Insect Olfaction Papers

Select Insect Olfaction Papers: Vogt Lab

1. Overview of olfaction in insects.

2. Metamorphosis

3. Chemosensory Sytems of Drosophila

4. Chemosensory Learning and Behavior -- Drosophila

5. Olfactory Sensilla: types, morphology, development.

6. Vertebrate Odor Receptors and Organization of Olfactory Neurons

7. VOGT PAPERS

BIOCHEMISTRY OF ODOR DETECTION: ORIGINS AND OVERVIEW
Odorant Binding Proteins (OBPs)
Odor Degrading Enzymes (ODEs)
SNMPs

Overview of olfaction in insects: perspectives from Moths (Hansson) and flies (Vosshall)

PDF Hansson BS (2002) A bug's smell - research into insect olfaction. Trends in Neuroscience. 25, 270-274. [An excellent overview of odor processing in moths. This story long preceedes the comparable story in Drosophila. However, moth and fly workers represent two very different cultures, and the perspectives presented by these two cultures offer unique insights. This short paper reviews odor detection to mushroom bodies and protocerebrum. Read this along with the Vosshall papers.]
PDF Vosshall LB (2000) Olfaction in Drosophila. Current Opinions in Neurobiology 10, 498?503. [Review of Drosophila Odor Receptors, about a year following their identification. Focus is on the diversity of ORs, and on the projections of neurons expressing specific OR genes.]
PDF Vosshall LB, Keller A (2003) Decoding olfaction in Drosophila. Current Opinions in Neurobiology 13, 103?110. [Update of their earlier review, focusing more on the olfactory neural pathways. This review complements the one of Hansson, from a different perspective. The pathways described start with primary sensory neurons which synapse onto projection neurons in the olfactory lobe (in glomerulae); projection neurons project to the protocerebrum (lateral horns), passing through and making "side synapses" with neurons of the mushroom bodies. No one has any idea what happens in either the mushroom bodies or the protocerebrum, besides combining olfactory information with that of other sensory modalities.]

Metamorphosis

PDF Tissot M, Stocker RF (2000) Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Progress in Neurobiology 62, 89-111.
[The major context of the work done in our lab may be viewed as strongly related to metamorphosis. This is an excellent overview.]

Chemosensory Sytems of Drosophila

PDF Stocker RF (1994). The organization of the chemosensory system in Drosophila melanogaster: a review. Cell and Tissue Research 275, 3?26. [Stocker has been a long standing and important contributor to Drosophila neurobiology, especially re. olfactory neural pathways. This is an imporant review, describing chemosensory pathways in both adults and larvae. A figure in the review is freqently seen in more recent papers by many authors.]
PDF de Bruyne M, Foster K and Carlson JR (2001). Odor coding in the Drosophila antenna. Neuron 30, 537?552. [An excellent study characterizing the physiological responses of basiconic sensilla. Drosophila antenna has three morphological classes of olfactory sensilla: trichodea, basiconica and coeloconica. The paper demonstrates that the basiconic sensilla can be subdivided into a number of distinct subclasses based on their odor sensitivities. The odors used in this study are not necessarily behaviorally relevant. The study by Stensmyr et al. (2003) identifies behaviorally relevant odorants.]
PDF Stensmyr MC, Giordano E, Balloi A, Angioy A-M, Hansson BS (2003) Novel natural ligands for Drosophila olfactory receptor neurones. Journal of Experimental Biology 206, 715-724. [Identification of behaviorally relevant odors. Product of an important and creative Swedish laboratory. ]

Chemosensory Learning and Behavior -- Drosophila.

