Skip to main content

Advertisement

Log in

The functional relevance of olfactory marker protein in the vertebrate olfactory system: a never-ending story

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Olfactory marker protein (OMP) was first described as a protein expressed in olfactory receptor neurons (ORNs) in the nasal cavity. In particular, OMP, a small cytoplasmic protein, marks mature ORNs and is also expressed in the neurons of other nasal chemosensory systems: the vomeronasal organ, the septal organ of Masera, and the Grueneberg ganglion. While its expression pattern was more easily established, OMP’s function remained relatively vague. To date, most of the work to understand OMP’s role has been done using mice lacking OMP. This mostly phenomenological work has shown that OMP is involved in sharpening the odorant response profile and in quickening odorant response kinetics of ORNs and that it contributes to targeting of ORN axons to the olfactory bulb to refine the glomerular response map. Increasing evidence shows that OMP acts at the early stages of olfactory transduction by modulating the kinetics of cAMP, the second messenger of olfactory transduction. However, how this occurs at a mechanistic level is not understood, and it might also not be the only mechanism underlying all the changes observed in mice lacking OMP. Recently, OMP has been detected outside the nose, including the brain and other organs. Although no obvious logic has become apparent regarding the underlying commonality between nasal and extranasal expression of OMP, a broader approach to diverse cellular systems might help unravel OMP’s functions and mechanisms of action inside and outside the nose.

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

Access this article

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

Similar content being viewed by others

Abbreviations

AC3:

Adenylyl cyclase type III

Ano2:

Anoctamin 2

AP:

Action potential

Bex1-6:

Brain-expressed X-linked protein 1–6

cAMP:

Cyclic adenosine monophosphate

CNG:

Cyclic nucleotide-gated

CNGA2, CNGA4:

cyclic nucleotide-gated alpha 2 or 4 subunit

CNGB1:

Cyclic nucleotide-gated beta 1 subunit

EOG:

Electro-olfactogram

EphA, EphB:

ephrin A or B receptor

ETC:

External tufted cell

FMRP:

Fragile X mental retardation protein

GBC:

Globose basal cell

GFP:

Green fluorescent protein

Golf :

Olfactory G protein

Gs :

G protein

HBC:

Horizontal basal cell

IBMX:

3-isobutyl-1-methylxanthine

K1-18:

Cytokeratin 1–18

Kir2.1:

Inwardly rectifying potassium channel

KO:

Knockout

M71:

Olfactory receptor type

mOR-23:

Olfactory receptor type

mOR-EG:

Olfactory receptor type

NCKX4:

K+-dependent Na+/Ca2+ exchanger 4

NCX:

Na+/Ca2+ exchanger

Nrp1:

Neuropilin 1

OB:

Olfactory bulb

OE:

Olfactory epithelium

OMP:

Olfactory marker protein

OR:

Olfactory receptor

ORN:

Olfactory receptor neuron

PDE:

Phosphodiesterases

PlxnA1:

Plexin A1

Sus:

 Sustentacular

WT:

Wild-type

References

  • Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48:417–430

    Article  CAS  PubMed  Google Scholar 

  • Akins MR, Berk-Rauch HE, Kwan KY et al (2017) Axonal ribosomes and mRNAs associate with fragile X granules in adult rodent and human brains. Hum Mol Genet 26:192–209

    CAS  PubMed  Google Scholar 

  • Akins MR, Leblanc HF, Stackpole EE et al (2012) Systematic mapping of fragile X granules in the mouse brain reveals a potential role for presynaptic FMRP in sensorimotor functions. J Comp Neurol 520:3687–3706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albeanu DF, Provost AC, Agarwal P et al (2018) Olfactory marker protein (OMP) regulates formation and refinement of the olfactory glomerular map. Nat Commun 9:5073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alvarez E, Zhou W, Witta SE et al (2005) Characterization of the Bex gene family in humans, mice, and rats. Gene 357:18–28

    Article  CAS  PubMed  Google Scholar 

  • Andres KH (1966) The fine structure of the olfactory region of macrosmatic animals. Z Zellforsch Mikrosk Anat 69:140–154

