Microglia-secreted galectin-3 acts as a toll-like receptor 4 ligand and contributes to microglial activation

Cell Reports

Volumn 10, Issue 9, 2015, Pages 1626-1638

  Burguillos, MiguelAngel ^a,b   Svensson, Martina ^b   Schulte, Tim ^a   Boza Serrano, Antonio ^b   Garcia Quintanilla, Albert ^c   Kavanagh, Edel ^a   Santiago, Martiniano ^c   Viceconte, Nikenza ^c   Oliva Martin, MariaJose ^c   Osman, AhmedMohamed ^d   Salomonsson, Emma ^e   Amar, Lahouari ^b   Persson, Annette ^f   Blomgren, Klas ^d   Achour, Adnane ^a   Englund, Elisabet ^f   Leffler, Hakon ^e   Venero, JoseLuis ^c   Joseph, Bertrand ^a   Deierborg, Tomas ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^e LUND UNIVERSITY   (Sweden)

^f LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; CASPASE 8; GALECTIN 1; GALECTIN 3; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANISOTROPY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN ISCHEMIA; CELL ACTIVATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MICRODIALYSIS; MICROGLIA; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

MURINAE;

EID: 84924548953     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.012     Document Type: Article

References (53)

1. Akashi S., Saitoh S., Wakabayashi Y., Kikuchi T., Takamura N., Nagai Y., Kusumoto Y., Fukase K., Kusumoto S., Adachi Y., et al. Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J.Exp. Med. 2003, 198:1035-1042.
2. Anderson A.C., Anderson D.E., Bregoli L., Hastings W.D., Kassam N., Lei C., Chandwaskar R., Karman J., Su E.W., Hirashima M., et al. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 2007, 318:1141-1143.
3. Barondes S.H., Castronovo V., Cooper D.N., Cummings R.D., Drickamer K., Feizi T., Gitt M.A., Hirabayashi J., Hughes C., Kasai K., et al. Galectins: a family of animal beta-galactoside-binding lectins. Cell 1994, 76:597-598.
4. Bocchini V., Mazzolla R., Barluzzi R., Blasi E., Sick P., Kettenmann H. An immortalized cell line expresses properties of activated microglial cells. J.Neurosci. Res. 1992, 31:616-621.
5. Boza-Serrano A., Reyes J.F., Rey N.L., Leffler H., Bousset L., Nilsson U., Brundin P., Venero J., Burguillos M., Deierborg T. The role of Galectin-3 in α-synuclein-induced microglial activation. Acta Neuropathol Commun 2014, 2:156.
6. Buchanan M.M., Hutchinson M., Watkins L.R., Yin H. Toll-like receptor 4 in CNS pathologies. J.Neurochem. 2010, 114:13-27.
7. Burguillos M.A., Deierborg T., Kavanagh E., Persson A., Hajji N., Garcia-Quintanilla A., Cano J., Brundin P., Englund E., Venero J.L., Joseph B. Caspase signalling controls microglia activation and neurotoxicity. Nature 2011, 472:319-324.
8. Carlsson S., Oberg C.T., Carlsson M.C., Sundin A., Nilsson U.J., Smith D., Cummings R.D., Almkvist J., Karlsson A., Leffler H. Affinity of galectin-8 and its carbohydrate recognition domains for ligands in solution and at the cell surface. Glycobiology 2007, 17:663-676.
9. Caso J.R., Pradillo J.M., Hurtado O., Lorenzo P., Moro M.A., Lizasoain I. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 2007, 115:1599-1608.
10. Castaño A., Herrera A.J., Cano J., Machado A. The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh-TNF-alpha, IL-1beta and IFN-gamma. J.Neurochem. 2002, 81:150-157.
11. Chen G.Y., Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
12. Colnot C., Fowlis D., Ripoche M.-A., Bouchaert I., Poirier F. Embryonic implantation in galectin 1/galectin 3 double mutant mice. Dev. Dyn. 1998, 211:306-313.
13. Debierre-Grockiego F., Niehus S., Coddeville B., Elass E., Poirier F., Weingart R., Schmidt R.R., Mazurier J., Guérardel Y., Schwarz R.T. Binding of Toxoplasma gondii glycosylphosphatidylinositols to galectin-3 is required for their recognition by macrophages. J.Biol. Chem. 2010, 285:32744-32750.
