Abnormal gene expression in cerebellum of Npc1-/- mice during postnatal development

Brain Research

Volumn 1325, Issue , 2010, Pages 128-140

  Liao, Guanghong ^a   Wen, Zhining ^c   Irizarry, Kristopher ^b   Huang, Ying ^b   Mitsouras, Katherine ^a   Darmani, Mariam ^a   Leon, Terry ^a   Shi, Leming ^c   Bi, Xiaoning ^a  

^a Western University of Health Sciences   (United States)

^b WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^c NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Cell adhesion; Cholesterol; Gene expression; Microarray; Niemann Pick type C disease

Indexed keywords

STEROID; TERPENOID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL ADHESION; CELL MOTILITY; CEREBELLUM; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNITY; KNOCKOUT MOUSE; LIPID TRANSPORT; MALE; MOUSE; NERVE DEGENERATION; NIEMANN PICK DISEASE; NONHUMAN; PATHOGENESIS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEROIDOGENESIS;

ANIMALS; CEREBELLUM; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOBLOTTING; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NIEMANN-PICK DISEASE, TYPE C; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; PROTEINS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

MUS;

EID: 77949912882     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.02.019     Document Type: Article

References (71)

1. Ahmad I., Lope-Piedrafita S., Bi X., Hicks C., Yao Y., Yu C., Chaitkin E., Howison C.M., Weberg L., Trouard T.P., and Erickson R.P. Allopregnanolone treatment, both as a single injection or repetitively, delays demyelination and enhances survival of Niemann-Pick C mice. J. Neurosci. Res. 82 (2005) 811-821
2. Akiyama H., Kawamata T., Yamada T., Tooyama I., Ishii T., and McGeer P.L. Expression of intercellular adhesion molecule (ICAM)-1 by a subset of astrocytes in Alzheimer disease and some other degenerative neurological disorders. Acta Neuropathol. 85 (1993) 628-634
3. Barres B.A., and Raff M.C. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361 (1993) 258-260
4. Barres B.A., and Raff M.C. Axonal control of oligodendrocyte development. J. Cell Biol. 147 (1999) 1123-1128
5. Baudry M., Yao Y., Simmons D., Liu J., and Bi X. Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp. Neurol. 184 (2003) 887-903
6. Bi X., and Liao G. Autophagic-lysosomal dysfunction and neurodegeneration in Niemann-Pick Type C mice: lipid starvation or indigestion?. Autophagy 3 (2007) 646-648
7. Boyles J.K., Pitas R.E., Wilson E., Mahley R.W., and Taylor J.M. Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 76 (1985) 1501-1513
8. Brecht W.J., Harris F.M., Chang S., Tesseur I., Yu G.Q., Xu Q., Dee Fish J., Wyss-Coray T., Buttini M., Mucke L., Mahley R.W., and Huang Y. Neuron-specific apolipoprotein e4 proteolysis is associated with increased tau phosphorylation in brains of transgenic mice. J. Neurosci. 24 (2004) 2527-2534
9. Canales R.D., Luo Y., Willey J.C., Austermiller B., Barbacioru C.C., Boysen C., Hunkapiller K., Jensen R.V., Knight C.R., Lee K.Y., Ma Y., Maqsodi B., Papallo A., Peters E.H., Poulter K., Ruppel P.L., Samaha R.R., Shi L., Yang W., Zhang L., and Goodsaid F.M. Evaluation of DNA microarray results with quantitative gene expression platforms. Nat. Biotechnol. 24 (2006) 1115-1122