    Article  CAS  PubMed  Google Scholar 

  • Antolin S, Matthews HR (2007) The effect of external sodium concentration on sodium-calcium exchange in frog olfactory receptor cells. J Physiol 581:495–503

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Asan E, Drenckhahn D (2005) Immunocytochemical characterization of two types of microvillar cells in rodent olfactory epithelium. Histochem Cell Biol 123:157–168

    Article  CAS  PubMed  Google Scholar 

  • Baker H, Grillo M, Margolis FL (1989) Biochemical and immunocytochemical characterization of olfactory marker protein in the rodent central nervous system. J Comp Neurol 285:246–261

    Article  CAS  PubMed  Google Scholar 

  • Baldisseri DM, Margolis JW, Weber DJ et al (2002) Olfactory marker protein (OMP) exhibits a beta-Clam fold in solution: implications for target peptide interaction and olfactory signal transduction. J Mol Biol 319:823–837

    Article  CAS  PubMed  Google Scholar 

  • Barber PC, Jensen S, Zimmer J (1982) Differentiation of neurons containing olfactory marker protein in adult rat olfactory epithelium transplanted to the anterior chamber of the eye. Neurosci 7:2687–2695

    Article  CAS  Google Scholar 

  • Behrens M, Margolis JW, Margolis FL (2003) Identification of members of the Bex gene family as olfactory marker protein (OMP) binding partners. J Neurochem 86:1289–1296

    Article  CAS  PubMed  Google Scholar 

  • Belluscio L, Gold GH, Nemes A, Axel R (1998) Mice deficient in Golf are anosmic. Neuron 20:69–81

    Article  CAS  PubMed  Google Scholar 

  • Belluscio L, Katz LC (2001) Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21:2113–2122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belluscio L, Lodovichi C, Feinstein P et al (2002) Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature 419:296–300

    Article  CAS  PubMed  Google Scholar 

  • Billig GM, Pal B, Fidzinski P et al (2011) Ca2+-activated Cl- currents are dispensable for olfaction. Nat Neurosci 14:763–769

    Article  CAS  PubMed  Google Scholar 

  • Boccaccio A, Menini A (2007) Temporal development of cyclic nucleotide-gated and Ca2+-activated Cl- currents in isolated mouse olfactory sensory neurons. J Neurophysiol 98:153–160

    Article  CAS  PubMed  Google Scholar 

  • Bouslama M, Durand E, Chauviere L et al (2005) Olfactory classical conditioning in newborn mice. Behav Brain Res 161:102–106

    Article  PubMed  Google Scholar 

  • Breipohl W, Naguro T, Walker DG (1989) The postnatal development of Masera’s organ in the rat. Chem Senses 14:649–662

    Article  Google Scholar 

  • Brunet LJ, Gold GH, Ngai J (1996) General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681–693

    Article  CAS  PubMed  Google Scholar 

  • Buck LB (1996) Information coding in the mammalian olfactory system. Cold Spring Harb Symp Quant Biol 61:147–155

    Article  CAS  PubMed  Google Scholar 

  • Buiakova OI, Baker H, Scott JW et al (1996) Olfactory marker protein (OMP) gene deletion causes altered physiological activity of olfactory sensory neurons. Proc Natl Acad Sci USA 93:9858–9863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caggiano M, Kauer JS, Hunter DD (1994) Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13:339–352

    Article  CAS  PubMed  Google Scholar 

  • Carey RM, Verhagen JV, Wesson DW et al (2009) Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J Neurophysiol 101:1073–1088

    Article  PubMed  Google Scholar 

  • Carter LA, MacDonald JL, Roskams AJ (2004) Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24:5670–5683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao TI, Kasa P, Wolff JR (1997) Distribution of astroglia in glomeruli of the rat main olfactory bulb: exclusion from the sensory subcompartment of neuropil. J Comp Neurol 388:191–210

    Article  CAS  PubMed  Google Scholar 

  • Chong E, Moroni M, Wilson C et al (2020) Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception. Science 368

  • Cleland TA, Morse A, Yue EL et al (2002) Behavioral models of odor similarity. Behav Neurosci 116:222–231

