Galectin-3 controls the response of microglial cells to limit cuprizone-induced demyelination

Neurobiology of Disease

Volumn 62, Issue , 2014, Pages 441-455

  Hoyos, H C ^a   Rinaldi, M ^a   Mendez Huergo, S P ^b,c   Marder, M ^a   Rabinovich, G A ^b,c   Pasquini, J M ^a   Pasquini, L A ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Cuprizone; Demyelination; Galectin 3; Microglial phenotype; Oligodendroglial differentiation; TREM 2b

Indexed keywords

CASPASE 3; CELL RECEPTOR; CUPRIZONE; ED1 PROTEIN; GALECTIN 3; MEMBRANE PROTEIN; TREM 2B PROTEIN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEMYELINATION; DISEASE PREDISPOSITION; ENZYME ACTIVATION; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MEMORY DISORDER; MICROGLIA; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WILD TYPE; WORKING MEMORY;

CUPRIZONE; DEMYELINATION; GALECTIN-3; MICROGLIAL PHENOTYPE; OLIGODENDROGLIAL DIFFERENTIATION; TREM-2B;

ANIMALS; ASTROCYTES; CORPUS CALLOSUM; CUPRIZONE; DEMYELINATING DISEASES; GALECTIN 3; LOCOMOTION; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NERVE FIBERS, MYELINATED; OLIGODENDROGLIA; PHAGOCYTOSIS;

EID: 84887590268     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.10.023     Document Type: Article

References (89)

