Innate immune responses in the brain of sphingolipid lysosomal storage diseases

Biological Chemistry

Volumn 396, Issue 6-7, 2015, Pages 659-667

  Vitner, Einat B ^a   Futerman, Anthony H ^a   Platt, Nick ^b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Gaucher disease; Microglia; Neuroinflammation; Niemann pick type C disease; Sandhoff disease

Indexed keywords

SPHINGOLIPID;

GAUCHER DISEASE; GBA GENE; GENE; GENE MUTATION; HUMAN; INNATE IMMUNITY; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NIEMANN PICK DISEASE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SANDHOFF DISEASE; ANIMAL; BRAIN; IMMUNOLOGY; LIPIDOSIS; LYSOSOME STORAGE DISEASE;

ANIMALS; BRAIN; GAUCHER DISEASE; HUMANS; IMMUNITY, INNATE; LYSOSOMAL STORAGE DISEASES; NIEMANN-PICK DISEASE, TYPE C; SPHINGOLIPIDOSES;

EID: 84949645255     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0301     Document Type: Review

References (60)

1. Baudry, M., Yao, Y., Simmons, D., Liu, J., and Bi, X. (2003). Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp. Neurol. 184, 887-903.
2. Bellettato, C. M. and Scarpa, M. (2010). Pathophysiology of neuropathic lysosomal storage disorders. J. Inherit. Metab. Dis. 33, 347-362.
3. Borbon, I., Totenhagen, J., Fiorenza, M. T., Canterini, S., Ke, W., Trouard, T., and Erickson, R. P. (2012). Niemann-Pick C1 mice, a model of "juvenile Alzheimer's disease", with normal gene expression in neurons and fibrillary astrocytes show long term survival and delayed neurodegeneration. J. Alzheimers Dis. 30, 875-887.
4. Boven, L. A., van Meurs, M., Boot, R. G., Mehta, A., Boon, L., Aerts, J. M., and Laman, J. D. (2004). Gaucher cells demonstrate a distinct macrophage phenotype and resemble alternatively activated macrophages. Am. J. Clin. Pathol. 122, 359-369.
5. Burrow, T. A., Sun, Y., Prada, C. E., Bailey, L., Zhang, W., Brewer, A., Wu, S. W., Setchell, K. D. R., Witte, D., Cohen, M. B., et al. (2015). CNS, lung, and lymph node involvement in Gaucher disease type 3 after 11 years of therapy: clinical, histopathologic, and biochemical findings. Mol. Genet. Metab. 114, 233-241.
6. Chovatiya, R. and Medzhitov, R. (2014). Stress, inflammation, and defense of homeostasis. Mol. Cell 54, 281-288.
7. Cologna, S. M., Cluzeau, C. V. M., Yanjanin, N. M., Blank, P. S., Dail, M. K., Siebel, S., Toth, C. L., Wassif, C. A., Lieberman, A. P., and Porter, F. D. (2014). Human and mouse neuroinflammation markers in Niemann-Pick disease, type C1. J. Inherit. Metab. Dis. 37, 83-92.
8. Conradi, N. G., Sourander, P., Nilsson, O., Svennerholm, L., and Erikson, A. (1984). Neuropathology of the Norrbottnian type of Gaucher disease. Morphological and biochemical studies. Acta Neuropathol. 65, 99-109.
9. Conradi, N. G., Kalimo, H., and Sourander, P. (1988). Reactions of vessel walls and brain parenchyma to the accumulation of Gaucher cells in the Norrbottnian type (type III) of Gaucher disease. Acta Neuropathol. 75, 385-390.
10. Conradi, N., Kyllerman, M., Mansson, J. E., Percy, A. K., and Svennerholm, L. (1991). Late-infantile Gaucher disease in a child with myoclonus and bulbar signs: neuropathological and neurochemical findings. Acta Neuropathol. 82, 152-157.
11. Cox, T. M. and Cachon-Gonzalez, M. B. (2012). The cellular pathology of lysosomal diseases. J. Pathol. 226, 241-254.
12. Cox, T. M. and Schofield, J. P. (1997). Gaucher's disease: clinical features and natural history. Baillieres Clin. Haematol. 10, 657-689.
13. Enquist, I. B., Nilsson, E., Ooka, A., Månsson, J.-E., Olsson, K., Ehinger, M., Brady, R. O., Richter, J., and Karlsson, S. (2006). Effective cell and gene therapy in a murine model of Gaucher disease. Proc. Natl. Acad. Sci. USA 103, 13819-13824.
14. Enquist, I. B., Lo Bianco, C., Ooka, A., Nilsson, E., Månsson, J.-E., Ehinger, M., Richter, J., Brady, R. O., Kirik, D., and Karlsson, S. (2007). Murine models of acute neuronopathic Gaucher disease. Proc. Natl. Acad. Sci. USA 104, 17483-17488.
15. Farfel-Becker, T., Vitner, E. B., and Futerman, A. H. (2011a). Animal models for Gaucher disease research. Dis. Model Mech. 4, 746-752.