10. Carstea E.D., Morris J.A., Coleman K.G., Loftus S.K., Zhang D., Cummings C., Gu J., Rosenfeld M.A., Pavan W.J., Krizman D.B., Nagle J., Polymeropoulos M.H., Sturley S.L., Ioannou Y.A., Higgins M.E., Comly M., Cooney A., Brown A., Kaneski C.R., Blanchette-Mackie E.J., Dwyer N.K., Neufeld E.B., Chang T.Y., Liscum L., Strauss III J.F., Ohno K., Zeigler M., Carmi R., Sokol J., Markie D., O'Neill R.R., van Diggelen O.P., Elleder M., Patterson M.C., Brady R.O., Vanier M.T., Pentchev P.G., and Tagle D.A. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277 (1997) 228-231
11. Cruz J.C., and Chang T.Y. Fate of endogenously synthesized cholesterol in Niemann-Pick type C1 cells. J. Biol. Chem. 275 (2000) 41309-41316
12. De Windt A., Rai M., Kytomaki L., Thelen K.M., Lutjohann D., Bernier L., Davignon J., Soini J., Pandolfo M., and Laaksonen R. Gene set enrichment analyses revealed several affected pathways in Niemann-Pick disease type C fibroblasts. DNA Cell Biol. 26 (2007) 665-671
13. Fang H., Harris S.C., Su Z., Chen M., Qian F., Shi L., Perkins R., and Tong W. ArrayTrack: an FDA and public genomic tool. Methods Mol. Biol. 563 (2009) 379-398
14. Fukuchi J., Song C., Ko A.L., and Liao S. Transcriptional regulation of farnesyl pyrophosphate synthase by liver X receptors. Steroids 68 (2003) 685-691
15. German D.C., Quintero E.M., Liang C., Xie C., and Dietschy J.M. Degeneration of neurons and glia in the Niemann-Pick C mouse is unrelated to the low-density lipoprotein receptor. Neuroscience 105 (2001) 999-1005
16. German D.C., Liang C.L., Song T., Yazdani U., Xie C., and Dietschy J.M. Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience 109 (2002) 437-450
17. Gong J.S., Kobayashi M., Hayashi H., Zou K., Sawamura N., Fujita S.C., Yanagisawa K., and Michikawa M. Apolipoprotein E (ApoE) isoform-dependent lipid release from astrocytes prepared from human ApoE3 and ApoE4 knock-in mice. J. Biol. Chem. 277 (2002) 29919-29926
18. Griffin L.D., Gong W., Verot L., and Mellon S.H. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med. 10 (2004) 704-711
19. Guo L., Lobenhofer E.K., Wang C., Shippy R., Harris S.C., Zhang L., Mei N., Chen T., Herman D., Goodsaid F.M., Hurban P., Phillips K.L., Xu J., Deng X., Sun Y.A., Tong W., Dragan Y.P., and Shi L. Rat toxicogenomic study reveals analytical consistency across microarray platforms. Nat. Biotechnol. 24 (2006) 1162-1169
20. Guo L., Li Q., Xia Q., Dial S., Chan P.C., and Fu P. Analysis of gene expression changes of drug metabolizing enzymes in the livers of F344 rats following oral treatment with kava extract. Food Chem. Toxicol. 47 (2009) 433-442
21. Jurevics H.A., Kidwai F.Z., and Morell P. Sources of cholesterol during development of the rat fetus and fetal organs. J. Lipid Res. 38 (1997) 723-733
22. Kadish I., Thibault O., Blalock E.M., Chen K.C., Gant J.C., Porter N.M., and Landfield P.W. Hippocampal and cognitive aging across the lifespan: a bioenergetic shift precedes and increased cholesterol trafficking parallels memory impairment. J. Neurosci. 29 (2009) 1805-1816
