Astrocyte galectin-9 potentiates microglial TNF secretion

Journal of Neuroinflammation

Volumn 11, Issue 1, 2014, Pages

  Steelman, Andrew J ^a   Li, Jianrong ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Astrocytes; Galectin 9; Microglia activation; Neuroinflammation; Poly(I:C); TNF

Indexed keywords

CELL PROTEIN; ECALECTIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN TIM 3; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; CELL SURFACE RECEPTOR; CYTOKINE; GALECTIN; GALECTIN 9, MOUSE; GLIAL FIBRILLARY ACIDIC PROTEIN; LGALS9 PROTEIN, MOUSE; POLY D(I-C); POLYDEOXYRIBONUCLEOTIDE; RECOMBINANT PROTEIN; TIM-3 PROTEIN, RAT; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL COMMUNICATION; CELLULAR DISTRIBUTION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MICROGLIA; NERVE CELL CULTURE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NULL ALLELE; OLIGODENDROGLIA; POLYMERASE CHAIN REACTION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; ANIMAL; CELL CULTURE; DEFICIENCY; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; NEWBORN; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; GALECTINS; GLIAL FIBRILLARY ACIDIC PROTEIN; MICE; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MICROGLIA; POLYDEOXYRIBONUCLEOTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; TIME FACTORS; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84908174624     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-014-0144-0     Document Type: Article

References (63)