1. Adams C.W., Poston R.N., Buk S.J. Pathology, histochemistry and immunocytochemistry of lesions in acute multiple sclerosis. J. Neurol. Sci. 1989, 92:291-306.
2. Arnett H.A., Mason J., Marino M., Suzuki K., Matsushima G.K., Ting J.P. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 2001, 4:1116-1122.
3. Bakker D.A., Ludwin S.K. Blood-brain barrier permeability during cuprizone-induced demyelination. Implications for the pathogenesis of immune-mediated demyelinating diseases. J. Neurol. Sci. 1987, 78:125-137.
4. Barnett M.H., Prineas J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 2004, 55:458-468.
5. Barnett M.H., Henderson A.P., Prineas J.W. The macrophage in MS: just a scavenger after all? Pathology and pathogenesis of the acute MS lesion. Mult. Scler. 2006, 12:121-132.
6. Blakemore W.F. Demyelination of the superior cerebellar peduncle in the mouse induced by cuprizone. J. Neurol. Sci. 1973, 20(1):63-72.
7. Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8:57-69.
8. Buschmann J.P., Berger K., Awad H., Clarner T., Beyer C., Kipp M. Inflammatory response and chemokine expression in the white matter corpus callosum and gray matter cortex region during cuprizone-induced demyelination. J. Mol. Neurosci. 2012, 48(1):66-76.
9. Chernoff G.F. Shiverer: an autosomal recessive mutant mouse with myelin deficiency. J. Hered. 1981, 72(2):128.
10. Comte I., Kim Y., Young C.C., van der Harg J.M., Hockberger P., Bolam P.J., Poirier F., Szele F.G. Galectin-3 maintains cell motility from the subventricular zone to the olfactory bulb. J. Cell Sci. 2011, 124(14):2438-2447.
11. Coughenour L.L., McLean J.R., Parker R.B. A new device for the rapid measurement of impaired motor function in mice. Pharmacol. Biochem. Behav. 1977, 6(3):351-353.
12. Dellu F., Contarino A., Simon H., Koob G.F., Gold L.H. Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiol. Learn. Mem. 2000, 73(1):31-48.
13. Demetriou M., Granovsky M., Quaggin S., Dennis J.W. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 2001, 409(6821):733-739.
14. Fernández S.P., Wasowski C., Loscalzo L.M., Granger R.E., Johnston G.A., Paladini A.C., Marder M. Central nervous system depressant action of flavonoid glycosides. Eur. J. Pharmacol. 2006, 539:168-176.
15. Ford A.L., Goodsall A.L., Hickey W.F., Sedgwick J.D. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J. Immunol. 1995, 154:4309-4321.
16. Franco-Pons N., Torrente M., Colomina M.T., Vilella E. Behavioral deficits in the cuprizone-induced murine model of demyelination/remyelination. Toxicol. Lett. 2007, 169(3):205-213. (30).
17. Franklin R.J. Why does remyelination fail in multiple sclerosis?. Nat. Rev. Neurosci. 2002, 3:705-714.
18. Gay F.W. Early cellular events in multiple sclerosis. Intimations of an extrinsic myelinolytic antigen. Clin. Neurol. Neurosurg. 2006, 108:234-240.
19. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
20. Gregg J.R., Herring N.R., Naydenov A.V., Hanlin R.P., Konradi C. Downregulation of oligodendrocyte transcripts is associated with impaired prefrontal cortex function in rats. Schizophr. Res. 2009, 113:277-287.
21. Gustavsson P., Linsmeier C.E., Leffler H., Kanje M. Galectin-3 inhibits Schwann cell proliferation in cultured sciatic nerve. Neuroreport 2007, 18:669-673.
22. Hakola H.P. Neuropsychiatric and genetic aspects of a new hereditary disease characterized by progressive dementia and lipomembranous polycystic osteodysplasia. Acta Psychiatr. Scand. Suppl. 1972, 232:1-173.
23. Hanisch U.K., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10:1387-1394.
24. Henderson A.P., Barnett M.H., Parratt J.D., Prineas J.W. Multiple sclerosis: distribution of inflammatory cells in newly forming lesions. Ann. Neurol. 2009, 66:739-753.
25. Hesse A., Wagner M., Held J., Bruck W., Salinas-Riester G., Hao Z., et al. In toxic demyelination oligodendroglial cell death occurs early and is FAS independent. Neurobiol. Dis. 2010, 37(2):362-369.
26. Hickey W.F. The pathology of multiple sclerosis: a historical perspective. J. Neuroimmunol. 1999, 98:37-44.
27. Hiremath M.M., Saito Y., Knapp G.W., Ting J.P., Suzuki K., Matsushima G.K. Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J. Neuroimmunol. 1998, 92(1-2):38-49.
28. Hsu D.K., Yang R.Y., Pan Z., Yu L., Salomon D.R., Fung-Leung W.P., et al. Targeted disruption of the Galectin-3 gene results in attenuated peritoneal inflammatory responses. Am. J. Pathol. 2000, 156(3):1073-1083.
29. Jiang H.R., Al Rasebi Z., Mensah-Brown E., Shahin A., Xu D., Goodyear C.S., et al. Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J. Immunol. 2009, 182:1167-1173.
30. Karpus W.J., Kennedy K.J. MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J. Leukoc. Biol. 1997, 62(5):681-687.
31. Kondo A., Nakano T., Suzuki K. Blood-brain barrier permeability to horseradish peroxidase in twitcher and cuprizone-intoxicated mice. Brain Res. 1987, 425:186-190.
32. Kotter M.R., Li W.W., Zhao C., Franklin R.J. Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J. Neurosci. 2006, 26:328-332.
