Complement protein C1q promotes macrophage anti-inflammatory M2-like polarization during the clearance of atherogenic lipoproteins

Inflammation Research

Volumn 63, Issue 10, 2014, Pages 885-893

  Spivia, Weston ^a   Magno, Patrick S ^a   Le, Patrick ^a   Fraser, Deborah A ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Atherosclerosis; Complement; Cytokine; Innate immunity; Macrophage; Oxidized LDL

Indexed keywords

COMPLEMENT COMPONENT C1Q; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LOW DENSITY LIPOPROTEIN;

ANIMAL; ATHEROSCLEROSIS; C57BL MOUSE; CELL CULTURE; CELL LINE; DRUG EFFECTS; GENETICS; MACROPHAGE; METABOLISM; MOUSE;

ANIMALS; ATHEROSCLEROSIS; CELL LINE; CELLS, CULTURED; COMPLEMENT C1Q; CYTOKINES; LIPOPROTEINS, LDL; MACROPHAGES; MICE; MICE, INBRED C57BL; NF-KAPPA B;

EID: 84929941312     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-014-0762-0     Document Type: Article

References (46)

1. Bohlson SS, Fraser DA, Tenner AJ. Complement proteins c1q and mbl are pattern recognition molecules that signal immediate and long-term protective immune functions. Mol Immunol. 2007;44:33–43.
2. Haskard DO, Boyle JJ, Mason JC. The role of complement in atherosclerosis. Curr Opin Lipidol. 2008;19:478–82.
3. Minino AM. Death in the United States, 2009. NCHS Data Brief. 2011;1–8.
4. Yasojima K, Schwab C, McGeer EG, McGeer PL. Complement components, but not complement inhibitors, are upregulated in atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2001;21:1214–9.
5. Buono C, Come CE, Witztum JL, Maguire GF, Connelly PW, Carroll M, Lichtman AH. Influence of c3 deficiency on atherosclerosis. Circulation. 2002;105:3025–31.
6. Schmiedt W, Kinscherf R, Deigner HP, Kamencic H, Nauen O, Kilo J, Oelert H, Metz J, Bhakdi S. Complement c6 deficiency protects against diet-induced atherosclerosis in rabbits. Arterioscler Thromb Vasc Biol. 1998;18:1790–5.
7. Walport MJ, Davies KA, Botto M. C1q and systemic lupus erythematosus. Immunobiology. 1998;199:265–85.
8. Andres V, Pello OM, Silvestre-Roig C. Macrophage proliferation and apoptosis in atherosclerosis. Curr Opin Lipidol. 2012;23:429–38.
9. Miller YI, Choi SH, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, Boullier A, Gonen A, Diehl CJ, Que X, Montano E, Shaw PX, Tsimikas S, Binder CJ, Witztum JL. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235–48.
10. Kojima C, Ino J, Ishii H, Nitta K, Yoshida M. Mmp-9 inhibition by ace inhibitor reduces oxidized ldl-mediated foam-cell formation. J Atheroscler Thromb. 2010;17:97–105.
11. Tabas I. Cholesterol and phospholipid metabolism in macrophages. Biochim Biophys Acta. 2000;1529:164–74.
12. Hansson GK, Robertson AK, Soderberg-Naucler C. Inflammation and atherosclerosis. Annu Rev Pathol. 2006;1:297–329.
13. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E. Nlrp3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010;464:1357–61.
14. Mantovani A, Garlanda C, Locati M. Macrophage diversity and polarization in atherosclerosis: a question of balance. Arterioscler Thromb Vasc Biol. 2009;29:1419–23.
15. Pello OM, Silvestre C, De Pizzol M, Andres V. A glimpse on the phenomenon of macrophage polarization during atherosclerosis. Immunobiology. 2011;216:1172–6.
16. Feig JE, Rong JX, Shamir R, Sanson M, Vengrenyuk Y, Liu J, Rayner K, Moore K, Garabedian M, Fisher EA. Hdl promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc Natl Acad Sci USA. 2011;108:7166–71.
17. Herranz S, Traves PG, Luque A, Hortelano S. Role of the tumor suppressor ARF in macrophage polarization: enhancement of the m2 phenotype in ARF-deficient mice. Oncoimmunology. 2012;1:1227–38.
18. Raes G, Noel W, Beschin A, Brys L, de Baetselier P, Hassanzadeh GH. Fizz1 and ym as tools to discriminate between differentially activated macrophages. Dev Immunol. 2002;9:151–9.
19. Stoger JL, Gijbels MJ, van der Velden S, Manca M, van der Loos CM, Biessen EA, Daemen MJ, Lutgens E, de Winther MP. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis. 2012;225:461–8.
20. Kirii H, Niwa T, Yamada Y, Wada H, Saito K, Iwakura Y, Asano M, Moriwaki H, Seishima M. Lack of interleukin-1beta decreases the severity of atherosclerosis in apoE-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:656–60.
21. Han X, Kitamoto S, Wang H, Boisvert WA. Interleukin-10 overexpression in macrophages suppresses atherosclerosis in hyperlipidemic mice. FASEB J. 2010;24:2869–80.
