Glycobiology of the Nervous System pp 517-542

Part of the Advances in Neurobiology book series (NEUROBIOL, volume 9) | Cite as

Galectins and Neuroinflammation

  • Hung-Lin Chen
  • Fang Liao
  • Teng-Nan Lin
  • Fu-Tong Liu
Chapter

Abstract

Galectins, β-galactoside-binding lectins, play multiple roles in the regulation of immune and inflammatory responses. The major galectins expressed in the CNS are galectins 1, 3, 4, 8, and 9. Under normal physiological conditions, galectins maintain CNS homeostasis by participating in neuronal myelination, neuronal stem cell proliferation, and apical vesicle transport in neuronal cells. In neuronal diseases and different experimental neuroinflammatory disease models, galectins may serve as extracellular mediators or intracellular regulators in controlling the inflammatory response or conferring the remodeling capacity in damaged CNS tissues. In general, galectins 1 and 9 attenuate experimental autoimmune encephalomyelitis (a model of multiple sclerosis), while galectin-3 promotes inflammation in this model. In brain ischemic lesions, both galectins 1 and 3 are induced to help neuronal regeneration. The expression of galectin-1 is required for astrocyte-derived neurotrophic factor secretion, and recombinant galectin-1 promotes neuronal regeneration. Galectin-3 promotes microglial cell proliferation and attenuates ischemic damage and neuronal apoptosis after cerebral ischemia. In amyotrophic lateral sclerosis models, galectin-3 is deleterious to neuroregeneration, while intramuscular administration of oxidized galectin-1 can improve neuromuscular disorders. In axotomy and Wallerian degeneration, galectin-3 helps phagocytosis of macrophages to clear degenerate myelin in the injured PNS or CNS. Thus, galectins are important modulators participating in homeostasis of the CNS and neuroinflammation. Continued investigations of the roles of galectins in neuroinflammation promise to provide a better understanding of the mechanism of this process and lead to new therapeutic approaches.

Keywords

Amyotrophic lateral sclerosis Experimental autoimmune encephalomyelitis Galectin Multiple sclerosis Wallerian degeneration 