33. Lalancette-Hébert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007, 27:2596-2605.
34. Lalancette-Hébert M., Swarup V., Beaulieu J.M., Bohacek I., Abdelhamid E., Weng Y.C., et al. Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J. Neurosci. 2012, 32(30):10383-10395.
35. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201(2):233-240.
36. Leffler H., Carlsson S., Hedlund M., Qian Y., Poirier F. Introduction to galectins. Glycoconj. J. 2004, 19(7-9):433-440.
37. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
38. Li Y., Komai-Koma M., Gilchrist D.S., Hsu D.K., Liu F.T., Springall T., et al. Galectin-3 is a negative regulator of lipopolysaccharide-mediated inflammation. J. Immunol. 2008, 181(4):2781-2789.
39. Lister R.G. The use of a plus maze to measure anxiety in the mouse. Psychopharmacology (Berl) 1987, 92:180-185.
40. Liu C., Li Y., Yu J., Feng L., Hou S., Liu Y., et al. Targeting the shift from M1 to M2 macrophages in experimental autoimmune encephalomyelitis mice treated with fasudil. PLoS One 2013, 8(2):e54841.
41. Ludwin S.K. Central nervous system demyelination and remyelination in the mouse: an ultrastructural study of cuprizone toxicity. Lab. Invest. 1978, 39:597-612.
42. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
43. Mason J.L., Suzuki K., Chaplin D.D., Matsushima G.K. Interleukin-1beta promotes repair of the CNS. J. Neurosci. 2001, 21:7046-7052.
44. Mason J.L., Langaman C., Morell P., Suzuki K., Matsushima G.K. Episodic demyelination and subsequent remyelination within the murine central nervous system: changes inaxonal calibre. Neuropathol. Appl. Neurobiol. 2001, 27(1):50-58.
45. Matsushima G.K., Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 2001, 11:107-116.
46. McMahon E.J., Suzuki K., Matsushima G.K. Peripheral macrophage recruitment in cuprizone-induced CNS demyelination despite an intact blood-brain barrier. J. Neuroimmunol. 2002, 130:32-45.
47. Miron V.E., Boyd A., Zhao J.W., Yuen T.J., Ruckh J.M., Shadrach J.L., et al. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 2013, 16(9):1211-1218.
48. Mok S.W., Thelen K.M., Riemer C., Bamme T., Gültner S., Lütjohann D., et al. Simvastatin prolongs survival times in prion infections of the central nervous system. Biochem. Biophys. Res. Commun. 2006, 348(2):697-702.
49. Mok S.W., Riemer C., Madela K., Hsu D.K., Liu F.T., Gültner S., et al. Role of galectin-3 in prion infections of the CNS. Biochem. Biophys. Res. Commun. 2007, 359(3):672-678.
50. Morell P., Barrett C.V., Mason J.L., Toews A.D., Hostettler J.D., Knapp G.W., et al. Gene expression in brain during cuprizone-induced demyelination and remyelination. Mol. Cell. Neurosci. 1998, 12(4-5):220-227.
51. Mosser D.M. Themany faces ofmacrophage activation. J. Leukoc. Biol. 2003, 73:209-212.
52. Mouse Brain Library A Human Brain Project, supported by the National Institue for Health (United States) and its institutes for Mental Health (NIMH), on Drug Abuse (NIDA) and on Alcohol Abuse and Alcoholism (NIAAA) 2003, www.mbl.org (on line version).
53. Nasu T., Tsukahara Y., Terayama K. A lipid metabolic disease-"membranous lipodystrophy"-an autopsy case demonstrating numerous peculiar membranestructures composed of compound lipid in bone and bone marrow and various adipose tissues. Acta Pathol. 1973, 23:539-558.
54. Nieminen J., St-Pierre C., Sato S. Galectin-3 interacts with naive and primed neutrophils, inducing innate immune responses. J. Leukoc. Biol. 2005, 78:1127-1135.
55. Olah M., Amor S., Brouwer N., Vinet J., Eggen B., Biber K., et al. Identification of a microglia phenotype supportive of remyelination. Glia 2012, 60(2):306-321.
56. Paloneva J., Autti T., Raininko R., Partanen J., Salonen O., Puranen M., et al. CNS manifestations of Nasu-Hakola disease: a frontal dementia with bone cysts. Neurology 2001, 56:1552-1558.
57. Paloneva J., Manninen T., Christman G., Hovanes K., Mandelin J., Adolfsson R., et al. Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am. J. Hum. Genet. 2002, 71:656-662.
58. Park J.B., Yiu G., Kaneko S., Wang J., Chang J., He X.L., et al. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005, 45(3):345-351.
59. Pasquini L.A., Calatayud C.A., Bertone Uña A.L., Millet V., Pasquini J.M., Soto E.F. The neurotoxic effect of cuprizone on oligodendrocytes depends on the presence of pro-inflammatory cytokines secreted by microglia. Neurochem. Res. 2007, 32(2):279-292.
60. Pasquini L.A., Millet V., Hoyos H.C., Giannoni J.P., Croci D.O., Marder M., et al. Galectin-3 drives oligodendrocyte differentiation to control myelin integrity and function. Cell Death Differ. 2011, 18:1746-1756.
61. Perry V.H., Gordon S. Macrophages and the nervous system. Int. Rev. Cytol. 1991, 125:203-244.
62. Pesheva P., Kuklinski S., Schmitz B., Probstmeier R. Galectin-3 promotes neural cell adhesion and neurite growth. J. Neurosci. Res. 1998, 54:639-654.