    Article  PubMed  Google Scholar 

  • Connelly T, Savigner A, Ma M (2013) Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors. J Neurophysiol 110:55–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coronas-Samano G, Ivanova AV, Verhagen JV (2016) The habituation/cross-habituation test revisited: guidance from sniffing and video tracking. Neural Plast 2016:9131284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cygnar KD, Zhao H (2009) Phosphodiesterase 1C is dispensable for rapid response termination of olfactory sensory neurons. Nat Neurosci 12:454–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dibattista M, Pifferi S, Boccaccio A et al (2017) The long tale of the calcium activated Cl- channels in olfactory transduction. Channels (Austin) 11:399–414

    Article  Google Scholar 

  • Dibattista M, Reisert J (2016) The odorant receptor-dependent role of olfactory marker protein in olfactory receptor neurons. J Neurosci 36:2995–3006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doving KB (1965) Studies on the responses of bulbar neurons of frog to different odour stimuli. Rev Laryngol Otol Rhinol (Bord) 86(Suppl):845–854

    Google Scholar 

  • Engstrom B, Ekblom A, Hansson P (1989) The olfactory and respiratory epithelium in rhesus and squirrel monkeys studied with freeze-fracture technique. Acta Otolaryngol 108:259–267

    Article  CAS  PubMed  Google Scholar 

  • Firestein S (2001) How the olfactory system makes sense of scents. Nature 413:211–218

    Article  CAS  PubMed  Google Scholar 

  • Fleischer J, Schwarzenbacher K, Besser S et al (2006) Olfactory receptors and signalling elements in the Grueneberg ganglion. J Neurochem 98:543–554

    Article  CAS  PubMed  Google Scholar 

  • Fletcher M, Wilson DA (2001) Ontogeny of odor discrimination: a method to assess novel odor discrimination in neonatal rats. Physiol Behav 74:589–593

    Article  CAS  PubMed  Google Scholar 

  • Fluegge D, Moeller LM, Cichy A et al (2012) Mitochondrial Ca2+ mobilization is a key element in olfactory signaling. Nat Neurosci 15:754–762

    Article  CAS  PubMed  Google Scholar 

  • Friedrich RW, Korsching SI (1998) Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. The Journal of Neuroscience 18:9977–9988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedrich RW, Stopfer M (2001) Recent dynamics in olfactory population coding. Curr Opin Neurobiol 11:468–474

    Article  CAS  PubMed  Google Scholar 

  • Genovese F, Tizzano M (2018) Microvillous cells in the olfactory epithelium express elements of the solitary chemosensory cell transduction signaling cascade. PLoS ONE 13:e0202754

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Getchell TV, Shepherd GM (1978) Responses of olfactory receptor cells to step pulses of odour at different concentration in the salamander. J Physiol 282:521–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghatpande AS, Reisert J (2011) Olfactory receptor neuron responses coding for rapid odor sampling. J Physiol 589:2261–2273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gire DH, Schoppa NE (2009) Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J Neurosci 29:13454–13464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graziadei PP, Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1–18

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanchate NK, Kondoh K, Lu Z et al (2015) Single-cell transcriptomics reveals receptor transformations during olfactory neurogenesis. Science 350:1251–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison TA, Scott JW (1986) Olfactory bulb responses to odor stimulation: analysis of response pattern and intensity relationships. J Neurosci 56:1571–1589

    CAS  Google Scholar 

  • Hartman BK, Margolis FL (1975) Immunofluorescence localization of the olfactory marker protein. Brain Res 96:176–180

    Article  CAS  PubMed  Google Scholar 

  • Hayar A, Shipley MT, Ennis M (2005) Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms. J Neurosci 25:8197–8208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hegg CC, Jia C, Chick WS et al (2010) Microvillous cells expressing IP3 receptor type 3 in the olfactory epithelium of mice. Eur J Neurosci 32:1632–1645

    Article  PubMed  PubMed Central  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631

    Article  CAS  PubMed  Google Scholar 

  • Holbrook EH, Wu E, Curry WT et al (2011) Immunohistochemical characterization of human olfactory tissue. Laryngoscope 121:1687–1701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ihara N, Nakashima A, Hoshina N et al (2016) Differential expression of axon-sorting molecules in mouse olfactory sensory neurons. Eur J Neurosci 44:1998–2003