Abbreviations

CNS

Central nervous system

BBB

Blood–brain barrier

PAMPs

Pathogen-associated molecular patterns

PRRs

Pattern recognition receptors

TCR

T-cell receptor

MHC

Major histocompatibility complex

APC

Antigen-presenting cells

Th

T helper cell

TFH

Follicular helper T cell

Treg

Regulatory T cells

IFN-γ

Interferon-gamma

EAE

Experimental autoimmune encephalitis

MS

Multiple sclerosis

TLRs

Toll-like receptors

RLRs

Retinoic acid-inducible gene I-like receptors

NLR

Nucleotide-binding oligomerization domain-like receptor

BCR

B-cell receptor

TNF-α

Tumor necrosis factor-alpha

CCL20

CC chemokine ligand 20

ROS

Reactive oxygen species

AA

Arachidonic acid

5-LO

5-Lipoxygenase

CRDs

Carbohydrate-recognition domains

OLG

Oligodendrocyte

NSCs

Neural stem cells

MBP

Myelin basic protein

IL-1β

Interleukin-1β

References

  1. Andersson, U., and Tracey, K.J. (2012a). Neural reflexes in inflammation and immunity. The Journal of experimental medicine 209, 1057–1068.PubMedCentralPubMedCrossRefGoogle Scholar
  2. Andersson, U., and Tracey, K.J. (2012b). Reflex principles of immunological homeostasis. Annual review of immunology 30, 313–335.PubMedCrossRefGoogle Scholar
  3. Arima, Y., Harada, M., Kamimura, D., Park, J.H., Kawano, F., Yull, F.E., Kawamoto, T., Iwakura, Y., Betz, U.A., Marquez, G., et al. (2012). Regional neural activation defines a gateway for autoreactive T cells to cross the blood-brain barrier. Cell 148, 447–457.PubMedCrossRefGoogle Scholar
  4. Bazan, N.G., Halabi, A., Ertel, M., and Petasis, N.A. (2012). Chapter 34 - Neuroinflammation. In Basic Neurochemistry (Eighth Edition), T.B. Scott, J.S. George, R.W. Albers, G.J.S.R.W.A. Donald L. PriceA2 - Scott T. Brady, and L.P. Donald, eds. (New York, Academic Press), pp. 610–620.Google Scholar
  5. Beutler, B., Eidenschenk, C., Crozat, K., Imler, J.L., Takeuchi, O., Hoffmann, J.A., and Akira, S. (2007). Genetic analysis of resistance to viral infection. Nature reviews Immunology 7, 753–766.PubMedCrossRefGoogle Scholar
  6. Bianchi, M.E. (2007). DAMPs, PAMPs and alarmins: all we need to know about danger. Journal of leukocyte biology 81, 1–5.PubMedCrossRefGoogle Scholar
  7. Bischoff, V., Deogracias, R., Poirier, F., and Barde, Y.-A. (2012). Seizure-induced neuronal death is suppressed in the absence of the endogenous lectin Galectin-1. J Neurosci 32, 15590–15600.PubMedCrossRefGoogle Scholar
  8. Blaser, C., Kaufmann, M., Müller, C., Zimmermann, C., Wells, V., Mallucci, L., and Pircher, H. (1998). Beta-galactoside-binding protein secreted by activated T cells inhibits antigen-induced proliferation of T cells. Eur J Immunol 28, 2311–2319.PubMedCrossRefGoogle Scholar
  9. Bolitho, P., Voskoboinik, I., Trapani, J.A., and Smyth, M.J. (2007). Apoptosis induced by the lymphocyte effector molecule perforin. Current opinion in immunology 19, 339–347.PubMedCrossRefGoogle Scholar
  10. Carson, M.J. (2012). Chapter 33 - Molecular Mechanisms and Consequences of Immune and Nervous System Interactions. In Basic Neurochemistry (Eighth Edition), T.B. Scott, J.S. George, R.W. Albers, G.J.S.R.W.A. Donald L. PriceA2 - Scott T. Brady, and L.P. Donald, eds. (New York, Academic Press), pp. 597–609.Google Scholar
  11. Chang-Hong, R., Wada, M., Koyama, S., Kimura, H., Arawaka, S., Kawanami, T., Kurita, K., Kadoya, T., Aoki, M., Itoyama, Y., et al. (2005). Neuroprotective effect of oxidized galectin-1 in a transgenic mouse model of amyotrophic lateral sclerosis. Exp Neurol 194, 203–211.PubMedCrossRefGoogle Scholar
  12. Colnot, C., Ripoche, M.A., Scaerou, F., Foulis, D., and Poirier, F. (1996). Galectins in mouse embryogenesis. Biochem Soc Trans 24, 141–146.PubMedGoogle Scholar
  13. Comte, I., Kim, Y., Young, C.C., van der Harg, J.M., Hockberger, P., Bolam, P.J., Poirier, F., and Szele, F.G. (2011). Galectin-3 maintains cell motility from the subventricular zone to the olfactory bulb. J Cell Sci 124, 2438–2447.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cooper, D.N.W. (2002). Galectinomics: finding themes in complexity. Biochim Biophys Acta 1572, 209–231.PubMedCrossRefGoogle Scholar
