Abstract
Reticulon 3 (RTN3), which is a member of the reticulon family of proteins, has a biochemical function of shaping tubular endoplasmic reticulum. RTN3 has also been found to interact with β-site amyloid precursor protein cleaving enzyme 1 (BACE1), which initiates the generation of β-amyloid peptides (Aβ) from amyloid precursor protein. Aβ is the major proteinaceous component in neuritic plaques, which constitute one of the major pathological features in brains of Alzheimer’s disease (AD) patients. Mice deficient in or overexpressing RTN3 have altered amyloid deposition through effects on BACE1 expression and activity. In this review, we will summarize the current findings concerning the role of RTN3 in AD pathogenesis and demonstrate that RTN3 protein levels act as age-dependent modulators of BACE1 activity and Aβ deposition during the pathogenic progression of AD.
Acknowledgment
R. Yan is supported by grants (AG025493, MH103942, NS074256, and AG046929) from the National Institutes of Health. There is no conflict of interest to declare by the authors.
References
Araki, W. (2016). Post-translational regulation of the β-secretase BACE1. Brain Res Bull. 126, 170–177.10.1016/j.brainresbull.2016.04.009Search in Google Scholar
Araki, W., Oda, A., Motoki, K., Hattori, K., Itoh, M., Yuasa, S., Konishi, Y., Shin, R.W., Tamaoka, A., and Ogino, K. (2013). Reduction of β-amyloid accumulation by reticulon 3 in transgenic mice. Curr. Alzheimer Res. 10, 135–142.10.2174/1567205011310020003Search in Google Scholar
Arancibia-Carcamo, I.L., Yuen, E.Y., Muir, J., Lumb, M.J., Michels, G., Saliba, R.S., Smart, T.G., Yan, Z., Kittler, J.T., and Moss, S.J. (2009). Ubiquitin-dependent lysosomal targeting of GABA(A) receptors regulates neuronal inhibition. Proc. Natl. Acad. Sci. USA 106, 17552–17557.10.1073/pnas.0905502106Search in Google Scholar
Blasko, I., Beer, R., Bigl, M., Apelt, J., Franz, G., Rudzki, D., Ransmayr, G., Kampfl, A., and Schliebs, R. (2004). Experimental traumatic brain injury in rats stimulates the expression, production and activity of Alzheimer’s disease β-secretase (BACE-1). J. Neural Transm. 111, 523–536.10.1007/s00702-003-0095-6Search in Google Scholar
Borchelt, D.R., Ratovitski, T., van Lare, J., Lee, M.K., Gonzales, V., Jenkins, N.A., Copeland, N.G., Price, D.L., and Sisodia, S.S. (1997). Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19, 939–945.10.1016/S0896-6273(00)80974-5Search in Google Scholar
Brunholz, S., Sisodia, S., Lorenzo, A., Deyts, C., Kins, S., and Morfini, G. (2012). Axonal transport of APP and the spatial regulation of APP cleavage and function in neuronal cells. Exp. Brain Res. 217, 353–364.10.1007/s00221-011-2870-1Search in Google Scholar
Buggia-Prevot, V., Fernandez, C.G., Riordan, S., Vetrivel, K.S., Roseman, J., Waters, J., Bindokas, V.P., Vassar, R., and Thinakaran, G. (2014). Axonal BACE1 dynamics and targeting in hippocampal neurons: a role for Rab11 GTPase. Mol. Neurodegener. 9, 1.10.1186/1750-1326-9-1Search in Google Scholar
Burdick, D., Soreghan, B., Kwon, M., Kosmoski, J., Knauer, M., Henschen, A., Yates, J., Cotman, C., and Glabe, C. (1992). Assembly and aggregation properties of synthetic Alzheimer’s A4/β amyloid peptide analogs. J. Biol. Chem. 267, 546–554.10.1016/S0021-9258(18)48529-8Search in Google Scholar
Butterfield, D.A. (2002). Amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer’s disease brain. Free Radic. Res. 36, 1307–1313.10.1080/1071576021000049890Search in Google Scholar PubMed