14. Devillers A., Courjol F., Fradin C., Coste A., Poulain D., Pipy B., Bernardes E.S., Jouault T. Deficient beta-mannosylation of Candida albicans phospholipomannan affects the proinflammatory response in macrophages. PLoS ONE 2013, 8:e84771.
15. Doverhag C., Hedtjärn M., Poirier F., Mallard C., Hagberg H., Karlsson A., Sävman K. Galectin-3 contributes to neonatal hypoxic-ischemic brain injury. Neurobiol. Dis. 2010, 38:36-46.
16. Hennessy E.J., Parker A.E., O'Neill L.A. Targeting Toll-like receptors: emerging therapeutics?. Nat. Rev. Drug Discov. 2010, 9:293-307.
17. Herrera A.J., Castaño A., Venero J.L., Cano J., Machado A. The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiol. Dis. 2000, 7:429-447.
18. Hoyos H.C., Rinaldi M., Mendez-Huergo S.P., Marder M., Rabinovich G.A., Pasquini J.M., Pasquini L.A. Galectin-3 controls the response of microglial cells to limit cuprizone-induced demyelination. Neurobiol. Dis. 2014, 62:441-455.
19. Hyakkoku K., Hamanaka J., Tsuruma K., Shimazawa M., Tanaka H., Uematsu S., Akira S., Inagaki N., Nagai H., Hara H. Toll-like receptor 4 (TLR4), but not TLR3 or TLR9, knock-out mice have neuroprotective effects against focal cerebral ischemia. Neuroscience 2010, 171:258-267.
20. Inácio A.R., Ruscher K., Leng L., Bucala R., Deierborg T. Macrophage migration inhibitory factor promotes cell death and aggravates neurologic deficits after experimental stroke. J.Cereb. Blood Flow Metab. 2011, 31:1093-1106.
21. Jeon S.B., Yoon H.J., Chang C.Y., Koh H.S., Jeon S.H., Park E.J. Galectin-3 exerts cytokine-like regulatory actions through the JAK-STAT pathway. J.Immunol. 2010, 185:7037-7046.
22. Jiang H.R., Al Rasebi Z., Mensah-Brown E., Shahin A., Xu D., Goodyear C.S., Fukada S.Y., Liu F.T., Liew F.Y., Lukic M.L. Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J.Immunol. 2009, 182:1167-1173.
23. Jouault T., El Abed-El Behi M., Martínez-Esparza M., Breuilh L., Trinel P.A., Chamaillard M., Trottein F., Poulain D. Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J.Immunol. 2006, 177:4679-4687.
24. Jung S., Aliberti J., Graemmel P., Sunshine M.J., Kreutzberg G.W., Sher A., Littman D.R. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 2000, 20:4106-4114.
25. Kasai K., Hirabayashi J. Galectins: a family of animal lectins that decipher glycocodes. J.Biochem. 1996, 119:1-8.
26. Lalancette-Hébert M., Swarup V., Beaulieu J.M., Bohacek I., Abdelhamid E., Weng Y.C., Sato S., Kriz J. Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J.Neurosci. 2012, 32:10383-10395.
27. Lambertsen K.L., Biber K., Finsen B. Inflammatory cytokines in experimental and human stroke. J.Cereb. Blood Flow Metab. 2012, 32:1677-1698.
28. Leffler H., Carlsson S., Hedlund M., Qian Y., Poirier F. Introduction to galectins. Glycoconj. J. 2004, 19:433-440.
29. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
30. Lepur A., Salomonsson E., Nilsson U.J., Leffler H. Ligand induced galectin-3 protein self-association. J.Biol. Chem. 2012, 287:21751-21756.
31. Lerman B.J., Hoffman E.P., Sutherland M.L., Bouri K., Hsu D.K., Liu F.T., Rothstein J.D., Knoblach S.M. Deletion of galectin-3 exacerbates microglial activation and accelerates disease progression and demise in a SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Brain Behav 2012, 2:563-575.
32. Li Y., Komai-Koma M., Gilchrist D.S., Hsu D.K., Liu F.T., Springall T., Xu D. Galectin-3 is a negative regulator of lipopolysaccharide-mediated inflammation. J.Immunol. 2008, 181:2781-2789.
33. Lin H.M., Pestell R.G., Raz A., Kim H.R. Galectin-3 enhances cyclin D(1) promoter activity through SP1 and a cAMP-responsive element in human breast epithelial cells. Oncogene 2002, 21:8001-8010.
34. MacKinnon A.C., Farnworth S.L., Hodkinson P.S., Henderson N.C., Atkinson K.M., Leffler H., Nilsson U.J., Haslett C., Forbes S.J., Sethi T. Regulation of alternative macrophage activation by galectin-3. J.Immunol. 2008, 180:2650-2658.