  15. Cua, D.J., Sherlock, J., Chen, Y., Murphy, C.A., Joyce, B., Seymour, B., Lucian, L., To, W., Kwan, S., Churakova, T., et al. (2003). Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744–748.PubMedCrossRefGoogle Scholar
  16. Cummings, R.D., and Liu, F.T. (2009). Galectins. In Essentials of Glycobiology, A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etzler, eds. (Cold Spring Harbor NY, The Consortium of Glycobiology Editors, La Jolla, California).Google Scholar
  17. Dagher, S.F., Wang, J.L., and Patterson, R.J. (1995). Identification of galectin-3 as a factor in pre-mRNA splicing. Proc Natl Acad Sci U S A 92, 1213–1217.PubMedCentralPubMedCrossRefGoogle Scholar
  18. Dubin, P.J., and Kolls, J.K. (2008). Th17 cytokines and mucosal immunity. Immunological reviews 226, 160–171.PubMedCrossRefGoogle Scholar
  19. Farina, C., Aloisi, F., and Meinl, E. (2007). Astrocytes are active players in cerebral innate immunity. Trends in immunology 28, 138–145.PubMedCrossRefGoogle Scholar
  20. Fazilleau, N., Mark, L., McHeyzer-Williams, L.J., and McHeyzer-Williams, M.G. (2009). Follicular helper T cells: lineage and location. Immunity 30, 324–335.PubMedCentralPubMedCrossRefGoogle Scholar
  21. Gaudin, J.C., Arar, C., Monsigny, M., and Legrand, A. (1997). Modulation of the expression of the rabbit galectin-3 gene by p53 and c-Ha-ras proteins and PMA. Glycobiology 7, 1089–1098.PubMedCrossRefGoogle Scholar
  22. Gendronneau, G., Sidhu, S.S., Delacour, D., Dang, T., Calonne, C., Houzelstein, D., Magnaldo, T., and Poirier, F. (2008). Galectin-7 in the control of epidermal homeostasis after injury. Mol Biol Cell 19, 5541–5549.PubMedCentralPubMedCrossRefGoogle Scholar
  23. Hadari, Y.R., Paz, K., Dekel, R., Mestrovic, T., Accili, D., and Zick, Y. (1995). Galectin-8. A new rat lectin, related to galectin-4. J Biol Chem 270, 3447–3453.PubMedCrossRefGoogle Scholar
  24. Hawkins, B.T., and Davis, T.P. (2005). The blood-brain barrier/neurovascular unit in health and disease. Pharmacological reviews 57, 173–185.PubMedCrossRefGoogle Scholar
  25. Heilmann, S., Hummel, T., Margolis, F.L., Kasper, M., and Witt, M. (2000). Immunohistochemical distribution of galectin-1, galectin-3, and olfactory marker protein in human olfactory epithelium. Histochem Cell Biol 113, 241–245.PubMedCrossRefGoogle Scholar
  26. Heneka, M.T., Kummer, M.P., Stutz, A., Delekate, A., Schwartz, S., Vieira-Saecker, A., Griep, A., Axt, D., Remus, A., Tzeng, T.C., et al. (2013). NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature 493, 674–678.Google Scholar
  27. Heusel, J.W., Wesselschmidt, R.L., Shresta, S., Russell, J.H., and Ley, T.J. (1994). Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76, 977–987.PubMedCrossRefGoogle Scholar
  28. Horie, H., Inagaki, Y., Sohma, Y., Nozawa, R., Okawa, K., Hasegawa, M., Muramatsu, N., Kawano, H., Horie, M., Koyama, H., et al. (1999). Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. J Neurosci 19, 9964–9974.PubMedGoogle Scholar
  29. Horie, H., and Kadoya, T. (2000). Identification of oxidized galectin-1 as an initial repair regulatory factor after axotomy in peripheral nerves. Neurosci Res 38, 131–137.PubMedCrossRefGoogle Scholar
  30. Iadecola, C., and Anrather, J. (2011). The immunology of stroke: from mechanisms to translation. Nat Med 17, 796–808.PubMedCentralPubMedCrossRefGoogle Scholar
  31. Imaizumi, Y., Sakaguchi, M., Morishita, T., Ito, M., Poirier, F., Sawamoto, K., and Okano, H. (2011). Galectin-1 is expressed in early-type neural progenitor cells and down-regulates neurogenesis in the adult hippocampus. Mol Brain 4, 7.PubMedCentralPubMedCrossRefGoogle Scholar
