Genomic Expression Analyses Reveal Lysosomal, Innate Immunity Proteins, as Disease Correlates in Murine Models of a Lysosomal Storage Disorder

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Alam, Md Suhail ^a   Getz, Michelle ^a   Safeukui, Innocent ^a   Yi, Sue ^a   Tamez, Pamela ^a,c   Shin, Jenny ^a   Velázquez, Peter ^a,b   Haldar, Kasturi ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ALPHA INTEGRIN; AXONEMAL DYNEIN; BIOLOGICAL MARKER; BLOOD CLOTTING FACTOR 10; CATHELICIDIN; CATHEPSIN D; CATHEPSIN S; CD68 ANTIGEN; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C4B; CYCLIN DEPENDENT KINASE INHIBITOR 1C; ELASTASE; FATTY ACID BINDING PROTEIN; FC RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEIN; HISTIDINE AMMONIALYASE; INTERLEUKIN 7 RECEPTOR; LECTIN; LYSOZYME; MACROPHAGE ELASTASE; MICROSOMAL AMINOPEPTIDASE; NUCLEAR PROTEIN; NUCLEOPROTEIN; OCTAMER TRANSCRIPTION FACTOR 6; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TUMOR NECROSIS FACTOR ALPHA;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BRAIN; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; GAUCHER DISEASE; GENE CONTROL; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LIVER; LYSOSOME; LYSOSOME STORAGE DISEASE; MOUSE; MOUSE STRAIN; NEUROLOGIC DISEASE; NEUTROPHIL; NIEMANN PICK DISEASE; NONHUMAN; PATHOPHYSIOLOGY; POINT MUTATION; SANDHOFF DISEASE; SPLEEN; UPREGULATION;

AGING; ANIMALS; BIOLOGICAL MARKERS; BRAIN; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; LIVER; LYSOSOMES; MALE; MICE; MICE, KNOCKOUT; MURAMIDASE; MUTATION; NEUTROPHIL INFILTRATION; NEUTROPHILS; NIEMANN-PICK DISEASE, TYPE C; PROTEINS; SPLEEN;

EID: 84867664574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048273     Document Type: Article

References (67)

