Overexpression of the Insulin-Like Growth Factor II Receptor Increases β-Amyloid Production and Affects Cell Viability

REFERENCES

• Bertram L, Tanzi RE. 2012. The genetics of Alzheimer's disease. Prog Mol Biol Transl Sci 107:79–100. http://dx.doi.org/10.1016/B978-0-12-385883-2.00008-4.
   PubMed Web of Science ®Google Scholar
• Selkoe DJ. 2011. Alzheimer's disease. Cold Spring Harb Perspect Biol 3:a004457. http://dx.doi.org/10.1101/cshperspect.a004457.
   PubMed Web of Science ®Google Scholar
• Karch CM, Cruchaga C, Goate AM. 2014. Alzheimer's disease genetics: from the bench to the clinic. Neuron 83:11–26. http://dx.doi.org/10.1016/j.neuron.2014.05.041.
   PubMed Web of Science ®Google Scholar
• Nelson PT, Braak H, Markesbery WR. 2009. Neuropathology and cognitive impairment in Alzheimer disease: a complex but coherent relationship. J Neuropathol Exp Neurol 68:1–14. http://dx.doi.org/10.1097/NEN.0b013e3181919a48.
   PubMed Web of Science ®Google Scholar
• Thinakaran G, Koo EH. 2008. Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283:29615–29619. http://dx.doi.org/10.1074/jbc.R800019200.
   PubMed Web of Science ®Google Scholar
• Haass C, Kaether C, Thinakaran G, Sisodia S. 2012. Trafficking and proteolytic processing of APP. Cold Spring Harb Perspect Med 2:a006270. http://dx.doi.org/10.1101/cshperspect.a006270.
   PubMed Web of Science ®Google Scholar
• Ghosh P, Dahms NM, Kornfeld S. 2003. Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 4:202–212. http://dx.doi.org/10.1038/nrm1050.
   PubMed Web of Science ®Google Scholar
• Hawkes C, Kar S. 2004. The insulin-like growth factor-II/mannose-6-phosphate receptor: structure, distribution and function in the central nervous system. Brain Res Brain Res Rev 44:117–140. http://dx.doi.org/10.1016/j.brainresrev.2003.11.002.
   PubMedGoogle Scholar
• El-Shewy HM, Luttrell LM. 2009. Insulin-like growth factor-2/mannose-6 phosphate receptors. Vitam Horm 80:667–697. http://dx.doi.org/10.1016/S0083-6729(08)00624-9.
   PubMedGoogle Scholar
• Kar S, Seto D, Dore S, Hanisch U, Quirion R. 1997. Insulin-like growth factors-I and -II differentially regulate endogenous acetylcholine release from the rat hippocampal formation. Proc Natl Acad Sci U S A 94:14054–14059. http://dx.doi.org/10.1073/pnas.94.25.14054.
   PubMedGoogle Scholar
• Dikkes P, Hawkes C, Kar S, Lopez MF. 2007. Effect of kainic acid treatment on insulin-like growth factor-2 receptors in the IGF2-deficient adult mouse brain. Brain Res 1131:77–87. http://dx.doi.org/10.1016/j.brainres.2006.11.022.
   PubMedGoogle Scholar
• Couce ME, Weatherington AJ, McGinty JF. 1992. Expression of insulin-like growth factor-II (IGF-II) and IGF-II/mannose-6-phosphate receptor in the rat hippocampus: an in situ hybridization and immunocytochemical study. Endocrinology 131:1636–1642. http://dx.doi.org/10.1210/en.131.4.1636.
   PubMed Web of Science ®Google Scholar
• Kar S, Chabot JG, Quirion R. 1993. Quantitative autoradiographic localization of [125I]insulin-like growth factor I, [125I]insulin-like growth factor II, and [125I]insulin receptor binding sites in developing and adult rat brain. J Comp Neurol 333:375–397. http://dx.doi.org/10.1002/cne.903330306.
   PubMed Web of Science ®Google Scholar
• Kar S, Baccichet A, Quirion R, Poirier J. 1993. Entorhinal cortex lesion induces differential responses in [125I]insulin-like growth factor I, [125I]insulin-like growth factor II and [125I]insulin receptor binding sites in the rat hippocampal formation. Neuroscience 55:69–80. http://dx.doi.org/10.1016/0306-4522(93)90455-O.
