Skip to main content

Advertisement

SpringerLink
Log in

Activity-dependent and graded BACE1 expression in the olfactory epithelium is mediated by the retinoic acid metabolizing enzyme CYP26B1

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

It is well established that environmental influences play a key role in sculpting neuronal connectivity in the brain. One example is the olfactory sensory map of topographic axonal connectivity. While intrinsic odorant receptor signaling in olfactory sensory neurons (OSN) determines anterior–posterior counter gradients of the axonal guidance receptors Neuropilin-1 and Plexin-A1, little is known about stimulus-dependent gradients of protein expression, which correlates with the functional organization of the olfactory sensory map along its dorsomedial (DM)–ventrolateral (VL) axis. Deficiency of the Alzheimer’s β-secretase BACE1, which is expressed in a DMlow–VLhigh gradient, results in OSN axon targeting errors in a DM > VL and gene dose-dependent manner. We show that expression of BACE1 and the all-trans retinoic acid (RA)-degrading enzyme Cyp26B1 form DM–VL counter gradients in the olfactory epithelium. Analyses of mRNA and protein levels in OSNs after naris occlusion, in mice deficient in the olfactory cyclic nucleotide-gated channel and in relation to onset of respiration, show that BACE1 and Cyp26B1 expression in OSNs inversely depend on neuronal activity. Overexpression of a Cyp26B1 or presence of a dominant negative RA receptor transgene selectively in OSNs, inhibit BACE1 expression while leaving the DMlow–VLhigh gradient of the axonal guidance protein Neuropilin-2 intact. We conclude that stimulus-dependent neuronal activity can control the expression of the RA catabolic enzyme Cyp26B1 and downstream genes such as BACE1. This result is pertinent to an understanding of the mechanisms by which a topographic pattern of connectivity is achieved and modified as a consequence of graded gene expression and sensory experience.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abu-Abed S, MacLean G, Fraulob V, Chambon P, Petkovich M, Dolle P (2002) Differential expression of the retinoic acid-metabolizing enzymes CYP26A1 and CYP26B1 during murine organogenesis. Mech Dev 110(1–2):173–177

    Article  CAS  PubMed  Google Scholar 

  • Alenius M, Bohm S (1997) Identification of a novel neural cell adhesion molecule-related gene with a potential role in selective axonal projection. J Biol Chem 272:26083–26086

    Article  CAS  PubMed  Google Scholar 

  • Alenius M, Bohm S (2003) Differential function of RNCAM isoforms in precise target selection of olfactory sensory neurons. Development 130:917–927

    Article  CAS  PubMed  Google Scholar 

  • Aoto J, Nam CI, Poon MM, Ting P, Chen L (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 60:308–320

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Asson-Batres MA, Smith WB (2006) Localization of retinaldehyde dehydrogenases and retinoid binding proteins to sustentacular cells, glia, Bowman’s gland cells, and stroma: potential sites of retinoic acid synthesis in the postnatal rat olfactory organ. J Comp Neurol 496(2):149–171. doi:10.1002/cne.20904

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Asson-Batres MA, Ahmad O, Smith WB (2003) Expression of the cellular retinoic acid binding proteins, type II and type I, in mature rat olfactory epithelium. Cell Tissue Res 312(1):9–19

    CAS  PubMed  Google Scholar 

  • Baker H, Cummings DM, Munger SD, Margolis JW, Franzen L, Reed RR, Margolis FL (1999) Targeted deletion of a cyclic nucleotide-gated channel subunit (OCNC1): biochemical and morphological consequences in adult mice. J Neurosci 19(21):9313–9321

    CAS  PubMed  Google Scholar 

  • Bolte S, Cordelieres FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Pt 3):213–232. doi:10.1111/j.1365-2818.2006.01706.x

    Article  CAS  PubMed  Google Scholar 

  • Boylan JF, Gudas LJ (1992) The level of Crabp-I expression influences the amounts and types of all-trans-retinoic acid metabolites in F9 teratocarcinoma stem-cells. J Biol Chem 267(30):21486–21491

