S1P2/G12/13 Signaling Negatively Regulates Macrophage Activation and Indirectly Shapes the Atheroprotective B1-Cell Population

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 1, 2016, Pages 37-48

  Grimm, Myriam ^a   Tischner, Denise ^a   Troidl, Kerstin ^a   Juárez, Julián Albarrán ^a   Sivaraj, Kishor K ^a   Bouzas, Nerea Ferreirós ^b   Geisslinger, Gerd ^b   Binder, Christoph J ^d   Wettschureck, Nina ^a,c  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b Clinical Pharmacology ^*  (United States)

^c GOETHE UNIVERSITY   (Germany)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

atherosclerosis; gene expression; GTP binding proteins; macrophages; signal transduction

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SPHINGOSINE 1 PHOSPHATE RECEPTOR SUBTYPE 2; UNCLASSIFIED DRUG; AUTACOID; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LOW DENSITY LIPOPROTEIN RECEPTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE-1-PHOSPHATE RECEPTOR-2, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATHEROGENESIS; B LYMPHOCYTE; BONE MARROW CELL; CELL EXPANSION; CELL MIGRATION; CELL POPULATION; CELL SHAPE; CONTROLLED STUDY; FEEDBACK SYSTEM; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MACROPHAGE ACTIVATION; MACROPHAGE MIGRATION; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM CELL; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; ANIMAL; AORTA; AORTIC DISEASES; ATHEROSCLEROSIS; AUTOCRINE EFFECT; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; AORTA; AORTIC DISEASES; ATHEROSCLEROSIS; AUTOCRINE COMMUNICATION; B-LYMPHOCYTE SUBSETS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; INFLAMMATION MEDIATORS; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; RECEPTORS, LDL; RECEPTORS, LYSOSPHINGOLIPID; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84952639790     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.306066     Document Type: Article

References (50)