   PubMedGoogle Scholar
• Stephenson DT, Rash K, Clemens JA. 1995. Increase in insulin-like growth factor II receptor within ischemic neurons following focal cerebral infarction. J Cereb Blood Flow Metab 15:1022–1031. http://dx.doi.org/10.1038/jcbfm.1995.128.
   PubMedGoogle Scholar
• Breese CR, D'Costa A, Rollins YD, Adams C, Booze RM, Sonntag WE, Leonard S. 1996. Expression of insulin-like growth factor-1 (IGF-1) and IGF-binding protein 2 (IGF-BP2) in the hippocampus following cytotoxic lesion of the dentate gyrus. J Comp Neurol 369:388–404.
   PubMedGoogle Scholar
• Walter HJ, Berry M, Hill DJ, Cwyfan-Hughes S, Holly JM, Logan A. 1999. Distinct sites of insulin-like growth factor (IGF)-II expression and localization in lesioned rat brain: possible roles of IGF binding proteins (IGFBPs) in the mediation of IGF-II activity. Endocrinology 140:520–532.
   PubMed Web of Science ®Google Scholar
• Hawkes C, Kar S. 2003. 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 458:113–127. http://dx.doi.org/10.1002/cne.10578.
   PubMedGoogle Scholar
• Hawkes C, Kabogo D, Amritraj A, Kar S. 2006. Up-regulation of cation-independent mannose 6-phosphate receptor and endosomal-lysosomal markers in surviving neurons after 192-IgG-saporin administrations into the adult rat brain. Am J Pathol 169:1140–1154. http://dx.doi.org/10.2353/ajpath.2006.051208.
   PubMedGoogle Scholar
• Konishi Y, Fushimi S, Shirabe T. 2005. Immunohistochemical distribution of cation-dependent mannose 6-phosphate receptors in the mouse central nervous system: comparison with that of cation-independent mannose 6-phophate receptors. Neurosci Lett 378:7–12. http://dx.doi.org/10.1016/j.neulet.2004.12.067.
   PubMedGoogle Scholar
• Pasternak SH, Callahan JW, Mahuran DJ. 2004. The role of the endosomal/lysosomal system in amyloid-beta production and the pathophysiology of Alzheimer's disease: reexamining the spatial paradox from a lysosomal perspective. J Alzheimers Dis 6:53–65.
   PubMed Web of Science ®Google Scholar
• Nixon RA, Cataldo AM. 2006. Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J Alzheimers Dis 9:277–289.
   PubMedGoogle Scholar
• Kar S, Poirier J, Guevara J, Dea D, Hawkes C, Robitaille Y, Quirion R. 2006. Cellular distribution of insulin-like growth factor-II/mannose-6-phosphate receptor in normal human brain and its alteration in Alzheimer's disease pathology. Neurobiol Aging 27:199–210. http://dx.doi.org/10.1016/j.neurobiolaging.2005.03.005.
   PubMedGoogle Scholar
• Cataldo AM, Peterhoff CM, Schmidt SD, Terio NB, Duff K, Beard M, Mathews PM, Nixon RA. 2004. Presenilin mutations in familial Alzheimer disease and transgenic mouse models accelerate neuronal lysosomal pathology. J Neuropathol Exp Neurol 63:821–830.
   PubMed Web of Science ®Google Scholar
• Amritraj A, Hawkes C, Phinney AL, Mount HT, Scott CD, Westaway D, Kar S. 2009. Altered levels and distribution of IGF-II/M6P receptor and lysosomal enzymes in mutant APP and APP + PS1 transgenic mouse brains. Neurobiol Aging 30:54–70. http://dx.doi.org/10.1016/j.neurobiolaging.2007.05.004.
   PubMedGoogle Scholar
• Watanabe H, Grubb JH, Sly WS. 1990. The overexpressed human 46-kDa mannose 6-phosphate receptor mediates endocytosis and sorting of beta-glucuronidase. Proc Natl Acad Sci U S A 87:8036–8040. http://dx.doi.org/10.1073/pnas.87.20.8036.