16. Farfel-Becker, T., Vitner, E. B., Pressey, S. N. R., Eilam, R., Cooper, J. D., and Futerman, A. H. (2011b). Spatial and temporal correlation between neuron loss and neuroinflammation in a mouse model of neuronopathic Gaucher disease. Hum. Mol. Genet. 20, 1375-1386.
17. Farfel-Becker, T., Vitner, E. B., Kelly, S. L., Bame, J. R., Duan, J., Shinder, V., Merrill, A. H., Dobrenis, K., and Futerman, A. H. (2014). Neuronal accumulation of glucosylceramide in a mouse model of neuronopathic Gaucher disease leads to neurodegeneration. Hum. Mol. Genet. 23, 843-854.
18. Gaucher, P. C. E. (1882). De l'epithelioma primitif de la rate. These de Paris.
19. Hickman, S. E., Kingery, N. D., Ohsumi, T. K., Borowsky, M. L., Wang, L.-C., Means, T. K., and El Khoury, J. (2013). The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16, 1896-1905.
20. Hong, Y. B., Kim, E. Y., and Jung, S.-C. (2006). Upregulation of proinflammatory cytokines in the fetal brain of the Gaucher mouse. J. Korean Med. Sci. 21, 733-738.
21. Jeyakumar, M., Thomas, R., Elliot-Smith, E., Smith, D. A., van der Spoel, A. C., d'Azzo, A., Perry, V. H., Butters, T. D., Dwek, R. A., and Platt, F. M. (2003). Central nervous system inflammation is a hallmark of pathogenesis in mouse models of GM1 and GM2 gangliosidosis. Brain 126, 974-987.
22. Jeyakumar, M., Smith, D. A., Williams, I. M., Borja, M. C., Neville, D. C. A., Butters, T. D., Dwek, R. A., and Platt, F. M. (2004). NSAIDs increase survival in the Sandhoff disease mouse: synergy with N-butyldeoxynojirimycin. Ann. Neurol. 56, 642-649.
23. Jeyakumar, M., Dwek, R. A., Butters, T. D., and Platt, F. M. (2005). Storage solutions: treating lysosomal disorders of the brain. Nat. Rev. Neurosci 6, 713-725.
24. Jmoudiak, M. and Futerman, A. H. (2005). Gaucher disease: pathological mechanisms and modern management. Br. J. Haematol. 129, 178-188.
25. Kanfer, J. N., Legler, G., Sullivan, J., Raghavan, S. S., and Mumford, R. A. (1975). The Gaucher mouse. Biochem. Biophys. Res. Commun. 67, 85-90.
26. Kang, T.-B., Yang, S.-H., Toth, B., Kovalenko, A., and Wallach, D. (2013). Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38, 27-40.
27. Kaye, E. M., Ullman, M. D., Wilson, E. R., and Barranger, J. A. (1986). Type 2 and type 3 Gaucher disease: a morphological and biochemical study. Ann. Neurol. 20, 223-230.
28. Kolter, T. and Sandhoff, K. (2006). Sphingolipid metabolism diseases. Biochim. Biophys. Acta 1758, 2057-2079.
29. Lahiri, S. and Futerman, A. H. (2007). The metabolism and function of sphingolipids and glycosphingolipids. Cell. Mol. Life Sci. 64, 2270-2284.
30. Lloyd-Evans, E., Morgan, A. J., He, X., Smith, D. A., Elliot-Smith, E., Sillence, D. J., Churchill, G. C., Schuchman, E. H., Galione, A., and Platt, F. M. (2008). Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247-1255.
31. McBrayer, M. and Nixon, R. A. (2013). Lysosome and calcium dysregulation in Alzheimer's disease: partners in crime. Biochem. Soc. Trans. 41, 1495-1502.
32. Moriwaki, K. and Chan, F. K. M. (2013). Necrosis-dependent and independent signaling of the RIP kinases in inflammation. Cytokine Growth Factor Rev. 25, 167-174.
33. Osellame, L. D., Rahim, A. A., Hargreaves, I. P., Gegg, M. E., Richard-Londt, A., Brandner, S., Waddington, S. N., Schapira, A. H. V., and Duchen, M. R. (2013). Mitochondria and quality control defects in a mouse model of Gaucher disease - links to Parkinson's disease. Cell Metab. 17, 941-953.
34. Pavlova, E. V., Wang, S. Z., Archer, J., Dekker, N., Aerts, J. M. F. G., Karlsson, S., and Cox, T. M. (2013). B cell lymphoma and myeloma in murine Gaucher's disease. J. Pathol. 231, 88-97.
35. Pekny, M. and Nilsson, M. (2005). Astrocyte activation and reactive gliosis. Glia 50, 427-434.
36. Pentchev, P. G., Comly, M. E., Kruth, H. S., Patel, S., Proestel, M., and Weintroub, H. (1986). The cholesterol storage disorder of the mutant BALB/c mouse. A primary genetic lesion closely linked to defective esterification of exogenously derived cholesterol and its relationship to human type C Niemann-Pick disease. J. Biol. Chem. 261, 2772-2777.
37. Platt, F. M. (2014). Sphingolipid lysosomal storage disorders. Nature 510, 68-75.
