. 103 2008 43 52
33. B.L. Viviano, S. Paine-Saunders, N. Gasiunas, J. Gallagher, and S. Saunders Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist Noggin J. Biol. Chem. 279 2004 5604 5611
34. X.A. Wang, R. Zhang, S. Zhang, S. Deng, D. Jiang, J. Zhong, L. Yang, T. Wang, S. Hong, and S. Guo Interferon regulatory factor 7 deficiency prevents diet-induced obesity and insulin resistance Am. J. Physiol. Endocrinol. Metab. 305 2013 E485 E495
35. W. Wei, M.R. Niñonuevo, A. Sharma, L.M. Danan-Leon, and J.A. Leary A comprehensive compositional analysis of heparin/heparan sulfate-derived disaccharides from human serum Anal. Chem. 83 2011 3703 3708
36. T.N. Wight Cell biology of arterial proteoglycans Arteriosclerosis 9 1989 1 20
37. J.L. Witztum, and A.H. Lichtman The influence of innate and adaptive immune responses on atherosclerosis Annu. Rev. Pathol. 9 2014 73 102
38. L. Yang, J.B. Yang, J. Chen, G.Y. Yu, P. Zhou, L. Lei, Z.Z. Wang, C. Cy Chang, X.Y. Yang, T.Y. Chang, and B.L. Li Enhancement of human ACAT1 gene expression to promote the macrophage-derived foam cell formation by dexamethasone Cell Res. 14 2004 315 323