   PubMedGoogle Scholar
• Nolan CM, Kyle JW, Watanabe H, Sly WS. 1990. Binding of insulin-like growth factor II (IGF-II) by human cation-independent mannose 6-phosphate receptor/IGF-II receptor expressed in receptor-deficient mouse L cells. Cell Regul 1:197–213.
   PubMedGoogle Scholar
• Wood RJ, Hulett MD. 2008. Cell surface-expressed cation-independent mannose 6-phosphate receptor (CD222) binds enzymatically active heparanase independently of mannose 6-phosphate to promote extracellular matrix degradation. J Biol Chem 283:4165–4176. http://dx.doi.org/10.1074/jbc.M708723200.
   PubMedGoogle Scholar
• Motyka B, Korbutt G, Pinkoski MJ, Heibein JA, Caputo A, Hobman M, Barry M, Shostak I, Sawchuk T, Holmes CF, Gauldie J, Bleackley RC. 2000. Mannose 6-phosphate/insulin-like growth factor II receptor is a death receptor for granzyme B during cytotoxic T cell-induced apoptosis. Cell 103:491–500. http://dx.doi.org/10.1016/S0092-8674(00)00140-9.
   PubMed Web of Science ®Google Scholar
• Di Bacco A, Gill G. 2003. The secreted glycoprotein CREG inhibits cell growth dependent on the mannose-6-phosphate/insulin-like growth factor II receptor. Oncogene 22:5436–5445. http://dx.doi.org/10.1038/sj.onc.1206670.
   PubMed Web of Science ®Google Scholar
• Oshima A, Nolan CM, Kyle JW, Grubb JH, Sly WS. 1988. The human cation-independent mannose 6-phosphate receptor. Cloning and sequence of the full-length cDNA and expression of functional receptor in COS cells. J Biol Chem 263:2553–2562.
   Google Scholar
• Dutta D, Williamson CD, Cole NB, Donaldson JG. 2012. Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis. PLoS One 7:e45799. http://dx.doi.org/10.1371/journal.pone.0045799.
   PubMedGoogle Scholar
• Amritraj A, Wang Y, Revett TJ, Vergote D, Westaway D, Kar S. 2013. Role of cathepsin D in U18666A-induced neuronal cell death: potential implication in Niemann-Pick type C disease pathogenesis. J Biol Chem 288:3136–3152. http://dx.doi.org/10.1074/jbc.M112.412460.
   PubMed Web of Science ®Google Scholar
• Kreiling JL, Montgomery MA, Wheeler JR, Kopanic JL, Connelly CM, Zavorka ME, Allison JL, Macdonald RG. 2012. Dominant-negative effect of truncated mannose 6-phosphate/insulin-like growth factor II receptor species in cancer. FEBS J 279:2695–2713. http://dx.doi.org/10.1111/j.1742-4658.2012.08652.x.
   PubMedGoogle Scholar
• Grimm MO, Grimm HS, Tomic I, Beyreuther K, Hartmann T, Bergmann C. 2008. Independent inhibition of Alzheimer disease beta- and gamma-secretase cleavage by lowered cholesterol levels. J Biol Chem 283:11302–11311. http://dx.doi.org/10.1074/jbc.M801520200.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Park JH, Schaffer BS, Garmroudi F, MacDonald RG. 2000. Dimerization of the insulin-like growth factor II/mannose 6-phosphate receptor. J Biol Chem 275:18647–18656. http://dx.doi.org/10.1074/jbc.M001273200.
   PubMedGoogle Scholar
• Maulik M, Ghoshal B, Kim J, Wang Y, Yang J, Westaway D, Kar S. 2012. Mutant human APP exacerbates pathology in a mouse model of NPC and its reversal by a beta-cyclodextrin. Hum Mol Genet 21:4857–4875. http://dx.doi.org/10.1093/hmg/dds322.
   PubMed Web of Science ®Google Scholar
• Wang Y, Thinakaran G, Kar S. 2014. Overexpression of the IGF-II/M6P receptor in mouse fibroblast cell lines differentially alters expression profiles of genes involved in Alzheimer's disease-related pathology. PLoS One 9:e98057. http://dx.doi.org/10.1371/journal.pone.0098057.