1. Bsibsi M, Ravid R, Gveric D, van Noort JM. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 2002, 61:1013-1021. 12430718.
2. Furr SR, Chauhan VS, Sterka D, Grdzelishvili V, Marriott I. Characterization of retinoic acid-inducible gene-I expression in primary murine glia following exposure to vesicular stomatitis virus. J Neurovirol 2008, 14:503-513. 10.1080/13550280802337217, 18991139.
3. De Miranda J, Yaddanapudi K, Hornig M, Lipkin WI. Astrocytes recognize intracellular polyinosinic-polycytidylic acid via MDA-5. FASEB J 2009, 23:1064-1071. 10.1096/fj.08-121434, 19036857.
4. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol 2007, 28:138-145. 10.1016/j.it.2007.01.005, 17276138.
5. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 2005, 175:4320-4330. 10.4049/jimmunol.175.7.4320, 16177072.
6. Engelhardt B, Ransohoff RM. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 2005, 26:485-495. 10.1016/j.it.2005.07.004, 16039904.
7. Ransohoff RM, Cardona AE. The myeloid cells of the central nervous system parenchyma. Nature 2010, 468:253-262. 10.1038/nature09615, 21068834.
8. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009, 29:13435-13444. 10.1523/JNEUROSCI.3257-09.2009, 19864556.
9. Miron VE, Boyd A, Zhao JW, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A, Franklin RJ, ffrench-Constant C. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 2013, 16:1211-1218. 10.1038/nn.3469, 23872599.
10. Williams A, Piaton G, Lubetzki C. Astrocytes - friends or foes in multiple sclerosis?. Glia 2007, 55:1300-1312. 10.1002/glia.20546, 17626262.
11. Taylor RA, Sansing LH. Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin Dev Immunol 2013, 2013:746068. 10.1155/2013/746068, 24223607.
12. Vezzani A, Aronica E, Mazarati A, Pittman QJ. Epilepsy and brain inflammation. Exp Neurol 2013, 244:11-21. 10.1016/j.expneurol.2011.09.033, 21985866.
13. Aronica E, Crino PB. Inflammation in epilepsy: clinical observations. Epilepsia 2011, 52(Suppl 3):26-32. 10.1111/j.1528-1167.2011.03033.x, 21542843.
14. Aronica E, Ravizza T, Zurolo E, Vezzani A. Astrocyte immune responses in epilepsy. Glia 2012, 60:1258-1268. 10.1002/glia.22312, 22331574.
15. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934. 10.1016/j.cell.2010.02.016, 20303880.
16. McCusker RH, Kelley KW. Immune-neural connections: how the immune system's response to infectious agents influences behavior. J Exp Biol 2013, 216:84-98. 10.1242/jeb.073411, 23225871.
17. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008, 9:46-56. 10.1038/nrn2297, 18073775.
18. Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 2009, 27:119-145. 10.1146/annurev.immunol.021908.132528, 19302036.
19. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hovelmeyer N, Waisman A, Rulicke T, Prinz M, Priller J, Becher B, Aguzzi A. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 2005, 11:146-152. 10.1038/nm1177, 15665833.
20. Goldmann T, Wieghofer P, Muller PF, Wolf Y, Varol D, Yona S, Brendecke SM, Kierdorf K, Staszewski O, Datta M, Luedde T, Heikenwalder M, Jung S, Prinz M. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 2013, 16:1618-1626. 10.1038/nn.3531, 24077561.
21. Cusick MF, Libbey JE, Patel DC, Doty DJ, Fujinami RS. Infiltrating macrophages are key to the development of seizures following virus infection. J Virol 2013, 87:1849-1860. 10.1128/JVI.02747-12, 23236075.
22. Howe CL, Lafrance-Corey RG, Sundsbak RS, Sauer BM, Lafrance SJ, Buenz EJ, Schmalstieg WF. Hippocampal protection in mice with an attenuated inflammatory monocyte response to acute CNS picornavirus infection. Sci Rep 2012, 2:545. 10.1038/srep00545, 22848791.
23. Kirkman NJ, Libbey JE, Wilcox KS, White HS, Fujinami RS. Innate but not adaptive immune responses contribute to behavioral seizures following viral infection. Epilepsia 2010, 51:454-464. 10.1111/j.1528-1167.2009.02390.x, 19845729.
24. Libbey JE, Kennett NJ, Wilcox KS, White HS, Fujinami RS. Interleukin-6, produced by resident cells of the central nervous system and infiltrating cells, contributes to the development of seizures following viral infection. J Virol 2011, 85:6913-6922. 10.1128/JVI.00458-11, 21543484.
25. Libbey JE, Kirkman NJ, Smith MC, Tanaka T, Wilcox KS, White HS, Fujinami RS. Seizures following picornavirus infection. Epilepsia 2008, 49:1066-1074. 10.1111/j.1528-1167.2008.01535.x, 18325012.