23. Karten B., Vance D.E., Campenot R.B., and Vance J.E. Cholesterol accumulates in cell bodies, but is decreased in distal axons, of Niemann-Pick C1-deficient neurons. J. Neurochem. 83 (2002) 1154-1163
24. Karten B., Vance D.E., Campenot R.B., and Vance J.E. Trafficking of cholesterol from cell bodies to distal axons in Niemann Pick C1-deficient neurons. J. Biol. Chem. 278 (2003) 4168-4175
25. Karten B., Hayashi H., Francis G.A., Campenot R.B., Vance D.E., and Vance J.E. Generation and function of astroglial lipoproteins from Niemann-Pick type C1-deficient mice. Biochem. J. 387 (2005) 779-788
26. Koh C.H., Peng Z.F., Ou K., Melendez A., Manikandan J., Qi R.Z., and Cheung N.S. Neuronal apoptosis mediated by inhibition of intracellular cholesterol transport: microarray and proteomics analyses in cultured murine cortical neurons. J. Cell Physiol. 211 (2007) 63-87
27. Korade Z., and Kenworthy A.K. Lipid rafts, cholesterol, and the brain. Neuropharmacology 55 (2008) 1265-1273
28. Li H., Repa J.J., Valasek M.A., Beltroy E.P., Turley S.D., German D.C., and Dietschy J.M. Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick type C disease. J. Neuropathol. Exp. Neurol. 64 (2005) 323-333
29. Liao G., Yao Y., Liu J., Yu Z., Cheung S., Xie A., Liang X., and Bi X. Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1-/- mouse brain. Am. J. Pathol. 171 (2007) 962-975
30. Liao G., Cheung S., Galeano J., Ji A.X., Qin Q., and Bi X. Allopregnanolone treatment delays cholesterol accumulation and reduces autophagic/lysosomal dysfunction and inflammation in Npc1-/- mouse brain. Brain Res. 1270 (2009) 140-151
31. Makgoba M.W., Sanders M.E., Ginther Luce G.E., Dustin M.L., Springer T.A., Clark E.A., Mannoni P., and Shaw S. ICAM-1 a ligand for LFA-1-dependent adhesion of B, T and myeloid cells. Nature 331 (1988) 86-88
32. Miklossy J., Doudet D.D., Schwab C., Yu S., McGeer E.G., and McGeer P.L. Role of ICAM-1 in persisting inflammation in Parkinson disease and MPTP monkeys. Exp. Neurol. 197 (2006) 275-283
33. Millard E.E., Gale S.E., Dudley N., Zhang J., Schaffer J.E., and Ory D.S. The sterol-sensing domain of the Niemann-Pick C1 (NPC1) protein regulates trafficking of low density lipoprotein cholesterol. J. Biol. Chem. 280 (2005) 28581-28590
34. Millat G., Marcais C., Tomasetto C., Chikh K., Fensom A.H., Harzer K., Wenger D.A., Ohno K., and Vanier M.T. Niemann-Pick C1 disease: correlations between NPC1 mutations, levels of NPC1 protein, and phenotypes emphasize the functional significance of the putative sterol-sensing domain and of the cysteine-rich luminal loop. Am. J. Hum. Genet. 68 (2001) 1373-1385
35. Miller R.M., Callahan L.M., Casaceli C., Chen L., Kiser G.L., Chui B., Kaysser-Kranich T.M., Sendera T.J., Palaniappan C., and Federoff H.J. Dysregulation of gene expression in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned mouse substantia nigra. J. Neurosci. 24 (2004) 7445-7454
36. Mondino A., and Jenkins M.K. Surface proteins involved in T cell costimulation. J. Leukoc. Biol. 55 (1994) 805-815
37. Naureckiene S., Sleat D.E., Lackland H., Fensom A., Vanier M.T., Wattiaux R., Jadot M., and Lobel P. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290 (2000) 2298-2301
