Neuronal and epithelial cell rescue resolves chronic systemic inflammation in the lipid storage disorder Niemann-Pick C

Human Molecular Genetics

Volumn 21, Issue 13, 2012, Pages 2946-2960

  Lopez, Manuel E ^a,b   Klein, Andrés D ^a,b   Hong, Jennifer ^a,b   Dimbil, Ubah J ^a,b   Scott, Matthew P ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CHRONIC INFLAMMATION; EPITHELIUM CELL; GENE DELETION; IMMUNOCOMPETENT CELL; LIVER INJURY; LUNG PARENCHYMA; MACROPHAGE; MOUSE; NERVE CELL; NERVE DEGENERATION; NIEMANN PICK DISEASE; NONHUMAN; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SANDHOFF DISEASE; TISSUE INJURY;

ANIMALS; CENTRAL NERVOUS SYSTEM; CHEMOKINE CCL3; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; INFLAMMATION; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NEURONS; NIEMANN-PICK DISEASE, TYPE C; PROTEINS;

MUS;

EID: 84863521004     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds126     Document Type: Article

References (67)

1. Castaneda, J.A., Lim, M.J., Cooper, J.D. and Pearce, D.A. (2008) Immune system irregularities in lysosomal storage disorders. Acta Neuropathol., 115, 159-174.
2. Vitner, E.B., Platt, F.M. and Futerman, A.H. (2010) Common and uncommon pathogenic cascades in lysosomal storage diseases. J. Biol. Chem., 285, 20423-20427.
3. Futerman, A.H. and van Meer, G. (2004) The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol., 5, 554-565.
4. 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.
5. Parkinson-Lawrence, E.J., Shandala, T., Prodoehl, M., Plew, R., Borlace, G.N. and Brooks, D.A. (2010) Lysosomal storage disease: revealing lysosomal function and physiology. Physiology (Bethesda), 25, 102-115.
6. Pressey, S.N., Smith, D.A., Wong, A.M., 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.
7. Vanier, M.T. (2010) Niemann-Pick disease type C. Orphanet J. Rare Dis., 5, 16.
8. Kaye, E.M. (2011) Niemann-Pick C disease: not your average lysosomal storage disease. Neurology, 76, 316-317.
9. Maxfield, F.R. and Tabas, I. (2005) Role of cholesterol and lipid organization in disease. Nature, 438, 612-621.
10. Tang, Y., Leao, I.C., Coleman, E.M., Broughton, R.S. and Hildreth, J.E. (2009) Deficiency of niemann-pick type C-1 protein impairs release of human immunodeficiency virus type 1 and results in Gag accumulation in late endosomal/lysosomal compartments. J. Virol., 83, 7982-7995.
11. Sagiv, Y., Hudspeth, K., Mattner, J., Schrantz, N., Stern, R.K., Zhou, D., Savage, P.B., Teyton, L. and Bendelac, A. (2006) Cutting edge: impaired glycosphingolipid trafficking and NKT cell development in mice lacking Niemann-Pick type C1 protein. J. Immunol., 177, 26-30.
12. Liao, G., Wen, Z., Irizarry, K., Huang, Y., Mitsouras, K., Darmani, M., Leon, T., Shi, L. and Bi, X. (2010) Abnormal gene expression in cerebellum of Npc1-/- mice during postnatal development. Brain Res., 1325, 128-140.
13. Infante, R.E., Abi-Mosleh, L., Radhakrishnan, A., Dale, J.D., Brown, M.S. and Goldstein, J.L. (2008) Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J. Biol. Chem., 283, 1052-1063.
14. Ohgami, N., Ko, D.C., Thomas, M., Scott, M.P., Chang, C.C. and Chang, T.Y. (2004) Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain. Proc. Natl Acad. Sci. USA, 101, 12473-12478.
