Microglial activatory (immunoreceptor tyrosine-based activation motif)- and inhibitory (immunoreceptor tyrosine-based inhibition motif)-signaling receptors for recognition of the neuronal glycocalyx

GLIA

Volumn 61, Issue 1, 2013, Pages 37-46

  Linnartz, Bettina ^a   Neumann, Harald ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Complement receptor 3; DAP12; Immunoreceptor tyrosine based activation motif; Immunoreceptor tyrosine based inhibition motif; Microglia; Sialic acid; Sialic acid binding immunoglobulin superfamily lectins; Triggering receptor expressed on myeloid cells 2

Indexed keywords

ADAPTOR PROTEIN; CARBOHYDRATE BINDING PROTEIN; CELL RECEPTOR; COMPLEMENT RECEPTOR; GLYCOLIPID; GLYCOPROTEIN; LECTIN; MEMBRANE RECEPTOR; MICROGLIAL ACTIVATORY SIGNALING RECEPTOR; MICROGLIAL INHIBITORY SIGNALING RECEPTOR; SIALIC ACID; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CELL MIGRATION; GLYCOCALYX; GLYCOSYLATION; HUMAN; IMMUNE RESPONSE; MICROGLIA; MOLECULAR RECOGNITION; NERVE CELL INHIBITION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; TARGET CELL;

ANIMALS; GLYCOCALYX; HUMANS; IMMUNORECEPTOR TYROSINE-BASED ACTIVATION MOTIF; IMMUNORECEPTOR TYROSINE-BASED INHIBITION MOTIF; MICROGLIA; NEURONS; SIGNAL TRANSDUCTION;

EID: 84869170399     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22359     Document Type: Article

References (92)

