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Journal of Inherited Metabolic Disease

, Volume 37, Issue 1, pp 1–12 | Cite as

Mucopolysaccharide diseases: A complex interplay between neuroinflammation, microglial activation and adaptive immunity

  • Louise D. Archer
  • Kia J. Langford-Smith
  • Brian W. Bigger
  • James E. Fildes
Review

Abstract

Mucopolysaccharide (MPS) diseases are lysosomal storage disorders (LSDs) caused by deficiencies in enzymes required for glycosaminoglycan (GAG) catabolism. Mucopolysaccharidosis I (MPS I), MPS IIIA, MPS IIIB and MPS VII are deficient in the enzymes α–L-Iduronidase, Heparan-N-Sulphatase, N-Acetylglucosaminidase and Beta-Glucuronidase, respectively. Enzyme deficiency leads to the progressive multi-systemic build-up of heparan sulphate (HS) and dermatan sulphate (DS) within cellular lysosomes, followed by cell, tissue and organ damage and in particular neurodegeneration. Clinical manifestations of MPS are well established; however as lysosomes represent vital components of immune cells, it follows that lysosomal accumulation of GAGs could affect diverse immune functions and therefore influence disease pathogenesis. Theoretically, MPS neurodegeneration and GAGs could be substantiating a threat of danger and damage to alert the immune system for cellular clearance, which due to the progressive nature of MPS storage would propagate disease pathogenesis. Innate immunity appears to have a key role in MPS; however the extent of adaptive immune involvement remains to be elucidated. The current literature suggests a complex interplay between neuroinflammation, microglial activation and adaptive immunity in MPS disease.

Keywords

Dendritic Cell Heparan Sulphate Microglial Activation Migration Inhibitory Factor iNKT Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Conflict of interest

None.

References

  1. Alegre ML, Frauwirth KA, Thompson CB (2001) T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 1(3):220–228PubMedCrossRefGoogle Scholar
  2. Annacker O, Burlen-Defranoux O, Pimenta-Araujo R, Cumano A, Bandeira A (2000) Regulatory CD4 T cells control the size of the peripheral activated/memory CD4 T cell compartment. J Immunol 164(7):3573–3580PubMedGoogle Scholar
  3. Archer LD, Langford-Smith KJ, Critchley WR, Bigger BW, Fildes JE (2013) Characterisation of the T cell and dendritic cell repertoire in a murine model of mucopolysaccharidosis I (MPS I). J Inherit Metab Dis 36(2):257-62Google Scholar
  4. Arfi A, Richard M, Gandolphe C, Bonnefont-Rousselot D, Therond P, Scherman D (2011) Neuroinflammatory and oxidative stress phenomena in MPS IIIA mouse model: the positive effect of long-term aspirin treatment. Mol Genet Metab 103(1):18–25PubMedCrossRefGoogle Scholar
  5. Ausseil J, Desmaris N, Bigou S et al (2008) Early neurodegeneration progresses independently of microglial activation by heparan sulfate in the brain of mucopolysaccharidosis IIIB mice. PLoS One 3(5):e2296PubMedCentralPubMedCrossRefGoogle Scholar
  6. Babcock AA, Wirenfeldt M, Holm T et al (2006) Toll-like receptor 2 signaling in response to brain injury: an innate bridge to neuroinflammation. J Neurosci 26(49):12826–12837PubMedCrossRefGoogle Scholar
  7. Bacher M, Deuster O, Aljabari B et al (2010) The role of macrophage migration inhibitory factor in Alzheimer’s disease. Mol Med 16(3–4):116–121PubMedCentralPubMedGoogle Scholar
  8. Berg M, Zavazava N (2008) Regulation of CD28 expression on CD8+ T cells by CTLA-4. J Leukoc Biol 83(4):853–863PubMedCrossRefGoogle Scholar