38. Ong W.Y., Kumar U., Switzer R.C., Sidhu A., Suresh G., Hu C.Y., and Patel S.C. Neurodegeneration in Niemann-Pick type C disease mice. Exp. Brain Res. 141 (2001) 218-231
39. Ong W.Y., Hu C.Y., and Patel S.C. Apolipoprotein D in the Niemann-Pick type C disease mouse brain: an ultrastructural immunocytochemical analysis. J. Neurocytol. 31 (2002) 121-129
40. Pacheco C.D., Kunkel R., and Lieberman A.P. Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects. Hum. Mol. Genet. 16 (2007) 1495-1503
41. Patel S.C., Asotra K., Patel Y.C., McConathy W.J., Patel R.C., and Suresh S. Astrocytes synthesize and secrete the lipophilic ligand carrier apolipoprotein D. Neuroreport 6 (1995) 653-657
42. Pedotti P., t Hoen P.A., Vreugdenhil E., Schenk G.J., Vossen R.H., Ariyurek Y., de Hollander M., Kuiper R., van Ommen G.J., den Dunnen J.T., Boer J.M., and de Menezes R.X. Can subtle changes in gene expression be consistently detected with different microarray platforms?. BMC Genomics 9 (2008) 124
43. Pitas R.E., Boyles J.K., Lee S.H., Foss D., and Mahley R.W. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim. Biophys. Acta 917 (1987) 148-161
44. Poirier S., Prat A., Marcinkiewicz E., Paquin J., Chitramuthu B.P., Baranowski D., Cadieux B., Bennett H.P., and Seidah N.G. Implication of the proprotein convertase NARC-1/PCSK9 in the development of the nervous system. J. Neurochem. 98 (2006) 838-850
45. Poirier S., Mayer G., Benjannet S., Bergeron E., Marcinkiewicz J., Nassoury N., Mayer H., Nimpf J., Prat A., and Seidah N.G. The proprotein convertase PCSK9 induces the degradation of low density lipoprotein receptor (LDLR) and its closest family members VLDLR and ApoER2. J. Biol. Chem. 283 (2008) 2363-2372
46. Quan G., Xie C., Dietschy J.M., and Turley S.D. Ontogenesis and regulation of cholesterol metabolism in the central nervous system of the mouse. Brain Res. Dev. Brain Res. 146 (2003) 87-98
47. Rashid S., Curtis D.E., Garuti R., Anderson N.N., Bashmakov Y., Ho Y.K., Hammer R.E., Moon Y.A., and Horton J.D. Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5374-5379
48. Reddy J.V., Ganley I.G., and Pfeffer S.R. Clues to neuro-degeneration in Niemann-Pick Type C disease from global gene expression profiling. PLoS ONE 1 (2006) e19
49. Reid P.C., Lin S., Vanier M.T., Ohno-Iwashita Y., Harwood Jr. H.J., Hickey W.F., Chang C.C., and Chang T.Y. Partial blockage of sterol biosynthesis with a squalene synthase inhibitor in early postnatal Niemann-Pick type C npcnih null mice brains reduces neuronal cholesterol accumulation, abrogates astrogliosis, but may inhibit myelin maturation. J. Neurosci. Methods 168 (2008) 15-25
50. Reilly J.F., Martinez S.D., Mickey G., and Maher P.A. A novel role for farnesyl pyrophosphate synthase in fibroblast growth factor-mediated signal transduction. Biochem. J. 366 (2002) 501-510
51. Repa J.J., Li H., Frank-Cannon T.C., Valasek M.A., Turley S.D., Tansey M.G., and Dietschy J.M. Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J. Neurosci. 27 (2007) 14470-14480
52. Ribeiro I., Marcao A., Amaral O., Sa Miranda M.C., Vanier M.T., and Millat G. Niemann-Pick type C disease: NPC1 mutations associated with severe and mild cellular cholesterol trafficking alterations. Hum. Genet. 109 (2001) 24-32