26. Fu X, Zunich SM, O'Connor JC, Kavelaars A, Dantzer R, Kelley KW. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2,3 dioxygenase in murine organotypic hippocampal slice cultures. J Neuroinflammation 2010, 7:43. 10.1186/1742-2094-7-43, 20678226.
27. Lawson MA, Parrott JM, McCusker RH, Dantzer R, Kelley KW, O'Connor JC. Intracerebroventricular administration of lipopolysaccharide induces indoleamine-2,3-dioxygenase-dependent depression-like behaviors. J Neuroinflammation 2013, 10:87. 10.1186/1742-2094-10-87, 23866724.
28. Park SE, Lawson M, Dantzer R, Kelley KW, McCusker RH. Insulin-like growth factor-I peptides act centrally to decrease depression-like behavior of mice treated intraperitoneally with lipopolysaccharide. J Neuroinflammation 2011, 8:179. 10.1186/1742-2094-8-179, 22189158.
29. Liu FT, Rabinovich GA. Galectins: regulators of acute and chronic inflammation. Ann N Y Acad Sci 2010, 1183:158-182. 10.1111/j.1749-6632.2009.05131.x, 20146714.
30. Rabinovich GA, Toscano MA. Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 2009, 9:338-352. 10.1038/nri2536, 19365409.
31. Sato S, St-Pierre C, Bhaumik P, Nieminen J. Galectins in innate immunity: dual functions of host soluble beta-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol Rev 2009, 230:172-187. 10.1111/j.1600-065X.2009.00790.x, 19594636.
32. Vasta GR. Roles of galectins in infection. Nat Rev Microbiol 2009, 7:424-438. 10.1038/nrmicro2146, 19444247.
33. Dai SY, Nakagawa R, Itoh A, Murakami H, Kashio Y, Abe H, Katoh S, Kontani K, Kihara M, Zhang SL, Hata T, Nakamura T, Yamauchi A, Hirashima M. Galectin-9 induces maturation of human monocyte-derived dendritic cells. J Immunol 2005, 175:2974-2981. 10.4049/jimmunol.175.5.2974, 16116184.
34. Anderson AC, Anderson DE, Bregoli L, Hastings WD, Kassam N, Lei C, Chandwaskar R, Karman J, Su EW, Hirashima M, Bruce JN, Kane LP, Kuchroo VK, Hafler DA. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 2007, 318:1141-1143. 10.1126/science.1148536, 18006747.
35. Wada J, Kanwar YS. Identification and characterization of galectin-9, a novel beta-galactoside-binding mammalian lectin. J Biol Chem 1997, 272:6078-6086. 10.1074/jbc.272.9.6078, 9038233.
36. Steelman AJ, Smith R, Welsh CJ, Li J. Galectin-9 is up-regulated in Astrocytes by tumor necrosis factor and promotes encephalitogenic T-cell Apoptosis. J Biol Chem 2013, 288:23776-23787. 10.1074/jbc.M113.451658, 23836896.
37. Bellac CL, Coimbra RS, Simon F, Imboden H, Leib SL. Gene and protein expression of galectin-3 and galectin-9 in experimental pneumococcal meningitis. Neurobiol Dis 2007, 28:175-183. 10.1016/j.nbd.2007.07.005, 17706429.
38. Reddy PB, Sehrawat S, Suryawanshi A, Rajasagi NK, Mulik S, Hirashima M, Rouse BT. Influence of galectin-9/Tim-3 interaction on herpes simplex virus-1 latency. J Immunol 2011, 187:5745-5755. 10.4049/jimmunol.1102105, 22021615.
39. Gupta N, Rao PV. Transcriptomic profile of host response in Japanese encephalitis virus infection. Virol J 2011, 8:92. 10.1186/1743-422X-8-92, 21371334.
40. Stancic M, van Horssen J, Thijssen VL, Gabius HJ, van der Valk P, Hoekstra D, Baron W. Increased expression of distinct galectins in multiple sclerosis lesions. Neuropathol Appl Neurobiol 2011, 37:654-671. 10.1111/j.1365-2990.2011.01184.x, 21501208.
41. Kim S, Steelman AJ, Koito H, Li J. Astrocytes promote TNF-mediated toxicity to oligodendrocyte precursors. J Neurochem 2011, 116:53-66. 10.1111/j.1471-4159.2010.07084.x, 21044081.
42. Li J, Ramenaden ER, Peng J, Koito H, Volpe JJ, Rosenberg PA. Tumor necrosis factor alpha mediates lipopolysaccharide-induced microglial toxicity to developing oligodendrocytes when astrocytes are present. J Neurosci 2008, 28:5321-5330. 10.1523/JNEUROSCI.3995-07.2008, 18480288.
43. Steelman AJ, Li J. Poly(I:C) promotes TNFalpha/TNFR1-dependent oligodendrocyte death in mixed glial cultures. J Neuroinflammation 2011, 8:89. 10.1186/1742-2094-8-89, 21812954.
44. Steelman AJ, Thompson JP, Li J. Demyelination and remyelination in anatomically distinct regions of the corpus callosum following cuprizone intoxication. Neurosci Res 2012, 72:32-42. 10.1016/j.neures.2011.10.002, 22015947.
45. Yoshida H, Imaizumi T, Kumagai M, Kimura K, Satoh C, Hanada N, Fujimoto K, Nishi N, Tanji K, Matsumiya T, Mori F, Cui XF, Tamo W, Shibata T, Takanashi S, Okumura K, Nakamura T, Wakabayashi K, Hirashima M, Sato Y, Satoh K. Interleukin-1beta stimulates galectin-9 expression in human astrocytes. Neuroreport 2001, 12:3755-3758. 10.1097/00001756-200112040-00030, 11726788.