   PubMedGoogle Scholar
• Hawkes C, Jhamandas JH, Harris KH, Fu W, MacDonald RG, Kar S. 2006. Single transmembrane domain insulin-like growth factor-II/mannose-6-phosphate receptor regulates central cholinergic function by activating a G-protein-sensitive, protein kinase C-dependent pathway. J Neurosci 26:585–596. http://dx.doi.org/10.1523/JNEUROSCI.2730-05.2006.
   PubMedGoogle Scholar
• Kojro E, Gimpl G, Lammich S, Marz W, Fahrenholz F. 2001. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc Natl Acad Sci U S A 98:5815–5820. http://dx.doi.org/10.1073/pnas.081612998.
   PubMed Web of Science ®Google Scholar
• Vetrivel KS, Cheng H, Lin W, Sakurai T, Li T, Nukina N, Wong PC, Xu H, Thinakaran G. 2004. Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J Biol Chem 279:44945–44954. http://dx.doi.org/10.1074/jbc.M407986200.
   PubMed Web of Science ®Google Scholar
• Wahrle S, Das P, Nyborg AC, McLendon C, Shoji M, Kawarabayashi T, Younkin LH, Younkin SG, Golde TE. 2002. Cholesterol-dependent gamma-secretase activity in buoyant cholesterol-rich membrane microdomains. Neurobiol Dis 9:11–23. http://dx.doi.org/10.1006/nbdi.2001.0470.
   PubMed Web of Science ®Google Scholar
• Ehehalt R, Keller P, Haass C, Thiele C, Simons K. 2003. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 160:113–123. http://dx.doi.org/10.1083/jcb.200207113.
   PubMed Web of Science ®Google Scholar
• Cheng H, Vetrivel KS, Gong P, Meckler X, Parent A, Thinakaran G. 2007. Mechanisms of disease: new therapeutic strategies for Alzheimer's disease–targeting APP processing in lipid rafts. Nat Clin Pract Neurol 3:374–382. http://dx.doi.org/10.1038/ncpneuro0549.
   PubMedGoogle Scholar
• Torgersen ML, Skretting G, van Deurs B, Sandvig K. 2001. Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 114:3737–3747.
   PubMed Web of Science ®Google Scholar
• Le PU, Nabi IR. 2003. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci 116:1059–1071. http://dx.doi.org/10.1242/jcs.00327.
   PubMed Web of Science ®Google Scholar
• Berger-Sweeney J, McPhie DL, Arters JA, Greenan J, Oster-Granite ML, Neve RL. 1999. Impairments in learning and memory accompanied by neurodegeneration in mice transgenic for the carboxyl-terminus of the amyloid precursor protein. Brain Res Mol Brain Res 66:150–162. http://dx.doi.org/10.1016/S0169-328X(99)00014-5.
   PubMedGoogle Scholar
• McPhie DL, Golde T, Eckman CB, Yager D, Brant JB, Neve RL. 2001. Beta-secretase cleavage of the amyloid precursor protein mediates neuronal apoptosis caused by familial Alzheimer's disease mutations. Brain Res Mol Brain Res 97:103–113. http://dx.doi.org/10.1016/S0169-328X(01)00294-7.
   PubMedGoogle Scholar
• Herbert JM, Seban E, Maffrand JP. 1990. Characterization of specific binding sites for [3H]-staurosporine on various protein kinases. Biochem Biophys Res Commun 171:189–195. http://dx.doi.org/10.1016/0006-291X(90)91375-3.
   PubMed Web of Science ®Google Scholar
• Ruegg UT, Burgess GM. 1989. Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends Pharmacol Sci 10:218–220. http://dx.doi.org/10.1016/0165-6147(89)90263-0.
   PubMed Web of Science ®Google Scholar
• Thinakaran G, Borchelt DR, Lee MK, Slunt HH, Spitzer L, Kim G, Ratovitsky T, Davenport F, Nordstedt C, Seeger M, Hardy J, Levey AI, Gandy SE, Jenkins NA, Copeland NG, Price DL, Sisodia SS. 1996. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17:181–190. http://dx.doi.org/10.1016/S0896-6273(00)80291-3.