    PubMed  Google Scholar 

  • Imai T, Sakano H (2008) Odorant receptor-mediated signaling in the mouse. Curr Opin Neurobiol 18:251–260

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ivic L, Pyrski MM, Margolis JW et al (2000) Adenoviral vector-mediated rescue of the OMP-null phenotype in vivo. Nat Neurosci 3:1113–1120

    Article  CAS  PubMed  Google Scholar 

  • Iwata R, Kiyonari H, Imai T (2017) Mechanosensory-based phase coding of odor identity in the olfactory bulb. Neuron 96:1139–1152

    Article  CAS  PubMed  Google Scholar 

  • Jung A, Lischka FW, Engel J et al (1994) Sodium/calcium exchanger in olfactory receptor neurons of Xenopus laevis. NeuroReport 5:1741–1744

    Article  CAS  PubMed  Google Scholar 

  • Kang CW, Han YE, Lee MK et al (2018) Olfactory marker protein regulates prolactin secretion and production by modulating Ca2+ and TRH signaling in lactotrophs. Exp Mol Med 50:15

    Article  PubMed Central  Google Scholar 

  • Kang N, Bahk YY, Lee N et al (2015) Olfactory receptor Olfr544 responding to azelaic acid regulates glucagon secretion in alpha-cells of mouse pancreatic islets. Biochem Biophys Res Commun 460:616–621

    Article  CAS  PubMed  Google Scholar 

  • Kang N, Kim H, Jae Y et al (2015) Olfactory marker protein expression is an indicator of olfactory receptor-associated events in non-olfactory tissues. PLoS ONE 10:e0116097

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kasowski HJ, Kim H, Greer CA (1999) Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261–274

    Article  CAS  PubMed  Google Scholar 

  • Kass MD, Moberly AH, McGann JP (2013) Spatiotemporal alterations in primary odorant representations in olfactory marker protein knockout mice. PLoS ONE 8:e61431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kass MD, Moberly AH, Rosenthal MC et al (2013) Odor-specific, olfactory marker protein-mediated sparsening of primary olfactory input to the brain after odor exposure. J Neurosci 33:6594–6602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauer JS (1974) Response patterns of amphibian olfactory bulb neurons to odour stimulation. J Physiol 243:695–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauer JS, Shepherd GM (1977) Analysis of the onset phase of olfactory bulb unit responses to odour pulses in the salamander. J Physiol 272:495–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazi JU, Kabir NN, Rönnstrand L (2015) Brain-expressed X-linked (BEX) proteins in human cancers. Biochem Biophys Acta 1856:226–233

    CAS  PubMed  Google Scholar 

  • Keller A, Margolis FL (1975) Immunological studies of the rat olfactory marker protein. J Neurochem 24:1101–1106

    Article  CAS  PubMed  Google Scholar 

  • Kelliher KR, Ziesmann J, Munger SD et al (2003) Importance of the CNGA4 channel gene for odor discrimination and adaptation in behaving mice. Proc Natl Acad Sci USA 100:4299–4304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koo JH, Gill S, Pannell LK et al (2004) The interaction of Bex and OMP reveals a dimer of OMP with a short half-life. J Neurochem 90:102–116

    Article  CAS  PubMed  Google Scholar 

  • Koo JH, Saraswati M, Margolis FL (2005) Immunolocalization of Bex protein in the mouse brain and olfactory system. J Comp Neurol 487:1–14

    Article  CAS  PubMed  Google Scholar 

  • Korsak LIT, Shepard KA, Akins MR (2017) Cell type-dependent axonal localization of translational regulators and mRNA in mouse peripheral olfactory neurons. J Comp Neurol 525:2202–2215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosaka K, Toida K, Margolis FL et al (1997) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb–II. Prominent differences in the intraglomerular dendritic arborization and their relationship to olfactory nerve terminals. Neurosci 76:775–786

    Article  CAS  Google Scholar 

  • Kream RM, Margolis FL (1984) Olfactory marker protein: turnover and transport in normal and regenerating neurons. J Neurosci 4:868–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusumakshi S, Voigt A, Hubner S et al (2015) A binary genetic approach to characterize TRPM5 cells in mice. Chem Senses 40:413–425