    CAS  PubMed  Google Scholar 

  • Cao L, Rickenbacher GT, Rodriguez S, Moulia TW, Albers MW (2012) The precision of axon targeting of mouse olfactory sensory neurons requires the BACE1 protease. Sci Rep 2:231. doi:10.1038/srep00231

    PubMed Central  PubMed  Google Scholar 

  • Chambon P (1996) A decade of molecular biology of retinoic acid receptors. FASEB J 10(9):940–954

    CAS  PubMed  Google Scholar 

  • Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M (1997) Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19(3):547–559

    Article  CAS  PubMed  Google Scholar 

  • Chen XM, Xia ZG, Storm DR (2012) Stimulation of electro-olfactogram responses in the main olfactory epithelia by airflow depends on the type 3 adenylyl cyclase. J Neurosci 32(45):15769–15778. doi:10.1523/Jneurosci.2180-12.2012

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chiang MY, Misner D, Kempermann G, Schikorski T, Giguere V, Sucov HM, Gage FH, Stevens CF, Evans RM (1998) An essential role for retinoid receptors RARbeta and RXRgamma in long-term potentiation and depression. Neuron 21(6):1353–1361

    Article  CAS  PubMed  Google Scholar 

  • Cho JH, Lepine M, Andrews W, Parnavelas J, Cloutier JF (2007) Requirement for Slit-1 and Robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J Neurosci 27(34):9094–9104. doi:10.1523/JNEUROSCI.2217-07.2007

    Article  CAS  PubMed  Google Scholar 

  • Cho JH, Prince JE, Cutforth T, Cloutier JF (2011) The pattern of glomerular map formation defines responsiveness to aversive odorants in mice. J Neurosci 31(21):7920–7926. doi:10.1523/JNEUROSCI.2460-10.2011

    Article  CAS  PubMed  Google Scholar 

  • Damm K, Heyman RA, Umesono K, Evans RM (1993) Functional inhibition of retinoic acid response by dominant negative retinoic acid receptor mutants. Proc Natl Acad Sci USA 90(7):2989–2993

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Danciger E, Mettling C, Vidal M, Morris R, Margolis F (1989) Olfactory marker protein gene: its structure and olfactory neuron-specific expression in transgenic mice. Proc Natl Acad Sci 86:8565–8569

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dewan A, Pacifico R, Zhan R, Rinberg D, Bozza T (2013) Non-redundant coding of aversive odours in the main olfactory pathway. Nature 497(7450):486–489. doi:10.1038/nature12114

    Article  CAS  PubMed  Google Scholar 

  • Etchamendy N, Enderlin V, Marighetto A, Pallet V, Higueret P, Jaffard R (2003) Vitamin A deficiency and relational memory deficit in adult mice: relationships with changes in brain retinoid signalling. Behav Brain Res 145(1–2):37–49

    Article  CAS  PubMed  Google Scholar 

  • Goodman T, Crandall JE, Nanescu SE, Quadro L, Shearer K, Ross A, McCaffery P (2012) Patterning of retinoic acid signaling and cell proliferation in the hippocampus. Hippocampus 22(11):2171–2183. doi:10.1002/hipo.22037

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M (2007) Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10(3):348–354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gussing F, Bohm S (2004) NQO1 activity in the main and the accessory olfactory systems correlates with the zonal topography of projection maps. Eur J Neurosci 19(9):2511–2518

    Article  PubMed  Google Scholar 

  • Gustafson AL, Eriksson U, Dencker L (1999) CRBP I and CRABP I localisation during olfactory nerve development. Brain Res Dev Brain Res 114(1):121–126

    Article  CAS  PubMed  Google Scholar 

  • Hagglund M, Berghard A, Strotmann J, Bohm S (2006) Retinoic acid receptor-dependent survival of olfactory sensory neurons in postnatal and adult mice. J Neurosci 26(12):3281–3291

    Article  PubMed  Google Scholar 

  • Helfer G, Ross AW, Russell L, Thomson LM, Shearer KD, Goodman TH, McCaffery PJ, Morgan PJ (2012) Photoperiod regulates vitamin A and Wnt/beta-catenin signaling in F344 rats. Endocrinology 153(2):815–824. doi:10.1210/En.2011-1792

