Niemann-Pick Type C1 deficiency in microglia does not cause neuron death in vitro

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 9, 2011, Pages 1121-1129

  Peake, Kyle B ^a   Campenot, Robert B ^a   Vance, Dennis E ^a   Vance, Jean E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Interleukin 10; Microglia; Neurodegeneration; Niemann Pick Type C; Tumor necrosis factor

Indexed keywords

CHOLESTEROL; GLUTAMINASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; INTERLEUKIN 10; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL DEATH; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROGLIA; MOUSE; NERVE CELL; NIEMANN PICK DISEASE; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CELL DEATH; CHOLESTEROL; COCULTURE TECHNIQUES; CYTOKINES; MICE; MICROGLIA; NEURONS; NIEMANN-PICK DISEASE, TYPE C; NIEMANN-PICK DISEASES; OXIDATIVE STRESS; PHAGOCYTOSIS; PROTEINS;

MUS;

EID: 79960563360     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.06.003     Document Type: Article

References (65)

1. Peake K.B., Vance J.E. Defective cholesterol trafficking in Niemann-Pick C-deficient cells. FEBS Lett. 2010, 584:2731-2739.
2. Liscum L., Faust J.R. Low density lipoprotein (LDL)-mediated suppression of cholesterol synthesis and LDL uptake is defective in Niemann-Pick type C fibroblasts. J. Biol. Chem. 1987, 262:17002-17008.
3. Pentchev P.G., Comly M.E., Kruth H.S., Vanier M.T., Wenger D.A., Patel S., Brady R.O. A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl Acad. Sci. U. S. A. 1985, 82:8247-8251.
4. Karten B., Vance D.E., Campenot R.B., Vance J.E. Cholesterol accumulates in cell bodies, but is decreased in distal axons, of Niemann-Pick C1-deficient neurons. J. Neurochem. 2002, 83:1154-1163.
5. Karten B., Hayashi H., Francis G.A., Campenot R.B., Vance D.E., Vance J.E. Generation and function of astroglial lipoproteins from Niemann-Pick type C1-deficient mice. Biochem. J. 2005, 387:779-788.
6. Wang M.L., Motamed M., Infante R.E., Abi-Mosleh L., Kwon H.J., Brown M.S., Goldstein J.L. Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab. 2010, 12:166-173.
7. Sarna J.R., Larouche M., Marzban H., Sillitoe R.V., Rancourt D.E., Hawkes R. Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neurol. 2003, 456:279-291.
8. Li H., Repa J.J., Valasek M.A., Beltroy E.P., Turley S.D., German D.C., Dietschy J.M. Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick type C disease. J. Neuropathol. Exp. Neurol. 2005, 64:323-333.
9. Wu Y.P., Mizukami H., Matsuda J., Saito Y., Proia R.L., Suzuki K. Apoptosis accompanied by up-regulation of TNF-alpha death pathway genes in the brain of Niemann-Pick type C disease. Mol. Genet. Metab. 2005, 84:9-17.
10. Alvarez A.R., Klein A., Castro J., Cancino G.I., Amigo J., Mosqueira M., Vargas L.M., Yevenes L.F., Bronfman F.C., Zanlungo S. Imatinib therapy blocks cerebellar apoptosis and improves neurological symptoms in a mouse model of Niemann-Pick type C disease. FASEB J. 2008, 22:3617-3627.
11. Repa J.J., Li H., Frank-Cannon T.C., Valasek M.A., Turley S.D., Tansey M.G., Dietschy J.M. Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J. Neurosci. 2007, 27:14470-14480.
12. Amritraj A., Peake K., Kodam A., Salio C., Merighi A., Vance J.E., Kar S. Increased activity and altered subcellular distribution of lysosomal enzymes determine neuronal vulnerability in Niemann-Pick Type C1-deficient mice. Am. J. Pathol. 2009, 175:2540-2556.
13. Baudry M., Yao Y., Simmons D., Liu J., Bi X. Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp. Neurol. 2003, 184:887-903.
14. Chen G., Li H.M., Chen Y.R., Gu X.S., Duan S. Decreased estradiol release from astrocytes contributes to the neurodegeneration in a mouse model of Niemann-Pick disease type C. Glia 2007, 55:1509-1518.
15. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
16. McGlade-McCulloh E., Morrissey A.M., Norona F., Muller K.J. Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc. Natl Acad. Sci. U. S. A. 1989, 86:1093-1097.
17. Tanga F.Y., Raghavendra V., DeLeo J.A. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem. Int. 2004, 45:397-407.