    Article  CAS  PubMed  Google Scholar 

  • Kwon HJ, Koo JH, Zufall F et al (2009) Ca extrusion by NCX is compromised in olfactory sensory neurons of OMP mice. PLoS ONE 4:e4260

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee AC, He J, Ma M (2011) Olfactory marker protein is critical for functional maturation of olfactory sensory neurons and development of mother preference. J Neurosci 31:2974–2982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linster C, Cleland TA (2009) Glomerular microcircuits in the olfactory bulb. Neural Net 22:1169–1173

    Article  Google Scholar 

  • Lodovichi C, Belluscio L (2012) Odorant receptors in the formation of the olfactory bulb circuitry. Physiology 27:200–212

    Article  CAS  PubMed  Google Scholar 

  • Lorenzon P, Redolfi N, Podolsky MJ et al (2015) Circuit formation and function in the olfactory bulb of mice with reduced spontaneous afferent activity. J Neurosci 35:146–160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Magklara A, Yen A, Colquitt BM et al (2011) An epigenetic signature for monoallelic olfactory receptor expression. Cell 145:555–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makeyeva Y, Nicol C, Ledger WL et al (2020) Immunocytochemical localization of olfactory-signaling molecules in human and rat spermatozoa. J Histochem Cytochem 68:491–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margolis FL (1972) A brain protein unique to the olfactory bulb. Proc Natl Acad Sci USA 69:1221–1224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margolis FL, Tarnoff JF (1973) Site of biosynthesis of the mouse brain olfactory bulb protein. J Biol Chem 248:451–455

    Article  CAS  PubMed  Google Scholar 

  • Maritan M, Monaco G, Zamparo I et al (2009) Odorant receptors at the growth cone are coupled to localized cAMP and Ca2+ increases. Proc Natl Acad Sci USA 106:3537–3542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathews DF (1972) Response pattern of single neurons in the tortoise olfactory epithelium and olfactory bulb. J Gen Physiol 60:166–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNamara AM, Magidson PD, Linster C et al (2008) Distinct neural mechanisms mediate olfactory memory formation at different timescales. Learn Mem 15:117–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menco BP (1980) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory structures of frog, ox, rat, and dog. I. A general survey Cell Tissue Res 207:183–209

    CAS  PubMed  Google Scholar 

  • Meredith M (1986) Patterned response to odor in mammalian olfactory bulb: the influence of intensity. J Neurosci 56:572–597

    CAS  Google Scholar 

  • Michalakis S, Reisert J, Geiger H et al (2006) Loss of CNGB1 protein leads to olfactory dysfunction and subciliary cyclic nucleotide-gated channel trapping. J Biol Chem 281:35156–35166

    Article  CAS  PubMed  Google Scholar 

  • Mombaerts P (2006) Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22:713–737

    Article  CAS  PubMed  Google Scholar 

  • Montani G, Tonelli S, Elsaesser R et al (2006) Neuropeptide Y in the olfactory microvillar cells. Eur J Neurosci 24:20–24

    Article  PubMed  Google Scholar 

  • Monti-Graziadei GA, Margolis FL, Harding JW et al (1977) Immunocytochemistry of the olfactory marker protein. J Histochem Cytochem 25:1311–1316

    Article  CAS  PubMed  Google Scholar 

  • Moran DT, Rowley JC 3rd, Jafek BW (1982) Electron microscopy of human olfactory epithelium reveals a new cell type: the microvillar cell. Brain Res 253:39–46

    Article  CAS  PubMed  Google Scholar 

  • Moran DT, Rowley JC 3rd, Jafek BW et al (1982) The fine structure of the olfactory mucosa in man. J Neurocytol 11:721–746

    Article  CAS  PubMed  Google Scholar 

  • Morrison EE, Costanzo RM (1990) Morphology of the human olfactory epithelium. J Comp Neurol 297:1–13

    Article  CAS  PubMed  Google Scholar 

  • Morrison EE, Costanzo RM (1992) Morphology of olfactory epithelium in humans and other vertebrates. Microsc Res Tech 23:49–61