Butterfield, D.A., Swomley, A.M., and Sultana, R. (2013). Amyloid β-peptide (1–42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid. Redox Signal 19, 823–835.10.1089/ars.2012.5027Search in Google Scholar PubMed PubMed Central
Cai, Y., Saiyin, H., Lin, Q., Zhang, P., Tang, L., Pan, X., and Yu, L. (2005). Identification of a new RTN3 transcript, RTN3-A1, and its distribution in adult mouse brain. Brain Res. Mol. Brain Res. 138, 236–243.10.1016/j.molbrainres.2005.04.020Search in Google Scholar
Chiurchiu, V., Maccarrone, M., and Orlacchio, A. (2014). The role of reticulons in neurodegenerative diseases. Neuromol. Med. 16, 3–15.10.1007/s12017-013-8271-9Search in Google Scholar
Cirrito, J.R., Yamada, K.A., Finn, M.B., Sloviter, R.S., Bales, K.R., May, P.C., Schoepp, D.D., Paul, S.M., Mennerick, S., and Holtzman, D.M. (2005). Synaptic activity regulates interstitial fluid amyloid-β levels in vivo. Neuron 48, 913–922.10.1016/j.neuron.2005.10.028Search in Google Scholar
Colledge, M., Snyder, E.M., Crozier, R.A., Soderling, J.A., Jin, Y., Langeberg, L.K., Lu, H., Bear, M.F., and Scott, J.D. (2003). Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40, 595–607.10.1016/S0896-6273(03)00687-1Search in Google Scholar
De Strooper, B., Saftig, P., Craessaerts, K., Vanderstichele, H., Guhde, G., Annaert, W., Von Figura, K., and Van Leuven, F. (1998). Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387–390.10.1038/34910Search in Google Scholar PubMed
Del Prete, D., Lombino, F., Liu, X., and D’Adamio, L. (2014). APP is cleaved by Bace1 in pre-synaptic vesicles and establishes a pre-synaptic interactome, via its intracellular domain, with molecular complexes that regulate pre-synaptic vesicles functions. PLoS One 9, e108576.10.1371/journal.pone.0108576Search in Google Scholar PubMed PubMed Central
Deng, M., He, W., Tan, Y., Han, H., Hu, X., Xia, K., Zhang, Z., and Yan, R. (2013). Increased expression of reticulon 3 in neurons leads to reduced axonal transport of β site amyloid precursor protein-cleaving enzyme 1. J. Biol. Chem. 288, 30236–30245.10.1074/jbc.M113.480079Search in Google Scholar PubMed PubMed Central
Di Scala, F., Dupuis, L., Gaiddon, C., De Tapia, M., Jokic, N., Gonzalez de Aguilar, J.L., Raul, J.S., Ludes, B. and Loeffler, J.P. (2005). Tissue specificity and regulation of the N-terminal diversity of reticulon 3. Biochem. J. 385, 125–134.10.1042/BJ20040458Search in Google Scholar PubMed PubMed Central
Dickson, T.C., King, C.E., McCormack, G.H., and Vickers, J.C. (1999). Neurochemical diversity of dystrophic neurites in the early and late stages of Alzheimer’s disease. Exp. Neurol. 156, 100–110.10.1006/exnr.1998.7010Search in Google Scholar PubMed
English, A.R. and Voeltz, G.K. (2013). Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol. 5, a013227.10.1101/cshperspect.a013227Search in Google Scholar PubMed PubMed Central
Finan, G.M., Okada, H., and Kim, T.W. (2011). BACE1 retrograde trafficking is uniquely regulated by the cytoplasmic domain of sortilin. J. Biol. Chem. 286, 12602–12616.10.1074/jbc.M110.170217Search in Google Scholar
Frampton, J.P., Guo, C., and Pierchala, B.A. (2012). Expression of axonal protein degradation machinery in sympathetic neurons is regulated by nerve growth factor. J. Neurosci. Res. 90, 1533–1546.10.1002/jnr.23041Search in Google Scholar
Francis, R., McGrath, G., Zhang, J., Ruddy, D.A., Sym, M., Apfeld, J., Nicoll, M., Maxwell, M., Hai, B., Ellis, M.C., et al. (2002). aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev. Cell 3, 85–97.10.1016/S1534-5807(02)00189-2Search in Google Scholar
Gregori, L., Hainfeld, J.F., Simon, M.N., and Goldgaber, D. (1997). Binding of amyloid β protein to the 20 S proteasome. J. Biol. Chem. 272, 58–62.10.1074/jbc.272.1.58Search in Google Scholar PubMed
