SIGN-R1, a C-type lectin, enhances apoptotic cell clearance through the complement deposition pathway by interacting with C1q in the spleen

Cell Death and Differentiation

Volumn 20, Issue 4, 2013, Pages 535-545

  Prabagar, M G ^a   Do, Y ^b   Ryu, S ^c   Park, J Y ^a   Choi, H J ^a   Choi, W S ^d   Yun, T J ^e   Moon, J ^f   Choi, I S ^a   Ko, K ^g,h   Young Shin, C ^h   Cheong, C ^f   Kang, Y S ^a  

^a Konkuk University   (South Korea)

^b Ulsan National Institute of Science and Technology   (South Korea)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d New Drug Development Center   (South Korea)

^e CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

^g Chung Ang University   (South Korea)

^h Konkuk University School of Medicine   (South Korea)

Author keywords

Apoptotic cells; Autoimmune disease; Complements; SIGN R1; Splenic marginal zone macrophages

Indexed keywords

COMPLEMENT COMPONENT C1Q; DOUBLE STRANDED DNA ANTIBODY; INTERLEUKIN 6; LECTIN; SIGN R1; SINGLE STRANDED DNA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CLEARANCE; COMPLEMENT DEPOSITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; LIVER; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; OPSONIZATION; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SPLEEN; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; APOPTOSIS; CELL ADHESION MOLECULES; CELLS, CULTURED; CHO CELLS; COMPLEMENT C1Q; COMPLEMENT C3; CRICETINAE; CRICETULUS; DNA, SINGLE-STRANDED; HUMANS; INTERLEUKIN-10; INTERLEUKIN-6; JURKAT CELLS; LECTINS, C-TYPE; LIVER; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPLEEN; THYMOCYTES; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

MUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84874948249     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.160     Document Type: Article

References (53)

1. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 2004; 14: 277-287.
2. Ravichandran KS, Lorenz U. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 2007; 7: 964-974.
3. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell 2002; 111: 927-930.
4. Erwig LP, Henson PM. Clearance of apoptotic cells by phagocytes. Cell Death Differ 2008; 15: 243-250.
5. Firestein GS, Yeo M, Zvaifler NJ. Apoptosis in rheumatoid arthritis synovium. J Clinic Invest 1995; 96: 1631-1638.
6. Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, Neuhuber WL et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 2002; 46: 191-201.
7. Botto M, Dell'Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F et al. Homozygous C1q deficiency causes glomerulonephrities associated with multiple apoptotic bodies. Nat Genet 1998; 19: 56-59.
8. Schrijvers DM, De Meyer GR, Kockx MM, Herman AG, Martinet W. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol 2005; 6: 1256-1261.
9. Miyake Y, Asano K, Kaise H, Uemura M, Nakayama M, Tanaka M. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J Clin Invest 2007; 117: 2268-2278.
10. McGaha TL, Chen Y, Ravishankar B, van Rooijen N, Karlsson MC. Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 2011; 117: 5403-5412.
11. Kraal G. Cells in the marginal zone of the spleen. Int Rev Cytol 1992; 132: 31-74.
12. Kraal G, Mebius R. New insights into the cell biology of the marginal zone of the spleen. Int Rev Cytol 2006; 250: 175-215.
13. Kang YS, Yamazaki S, Iyoda T, Pack M, Bruening SA, Kim JY et al. SIGN-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int Immunol 2003; 15: 177-186.
14. Miyake Y, Asano K, Kaise H, Uemura M, Nakayama M, Tanaka M. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J Clin Invest 2007; 117: 2268-2278.
15. Morelli AE, Larregina AT, Shufesky WJ, Zahorchak AF, Logar AJ, Papworth GD et al. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 2003; 101: 611-620.
16. Takizawa F, Tsuji S, Nagasawa S. Enhancement of macrophage phagocytosis upon iC3b deposition on apoptotic cells. FEBS Lett 1996; 397: 269-272.
17. Mevorach D, Mascarenhas JO, Gershov D, Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 1998; 188: 2313-2320.
18. Flierman R, Daha MR. The clearance of apoptotic cells by complement. Immunobiol 2006; 212: 363-370.
19. Trouw LA, Blom AM, Gasque P. Role of complement and complement regulators in the removal of apoptotic cells. Mol Immunol 2008; 45: 1199-1207.
20. 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: 4525-4528.
21. Navratil JS, Watkin SC, Wisnieski JJ, Ahearn JM. The globular heads of C1q specifically recognize surface blebs of apoptotic vascular endothelial cells. J Immunol 2001; 166: 3231-3239.
22. Ogden CA, deCathelineau A, Hoffmann PR, Bratton D, Ghebrehiwet B, Fadok VA et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001; 194: 781-795.
23. Nauta AJ, Trouw LA, Daha MR, Tijsma O, Nieuwland R, Schwaeble WJ et al. Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur J Immunol 2002; 32: 1726-1736.
24. Nauta AJ, Raaschou-Jensen N, Roos A, Daha MR, Madsen HO, Borrias-Essers MC et al. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur J Immunol 2003; 33: 2853-2863.
25. Roos A, Xu W, Castellano G, Nauta AJ, Garred P, Daha MR et al. Mini-review: a pivotal role for innate immunity in the clearance of apoptotic cells. Eur J Immunol 2004; 34: 921-929.
26. Kang YS, Do Y, Lee HK, Park SH, Cheong C, Lynch RM et al. A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 2006; 125: 47-58.
27. Lanoue A, Clatworthy MR, Smith P, Green S, Townsend MJ, Jolin HE et al. SIGN-R1 contribute to protection against lethal pneumococcal infection in mice. J Exp Med 2004; 6: 1383-1393.
28. Anthony RM, Wermeling F, Karlsson MCI, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 2008; 105: 19571-19578.
29. Anthony RM, Nimmerjahn F, Ashline DJ, Reinhold VN, Paulson JC, Ravetch JV. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 2008; 320: 373-376.
30. Bajenoff M, Narni-Mancinelli E, Brau F, Lauvau G. Visualizing early splenic memory CD8+ T cells reactivation against intracellular bacteria in the mouse. PLoS One 2010; 12: e11524.
31. Langeveld M, Gamadia LE, ten Berge IJ. T-lymphocyte subset distribution in human spleen. Eur J Clin Invest 2006; 36: 250-256.
32. Wermeling F, Chen Y, Pikkarainen T, Scheynius A, Winqvist O, Izui S et al. Class A scavenger receptors regulate tolerance against apoptotic cells, and autoantibodies against these receptors are predictive of systemic lupus. J Exp Med 2007; 204: 2259-2265.
33. Kang YS, Kim JY, Bruening SA, Pack M, Charalambous A, Pritsker A et al. The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen. Proc Natl Acad Sci USA 2004; 101: 215-220.
34. Taylor PR, Brown GD, Herre J, Williams DL, Willment JA, Gordon S. The role of SIGN-R1 ant the b-glucan receptor (Dectin-1) in the nonopsonic recognition of yeast by specific macrophages. J Immunol 2004; 172: 1157-1162.
35. Stuart LM, Takahashi K, Shi L, Savil J, RAB Ezekowitz. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol 2005; 174: 3220-3226.
36. Munoz L, van Bavel C, Franz S, Berden J, Herrmann M, van der Vlag J. Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus 2008; 17: 371-375.
37. Sule S, Rosen A, Petri M, Akhter E, Andrade F. Abnormal production of pro-and antiinflammatory cytokines by lupus monocytes in response to apoptotic cells. PLos ONE 2011; 6: e17495.
38. Kurosaka K, Watanabe N, Kobayashi Y. Production of proinflammatory cytokines by resident tissue macrophages after phagocytosis of apoptotic cells. Cell Immunol 2001; 211: 1-7.
39. Yamazaki T, Naqata K, Kobayashi Y. Cytokine production by M-CSF and GM-CSFinduced mouse bone marrow-derived macrophages upon coculturing with late apoptotic cells. Cell Immunol 2008; 251: 124-130.
40. Takahashi M, Kobayashi Y. Cytokine production in association with phagocytosis of apoptotic cells by immature dendritic cells. Cell Immunol 2003; 226: 105-115.
41. Gaipl US, Kuenkele S, Voll RE, Beyer TD, Kolowos W, Heyder P et al. Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ 2001; 8: 327-334.
42. Quartier P, Potter PK, Ehrenstein MR, Walport MJ, Botto M. Predominant role of IgM-dependant activation of the classical pathway in the clearance of dying cells by murine marrow-derived macrophages in vitro. Eur J Immunol 2004; 35: 252-260.
43. Parent SA, Zhang T, Chrebet G, Clemas JA, Figueroa DJ, Ky B et al. Molecular characterization of the murine SIGNR1 gene encoding a C-type lectin homologous to human DC-SIGN and DC-SIGNR. Gene 2002; 293: 33-46.
44. Choi HJ, Choi WS, Park JY, Prabagar MG, Kang KH, Jeon SJ et al. SIGN-R1, a C-type lectin, binds to Bip/GRP78 and this interaction mediates the regurgitation of T-cellindependent type 2 antigen dextran through the endoplasmic reticulum. Immunobiol 2011; 216: 437-446.
45. McGaha TL, Chen Y, Ravishankar B, van Rooijen N, Karlsson MC. Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 117: 5403-5412.
46. Ato M, Nakano H, Kakiuchi T, Kaye PM. Localization of marginal zone macrophages is regulated by C-C chemokine ligands 21/19. J Immunol 2004; 173: 4815-4820.
47. Cesta MF. Normal structure, function, and histology of the spleen. Toxicol Pathol 2006; 34: 455-465.
48. Qin X, Gao B. The complement system in liver diseases. Cell Mol Immunol 2006; 3: 333-340.
49. Dini L, Pagliara P, Carla EC. Phagocytosis of apoptotic cells by liver: a morphological study. Microsc Res Tech 2002; 57: 530-540.
50. Helmy KY, Katschke KJ Jr., Gorgani NN, Elliott JM, Diehl L et al. CRIg: a macrophage complement receptor required for phagocytosis of circulating pathogens. Cell 2006; 124: 915-927.
51. Huynh ML, Fadok VA, Henson PM. Phosphatidyl-dependant ingestion of apoptotic cells promotes TGF-b1 secretion and the resolution of inflammation. J Clin Invest 2002; 109: 41-50.
52. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature 1997; 390: 350-351.
53. Fukuyama H, Nimmerjahn F, Ravetch JV. The inhibitory Fcgamma receptor modulates autoimmunity by limiting the accumulation of immunoglobulin G+ anti-DNA plasma cells. Nat Immunol 2005; 6: 99-106.