    Article  CAS  PubMed  Google Scholar 

  • Naderi A (2019) Molecular functions of brain expressed X-linked 2 (BEX2) in malignancies. Exp Cell Res 376:221–226

    Article  CAS  PubMed  Google Scholar 

  • Nagayama S, Homma R, Imamura F (2014) Neuronal organization of olfactory bulb circuits. Front Neural Circuits 8:98

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakashima A, Ihara N, Shigeta M et al (2019) Structured spike series specify gene expression patterns for olfactory circuit formation. Science 365(6448):eaaw5030

    Article  CAS  PubMed  Google Scholar 

  • Nakashima A, Takeuchi H, Imai T et al (2013) Agonist-independent GPCR activity regulates anterior-posterior targeting of olfactory sensory neurons. Cell 154:1314–1325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima N, Nakashima K, Taura A et al (2020) Olfactory marker protein directly buffers cAMP to avoid depolarization-induced silencing of olfactory receptor neurons. Nat Commun 11:2188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neureither F, Stowasser N, Frings S et al (2017) Tracking of unfamiliar odors is facilitated by signal amplification through anoctamin 2 chloride channels in mouse olfactory receptor neurons. Physiol Rep 5(15):e13373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Noe J, Tareilus E, Boekhoff I et al (1997) Sodium/calcium exchanger in rat olfactory neurons. Neurochem Int 30:523–531

    Article  CAS  PubMed  Google Scholar 

  • O’Connell RJ, Mozell MM (1969) Quantitative stimulation of frog olfactory receptors. J Neurophysiol 32:51–63

    Article  CAS  PubMed  Google Scholar 

  • Perez-Orive J, Mazor O, Turner GC et al (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297:359–365

    Article  CAS  PubMed  Google Scholar 

  • Peterson J, Lin B, Barrios-Camacho CM et al (2019) Activating a reserve neural stem cell population in vitro enables engraftment and multipotency after transplantation. Stem Cell Rep 12:680–695

    Article  CAS  Google Scholar 

  • Pietra G, Dibattista M, Menini A et al (2016) The Ca2+-activated Cl- channel TMEM16B regulates action potential firing and axonal targeting in olfactory sensory neurons. J Gen Physiol 148:293–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piper M, van Horck F, Holt C (2007) The role of cyclic nucleotides in axon guidance. Adv Exp Med Biol 621:134–143

    Article  PubMed  PubMed Central  Google Scholar 

  • Pluznick JL, Zou DJ, Zhang X et al (2009) Functional expression of the olfactory signaling system in the kidney. Proc Natl Acad Sci USA 106:2059–2064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pronin A, Levay K, Velmeshev D et al (2014) Expression of olfactory signaling genes in the eye. PLoS ONE 9:e96435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rankin CH, Abrams T, Barry RJ et al (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92:135–138

    Article  PubMed  Google Scholar 

  • Rasche S, Toetter B, Adler J et al (2010) Tmem16b is specifically expressed in the cilia of olfactory sensory neurons. Chem Senses 35:239–245

    Article  CAS  PubMed  Google Scholar 

  • Reisert J (2010) Origin of basal activity in mammalian olfactory receptor neurons. J Gen Physiol 136:529–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisert J, Matthews HR (1998) Na+-dependent Ca2+ extrusion governs response recovery in frog olfactory receptor cells. J Gen Physiol 112:529–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisert J, Matthews HR (1999) Adaptation of the odour-induced response in frog olfactory receptor cells. J Physiol 519:801–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisert J, Matthews HR (2001) Responses to prolonged odour stimulation in frog olfactory receptor cells. J Physiol 534:179–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisert J, Yau KW, Margolis FL (2007) Olfactory marker protein modulates the cAMP kinetics of the odour-induced response in cilia of mouse olfactory receptor neurons. J Physiol 585:731–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisert J, Zhao H (2011) Perspectives on: Information and coding in mammalian sensory physiology: response kinetics of olfactory receptor neurons and the implications in olfactory coding. J Gen Physiol 138:303–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Riera CE, Tsaousidou E, Halloran J et al (2017) The sense of smell impacts metabolic health and obesity. Cell Metab 26(198–211):e195