    Article  CAS  PubMed  Google Scholar 

  • Holback S, Adlerz L, Gatsinzi T, Jacobsen KT, Iverfeldt K (2008) PI3-K- and PKC-dependent up-regulation of APP processing enzymes by retinoic acid. Biochem Biophys Res Commun 365(2):298–303. doi:10.1016/j.bbrc.2007.10.167

    Article  CAS  PubMed  Google Scholar 

  • Hornberg M, Gussing F, Berghard A, Bohm S (2009) Retinoic acid selectively inhibits death of basal vomeronasal neurons during late stage of neural circuit formation. J Neurochem 110(4):1263–1275. doi:10.1111/j.1471-4159.2009.06216.x

    Article  PubMed  Google Scholar 

  • Husson M, Enderlin V, Delacourte A, Ghenimi N, Alfos S, Pallet V, Higueret P (2006) Retinoic acid normalizes nuclear receptor mediated hypo-expression of proteins involved in beta-amyloid deposits in the cerebral cortex of vitamin A deprived rats. Neurobiol Dis 23(1):1–10. doi:10.1016/j.nbd.2006.01.008

    Article  CAS  PubMed  Google Scholar 

  • Imai T, Suzuki M, Sakano H (2006) Odorant receptor-derived cAMP signals direct axonal targeting. Science 314(5799):657–661

    Article  CAS  PubMed  Google Scholar 

  • Imai T, Yamazaki T, Kobayakawa R, Kobayakawa K, Abe T, Suzuki M, Sakano H (2009) Pre-target axon sorting establishes the neural map topography. Science 325(5940):585–590. doi:10.1126/science.1173596

    Article  CAS  PubMed  Google Scholar 

  • Ishii T, Omura M, Mombaerts P (2004) Protocols for two- and three-color fluorescent RNA in-situ hybridization of the main and accessory olfactory epithelia in mouse. J Neurocytol 33(6):657–669

    Article  CAS  PubMed  Google Scholar 

  • Kandalepas PC, Vassar R (2012) Identification and biology of beta-secretase. J Neurochem 120(Suppl 1):55–61. doi:10.1111/j.1471-4159.2011.07512.x

    Article  CAS  PubMed  Google Scholar 

  • Kerr MA, Belluscio L (2006) Olfactory experience accelerates glomerular refinement in the mammalian olfactory bulb. Nat Neurosci 9(4):484–486

    Article  CAS  PubMed  Google Scholar 

  • Kimbell JS, Godo MN, Gross EA, Joyner DR, Richardson RB, Morgan KT (1997) Computer simulation of inspiratory airflow in all regions of the F344 rat nasal passages. Toxicol Appl Pharmacol 145(2):388–398. doi:10.1006/taap.1997.8206

    Article  CAS  PubMed  Google Scholar 

  • Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature 450(7169):503–508. doi:10.1038/nature06281

    Article  CAS  PubMed  Google Scholar 

  • Koryakina A, Aeberhard J, Kiefer S, Hamburger M, Kuenzi P (2009) Regulation of secretases by all-trans-retinoic acid. FEBS J 276(9):2645–2655. doi:10.1111/j.1742-4658.2009.06992.x

    Article  CAS  PubMed  Google Scholar 

  • Lein ES et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445(7124):168–176. doi:10.1038/nature05453

    Article  CAS  PubMed  Google Scholar 

  • Lin DM, Wang F, Lowe G, Gold GH, Axel R, Ngai J, Brunet L (2000) Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26(1):69–80

    Article  CAS  PubMed  Google Scholar 

  • Luo TL, Sakai Y, Wagner E, Drager UC (2006) Retinoids, eye development, and maturation of visual function. J Neurobiol 66(7):677–686. doi:10.1002/Neu.20239

    Article  CAS  PubMed  Google Scholar 

  • MacLean G, Abu-Abed S, Dolle P, Tahayato A, Chambon P, Petkovich M (2001) Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech Dev 107(1–2):195–201