46. Shim JA, Park S, Lee ES, Niki T, Hirashima M, Sohn S. Galectin-9 ameliorates herpes simplex virus-induced inflammation through apoptosis. Immunobiology 2012, 217:657-666. 10.1016/j.imbio.2011.11.002, 22204815.
47. Alam S, Li H, Margariti A, Martin D, Zampetaki A, Habi O, Cockerill G, Hu Y, Xu Q, Zeng L. Galectin-9 protein expression in endothelial cells is positively regulated by histone deacetylase 3. J Biol Chem 2011, 286:44211-44217. 10.1074/jbc.M111.242289, 22027828.
48. Imaizumi T, Yoshida H, Nishi N, Sashinami H, Nakamura T, Hirashima M, Ohyama C, Itoh K, Satoh K. Double-stranded RNA induces galectin-9 in vascular endothelial cells: involvement of TLR3, PI3K, and IRF3 pathway. Glycobiology 2007, 17:12C-15C. 10.1093/glycob/cwm045, 17449641.
49. Ishikawa A, Imaizumi T, Yoshida H, Nishi N, Nakamura T, Hirashima M, Satoh K. Double-stranded RNA enhances the expression of galectin-9 in vascular endothelial cells. Immunol Cell Biol 2004, 82:410-414. 10.1111/j.0818-9641.2004.01248.x, 15283851.
50. Gieseke F, Kruchen A, Tzaribachev N, Bentzien F, Dominici M, Muller I. Proinflammatory stimuli induce galectin-9 in human mesenchymal stromal cells to suppress T-cell proliferation. Eur J Immunol 2013, 43:2741-2749. 10.1002/eji.201343335, 23817958.
51. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA, Volpe JJ, Vartanian T. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 2002, 22:2478-2486. 11923412.
52. Holm TH, Draeby D, Owens T. Microglia are required for astroglial Toll-like receptor 4 response and for optimal TLR2 and TLR3 response. Glia 2012, 60:630-638. 10.1002/glia.22296, 22271465.
53. Yamauchi A, Dai SY, Nakagawa R, Kashio Y, Abe H, Katoh S, Kontani K, Hirashima M. Galectin-9 induces maturation of human monocyte-derived dendritic cells. Nihon Rinsho Meneki Gakkai Kaishi 2005, 28:381-388. 10.2177/jsci.28.381, 16394641.
54. Jayaraman P, Sada-Ovalle I, Nishimura T, Anderson AC, Kuchroo VK, Remold HG, Behar SM. IL-1beta promotes antimicrobial immunity in macrophages by regulating TNFR signaling and caspase-3 activation. J Immunol 2013, 190:4196-4204. 10.4049/jimmunol.1202688, 23487424.
55. Jayaraman P, Sada-Ovalle I, Beladi S, Anderson AC, Dardalhon V, Hotta C, Kuchroo VK, Behar SM. Tim3 binding to galectin-9 stimulates antimicrobial immunity. J Exp Med 2010, 207:2343-2354. 10.1084/jem.20100687, 20937702.
56. Ma CJ, Li GY, Cheng YQ, Wang JM, Ying RS, Shi L, Wu XY, Niki T, Hirashima M, Li CF, Moorman JP, Yao ZQ. Cis association of galectin-9 with Tim-3 differentially regulates IL-12/IL-23 expressions in monocytes via TLR signaling. PLoS ONE 2013, 8:e72488. 10.1371/journal.pone.0072488, 23967307.
57. Wang JM, Shi L, Ma CJ, Ji XJ, Ying RS, Wu XY, Wang KS, Li G, Moorman JP, Yao ZQ. Differential regulation of interleukin-12 (IL-12)/IL-23 by Tim-3 drives T(H)17 cell development during hepatitis C virus infection. J Virol 2013, 87:4372-4383. 10.1128/JVI.03376-12, 23388728.
58. Lee SY, Goverman JM. The influence of T cell Ig mucin-3 signaling on central nervous system autoimmune disease is determined by the effector function of the pathogenic T cells. J Immunol 2013, 190:4991-4999. 10.4049/jimmunol.1300083, 23562810.
59. Sabatos CA, Chakravarti S, Cha E, Schubart A, Sanchez-Fueyo A, Zheng XX, Coyle AJ, Strom TB, Freeman GJ, Kuchroo VK. Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat Immunol 2003, 4:1102-1110. 10.1038/ni988, 14556006.
60. Vaitaitis GM, Wagner DH. Galectin-9 controls CD40 signaling through a Tim-3 independent mechanism and redirects the cytokine profile of pathogenic T cells in autoimmunity. PLoS ONE 2012, 7:e38708. 10.1371/journal.pone.0038708, 22685601.
61. Clayton KL, Haaland MS, Douglas-Vail MB, Mujib S, Chew GM, Ndhlovu LC, Ostrowski MA. T cell Ig and mucin domain-containing protein 3 is recruited to the immune synapse, disrupts stable synapse formation, and associates with receptor phosphatases. J Immunol 2014, 192:782-791. 10.4049/jimmunol.1302663, 24337741.
62. Bi S, Hong PW, Lee B, Baum LG. Galectin-9 binding to cell surface protein disulfide isomerase regulates the redox environment to enhance T-cell migration and HIV entry. Proc Natl Acad Sci U S A 2011, 108:10650-10655. 10.1073/pnas.1017954108, 21670307.
63. Grigorian A, Demetriou M. Manipulating cell surface glycoproteins by targeting N-glycan-galectin interactions. Methods Enzymol 2010, 480:245-266. 10.1016/S0076-6879(10)80012-6, 20816213.