  9. Bernsen PL, Wevers RA, Gabreels FJ, Lamers KJ, Sonnen AE, Stekhoven JH (1987) Phenotypic expression in mucopolysaccharidosis VII. J Neurol Neurosurg Psychiatry 50(6):699–703PubMedCrossRefGoogle Scholar
  10. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81(1):1–5PubMedCrossRefGoogle Scholar
  11. Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8(1):57–69PubMedCrossRefGoogle Scholar
  12. Boje KM, Arora PK (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res 587(2):250–256PubMedCrossRefGoogle Scholar
  13. Bossi G, Griffiths GM (1999) Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat Med 5(1):90–96PubMedCrossRefGoogle Scholar
  14. Boya P, Gonzalez-Polo RA, Casares N et al (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25(3):1025–1040PubMedCentralPubMedCrossRefGoogle Scholar
  15. Burman C, Ktistakis NT (2010) Autophagosome formation in mammalian cells. Semin Immunopathol 32(4):397–413PubMedCrossRefGoogle Scholar
  16. Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M (2005) Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol Cell Neurosci 29(3):381–393PubMedCrossRefGoogle Scholar
  17. Butovsky O, Landa G, Kunis G et al (2006a) Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 116(4):905–915PubMedCentralPubMedCrossRefGoogle Scholar
  18. Butovsky O, Ziv Y, Schwartz A et al (2006b) Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31(1):149–160PubMedCrossRefGoogle Scholar
  19. Castaneda JA, Lim MJ, Cooper JD, Pearce DA (2008) Immune system irregularities in lysosomal storage disorders. Acta Neuropathol 115(2):159–174PubMedCrossRefGoogle Scholar
  20. Cebecauer M, Guillaume P, Mark S et al (2005) CD8+ cytotoxic T lymphocyte activation by soluble major histocompatibility complex-peptide dimers. J Biol Chem 280(25):23820–23828PubMedCrossRefGoogle Scholar
  21. Chandran SS, Verhoeven D, Teijaro JR, Fenton MJ, Farber DL (2009) TLR2 engagement on dendritic cells promotes high frequency effector and memory CD4 T cell responses. J Immunol 183(12):7832–7841PubMedCrossRefGoogle Scholar
  22. Cheng Q, McKeown SJ, Santos L et al (2010) Macrophage migration inhibitory factor increases leukocyte-endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J Immunol 185(2):1238–1247PubMedCrossRefGoogle Scholar
  23. Cleary MA, Wraith JE (1993) Management of mucopolysaccharidosis type III. Arch Dis Child 69(3):403–406PubMedCrossRefGoogle Scholar
  24. Codogno P, Meijer AJ (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12(Suppl 2):1509–1518PubMedCrossRefGoogle Scholar
  25. Colton CA (2009) Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4(4):399–418PubMedCentralPubMedCrossRefGoogle Scholar
  26. Colton CA, Gilbert DL (1987) Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 223(2):284–288PubMedCrossRefGoogle Scholar
  27. Conductier G, Blondeau N, Guyon A, Nahon JL, Rovere C (2010) The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J Neuroimmunol 224(1–2):93–100PubMedCrossRefGoogle Scholar
  28. Constantopoulos G, Dekaban AS (1978) Neurochemistry of the mucopolysaccharidoses: brain lipids and lysosomal enzymes in patients with four types of mucopolysaccharidosis and in normal controls. J Neurochem 30(5):965–973PubMedCrossRefGoogle Scholar
  29. Curtsinger JM, Mescher MF (2010) Inflammatory cytokines as a third signal for T cell activation. Curr Opin Immunol 22(3):333–340PubMedCentralPubMedCrossRefGoogle Scholar
  30. Curtsinger JM, Lins DC, Mescher MF (2003) Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med 197(9):1141–1151PubMedCentralPubMedCrossRefGoogle Scholar
  31. Daly TM, Lorenz RG, Sands MS (2000) Abnormal immune function in vivo in a murine model of lysosomal storage disease. Pediatr Res 47(6):757–762PubMedCrossRefGoogle Scholar