  32. Imbe, H., Okamoto, K., Kadoya, T., Horie, H., and Senba, E. (2003). Galectin-1 is involved in the potentiation of neuropathic pain in the dorsal horn. Brain Res 993, 72–83.PubMedCrossRefGoogle Scholar
  33. Ishibashi, S., Kuroiwa, T., Sakaguchi, M., Sun, L., Kadoya, T., Okano, H., and Mizusawa, H. (2007). Galectin-1 regulates neurogenesis in the subventricular zone and promotes functional recovery after stroke. Exp Neurol 207, 302–313.PubMedCrossRefGoogle Scholar
  34. Jack, C.S., Arbour, N., Manusow, J., Montgrain, V., Blain, M., McCrea, E., Shapiro, A., and Antel, J.P. (2005). TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175, 4320–4330.PubMedCrossRefGoogle Scholar
  35. Jha, S., Srivastava, S.Y., Brickey, W.J., Iocca, H., Toews, A., Morrison, J.P., Chen, V.S., Gris, D., Matsushima, G.K., and Ting, J.P. (2010). The inflammasome sensor, NLRP3, regulates CNS inflammation and demyelination via caspase-1 and interleukin-18. The Journal of neuroscience : the official journal of the Society for Neuroscience 30, 15811–15820.CrossRefGoogle Scholar
  36. 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., and Lukic, M.L. (2009). Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J Immunol 182, 1167–1173.PubMedCrossRefGoogle Scholar
  37. Kadoya, T., Oyanagi, K., Kawakami, E., Hasegawa, M., Inagaki, Y., Sohma, Y., and Horie, H. (2005). Oxidized galectin-1 advances the functional recovery after peripheral nerve injury. Neurosci Lett 380, 284–288.PubMedCrossRefGoogle Scholar
  38. Kajitani, K., Nomaru, H., Ifuku, M., Yutsudo, N., Dan, Y., Miura, T., Tsuchimoto, D., Sakumi, K., Kadoya, T., Horie, H., et al. (2009). Galectin-1 promotes basal and kainate-induced proliferation of neural progenitors in the dentate gyrus of adult mouse hippocampus. Cell Death Differ 16, 417–427.PubMedCrossRefGoogle Scholar
  39. Kipnis, J., Cohen, H., Cardon, M., Ziv, Y., and Schwartz, M. (2004). T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proceedings of the National Academy of Sciences of the United States of America 101, 8180–8185.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Kipnis, J., Mizrahi, T., Hauben, E., Shaked, I., Shevach, E., and Schwartz, M. (2002). Neuroprotective autoimmunity: naturally occurring CD4+CD25+ regulatory T cells suppress the ability to withstand injury to the central nervous system. Proceedings of the National Academy of Sciences of the line United States of America 99, 15620–15625.CrossRefGoogle Scholar
  41. Koch, A., Poirier, F., Jacob, R., and Delacour, D. (2010). Galectin-3, a novel centrosome-associated protein, required for epithelial morphogenesis. Mol Biol Cell 21, 219–231.PubMedCentralPubMedCrossRefGoogle Scholar
  42. Kopitz, J., André, S., von Reitzenstein, C., Versluis, K., Kaltner, H., Pieters, R.J., Wasano, K., Kuwabara, I., Liu, F.-T., Cantz, M., et al. (2003). Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene 22, 6277–6288.PubMedCrossRefGoogle Scholar
  43. Kurushima, H., Ohno, M., Miura, T., Nakamura, T.Y., Horie, H., Kadoya, T., Ooboshi, H., Kitazono, T., Ibayashi, S., Iida, M., et al. (2005). Selective induction of DeltaFosB in the brain after transient forebrain ischemia accompanied by an increased expression of galectin-1, and the implication of DeltaFosB and galectin-1 in neuroprotection and neurogenesis. Cell Death Differ 12, 1078–1096.PubMedCrossRefGoogle Scholar
  44. Lalancette-Hébert, M., Swarup, V., Beaulieu, J.M., Bohacek, I., Abdelhamid, E., Weng, Y.C., Sato, S., and Kriz, J. (2012). Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J Neurosci 32, 10383–10395.PubMedCrossRefGoogle Scholar
  45. Langrish, C.L., Chen, Y., Blumenschein, W.M., Mattson, J., Basham, B., Sedgwick, J.D., McClanahan, T., Kastelein, R.A., and Cua, D.J. (2005). IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. The Journal of experimental medicine 201, 233–240.PubMedCentralPubMedCrossRefGoogle Scholar
  46. Lehnardt, S. (2010). Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 58, 253–263.PubMedGoogle Scholar