1. Angata T, Kerr SC, Greaves DR, Varki NM, Crocker PR, Varki A. 2002. Cloning and characterization of human Siglec-11-A recently evolved signaling molecule that can interact with SHP-1 and SHP-2 and is expressed by tissue macrophages, including brain microglia. J Biol Chem 277: 24466.
2. Azuma Y, Taniguchi A, Matsumoto K. 2000. Decrease in cell surface sialic acid in etoposide-treated Jurkat cells and the role of cell surface sialidase. Glycoconj J 17: 301-306.
3. Barclay AN, Brown MH. 2006. The SIRP family of receptors and immune regulation. Nat Rev Immunol 6: 457-464.
4. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang JP, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Lieberburg I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, Yednock T. 2000. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease 6: 916.
5. Barrier L, Barrier J, Arnaud M, Piriou A, Tallineau C. 1997. Alterations in the ganglioside composition of rat cortical brain slices during experimental lactic acidosis: Implications of an enzymatic process independent of the oxidative stress. Biochim Biophys Acta 1336: 15-22.
6. Biber K, Neumann H, Inoue K, Boddeke HW. 2007. Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 30: 596-602.
7. Billadeau DD, Leibson PJ. 2002. ITAMs versus ITIMs: Striking a balance during cell regulation. J Clin Invest 109: 161.
8. Boyd CR, Orr SJ, Spence S, Burrows JF, Elliott J, Carroll HP, Brennan K, Gabhann JN, Coulter WA, Johnston JA, Jefferies CA. 2009. Siglec-E is up-regulated and phosphorylated following lipopolysaccharide stimulation in order to limit TLR-driven cytokine production. J Immunol 183: 7703.
9. Brouwers N, Cauwenberghe CV, Engelborghs S, Lambert JC, Bettens K, Bastard NL, Pasquier F, Montoya AG, Peeters K, Mattheijssens M, Vandenberghe R, De Deyn PP, Cruts M, Amouyel P, Sleegers K, Van Broeckhoven C. 2011. Alzheimer risk associated with a copy number variation in the complement receptor 1 increasing C3b/C4b binding sites. Mol Psychiatry 17: 223-233.
10. Cao H, de Bono B, Belov K, Wong ES, Trowsdale J, Barrow AD. 2009. Comparative genomics indicates the mammalian CD33rSiglec locus evolved by an ancient large-scale inverse duplication and suggests all Siglecs share a common ancestral region. Immunogenetics 61: 401.
11. Cao H, Lakner U, de Bono B, Traherne JA, Trowsdale J, Barrow AD. 2008. SIGLEC16 encodes a DAP12-associated receptor expressed in macrophages that evolved from its inhibitory counterpart SIGLEC11 and has functional and non-functional alleles in humans. Eur J Immunol 38: 2303.
12. Carson MJ, Doose JM, Melchior B, Schmid CD, Ploix CC. 2006. CNS immune privilege: Hiding in plain sight. Immunol Rev 213: 48-65.
13. Chan WY, Kohsaka S, Rezaie P. 2007. The origin and cell lineage of microglia: New concepts. Brain Res Rev 53: 344-354.
14. Chouery E, Delague V, Bergougnoux A, Koussa S, Serre JL, Megarbane A. 2008. Mutations in TREM2 lead to pure early-onset dementia without bone cysts. Hum Mutat 29: E194.
15. Colonna M. 2003. Trems in the immune system and beyond. Nat Rev Immunol 3: 445.
16. Crehan H, Holton P, Wray S, Pocock J, Guerreiro R, Hardy J. 2011. Complement receptor 1 (CR1) and Alzheimer's disease. Immunobiology 217: 244-250.
17. Crocker PR. 2005. Siglecs in innate immunity. Curr Opin Pharmacol 5: 431.
18. Crocker PR, Paulson JC, Varki A. 2007. Siglecs and their roles in the immune system. Nat Rev Immunol 7: 255.
19. Dam TK, Brewer CF. 2010. Lectins as pattern recognition molecules: The effects of epitope density in innate immunity. Glycobiology 20: 270-279.
20. Daws MR, Sullam PM, Niemi EC, Chen TT, Tchao NK, Seaman WE. 2003. Pattern recognition by TREM-2: Binding of anionic ligands. J Immunol 171: 594-599.
21. 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.
22. Fallman M, Andersson R, Andersson T. 1993. Signaling properties of CR3 (CD11b/CD18) and CR1 (CD35) in relation to phagocytosis of complement-opsonized particles. J Immunol 151: 330-338.