18. Graeber M.B., Streit W.J., Kreutzberg G.W. Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J. Neurosci. Res. 1988, 21:18-24.
19. Giulian D., Chen J., Ingeman J.E., George J.K., Noponen M. The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J. Neurosci. 1989, 9:4416-4429.
20. Buttini M., Appel K., Sauter A., Gebicke-Haerter P.J., Boddeke H.W. Expression of tumor necrosis factor alpha after focal cerebral ischaemia in the rat. Neuroscience 1996, 71:1-16.
21. Nakamura Y., Si Q.S., Kataoka K. Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci. Res. 1999, 35:95-100.
22. Patrizio M., Levi G. Glutamate production by cultured microglia: differences between rat and mouse, enhancement by lipopolysaccharide and lack effect of HIV coat protein gp120 and depolarizing agents. Neurosci. Lett. 1994, 178:184-189.
23. Colton C.A., Gilbert D.L. Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett. 1987, 223:284-288.
24. Ballou L.R., Chao C.P., Holness M.A., Barker S.C., Raghow R. J. Biol. Chem. 1992, 267:20044-20050.
25. Lindholm D., Castren E., Kiefer R., Zafra F., Thoenen H. Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J. Cell Biol. 1992, 117:395-400.
26. Mizuno T., Sawada M., Marunouchi T., Suzumura A. Production of interleukin-10 by mouse glial cells in culture. Biochem. Biophys. Res. Commun. 1994, 205:1907-1915.
27. Nakajima K., Honda S., Tohyama Y., Imai Y., Kohsaka S., Kurihara T. Neurotrophin secretion from cultured microglia. J. Neurosci. Res. 2001, 65:322-331.
28. Colton C.A. Heterogeneity of microglial activation in the innate immune response in the brain. J. Neuroimmune Pharmacol. 2009, 4:399-418.
29. Dheen S.T., Kaur C., Ling E.A. Microglial activation and its implications in the brain diseases. Curr. Med. Chem. 2007, 14:1189-1197.
30. Wada R., Tifft C.J., Proia R.L. Microglial activation precedes acute neurodegeneration in Sandhoff disease and is suppressed by bone marrow transplantation. Proc. Natl Acad. Sci. U. S. A. 2000, 97:10954-10959.
31. Beers D.R., Henkel J.S., Xiao Q., Zhao W., Wang J., Yen A.A., Siklos L., McKercher S.R., Appel S.H. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. U. S. A. 2006, 103:16021-16026.
32. Enquist I.B., Lo Bianco C., Ooka A., Nilsson E., Mansson J.E., Ehinger M., Richter J., Brady R.O., Kirik D., Karlsson S. Murine models of acute neuronopathic Gaucher disease. Proc. Natl Acad. Sci. U. S. A. 2007, 104:17483-17488.
33. German D.C., Liang C.L., Song T., Yazdani U., Xie C., Dietschy J.M. Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience 2002, 109:437-450.
34. Bae J.S., Furuya S., Ahn S.J., Yi S.J., Hirabayashi Y., Jin H.K. Neuroglial activation in Niemann-Pick Type C mice is suppressed by intracerebral transplantation of bone marrow-derived mesenchymal stem cells. Neurosci. Lett. 2005, 381:234-236.
35. 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., Pentchev P.G., Pavan W.J. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 1997, 277:232-235.
36. Jafferali S., Dumont Y., Sotty F., Robitaille Y., Quirion R., Kar S. Insulin-like growth factor-I and its receptor in the frontal cortex, hippocampus, and cerebellum of normal human and alzheimer disease brains. Synapse 2000, 38:450-459.
37. Hawkes C., Kar S. Insulin-like growth factor-II/mannose-6-phosphate receptor: widespread distribution in neurons of the central nervous system including those expressing cholinergic phenotype. J. Comp. Neurol. 2003, 458:113-127.
38. Gong J.S., Kobayashi M., Hayashi H., Zou K., Sawamura N., Fujita S.C., Yanagisawa K., Michikawa M. Apolipoprotein E (ApoE) isoform-dependent lipid release from astrocytes prepared from human ApoE3 and ApoE4 knock-in mice. J. Biol. Chem. 2002, 277:29919-29926.
39. Saura J., Tusell J.M., Serratosa J. High-yield isolation of murine microglia by mild trypsinization. Glia 2003, 44:183-189.
40. Michikawa M., Yanagisawa K. Apolipoprotein E4 induces neuronal cell death under conditions of suppressed de novo cholesterol synthesis. J. Neurosci. Res. 1998, 54:58-67.