  47. Lerman, B.J., Hoffman, E.P., Sutherland, M.L., Bouri, K., Hsu, D.K., Liu, F.-T., Rothstein, J.D., and Knoblach, S.M. (2012). 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 2, 563–575.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Lippai, D., Bala, S., Petrasek, J., Csak, T., Levin, I., Kurt-Jones, E.A., and Szabo, G. (2013). Alcohol-induced IL-1beta in the brain is mediated by NLRP3/ASC inflammasome activation that amplifies neuroinflammation. Journal of leukocyte biology 94, 171–182.PubMedCentralPubMedCrossRefGoogle Scholar
  49. Liu, F.T., Hsu, D.K., Zuberi, R.I., Kuwabara, I., Chi, E.Y., and Henderson, W.R. (1995). Expression and function of galectin-3, a beta-galactoside-binding lectin, in human monocytes and macrophages. Am J Pathol 147, 1016–1028.PubMedCentralPubMedGoogle Scholar
  50. Liu, L., Sakai, T., Sano, N., and Fukui, K. (2004). Nucling mediates apoptosis by inhibiting expression of galectin-3 through interference with nuclear factor kappaB signalling. Biochem J 380, 31–41.PubMedCentralPubMedCrossRefGoogle Scholar
  51. Liu, W., Hsu, D.K., Chen, H.-Y., Yang, R.-Y., Carraway, K.L., 3rd, Isseroff, R.R., and Liu, F.-T. (2012). Galectin-3 Regulates Intracellular Trafficking of EGFR through Alix and Promotes Keratinocyte Migration. J Invest Dermatol 132, 2828–2837.PubMedCentralPubMedCrossRefGoogle Scholar
  52. Mahanthappa, N.K., Cooper, D.N., Barondes, S.H., and Schwarting, G.A. (1994). Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120, 1373–1384.PubMedGoogle Scholar
  53. Martinon, F., Burns, K., and Tschopp, J. (2002). The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Molecular cell 10, 417–426.PubMedCrossRefGoogle Scholar
  54. McGraw, J., Gaudet, A.D., Oschipok, L.W., Kadoya, T., Horie, H., Steeves, J.D., Tetzlaff, W., and Ramer, M.S. (2005). Regulation of neuronal and glial galectin-1 expression by peripheral and central axotomy of rat primary afferent neurons. Exp Neurol 195, 103–114.PubMedCrossRefGoogle Scholar
  55. McGraw, J., McPhail, L.T., Oschipok, L.W., Horie, H., Poirier, F., Steeves, J.D., Ramer, M.S., and Tetzlaff, W. (2004). Galectin-1 in regenerating motoneurons. Eur J Neurosci 20, 2872–2880.PubMedCrossRefGoogle Scholar
  56. Mensah-Brown, E.P.K., Al Rabesi, Z., Shahin, A., Al Shamsi, M., Arsenijevic, N., Hsu, D.K., Liu, F.-T., and Lukic, M.L. (2009). Targeted disruption of the galectin-3 gene results in decreased susceptibility to multiple low dose streptozotocin-induced diabetes in mice. Clin Immunol 130, 83–88.PubMedCrossRefGoogle Scholar
  57. Mina-Osorio, P., Rosas-Ballina, M., Valdes-Ferrer, S.I., Al-Abed, Y., Tracey, K.J., and Diamond, B. (2012). Neural signaling in the spleen controls B-cell responses to blood-borne antigen. Mol Med 18, 618–627.PubMedCentralPubMedGoogle Scholar
  58. Mishra, R., Grzybek, M., Niki, T., Hirashima, M., and Simons, K. (2010). Galectin-9 trafficking regulates apical-basal polarity in Madin-Darby canine kidney epithelial cells. Proc Natl Acad Sci U S A 107, 17633–17638.PubMedCentralPubMedCrossRefGoogle Scholar
  59. Mrass, P., and Weninger, W. (2006). Immune cell migration as a means to control immune privilege: lessons from the CNS and tumors. Immunological reviews 213, 195–212.PubMedCrossRefGoogle Scholar
  60. Narciso, M.S., Mietto, B.d.S., Marques, S.A., Soares, C.P., Mermelstein, C.d.S., El-Cheikh, M.C., and Martinez, A.M.B. (2009). Sciatic nerve regeneration is accelerated in galectin-3 knockout mice. Exp Neurol 217, 7–15.Google Scholar
  61. Novak, R., Dabelic, S., and Dumic, J. (2012). Galectin-1 and galectin-3 expression profiles in classically and alternatively activated human macrophages. Biochim Biophys Acta 1820, 1383–1390.PubMedCrossRefGoogle Scholar
  62. O’Shea, J.J., and Paul, W.E. (2010). Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 327, 1098–1102.PubMedCentralPubMedCrossRefGoogle Scholar