1. Vanier MT, (2010) Niemann-Pick disease type C. Orphanet J Rare Dis. 5: 16.
2. Rimkunas VM, Graham MJ, Crooke RM, Liscum L, (2008) In vivo antisense oligonucleotide reduction of NPC1 expression as a novel mouse model for Niemann Pick type C- associated liver disease. Hepatology 47: 1504-1512.
3. Sayre NL, Rimkunas VM, Graham MJ, Crooke RM, Liscum L, (2010) Recovery from liver disease in a Niemann-Pick type C mouse model. J Lipid Res 51: 2372-2383.
4. 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: 242-251.
5. Vazquez MC, Del Pozo T, Robledo FA, Carrasco G, Pavez L, et al. (2011) Alteration of gene expression profile in niemann-pick type C mice correlates with tissue damage and oxidative stress. PLoS One 6: e28777.
6. Liao G, Cheung S, Galeano J, Ji AX, Qin Q, et al. (2009) Allopregnanolone treatment delays cholesterol accumulation and reduces autophagic/lysosomal dysfunction and inflammation in Npc1-/- mouse brain. Brain Res 1270: 140-151.
7. Rimkunas VM, Graham MJ, Crooke RM, Liscum L, (2009) TNF-{alpha} plays a role in hepatocyte apoptosis in Niemann-Pick type C liver disease. J Lipid Res 50: 327-333.
8. Beltroy EP, Richardson JA, Horton JD, Turley SD, Dietschy JM, (2005) Cholesterol accumulation and liver cell death in mice with Niemann-Pick type C disease. Hepatology 42: 886-893.
9. 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: 1086-1100.
10. Schrantz N, Sagiv Y, Liu Y, Savage PB, Bendelac A, et al. (2007) The Niemann-Pick type C2 protein loads isoglobotrihexosylceramide onto CD1d molecules and contributes to the thymic selection of NKT cells. J Exp Med 204: 841-852.
11. Sagiv Y, Hudspeth K, Mattner J, Schrantz N, Stern RK, et al. (2006) Cutting edge: impaired glycosphingolipid trafficking and NKT cell development in mice lacking Niemann-Pick type C1 protein. J Immunol 177: 26-30.
12. 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: 887-903.
13. Liao G, Wen Z, Irizarry K, Huang Y, Mitsouras K, et al. (2010) Abnormal gene expression in cerebellum of Npc1-/- mice during postnatal development. Brain Res 1325: 128-140.
14. 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 doi:101093/hmg/dds126.
15. 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.
16. De Windt A, Rai M, Kytomaki L, Thelen KM, Lutjohann D, et al. (2007) Gene set enrichment analyses revealed several affected pathways in Niemann-pick disease type C fibroblasts. DNA Cell Biol 26: 665-671.
17. Tang Y, Leao IC, Coleman EM, Broughton RS, Hildreth JE, (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.
18. Watarai M, Makino S, Michikawa M, Yanagisawa K, Murakami S, et al. (2002) Macrophage plasma membrane cholesterol contributes to Brucella abortus infection of mice. Infect Immun 70: 4818-4825.
19. Goluszko P, Nowicki B, (2005) Membrane cholesterol: a crucial molecule affecting interactions of microbial pathogens with mammalian cells. Infect Immun 73: 7791-7796.
20. Coppens I, Sinai AP, Joiner KA, (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149: 167-180.
21. Gatfield J, Pieters J, (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288: 1647-1650.
22. Samuel BU, Mohandas N, Harrison T, McManus H, Rosse W, et al. (2001) The role of cholesterol and glycosylphosphatidylinositol-anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J Biol Chem 276: 29319-29329.
23. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, et al. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477: 340-343.
24. Cote M, Misasi J, Ren T, Bruchez A, Lee K, et al. (2011) Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477: 344-348.
25. Tsolis RM, Kingsley RA, Townsend SM, Ficht TA, Adams LG, et al. (1999) Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 473: 261-274.
26. Haraga A, Ohlson MB, Miller SI, (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6: 53-66.
27. Monack DM, Bouley DM, Falkow S, (2004) Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J Exp Med 199: 231-241.
28. Li H, Repa JJ, Valasek MA, Beltroy EP, Turley SD, et al. (2005) Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick type C disease. J Neuropathol Exp Neurol 64: 323-333.
29. Parra J, Klein AD, Castro J, Morales MG, Mosqueira M, et al. (2011) Npc1 deficiency in the C57BL/6J genetic background enhances Niemann-Pick disease type C spleen pathology. Biochem Biophys Res Commun 413: 400-406.
30. Maue RA, Burgess RW, Wang B, Wooley CM, Seburn KL, et al. (2012) A novel mouse model of Niemann-Pick type C disease carrying a D1005G-Npc1 mutation comparable to commonly observed human mutations. Hum Mol Genet 21: 730-750.
31. Voikar V, Rauvala H, Ikonen E, (2002) Cognitive deficit and development of motor impairment in a mouse model of Niemann-Pick type C disease. Behav Brain Res 132: 1-10.
32. Lynn DJ, Winsor GL, Chan C, Richard N, Laird MR, et al. (2008) InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol 4: 218.
33. Drummond RA, Brown GD, (2011) The role of Dectin-1 in the host defence against fungal infections. Curr Opin Microbiol 14: 392-399.
34. Lee KH, Ono M, Inui M, Yuasa T, Takai T, (2000) Stimulatory function of gp49A, a murine Ig-like receptor, in rat basophilic leukemia cells. J Immunol 165: 4970-4977.
35. Nakatsuji T, Gallo RL (2011) Antimicrobial Peptides: Old Molecules with New Ideas. J Invest Dermatol.
36. Repa JJ, Li H, Frank-Cannon TC, Valasek MA, Turley SD, et al. (2007) Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J Neurosci 27: 14470-14480.