  32. Dani A, Chaudhry A, Mukherjee P et al (2004) The pathway for MHCII-mediated presentation of endogenous proteins involves peptide transport to the endo-lysosomal compartment. J Cell Sci 117(Pt 18):4219–4230PubMedCrossRefGoogle Scholar
  33. Davies JD, O’Connor E, Hall D, Krahl T, Trotter J, Sarvetnick N (1999) CD4+ CD45RB low-density cells from untreated mice prevent acute allograft rejection. J Immunol 163(10):5353–5357PubMedGoogle Scholar
  34. de Groot RP, Coffer PJ, Koenderman L (1998) Regulation of proliferation, differentiation and survival by the IL-3/IL-5/GM-CSF receptor family. Cell Signal 10(9):619–628PubMedCrossRefGoogle Scholar
  35. Dickson P, Peinovich M, McEntee M et al (2008) Immune tolerance improves the efficacy of enzyme replacement therapy in canine mucopolysaccharidosis I. J Clin Invest 118(8):2868–2876PubMedCentralPubMedGoogle Scholar
  36. DiRosario J, Divers E, Wang C et al (2009) Innate and adaptive immune activation in the brain of MPS IIIB mouse model. J Neurosci Res 87(4):978–990PubMedCrossRefGoogle Scholar
  37. Dower SK, Kronheim SR, Hopp TP et al (1986) The cell surface receptors for interleukin-1 alpha and interleukin-1 beta are identical. Nature 324(6094):266–268PubMedCrossRefGoogle Scholar
  38. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100(23):13632–13637PubMedCrossRefGoogle Scholar
  39. Ekdahl CT, Kokaia Z, Lindvall O (2009) Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158(3):1021–1029PubMedCrossRefGoogle Scholar
  40. Eskelinen EL, Saftig P (2009) Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim Biophys Acta 1793(4):664–673PubMedCrossRefGoogle Scholar
  41. Fraldi A, Annunziata F, Lombardi A et al (2010) Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. Embo J 29(21):3607–3620PubMedCrossRefGoogle Scholar
  42. Gadola SD, Silk JD, Jeans A et al (2006) Impaired selection of invariant natural killer T cells in diverse mouse models of glycosphingolipid lysosomal storage diseases. J Exp Med 203(10):2293–2303PubMedCentralPubMedCrossRefGoogle Scholar
  43. Gallucci S, Lolkema M, Matzinger P (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5(11):1249–1255PubMedCrossRefGoogle Scholar
  44. Giugliani R, Federhen A, Rojas MV et al (2010) Mucopolysaccharidosis I, II, and VI: Brief review and guidelines for treatment. Genet Mol Biol 33(4):589–604PubMedCrossRefGoogle Scholar
  45. Greenwald RJ, Boussiotis VA, Lorsbach RB, Abbas AK, Sharpe AH (2001) CTLA-4 regulates induction of anergy in vivo. Immunity 14(2):145–155PubMedCrossRefGoogle Scholar
  46. Groux H, O’Garra A, Bigler M et al (1997) A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389(6652):737–742PubMedCrossRefGoogle Scholar
  47. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387–1394PubMedCrossRefGoogle Scholar
  48. Hara M, Kingsley CI, Niimi M et al (2001) IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J Immunol 166(6):3789–3796PubMedGoogle Scholar
  49. Harr MW, Distelhorst CW (2010) Apoptosis and autophagy: decoding calcium signals that mediate life or death. Cold Spring Harb Perspect Biol 2(10):a005579PubMedCrossRefGoogle Scholar
  50. Hermans IF, Silk JD, Gileadi U et al (2003) NKT cells enhance CD4+ and CD8+ T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J Immunol 171(10):5140–5147PubMedGoogle Scholar
  51. Hermans IF, Silk JD, Gileadi U et al (2007) Dendritic cell function can be modulated through cooperative actions of TLR ligands and invariant NKT cells. J Immunol 178(5):2721–2729PubMedGoogle Scholar