  63. Offner, H., Celnik, B., Bringman, T.S., Casentini-Borocz, D., Nedwin, G.E., and Vandenbark, A.A. (1990). Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis. J Neuroimmunol 28, 177–184.PubMedCrossRefGoogle Scholar
  64. Ohshima, S., Kuchen, S., Seemayer, C.A., Kyburz, D., Hirt, A., Klinzing, S., Michel, B.A., Gay, R.E., Liu, F.-T., Gay, S., et al. (2003). Galectin 3 and its binding protein in rheumatoid arthritis. Arthritis Rheum 48, 2788–2795.PubMedCrossRefGoogle Scholar
  65. Olson, J.K., and Miller, S.D. (2004). Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173, 3916–3924.PubMedCrossRefGoogle Scholar
  66. Owens, T., Wekerle, H., and Antel, J. (2001). Genetic models for CNS inflammation. Nat Med 7, 161–166.PubMedCrossRefGoogle Scholar
  67. Park, J.W., Voss, P.G., Grabski, S., Wang, J.L., and Patterson, R.J. (2001). Association of galectin-1 and galectin-3 with Gemin4 in complexes containing the SMN protein. Nucleic Acids Res 29, 3595–3602.PubMedCentralPubMedCrossRefGoogle Scholar
  68. Paron, I., Scaloni, A., Pines, A., Bachi, A., Liu, F.T., Puppin, C., Pandolfi, M., Ledda, L., Di Loreto, C., Damante, G., et al. (2003). Nuclear localization of Galectin-3 in transformed thyroid cells: a role in transcriptional regulation. Biochem Biophys Res Commun 302, 545–553.PubMedCrossRefGoogle Scholar
  69. Pasquini, L.A., Millet, V., Hoyos, H.C., Giannoni, J.P., Croci, D.O., Marder, M., Liu, F.T., Rabinovich, G.A., and Pasquini, J.M. (2011). Galectin-3 drives oligodendrocyte differentiation to control myelin integrity and function. Cell Death Differ 18, 1746–1756.PubMedCentralPubMedCrossRefGoogle Scholar
  70. Peters, P.J., Borst, J., Oorschot, V., Fukuda, M., Krahenbuhl, O., Tschopp, J., Slot, J.W., and Geuze, H.J. (1991). Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. The Journal of experimental medicine 173, 1099–1109.PubMedCrossRefGoogle Scholar
  71. Plachta, N., Annaheim, C., Bissière, S., Lin, S., Rüegg, M., Hoving, S., Müller, D., Poirier, F., Bibel, M., and Barde, Y.-A. (2007). Identification of a lectin causing the degeneration of neuronal processes using engineered embryonic stem cells. Nat Neurosci 10, 712–719.PubMedCrossRefGoogle Scholar
  72. Poirier, F., and Robertson, E.J. (1993). Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development 119, 1229–1236.PubMedGoogle Scholar
  73. Polyak, K., Xia, Y., Zweier, J.L., Kinzler, K.W., and Vogelstein, B. (1997). A model for p53-induced apoptosis. Nature 389, 300–305.PubMedCrossRefGoogle Scholar
  74. Qu, W.-S., Wang, Y.-H., Ma, J.-F., Tian, D.-S., Zhang, Q., Pan, D.-J., Yu, Z.-Y., Xie, M.-J., Wang, J.-P., and Wang, W. (2011). Galectin-1 attenuates astrogliosis-associated injuries and improves recovery of rats following focal cerebral ischemia. J Neurochem 116, 217–226.PubMedCrossRefGoogle Scholar
  75. Radosavljevic, G., Volarevic, V., Jovanovic, I., Milovanovic, M., Pejnovic, N., Arsenijevic, N., Hsu, D.K., and Lukic, M.L. (2012). The roles of Galectin-3 in autoimmunity and tumor progression. Immunol Res 52, 100–110.PubMedCrossRefGoogle Scholar
  76. Ramos, H.J., Lanteri, M.C., Blahnik, G., Negash, A., Suthar, M.S., Brassil, M.M., Sodhi, K., Treuting, P.M., Busch, M.P., Norris, P.J., et al. (2012). IL-1beta signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS pathogens 8, e1003039.PubMedCentralPubMedCrossRefGoogle Scholar
  77. Ransohoff, R.M., and Brown, M.A. (2012). Innate immunity in the central nervous system. The Journal of clinical investigation 122, 1164–1171.PubMedCentralPubMedCrossRefGoogle Scholar
  78. Reboldi, A., Coisne, C., Baumjohann, D., Benvenuto, F., Bottinelli, D., Lira, S., Uccelli, A., Lanzavecchia, A., Engelhardt, B., and Sallusto, F. (2009). C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nature immunology 10, 514–523.PubMedCrossRefGoogle Scholar
  79. Reichert, F., and Rotshenker, S. (1999). Galectin-3/MAC-2 in experimental allergic encephalomyelitis. Exp Neurol 160, 508–514.PubMedCrossRefGoogle Scholar