PDF Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807.
PDF Stensmyr MC, Giordano E, Balloi A, Angioy A-M, Hansson BS (2003) Novel natural ligands for Drosophila olfactory receptor neurones. Journal of Experimental Biology 206, 715-724. [Use of T-maze assay to confirm behavioral relvance of antennal recordings]
PDF Scherer S, Stocker RF, Gerber B (2003) Olfactory learning in individually assayed Drosophila larvae. Learning and Memory 10, 217-225.
[Assay details; includes explanation of odor choice.]
PDF Gerber B, Scherer S, Neuser K, Michels B, Hendel T, Stocker RF, Heisenberg M. (2004) Visual learning in individually assayed Drosophila larvae. J. Exp. Biol. 207, 179-188.
[Assay details.]
PDF Gerber B, Tanimoto H, Heisenberg M (2004) An engram found? Evaluating the evidence from fruit flies. Current Opinion in Neurobiology 14, 737-744.
[Use of the same T-maze apparatus used in above Stensmyr etal (2003) paper.]
PDF Michels B, Diegelmann S, Tanimoto H, Schwenkert I, Buchner E, Gerber B (2005) A role for Synapsin in associative learning: The Drosophila larva as a study case. Learning and Memory 12, 224-231.
[Use of associative learning assay (petri dish), and as well showing surprisingly minimal effects of synapsin deletion on learning. ]
PDF Neuser K, Husse J, Stock P, Gerber B (2005) Appetitive olfactory learning in Drosophila larvae: effects of repetition, reward strength, age, gender, assay type and memory span. Animal Behavior, 69, 891-898.
[Details / methodology of associative learning assay (petri dish).]
PDF Hendel T, Michels B, Neuser K, Schipanski A, Haum K, Sokolowski MB, Marohn F, Michel R, Heisenberg M, Gerber B J. (2005) The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. Comp. Physiol. A 191, 265-279.
[Study of fructose, salt and quinine on associative and non-associative learning of Drosophila larvae, petri dish assay.]
PDF Cobb M, Domain I (2000) Olfactory coding in a simple system: adaptation in Drosophila larvae. Proc. Roy. Soc. London B 267, 2119-2125.
[An alternative petri dish assay -- adaptation / cross adaptation]
PDF Boyle J, Cobb M (2005) Olfactory coding in Drosophila larvae investigated by cross-adaptation. J. Exp. Biol. 208, 3483-3491.

Olfactory Sensilla: types, morphology, development.

PDF Shanbhag SR, M?ller B, Steinbrecht RA (1999) Atlas of olfactory organs of Drosophila melanogaster. I. Types, external organization, innervation and distribution of olfactory sensilla. International Journal of Insect Morphology Embryology 28, 377-397. [An excellent study of the morphology of Drosophila antennae, with specific focus on the types of chemosensory/olfactory sensilla on the antennae.]
PDF Steinbrecht RA (1997) Pore structures in insect olfactory sensilla: a review of data and concepts. International Journal of Insect Morphology and Embryology. 26, 229-245. [Insect olfactory sensilla are cuticular hair-like structures that ensheath the sensory neurons. Odors have to pass through the cuticle walls to gain access; passage is thought to be via pores/holes through the cuticle. Understanding these pores has been critical to various models suggesting how odors are detected. When I started, the pores were thought to extend to the neurons via small tubules. I challanged and evidently destroyed that notion by suggesting that odors were transported to the neurons via Odorant Binding Proteins (see Vogt et al., 1985, PNAS). Steinbrecht is the world authority on the morphology of insect sensilla; this is a summary of the history of pore-tubules ? a tale he has had a great deal to do with.]
PDF Keil TA (1997) Comparative morphogenesis of sensilla: a review. International Journal of Insect Morphologys and Embryology. 26, 151-160. [Development of sensory hairs is an important story that started in the 1950s. Sensilla include several cell types, including three support cells (trichogen, tormogen and thecogen plus 1 to several neurons. Each sensillum with its 4+ cells comprises a complete olfactory organ. Each cell type has a different function, and the question is how do these cells get toghether. There are two prevailing views, the most interesting of which is that the cells are all releated. A sensory mother cell divides, and these progeny divide again to produce the distinct cell types. This system (really, mechanosensory sensilla of the Drosophila larva) has been a model of how such phenotypic assymetry can be established. Keil's paper is merely a review of the morphological observations that argue in favor of sensory mother cells. The alternative view is that the cells simply associate with one another during development (based on experiments in Drosophila. I am actually very interested in understanding olfactory development in both Drosophila and Manduca to test such differences.]