63. Piccio L., Buonsanti C., Mariani M., Cella M., Gilfillan S., Cross A.H., et al. Blockade of TREM-2 exacerbates experimental autoimmune encephalomyelitis. Eur. J. Immunol. 2007, 37:1290-1301.
64. Quinta H.R., Galigniana M.D. The neuroregenerative mechanism mediated by the Hsp90-binding immunophilin FKBP52 resembles the early steps of neuronal differentiation. Br. J. Pharmacol. 2012, 166:637-649.
65. Rabinovich G.A., Croci D.O. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012, 36:322-335.
66. Rabinovich G.A., Toscano M.A., Jackson S.S., Vasta G.R. Functions of cell surface galectin-glycoprotein lattices. Curr. Opin. Struct. Biol. 2007, 17:513-520.
67. Reichert F., Rotshenker S. Galectin-3/MAC-2 in experimental allergic encephalomyelitis. Exp. Neurol. 1999, 160(2):8-514.
68. Riemer C., Neidhold S., Burwinkel M., Schwarz A., Schultz J., Krätzschmar J., et al. Gene expression profiling of scrapie-infected brain tissue. Biochem. Biophys. Res. Commun. 2004, 323(2):556-564.
69. Rotshenker S. The role of Galectin-3/MAC-2 in the activation of the innate-immune function of phagocytosis in microglia in injury and disease. J. Mol. Neurosci. 2009, 39:99-103.
70. Rotshenker S., Reichert F., Gitik M., Haklai R., Elad-Sfadia G., Kloog Y. Galectin-3/MAC-2, Ras and PI3K activate complement receptor-3 and scavenger receptor-AI/II mediated myelin phagocytosis in microglia. Glia 2008, 56:1607-1613.
71. Sato S., Hughes R.C. Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem. 1994, 269(6):4424-4430.
72. Sato S., Nieminen J. Seeing strangers or announcing "danger": galectin-3 in two models of innate immunity. Glycoconj. J. 2004, 19:583-591.
73. Sato S., Burdett I., Hughes R.C. Secretion of the baby hamster kidney 30-kDa galactose-binding lectin from polarized and nonpolarized cells: a pathway independent of the endoplasmic reticulum-Golgi complex. Exp. Cell Res. 1993, 207(1):8-18.
74. Sato S., Ouellet N., Pelletier I., Simard M., Rancourt A., Bergeron M.G. Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J. Immunol. 2002, 168:1813-1822.
75. Sedgwick J.D., Schwender S., Imrich H., Dorries R., Butcher G.W., ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:7438-7442.
76. Smith G.S., Samborska B., Hawley S.P., Klaiman J.M., Gillis T.E., Jones N., et al. Nucleus-localized 21.5-kDa myelin basic protein promotes oligodendrocyte proliferation and enhances neurite outgrowth in coculture, unlike the plasma membrane-associated 18.5-kDa isoform. J. Neurosci. Res. 2013, 91:349-362.
77. Starossom S.C., Mascanfroni I.D., Imitola J., Cao L., Raddassi K., Hernandez S.F., et al. Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 2012, 37:249-263.
78. Suzuki K., Kikkawa Y. Status spongiosus of CNS and hepatic changes induced by cuprizone (biscyclohexanone oxalyldihydrazone). Am. J. Pathol. 1969, 54:307-325.
79. Takahashi K., Prinz M., Stagi M., Chechneva O., Neumann H. TREM2- transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. PLoS Med. 2007, 4:e124.
80. Voß E.V., Škuljec J., Gudi V., Skripuletz T., Pul R., Trebst C., et al. Characterisation of microglia during de- and remyelination: can they create a repair promoting environment?. Neurobiol. Dis. 2011, 45(1):519-528.
81. Weiner H.L. A shift from adaptive to innate immunity: a potential mechanism of disease progression in multiple sclerosis. J. Neurol. 2008, 255(1):3-11.
82. Wu L., Zhao Q., Zhu X., Peng M., Jia C., Wu W., et al. A novel function of microRNA let-7d in regulation of galectin-3 expression in attention deficit hyperactivity disorder rat brain. Brain Pathol. 2010, 20:1042-1054.
83. Xu H., Yang H.J., Zhang Y., Clough R., Browning R., Li X.M. Behavioral and neurobiological changes in C57BL/6 mice exposed to cuprizone. Behav. Neurosci. 2009, 123(2):418-429.
84. Xu H., Yang H.J., McConomy B., Browning R., Li X.M. Behavioral and neurobiological changes in C57BL/6 mouse exposed to cuprizone: effects of antipsychotics. Front. Behav. Neurosci. 2010, 4:8.
85. Xu H., Yang H.J., Rose G.M., Li X.M. Recovery of behavioral changes and compromised white matter in C57BL/6 mice exposed to cuprizone: effects of antipsychotic drugs. Front. Behav. Neurosci. 2011, 5:31.
86. Yagi T., Matsuda J., Takikita S., Mohri I., Suzuki K., Suzuki K. Comparative clinico-pathological study of saposin-A-deficient (SAP-A-/-) and Twitcher mice. J. Neuropathol. Exp. Neurol. 2004, 63(7):721-734.
87. Yang L.J., Zeller C.B., Shaper N.L., Kiso M., Hasegawa A., Shapiro R.E., et al. Gangliosides are neuronal ligands for myelin-associated glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(2):814-818.
88. Yang Z., Tsai M.S., Wu J.H., Herp A., Wu A.M. Defining the carbohydrate specificities of Erythrina corallodendron lectin (ECorL) as polyvalent Galbeta1-4GlcNAc (II)>monomeric II>monomeric Gal and GalNAc. Chang Gung Med. J. 2008, 31(1):26-43.
89. Zhang Y., Xu H., Jiang W., Xiao L., Yan B., He J., Wang Y., et al. Quetiapine alleviates the cuprizone-induced white matter pathology in the brain of C57BL/6 mouse. Schizophr. Res. 2008, 106:182-191.