41. Liscum L., Ruggiero R.M., Faust J.R. The intracellular transport of low density-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J. Cell Biol. 1989, 108:1625-1636.
42. Mukherjee S., Zha X., Tabas I., Maxfield F.R. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 1998, 75:1915-1925.
43. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001, 357:593-615.
44. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4:181-189.
45. Takeuchi H., Jin S., Wang J., Zhang G., Kawanokuchi J., Kuno R., Sonobe Y., Mizuno T., Suzumura A. Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem. 2006, 281:21362-21368.
46. Mitrasinovic O.M., Perez G.V., Zhao F., Lee Y.L., Poon C., Murphy G.M. Overexpression of macrophage colony-stimulating factor receptor on microglial cells induces an inflammatory response. J. Biol. Chem. 2001, 276:30142-30149.
47. Hayashi H.H., Campenot R.B., Vance D.E., Vance J.E. Apolipoprotein E-containing lipoproteins protect neurons from apoptosis via a signaling pathway involving low-density lipoprotein receptor-related protein-1. J. Neurosci. 2007, 27:1933-1941.
48. Elrick M.J., Pacheco C.D., Yu T., Dadgar N., Shakkottai V.G., Ware C., Paulson H.L., Lieberman A.P. Conditional Niemann-Pick C mice demonstrate cell autonomous Purkinje cell neurodegeneration. Hum. Mol. Genet. 2010, 19:837-847.
49. Massengale M., Wagers A.J., Vogel H., Weissman I.L. Hematopoietic cells maintain hematopoietic fates upon entering the brain. J. Exp. Med. 2005, 201:1579-1589.
50. D'Mello C., Le T., Swain M.G. Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation. J. Neurosci. 2009, 29:2089-2102.
51. Imai Y., Ibata I., Ito D., Ohsawa K., Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 1996, 224:855-862.
52. Ito D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res. Mol. Brain Res. 1998, 57:1-9.
53. Sawada M., Kondo N., Suzumura A., Marunouchi T. Production of tumor necrosis factor-alpha by microglia and astrocytes in culture. Brain Res. 1989, 491:394-397.
54. Beltroy E.P., Richardson J.A., Horton J.D., Turley S.D., Dietschy J.M. Cholesterol accumulation and liver cell death in mice with Niemann-Pick type C disease. Hepatology 2005, 42:886-893.
55. Rimkunas V.M., Graham M.J., Crooke R.M., Liscum L. TNF-{alpha} plays a role in hepatocyte apoptosis in Niemann-Pick type C liver disease. J. Lipid Res. 2009, 50:327-333.
56. Lopez M.E., Klein A.D., Dimbil U.J., Scott M.P. Anatomically defined neuron-based rescue of neurodegenerative niemann-pick type C disorder. J. Neurosci. 2011, 31:4367-4378.
57. Bogdan C., Vodovotz Y., Nathan C. Macrophage deactivation by interleukin 10. J. Exp. Med. 1991, 174:1549-1555.
58. Wang P., Wu P., Siegel M.I., Egan R.W., Billah M.M. IL-10 inhibits transcription of cytokine genes in human peripheral blood mononuclear cells. J. Immunol. 1994, 153:811-816.
59. Di Santo E., Adami M., Bertorelli R., Ghezzi P. Systemic interleukin 10 administration inhibits brain tumor necrosis factor production in mice. Eur. J. Pharmacol. 1997, 336:197-202.
60. Sawada M., Suzumura A., Hosoya H., Marunouchi T., Nagatsu T. Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J. Neurochem. 1999, 72:1466-1471.
61. Keun W.P., Hwan G.L., Byung K.J., Yong B.L. Interleukin-10 endogenously expressed in microglia prevents lipopolysaccharide-induced neruondegeneration in the rat cerebral cortex in vivo. Exp. Mol. Med. 2007, 39:812-819.
62. Grilli M., Barbieri I., Basudev H., Brusa R., Casati C., Lozza G., Ongini E. Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage. Eur. J. Neurosci. 2000, 12:2265-2272.
63. Bachis A., Colangelo A.M., Vicini S., Doe P.P., De Bernardi M.A., Brooker G., Mocchetti I. Interleukin-10 prevents glutamate-mediated cerebellar granule cell death by blocking caspase-3-like activity. J. Neurosci. 2001, 21:3104-3112.
64. Ko D.C., Milenkovic L., Beier S.M., Manuel H., Buchanan J., Scott M.P. Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet. 2005, 1:81-95.
65. Smith D., Wallom K.L., Williams I.M., Jeyakumar M., Platt F.M. Beneficial effects of anti-inflammatory therapy in a mouse model of Niemann-Pick disease type C1. Neurobiol. Dis. 2009, 36:242-251.