35. Mey A., Leffler H., Hmama Z., Normier G., Revillard J.P. The animal lectin galectin-3 interacts with bacterial lipopolysaccharides via two independent sites. J.Immunol. 1996, 156:1572-1577.
36. Mizutani M., Pino P.A., Saederup N., Charo I.F., Ransohoff R.M., Cardona A.E. The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J.Immunol. 2012, 188:29-36.
37. Nakahara S., Oka N., Raz A. On the role of galectin-3 in cancer apoptosis. Apoptosis 2005, 10:267-275.
38. Olsson T., Wieloch T., Smith M.L. Brain damage in a mouse model of global cerebral ischemia. Effect of NMDA receptor blockade. Brain Res. 2003, 982:260-269.
39. Deierborg T., Wieloch T., Diano S., Warden C.H., Horvath T.L., Mattiasson G. Overexpression of UCP2 protects thalamic neurons following global ischemia in the mouse. J.Cereb. Blood Flow Metab. 2008, 28:1186-1195.
40. Saederup N., Cardona A.E., Croft K., Mizutani M., Cotleur A.C., Tsou C.L., Ransohoff R.M., Charo I.F. Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE 2010, 5:e13693.
41. Saijo K., Glass C.K. Microglial cell origin and phenotypes in health and disease. Nat. Rev. Immunol. 2011, 11:775-787.
42. Salomonsson E., Carlsson M.C., Osla V., Hendus-Altenburger R., Kahl-Knutson B., Oberg C.T., Sundin A., Nilsson R., Nordberg-Karlsson E., Nilsson U.J., et al. Mutational tuning of galectin-3 specificity and biological function. J.Biol. Chem. 2010, 285:35079-35091.
43. Salomonsson E., Larumbe A., Tejler J., Tullberg E., Rydberg H., Sundin A., Khabut A., Frejd T., Lobsanov Y.D., Rini J.M., et al. Monovalent interactions of galectin-1. Biochemistry 2010, 49:9518-9532.
44. Satoh K., Niwa M., Binh N.H., Nakashima M., Kobayashi K., Takamatsu M., Hara A. Increase of galectin-3 expression in microglia by hyperthermia in delayed neuronal death of hippocampal CA1 following transient forebrain ischemia. Neurosci. Lett. 2011, 504:199-203.
45. Satoh K., Niwa M., Goda W., Binh N.H., Nakashima M., Takamatsu M., Hara A. Galectin-3 expression in delayed neuronal death of hippocampal CA1 following transient forebrain ischemia, and its inhibition by hypothermia. Brain Res. 2011, 1382:266-274.
46. Seidel S.A., Dijkman P.M., Lea W.A., van den Bogaart G., Jerabek-Willemsen M., Lazic A., Joseph J.S., Srinivasan P., Baaske P., Simeonov A., et al. Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. Methods 2013, 59:301-315.
47. Shimura T., Takenaka Y., Tsutsumi S., Hogan V., Kikuchi A., Raz A. Galectin-3, a novel binding partner of beta-catenin. Cancer Res. 2004, 64:6363-6367.
48. Sörme P., Qian Y., Nyholm P.G., Leffler H., Nilsson U.J. Low micromolar inhibitors of galectin-3 based on 3'-derivatization of N-acetyllactosamine. ChemBioChem 2002, 3:183-189.
49. Starossom S.C., Mascanfroni I.D., Imitola J., Cao L., Raddassi K., Hernandez S.F., Bassil R., Croci D.O., Cerliani J.P., Delacour D., et al. Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 2012, 37:249-263.
50. Stowell S.R., Arthur C.M., Mehta P., Slanina K.A., Blixt O., Leffler H., Smith D.F., Cummings R.D. Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens. J.Biol. Chem. 2008, 283:10109-10123.
51. Suzuki Y., Hattori K., Hamanaka J., Murase T., Egashira Y., Mishiro K., Ishiguro M., Tsuruma K., Hirose Y., Tanaka H., et al. Pharmacological inhibition of TLR4-NOX4 signal protects against neuronal death in transient focal ischemia. Sci Rep 2012, 2:896.
52. Venero J.L., Burguillos M.A., Brundin P., Joseph B. The executioners sing a new song: killer caspases activate microglia. Cell Death Differ. 2011, 18:1679-1691.
53. Wesley U.V., Vemuganti R., Ayvaci E.R., Dempsey R.J. Galectin-3 enhances angiogenic and migratory potential of microglial cells via modulation of integrin linked kinase signaling. Brain Res. 2013, 1496:1-9.