15. Storch, J. and Xu, Z. (2009) Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochim. Biophys. Acta, 1791, 671-678.
16. Infante, R.E., Wang, M.L., Radhakrishnan, A., Kwon, H.J., Brown, M.S. and Goldstein, J.L. (2008) NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc. Natl Acad. Sci. USA, 105, 15287-15292.
17. Cheruku, S.R., Xu, Z., Dutia, R., Lobel, P. and Storch, J. (2006) Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J. Biol. Chem., 281, 31594-31604.
18. Ko, D.C., Gordon, M.D., Jin, J.Y. and Scott, M.P. (2001) Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol. Biol. Cell, 12, 601-614.
19. Blom, T.S., Linder, M.D., Snow, K., Pihko, H., Hess, M.W., Jokitalo, E., Veckman, V., Syvanen, A.C. and Ikonen, E. (2003) Defective endocytic trafficking of NPC1 and NPC2 underlying infantile Niemann-Pick type C disease. Hum. Mol. Genet., 12, 257-272.
20. Fessler, M.B. and Parks, J.S. (2011) Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling. J. Immunol., 187, 1529-1535.
21. 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.
22. Zhang, J.R., Coleman, T., Langmade, S.J., Scherrer, D.E., Lane, L., Lanier, M.H., Feng, C., Sands, M.S., Schaffer, J.E., Semenkovich, C.F. et al. (2008) Niemann-Pick C1 protects against atherosclerosis in mice via regulation of macrophage intracellular cholesterol trafficking. J. Clin. Invest., 118, 2281-2290.
23. te Vruchte, D., Jeans, A., Platt, F.M. and Sillence, D.J. (2010) Glycosphingolipid storage leads to the enhanced degradation of the B cell receptor in Sandhoff disease mice. J. Inherit. Metab. Dis., 33, 261-270.
24. Loftus, S.K., Morris, J.A., Carstea, E.D., Gu, J.Z., Cummings, C., Brown, A., Ellison, J., Ohno, K., Rosenfeld, M.A., Tagle, D.A. et al. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science, 277, 232-235.
25. Somers, K.L., Wenger, D.A., Royals, M.A., Carstea, E.D., Connally, H.E., Kelly, T., Kimball, R. and Thrall, M.A. (1999) Complementation studies in human and feline Niemann-Pick type C disease. Mol. Genet. Metab., 66, 117-121.
26. Miyazaki, D., Nakamura, T., Toda, M., Cheung-Chau, K.W., Richardson, R.M. and Ono, S.J. (2005) Macrophage inflammatory protein-1alpha as a costimulatory signal for mast cell-mediated immediate hypersensitivity reactions. J. Clin. Invest., 115, 434-442.
27. Liu, B., Ramirez, C.M., Miller, A.M., Repa, J.J., Turley, S.D. and Dietschy, J.M. (2010) Cyclodextrin overcomes the transport defect in nearly every organ of NPC1 mice leading to excretion of sequestered cholesterol as bile acid. J. Lipid Res., 51, 933-944.
28. van Breemen, M.J., de Fost, M., Voerman, J.S., Laman, J.D., Boot, R.G., Maas, M., Hollak, C.E., Aerts, J.M. and Rezaee, F. (2007) Increased plasma macrophage inflammatory protein (MIP)-1alpha and MIP-1beta levels in type 1 Gaucher disease. Biochim. Biophys. Acta, 1772, 788-796.
29. Sano, R., Tessitore, A., Ingrassia, A. and d'Azzo, A. (2005) Chemokine-induced recruitment of genetically modified bone marrow cells into the CNS of GM1-gangliosidosis mice corrects neuronal pathology. Blood, 106, 2259-2268.
30. Ohmi, K., Greenberg, D.S., Rajavel, K.S., Ryazantsev, S., Li, H.H. and Neufeld, E.F. (2003) Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc. Natl Acad. Sci. USA, 100, 1902-1907.
