Sialic acid on the neuronal glycocalyx prevents complement c1 binding and complement receptor-3-mediated removal by microglia

Journal of Neuroscience

Volumn 32, Issue 3, 2012, Pages 946-952

  Linnartz, Bettina ^a   Kopatz, Jens ^a   Tenner, Andrea J ^b   Neumann, Harald ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD11B ANTIGEN; CD18 ANTIGEN; COMPLEMENT COMPONENT C1; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C1R; COMPLEMENT COMPONENT C1S; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3 RECEPTOR; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; SIALIC ACID; SIALIDASE;

ANIMAL TISSUE; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EMBRYO; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GLYCOCALYX; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVE CELL CULTURE; NEURITE; NONHUMAN; PLASMA PROTEIN BINDING; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIALYLATION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD; ANTIGENS, CD11B; BRAIN; CELLS, CULTURED; COCULTURE TECHNIQUES; COMPLEMENT C1Q; COMPLEMENT C3; CYTOKINES; EMBRYO, MAMMALIAN; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GLYCOCALYX; GREEN FLUORESCENT PROTEINS; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NEURAMINIDASE; NEURONS; PROTEIN BINDING; RECEPTORS, COMPLEMENT; SIALIC ACIDS; TRANSFECTION; TUBULIN;

EID: 84856007233     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3830-11.2012     Document Type: Article

References (28)

1. Benoit ME, Tenner AJ (2011) Complement protein C1q-mediated neuroprotection is correlated with regulation of neuronal gene and microRNA expression. J Neurosci 31:3459-3469.
2. Beutner C, Roy K, Linnartz B, Napoli I, Neumann H (2010) Generation of microglial cells from mouse embryonic stem cells. Nat Protoc 5: 1481-1494.
3. Depboylu C, Schäfer MK, Arias-Carrión O, Oertel WH, Weihe E, Höglinger GU (2011) Possible involvement of complement factor C1q in the clearance of extracellular neuromelanin from the substantia nigra in Parkinson disease. J Neuropathol Exp Neurol 70:125-132.
4. Eguchi H, Ikeda Y, Koyota S, Honke K, Suzuki K, Gutteridge JM, Taniguchi N (2002) Oxidative damage due to copper ion and hydrogen peroxide induces GlcNAc-specific cleavage of an Asn-linked oligosaccharide. J Biochem 131:477-484.
5. Ferreira VP, Pangburn MK, Cortés C (2010) Complement control protein factor H: the good, the bad, and the inadequate. Mol Immunol 47:2187-2197.
6. Fraser DA, Tenner AJ (2008) Directing an appropriate immune response: the role of defense collagens and other soluble pattern recognition molecules. Curr Drug Targets 9:113-122.
7. Fraser DA, Pisalyaput K, Tenner AJ (2009) C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J Neurochem 112:733-743.
8. Gorlovoy P, Larionov S, Pham TT, Neumann H (2009) Accumulation of tau induced in neurites by microglial proinflammatory mediators. FASEB J 23:2502-2513.
9. Goswami K, Nandakumar DN, Koner BC, Bobby Z, Sen SK (2003) Oxidative changes and desialylation of serum proteins in hyperthyroidism. Clin Chim Acta 337:163-168.
10. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
11. Howell GR, Macalinao DG, Sousa GL, Walden M, Soto I, Kneeland SC, Barbay JM, King BL, Marchant JK, Hibbs M, Stevens B, Barres BA, Clark AF, Libby RT, John SW (2011) Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J Clin Invest 121:1429-1444.
12. Inforzato A, Peri G, Doni A, Garlanda C, Mantovani A, Bastone A, Carpentieri A, Amoresano A, Pucci P, Roos A, Daha MR, Vincenti S, Gallo G, Carminati P, De Santis R, Salvatori G (2006) Structure and function of the long pentraxin PTX3 glycosidic moiety: fine-tuning of the interaction with C1q and complement activation. Biochemistry 45:11540-11551.
13. Ivashkiv LB (2009) Cross-regulation of signaling by ITAM-associated receptors. Nat Immunol 10:340-347.
14. Khatua B, Ghoshal A, Bhattacharya K, Mandal C, Saha B, Crocker PR, Mandal C (2010) Sialic acids acquired by Pseudomonas aeruginosa are involved in reduced complement deposition and siglec mediated host-cell recognition. FEBS Lett 584:555-561.
15. Lund J, Takahashi N, Pound JD, Goodall M, Jefferis R (1996) Multiple interactions of IgG with its core oligosaccharide can modulate recognition by complement and human Fc gamma receptor I and influence the synthesis of its oligosaccharide chains. J Immunol 157:4963-4969.
16. Monti E, Bassi MT, Papini N, Riboni M, Manzoni M, Venerando B, Croci G, Preti A, Ballabio A, Tettamanti G, Borsani G (2000) Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem J 349:343-351.
17. Napoli I, Kierdorf K, Neumann H (2009) Microglial precursors derived from mouse embryonic stem cells. Glia 57:1660-1671.
18. Neumann H, Kotter MR, Franklin RJ (2009) Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132:288-295.
19. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458.
20. Ransohoff RM, Cardona AE (2010) The myeloid cells of the central nervous system parenchyma. Nature 468:253-262.
21. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119-145.
22. Shi Y, Tohyama Y, Kadono T, He J, Miah SM, Hazama R, Tanaka C, Tohyama K, Yamamura H (2006) Protein-tyrosine kinase Syk is required for pathogen engulfment in complement-mediated phagocytosis. Blood 107:4554-4562.
23. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164-1178.
24. Takahashi K, Rochford CD, Neumann H (2005) Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201:647-657.
25. Tateno H, Crocker PR, Paulson JC (2005) Mouse Siglec-F and human Siglec-8 are functionally convergent paralogs that are selectively expressed on eosinophils and recognize 6'-sulfo-sialyl Lewis X as a preferred glycan ligand. Glycobiology 15:1125-1135.
26. Wakselman S, Béchade C, Roumier A, Bernard D, Triller A, Bessis A (2008) Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J Neurosci 28:8138-8143.
27. Walker DG, Kim SU, McGeer PL (1995) Complement and cytokine gene expression in cultured microglial derived from postmortem human brains. J Neurosci Res 40:478-493.
28. Ziegenfuss JS, Biswas R, Avery MA, Hong K, Sheehan AE, Yeung YG, Stanley ER, Freeman MR (2008) Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453:935-939.