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

Journal of Inherited Metabolic Disease

Volumn 37, Issue 1, 2014, Pages 1-12

  Archer, Louise D ^a   Langford Smith, Kia J ^a   Bigger, Brian W ^a   Fildes, James E ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b Manchester Academic Health Science Centre   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLGLUCOSAMINIDASE; BETA GLUCURONIDASE; DERMATAN SULFATE; HEPARAN N SULFATASE; HEPARAN SULFATE; LEVO IDURONIDASE; SULFATASE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; AUTOPHAGY; B LYMPHOCYTE; HURLER SYNDROME; IMMUNOCOMPETENT CELL; LYSOSOME; LYSOSOME STORAGE DISEASE; MICROGLIA; MUCOPOLYSACCHARIDE DISEASE; MUCOPOLYSACCHARIDOSIS 7; NATURAL KILLER T CELL; NERVOUS SYSTEM INFLAMMATION; REVIEW; SANFILIPPO SYNDROME; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; AUTOPHAGY; B-LYMPHOCYTES; DENDRITIC CELLS; ENZYMES; HUMANS; INFLAMMATION; LYSOSOMES; MICROGLIA; MUCOPOLYSACCHARIDOSES; NEURODEGENERATIVE DISEASES; NEURONS; OXIDATIVE STRESS; PEPTIDES; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

EID: 84891815970     PISSN: 01418955     EISSN: 15732665     Source Type: Journal    
DOI: 10.1007/s10545-013-9613-3     Document Type: Review

References (148)