   PubMed Web of Science ®Google Scholar
• Thinakaran G, Harris CL, Ratovitski T, Davenport F, Slunt HH, Price DL, Borchelt DR, Sisodia SS. 1997. Evidence that levels of presenilins (PS1 and PS2) are coordinately regulated by competition for limiting cellular factors. J Biol Chem 272:28415–28422. http://dx.doi.org/10.1074/jbc.272.45.28415.
   PubMed Web of Science ®Google Scholar
• Takasugi N, Tomita T, Hayashi I, Tsuruoka M, Niimura M, Takahashi Y, Thinakaran G, Iwatsubo T. 2003. The role of presenilin cofactors in the gamma-secretase complex. Nature 422:438–441. http://dx.doi.org/10.1038/nature01506.
   PubMed Web of Science ®Google Scholar
• Miners JS, Baig S, Palmer J, Palmer LE, Kehoe PG, Love S. 2008. Abeta-degrading enzymes in Alzheimer's disease. Brain Pathol 18:240–252. http://dx.doi.org/10.1111/j.1750-3639.2008.00132.x.
   PubMedGoogle Scholar
• Saido T, Leissring MA. 2012. Proteolytic degradation of amyloid beta-protein. Cold Spring Harb Perspect Med 2:a006379. http://dx.doi.org/10.1101/cshperspect.a006379.
   PubMed Web of Science ®Google Scholar
• Maulik M, Westaway D, Jhamandas JH, Kar S. 2013. Role of cholesterol in APP metabolism and its significance in Alzheimer's disease pathogenesis. Mol Neurobiol 47:37–63. http://dx.doi.org/10.1007/s12035-012-8337-y.
   PubMed Web of Science ®Google Scholar
• Hemming ML, Elias JE, Gygi SP, Selkoe DJ. 2009. Identification of beta-secretase (BACE1) substrates using quantitative proteomics. PLoS One 4:e8477. http://dx.doi.org/10.1371/journal.pone.0008477.
   PubMedGoogle Scholar
• Haque A, Banik NL, Ray SK. 2008. New insights into the roles of endolysosomal cathepsins in the pathogenesis of Alzheimer's disease: cathepsin inhibitors as potential therapeutics. CNS Neurol Disord Drug Targets 7:270–277. http://dx.doi.org/10.2174/187152708784936653.
   PubMedGoogle Scholar
• Yamashima T. 2013. Reconsider Alzheimer's disease by the “calpain-cathepsin hypothesis”–a perspective review. Prog Neurobiol 105:1–23. http://dx.doi.org/10.1016/j.pneurobio.2013.02.004.
   PubMed Web of Science ®Google Scholar
• Mathews PM, Guerra CB, Jiang Y, Grbovic OM, Kao BH, Schmidt SD, Dinakar R, Mercken M, Hille-Rehfeld A, Rohrer J, Mehta P, Cataldo AM, Nixon RA. 2002. Alzheimer's disease-related overexpression of the cation-dependent mannose 6-phosphate receptor increases Abeta secretion: role for altered lysosomal hydrolase distribution in beta-amyloidogenesis. J Biol Chem 277:5299–5307. http://dx.doi.org/10.1074/jbc.M108161200.
   PubMed Web of Science ®Google Scholar
• Ghosh P, Griffith J, Geuze HJ, Kornfeld S. 2003. Mammalian GGAs act together to sort mannose 6-phosphate receptors. J Cell Biol 163:755–766. http://dx.doi.org/10.1083/jcb.200308038.
   PubMed Web of Science ®Google Scholar
• He X, Li F, Chang WP, Tang J. 2005. GGA proteins mediate the recycling pathway of memapsin 2 (BACE). J Biol Chem 280:11696–11703. http://dx.doi.org/10.1074/jbc.M411296200.
   PubMed Web of Science ®Google Scholar
• Wahle T, Prager K, Raffler N, Haass C, Famulok M, Walter J. 2005. GGA proteins regulate retrograde transport of BACE1 from endosomes to the trans-Golgi network. Mol Cell Neurosci 29:453–461. http://dx.doi.org/10.1016/j.mcn.2005.03.014.