    Google Scholar 

  • Rodriguez-Gil DJ, Bartel DL, Jaspers AW et al (2015) Odorant receptors regulate the final glomerular coalescence of olfactory sensory neuron axons. Proc Natl Acad Sci USA 112:5821–5826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers KE, Dasgupta P, Gubler U et al (1987) Molecular cloning and sequencing of a cDNA for olfactory marker protein. Proc Natl Acad Sci USA 84:1704–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rössler P, Mezler P, Breer H (1998) Two olfactory marker proteins in Xenopus laevis. J Comp Neurol 395:273–280

    Article  PubMed  Google Scholar 

  • Royal SJ, Key B (1999) Development of P2 olfactory glomeruli in P2-internal ribosome entry site-tau-lacZ transgenic mice. J Neurosci 19:9856–9864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakano H (2020) Developmental regulation of olfactory circuit formation in mice. Dev Growth Differ 62:199–213

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmid A, Pyrski M, Biel M et al (2010) Grueneberg ganglion neurons are finely tuned cold sensors. J Neurosci 30:7563–7568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoppa NE, Urban NN (2003) Dendritic processing within olfactory bulb circuits. Trends Neurosci 26:501–506

    Article  CAS  PubMed  Google Scholar 

  • Schwob JE, Huard JM, Luskin MB et al (1994) Retroviral lineage studies of the rat olfactory epithelium. Chem Senses 19:671–682

    Article  CAS  PubMed  Google Scholar 

  • Schwob JE, Jang W, Holbrook EH, Lin B, Herrick DB, Peterson JN, Hewitt Coleman J (2017) Stem and progenitor cells of the mammalian olfactory epithelium: taking poietic license. J Comp Neurol 525:1034–1054

    Article  CAS  PubMed  Google Scholar 

  • Scott JW, Scott-Johnson PE (2002) The electroolfactogram: a review of its history and uses. Microsc Res Tech 58:152–160

    Article  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 127:1057–1069

    Article  CAS  PubMed  Google Scholar 

  • Shepherd GM (1972) Synaptic organization of the mammalian olfactory bulb. Physiol Rev 52:864–917

    Article  CAS  PubMed  Google Scholar 

  • Smith PC, Firestein S, Hunt JF (2002) The crystal structure of the olfactory marker protein at 2.3 a resolution. J Mol Biol 319:807–821

    Article  CAS  PubMed  Google Scholar 

  • Soucy ER, Albeanu DF, Fantana AL et al (2009) Precision and diversity in an odor map on the olfactory bulb. Nat Neurosci 12:210–220

    Article  CAS  PubMed  Google Scholar 

  • Spors H, Grinvald A (2002) Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34:301–315

    Article  CAS  PubMed  Google Scholar 

  • Spors H, Wachowiak M, Cohen LB et al (2006) Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 26:1247–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Springer MS, Gatesy J (2017) Inactivation of the olfactory marker protein (OMP) gene in river dolphins and other odontocete cetaceans. Mol Phylogenet Evol 109:375–387

    Article  CAS  PubMed  Google Scholar 

  • St John JA, Key B (2001) EphB2 and two of its ligands have dynamic protein expression patterns in the developing olfactory system. Brain Res Dev Brain Res 126:43–56

    Article  CAS  PubMed  Google Scholar 

  • St John JA, Key B (2005) Olfactory marker protein modulates primary olfactory axon overshooting in the olfactory bulb. J Comp Neurol

  • Stephan AB, Shum EY, Hirsh S et al (2009) ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci USA 106:11776–11781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephan AB, Tobochnik S, Dibattista M et al (2012) The Na+/Ca2+ exchanger NCKX4 governs termination and adaptation of the mammalian olfactory response. Nat Neurosci 15:131–137

    Article  CAS  Google Scholar 

  • Stewart WB, Kauer JS, Shepherd GM (1979) Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. J Comp Neurol 185:715–734

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Nikaido M, Hagino-Yamagishi K et al (2015) Distinct functions of two olfactory marker protein genes derived from teleost-specific whole genome duplication. BMC Evol Biol 15:245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Syed AS, Sansone A, Nadler W et al (2013) Ancestral amphibian v2rs are expressed in the main olfactory epithelium. Proc Natl Acad Sci USA 110:7714–7719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43