  52. Hodgkin PD, Castle BE, Kehry MR (1994) B cell differentiation induced by helper T cell membranes: evidence for sequential isotype switching and a requirement for lymphokines during proliferation. Eur J Immunol 24(1):239–246PubMedCrossRefGoogle Scholar
  53. Hoffmann O, Braun JS, Becker D et al (2007) TLR2 mediates neuroinflammation and neuronal damage. J Immunol 178(10):6476–6481PubMedGoogle Scholar
  54. Holley RJ, Deligny A, Wei W et al (2011) Mucopolysaccharidosis type I, unique structure of accumulated heparan sulfate and increased N-sulfotransferase activity in mice lacking alpha-l-iduronidase. J Biol Chem 286(43):37515–37524PubMedCrossRefGoogle Scholar
  55. Hsieh J, Aimone JB, Kaspar BK, Kuwabara T, Nakashima K, Gage FH (2004) IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J Cell Biol 164(1):111–122PubMedCrossRefGoogle Scholar
  56. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677–736PubMedCentralPubMedCrossRefGoogle Scholar
  57. Jeyakumar M, Smith DA, Williams IM et al (2004) NSAIDs increase survival in the Sandhoff disease mouse: synergy with N-butyldeoxynojirimycin. Ann Neurol 56(5):642–649PubMedCrossRefGoogle Scholar
  58. Joffre O, Nolte MA, Sporri R, Reis E, Sousa C (2009) Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev 227(1):234–247PubMedCrossRefGoogle Scholar
  59. Johnson DE (1998) Regulation of survival pathways by IL-3 and induction of apoptosis following IL-3 withdrawal. Front Biosci 3:d313–324PubMedGoogle Scholar
  60. Johnson GB, Brunn GJ, Kodaira Y, Platt JL (2002) Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 168(10):5233–5239PubMedGoogle Scholar
  61. Kawasaki N, Rademacher C, Paulson JC (2010) CD22 regulates adaptive and innate immune responses of B cells. J Innate Immun 3(4):411–419PubMedCrossRefGoogle Scholar
  62. Kawashita E, Tsuji D, Toyoshima M, Kanno Y, Matsuno H, Itoh K (2011) Prostaglandin E2 reverses aberrant production of an inflammatory chemokine by microglia from Sandhoff disease model mice through the cAMP-PKA pathway. PLoS One 6(1):e16269PubMedCentralPubMedCrossRefGoogle Scholar
  63. Kehry MR, Hodgkin PD (1993) Helper T cells: delivery of cell contact and lymphokine-dependent signals to B cells. Semin Immunol 5(6):393–400PubMedCrossRefGoogle Scholar
  64. Killedar S, Dirosario J, Divers E, Popovich PG, McCarty DM, Fu H (2010) Mucopolysaccharidosis IIIB, a lysosomal storage disease, triggers a pathogenic CNS autoimmune response. J Neuroinflammation 7:39PubMedCentralPubMedCrossRefGoogle Scholar
  65. Kiselyov K, Jennigs JJ Jr, Rbaibi Y, Chu CT (2007) Autophagy, mitochondria and cell death in lysosomal storage diseases. Autophagy 3(3):259–262PubMedCentralPubMedGoogle Scholar
  66. Kithcart AP, Cox GM, Sielecki T et al (2010) A small-molecule inhibitor of macrophage migration inhibitory factor for the treatment of inflammatory disease. Faseb J 24(11):4459–4466PubMedCrossRefGoogle Scholar
  67. Kodaira Y, Nair SK, Wrenshall LE, Gilboa E, Platt JL (2000) Phenotypic and functional maturation of dendritic cells mediated by heparan sulfate. J Immunol 165(3):1599–1604PubMedGoogle Scholar
  68. Komai-Koma M, Jones L, Ogg GS, Xu D, Liew FY (2004) TLR2 is expressed on activated T cells as a costimulatory receptor. Proc Natl Acad Sci USA 101(9):3029–3034PubMedCrossRefGoogle Scholar
  69. Kyrkanides S, Miller AW, Miller JN et al (2008) Peripheral blood mononuclear cell infiltration and neuroinflammation in the HexB-/- mouse model of neurodegeneration. J Neuroimmunol 203(1):50–57PubMedCentralPubMedCrossRefGoogle Scholar
  70. Langford-Smith A, Langford-Smith KJ, Jones SA et al (2011a) Female mucopolysaccharidosis IIIA mice exhibit hyperactivity and a reduced sense of danger in the open field test. PLoS One 6(10):e25717PubMedCentralPubMedCrossRefGoogle Scholar