Vertebrate Odor Receptors and the Organization of Olfactory Neurons

PDF Korsching S (2002) Olfactory maps and odor images. Current Opinions in Neurobiology 12, 387?392. [Korshing has been a leader in olfactory neurobiology of zebrafish; this is an excellent review of neuroanatomy and olfactory coding in vertebrates ? remarkable similarity to insects.]
PDF Vosshall LB (2003) Putting smell on the map. Trends in Neuroscience 26, 169-170.[Vertebrate Olfaction: organization with interesting parallels with insect olfaction. Vosshall came from a lab (Richard Axel) that has been important in identifying olfactory pathways and genetics in vertebrates and in Drosophila, and thus has a unique perspective.]

VOGT PAPERS

BIOCHEMISTRY OF ODOR DETECTION: ORIGINS AND OVERVIEW

PDF

Pheromone binding and inactivation by moth antennae.

Nature

[ Identification of Odorant Binding Proteins and Odor Degrading Enzymes. I fit these proteins into an exisiting model for odor detection that involved pore-tubules as the delivery mechanism for transporting odors from air to neuron. ]

PDF Vogt RG, Riddiford LM, Prestwich GD (1985). Kinetic properties of a pheromone degrading enzyme: the sensillar esterase of Antheraea polyphemus. Proceedings National Academy of Sciences, U.S.A. 82, 8827-8831.
[NEW MODEL for odor detection. Enzyme degrades pheromone very fast. Had learned that contacts between pore-tubules and dendrites were rare. Proposed OBPs act as transporters, binding pheromone molecules and delivering them to receptors; enzymes degrade the pheromones. ]

PDF Vogt RG (2004) Molecular basis of pheromone detection in insects. In Comprehensive Insect Physiology, Biochemistry, Pharmacology and Molecular Biology. (LI Gilbert, K Iatro, S Gill eds). Elsevier. In Press (Submitted 9/03, to be published 2004).
[My most comprehensive review on the biochemistry of odor detection in insects, focusing on but not exclusive to pheromone detection. ]

OBP History

PDF

Pheromone binding and inactivation by moth antennae.

Nature

[Paper starting it all ? identification of first insect OBP and ODE: Pheromone Binding Protein (PBP) and Sensilla Esterase (SE).]

PDF Vogt RG, Koehne AC, Dubnau JT, Prestwich GD (1989). Expression of pheromone binding proteins during antennae development in the gypsy moth Lymantria dispar. Journal of Neuroscience 9, 3332-3346.
[Characterization of PBPs in gypsy moth; establishing first developmental protocols.]

Vogt RG, Prestwich GD, Lerner MR (1991). Odorant-Binding-Protein subfamilies associate with distinct classes of olfactory receptor neurons in insects. Journal of Neurobiology 22, 74-84.
[Demonstration that PBPs are part of a larger OBP family: PBPs GOBP1, GOBP2.]

Vogt RG, Rybczynski R, Lerner MR (1991). Molecular cloning and sequencing of General-Odorant Binding Proteins GOBP1 and GOBP2 from the Tobacco Hawk Moth Manduca sexta: Comparisons with other insect OBPs and their signal peptides. Journal of Neuroscience 11, 2972-2984.
[Clonining GOBPs; PBPs were being cloned by other labs]

Vogt RG,Rybczynski R, Cruz M, Lerner MR (1993) Ecdysteroid regulation of olfactory protein expression in the developing antenna of the tobacco hawk moth, Manduca sexta. Journal of Neurobiology 22, 581-597.
[Title says it all; most of the genes and processes we study are regulated by ecdysteroids.]

PDF Dickens JC, Callahan FE, Wergin WP, Murphy CA, Vogt RG (1998) Immunolocalization and Intergeneric Distribution of a Putative Odorant-Binding Protein in True Bugs (Heteroptera: Miridae). Journal of Experimental Biology , 201, 33-41.
[This and following paper: important comparative study ? identification of an OBP in a bug indicated gene family was ancestral to the holometabolous and hemipteran lineages. Now also known from orthopteroids, indicating the genes are ancestral to neopterous insects.]