31. Wu, Y.P. and Proia, R.L. (2004) Deletion of macrophage-inflammatory protein 1 alpha retards neurodegeneration in Sandhoff disease mice. Proc. Natl Acad. Sci. USA, 101, 8425-8430.
32. Dhami, R., Passini, M.A. and Schuchman, E.H. (2006) Identification of novel biomarkers for Niemann-Pick disease using gene expression analysis of acid sphingomyelinase knockout mice. Mol. Ther., 13, 556-564.
33. Gadola, S.D., Silk, J.D., Jeans, A., Illarionov, P.A., Salio, M., Besra, G.S., Dwek, R., Butters, T.D., Platt, F.M. and Cerundolo, V. (2006) Impaired selection of invariant natural killer T cells in diverse mouse models of glycosphingolipid lysosomal storage diseases. J. Exp. Med., 203, 2293-2303.
34. Ramirez, C.M., Liu, B., Taylor, A.M., Repa, J.J., Burns, D.K., Weinberg, A.G., Turley, S.D. and Dietschy, J.M. (2010) Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr. Res., 68, 309-315.
35. Lopez, M.E., Klein, A.D., Dimbil, U.J. and Scott, M.P. (2011) Anatomically defined neuron-based rescue of neurodegenerative Niemann-Pick type C disorder. J. Neurosci., 31, 4367-4378.
36. Tusher, V.G., Tibshirani, R. and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA, 98, 5116-5121.
37. 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.
38. Xu, Y.H., Jia, L., Quinn, B., Zamzow, M., Stringer, K., Aronow, B., Sun, Y., Zhang, W., Setchell, K.D. and Grabowski, G.A. (2011) Global gene expression profile progression in Gaucher disease mouse models. BMC Genomics, 12, 20.
39. Tuppo, E.E. and Arias, H.R. (2005) The role of inflammation in Alzheimer's disease. Int. J. Biochem. Cell Biol., 37, 289-305.
40. Ray, A. and Dittel, B.N. (2010) Isolation of mouse peritoneal cavity cells. J. Vis. Exp., 35, e1488.
41. Gordon, S. and Taylor, P.R. (2005) Monocyte and macrophage heterogeneity. Nat. Rev. Immunol., 5, 953-964.
42. Fang, K.M., Wang, Y.L., Huang, M.C., Sun, S.H., Cheng, H. and Tzeng, S.F. (2011) Expression of macrophage inflammatory protein-1alpha and monocyte chemoattractant protein-1 in glioma-infiltrating microglia: involvement of ATP and P2X receptor. J. Neurosci. Res., 89, 199-211.
43. Cook, D.N., Beck, M.A., Coffman, T.M., Kirby, S.L., Sheridan, J.F., Pragnell, I.B. and Smithies, O. (1995) Requirement of MIP-1 alpha for an inflammatory response to viral infection. Science, 269, 1583-1585.
44. Liu, B., Li, H., Repa, J.J., Turley, S.D. and Dietschy, J.M. (2008) Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res., 49, 663-669.
45. Parra, J., Klein, A.D., Castro, J., Morales, M.G., Mosqueira, M., Valencia, I., Cortes, V., Rigotti, A. and Zanlungo, S. (2011) Npc1 deficiency in the C57BL/6J genetic background enhances Niemann-Pick disease type C spleen pathology. Biochem. Biophys. Res. Commun., 413, 400-406.
46. Faustino, J.V., Wang, X., Johnson, C.E., Klibanov, A., Derugin, N., Wendland, M.F. and Vexler, Z.S. (2011) Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J. Neurosci., 31, 12992-13001.
47. Buiting, A.M. and Van Rooijen, N. (1994) Liposome mediated depletion of macrophages: an approach for fundamental studies. J. Drug Target, 2, 357-362.
48. Rong, Y., Wang, T. and Morgan, J.I. (2004) Identification of candidate Purkinje cell-specific markers by gene expression profiling in wild-type and pcd(3J) mice. Mol. Brain Res., 132, 128-145.