    Article  CAS  PubMed  Google Scholar 

  • Maden M (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 8(10):755–765. doi:10.1038/nrn2212

    Article  CAS  PubMed  Google Scholar 

  • Misner DL, Jacobs S, Shimizu Y, de Urquiza AM, Solomin L, Perlmann T, De Luca LM, Stevens CF, Evans RM (2001) Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc Natl Acad Sci USA 98(20):11714–11719

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakashima A, Takeuchi H, Imai T, Saito H, Kiyonari H, Abe T, Chen M, Weinstein LS, Yu CR, Storm DR, Nishizumi H, Sakano H (2013a) Agonist-independent GPCR activity regulates anterior-posterior targeting of olfactory sensory neurons. Cell 154(6):1314–1325. doi:10.1016/j.cell.2013.08.033

    Article  CAS  PubMed  Google Scholar 

  • Nakashima N, Ishii TM, Bessho Y, Kageyama R, Ohmori H (2013b) Hyperpolarisation-activated cyclic nucleotide-gated channels regulate the spontaneous firing rate of olfactory receptor neurons and affect glomerular formation in mice. J Physiol 591(Pt 7):1749–1769. doi:10.1113/jphysiol.2012.247361

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakatani H, Serizawa S, Nakajima M, Imai T, Sakano H (2003) Developmental elimination of ectopic projection sites for the transgenic OR gene that has lost zone specificity in the olfactory epithelium. Eur J Neurosci 18(9):2425–2432

    Article  PubMed  Google Scholar 

  • Nelson DR (1999) A second CYP26 P450 in humans and zebrafish: CYP26B1. Arch Biochem Biophys 371(2):345–347. doi:10.1006/abbi.1999.1438

    Article  CAS  PubMed  Google Scholar 

  • Niederreither K, Fraulob V, Garnier JM, Chambon P, Dolle P (2002) Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech Dev 110(1–2):165–171

    Article  CAS  PubMed  Google Scholar 

  • Nomoto M, Takeda Y, Uchida S, Mitsuda K, Enomoto H, Saito K, Choi T, Watabe AM, Kobayashi S, Masushige S, Manabe T, Kida S (2012) Dysfunction of the RAR/RXR signaling pathway in the forebrain impairs hippocampal memory and synaptic plasticity. Mol Brain 5:1–15. doi:10.1186/1756-6606-5-8

  • Norlin EM, Berghard A (2001) Spatially restricted expression of regulators of G-protein signaling in primary olfactory neurons. Mol Cell Neurosci 17(5):872–882

    Article  CAS  PubMed  Google Scholar 

  • Norlin EM, Alenius M, Gussing F, Hägglund M, Vedin V, Bohm S (2001) Evidence for gradients of gene expression correlating with zonal topography of the olfactory sensory map. Mol Cell Neurosci 18:283–295

    Article  CAS  PubMed  Google Scholar 

  • Oka Y, Katada S, Omura M, Suwa M, Yoshihara Y, Touhara K (2006) Odorant receptor map in the mouse olfactory bulb: in vivo sensitivity and specificity of receptor-defined glomeruli. Neuron 52(5):857–869. doi:10.1016/j.neuron.2006.10.019

    Article  CAS  PubMed  Google Scholar 

  • Oztokatli H, Hornberg M, Berghard A, Bohm S (2012) Retinoic acid receptor and CNGA2 channel signaling are part of a regulatory feedback loop controlling axonal convergence and survival of olfactory sensory neurons. FASEB J 26(2):617–627. doi:10.1096/fj.11-192450

    Article  PubMed Central  PubMed  Google Scholar 

  • Peluso CE, Jang W, Drager UC, Schwob JE (2012) Differential expression of components of the retinoic acid signaling pathway in the adult mouse olfactory epithelium. J Comp Neurol 520(16):3707–3726. doi:10.1002/cne.23124

    Article  CAS  PubMed  Google Scholar 

  • Rajapaksha TW, Eimer WA, Bozza TC, Vassar R (2011) The Alzheimer’s beta-secretase enzyme BACE1 is required for accurate axon guidance of olfactory sensory neurons and normal glomerulus formation in the olfactory bulb. Mol Neurodegener 6:88. doi:10.1186/1750-1326-6-88