Haass, C. (2004). Take five—BACE and the gamma-secretase quartet conduct Alzheimer’s amyloid β-peptide generation. EMBO J. 23, 483–488.10.1038/sj.emboj.7600061Search in Google Scholar PubMed PubMed Central
Hardy, J.A. and Higgins, G.A. (1992). Alzheimer’s disease: the amyloid cascade hypothesis. Science 256, 184–185.10.1126/science.1566067Search in Google Scholar PubMed
Hardy, J. and Selkoe, D.J. (2002). The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297, 353–356.10.1126/science.1072994Search in Google Scholar PubMed
He, W., Lu, Y., Qahwash, I., Hu, X.Y., Chang, A., and Yan, R. (2004). Reticulon family members modulate BACE1 activity and amyloid-beta peptide generation. Nat. Med. 10, 959–965.10.1038/nm1088Search in Google Scholar PubMed
He, X., Li, F., Chang, W.P., and Tang, J. (2005). GGA proteins mediate the recycling pathway of memapsin 2 (BACE). J. Biol. Chem. 280, 11696–11703.10.1074/jbc.M411296200Search in Google Scholar PubMed
He, W., Hu, X., Shi, Q., Zhou, X., Lu, Y., Fisher, C., and Yan, R. (2006). Mapping of interaction domains mediating binding between BACE1 and RTN/Nogo proteins. J. Mol. Biol. 363, 625–634.10.1016/j.jmb.2006.07.094Search in Google Scholar PubMed
He, W., Shi, Q., Hu, X., and Yan, R. (2007). The membrane topology of RTN3 and its effect on binding of RTN3 to BACE1. J. Biol. Chem. 282, 29144–29151.10.1074/jbc.M704181200Search in Google Scholar
Heath, J.E., Siedlak, S.L., Zhu, X., Lee, H.G., Thakur, A., Yan, R., Perry, G., Smith, M.A., and Castellani, R.J. (2010). Widespread distribution of reticulon-3 in various neurodegenerative diseases. Neuropathology 30, 574–579.10.1111/j.1440-1789.2010.01107.xSearch in Google Scholar
Holtzman, D.M., Morris, J.C., and Goate, A.M. (2011). Alzheimer’s disease: the challenge of the second century. Sci. Translat. Med. 3, 77sr1.10.1126/scitranslmed.3002369Search in Google Scholar
Hu, X., Shi, Q., Zhou, X., He, W., Yi, H., Yin, X., Gearing, M., Levey, A., and Yan, R. (2007). Transgenic mice overexpressing reticulon 3 develop neuritic abnormalities. EMBO J. 26, 2755–2767.10.1038/sj.emboj.7601707Search in Google Scholar
Huse, J.T. and Doms, R.W. (2001). Neurotoxic traffic: uncovering the mechanics of amyloid production in Alzheimer’s disease. Traffic 2, 75–81.10.1034/j.1600-0854.2001.020201.xSearch in Google Scholar
Huse, J.T., Pijak, D.S., Leslie, G.J., Lee, V.M., and Doms, R.W. (2000). Maturation and endosomal targeting of β-site amyloid precursor protein-cleaving enzyme. The Alzheimer’s disease beta-secretase. J. Biol. Chem. 275, 33729–33737.10.1074/jbc.M004175200Search in Google Scholar
Hussain, I., Powell, D., Howlett, D.R., Tew, D.G., Meek, T.D., Chapman, C., Gloger, I.S., Murphy, K.E., Southan, C.D., Ryan, D.M., et al. (1999). Identification of a novel aspartic protease (Asp 2) as β-secretase. Mol. Cell. Neurosci. 14, 419–427.10.1006/mcne.1999.0811Search in Google Scholar
Jarrett, J.T., Berger, E.P., and Lansbury, P.T., Jr. (1993). The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32, 4693–4697.10.1021/bi00069a001Search in Google Scholar
Kandalepas, P.C., Sadleir, K.R., Eimer, W.A., Zhao, J., Nicholson, D.A., and Vassar, R. (2013). The Alzheimer’s β-secretase BACE1 localizes to normal presynaptic terminals and to dystrophic presynaptic terminals surrounding amyloid plaques. Acta Neuropathol. 126, 329–352.10.1007/s00401-013-1152-3Search in Google Scholar
Kasa, P., Papp, H., and Pakaski, M. (2001). Presenilin-1 and its N-terminal and C-terminal fragments are transported in the sciatic nerve of rat. Brain Res. 909, 159–169.10.1016/S0006-8993(01)02679-8Search in Google Scholar