  71. Langford-Smith A, Malinowska M, Langford-Smith KJ et al (2011b) Hyperactive behaviour in the mouse model of mucopolysaccharidosis IIIB in the open field and home cage environments. Genes Brain Behav 10(6):673–682PubMedCrossRefGoogle Scholar
  72. Ledeboer A, Breve JJ, Poole S, Tilders FJ, Van Dam AM (2000) Interleukin-10, interleukin-4, and transforming growth factor-beta differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells. Glia 30(2):134–142PubMedCrossRefGoogle Scholar
  73. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW (1993) Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J Immunol 150(7):2659–2667PubMedGoogle Scholar
  74. Lehman TJ, Miller N, Norquist B, Underhill L, Keutzer J (2011) Diagnosis of the mucopolysaccharidoses. Rheumatology (Oxford) 50(Suppl 5):v41–48CrossRefGoogle Scholar
  75. Lim B, Sutherland RM, Zhan Y, Deliyannis G, Brown LE, Lew AM (2006) Targeting CD45RB alters T cell migration and delays viral clearance. Int Immunol 18(2):291–300PubMedCrossRefGoogle Scholar
  76. Linsen L, Somers V, Stinissen P (2005) Immunoregulation of autoimmunity by natural killer T cells. Hum Immunol 66(12):1193–1202PubMedCrossRefGoogle Scholar
  77. Liu B, Gao HM, Wang JY, Jeohn GH, Cooper CL, Hong JS (2002) Role of nitric oxide in inflammation-mediated neurodegeneration. Ann NY Acad Sci 962:318–331PubMedCrossRefGoogle Scholar
  78. Luke PP, Deng JP, Lian D et al (2006) Prolongation of allograft survival by administration of anti-CD45RB monoclonal antibody is due to alteration of CD45RBhi: CD45RBlo T-cell proportions. Am J Transplant 6(9):2023–2034PubMedCrossRefGoogle Scholar
  79. Lum JJ, DeBerardinis RJ, Thompson CB (2005) Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol 6(6):439–448PubMedCrossRefGoogle Scholar
  80. Lutz MB (2004) IL-3 in dendritic cell development and function: a comparison with GM-CSF and IL-4. Immunobiology 209(1–2):79–87PubMedCrossRefGoogle Scholar
  81. Mahad DJ, Ransohoff RM (2003) The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin Immunol 15(1):23–32PubMedCrossRefGoogle Scholar
  82. Mahad D, Callahan MK, Williams KA et al (2006) Modulating CCR2 and CCL2 at the blood-brain barrier: relevance for multiple sclerosis pathogenesis. Brain 129(Pt 1):212–223PubMedGoogle Scholar
  83. Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12:991–1045PubMedCrossRefGoogle Scholar
  84. Matzinger P (2002) The danger model: a renewed sense of self. Science 296(5566):301–305PubMedCrossRefGoogle Scholar
  85. McGlynn R, Dobrenis K, Walkley SU (2004) Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J Comp Neurol 480(4):415–426PubMedCrossRefGoogle Scholar
  86. Min KJ, Pyo HK, Yang MS, Ji KA, Jou I, Joe EH (2004) Gangliosides activate microglia via protein kinase C and NADPH oxidase. Glia 48(3):197–206PubMedCrossRefGoogle Scholar
  87. Mitchell RA, Liao H, Chesney J et al (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci USA 99(1):345–350PubMedCrossRefGoogle Scholar
  88. Mizushima N (2009) Physiological functions of autophagy. Curr Top Microbiol Immunol 335:71–84PubMedGoogle Scholar
  89. Mizutani K, Oka N, Akiguchi I et al (1999) Enhancement of TNF-alpha production by ganglioside GM2 in human mononuclear cell culture. Neuroreport 10(4):703–706PubMedCrossRefGoogle Scholar
  90. Muenzer J (2004) The mucopolysaccharidoses: a heterogeneous group of disorders with variable pediatric presentations. J Pediatr 144(5 Suppl):S27–34PubMedCrossRefGoogle Scholar
  91. Muenzer J, Wraith JE, Clarke LA (2009) Mucopolysaccharidosis I: management and treatment guidelines. Pediatrics 123(1):19–29PubMedCrossRefGoogle Scholar