   PubMedGoogle Scholar
• Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS. 2004. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165:123–133. http://dx.doi.org/10.1083/jcb.200312055.
   PubMed Web of Science ®Google Scholar
• Seaman MN. 2005. Recycle your receptors with retromer. Trends Cell Biol 15:68–75. http://dx.doi.org/10.1016/j.tcb.2004.12.004.
   PubMed Web of Science ®Google Scholar
• McGough IJ, Cullen PJ. 2011. Recent advances in retromer biology. Traffic 12:963–971. http://dx.doi.org/10.1111/j.1600-0854.2011.01201.x.
   PubMed Web of Science ®Google Scholar
• Siegenthaler BM, Rajendran L. 2012. Retromers in Alzheimer's disease. Neurodegener Dis 10:116–121. http://dx.doi.org/10.1159/000335910.
   PubMedGoogle Scholar
• Buggia-Prevot V, Thinakaran G. 2014. Sorting the role of SORLA in Alzheimer's disease. Sci Transl Med 6:223–228. http://dx.doi.org/10.1126/scitranslmed.3008562.
   Google Scholar
• Jiang S, Li Y, Zhang X, Bu G, Xu H, Zhang YW. 2014. Trafficking regulation of proteins in Alzheimer's disease. Mol Neurodegener 9:6. http://dx.doi.org/10.1186/1750-1326-9-6.
   PubMedGoogle Scholar
• Schmidt V, Sporbert A, Rohe M, Reimer T, Rehm A, Andersen OM, Willnow TE. 2007. SorLA/LR11 regulates processing of amyloid precursor protein via interaction with adaptors GGA and PACS-1. J Biol Chem 282:32956–32964. http://dx.doi.org/10.1074/jbc.M705073200.
   PubMedGoogle Scholar
• Burgert T, Schmidt V, Caglayan S, Lin F, Fuchtbauer A, Fuchtbauer EM, Nykjaer A, Carlo AS, Willnow TE. 2013. SORLA-dependent and -independent functions for PACS1 in control of amyloidogenic processes. Mol Cell Biol 33:4308–4320. http://dx.doi.org/10.1128/MCB.00628-13.
   PubMedGoogle Scholar
• Okada H, Zhang W, Peterhoff C, Hwang JC, Nixon RA, Ryu SH, Kim TW. 2010. Proteomic identification of sorting nexin 6 as a negative regulator of BACE1-mediated APP processing. FASEB J 24:2783–2794. http://dx.doi.org/10.1096/fj.09-146357.
   PubMedGoogle Scholar
• Vekrellis K, Ye Z, Qiu WQ, Walsh D, Hartley D, Chesneau V, Rosner MR, Selkoe DJ. 2000. Neurons regulate extracellular levels of amyloid beta-protein via proteolysis by insulin-degrading enzyme. J Neurosci 20:1657–1665.
   PubMed Web of Science ®Google Scholar
• Simons K, Ehehalt R. 2002. Cholesterol, lipid rafts, and disease. J Clin Investig 110:597–603. http://dx.doi.org/10.1172/JCI16390.
   PubMed Web of Science ®Google Scholar
• Jacobson K, Mouritsen OG, Anderson RG. 2007. Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol 9:7–14. http://dx.doi.org/10.1038/ncb0107-7.
   PubMed Web of Science ®Google Scholar
• Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327:46–50. http://dx.doi.org/10.1126/science.1174621.
   PubMed Web of Science ®Google Scholar
• Riddell DR, Christie G, Hussain I, Dingwall C. 2001. Compartmentalization of beta-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr Biol 11:1288–1293. http://dx.doi.org/10.1016/S0960-9822(01)00394-3.
   PubMed Web of Science ®Google Scholar
• Vetrivel KS, Cheng H, Kim SH, Chen Y, Barnes NY, Parent AT, Sisodia SS, Thinakaran G. 2005. Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J Biol Chem 280:25892–25900. http://dx.doi.org/10.1074/jbc.M503570200.