Keck, S., Nitsch, R., Grune, T., and Ullrich, O. (2003). Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer’s disease. J. Neurochem. 85, 115–122.10.1046/j.1471-4159.2003.01642.xSearch in Google Scholar
Keller, J.N., Hanni, K.B., and Markesbery, W.R. (2000). Impaired proteasome function in Alzheimer’s disease. J. Neurochem. 75, 436–439.10.1046/j.1471-4159.2000.0750436.xSearch in Google Scholar
Klinger, M., Diekmann, H., Heinz, D., Hirsch, C., Hannbeck von Hanwehr, S., Petrausch, B., Oertle, T., Schwab, M.E., and Stuermer, C.A. (2004). Identification of two NOGO/RTN4 genes and analysis of Nogo-A expression in Xenopus laevis. Mol. Cell. Neurosci. 25, 205–216.10.1016/j.mcn.2003.09.021Search in Google Scholar
Koh, Y.H., von Arnim, C.A., Hyman, B.T., Tanzi, R.E., and Tesco, G. (2005). BACE is degraded via the lysosomal pathway. J. Biol. Chem. 280, 32499–32504.10.1074/jbc.M506199200Search in Google Scholar
Koo, E.H. and Squazzo, S.L. (1994). Evidence that production and release of amyloid β-protein involves the endocytic pathway. J. Biol. Chem. 269, 17386–17389.10.1016/S0021-9258(17)32449-3Search in Google Scholar
Koo, E.H., Sisodia, S.S., Archer, D.R., Martin, L.J., Weidemann, A., Beyreuther, K., Fischer, P., Masters, C.L., and Price, D.L. (1990). Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. USA 87, 1561–1565.10.1073/pnas.87.4.1561Search in Google Scholar PubMed PubMed Central
Kume, H., Murayama, K.S., and Araki, W. (2009). The two-hydrophobic domain tertiary structure of reticulon proteins is critical for modulation of β-secretase BACE1. J. Neurosci. Res. 87, 2963–2972.10.1002/jnr.22112Search in Google Scholar PubMed
Lazarov, O., Lee, M., Peterson, D.A., and Sisodia, S.S. (2002). Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22, 9785–9793.10.1523/JNEUROSCI.22-22-09785.2002Search in Google Scholar
Lee, E.B., Zhang, B., Liu, K., Greenbaum, E.A., Doms, R.W., Trojanowski, J.Q., and Lee, V.M. (2005). BACE overexpression alters the subcellular processing of APP and inhibits Abeta deposition in vivo. J. Cell. Biol. 168, 291–302.10.1083/jcb.200407070Search in Google Scholar PubMed PubMed Central
Lee, S., Sato, Y., and Nixon, R.A. (2011). Lysosomal proteolysis inhibition selectively disrupts axonal transport of degradative organelles and causes an Alzheimer’s-like axonal dystrophy. J. Neurosci. 31, 7817–7830.10.1523/JNEUROSCI.6412-10.2011Search in Google Scholar PubMed PubMed Central
Li, Y.M., Lai, M.T., Xu, M., Huang, Q., DiMuzio-Mower, J., Sardana, M.K., Shi, X.P., Yin, K.C., Shafer, J.A., and Gardell, S.J. (2000). Presenilin 1 is linked with gamma-secretase activity in the detergent solubilized state. Proc. Natl. Acad. Sci. USA 97, 6138–6143.10.1073/pnas.110126897Search in Google Scholar
Lin, X., Koelsch, G., Wu, S., Downs, D., Dashti, A., and Tang, J. (2000). Human aspartic protease memapsin 2 cleaves the beta-secretase site of beta-amyloid precursor protein. Proc. Natl. Acad. Sci. USA 97, 1456–1460.10.1073/pnas.97.4.1456Search in Google Scholar
Lindsten, K., Menendez-Benito, V., Masucci, M.G., and Dantuma, N.P. (2003). A transgenic mouse model of the ubiquitin/proteasome system. Nat. Biotechnol. 21, 897–902.10.1038/nbt851Search in Google Scholar
Lopez Salon, M., Morelli, L., Castano, E.M., Soto, E.F., and Pasquini, J.M. (2000). Defective ubiquitination of cerebral proteins in Alzheimer’s disease. J. Neurosci. Res. 62, 302–310.10.1002/1097-4547(20001015)62:2<302::AID-JNR15>3.0.CO;2-LSearch in Google Scholar
