Human and mouse neuroinflammation markers in Niemann‐Pick disease, type C1
dc.contributor.author | Cologna, Stephanie M. | |
dc.contributor.author | Cluzeau, Celine V. M. | |
dc.contributor.author | Yanjanin, Nicole M. | |
dc.contributor.author | Blank, Paul S. | |
dc.contributor.author | Dail, Michelle K. | |
dc.contributor.author | Siebel, Stephan | |
dc.contributor.author | Toth, Cynthia L. | |
dc.contributor.author | Wassif, Christopher A. | |
dc.contributor.author | Lieberman, Andrew P. | |
dc.contributor.author | Porter, Forbes D. | |
dc.date.accessioned | 2019-01-15T20:30:50Z | |
dc.date.available | 2019-01-15T20:30:50Z | |
dc.date.issued | 2014-01 | |
dc.identifier.citation | Cologna, Stephanie M.; Cluzeau, Celine V. M.; Yanjanin, Nicole M.; Blank, Paul S.; Dail, Michelle K.; Siebel, Stephan; Toth, Cynthia L.; Wassif, Christopher A.; Lieberman, Andrew P.; Porter, Forbes D. (2014). "Human and mouse neuroinflammation markers in Niemann‐Pick disease, type C1." Journal of Inherited Metabolic Disease 37(1): 83-92. | |
dc.identifier.issn | 0141-8955 | |
dc.identifier.issn | 1573-2665 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/147148 | |
dc.description.abstract | Niemann‐Pick disease, type C1 (NPC1) is an autosomal recessive lipid storage disorder in which a pathological cascade, including neuroinflammation occurs. While data demonstrating neuroinflammation is prevalent in mouse models, data from NPC1 patients is lacking. The current study focuses on identifying potential markers of neuroinflammation in NPC1 from both the Npc1 mouse model and NPC1 patients. We identified in the mouse model significant changes in expression of genes associated with inflammation and compared these results to the pattern of expression in human cortex and cerebellar tissue. From gene expression array analysis, complement 3 (C3) was increased in mouse and human post‐mortem NPC1 brain tissues. We also characterized protein levels of inflammatory markers in cerebrospinal fluid (CSF) from NPC1 patients and controls. We found increased levels of interleukin 3, chemokine (C‐X‐C motif) ligand 5, interleukin 16 and chemokine ligand 3 (CCL3), and decreased levels of interleukin 4, 10, 13 and 12p40 in CSF from NPC1 patients. CSF markers were evaluated with respect to phenotypic severity. Miglustat treatment in NPC1 patients slightly decreased IL‐3, IL‐10 and IL‐13 CSF levels; however, further studies are needed to establish a strong effect of miglustat on inflammation markers. The identification of inflammatory markers with altered levels in the cerebrospinal fluid of NPC1 patients may provide a means to follow secondary events in NPC1 disease during therapeutic trials. | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.publisher | Springer Netherlands | |
dc.title | Human and mouse neuroinflammation markers in Niemann‐Pick disease, type C1 | |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Medicine (General) | |
dc.subject.hlbtoplevel | Health Sciences | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/147148/1/jimd0083.pdf | |
dc.identifier.doi | 10.1007/s10545-013-9610-6 | |
dc.identifier.source | Journal of Inherited Metabolic Disease | |
dc.identifier.citedreference | Smith D, Wallom KL, Williams IM, Jeyakumar M, Platt FM ( 2009 ) Beneficial effects of anti‐inflammatory therapy in a mouse model of Niemann‐Pick disease type C1. Neurobiol Dis, 36 ( 2 ): 242 – 251, 10.1016/j.nbd.2009.07.010 -->. | |
dc.identifier.citedreference | Pineda M, Wraith JE, Mengel E, etal ( 2009 ) Miglustat in patients with Niemann‐Pick disease Type C (NP‐C): a multicenter observational retrospective cohort study. Mol Genet Metab, 98 ( 3 ): 243 – 249, 10.1016/j.ymgme.2009.07.003 -->. | |