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73(3):597–609

    Article  CAS  PubMed  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79(7):1245–1255

    Article  CAS  PubMed  Google Scholar 

  • Rhinn M, Dolle P (2012) Retinoic acid signalling during development. Development 139(5):843–858. doi:10.1242/Dev.065938

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Gil DJ, Hu W, Greer CA (2013) Dishevelled proteins are associated with olfactory sensory neuron presynaptic terminals. PLoS One 8(2):e56561. doi:10.1371/journal.pone.0056561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sarti F, Schroeder J, Aoto J, Chen L (2012) Conditional RARalpha knockout mice reveal acute requirement for retinoic acid and RARalpha in homeostatic plasticity. Front Mol Neurosci 5:16. doi:10.3389/fnmol.2012.00016

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sarti F, Zhang Z, Schroeder J, Chen L (2013) Rapid suppression of inhibitory synaptic transmission by retinoic acid. J Neurosci 33(28):11440–11450. doi:10.1523/JNEUROSCI.1710-13.2013

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Satoh J, Kuroda Y (2000) Amyloid precursor protein beta-secretase (BACE) mRNA expression in human neural cell lines following induction of neuronal differentiation and exposure to cytokines and growth factors. Neuropathology 20(4):289–296

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675

    Article  CAS  PubMed  Google Scholar 

  • Scott JW (2006) Sniffing and spatiotemporal coding in olfaction. Chem Senses 31(2):119–130. doi:10.1093/chemse/bjj013

    Article  PubMed Central  PubMed  Google Scholar 

  • Serizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M, Sakano H (2006) A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127(5):1057–1069

    Article  CAS  PubMed  Google Scholar 

  • Shearer KD, Stoney PN, Morgan PJ, McCaffery PJ (2012) A vitamin for the brain. Trends Neurosci 35(12):733–741. doi:10.1016/j.tins.2012.08.005

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi H, Inokuchi K, Aoki M, Suto F, Tsuboi A, Matsuda I, Suzuki M, Aiba A, Serizawa S, Yoshihara Y, Fujisawa H, Sakano H (2010) Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 141(6):1056–1067. doi:10.1016/j.cell.2010.04.041

    Article  CAS  PubMed  Google Scholar 

  • Thatcher JE, Isoherranen N (2009) The role of CYP26 enzymes in retinoic acid clearance. Expert Opin Drug Metab Toxicol 5(8):875–886. doi:10.1517/17425250903032681

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uehara M, Yashiro K, Takaoka K, Yamamoto M, Hamada H (2009) Removal of maternal retinoic acid by embryonic CYP26 is required for correct Nodal expression during early embryonic patterning. Genes Dev 23(14):1689–1698. doi:10.1101/gad.1776209

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vassar R, Ngai J, Axel R (1993) Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74(2):309–318

    Article  CAS  PubMed  Google Scholar 

  • Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79(6):981–991

    Article  CAS  PubMed  Google Scholar 

  • Vedin V, Molander M, Bohm S, Berghard A (2009) Regional differences in olfactory epithelial homeostasis in the adult mouse. J Comp Neurol 513(4):375–384. doi:10.1002/cne.21973

    Article  PubMed  Google Scholar 

  • Verhagen JV, Wesson DW, Netoff TI, White JA, Wachowiak M (2007) Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10(5):631–639. doi:10.1038/Nn1892

    Article  CAS  PubMed  Google Scholar 

  • Wang HL, Zhang ZJ, Hintze M, Chen L (2011) Decrease in calcium concentration triggers neuronal retinoic acid synthesis during homeostatic synaptic plasticity. J Neurosci 31(49):17764–17771. doi:10.1523/Jneurosci.3964-11.2011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • White RJ, Schilling TF (2008) How degrading: Cyp26s in hindbrain development. Dev Dynam 237(10):2775–2790. doi:10.1002/Dvdy.21695