1. Moore KJ, Sheedy FJ, Fisher EA, Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol 2013 13 709 721. doi: 10.1038/nri3520
2. Ley K, Miller YI, Hedrick CC, Monocyte and macrophage dynamics during atherogenesis. Arterioscler Thromb Vasc Biol 2011 31 1506 1516. doi: 10.1161/ATVBAHA.110.221127
3. Randolph GJ, Emigration of monocyte-derived cells to lymph nodes during resolution of inflammation and its failure in atherosclerosis. Curr Opin Lipidol 2008 19 462 468. doi: 10.1097/MOL.0b013e32830d5f09
4. Zernecke A, Shagdarsuren E, Weber C, Chemokines in atherosclerosis: an update. Arterioscler Thromb Vasc Biol 2008 28 1897 1908. doi: 10.1161/ATVBAHA.107.161174
5. Leitinger N, Schulman IG, Phenotypic polarization of macrophages in atherosclerosis. Arterioscler Thromb Vasc Biol 2013 33 1120 1126. doi: 10.1161/ATVBAHA.112.300173
6. Mantovani A, Garlanda C, Locati M, Macrophage diversity and polarization in atherosclerosis: a question of balance. Arterioscler Thromb Vasc Biol 2009 29 1419 1423. doi: 10.1161/ATVBAHA.108.180497
7. Weber C, Noels H, Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011 17 1410 1422. doi: 10.1038/nm.2538
8. Westerterp M, Bochem AE, Yvan-Charvet L, Murphy AJ, Wang N, Tall AR, ATP-binding cassette transporters, atherosclerosis, and inflammation. Circ Res 2014 114 157 170. doi: 10.1161/CIRCRESAHA.114.300738
9. Rosenson RS, Brewer HB Jr, Davidson WS, Fayad ZA, Fuster V, Goldstein J, Hellerstein M, Jiang XC, Phillips MC, Rader DJ, Remaley AT, Rothblat GH, Tall AR, Yvan-Charvet L, Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation 2012 125 1905 1919. doi: 10.1161/CIRCULATIONAHA.111.066589
10. Maiolino G, Rossitto G, Caielli P, Bisogni V, Rossi GP, Calò LA, The role of oxidized low-density lipoproteins in atherosclerosis: the myths and the facts. Mediators Inflamm 2013 2013 714653. doi: 10.1155/2013/714653
11. Ozkanlar S, Akcay F, Antioxidant vitamins in atherosclerosis-animal experiments and clinical studies. Adv Clin Exp Med 2012 21 115 123
12. Perry HM, Bender TP, McNamara CA, B cell subsets in atherosclerosis. Front Immunol 2012 3 373. doi: 10.3389/fimmu.2012.00373
13. Kyaw T, Tipping P, Bobik A, Toh BH, Protective role of natural IgM-producing B1a cells in atherosclerosis. Trends Cardiovasc Med 2012 22 48 53. doi: 10.1016/j.tcm.2012.06.011
14. Kawamoto H, Minato N, Myeloid cells. Int J Biochem Cell Biol 2004 36 1374 1379. doi: 10.1016/j.biocel.2004.01.020
15. Lattin J, Zidar DA, Schroder K, Kellie S, Hume DA, Sweet MJ, G-protein-coupled receptor expression, function, and signaling in macrophages. J Leukoc Biol 2007 82 16 32. doi: 10.1189/jlb.0107051
16. Wettschureck N, Offermanns S, Mammalian G proteins and their cell type specific functions. Physiol Rev 2005 85 1159 1204. doi: 10.1152/physrev.00003.2005
17. Worzfeld T, Wettschureck N, Offermanns S, G(12)/G(13)-mediated signalling in mammalian physiology and disease. Trends Pharmacol Sci 2008 29 582 589. doi: 10.1016/j.tips.2008.08.002
18. Siehler S, Regulation of RhoGEF proteins by G12/13-coupled receptors. Br J Pharmacol 2009 158 41 49. doi: 10.1111/j.1476-5381.2009.00121.x
19. Fukuhara S, Chikumi H, Gutkind JS, RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene 2001 20 1661 1668. doi: 10.1038/sj.onc.1204182
20. Herroeder S, Reichardt P, Sassmann A, Zimmermann B, Jaeneke D, Hoeckner J, Hollmann MW, Fischer KD, Vogt S, Grosse R, Hogg N, Gunzer M, Offermanns S, Wettschureck N, Guanine nucleotide-binding proteins of the G12 family shape immune functions by controlling CD4+ T cell adhesiveness and motility. Immunity 2009 30 708 720. doi: 10.1016/j.immuni.2009.02.010
21. Rieken S, Sassmann A, Herroeder S, Wallenwein B, Moers A, Offermanns S, Wettschureck N, G12/G13 family G proteins regulate marginal zone B cell maturation, migration, and polarization. J Immunol 2006 177 2985 2993
22. Xu J, Wang F, Van Keymeulen A, Herzmark P, Straight A, Kelly K, Takuwa Y, Sugimoto N, Mitchison T, Bourne HR, Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 2003 114 201 214
23. Sivaraj KK, Takefuji M, Schmidt I, Adams RH, Offermanns S, Wettschureck N, G13 controls angiogenesis through regulation of VEGFR-2 expression. Dev Cell 2013 25 427 434. doi: 10.1016/j.devcel.2013.04.008
24. Brown JH, Del Re DP, Sussman MA, The Rac and Rho hall of fame: a decade of hypertrophic signaling hits. Circ Res 2006 98 730 742. doi: 10.1161/01.RES.0000216039.75913.9e
25. Althoff TF, Albarrán Juárez J, Troidl K, Tang C, Wang S, Wirth A, Takefuji M, Wettschureck N, Offermanns S, Procontractile G protein-mediated signaling pathways antagonistically regulate smooth muscle differentiation in vascular remodeling. J Exp Med 2012 209 2277 2290. doi: 10.1084/jem.20120350
26. Takefuji M, Wirth A, Lukasova M, Takefuji S, Boettger T, Braun T, Althoff T, Offermanns S, Wettschureck N, G(13)-mediated signaling pathway is required for pressure overload-induced cardiac remodeling and heart failure. Circulation 2012 126 1972 1982. doi: 10.1161/CIRCULATIONAHA.112.109256
27. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I, Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999 8 265 277
28. Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J, Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest 1993 92 883 893. doi: 10.1172/JCI116663
29. Ghosn EE, Cassado AA, Govoni GR, Fukuhara T, Yang Y, Monack DM, Bortoluci KR, Almeida SR, Herzenberg LA, Herzenberg LA, Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc Natl Acad Sci USA 2010 107 2568 2573. doi: 10.1073/pnas.0915000107
30. Davies LC, Jenkins SJ, Allen JE, Taylor PR, Tissue-resident macrophages. Nat Immunol 2013 14 986 995. doi: 10.1038/ni.2705
31. Ye M, Iwasaki H, Laiosa CV, Stadtfeld M, Xie H, Heck S, Clausen B, Akashi K, Graf T, Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage repopulation potential. Immunity 2003 19 689 699
32. Fagarasan S, Watanabe N, Honjo T, Generation, expansion, migration and activation of mouse B1 cells. Immunol Rev 2000 176 205 215
33. Thies FG, Laurindo MF, Perez EC, Novaes e Brito RR, Mariano M, Popi AF, Cross talk between peritoneal macrophages and B-1 cells in vitro. PLoS One 2013 8 e62805. doi: 10.1371/journal.pone.0062805
34. Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A, Tipping P, Bobik A, Toh BH, B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res 2011 109 830 840. doi: 10.1161/CIRCRESAHA.111.248542
35. Binder CJ, Hörkkö S, Dewan A, Chang MK, Kieu EP, Goodyear CS, Shaw PX, Palinski W, Witztum JL, Silverman GJ, Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med 2003 9 736 743. doi: 10.1038/nm876
36. Binder CJ, Shaw PX, Chang MK, Boullier A, Hartvigsen K, Hörkkö S, Miller YI, Woelkers DA, Corr M, Witztum JL, The role of natural antibodies in atherogenesis. J Lipid Res 2005 46 1353 1363. doi: 10.1194/jlr.R500005-JLR200
37. Burridge K, Wennerberg K, Rho and Rac take center stage. Cell 2004 116 167 179
38. Jiang LI, Collins J, Davis R, Lin KM, DeCamp D, Roach T, Hsueh R, Rebres RA, Ross EM, Taussig R, Fraser I, Sternweis PC, Use of a cAMP BRET sensor to characterize a novel regulation of cAMP by the sphingosine 1-phosphate/G13 pathway. J Biol Chem 2007 282 10576 10584. doi: 10.1074/jbc.M609695200
39. Gerlo S, Kooijman R, Beck IM, Kolmus K, Spooren A, Haegeman G, Cyclic AMP: a selective modulator of NF-κB action. Cell Mol Life Sci 2011 68 3823 3841. doi: 10.1007/s00018-011-0757-8
40. Rotsch J, Rohrbeck A, May M, Kolbe T, Hagemann S, Schelle I, Just I, Genth H, Huelsenbeck SC, Inhibition of macrophage migration by C. botulinum exoenzyme C3. Naunyn Schmiedebergs Arch Pharmacol 2012 385 883 890. doi: 10.1007/s00210-012-0764-9
41. Rattan R, Giri S, Singh AK, Singh I, Rho A negatively regulates cytokine-mediated inducible nitric oxide synthase expression in brain-derived transformed cell lines: negative regulation of IKKalpha. Free Radic Biol Med 2003 35 1037 1050
42. Fessler MB, Arndt PG, Just I, Nick JA, Malcolm KC, Worthen GS, Dual role for RhoA in suppression and induction of cytokines in the human neutrophil. Blood 2007 109 1248 1256. doi: 10.1182/blood-2006-03-012898
43. Guilluy C, Garcia-Mata R, Burridge K, Rho protein crosstalk: another social network? Trends Cell Biol 2011 21 718 726. doi: 10.1016/j.tcb.2011.08.002
44. Obinata H, Hla T, Sphingosine 1-phosphate in coagulation and inflammation. Semin Immunopathol 2012 34 73 91. doi: 10.1007/s00281-011-0287-3
45. Muppidi JR, Schmitz R, Green JA, Loss of signalling via Gα13 in germinal centre B-cell-derived lymphoma. Nature 2014 516 254 258. doi: 10.1038/nature13765
46. Skoura A, Michaud J, Im DS, Thangada S, Xiong Y, Smith JD, Hla T, Sphingosine-1-phosphate receptor-2 function in myeloid cells regulates vascular inflammation and atherosclerosis. Arterioscler Thromb Vasc Biol 2011 31 81 85. doi: 10.1161/ATVBAHA.110.213496
47. Michaud J, Im DS, Hla T, Inhibitory role of sphingosine 1-phosphate receptor 2 in macrophage recruitment during inflammation. J Immunol 2010 184 1475 1483. doi: 10.4049/jimmunol.0901586
48. Sugimoto N, Takuwa N, Okamoto H, Sakurada S, Takuwa Y, Inhibitory and stimulatory regulation of Rac and cell motility by the G12/13-Rho and Gi pathways integrated downstream of a single G protein-coupled sphingosine-1-phosphate receptor isoform. Mol Cell Biol 2003 23 1534 1545
49. Zhou Q, Mei Y, Shoji T, Han X, Kaminski K, Oh GT, Ongusaha PP, Zhang K, Schmitt H, Moser M, Bode C, Liao JK, Rho-associated coiled-coil-containing kinase 2 deficiency in bone marrow-derived cells leads to increased cholesterol efflux and decreased atherosclerosis. Circulation 2012 126 2236 2247. doi: 10.1161/CIRCULATIONAHA.111.086041
50. Joseph SB, Bradley MN, Castrillo A, Bruhn KW, Mak PA, Pei L, Hogenesch J, O'connell RM, Cheng G, Saez E, Miller JF, Tontonoz P, LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 2004 119 299 309. doi: 10.1016/j.cell.2004.09.032