dc.identifier.citedreference | Porter FD, Scherrer DE, Lanier MH, etal ( 2010 ) Cholesterol oxidation products are sensitive and specific blood‐based biomarkers for Niemann‐Pick C1 disease. Sci Trans Med, 2 ( 56 ): 56ra81, 10.1126/scitranslmed.3001417 -->. | |
dc.identifier.citedreference | Pressey SN, Smith DA, Wong AM, Platt FM, Cooper JD ( 2012 ) Early glial activation, synaptic changes and axonal pathology in the thalamocortical system of Niemann‐Pick type C1 mice. Neurobiol Dis, 45 ( 3 ): 1086 – 1100, 3657200 10.1016/j.nbd.2011.12.027 -->. | |
dc.identifier.citedreference | Ramirez CM, Liu B, Taylor AM, etal ( 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 ( 4 ): 309 – 315, 3065173 10.1203/PDR.0b013e3181ee4dd2 -->. | |
dc.identifier.citedreference | Ransohoff RM, Brown MA ( 2012 ) Innate immunity in the central nervous system. J Clin Invest, 122 ( 4 ): 1164 – 1171, 3314450 10.1172/JCI58644 -->. | |
dc.identifier.citedreference | Reddy JV, Ganley IG, Pfeffer SR ( 2006 ) Clues to neuro‐degeneration in Niemann‐Pick type C disease from global gene expression profiling. PLoS One, 1: e19, 1762405 10.1371/journal.pone.0000019 -->. | |
dc.identifier.citedreference | Repa JJ, Li H, Frank‐Cannon TC, etal ( 2007 ) Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J Neurosci, 27 ( 52 ): 14470 – 14480, 10.1523/JNEUROSCI.4823‐07.2007 -->. | |
dc.identifier.citedreference | Rubio‐Perez JM, Morillas‐Ruiz JM ( 2012 ) A review: inflammatory process in Alzheimer’s disease, role of cytokines. SciWorld J, 2012: 756357. | |
dc.identifier.citedreference | Sarna JR, Larouche M, Marzban H, Sillitoe RV, Rancourt DE, Hawkes R ( 2003 ) Patterned Purkinje cell degeneration in mouse models of Niemann‐Pick type C disease. J Comp Neurol, 456 ( 3 ): 279 – 291, 10.1002/cne.10522 -->. | |
dc.identifier.citedreference | Stein VM, Crooks A, Ding W, etal ( 2012 ) Miglustat improves purkinje cell survival and alters microglial phenotype in feline Niemann‐Pick disease type C. J Neuropathol Exp Neurol, 71 ( 5 ): 434 – 448, 3352323 10.1097/NEN.0b013e31825414a6 -->. | |
dc.identifier.citedreference | Suk K ( 2010 ) Combined analysis of the glia secretome and the CSF proteome: neuroinflammation and novel biomarkers. Expert Rev proteomics, 7 ( 2 ): 263 – 274, 10.1586/epr.10.6 -->. | |
dc.identifier.citedreference | Suzuki K, Parker CC, Pentchev PG, etal ( 1995 ) Neurofibrillary tangles in Niemann‐Pick disease type C. Acta Neuropathol, 89 ( 3 ): 227 – 238, 10.1007/BF00309338 -->. | |
dc.identifier.citedreference | Vanier MT ( 2010 ) Niemann‐Pick disease type C. Orphanet J Rare Dis, 5: 16, 2902432 10.1186/1750‐1172‐5‐16 -->. | |
dc.identifier.citedreference | Vanier MT, Millat G ( 2003 ) Niemann‐Pick disease type C. Clin Genet, 64 ( 4 ): 269 – 281, 10.1034/j.1399‐0004.2003.00147.x -->. | |
dc.identifier.citedreference | Vazquez MC, Del Pozo T, Robledo FA, etal ( 2011 ) Alteration of gene expression profile in niemann‐pick type C mice correlates with tissue damage and oxidative stress. PLoS One, 6 ( 12 ): e28777, 3245218 10.1371/journal.pone.0028777 -->. | |
dc.identifier.citedreference | Veerhuis R, Nielsen HM, Tenner AJ ( 2011 ) Complement in the brain. Mol Immunol, 48 ( 14 ): 1592 – 1603, 3142281 10.1016/j.molimm.2011.04.003 -->. | |
dc.identifier.citedreference | Ward S, O’Donnell P, Fernandez S, Vite CH ( 2010 ) 2‐hydroxypropyl‐beta‐cyclodextrin raises hearing threshold in normal cats and in cats with Niemann‐Pick type C disease. Pediatr Res, 68 ( 1 ): 52 – 56, 2913583 10.1203/PDR.0b013e3181df4623 -->. | |
dc.identifier.citedreference | Wraith JE, Vecchio D, Jacklin E, etal ( 2010 ) Miglustat in adult and juvenile patients with Niemann‐Pick disease type C: long‐term data from a clinical trial. Mol Genet Metab, 99 ( 4 ): 351 – 357, 10.1016/j.ymgme.2009.12.006 -->. | |
dc.identifier.citedreference | Wu YP, Mizukami H, Matsuda J, Saito Y, Proia RL, Suzuki K ( 2005 ) Apoptosis accompanied by up‐regulation of TNF‐alpha death pathway genes in the brain of Niemann‐Pick type C disease. Mol Genet Metab, 84 ( 1 ): 9 – 17, 10.1016/j.ymgme.2004.08.017 -->. | |