  92. Muessel MJ, Berman NE, Klein RM (2000) Early and specific expression of monocyte chemoattractant protein-1 in the thalamus induced by cortical injury. Brain Res 870(1–2):211–221PubMedCrossRefGoogle Scholar
  93. Muessel MJ, Klein RM, Wilson AM, Berman NE (2002) Ablation of the chemokine monocyte chemoattractant protein-1 delays retrograde neuronal degeneration, attenuates microglial activation, and alters expression of cell death molecules. Brain Res Mol Brain Res 103(1–2):12–27PubMedCrossRefGoogle Scholar
  94. Muhlebach MS, Wooten W, Muenzer J (2011) Respiratory manifestations in mucopolysaccharidoses. Paediatr Respir Rev 12(2):133–138PubMedCrossRefGoogle Scholar
  95. Nakao Y, Funami K, Kikkawa S et al (2005) Surface-expressed TLR6 participates in the recognition of diacylated lipopeptide and peptidoglycan in human cells. J Immunol 174(3):1566–1573PubMedGoogle Scholar
  96. Neumann H, Kotter MR, Franklin RJ (2009) Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132(Pt 2):288–295PubMedGoogle Scholar
  97. Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev S, Li HH, Neufeld EF (2003) Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci USA 100(4):1902–1907PubMedCrossRefGoogle Scholar
  98. Ohta T, Kinoshita T, Naito M et al (1997) Requirement of the caspase-3/CPP32 protease cascade for apoptotic death following cytokine deprivation in hematopoietic cells. J Biol Chem 272(37):23111–23116PubMedCrossRefGoogle Scholar
  99. Olson JK, Miller SD (2004) Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173(6):3916–3924PubMedGoogle Scholar
  100. Ozinsky A, Underhill DM, Fontenot JD et al (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci USA 97(25):13766–13771PubMedCrossRefGoogle Scholar
  101. Pais TF, Figueiredo C, Peixoto R, Braz MH, Chatterjee S (2008) Necrotic neurons enhance microglial neurotoxicity through induction of glutaminase by a MyD88-dependent pathway. J Neuroinflammation 5:43PubMedCentralPubMedCrossRefGoogle Scholar
  102. Pamer E, Cresswell P (1998) Mechanisms of MHC class I–restricted antigen processing. Annu Rev Immunol 16:323–358PubMedCrossRefGoogle Scholar
  103. Parker DC (1993) T cell-dependent B cell activation. Annu Rev Immunol 11:331–360PubMedCrossRefGoogle Scholar
  104. Pasare C, Medzhitov R (2005) Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol 560:11–18PubMedCrossRefGoogle Scholar
  105. Peters PJ, Borst J, Oorschot V et al (1991) Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J Exp Med 173(5):1099–1109PubMedCrossRefGoogle Scholar
  106. Piccinini AM, Midwood KS (2010) DAMPening inflammation by modulating TLR signalling. Mediators Inflamm doi: 10.1155/2010/672395 PubMedCentralPubMedGoogle Scholar
  107. Plati T, Visigalli I, Capotondo A et al (2009) Development and maturation of invariant NKT cells in the presence of lysosomal engulfment. Eur J Immunol 39(10):2748–2754PubMedCrossRefGoogle Scholar
  108. Ponder KP (2008) Immune response hinders therapy for lysosomal storage diseases. J Clin Invest 118(8):2686–2689PubMedCentralPubMedGoogle Scholar
  109. Powrie F, Carlino J, Leach MW, Mauze S, Coffman RL (1996) A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J Exp Med 183(6):2669–2674PubMedCrossRefGoogle Scholar
  110. Purbhoo MA, Irvine DJ, Huppa JB, Davis MM (2004) T cell killing does not require the formation of a stable mature immunological synapse. Nat Immunol 5(5):524–530PubMedCrossRefGoogle Scholar
  111. Puri N, Roche PA (2008) Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc Natl Acad Sci USA 105(7):2580–2585PubMedCrossRefGoogle Scholar