PDF Vogt RG, Callahan FE, Rogers ME, and Dickens JC (1999) Odorant Binding Protein Diversity and Distribution among the Insect Orders, as indicated by LAP, an OBP-related protein of the True Bug Lygus lineolaris (Hemiptera, Heteroptera). Chemical Senses 24, 481-495.
[This and preceeding paper: important comparative study ? identification of an OBP in a bug indicated gene family was ancestral to the holometabolous and hemipteran lineages. Now also known from orthopteroids, indicating the genes are ancestral to neopterous insects.]

PDF Vogt RG, Rogers ME, Franco M-d, Sun M (2002). A Comparative Study of Odorant Binding Protein Genes: Differential Expression of the PBP1 - GOBP2 Gene Cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). Journal of Experimental Biology 205, 719-744.
[Expression of PBPs/GOBPs in larval and adult Manduca, as well as characterization of Manduca and Drosophila OBP genes.]

PDF Vogt RG (2002) Odorant Binding Proteins of the Malaria Mosquito Anopheles gambiae; Possible Orthologues of the OS-E and OS-F OBPs of Drosophila melanogaster. Journal of Chemical Ecology 28, 2371-2376.
[Genomic / bioinformatic study of mosquito and fly OBP genes.]

SNMPs

PDF

Sex-pheromone receptor proteins: visualization using a radiolabeled photoaffinity analog.

Journal of Biological Chemistry

[ID of a candidate OR using a radioactive pheromone analog ? protein identified here prompted identification of SNMPs.]

PDF Rogers M, Sun M, Lerner MR, Vogt RG (1997) Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins. Journal of Biological Chemistry 272, 14792-14804.
[Cloning and characterization of SNMP1 in silk moth.]

PDF Rogers ME, Steinbrecht RA, Vogt RG (2001) Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus. Cell and Tissue Research, 303, 433-446.
[Localization of SNMP protein in neurons.]

PDF Rogers ME, Krieger J, Vogt RG (2001) Antennal SNMPs (Sensory Neuron Membrane Proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. Journal of Neurobiology 49, 47-61.
[Identification /cloning of SNMPs from several species.]

PDF Krieger J, Raming K, Dewer YME, Bete S, Conzelmann S, Breer H (2002) A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. European Journal of Neuroscience 16, 619-628.
[NOT one of mine. But Krieger used SNMP to counter stain olfactory receptor neurons while characterizing the more restricted expression of OR genes.]

ODEs

Scale esterase: a pheromone degrading enzyme from the wing scales of the silk moth Antheraea polyphemus.

J. Chem. Ecol.

[ODEs covering body surface ? behaviorally relevant genes are not exclusively expressed in neurons.]

PDF Vogt RG, Riddiford LM, Prestwich GD (1985). Kinetic properties of a pheromone degrading enzyme: the sensillar esterase of Antheraea polyphemus. Proceedings National Academy of Sciences, U.S.A. 82, 8827-8831.
[Characterization of antennal esterase suggests new model for odor detection: OBP transport and ODE signal termination.]

PDF Rybczynski R, Vogt RG, Lerner, MR (1990). Antennal-specific pheromone-degrading aldehyde oxidases from the moths Antheraea polyphemus and Bombyx mori. Journal of Biological Chemistry 32, 19712-14715.
[ODEs characterized in several species.]

PDF Rogers ME, Jani MK, Vogt RG (1999) An olfactory specific glutathione S-transferase in the Sphinx moth Manduca sexta. Journal of Experimental Biology, 202, 1625-1637.
[Biotransformation Enzymes as candidate ODEs]

PDF Ishida Y, Leal WS (2002) Cloning of putative odorant-degrading enzyme and integumental estease cDNAs from the wild silkmoth, Antheraea polyphemus. Insect Biochemistry and Molecular Biology. 32, 1775-1780. [Work of a colleague, but cloning of the enzymes that "started it all": SE of A. polyphemus]