    Article  CAS  PubMed  Google Scholar 

  • Tirindelli R, Dibattista M, Pifferi S et al (2009) From pheromones to behavior. Physiol Rev 89:921–956

    Article  CAS  PubMed  Google Scholar 

  • Tirindelli R, Ryba NJP (1996) The G-protein gamma-subunit G gamma 8 is expressed in the developing axons of olfactory and vomeronasal neurons. Eur J Neurosci 8:2388–2398

    Article  CAS  PubMed  Google Scholar 

  • Uchida N, Takahashi YK, Tanifuji M et al (2000) Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci 3:1035–1043

    Article  CAS  PubMed  Google Scholar 

  • Ukhanov K, Bobkov YV, Martens JR et al (2019) Initial characterization of a subpopulation of inherent oscillatory mammalian olfactory receptor neurons. Chem Senses 44:583–592

    Article  PubMed  PubMed Central  Google Scholar 

  • Vassar R, Chao SK, Sitcheran R et al (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981–991

    Article  CAS  PubMed  Google Scholar 

  • Verhaagen J, Oestreicher AB, Gispen WH et al (1989) The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J Neurosci 9:683–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wachowiak M, Cohen LB (2003) Correspondence between odorant-evoked patterns of receptor neuron input and intrinsic optical signals in the mouse olfactory bulb. J Neurophysiol 89:1623–1639

    Article  PubMed  Google Scholar 

  • Wachowiak M, Denk W, Friedrich RW (2004) Functional organization of sensory input to the olfactory bulb glomerulus analyzed by two-photon calcium imaging. Proc Natl Acad Sci USA 101:9097–9102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wachowiak M, Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol

  • Weiler E, Farbman AI (2003) The septal organ of the rat during postnatal development. Chem Senses 28:581–593

    Article  PubMed  Google Scholar 

  • Whitesell JD, Sorensen KA, Jarvie BC et al (2013) Interglomerular lateral inhibition targeted on external tufted cells in the olfactory bulb. J Neurosci 33:1552–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willmore B, Tolhurst DJ (2001) Characterizing the sparseness of neural codes. Network 12:255–270

    Article  CAS  PubMed  Google Scholar 

  • Wong ST, Trinh K, Hacker B et al (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487–497

    Article  CAS  PubMed  Google Scholar 

  • Wright NT, Margolis JW, Margolis FL et al (2005) Refinement of the solution structure of rat olfactory marker protein (OMP). J Biomol NMR 33:63–68

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Greer CA, Shepherd GM (2000) Odor maps in the olfactory bulb. J Comp Neurol 422:489–495

    Article  CAS  PubMed  Google Scholar 

  • Youngentob SL, Kent PF, Margolis FL (2003) OMP gene deletion results in an alteration in odorant-induced mucosal activity patterns. J Neurophysiol 13:13

    Google Scholar 

  • Youngentob SL, Margolis FL (1999) OMP gene deletion causes an elevation in behavioral threshold sensitivity. NeuroReport 10:15–19

    Article  CAS  PubMed  Google Scholar 

  • Youngentob SL, Margolis FL, Youngentob LM (2001) OMP gene deletion results in an alteration in odorant quality perception. Behav Neurosci 115:626–631

    Article  CAS  PubMed  Google Scholar 

  • Youngentob SL, Pyrski MM, Margolis FL (2004) Adenoviral vector-mediated rescue of the OMP-null behavioral phenotype: enhancement of odorant threshold sensitivity. Behav Neurosci 118:636–642

    Article  CAS  PubMed  Google Scholar 

  • Yu CR, Power J, Barnea G et al (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553–566

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by NIH/NIDCD grants R01DC016647 (JR) and R21DC018358 (FG). DAK is supported by NIH/NIDCD-funded Monell Institutional Training Grant T32DC000014.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johannes Reisert.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dibattista, M., Al Koborssy, D., Genovese, F. et al. The functional relevance of olfactory marker protein in the vertebrate olfactory system: a never-ending story. Cell Tissue Res 383, 409–427 (2021). https://doi.org/10.1007/s00441-020-03349-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-020-03349-9

Keywords

Navigation