Lundgren, J.L., Ahmed, S., Schedin-Weiss, S., Gouras, G.K., Winblad, B., Tjernberg, L.O., and Frykman, S. (2015). ADAM10 and BACE1 are localized to synaptic vesicles. J. Neurochem. 135, 606–615.10.1111/jnc.13287Search in Google Scholar
Masliah, E., Mallory, M., Hansen, L., Alford, M., Albright, T., DeTeresa, R., Terry, R., Baudier, J., and Saitoh, T. (1991). Patterns of aberrant sprouting in Alzheimer’s disease. Neuron 6, 729–739.10.1016/0896-6273(91)90170-5Search in Google Scholar
Masliah, E., Mallory, M., Hansen, L., Alford, M., DeTeresa, R., and Terry, R. (1993). An antibody against phosphorylated neurofilaments identifies a subset of damaged association axons in Alzheimer’s disease. Am. J. Pathol. 142, 871–882.Search in Google Scholar
Maxfield, F.R. and Yamashiro, D.J. (1987). Endosome acidification and the pathways of receptor-mediated endocytosis. Adv. Exp. Med. Biol. 225, 189–198.10.1007/978-1-4684-5442-0_16Search in Google Scholar
Moreira, E.F., Jaworski, C.J., and Rodriguez, I.R. (1999). Cloning of a novel member of the reticulon gene family (RTN3): gene structure and chromosomal localization to 11q13. Genomics 58, 73–81.10.1006/geno.1999.5807Search in Google Scholar
Murayama, K.S., Kametani, F., Saito, S., Kume, H., Akiyama, H., and Araki, W. (2006). Reticulons RTN3 and RTN4-B/C interact with BACE1 and inhibit its ability to produce amyloid beta-protein. Eur. J. Neurosci. 24, 1237–1244.10.1111/j.1460-9568.2006.05005.xSearch in Google Scholar
Natunen, T., Parrado, A.R., Helisalmi, S., Pursiheimo, J.P., Sarajarvi, T., Makinen, P., Kurkinen, K.M., Mullin, K., Alafuzoff, I., Haapasalo, A., et al. (2013). Elucidation of the BACE1 regulating factor GGA3 in Alzheimer’s disease. J. Alzheimers Dis. 37, 217–232.10.3233/JAD-130104Search in Google Scholar
Nziengui, H., Bouhidel, K., Pillon, D., Der, C., Marty, F., and Schoefs, B. (2007). Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Lett. 581, 3356–3362.10.1016/j.febslet.2007.06.032Search in Google Scholar
Oertle, T. and Schwab, M.E. (2003). Nogo and its partners. Trends Cell. Biol. 13, 187–194.10.1016/S0962-8924(03)00035-7Search in Google Scholar
Oertle, T., Huber, C., van der Putten, H., and Schwab, M.E. (2003a). Genomic structure and functional characterisation of the promoters of human and mouse nogo/rtn4. J. Mol. Biol. 325, 299–323.10.1016/S0022-2836(02)01179-8Search in Google Scholar
Oertle, T., Klinger, M., Stuermer, C.A., and Schwab, M.E. (2003b). A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family. FASEB J. 17, 1238–1247.10.1096/fj.02-1166hypSearch in Google Scholar PubMed
Park, J.H., Gimbel, D.A., GrandPre, T., Lee, J.K., Kim, J.E., Li, W., Lee, D.H., and Strittmatter, S.M. (2006). Alzheimer precursor protein interaction with the Nogo-66 receptor reduces amyloid-beta plaque deposition. J. Neurosci. 26, 1386–1395.10.1523/JNEUROSCI.3291-05.2006Search in Google Scholar PubMed PubMed Central
Pliassova, A., Lopes, J.P., Lemos, C., Oliveira, C.R., Cunha, R.A., and Agostinho, P. (2016). The association of amyloid-beta protein precursor with alpha- and beta-secretases in mouse cerebral cortex synapses is altered in early Alzheimer’s disease. Mol. Neurobiol. 53, 5710–5721.10.1007/s12035-015-9491-9Search in Google Scholar PubMed
Prior, M., Shi, Q., Hu, X., He, W., Levey, A., and Yan, R. (2010). RTN/Nogo in forming Alzheimer’s neuritic plaques. Neurosci. Biobehav. Rev. 34, 1201–1206.10.1016/j.neubiorev.2010.01.017Search in Google Scholar PubMed PubMed Central
Qing, H., Zhou, W., Christensen, M.A., Sun, X., Tong, Y., and Song, W. (2004). Degradation of BACE by the ubiquitin-proteasome pathway. FASEB J. 18, 1571–1573.10.1096/fj.04-1994fjeSearch in Google Scholar PubMed