  112. Qin L, Liu Y, Wang T et al (2004) NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 279(2):1415–1421PubMedCrossRefGoogle Scholar
  113. Quigley M, Martinez J, Huang X, Yang Y (2009) A critical role for direct TLR2-MyD88 signaling in CD8 T-cell clonal expansion and memory formation following vaccinia viral infection. Blood 113(10):2256–2264PubMedCrossRefGoogle Scholar
  114. Rego AC, Oliveira CR (2003) Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochem Res 28(10):1563–1574PubMedCrossRefGoogle Scholar
  115. Reolon GK, Reinke A, de Oliveira MR et al (2009) Alterations in oxidative markers in the cerebellum and peripheral organs in MPS I mice. Cell Mol Neurobiol 29(4):443–448PubMedCrossRefGoogle Scholar
  116. Schmidt CS, Mescher MF (2002) Peptide antigen priming of naive, but not memory, CD8 T cells requires a third signal that can be provided by IL-12. J Immunol 168(11):5521–5529PubMedGoogle Scholar
  117. Seong SY, Matzinger P (2004) Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 4(6):469–478PubMedCrossRefGoogle Scholar
  118. Settembre C, Fraldi A, Jahreiss L et al (2008) A block of autophagy in lysosomal storage disorders. Hum Mol Genet 17(1):119–129PubMedCrossRefGoogle Scholar
  119. Siebert H, Sachse A, Kuziel WA, Maeda N, Bruck W (2000) The chemokine receptor CCR2 is involved in macrophage recruitment to the injured peripheral nervous system. J Neuroimmunol 110(1–2):177–185PubMedCrossRefGoogle Scholar
  120. Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176(1):287–292PubMedCrossRefGoogle Scholar
  121. Stober D, Jomantaite I, Schirmbeck R, Reimann J (2003) NKT cells provide help for dendritic cell-dependent priming of MHC class I-restricted CD8+ T cells in vivo. J Immunol 170(5):2540–2548PubMedGoogle Scholar
  122. Strawbridge AB, Blum JS (2007) Autophagy in MHC class II antigen processing. Curr Opin Immunol 19(1):87–92PubMedCrossRefGoogle Scholar
  123. Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN (1996) Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4(6):565–571PubMedCrossRefGoogle Scholar
  124. Ten Hove T, The Olle F, Berkhout M et al (2004) Expression of CD45RB functionally distinguishes intestinal T lymphocytes in inflammatory bowel disease. J Leukoc Biol 75(6):1010–1015PubMedCrossRefGoogle Scholar
  125. Thiery J, Keefe D, Boulant S et al (2011) Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol 12(8):770–777PubMedCentralPubMedCrossRefGoogle Scholar
  126. Thoma-Uszynski S, Kiertscher SM, Ochoa MT et al (2000) Activation of toll-like receptor 2 on human dendritic cells triggers induction of IL-12, but not IL-10. J Immunol 165(7):3804–3810PubMedGoogle Scholar
  127. Trapani JA, Smyth MJ (2002) Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2(10):735–747PubMedCrossRefGoogle Scholar
  128. Van Kaer L, Parekh VV, Wu L (2011) Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res 343(1):43–55PubMedCentralPubMedCrossRefGoogle Scholar
  129. Veugelers K, Motyka B, Goping IS, Shostak I, Sawchuk T, Bleackley RC (2006) Granule-mediated killing by granzyme B and perforin requires a mannose 6-phosphate receptor and is augmented by cell surface heparan sulfate. Mol Biol Cell 17(2):623–633PubMedCentralPubMedCrossRefGoogle Scholar
  130. Villani GR, Gargiulo N, Faraonio R, Castaldo S, Gonzalez YRE, Di Natale P (2007) Cytokines, neurotrophins, and oxidative stress in brain disease from mucopolysaccharidosis IIIB. J Neurosci Res 85(3):612–622PubMedCrossRefGoogle Scholar
  131. Villani GR, Di Domenico C, Musella A, Cecere F, Di Napoli D, Di Natale P (2009) Mucopolysaccharidosis IIIB: oxidative damage and cytotoxic cell involvement in the neuronal pathogenesis. Brain Res 1279:99–108PubMedCrossRefGoogle Scholar