38. Platt, F. M., Boland, B., and van der Spoel, A. C. (2012). The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J. Cell Biol. 199, 723-734.
39. Pressey, S. N. R., Smith, D. A., Wong, A. M. S., Platt, F. M., and Cooper, J. D. (2012). Early glial activation, synaptic changes and axonal pathology in the thalamocortical system of Niemann-Pick type C1 mice. Neurobiol. Dis. 45, 1086-1100.
40. Rosenbaum, A. I. and Maxfield, F. R. (2011). Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J. Neurochem. 116, 789-795.
41. Sandhoff, K. and Harzer, K. (2013). Gangliosides and gangliosidoses: principles of molecular and metabolic pathogenesis. J. Neurosci. 33, 10195-10208.
42. Sango, K., Yamanaka, S., Hoffmann, A., Okuda, Y., Grinberg, A., Westphal, H., McDonald, M. P., Crawley, J. N., Sandhoff, K., Suzuki, K., et al. (1995). Mouse models of Tay-Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nat. Genet. 11, 170-176.
43. Schiffmann, R. and Vellodi, A. (2007). Neuronopathic Gaucher disease. In: Gaucher Disease, A. H. Futerman, and A. Zimran, eds. (Boca Raton: Taylor & Francis Group), pp. 175-196.
44. Schultz, M. L., Tecedor, L., Chang, M., and Davidson, B. L. (2011). Clarifying lysosomal storage diseases. Trends Neurosci. 34, 401-410.
45. Sidransky, E. (2004). Gaucher disease: complexity in a "simple" disorder. Mol. Genet. Metab. 83, 6-15.
46. Sidransky, E., Nalls, M. A., Aasly, J. O., Aharon-Peretz, J., Annesi, G., Barbosa, E. R., Bar-Shira, A., Berg, D., Bras, J., Brice, A., et al. (2009). Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N. Engl. J. Med. 361, 1651-1661.
47. Smith, D., Wallom, K.-L., Williams, I. M., Jeyakumar, M., and Platt, F. M. (2009). Beneficial effects of anti-inflammatory therapy in a mouse model of Niemann-Pick disease type C1. Neurobiol. Dis. 36, 242-251.
48. Streit, W. J., Mrak, R. E., and Griffin, W. S. T. (2004). Microglia and neuroinflammation: a pathological perspective. J. Neuroinflamm. 1, 14.
49. Takeuchi, O. and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820.
50. Vanier, M. T. (2010). Niemann-Pick disease type C. Orphanet J. Rare Dis. 5, 16.
51. Vitner, E. B., Farfel-Becker, T., Eilam, R., Biton, I., and Futerman, A. H. (2012). Contribution of brain inflammation to neuronal cell death in neuronopathic forms of Gaucher's disease. Brain 135, 1724-1735.
52. Vitner, E. B., Salomon, R., Farfel-Becker, T., Meshcheriakova, A., Ali, M., Klein, A. D., Platt, F. M., Cox, T. M., and Futerman, A. H. (2014). RIPK3 as a potential therapeutic target for Gaucher's disease. Nat. Med. 20, 204-208.
53. Wada, R., Tifft, C. J., and Proia, R. L. (2000). Microglial activation precedes acute neurodegeneration in Sandhoff disease and is suppressed by bone marrow transplantation. Proc. Natl. Acad. Sci. USA 97, 10954-10959.
54. Westbroek, W., Gustafson, A. M., and Sidransky, E. (2011). Exploring the link between glucocerebrosidase mutations and parkinsonism. Trends Mol. Med. 17, 485-493.
55. Williams, I. M., Wallom, K.-L., Smith, D. A., Al Eisa, N., Smith, C., and Platt, F. M. (2014). Improved neuroprotection using miglustat, curcumin and ibuprofen as a triple combination therapy in Niemann-Pick disease type C1 mice. Neurobiol. Dis. 67, 9-17.
56. Wong, K., Sidransky, E., Verma, A., Mixon, T., Sandberg, G. D., Wakefield, L. K., Morrison, A., Lwin, A., Colegial, C., Allman, J. M., et al. (2004). Neuropathology provides clues to the pathophysiology of Gaucher disease. Mol. Genet. Metab. 82, 192-207.
57. Wu, Y.-P. and Proia, R. L. (2004). Deletion of macrophageinflammatory protein 1 alpha retards neurodegeneration in Sandhoff disease mice. Proc. Natl. Acad. Sci. USA 101, 8425-8430.
58. Wynn, T. A., Chawla, A., and Pollard, J. W. (2013). Macrophage biology in development, homeostasis and disease. Nature 496, 445-455.
59. Zhang, M., Strnatka, D., Donohue, C., Hallows, J. L., Vincent, I., and Erickson, R. P. (2008). Astrocyte-only Npc1 reduces neuronal cholesterol and triples life span of Npc1-/-mice. J. Neurosci. Res. 86, 2848-2856.
60. Zipp, F. and Aktas, O. (2006). The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci. 29, 518-527.