53. Rollins B., Martin M.V., Sequeira P.A., Moon E.A., Morgan L.Z., Watson S.J., Schatzberg A., Akil H., Myers R.M., Jones E.G., Wallace D.C., Bunney W.E., and Vawter M.P. Mitochondrial variants in schizophrenia, bipolar disorder, and major depressive disorder. PLoS One 4 (2009) e4913
54. Satoh J., Lee Y.B., and Kim S.U. T-cell costimulatory molecules B7-1 (CD80) and B7-2 (CD86) are expressed in human microglia but not in astrocytes in culture. Brain Res. 704 (1995) 92-96
55. Schedin S., Pentchev P.G., Brunk U., and Dallner G. Changes in the levels of dolichol and dolichyl phosphate in a murine model of Niemann-Pick's type C disease. J. Neurochem. 65 (1995) 670-676
56. Schedin S., Nilsson M., Chojnacki T., and Dallner G. Alterations in the biosynthesis of cholesterol, dolichol and dolichyl-P in the genetic cholesterol homeostasis disorder, Niemann-Pick type C disease. Biochim. Biophys. Acta 1394 (1998) 177-186
57. Shi L., Tong W., Fang H., Scherf U., Han J., Puri R.K., Frueh F.W., Goodsaid F.M., Guo L., Su Z., Han T., Fuscoe J.C., Xu Z.A., Patterson T.A., Hong H., Xie Q., Perkins R.G., Chen J.J., and Casciano D.A. Cross-platform comparability of microarray technology: intra-platform consistency and appropriate data analysis procedures are essential. BMC Bioinformatics 6 Suppl 2 (2005) S12
58. Shi L., Reid L.H., Jones W.D., Shippy R., Warrington J.A., Baker S.C., Collins P.J., de Longueville F., Kawasaki E.S., Lee K.Y., Luo Y., Sun Y.A., Willey J.C., Setterquist R.A., Fischer G.M., Tong W., Dragan Y.P., Dix D.J., Frueh F.W., Goodsaid F.M., Herman D., Jensen R.V., Johnson C.D., Lobenhofer E.K., Puri R.K., Schrf U., Thierry-Mieg J., Wang C., Wilson M., Wolber P.K., Zhang L., Amur S., Bao W., Barbacioru C.C., Lucas A.B., Bertholet V., Boysen C., Bromley B., Brown D., Brunner A., Canales R., Cao X.M., Cebula T.A., Chen J.J., Cheng J., Chu T.M., Chudin E., Corson J., Corton J.C., Croner L.J., Davies C., Davison T.S., Delenstarr G., Deng X., Dorris D., Eklund A.C., Fan X.H., Fang H., Fulmer-Smentek S., Fuscoe J.C., Gallagher K., Ge W., Guo L., Guo X., Hager J., Haje P.K., Han J., Han T., Harbottle H.C., Harris S.C., Hatchwell E., Hauser C.A., Hester S., Hong H., Hurban P., Jackson S.A., Ji H., Knight C.R., Kuo W.P., LeClerc J.E., Levy S., Li Q.Z., Liu C., Liu Y., Lombardi M.J., Ma Y., Magnuson S.R., Maqsodi B., McDaniel T., Mei N., Myklebost O., Ning B., Novoradovskaya N., Orr M.S., Osborn T.W., Papallo A., Patterson T.A., Perkins R.G., Peters E.H., Peterson R., Philips K.L., Pine P.S., Pusztai L., Qian F., Ren H., Rosen M., Rosenzweig B.A., Samaha R.R., Schena M., Schroth G.P., Shchegrova S., Smith D.D., Staedtler F., Su Z., Sun H., Szallasi Z., Tezak Z., Thierry-Mieg D., Thompson K.L., Tikhonova I., Turpaz Y., Vallanat B., Van C., Walker S.J., Wang S.J., Wang Y., Wolfinger R., Wong A., Wu J., Xiao C., Xie Q., Xu J., Yang W., Zhong S., Zong Y., and Slikker Jr. W. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 24 (2006) 1151-1161