dc.identifier.citedreference | 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, 10.1073/pnas.0400625101 -->. | |
dc.identifier.citedreference | Yanjanin NM, Velez JI, Gropman A, etal ( 2010 ) Linear clinical progression, independent of age of onset, in Niemann‐Pick disease, type C. Am J Med Genet B Neuropsychiatr Genet, 153B ( 1 ): 132 – 140, 2798912 | |
dc.identifier.citedreference | Zampieri S, Mellon SH, Butters TD, etal ( 2009 ) Oxidative stress in NPC1 deficient cells: protective effect of allopregnanolone. J Cell Mol Med, 13 ( 9B ): 3786 – 3796, 2832077 10.1111/j.1582‐4934.2008.00493.x -->. | |
dc.identifier.citedreference | Zervas M, Dobrenis K, Walkley SU ( 2001 ) Neurons in Niemann‐Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations. J Neuropathol Exp Neurol, 60 ( 1 ): 49 – 64. | |
dc.identifier.citedreference | Aqul A, Liu B, Ramirez CM, etal ( 2011 ) Unesterified cholesterol accumulation in late endosomes/lysosomes causes neurodegeneration and is prevented by driving cholesterol export from this compartment. J Neurosci, 31 ( 25 ): 9404 – 9413, 3134878 10.1523/JNEUROSCI.1317‐11.2011 -->. | |
dc.identifier.citedreference | Baudry M, Yao Y, Simmons D, Liu J, 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 ( 2 ): 887 – 903, 10.1016/S0014‐4886(03)00345‐5 -->. | |
dc.identifier.citedreference | Carstea ED, Morris JA, Coleman KG, etal ( 1997 ) Niemann‐Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science, 277 ( 5323 ): 228 – 231, 10.1126/science.277.5323.228 -->. | |
dc.identifier.citedreference | Chabot S, Williams G, Hamilton M, Sutherland G, Yong VW ( 1999 ) Mechanisms of IL‐10 production in human microglia‐T cell interaction. J Immunol, 162 ( 11 ): 6819 – 6828. | |
dc.identifier.citedreference | Davidson CD, Ali NF, Micsenyi MC, etal ( 2009 ) Chronic cyclodextrin treatment of murine Niemann‐Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One, 4 ( 9 ): e6951, 2736622 10.1371/journal.pone.0006951 -->. | |
dc.identifier.citedreference | Eng LF, Ghirnikar RS, Lee YL ( 2000 ) Glial fibrillary acidic protein: GFAP‐thirty‐one years (1969–2000). Neurochem Res, 25 ( 9–10 ): 1439 – 1451, 10.1023/A:1007677003387 -->. | |
dc.identifier.citedreference | Fu R, Yanjanin NM, Bianconi S, Pavan WJ, Porter FD ( 2010 ) Oxidative stress in Niemann‐Pick disease, type C. Mol Genet Metab, 101 ( 2–3 ): 214 – 218, 2950258 10.1016/j.ymgme.2010.06.018 -->. | |
dc.identifier.citedreference | Ganser GH, Hewett P ( 2010 ) An accurate substitution method for analyzing censored data. J Occup Environ Hyg, 7 ( 4 ): 233 – 244, 10.1080/15459621003609713 -->. | |
dc.identifier.citedreference | Graeber MB, Li W, Rodriguez ML ( 2011 ) Role of microglia in CNS inflammation. FEBS Lett, 585 ( 23 ): 3798 – 3805, 10.1016/j.febslet.2011.08.033 -->. | |
dc.identifier.citedreference | Henry CJ, Huang Y, Wynne AM, Godbout JP ( 2009 ) Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro‐inflammatory IL‐1beta and anti‐inflammatory IL‐10 cytokines. Brain Behav Immun, 23 ( 3 ): 309 – 317, 2692986 10.1016/j.bbi.2008.09.002 -->. | |
dc.identifier.citedreference | Klein A, Maldonado C, Vargas LM, etal ( 2011 ) Oxidative stress activates the c‐Abl/p73 proapoptotic pathway in Niemann‐Pick type C neurons. Neurobiol Dis, 41 ( 1 ): 209 – 218, 10.1016/j.nbd.2010.09.008 -->. | |
dc.identifier.citedreference | Kunisch E, Fuhrmann R, Roth A, Winter R, Lungershausen W, Kinne RW ( 2004 ) Macrophage specificity of three anti‐CD68 monoclonal antibodies (KP1, EBM11, and PGM1) widely used for immunohistochemistry and flow cytometry. Ann Rheum Dis, 63 ( 7 ): 774 – 784, 10.1136/ard.2003.013029 -->. | |
