Sialylation of neurites inhibits complement-mediated macrophage removal in a human macrophage-neuron Co-Culture System

GLIA

Volumn 64, Issue 1, 2016, Pages 35-47

  Linnartz Gerlach, Bettina ^a   Schuy, Christine ^a   Shahraz, Anahita ^a   Tenner, Andrea J ^b   Neumann, Harald ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Complement; Human; Macrophage; Neurons; Phagocytosis; Sialic acid

Indexed keywords

BETA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CD11B ANTIGEN; CD18 ANTIGEN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT RECEPTOR 3; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MICROTUBULE ASSOCIATED PROTEIN 2; NERVE CELL ADHESION MOLECULE; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; CR1 PROTEIN, HUMAN; ITGAM PROTEIN, HUMAN; N ACETYLNEURAMINIC ACID;

ARTICLE; COCULTURE; COMPLEMENT FIXATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; GLYCOCALYX; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE; NEURITE; NEUROFILAMENT; OPSONIZATION; PHAGOCYTOSIS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIALYLATION; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MUCOLIPIDOSIS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY;

ANTIGENS, CD11B; COCULTURE TECHNIQUES; COMPLEMENT C1Q; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MACROPHAGE-1 ANTIGEN; MACROPHAGES; MONOCYTES; MUCOLIPIDOSES; N-ACETYLNEURAMINIC ACID; NEURAL STEM CELLS; NEURITES; NEUROGENESIS; NEURONS; PHAGOCYTOSIS; RECEPTORS, COMPLEMENT 3B;

EID: 84954370985     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22901     Document Type: Article

References (44)