Rifenburg, R.P. and Perry, G. (1995). Dystrophic neurites define diffuse as well as core-containing senile plaques in Alzheimer’s disease. Neurodegeneration 4, 235–237.Search in Google Scholar
Selkoe, D.J. (2004). Alzheimer disease: mechanistic understanding predicts novel therapies. Ann. Intern. Med. 140, 627–638.10.7326/0003-4819-140-8-200404200-00047Search in Google Scholar PubMed
Sharoar, M.G., Shi, Q., Ge, Y., He, W., Hu, X., Perry, G., Zhu, X., and Yan, R. (2015). Dysfunctional tubular endoplasmic reticulum constitutes a pathological feature of Alzheimer’s disease. Mol. Psychiatry 21, 1263–1271.10.1038/mp.2015.181Search in Google Scholar PubMed PubMed Central
Shi, Q., Hu, X., Prior, M., and Yan, R. (2009a). The occurrence of aging-dependent reticulon 3 immunoreactive dystrophic neurites decreases cognitive function. J Neurosci. 29, 5108–5115.10.1523/JNEUROSCI.5887-08.2009Search in Google Scholar PubMed PubMed Central
Shi, Q., Prior, M., He, W., Tang, X., Hu, X., and Yan, R. (2009b). Reduced amyloid deposition in mice overexpressing RTN3 is adversely affected by preformed dystrophic neurites. J. Neurosci. 29, 9163–9173.10.1523/JNEUROSCI.5741-08.2009Search in Google Scholar PubMed PubMed Central
Shi, Q., Prior, M., Zhou, X., Tang, X., He, W., Hu, X., and Yan, R. (2013). Preventing formation of reticulon 3 immunoreactive dystrophic neurites improves cognitive function in mice. J. Neurosci. 33, 3059–3066.10.1523/JNEUROSCI.2445-12.2013Search in Google Scholar PubMed PubMed Central
Shi, Q., Ge, Y., Sharoar, M.G., He, W., Xiang, R., Zhang, Z., Hu, X., and Yan, R. (2014). Impact of RTN3 deficiency on expression of BACE1 and amyloid deposition. J. Neurosci. 34, 13954–13962.10.1523/JNEUROSCI.1588-14.2014Search in Google Scholar PubMed PubMed Central
Shibata, Y., Voss, C., Rist, J.M., Hu, J., Rapoport, T.A., Prinz, W.A., and Voeltz, G.K. (2008). The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 283, 18892–18904.10.1074/jbc.M800986200Search in Google Scholar PubMed PubMed Central
Shibata, Y., Shemesh, T., Prinz, W.A., Palazzo, A.F., Kozlov, M.M., and Rapoport, T.A. (2010). Mechanisms determining the morphology of the peripheral ER. Cell 143, 774–788.10.1016/j.cell.2010.11.007Search in Google Scholar PubMed PubMed Central
Siegenthaler, B.M. and Rajendran, L. (2012). Retromers in Alzheimer’s disease. Neurodegener. Dis. 10, 116–121.10.1159/000335910Search in Google Scholar PubMed
Sinha, S., Anderson, J.P., Barbour, R., Basi, G.S., Caccavello, R., Davis, D., Doan, M., Dovey, H.F., Frigon, N., Hong, J., et al. (1999). Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 402, 537–540.10.1038/990114Search in Google Scholar PubMed
Sisodia, S.S. and St George-Hyslop, P.H. (2002). gamma-Secretase, Notch, Abeta and Alzheimer’s disease: where do the presenilins fit in? Nat. Rev. Neurosci. 3, 281–290.10.1038/nrn785Search in Google Scholar PubMed
Sun, X., Bromley-Brits, K., and Song, W. (2012). Regulation of beta-site APP-cleaving enzyme 1 gene expression and its role in Alzheimer’’s disease. J. Neurochem. 120 Suppl 1, 62–70.10.1111/j.1471-4159.2011.07515.xSearch in Google Scholar PubMed
Takahashi, R.H., Nam, E.E., Edgar, M., and Gouras, G.K. (2002). Alzheimer beta-amyloid peptides: normal and abnormal localization. Histol. Histopathol. 17, 239–246.Search in Google Scholar
Tamagno, E., Bardini, P., Obbili, A., Vitali, A., Borghi, R., Zaccheo, D., Pronzato, M.A., Danni, O., Smith, M.A., Perry, G., et al. (2002). Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol. Dis. 10, 279–288.10.1006/nbdi.2002.0515Search in Google Scholar