22. Benoit ME, Clarke EV, Morgado P, Fraser DA, Tenner AJ. Complement protein c1q directs macrophage polarization and limits inflammasome activity during the uptake of apoptotic cells. J Immunol. 2012;188:5682–93.
23. Fraser DA, Laust AK, Nelson EL, Tenner AJ. C1q differentially modulates phagocytosis and cytokine responses during ingestion of apoptotic cells by human monocytes, macrophages, and dendritic cells. J Immunol. 2009;183:6175–85.
24. Fraser DA, Pisalyaput K, Tenner AJ. C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J Neurochem. 2010;112:733–43.
25. Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ. Homozygous c1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet. 1998;19:56–9.
26. de Winther MP, Kanters E, Kraal G, Hofker MH. Nuclear factor kappaB signaling in atherogenesis. Arterioscler Thromb Vasc Biol. 2005;25:904–14.
27. Fraser DA, Arora M, Bohlson SS, Lozano E, Tenner AJ. Generation of inhibitory nfkappaB complexes and phosphorylated camp response element-binding protein correlates with the anti-inflammatory activity of complement protein c1q in human monocytes. J Biol Chem. 2007;282:7360–7.
28. Adamson S, Leitinger N. Phenotypic modulation of macrophages in response to plaque lipids. Curr Opin Lipidol. 2011;22:335–42.
29. Im SS, Yousef L, Blaschitz C, Liu JZ, Edwards RA, Young SG, Raffatellu M, Osborne TF. Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell Metab. 2011;13:540–9.
30. Fraser DA, Tenner AJ. Innate immune proteins c1q and mannan-binding lectin enhance clearance of atherogenic lipoproteins by human monocytes and macrophages. J Immunol. 2010;185:3932–9.
31. −/−) mice with wild-type bone marrow cells. J Immunol. 2001;167:4033–7.
32. Greenlee MC, Sullivan SA, Bohlson SS. Detection and characterization of soluble cd93 released during inflammation. Inflamm Res. 2009;58:909–19.
33. Nauta AJ, Castellano G, Xu W, Woltman AM, Borrias MC, Daha MR, van Kooten C, Roos A. Opsonization with c1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J Immunol. 2004;173:3044–50.
34. Nauta AJ, Raaschou-Jensen N, Roos A, Daha MR, Madsen HO, Borrias-Essers MC, Ryder LP, Koch C, Garred P. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur J Immunol. 2003;33:2853–63.
35. Korb LC, Ahearn JM. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol. 1997;158:4525–8.
36. Monaco C, Paleolog E. Nuclear factor kappaB: a potential therapeutic target in atherosclerosis and thrombosis. Cardiovasc Res. 2004;61:671–82.
37. Bhatia VK, Yun S, Leung V, Grimsditch DC, Benson GM, Botto MB, Boyle JJ, Haskard DO. Complement c1q reduces early atherosclerosis in low-density lipoprotein receptor-deficient mice. Am J Pathol. 2007;170:416–26.
38. Galvan MD, Greenlee-Wacker MC, Bohlson SS. C1q and phagocytosis: the perfect complement to a good meal. J Leukoc Biol. 2012;92:489–97.
39. Fraser DA, Tenner AJ. Directing an appropriate immune response: the role of defense collagens and other soluble pattern recognition molecules. Curr Drug Targets. 2008;9:113–22.
40. Galvan MD, Foreman DB, Zeng E, Tan JC, Bohlson SS. Complement component c1q regulates macrophage expression of mer tyrosine kinase to promote clearance of apoptotic cells. J Immunol. 2012;188:3716–23.
41. Jiang Y, Wang M, Huang K, Zhang Z, Shao N, Zhang Y, Wang W, Wang S. Oxidized low-density lipoprotein induces secretion of interleukin-1beta by macrophages via reactive oxygen species-dependent NLRP3 inflammasome activation. Biochem Biophys Res Commun. 2012;425:121–6.
42. Kannan Y, Sundaram K, Aluganti Narasimhulu C, Parthasarathy S, Wewers MD. Oxidatively modified low density lipoprotein (ldl) inhibits tlr2 and tlr4 cytokine responses in human monocytes but not in macrophages. J Biol Chem. 2012;287:23479–88.
43. Min KJ, Cho KH, Kwon TK. The effect of oxidized low density lipoprotein (oxldl)-induced heme oxygenase-1 on lps-induced inflammation in raw 264.7 macrophage cells. Cell Signal. 2012;24:1215–21.
44. Hartman J, Frishman WH. Inflammation and atherosclerosis: a review of the role of interleukin-6 in the development of atherosclerosis and the potential for targeted drug therapy. Cardiol Rev. 2014;22:147–51.
45. Lawrence T. The nuclear factor nf-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol. 2009;1:a001651.
46. Cominacini L, Pasini AF, Garbin U, Davoli A, Tosetti ML, Campagnola M, Rigoni A, Pastorino AM, Lo Cascio V, Sawamura T. Oxidized low density lipoprotein (ox-ldl) binding to ox-ldl receptor-1 in endothelial cells induces the activation of nf-kappaB through an increased production of intracellular reactive oxygen species. J Biol Chem. 2000;275:12633–8.