    Article  CAS  Google Scholar 

  • White JA, Guo YD, Baetz K, Beckett-Jones B, Bonasoro J, Hsu KE, Dilworth FJ, Jones G, Petkovich M (1996) Identification of the retinoic acid-inducible all-trans-retinoic acid 4-hydroxylase. J Biol Chem 271(47):29922–29927

    Article  CAS  PubMed  Google Scholar 

  • Won JY, Nam EC, Yoo SJ, Kwon HJ, Um SJ, Han HS, Kim SH, Byun Y, Kim SY (2004) The effect of cellular retinoic acid binding protein-I expression on the CYP26-mediated catabolism of all-trans retinoic acid and cell proliferation in head and neck squamous cell carcinoma. Metabolism 53(8):1007–1012. doi:10.1016/j.metabol.2003.12.015

    Article  CAS  PubMed  Google Scholar 

  • Yan XX, Xiong K, Luo XG, Struble RG, Clough RW (2007) Beta-secretase expression in normal and functionally deprived rat olfactory bulbs: inverse correlation with oxidative metabolic activity. J Comp Neurol 501(1):52–69. doi:10.1002/cne.21239

    Article  CAS  PubMed  Google Scholar 

  • Yu CR, Power J, Barnea G, O’Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42(4):553–566

    Article  CAS  PubMed  Google Scholar 

  • Zhang XM, Xiong K, Cai Y, Cai H, Luo XG, Feng JC, Clough RW, Patrylo PR, Struble RG, Yan XX (2010) Functional deprivation promotes amyloid plaque pathogenesis in Tg2576 mouse olfactory bulb and piriform cortex. Eur J Neurosci 31(4):710–721. doi:10.1111/j.1460-9568.2010.07103.x

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhao H, Reed RR (2001) X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104(5):651–660

    Article  CAS  PubMed  Google Scholar 

  • Zhao K, Dalton P, Yang GC, Scherer PW (2006) Numerical modeling of turbulent and laminar airflow and odorant transport during sniffing in the human and rat nose. Chem Senses 31(2):107–118. doi:10.1093/chemse/bjj008

    Article  PubMed  Google Scholar 

  • Zhao S, Tian H, Ma L, Yuan Y, Yu CR, Ma M (2013) Activity-dependent modulation of odorant receptor gene expression in the mouse olfactory epithelium. PLoS One 8(7):e69862. doi:10.1371/journal.pone.0069862

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zheng C, Feinstein P, Bozza T, Rodriguez I, Mombaerts P (2000) Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron 26(1):81–91

    Article  CAS  PubMed  Google Scholar 

  • Zou DJ, Feinstein P, Rivers AL, Mathews GA, Kim A, Greer CA, Mombaerts P, Firestein S (2004) Postnatal refinement of peripheral olfactory projections. Science 304(5679):1976–1979

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Viktoria Vedin for expert advice on immunohistochemistry; Dr. Maria Hörnberg for transgenic expertise; Dr. Peter Mombaerts (Max-Planck-Institut für Biophysik, Frankfurt, Germany) for the OCNC1 mutant strains, and Drs. Sara Wilson, Paolo Medini, Christophe Laumonnerie and Anna Berghard for critical reading the manuscript. This work was supported by the Swedish Medical Science Research Council (K2008-63X-20726-01-3).

Conflict of interest

The authors declare no competing financial interests.

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Umeå University, 901 87, Umeå, Sweden

    Hande Login & Staffan Bohm

  2. Department of Molecular Cell Genetics, L. Rydygier Collegium Medicum, Nicolaus Copernicus University, Curie-Sklodowskiej 9, 85-093, Bydgoszcz, Poland

    Rafal Butowt

Authors
  1. Hande Login
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rafal Butowt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Staffan Bohm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Staffan Bohm.

Additional information

H. Login and R. Butowt equally contributed to this paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Login, H., Butowt, R. & Bohm, S. Activity-dependent and graded BACE1 expression in the olfactory epithelium is mediated by the retinoic acid metabolizing enzyme CYP26B1. Brain Struct Funct 220, 2143–2157 (2015). https://doi.org/10.1007/s00429-014-0783-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-014-0783-z

Keywords

Search

Navigation