49. Sarna, J.R., Larouche, M., Marzban, H., Sillitoe, R.V., Rancourt, D.E. and Hawkes, R. (2003) Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neurol., 456, 279-291.
50. Perry, V.H. and O'Connor, V. (2008) C1q: the perfect complement for a synaptic feast? Nat. Rev. Neurosci., 9, 807-811.
51. Yu, T., Shakkottai, V.G., Chung, C. and Lieberman, A.P. (2011) Temporal and cell-specific deletion establishes that neuronal Npc1 deficiency is sufficient to mediate neurodegeneration. Hum. Mol. Genet., 20, 4440-4451.
52. Zu, T., Duvick, L.A., Kaytor, M.D., Berlinger, M.S., Zoghbi, H.Y., Clark, H.B. and Orr, H.T. (2004) Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J. Neurosci., 24, 8853-8861.
53. Ko, D.C., Milenkovic, L., Beier, S.M., Manuel, H., Buchanan, J. and Scott, M.P. (2005) Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet., 1, 81-95.
54. Beltroy, E.P., Liu, B., Dietschy, J.M. and Turley, S.D. (2007) Lysosomal unesterified cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J. Lipid. Res., 48, 869-881.
55. Palmeri, S., Tarugi, P., Sicurelli, F., Buccoliero, R., Malandrini, A., De Santi, M.M., Marciano, G., Battisti, C., Dotti, M.T., Calandra, S. et al. (2005) Lung involvement in Niemann-Pick disease type C1: improvement with bronchoalveolar lavage. Neurol. Sci., 26, 171-173.
56. Yerushalmi, B., Sokol, R.J., Narkewicz,M.R., Smith, D.,Ashmead, J.W. and Wenger, D.A. (2002) Niemann-pick disease type C in neonatal cholestasis at a North American Center. J. Pediatr. Gastroenterol. Nutr., 35, 44-50.
57. Hochedlinger, K., Yamada, Y., Beard, C. and Jaenisch, R. (2005) Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell, 121, 465-477.
58. Rimkunas, V.M., Graham, M.J., Crooke, R.M. and Liscum, L. (2009) TNF-{alpha} plays a role in hepatocyte apoptosis in Niemann-Pick type C liver disease. J. Lipid Res., 50, 327-333.
59. Serhan, C.N. and Savill, J. (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol., 6, 1191-1197.
60. Peake, K.B., Campenot, R.B., Vance, D.E. and Vance, J.E. (2011) Niemann-Pick Type C1 deficiency in microglia does not cause neuron death in vitro. Biochim. Biophys. Acta, 1812, 1121-1129.
61. Elrick, M.J., Pacheco, C.D., Yu, T., Dadgar, N., Shakkottai, V.G., Ware, C., Paulson, H.L. and Lieberman, A.P. (2010) Conditional Niemann-Pick C mice demonstrate cell autonomous Purkinje cell neurodegeneration. Hum. Mol. Genet., 19, 837-847.
62. Finkelstein, A., Kunis, G., Seksenyan, A., Ronen, A., Berkutzki, T., Azoulay, D., Koronyo-Hamaoui, M. and Schwartz, M. (2011) Abnormal changes in NKT cells, the IGF-1 axis, and liver pathology in an animal model of ALS. PLoS ONE, 6, e22374.
63. Patterson, M.C. (2003) A riddle wrapped in a mystery: understanding Niemann-Pick disease, type C. Neurologist, 9, 301-310.
64. Zhang, J. and Erickson, R.P. (2000) A modifier of Niemann Pick C 1 maps to mouse chromosome 19. Mamm. Genome, 11, 69-71.
65. Carette, J.E., Raaben, M., Wong, A.C., Herbert, A.S., Obernosterer, G., Mulherkar, N., Kuehne, A.I., Kranzusch, P.J., Griffin, A.M., Ruthel, G. et al. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature, 477, 340-343.
66. Edgar, R., Domrachev, M. and Lash, A.E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res., 30, 207-210.
67. Huang Da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.