dc.identifier.citedreference | Langmade SJ, Gale SE, Frolov A, etal ( 2006 ) Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann‐Pick C disease. Proc Natl Acad Sci USA, 103 ( 37 ): 13807 – 13812, 10.1073/pnas.0606218103 -->. | |
dc.identifier.citedreference | Li H, Repa JJ, Valasek MA, etal ( 2005 ) Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann‐Pick type C disease. J Neuropathol Exp Neurol, 64 ( 4 ): 323 – 333. | |
dc.identifier.citedreference | Liao G, Wen Z, Irizarry K, etal ( 2010 ) Abnormal gene expression in cerebellum of Npc1−/− mice during postnatal development. Brain Res, 1325: 128 – 140, 10.1016/j.brainres.2010.02.019 -->. | |
dc.identifier.citedreference | Liu B, Ramirez CM, Miller AM, Repa JJ, Turley SD, Dietschy JM ( 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 ( 5 ): 933 – 944, 10.1194/jlr.M000257 -->. | |
dc.identifier.citedreference | Liu B, Turley SD, Burns DK, Miller AM, Repa JJ, Dietschy JM ( 2009 ) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1−/− mouse. Proc Natl Acad Sci USA, 106 ( 7 ): 2377 – 2382, 10.1073/pnas.0810895106 -->. | |
dc.identifier.citedreference | Livak KJ, Schmittgen TD ( 2001 ) Analysis of relative gene expression data using real‐time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods, 25 ( 4 ): 402 – 408, 10.1006/meth.2001.1262 -->. | |
dc.identifier.citedreference | Loftus SK, Morris JA, Carstea ED, etal ( 1997 ) Murine model of Niemann‐Pick C disease: mutation in a cholesterol homeostasis gene. Science, 277 ( 5323 ): 232 – 235, 10.1126/science.277.5323.232 -->. | |
dc.identifier.citedreference | Lopez ME, Klein AD, Hong J, Dimbil UJ, Scott MP ( 2012 ) Neuronal and epithelial cell rescue resolves chronic systemic inflammation in the lipid storage disorder Niemann‐Pick C. Hum Mol Genet, 21 ( 13 ): 2946 – 2960, 10.1093/hmg/dds126 -->. | |
dc.identifier.citedreference | Lopez ME, Klein AD, Scott MP ( 2012 ) Complement is dispensable for neurodegeneration in Niemann‐Pick disease type C. J Neuroinflamm, 9 ( 1 ): 216, 10.1186/1742‐2094‐9‐216 -->. | |
dc.identifier.citedreference | Love S, Bridges LR, Case CP ( 1995 ) Neurofibrillary tangles in Niemann‐Pick disease type C. Brain, 118 ( Pt 1 ): 119 – 129, 10.1093/brain/118.1.119 -->. | |
dc.identifier.citedreference | Marin‐Teva JL, Cuadros MA, Martin‐Oliva D, Navascues J ( 2012 ) Microglia and neuronal cell death. Neuron Glia Biol, 7 ( 1 ): 25 – 40, 10.1017/S1740925X12000014 -->. | |
dc.identifier.citedreference | Ong WY, Kumar U, Switzer RC, etal ( 2001 ) Neurodegeneration in Niemann‐Pick type C disease mice. Exp Brain Res, 141 ( 2 ): 218 – 231, 10.1007/s002210100870 -->. | |
dc.identifier.citedreference | Park KW, Lee DY, Joe EH, Kim SU, Jin BK ( 2005 ) Neuroprotective role of microglia expressing interleukin‐4. J Neurosci Res, 81 ( 3 ): 397 – 402, 10.1002/jnr.20483 -->. | |
dc.identifier.citedreference | Parra J, Klein AD, Castro J, etal ( 2011 ) Npc1 deficiency in the C57BL/6J genetic background enhances Niemann‐Pick disease type C spleen pathology. Biochem Biophys Res Commun, 413 ( 3 ): 400 – 406, 10.1016/j.bbrc.2011.08.096 -->. | |
dc.identifier.citedreference | Patterson MC, Vecchio D, Jacklin E, etal ( 2010 ) Long‐term miglustat therapy in children with Niemann‐Pick disease type C. J Child Neurol, 25 ( 3 ): 300 – 305, 10.1177/0883073809344222 -->. | |
dc.identifier.citedreference | Patterson MC, Vecchio D, Prady H, Abel L, Wraith JE ( 2007 ) Miglustat for treatment of Niemann‐Pick C disease: a randomised controlled study. Lancet Neurol, 6 ( 9 ): 765 – 772, 10.1016/S1474‐4422(07)70194‐1 -->. | |
dc.identifier.citedreference | Pentchev PG, Comly ME, Kruth HS, etal ( 1987 ) Group C Niemann‐Pick disease: faulty regulation of low‐density lipoprotein uptake and cholesterol storage in cultured fibroblasts. FASEB J, 1 ( 1 ): 40 – 45. | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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