  80. Reichert, F., Saada, A., and Rotshenker, S. (1994). Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: phagocytosis and the galactose-specific lectin MAC-2. J Neurosci 14, 3231–3245.PubMedGoogle Scholar
  81. Rosas-Ballina, M., Olofsson, P.S., Ochani, M., Valdes-Ferrer, S.I., Levine, Y.A., Reardon, C., Tusche, M.W., Pavlov, V.A., Andersson, U., Chavan, S., et al. (2011). Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334, 98–101.PubMedCrossRefGoogle Scholar
  82. Rotshenker, S. (2011). Wallerian degeneration: the innate-immune response to traumatic nerve injury. J Neuroinflammation 8, 109.PubMedCentralPubMedCrossRefGoogle Scholar
  83. Sakaguchi, M., Arruda-Carvalho, M., Kang, N.H., Imaizumi, Y., Poirier, F., Okano, H., and Frankland, P.W. (2011). Impaired spatial and contextual memory formation in galectin-1 deficient mice. Mol Brain 4, 33.PubMedCentralPubMedCrossRefGoogle Scholar
  84. Sakaguchi, M., Imaizumi, Y., and Okano, H. (2007). Expression and function of galectin-1 in adult neural stem cells. Cell Mol Life Sci 64, 1254–1258.PubMedCrossRefGoogle Scholar
  85. Sakaguchi, M., Shingo, T., Shimazaki, T., Okano, H.J., Shiwa, M., Ishibashi, S., Oguro, H., Ninomiya, M., Kadoya, T., Horie, H., et al. (2006). A carbohydrate-binding protein, Galectin-1, promotes proliferation of adult neural stem cells. Proc Natl Acad Sci U S A 103, 7112–7117.PubMedCentralPubMedCrossRefGoogle Scholar
  86. Sakaguchi, S., Yamaguchi, T., Nomura, T., and Ono, M. (2008). Regulatory T cells and immune tolerance. Cell 133, 775–787.PubMedCrossRefGoogle Scholar
  87. Sancho, D., and Reis e Sousa, C. (2012). Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annual review of immunology 30, 491–529.Google Scholar
  88. Savarin, C., and Bergmann, C.C. (2008). Neuroimmunology of central nervous system viral infections: the cells, molecules and mechanisms involved. Current opinion in pharmacology 8, 472–479.PubMedCentralPubMedCrossRefGoogle Scholar
  89. Schwartz, M., and Kipnis, J. (2011). A conceptual revolution in the relationships between the brain and immunity. Brain, behavior, and immunity 25, 817–819.PubMedCentralPubMedCrossRefGoogle Scholar
  90. Seil, F.J. (2001). Interactions between cerebellar Purkinje cells and their associated astrocytes. Histology and histopathology 16, 955–968.PubMedGoogle Scholar
  91. Seo, T.B., Chang, I.A., Lee, J.H., and Namgung, U. (2013). Beneficial function of cell division cycle 2 activity in astrocytes on axonal regeneration after spinal cord injury. Journal of neurotrauma 30, 1053–1061.PubMedCrossRefGoogle Scholar
  92. Shevach, E.M., DiPaolo, R.A., Andersson, J., Zhao, D.M., Stephens, G.L., and Thornton, A.M. (2006). The lifestyle of naturally occurring CD4+ CD25+ Foxp3+ regulatory T cells. Immunological reviews 212, 60–73.PubMedCrossRefGoogle Scholar
  93. Stancic, M., Slijepcevic, D., Nomden, A., Vos, M.J., de Jonge, J.C., Sikkema, A.H., Gabius, H.-J., Hoekstra, D., and Baron, W. (2012). Galectin-4, a novel neuronal regulator of myelination. Glia 60, 919–935.PubMedCrossRefGoogle Scholar
  94. Stancic, M., van Horssen, J., Thijssen, V.L., Gabius, H.-J., van der Valk, P., Hoekstra, D., and Baron, W. (2011). Increased expression of distinct galectins in multiple sclerosis lesions. Neuropathol Appl Neurobiol 37, 654–671.PubMedCrossRefGoogle Scholar
  95. Straube, T., von Mach, T., Hönig, E., Greb, C., Schneider, D., and Jacob, R. (2013). PH-dependent recycling of galectin-3 at the apical membrane of epithelial cells. Traffic.Google Scholar
  96. Takaku, S., Yanagisawa, H., Watabe, K., Horie, H., Kadoya, T., Sakumi, K., Nakabeppu, Y., Poirier, F., and Sango, K. (2013). GDNF promotes neurite outgrowth and upregulates galectin-1 through the RET/PI3K signaling in cultured adult rat dorsal root ganglion neurons. Neurochem Int 62, 330–339.PubMedCrossRefGoogle Scholar