1. Alegre ML, Frauwirth KA, Thompson CB (2001) T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 1(3):220-228
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):3573-3580
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):257-62
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):18-25
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):e2296
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):12826-12837
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):116-121
8. Berg M, Zavazava N (2008) Regulation of CD28 expression on CD8+ T cells by CTLA-4. J Leukoc Biol 83(4):853-863
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):699-703
10. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81(1):1-5
11. Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8(1):57-69
12. Boje KM, Arora PK (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res 587(2):250-256
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):90-96
14. Boya P, Gonzalez-Polo RA, Casares N et al (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25(3):1025-1040
15. Burman C, Ktistakis NT (2010) Autophagosome formation in mammalian cells. Semin Immunopathol 32(4):397-413
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):381-393
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):905-915
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):149-160
19. Castaneda JA, Lim MJ, Cooper JD, Pearce DA (2008) Immune system irregularities in lysosomal storage disorders. Acta Neuropathol 115(2):159-174
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):23820-23828
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):7832-7841
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):1238-1247
23. Cleary MA, Wraith JE (1993) Management of mucopolysaccharidosis type III. Arch Dis Child 69(3):403-406
24. Codogno P, Meijer AJ (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12(Suppl 2):1509-1518
25. Colton CA (2009) Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4(4):399-418
26. Colton CA, Gilbert DL (1987) Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 223(2):284-288
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):93-100
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):965-973
29. Curtsinger JM, Mescher MF (2010) Inflammatory cytokines as a third signal for T cell activation. Curr Opin Immunol 22(3):333-340
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):1141-1151
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):757-762
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):4219-4230
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):5353-5357
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):619-628
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):2868-2876
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):978-990
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):266-268
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):13632-13637
39. Ekdahl CT, Kokaia Z, Lindvall O (2009) Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158(3):1021-1029
40. Eskelinen EL, Saftig P (2009) Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim Biophys Acta 1793(4):664-673
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):3607-3620
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):2293-2303
43. Gallucci S, Lolkema M, Matzinger P (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5(11):1249-1255
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):589-604
45. Greenwald RJ, Boussiotis VA, Lorsbach RB, Abbas AK, Sharpe AH (2001) CTLA-4 regulates induction of anergy in vivo. Immunity 14(2):145-155
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):737-742
47. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387-1394
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):3789-3796
49. Harr MW, Distelhorst CW (2010) Apoptosis and autophagy: decoding calcium signals that mediate life or death. Cold Spring Harb Perspect Biol 2(10):a005579
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):5140-5147
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):2721-2729
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):239-246
53. Hoffmann O, Braun JS, Becker D et al (2007) TLR2 mediates neuroinflammation and neuronal damage. J Immunol 178(10):6476-6481
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):37515-37524
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):111-122
56. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677-736
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):642-649
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):234-247
59. Johnson DE (1998) Regulation of survival pathways by IL-3 and induction of apoptosis following IL-3 withdrawal. Front Biosci 3:d313-324
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):5233-5239
61. Kawasaki N, Rademacher C, Paulson JC (2010) CD22 regulates adaptive and innate immune responses of B cells. J Innate Immun 3(4):411-419
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):e16269
63. Kehry MR, Hodgkin PD (1993) Helper T cells: delivery of cell contact and lymphokine-dependent signals to B cells. Semin Immunol 5(6):393-400
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 7:39
65. Kiselyov K, Jennigs JJ Jr, Rbaibi Y, Chu CT (2007) Autophagy, mitochondria and cell death in lysosomal storage diseases. Autophagy 3(3):259-262
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):4459-4466
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):1599-1604
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):3029-3034
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):50-57
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):e25717
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):673-682
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):134-142
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):2659-2667
74. Lehman TJ, Miller N, Norquist B, Underhill L, Keutzer J (2011) Diagnosis of the mucopolysaccharidoses. Rheumatology (Oxford) 50(Suppl 5):v41-48
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):291-300
76. Linsen L, Somers V, Stinissen P (2005) Immunoregulation of autoimmunity by natural killer T cells. Hum Immunol 66(12):1193-1202
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 962:318-331
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):2023-2034
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):439-448
80. Lutz MB (2004) IL-3 in dendritic cell development and function: a comparison with GM-CSF and IL-4. Immunobiology 209(1-2):79-87
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):23-32
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):212-223
83. Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12:991-1045
84. Matzinger P (2002) The danger model: a renewed sense of self. Science 296(5566):301-305
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):415-426
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):197-206
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):345-350
88. Mizushima N (2009) Physiological functions of autophagy. Curr Top Microbiol Immunol 335:71-84
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):703-706
90. Muenzer J (2004) The mucopolysaccharidoses: a heterogeneous group of disorders with variable pediatric presentations. J Pediatr 144(5 Suppl):S27-34
91. Muenzer J, Wraith JE, Clarke LA (2009) Mucopolysaccharidosis I: management and treatment guidelines. Pediatrics 123(1):19-29
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):211-221
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):12-27
94. Muhlebach MS, Wooten W, Muenzer J (2011) Respiratory manifestations in mucopolysaccharidoses. Paediatr Respir Rev 12(2):133-138
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):1566-1573
96. Neumann H, Kotter MR, Franklin RJ (2009) Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132(Pt 2):288-295
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):1902-1907
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):23111-23116
99. Olson JK, Miller SD (2004) Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173(6):3916-3924
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):13766-13771
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 5:43
102. Pamer E, Cresswell P (1998) Mechanisms of MHC class I-restricted antigen processing. Annu Rev Immunol 16:323-358
103. Parker DC (1993) T cell-dependent B cell activation. Annu Rev Immunol 11:331-360
104. Pasare C, Medzhitov R (2005) Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol 560:11-18
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):1099-1109
106. Piccinini AM, Midwood KS (2010) DAMPening inflammation by modulating TLR signalling. Mediators Inflamm doi: 10.1155/2010/672395
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):2748-2754
108. Ponder KP (2008) Immune response hinders therapy for lysosomal storage diseases. J Clin Invest 118(8):2686-2689
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):2669-2674
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):524-530
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):2580-2585
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):1415-1421
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):2256-2264
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):1563-1574
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):443-448
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):5521-5529
117. Seong SY, Matzinger P (2004) Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 4(6):469-478
118. Settembre C, Fraldi A, Jahreiss L et al (2008) A block of autophagy in lysosomal storage disorders. Hum Mol Genet 17(1):119-129
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):177-185
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):287-292
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):2540-2548
122. Strawbridge AB, Blum JS (2007) Autophagy in MHC class II antigen processing. Curr Opin Immunol 19(1):87-92
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):565-571
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):1010-1015
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):770-777
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):3804-3810
127. Trapani JA, Smyth MJ (2002) Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2(10):735-747
128. Van Kaer L, Parekh VV, Wu L (2011) Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res 343(1):43-55
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):623-633
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):612-622
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 1279:99-108
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):10954-10959
133. Walker JA, Smith KG (2008) CD22: an inhibitory enigma. Immunology 123(3):314-325
134. Walter L, Neumann H (2009) Role of microglia in neuronal degeneration and regeneration. Semin Immunopathol 31(4):513-525
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):2000-2007
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):e35787
137. Wraith JE (1995) The mucopolysaccharidoses: a clinical review and guide to management. Arch Dis Child 72(3):263-267
138. Wrenshall LE, Cerra FB, Carlson A, Bach FH, Platt JL (1991) Regulation of murine splenocyte responses by heparan sulfate. J Immunol 147(2):455-459
139. Wrenshall LE, Carlson A, Cerra FB, Platt JL (1994) Modulation of cytolytic T cell responses by heparan sulfate. Transplantation 57(7):1087-1094
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):871-880
141. Wrenshall LE, Stevens RB, Cerra FB, Platt JL (1999) Modulation of macrophage and B cell function by glycosaminoglycans. J Leukoc Biol 66(3):391-400
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):8425-8430
143. Wu L, Van Kaer L (2009) Natural killer T cells and autoimmune disease. Curr Mol Med 9(1):4-14
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):200-208
145. York IA, Rock KL (1996) Antigen processing and presentation by the class I major histocompatibility complex. Annu Rev Immunol 14:369-396
146. Yoshimori T (2004) Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 313(2):453-458
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):1176-1187
148. Zhou D, Mattner J, Cantu C 3rd et al (2004) Lysosomal glycosphingolipid recognition by NKT cells. Science 306(5702):1786-1789