37. Hofmann E, Reichart U, Gausterer C, Guelly C, Meijer D, et al. (2010) Octamer-binding factor 6 (Oct-6/Pou3f1) is induced by interferon and contributes to dsRNA-mediated transcriptional responses. BMC Cell Biol 11: 61.
38. Jiang Q, Li WQ, Aiello FB, Klarmann KD, Keller JR, et al. (2005) Retroviral transduction of IL-7Ralpha into IL-7Ralpha-/- bone marrow progenitors: correction of lymphoid deficiency and induction of neutrophilia. Gene Ther 12: 1761-1768.
39. Kasten KR, Prakash PS, Unsinger J, Goetzman HS, England LG, et al. (2010) Interleukin-7 (IL-7) treatment accelerates neutrophil recruitment through gamma delta T-cell IL-17 production in a murine model of sepsis. Infect Immun 78: 4714-4722.
40. Parikh SS, Litherland SA, Clare-Salzler MJ, Li W, Gulig PA, et al. (2003) CapG(-/-) mice have specific host defense defects that render them more susceptible than CapG(+/+) mice to Listeria monocytogenes infection but not to Salmonella enterica serovar Typhimurium infection. Infect Immun 71: 6582-6590.
41. Ripoll VM, Irvine KM, Ravasi T, Sweet MJ, Hume DA, (2007) Gpnmb is induced in macrophages by IFN-gamma and lipopolysaccharide and acts as a feedback regulator of proinflammatory responses. J Immunol 178: 6557-6566.
42. Wraith JE, Baumgartner MR, Bembi B, Covanis A, Levade T, et al. (2009) Recommendations on the diagnosis and management of Niemann-Pick disease type C. Mol Genet Metab. 98: 152-165.
43. Yanjanin NM, Velez JI, Gropman A, King K, Bianconi SE, et al. (2010) Linear clinical progression, independent of age of onset, in Niemann-Pick disease, type C. Am J Med Genet B Neuropsychiatr Genet. 153B: 132-140.
44. Porter FD, Scherrer DE, Lanier MH, Langmade SJ, Molugu V, et al. (2010) Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Sci Transl Med 2: 56ra81.
45. 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: 765-772.
46. Liu B, Turley SD, Burns DK, Miller AM, Repa JJ, et al. (2009) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/- mouse. Proc Natl Acad Sci U S A 106: 2377-2382.
47. Davidson CD, Ali NF, Micsenyi MC, Stephney G, Renault S, et al. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 4: e6951.
48. Ramirez CM, Liu B, Taylor AM, Repa JJ, Burns DK, et al. (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.
49. Xie X, Brown MS, Shelton JM, Richardson JA, Goldstein JL, et al. (2011) Amino acid substitution in NPC1 that abolishes cholesterol binding reproduces phenotype of complete NPC1 deficiency in mice. Proc Natl Acad Sci U S A 108: 15330-15335.
50. Jethwaney D, Islam MR, Leidal KG, de Bernabe DB, Campbell KP, et al. (2007) Proteomic analysis of plasma membrane and secretory vesicles from human neutrophils. Proteome Sci 5: 12.
51. Lominadze G, Powell DW, Luerman GC, Link AJ, Ward RA, et al. (2005) Proteomic analysis of human neutrophil granules. Mol Cell Proteomics 4: 1503-1521.
52. Vitner EB, Dekel H, Zigdon H, Shachar T, Farfel-Becker T, et al. (2010) Altered expression and distribution of cathepsins in neuronopathic forms of Gaucher disease and in other sphingolipidoses. Hum Mol Genet 19: 3583-3590.
53. Myerowitz R, Lawson D, Mizukami H, Mi Y, Tifft CJ, et al. (2002) Molecular pathophysiology in Tay-Sachs and Sandhoff diseases as revealed by gene expression profiling. Hum Mol Genet 11: 1343-1350.
54. Cluzeau CV, Watkins-Chow DE, Fu R, Borate B, Yanjanin N, et al. (2012) Microarray expression analysis and identification of serum biomarkers for Niemann-Pick disease, type C1. Hum Mol Genet 21: 3632-3646.
55. Segal AW, (2005) How neutrophils kill microbes. Annu Rev Immunol 23: 197-223.
56. Kumar V, Sharma A, (2010) Neutrophils: Cinderella of innate immune system. Int Immunopharmacol 10: 1325-1334.
57. Nathan C, (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182.
58. Mantovani A, Cassatella MA, Costantini C, Jaillon S, (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11: 519-531.
59. El Kebir D, Filep JG, (2010) Role of neutrophil apoptosis in the resolution of inflammation. ScientificWorldJournal 10: 1731-1748.
60. Silva MT, (2011) Macrophage phagocytosis of neutrophils at inflammatory/infectious foci: a cooperative mechanism in the control of infection and infectious inflammation. J Leukoc Biol 89: 675-683.
61. Ajuebor MN, Hogaboam CM, Le T, Proudfoot AE, Swain MG, (2004) CCL3/MIP-1alpha is pro-inflammatory in murine T cell-mediated hepatitis by recruiting CCR1-expressing CD4(+) T cells to the liver. Eur J Immunol 34: 2907-2918.
62. Silverstein E, Friedland J, (1977) Elevated serum and spleen angiotensin converting enzyme and serum lysozyme in Gaucher's disease. Clin Chim Acta 74: 21-25.
63. DiRosario J, Divers E, Wang C, Etter J, Charrier A, et al. (2009) Innate and adaptive immune activation in the brain of MPS IIIB mouse model. J Neurosci Res 87: 978-990.
64. Ohmi K, Kudo LC, Ryazantsev S, Zhao HZ, Karsten SL, et al. (2009) Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy. Proc Natl Acad Sci U S A 106: 8332-8337.
65. Trexler AJ, Nilsson MR, (2007) The formation of amyloid fibrils from proteins in the lysozyme family. Curr Protein Pept Sci 8: 537-557.
66. Vieira MN, Forny-Germano L, Saraiva LM, Sebollela A, Martinez AM, et al. (2007) Soluble oligomers from a non-disease related protein mimic Abeta-induced tau hyperphosphorylation and neurodegeneration. J Neurochem 103: 736-748.
67. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, et al. (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277: 232-235.