  97. Takeuchi, O., and Akira, S. (2009). Innate immunity to virus infection. Immunological reviews 227, 75–86.PubMedCrossRefGoogle Scholar
  98. Thomsen, M.K., Hansen, G.H., and Danielsen, E.M. (2009). Galectin-2 at the enterocyte brush border of the small intestine. Mol Membr Biol 26, 347–355.PubMedCrossRefGoogle Scholar
  99. Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Zwirner, N.W., Poirier, F., Riley, E.M., Baum, L.G., et al. (2007). Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol 8, 825–834.PubMedCrossRefGoogle Scholar
  100. Velasco, S., Díez-Revuelta, N., Hernández-Iglesias, T., Kaltner, H., André, S., Gabius, H.-J., and Abad-Rodríguez, J. (2013). Neuronal Galectin-4 is required for axon growth and for the organization of axonal membrane L1 delivery and clustering. J Neurochem 125, 49–62.PubMedCrossRefGoogle Scholar
  101. Vidal, P.M., Lemmens, E., Dooley, D., and Hendrix, S. (2013). The role of “anti-inflammatory” cytokines in axon regeneration. Cytokine & growth factor reviews 24, 1–12.CrossRefGoogle Scholar
  102. Wei, Q., Eviatar-Ribak, T., Miskimins, W.K., and Miskimins, R. (2007). Galectin-4 is involved in p27-mediated activation of the myelin basic protein promoter. J Neurochem 101, 1214–1223.PubMedCrossRefGoogle Scholar
  103. Willing, A., and Friese, M.A. (2012). CD8-mediated inflammatory central nervous system disorders. Current opinion in neurology 25, 316–321.PubMedCrossRefGoogle Scholar
  104. Wolf, S.A., Steiner, B., Akpinarli, A., Kammertoens, T., Nassenstein, C., Braun, A., Blankenstein, T., and Kempermann, G. (2009a). CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J Immunol 182, 3979–3984.PubMedCrossRefGoogle Scholar
  105. Wolf, S.A., Steiner, B., Wengner, A., Lipp, M., Kammertoens, T., and Kempermann, G. (2009b). Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 23, 3121–3128.CrossRefGoogle Scholar
  106. Yamane, J., Nakamura, M., Iwanami, A., Sakaguchi, M., Katoh, H., Yamada, M., Momoshima, S., Miyao, S., Ishii, K., Tamaoki, N., et al. (2010). Transplantation of galectin-1-expressing human neural stem cells into the injured spinal cord of adult common marmosets. J Neurosci Res 88, 1394–1405.PubMedGoogle Scholar
  107. Yan, Y.-P., Lang, B.T., Vemuganti, R., and Dempsey, R.J. (2009). Galectin-3 mediates post-ischemic tissue remodeling. Brain Res 1288, 116–124.PubMedCrossRefGoogle Scholar
  108. Yang, R.-Y., Hsu, D.K., Yu, L., Chen, H.-Y., and Liu, F.-T. (2004). Galectin-12 is required for adipogenic signaling and adipocyte differentiation. J Biol Chem 279, 29761–29766.PubMedCrossRefGoogle Scholar
  109. Ye, Z., and Ting, J.P. (2008). NLR, the nucleotide-binding domain leucine-rich repeat containing gene family. Current opinion in immunology 20, 3–9.PubMedCrossRefGoogle Scholar
  110. Yoshida, H., Imaizumi, T., Kumagai, M., Kimura, K., Satoh, C., Hanada, N., Fujimoto, K., Nishi, N., Tanji, K., Matsumiya, T., et al. (2001). Interleukin-1beta stimulates galectin-9 expression in human astrocytes. Neuroreport 12, 3755–3758.PubMedCrossRefGoogle Scholar
  111. Yu, F., Finley, R.L., Jr., Raz, A., and Kim, H.R. (2002). Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome c release from the mitochondria. A role for synexin in galectin-3 translocation. J Biol Chem 277, 15819–15827.PubMedCrossRefGoogle Scholar
  112. Zhu, C., Anderson, A.C., Schubart, A., Xiong, H., Imitola, J., Khoury, S.J., Zheng, X.X., Strom, T.B., and Kuchroo, V.K. (2005). The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6, 1245–1252.PubMedCrossRefGoogle Scholar
  113. Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J., and Schwartz, M. (2006). Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nature neuroscience 9, 268–275.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Hung-Lin Chen
    • 1
  • Fang Liao
    • 1
  • Teng-Nan Lin
    • 1
  • Fu-Tong Liu
    • 1
  1. 1.Institute of Biomedical SciencesAcademia SinicaTaipeiTaiwan

Personalised recommendations