Tamagno, E., Guglielmotto, M., Monteleone, D., Vercelli, A., and Tabaton, M. (2012). Transcriptional and post-transcriptional regulation of beta-secretase. IUBMB Life 64, 943–950.10.1002/iub.1099Search in Google Scholar
Tan, J. and Evin, G. (2012). Beta-site APP-cleaving enzyme 1 trafficking and Alzheimer’s disease pathogenesis. J. Neurochem. 120, 869–880.Search in Google Scholar
Tanzi, R.E. and Bertram, L. (2005). Twenty years of the Alzheimer’s disease amyloid hypothesis: a genetic perspective. Cell 120, 545–555.10.1016/j.cell.2005.02.008Search in Google Scholar
Tesco, G., Koh, Y.H., Kang, E.L., Cameron, A.N., Das, S., Sena-Esteves, M., Hiltunen, M., Yang, S.H., Zhong, Z., Shen, Y., et al. (2007). Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54, 721–737.10.1016/j.neuron.2007.05.012Search in Google Scholar
Tienari, P.J., Ida, N., Ikonen, E., Simons, M., Weidemann, A., Multhaup, G., Masters, C.L., Dotti, C.G., and Beyreuther, K. (1997). Intracellular and secreted Alzheimer beta-amyloid species are generated by distinct mechanisms in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 94, 4125–4130.10.1073/pnas.94.8.4125Search in Google Scholar
Tong, Y., Zhou, W., Fung, V., Christensen, M.A., Qing, H., Sun, X., and Song, W. (2005). Oxidative stress potentiates BACE1 gene expression and Abeta generation. J. Neural Transm. 112, 455–469.10.1007/s00702-004-0255-3Search in Google Scholar
Trojanowski, J.Q. and Lee, V.M. (2002). The role of tau in Alzheimer’s disease. Med. Clin. North Am. 86, 615–627.10.1016/S0025-7125(02)00002-0Search in Google Scholar
van de Velde, H.J., Roebroek, A.J., Senden, N.H., Ramaekers, F.C., and Van de Ven, W.J. (1994). NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum. J. Cell Sci. 107, 2403–2416.10.1242/jcs.107.9.2403Search in Google Scholar PubMed
Vassar, R., Bennett, B.D., Babu-Khan, S., Kahn, S., Mendiaz, E.A., Denis, P., Teplow, D.B., Ross, S., Amarante, P., Loeloff, R., et al. (1999). Beta-secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735–741.10.1126/science.286.5440.735Search in Google Scholar PubMed
Vassar, R., Kovacs, D.M., Yan, R., and Wong, P.C. (2009). The beta-secretase enzyme BACE in health and Alzheimer’s disease: regulation, cell biology, function, and therapeutic potential. J. Neurosci. 29, 12787–12794.10.1523/JNEUROSCI.3657-09.2009Search in Google Scholar PubMed PubMed Central
Vickers, J.C., Chin, D., Edwards, A.M., Sampson, V., Harper, C., and Morrison, J. (1996). Dystrophic neurite formation associated with age-related beta amyloid deposition in the neocortex: clues to the genesis of neurofibrillary pathology. Exp. Neurol. 141, 1–11.10.1006/exnr.1996.0133Search in Google Scholar
Voeltz, G.K., Prinz, W.A., Shibata, Y., Rist, J.M., and Rapoport, T.A. (2006). A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573–586.10.1016/j.cell.2005.11.047Search in Google Scholar
Wahle, T., Prager, K., Raffler, N., Haass, C., Famulok, M., and Walter, J. (2005). GGA proteins regulate retrograde transport of BACE1 from endosomes to the trans-Golgi network. Mol. Cell. Neurosci. 29, 453–461.10.1016/j.mcn.2005.03.014Search in Google Scholar
Walker, K.R., Kang, E.L., Whalen, M.J., Shen, Y., and Tesco, G. (2012). Depletion of GGA1 and GGA3 mediates postinjury elevation of BACE1. J. Neurosci. 32, 10423–10437.10.1523/JNEUROSCI.5491-11.2012Search in Google Scholar
Walsh, D.M., Minogue, A.M., Sala Frigerio, C., Fadeeva, J.V., Wasco, W., and Selkoe, D.J. (2007). The APP family of proteins: similarities and differences. Biochem. Soc. Trans. 35, 416–420.10.1042/BST0350416Search in Google Scholar