23. Flannagan RS, Jaumouille V, Grinstein S. 2011. The cell biology of phagocytosis. Annu Rev Pathol 7: 61-98.
24. Frank MG, Barrientos RM, Biedenkapp JC, Rudy JW, Watkins LR, Maier SF. 2006. mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol Aging 27: 717-722.
25. 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.
26. Fu H, Liu B, Frost J, Hong S, Jin M, Ostaszewski B, Shankar G, Costantino I, Carroll M, Mayadas T, Lemere CA. 2012. Complement component C3 and complement receptor type 3 contribute to the phagocytosis and clearance of fibrillar Aβ by microglia. Glia 60: 993.
27. Gaikwad S, Larionov S, Wang Y, Dannenberg H, Matozaki T, Monsonego A, Thal DR, Neumann H. 2009. Signal regulatory protein-beta 1 a microglial modulator of phagocytosis in Alzheimer's disease. Am J Pathol 175: 2528.
28. Garcia-Garcia E, Rosales C. 2002. Signal transduction during Fc receptor-mediated phagocytosis. J Leukoc Biol 72: 1092.
29. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalvov IM, Merad M. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330: 841-845.
30. Gitik M, Liraz-Zaltsman S, Oldenborg PA, Reichert F, Rotshenker S. 2011. Myelin down-regulates myelin phagocytosis by microglia and macrophages through interactions between CD47 on myelin and SIRPalpha (signal regulatory protein-alpha) on phagocytes. J Neuroinflammation 8: 24.
31. 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.
32. Hanisch UK, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
33. Hayakawa T, Angata T, Lewis AL, Mikkelsen TS, Varki NM, Varki A. 2005. A human-specific gene in microglia. Science 309: 1693.
34. Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, Barclay AN, Sedgwick JD. 2000. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290: 1768-1771.
35. 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.
36. Inoue S, Lin SL, Lee YC, Inoue Y. 2001. An ultrasensitive chemical method for polysialic acid analysis. Glycobiology 11: 759-767.
37. Ivashkiv LB. 2009. Cross-regulation of signaling by ITAM-associated receptors. Nat Immunol 10: 340-347.
38. Jandus C, Simon HU, von Gunten S. 2011. Targeting Siglecs-A novel pharmacological strategy for immuno- and glycotherapy. Biochem Pharmacol 82: 323-332.
39. Kim MK, Pan XQ, Huang ZY, Hunter S, Hwang PH, Indik ZK, Schreiber AD. 2001. Fc gamma receptors differ in their structural requirements for interaction with the tyrosine kinase Syk in the initial steps of signaling for phagocytosis. Clin Immunol 98: 125-132.
40. Lambert JC, Heath S, Even G, Campion D, Sleegers K, Hiltunen M, Combarros O, Zelenika D, Bullido MJ, Tavernier B, Letenneur L, Bettens K, Berr C, Pasquier F, Fiévet N, Barberger-Gateau P, Engelborghs S, De Deyn P, Mateo I, Franck A, Helisalmi S, Percellini E, Hanon O, the European Alzheimer's Disease Initiative Investigators, de Pancorbo MM, Lendon C, Dufouil C, Jaillard C, Leveillard T, Alvarez V, Bosco P, Mancuso M, Panza F, Nacmias B, Bossú P, Piccardi P, Annoni G, Seripa D, Galimberti D, Hannequin D, Licastro F, Soininen H, Ritchie K, Blanché H, Dartigues JF, Tzourio C, Gut I, Van Broeckhoven C, Alpérovitch A, Lathrop M, Amouyel P. 2009. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 41: 1094-1099.
41. Lanier LL, Bakker AB. 2000. The ITAM-bearing transmembrane adaptor DAP12 in lymphoid and myeloid cell function. Immunol Today 21: 611.
42. Linnartz B, Kopatz J, Tenner AJ, Neumann H. 2012. Sialic acid on the neuronal glycocalyx prevents complement C1 binding and complement receptor-3 mediated removal by microglia. J Neurosci 32: 946-952.
43. Linnartz B, Wang Y, Neumann H. 2010. Microglial immunoreceptor tyrosine-based activation and inhibition motif signaling in neuroinflammation. Int J Alzheimers Dis. doi:10.4061/2010/587463.
44. Lock K, Zhang J, Lu J, Lee SH, Crocker PR. 2004. Expression of CD33-related siglecs on human mononuclear phagocytes, monocyte-derived dendritic cells and plasmacytoid dendritic cells. Immunobiology 209: 199-207.