   PubMedGoogle Scholar
• Lee SJ, Liyanage U, Bickel PE, Xia W, Lansbury PT, Jr, Kosik KS. 1998. A detergent-insoluble membrane compartment contains A beta in vivo. Nat Med 4:730–734. http://dx.doi.org/10.1038/nm0698-730.
   PubMed Web of Science ®Google Scholar
• Vetrivel KS, Thinakaran G. 2010. Membrane rafts in Alzheimer's disease beta-amyloid production. Biochim Biophys Acta 1801:860–867. http://dx.doi.org/10.1016/j.bbalip.2010.03.007.
   PubMed Web of Science ®Google Scholar
• Wirths O, Multhaup G, Bayer TA. 2004. A modified beta-amyloid hypothesis: intraneuronal accumulation of the beta-amyloid peptide–the first step of a fatal cascade. J Neurochem 91:513–520. http://dx.doi.org/10.1111/j.1471-4159.2004.02737.x.
   PubMed Web of Science ®Google Scholar
• Li Y, Xu C, Schubert D. 1999. The up-regulation of endosomal-lysosomal components in amyloid beta-resistant cells. J Neurochem 73:1477–1482.
   PubMedGoogle Scholar
• Zhou G, Roizman B. 2002. Cation-independent mannose 6-phosphate receptor blocks apoptosis induced by herpes simplex virus 1 mutants lacking glycoprotein D and is likely the target of antiapoptotic activity of the glycoprotein. J Virol 76:6197–6204. http://dx.doi.org/10.1128/JVI.76.12.6197-6204.2002.
   PubMedGoogle Scholar
• Weng YS, Kuo WW, Lin YM, Kuo CH, Tzang BS, Tsai FJ, Tsai CH, Lin JA, Hsieh DJ, Huang CY. 2013. Danshen mediates through estrogen receptors to activate Akt and inhibit apoptosis effect of Leu27IGF-II-induced IGF-II receptor signaling activation in cardiomyoblasts. Food Chem Toxicol 56:28–39. http://dx.doi.org/10.1016/j.fct.2013.01.008.
   PubMed Web of Science ®Google Scholar
• Gil J, Almeida S, Oliveira CR, Rego AC. 2003. Cytosolic and mitochondrial ROS in staurosporine-induced retinal cell apoptosis. Free Radic Biol Med 35:1500–1514. http://dx.doi.org/10.1016/j.freeradbiomed.2003.08.022.
   PubMed Web of Science ®Google Scholar
• Pong K, Doctrow SR, Huffman K, Adinolfi CA, Baudry M. 2001. Attenuation of staurosporine-induced apoptosis, oxidative stress, and mitochondrial dysfunction by synthetic superoxide dismutase and catalase mimetics, in cultured cortical neurons. Exp Neurol 171:84–97. http://dx.doi.org/10.1006/exnr.2001.7747.
   PubMed Web of Science ®Google Scholar
• Kruman I, Guo Q, Mattson MP. 1998. Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J Neurosci Res 51:293–308.
   PubMed Web of Science ®Google Scholar
• Butterfield DA, Boyd-Kimball D. 2004. Amyloid beta-peptide(1-42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol 14:426–432. http://dx.doi.org/10.1111/j.1750-3639.2004.tb00087.x.
   PubMed Web of Science ®Google Scholar
• Cenini G, Cecchi C, Pensalfini A, Bonini SA, Ferrari-Toninelli G, Liguri G, Memo M, Uberti D. 2010. Generation of reactive oxygen species by beta amyloid fibrils and oligomers involves different intra/extracellular pathways. Amino Acids 38:1101–1106. http://dx.doi.org/10.1007/s00726-009-0319-7.
   PubMedGoogle Scholar
• Araki W, Yuasa K, Takeda S, Takeda K, Shirotani K, Takahashi K, Tabira T. 2001. Pro-apoptotic effect of presenilin 2 (PS2) overexpression is associated with down-regulation of Bcl-2 in cultured neurons. J Neurochem 79:1161–1168. http://dx.doi.org/10.1046/j.1471-4159.2001.00638.x.
   PubMedGoogle Scholar