Walter, J., Fluhrer, R., Hartung, B., Willem, M., Kaether, C., Capell, A., Lammich, S., Multhaup, G., and Haass, C. (2001). Phosphorylation regulates intracellular trafficking of beta-secretase. J. Biol. Chem. 276, 14634–14641.10.1074/jbc.M011116200Search in Google Scholar
Wen, L., Tang, F.L., Hong, Y., Luo, S.W., Wang, C.L., He, W., Shen, C., Jung, J.U., Xiong, F., Lee, D.H., et al. (2011). VPS35 haploinsufficiency increases Alzheimer’s disease neuropathology. J. Cell. Biol. 195, 765–779.10.1083/jcb.201105109Search in Google Scholar
Wojcik, S., Engel, W.K., Yan, R., McFerrin, J., and Askanas, V. (2007). NOGO is increased and binds to BACE1 in sporadic inclusion-body myositis and in A beta PP-overexpressing cultured human muscle fibers. Acta Neuropathol. 114, 517–526.10.1007/s00401-007-0281-ySearch in Google Scholar
Yan, R. and Vassar, R. (2014). Targeting the beta secretase BACE1 for Alzheimer’s disease therapy. Lancet Neurol. 13, 319–329.10.1016/S1474-4422(13)70276-XSearch in Google Scholar
Yan, R., Bienkowski, M.J., Shuck, M.E., Miao, H., Tory, M.C., Pauley, A.M., Brashier, J.R., Stratman, N.C., Mathews, W.R., Buhl, A.E., et al. (1999). Membrane-anchored aspartyl protease with Alzheimer’s disease beta-secretase activity. Nature 402, 533–537.10.1038/990107Search in Google Scholar PubMed
Yan, R., Shi, Q., Hu, X., and Zhou, X. (2006). Reticulon proteins: emerging players in neurodegenerative diseases. Cell. Mol. Life Sci. 63, 877–889.10.1007/s00018-005-5338-2Search in Google Scholar PubMed
Yang, Y.S. and Strittmatter, S.M. (2007). The reticulons: a family of proteins with diverse functions. Genome Biol. 8, 234.10.1186/gb-2007-8-12-234Search in Google Scholar PubMed PubMed Central
Yu, G., Nishimura, M., Arawaka, S., Levitan, D., Zhang, L., Tandon, A., Song, Y.Q., Rogaeva, E., Chen, F., Kawarai, T., et al. (2000). Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature 407, 48–54.10.1038/35024009Search in Google Scholar PubMed
Zhao, B., Pan, B.S., Shen, S.W., Sun, X., Hou, Z.Z., Yan, R., and Sun, F.Y. (2013). Diabetes-induced central neuritic dystrophy and cognitive deficits are associated with the formation of oligomeric reticulon-3 via oxidative stress. J. Biol. Chem. 288, 15590–15599.10.1074/jbc.M112.440784Search in Google Scholar PubMed PubMed Central
©2017 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- New dimensions of connectomics and network plasticity in the central nervous system
- Redox-sensitive GFP to monitor oxidative stress in neurodegenerative diseases
- Effects of altered RTN3 expression on BACE1 activity and Alzheimer’s neuritic plaques
- Role of ABC transporters in the pathology of Alzheimer’s disease
- The guilty brain: the utility of neuroimaging and neurostimulation studies in forensic field
- Applications of transcranial direct current stimulation in children and pediatrics
- Epilepsy and vitamin D: a comprehensive review of current knowledge
- The thalamus as a relay station and gatekeeper: relevance to brain disorders
Articles in the same Issue
- Frontmatter
- New dimensions of connectomics and network plasticity in the central nervous system
- Redox-sensitive GFP to monitor oxidative stress in neurodegenerative diseases
- Effects of altered RTN3 expression on BACE1 activity and Alzheimer’s neuritic plaques
- Role of ABC transporters in the pathology of Alzheimer’s disease
- The guilty brain: the utility of neuroimaging and neurostimulation studies in forensic field
- Applications of transcranial direct current stimulation in children and pediatrics
- Epilepsy and vitamin D: a comprehensive review of current knowledge
- The thalamus as a relay station and gatekeeper: relevance to brain disorders