45. Lowell CA. 2011. Src-family and Syk kinases in activating and inhibitory pathways in innate immune cells: Signaling cross talk. Cold Spring Harb Perspect Biol 3.
46. Lue LF, Walker DG. 2002. Modeling Alzheimer's disease immune therapy mechanisms: Interactions of human postmortem microglia with antibody-opsonized amyloid beta peptide. J Neurosci Res 70: 599-610.
47. 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.
48. Lunnon K, Teeling JL, Tutt AL, Cragg MS, Glennie MJ, Perry VH. 2011. Systemic inflammation modulates Fc receptor expression on microglia during chronic neurodegeneration. J Immunol 186: 7215-7224.
49. Lyons A, Downer EJ, Crotty S, Nolan YM, Mills KH, Lynch MA. 2007. CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: A role for IL-4. J Neurosci 27: 8309-8313.
50. Matani P, Sharrow M, Tiemeyer M. 2007. Ligand, modulatory, and co-receptor functions of neural glycans. Front Biosci 12: 3852-3879.
51. Meesmann HM, Fehr EM, Kierschke S, Herrmann M, Bilyy R, Heyder P, Blank N, Krienke S, Lorenz HM, Schiller M. 2010. Decrease of sialic acid residues as an eat-me signal on the surface of apoptotic lymphocytes. J Cell Sci 123(Pt 19): 3347-3356.
52. Melchior B, Garcia AE, Hsiung BK, Lo KM, Doose JM, Thrash JC, Stalder AK, Staufenbiel M, Neumann H, Carson MJ. 2010. Dual induction of TREM2 and tolerance-related transcript, Tmem176b, in amyloid transgenic mice: Implications for vaccine-based therapies for Alzheimer's disease. ASN Neuro 2: e00037.
53. 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(Pt 1): 343-351.
54. Moseley R, Waddington R, Evans P, Halliwell B, Embery G. 1995. The chemical modification of glycosaminoglycan structure by oxygen-derived species in vitro. Biochim Biophys Acta 1244: 245-252.
55. Moseley R, Waddington RJ, Embery G. 1997. Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes. Biochim Biophys Acta 1362: 221-231.
56. N'Diaye EN, Branda CS, Branda SS, Nevarez L, Colonna M, Lowell C, Hamerman JA, Seaman WE. 2009. TREM-2 (triggering receptor expressed on myeloid cells 2) is a phagocytic receptor for bacteria. J Cell Biol 184: 215.
57. Nguyen DH, Hurtado-Ziola N, Gagneux P, Varki A. 2006. Loss of Siglec expression on T lymphocytes during human evolution. Proc Natl Acad Sci U S A 103: 7765-7770.
58. Nimmerjahn F, Ravetch JV. 2006. Fc gamma receptors: Old friends and new family members. Immunity 24: 19.
59. Nimmerjahn F, Ravetch JV. 2008. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8: 34-47.
60. O'Neill SK, Getahun A, Gauld SB, Merrell KT, Tamir I, Smith MJ, Dal Porto JM, Li QZ, Cambier JC. 2011. Monophosphorylation of CD79a and CD79b ITAM motifs initiates a SHIP-1 phosphatase-mediated inhibitory signaling cascade required for B cell anergy. Immunity 35: 746-756.
61. Oyelaran O, Li Q, Farnsworth D, Gildersleeve JC. 2009. Microarrays with varying carbohydrate density reveal distinct subpopulations of serum antibodies. J Proteome Res 8: 3529-3538.
62. Painbeni T, Gamelin E, Cailleux A, Le Bouil A, Boisdron-Celle M, Daver A, Larra F, Allain P. 1997. Plasma sialic acid as a marker of the effect of the treatment on metastatic colorectal cancer. Eur J Cancer 33: 2216-2220.
63. Paloneva J, Kestila M, Wu J, Salminen A, Bohling T, Ruotsalainen V, Hakola P, Bakker AB, Phillips JH, Pekkarinen P, Lanier LL, Timonen T, Peltonen L. 2000. Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25: 357.
64. Paul SP, Taylor LS, Stansbury EK, McVicar DW. 2000. Myeloid specific human CD33 is an inhibitory receptor with differential ITIM function in recruiting the phosphatases SHP-1 and SHP-2. Blood 96: 483-490.
65. Peress NS, Siegelman J, Fleit HB, Fanger MW, Perillo E. 1989. Monoclonal antibodies identify three IgG Fc receptors in normal human central nervous system. Clin Immunol Immunopathol 53: 268.
66. Perez-Oliva AB, Martinez-Esparza M, Vicente-Fernandez JJ, Corral-San Miguel R, Garcia-Penarrubia P, Hernandez-Caselles T. 2011. Epitope mapping, expression and post-translational modifications of two isoforms of CD33 (CD33M and CD33m) on lymphoid and myeloid human cells. Glycobiology 21: 757-770.