1. Barnum SR. 1995. Complement biosynthesis in the central nervous system. Crit Rev Oral Biol Med 6:132-146.
2. 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.
3. Beller DI, Springer TA, Schreiber RD. 1982. Anti-Mac-1 Selectively Inhibits the Mouse and Human Type 3 Complement Receptor. J Exp Med 156:1000
4. 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.
5. Bobak DA, Frank MM, Tenner AJ. 1988. C1q acts synergistically with phorbol dibutyrate to activate CR1-mediated phagocytosis by human mononuclear phagocytes. Eur J Immunol 18:2001-2007.
6. Brinkman-Van der Linden EC, Angata T, Reynolds SA, Powell LD, Hedrick SM, Varki A. 2003. CD33/Siglec-3 binding specificity, expression pattern, and consequences of gene deletion in mice. Mol Cell Biol 23:4199-41206.
7. Brouwers N, Cauwenberghe CV, Engelborghs S, Lambert JC, Bettens K, Bastard NL, Pasquier F, Montoya AG, Peeters K, Mattheijssens M, Vandenberghe R, Deyn PP, Crusts M, Amouyel P, Sleegers K, Broeckhoven CV. 2011. Alzheimer risk associated with a copy number variation in the complement receptor 1 increasing C3b/C4b binding sites. Mol Psychiatry 17:223-233.
8. Brown GC, Neher JJ. 2014. Microglial phagocytosis of live neurons. Nat Rev Neurosci 15:209-216.
9. Bruhns P. 2012. Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119:5640-5649.
10. Chung WS, Clarke LE, Wang GX, Stafford BK, Sher A, Chakraborty C, Joung J, Foo LC, Thompson A, Chen C, Smith SJ, Barres BA. 2013. Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504:394-400.
11. Crehan H, Hardy J, Pocock J. 2013. Blockage of CR1 prevents activation of rodent microglia. Neurobiol Dis 54:139-149.
12. Crocker PR, Paulson JC, Varki A. 2007. Siglecs and their roles in the immune system. Nat Rev Immunol 7:255-266.
13. Cross AS, Sakarya S, Rifat S, Held TK, Drysdale BE, Grange PA, Cassels FJ, Wang LX, Stamatos N, Farese A, Casey D, Powell J, Bhattacharjee AK, Kleinberg M, Goldblum SE. 2003. Recruitment of murine neutrophils in vivo through endogenous sialidase activity. J Biol Chem 278:4112-4120.
14. 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.
15. Ferreira VP, Pangburn MK, Cortes C. 2010. Complement control protein factor H: The good, the bad, and the inadequate. Mol Immunol 47:2187-2197.
16. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841-845.
17. Hanisch UK, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
18. Hayakawa T, Angata T, Lewis AL, Mikkelsen TS, Varki NM, Varki A. 2005. A human-specific gene in microglia. Science 309:1693
19. Holers VM, Kinoshita T, Molina H. 1992. The evolution of mouse and human complement C3-binding proteins: Divergence of form but conservation of function. Immunol Today 13:231-236.
20. 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.
21. Inoue S, Inoue Y. 2001. Developmental profile of neural cell adhesion molecule glycoforms with a varying degree of polymerization of polysialic acid chains. J Biol Chem 276:31863-31870.
22. Jacobson AC, Weis JH. 2008. Comparative functional evolution of human and mouse CR1 and CR2. J Immunol 181:2953-2959.
23. Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, Muller DN, Luckow B, Brocker T, Debowski K, Fritz G, Opdenakker G, Diefenbach A, Biber K, Heikenwalder M, Geissmann F, Rosenbauer F, Prinz M. 2013. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16:273-280.
24. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B. 2009. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29:1319
25. Li W, Sun W, Zhang Y, Wei W, Ambasudhan R, Xia P, Talantova M, Lin T, Kim J, Wang X, Kim WR, Lipton SA, Zhang K, Ding S. 2011. Rapid induction and long-term self-renewal of primitive neural precursors from human embryonic stem cells by small molecule inhibitors. Proc Natl Acad Sci USA 108:8299-8304.
26. Liang F, Seyrantepe V, Landry K, Ahmad R, Ahmad A, Stamatos NM, Pshezhetsky AV. 2006. Monocyte differentiation up-regulates the expression of the lysosomal sialidase, Neu1, and triggers its targeting to the plasma membrane via major histocompatibility complex class II-positive compartments. J Biol Chem 281:27526-27538.
27. Linnartz-Gerlach B, Mathews M, Neumann H. 2014. Sensing the neuronal glycocalyx by glial sialic acid binding immunoglobulin-like lectins. Neuroscience 275:113-124. C:
28. 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.
29. Linnartz B, Neumann H. 2013. Microglial activatory (immunoreceptor tyrosine-based activation motif)- and inhibitory (immunoreceptor tyrosine-based inhibition motif)-signaling receptors for recognition of the neuronal glycocalyx. Glia 61:37-46.
30. Lukong KE, Seyrantepe V, Landry K, Trudel S, Ahmad A, Gahl WA, Lefrancois S, Morales CR, Pshezhetsky AV. 2001. Intracellular distribution of lysosomal sialidase is controlled by the internalization signal in its cytoplasmic tail. J Biol Chem 276:46172-46181.
31. 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 123:3347-3356.
32. Rachmilewitz J. 2010. Glycosylation: An intrinsic sign of "danger". Self Nonself 1:250-254.
33. Ransohoff RM, Perry VH. 2009. Microglial physiology: Unique stimuli, specialized responses. Annu Rev Immunol 27:119-145.
34. 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.
35. 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.
36. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. 2012. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691-705.
37. Seyrantepe V, Iannello A, Liang F, Kanshin E, Jayanth P, Samarani S, Szewczuk MR, Ahmad A, Pshezhetsky AV. 2009. Regulation of phagocytosis in macrophages by neuraminidase 1. J Biol Chem 285:206-215.
38. Shay T, Jojic V, Zuk O, Rothamel K, Puyraimond-Zemmour D, Feng T, Wakamatsu E, Benoist C, Koller D, Regev A, ImmGen Consortium 2013. Conservation and divergence in the transcriptional programs of the human and mouse immune systems. Proc Natl Acad Sci USA 110:2946-2951.
39. Smith AM, Dragunow M. 2014. The human side of microglia. Trends Neurosci 37:125-135.
40. 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 SWM, Barres BA. 2007. The classical complement cascade mediates CNS synapse elimination. Cell 131:1164-1178.
41. Sutterwala FS, Rosenthal LA, Mosser DM. 1996. Cooperation between CR1 (CD35) and CR3 (CD 11b/CD18) in the binding of complement-opsonized particles. J Leukoc Biol 59:883-890.
42. Tchilian EZ, Beverley PC, Young BD, Watt SM. 1994. Molecular cloning of two isoforms of the murine homolog of the myeloid CD33 antigen. Blood 83:3188-3198.
43. Varki A. 2010. Colloquium paper: Uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci USA 107 Suppl 2:8939-8946.
44. 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.