  132. Wada R, Tifft CJ, Proia RL (2000) Microglial activation precedes acute neurodegeneration in Sandhoff disease and is suppressed by bone marrow transplantation. Proc Natl Acad Sci USA 97(20):10954–10959PubMedCrossRefGoogle Scholar
  133. Walker JA, Smith KG (2008) CD22: an inhibitory enigma. Immunology 123(3):314–325PubMedCrossRefGoogle Scholar
  134. Walter L, Neumann H (2009) Role of microglia in neuronal degeneration and regeneration. Semin Immunopathol 31(4):513–525PubMedCrossRefGoogle Scholar
  135. Wang SH, Chen GH, Fan Y, Van Antwerp M, Baker JR Jr (2009) Tumor necrosis factor-related apoptosis-inducing ligand inhibits experimental autoimmune thyroiditis by the expansion of CD4+CD25+ regulatory T cells. Endocrinology 150(4):2000–2007PubMedCrossRefGoogle Scholar
  136. Wilkinson FL, Holley RJ, Langford-Smith KJ et al (2012) Neuropathology in mouse models of mucopolysaccharidosis type I, IIIA and IIIB. PLoS One 7(4):e35787PubMedCentralPubMedCrossRefGoogle Scholar
  137. Wraith JE (1995) The mucopolysaccharidoses: a clinical review and guide to management. Arch Dis Child 72(3):263–267PubMedCrossRefGoogle Scholar
  138. Wrenshall LE, Cerra FB, Carlson A, Bach FH, Platt JL (1991) Regulation of murine splenocyte responses by heparan sulfate. J Immunol 147(2):455–459PubMedGoogle Scholar
  139. Wrenshall LE, Carlson A, Cerra FB, Platt JL (1994) Modulation of cytolytic T cell responses by heparan sulfate. Transplantation 57(7):1087–1094PubMedGoogle Scholar
  140. Wrenshall LE, Cerra FB, Singh RK, Platt JL (1995) Heparan sulfate initiates signals in murine macrophages leading to divergent biologic outcomes. J Immunol 154(2):871–880PubMedGoogle Scholar
  141. Wrenshall LE, Stevens RB, Cerra FB, Platt JL (1999) Modulation of macrophage and B cell function by glycosaminoglycans. J Leukoc Biol 66(3):391–400PubMedGoogle Scholar
  142. Wu YP, Proia RL (2004) Deletion of macrophage-inflammatory protein 1 alpha retards neurodegeneration in Sandhoff disease mice. Proc Natl Acad Sci USA 101(22):8425–8430PubMedCrossRefGoogle Scholar
  143. Wu L, Van Kaer L (2009) Natural killer T cells and autoimmune disease. Curr Mol Med 9(1):4–14PubMedCrossRefGoogle Scholar
  144. Yamaguchi A, Katsuyama K, Nagahama K, Takai T, Aoki I, Yamanaka S (2004) Possible role of autoantibodies in the pathophysiology of GM2 gangliosidoses. J Clin Invest 113(2):200–208PubMedCentralPubMedGoogle Scholar
  145. York IA, Rock KL (1996) Antigen processing and presentation by the class I major histocompatibility complex. Annu Rev Immunol 14:369–396PubMedCrossRefGoogle Scholar
  146. Yoshimori T (2004) Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 313(2):453–458PubMedCrossRefGoogle Scholar
  147. Zhao W, Xie W, Xiao Q, Beers DR, Appel SH (2006) Protective effects of an anti-inflammatory cytokine, interleukin-4, on motoneuron toxicity induced by activated microglia. J Neurochem 99(4):1176–1187PubMedCrossRefGoogle Scholar
  148. Zhou D, Mattner J, Cantu C 3rd et al (2004) Lysosomal glycosphingolipid recognition by NKT cells. Science 306(5702):1786–1789PubMedCrossRefGoogle Scholar

Copyright information

© SSIEM and Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Louise D. Archer
    • 1
  • Kia J. Langford-Smith
    • 2
  • Brian W. Bigger
    • 2
  • James E. Fildes
    • 1
    • 3
  1. 1.The Transplant Centre, UHSMUniversity of ManchesterManchesterUK
  2. 2.Stem Cell & Neurotherapies LaboratoryUniversity of ManchesterManchesterUK
  3. 3.The Manchester Collaborative Centre for Inflammation Research (MCCIR)University of South ManchesterManchesterUK

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