67. Powell LD, Sgroi D, Sjoberg ER, Stamenkovic I, Varki A. 1993. Natural ligands of the B cell adhesion molecule CD22 beta carry N-linked oligosaccharides with alpha-2, 6-linked sialic acids that are required for recognition. J Biol Chem 268: 7019-7027.
68. Rachmilewitz J. 2010. Glycosylation: An intrinsic sign of "danger". Self Nonself 1: 250-254.
69. Ransohoff RM, Perry VH. 2009. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27: 119-145.
70. Roberts GP. 1977. Histochemical detection of sialic acid residues using periodate oxidation. Histochem J 9: 97-102.
71. Rodriguez PE, Maggio B, Cumar FA. 1996. Acid and enzymatic hydrolysis of the internal sialic acid residue in native and chemically modified ganglioside GM1. J Lipid Res 37: 382-390.
72. Ross GD, Newman SL, Lambris JD, Devery-Pocius JE, Cain JA, Lachmann PJ. 1983. Generation of three different fragments of bound C3 with purified factor I or serum. II. Location of binding sites in the C3 fragments for factors B and H, complement receptors, and bovine conglutinin. J Exp Med 158: 334-352.
73. Salminen A, Kaarniranta K. 2009. Siglec receptors and hiding plaques in Alzheimer's disease. J Mol Med 87: 697.
74. Schmid CD, Sautkulis LN, Danielson PE, Cooper J, Hasel KW, Hilbush BS, Sutcliffe JG, Carson MJ. 2002. Heterogeneous expression of the triggering receptor expressed on myeloid cells-2 on adult murine microglia. J Neurochem 83: 1309.
75. 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.
76. Stephens L, Ellson C, Hawkins P. 2002. Roles of PI3Ks in leukocyte chemotaxis and phagocytosis. Curr Opin Cell Biol 14: 203.
77. Takahashi K, Prinz M, Stagi M, Chechneva O, Neumann H. 2007. TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. Plos Med 4: 675.
78. Takahashi K, Rochford CDP, Neumann H. 2005. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201: 647-657.
79. Tomasello E, Cant C, Buhring HJ, Vely F, Andre P, Seiffert M, Ullrich A, Vivier E. 2000. Association of signal-regulatory proteins beta with KARAP/DAP-12. Eur J Immunol 30: 2147.
80. Ulvestad E, Williams K, Vedeler C, Antel J, Nyland H, Mork S, Matre R. 1994. Reactive microglia in multiple-sclerosis lesions have an increased expression of receptors for the Fe part of Igg. J Neurol Sci 121: 125.
81. Varki A. 2007. Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 446: 1023.
82. Varki A. 2009. Natural ligands for CD33-related Siglecs? Glycobiology 19: 810.
83. Varki A. 2011. Since there are PAMPs and DAMPs, there must be SAMPs? Glycan "self-associated molecular patterns" dampen innate immunity, but pathogens can mimic them. Glycobiology 21: 1121-1124.
84. Varki A, Angata T. 2006. Siglecs-the major subfamily of I-type lectins. Glycobiology 16: 1R.
85. Wakselman S, Bechade 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.
86. Wang XJ, Ye M, Zhang YH, Chen SD. 2007. CD200-CD200R regulation of microglia activation in the pathogenesis of Parkinson's disease. J Neuroimmune Pharmacol 2: 259-264.
87. Wang Y, Neumann H. 2010. Alleviation of neurotoxicity by microglial human Siglec-11. J Neurosci 30: 3482-3488.
88. Wirenfeldt M, Babcock AA, Vinters HV. 2011. Microglia-insights into immune system structure, function, and reactivity in the central nervous system. Histol Histopathol 26: 519-530.
89. Wright GJ, Cherwinski H, Foster-Cuevas M, Brooke G, Puklavec MJ, Bigler M, Song Y, Jenmalm M, Gorman D, McClanahan T, Liu MR, Brown MH, Sedgwick JD, Phillips JH, Barclay AN. 2003. Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J Immunol 171: 3034-3046.
90. Wright GJ, Puklavec MJ, Willis AC, Hoek RM, Sedgwick JD, Brown MH, Barclay AN. 2000. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity 13: 233-242.
91. Zhang S, Cherwinski H, Sedgwick JD, Phillips JH. 2004. Molecular mechanisms of CD200 inhibition of mast cell activation. J Immunol 173: 6786-6793.
92. 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: 935-940.