59. Shi L., Jones W.D., Jensen R.V., Harris S.C., Perkins R.G., Goodsaid F.M., Guo L., Croner L.J., Boysen C., Fang H., Qian F., Amur S., Bao W., Barbacioru C.C., Bertholet V., Cao X.M., Chu T.M., Collins P.J., Fan X.H., Frueh F.W., Fuscoe J.C., Guo X., Han J., Herman D., Hong H., Kawasaki E.S., Li Q.Z., Luo Y., Ma Y., Mei N., Peterson R.L., Puri R.K., Shippy R., Su Z., Sun Y.A., Sun H., Thorn B., Turpaz Y., Wang C., Wang S.J., Warrington J.A., Willey J.C., Wu J., Xie Q., Zhang L., Zhong S., Wolfinger R.D., and Tong W. The balance of reproducibility, sensitivity, and specificity of lists of differentially expressed genes in microarray studies. BMC Bioinformatics 9 Suppl 9 (2008) S10
60. Storch J., and Xu Z. Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochim. Biophys. Acta 1791 (2009) 671-678
61. Suresh S., Yan Z., Patel R.C., Patel Y.C., and Patel S.C. Cellular cholesterol storage in the Niemann-Pick disease type C mouse is associated with increased expression and defective processing of apolipoprotein D. J. Neurochem. 70 (1998) 242-251
62. Sutherland G.T., Matigian N.A., Chalk A.M., Anderson M.J., Silburn P.A., Mackay-Sim A., Wells C.A., and Mellick G.D. A cross-study transcriptional analysis of Parkinson's disease. PLoS One 4 (2009) e4955
63. Takikita S., Fukuda T., Mohri I., Yagi T., and Suzuki K. Perturbed myelination process of premyelinating oligodendrocyte in Niemann-Pick type C mouse. J. Neuropathol. Exp. Neurol. 63 (2004) 660-673
64. Tong W., Cao X., Harris S., Sun H., Fang H., Fuscoe J., Harris A., Hong H., Xie Q., Perkins R., Shi L., and Casciano D. ArrayTrack-supporting toxicogenomic research at the U.S. Food and Drug Administration National Center for Toxicological Research. Environ. Health Perspect. 111 (2003) 1819-1826
65. Turley S.D., Burns D.K., Rosenfeld C.R., and Dietschy J.M. Brain does not utilize low density lipoprotein-cholesterol during fetal and neonatal development in the sheep. J. Lipid Res. 37 (1996) 1953-1961
66. Wang L., Schuster G.U., Hultenby K., Zhang Q., Andersson S., and Gustafsson J.A. Liver X receptors in the central nervous system: from lipid homeostasis to neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 13878-13883
67. Watari H., Blanchette-Mackie E.J., Dwyer N.K., Sun G., Glick J.M., Patel S., Neufeld E.B., Pentchev P.G., and Strauss III J.F. NPC1-containing compartment of human granulosa-lutein cells: a role in the intracellular trafficking of cholesterol supporting steroidogenesis. Exp. Cell Res. 255 (2000) 56-66
68. Weisgraber K.H., Roses A.D., and Strittmatter W.J. The role of apolipoprotein E in the nervous system. Curr. Opin. Lipidol. 5 (1994) 110-116
69. Xie C., Burns D.K., Turley S.D., and Dietschy J.M. Cholesterol is sequestered in the brains of mice with Niemann-Pick type C disease but turnover is increased. J. Neuropathol. Exp. Neurol. 59 (2000) 1106-1117
70. Yanagimoto C., Harada M., Kumemura H., Koga H., Kawaguchi T., Terada K., Hanada S., Taniguchi E., Koizumi Y., Koyota S., Ninomiya H., Ueno T., Sugiyama T., and Sata M. Niemann-Pick C1 protein transports copper to the secretory compartment from late endosomes where ATP7B resides. Exp. Cell Res. 315 (2009) 119-126
71. Yoshida K., Cleaveland E.S., Nagle J.W., French S., Yaswen L., Ohshima T., Brady R.O., Pentchev P.G., and Kulkarni A.B. Molecular cloning of the mouse apolipoprotein D gene and its upregulated expression in Niemann-Pick disease type C mouse model. DNA Cell Biol. 15 (1996) 873-882