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Dual processing of sulfated steroids in the olfactory system of an anuran amphibian.

Sansone A, Hassenklöver T, Offner T, Fu X, Holy TE, Manzini I - Front Cell Neurosci (2015)

Bottom Line: Chemical communication is widespread in amphibians, but if compared to later diverging tetrapods the available functional data is limited.Furthermore, we found that larval and adult animals excrete multiple sulfated compounds with physical properties consistent with sulfated steroids.Breeding tadpole and frog water including these compounds activated a large subset of sensory neurons that also responded to synthetic steroids, showing that sulfated steroids are likely to convey intraspecific information.

View Article: PubMed Central - PubMed

Affiliation: Institute of Neurophysiology and Cellular Biophysics, University of Göttingen Göttingen, Germany ; Center for Nanoscale Microscopy and Molecular Physiology of the Brain Göttingen, Germany.

ABSTRACT
Chemical communication is widespread in amphibians, but if compared to later diverging tetrapods the available functional data is limited. The existing information on the vomeronasal system of anurans is particularly sparse. Amphibians represent a transitional stage in the evolution of the olfactory system. Most species have anatomically separated main and vomeronasal systems, but recent studies have shown that in anurans their molecular separation is still underway. Sulfated steroids function as migratory pheromones in lamprey and have recently been identified as natural vomeronasal stimuli in rodents. Here we identified sulfated steroids as the first known class of vomeronasal stimuli in the amphibian Xenopus laevis. We show that sulfated steroids are detected and concurrently processed by the two distinct olfactory subsystems of larval Xenopus laevis, the main olfactory system and the vomeronasal system. Our data revealed a similar but partially different processing of steroid-induced responses in the two systems. Differences of detection thresholds suggest that the two information channels are not just redundant, but rather signal different information. Furthermore, we found that larval and adult animals excrete multiple sulfated compounds with physical properties consistent with sulfated steroids. Breeding tadpole and frog water including these compounds activated a large subset of sensory neurons that also responded to synthetic steroids, showing that sulfated steroids are likely to convey intraspecific information. Our findings indicate that sulfated steroids are conserved vomeronasal stimuli functioning in phylogenetically distant classes of tetrapods living in aquatic and terrestrial habitats.

No MeSH data available.


Related in: MedlinePlus

Sulfated steroids are processed in the olfactory bulb. (A) 3D rendering of reactive volumes in the MOB (left hand side) and AOB (right hand side) upon mucosal application of E and P mix (E mix-responsive areas, blue; P mix-responsive areas, red). Active regions always contained both cell somata and glomerular structures. Schematics of the olfactory bulb in the upper part show the approximate location of the responsive regions. (B) Calcium responses of the glomerular regions indicated by an arrow and green color in A (MOB, green traces; AOB, magenta traces). Amino acid mixture (AA, 100 μM) was applied as a positive control for activation of the MOB. (C) Representative calcium responses of mitral/tufted cells in the MOB (green) and AOB (magenta) upon mucosal application of sulfated steroids (E mix and P mix, 200 μM) and amino acids (AA, 100 μM). In both main and accessory olfactory bulb, mitral/tufted cells were activated by either E or P steroids, or both stimuli. Amino acids only elicited calcium responses in mitral/tufted cells of the MOB. Similar results were obtained in 4 MOBs and 3 AOBs.
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Figure 4: Sulfated steroids are processed in the olfactory bulb. (A) 3D rendering of reactive volumes in the MOB (left hand side) and AOB (right hand side) upon mucosal application of E and P mix (E mix-responsive areas, blue; P mix-responsive areas, red). Active regions always contained both cell somata and glomerular structures. Schematics of the olfactory bulb in the upper part show the approximate location of the responsive regions. (B) Calcium responses of the glomerular regions indicated by an arrow and green color in A (MOB, green traces; AOB, magenta traces). Amino acid mixture (AA, 100 μM) was applied as a positive control for activation of the MOB. (C) Representative calcium responses of mitral/tufted cells in the MOB (green) and AOB (magenta) upon mucosal application of sulfated steroids (E mix and P mix, 200 μM) and amino acids (AA, 100 μM). In both main and accessory olfactory bulb, mitral/tufted cells were activated by either E or P steroids, or both stimuli. Amino acids only elicited calcium responses in mitral/tufted cells of the MOB. Similar results were obtained in 4 MOBs and 3 AOBs.

Mentions: To gain information about the processing of sulfated steroids in the first relay center of the system, we recorded odorant-induced calcium responses in whole mounts of the olfactory system. Nasal application of P and E mix sulfated steroids elicited transient increases in intracellular Ca2+ concentration in the main and accessory olfactory bulb. We detected responses in glomerular tufts and in somata of mitral/tufted cells (Figures 4A–C). Glomerular responses to the E mix were strongly overlapping with the P mix-responsive areas, but we also found regions reacting individually to each mixture (Figure 4A). Amino acid-evoked response patterns in the main olfactory bulb were also in part overlapping with the steroid-reactive areas (Figure 4B). Amino acids did not evoke any activity in the accessory olfactory bulb (Figures 4B,C). Signals detected in individual cell somata of the olfactory bulb showed various reactivity patterns to the different odorant stimuli (Figure 4C). Transection of the olfactory nerve abolished all olfactory bulb responses to odorant stimulation (data not shown).


Dual processing of sulfated steroids in the olfactory system of an anuran amphibian.

Sansone A, Hassenklöver T, Offner T, Fu X, Holy TE, Manzini I - Front Cell Neurosci (2015)

Sulfated steroids are processed in the olfactory bulb. (A) 3D rendering of reactive volumes in the MOB (left hand side) and AOB (right hand side) upon mucosal application of E and P mix (E mix-responsive areas, blue; P mix-responsive areas, red). Active regions always contained both cell somata and glomerular structures. Schematics of the olfactory bulb in the upper part show the approximate location of the responsive regions. (B) Calcium responses of the glomerular regions indicated by an arrow and green color in A (MOB, green traces; AOB, magenta traces). Amino acid mixture (AA, 100 μM) was applied as a positive control for activation of the MOB. (C) Representative calcium responses of mitral/tufted cells in the MOB (green) and AOB (magenta) upon mucosal application of sulfated steroids (E mix and P mix, 200 μM) and amino acids (AA, 100 μM). In both main and accessory olfactory bulb, mitral/tufted cells were activated by either E or P steroids, or both stimuli. Amino acids only elicited calcium responses in mitral/tufted cells of the MOB. Similar results were obtained in 4 MOBs and 3 AOBs.
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Related In: Results  -  Collection

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Figure 4: Sulfated steroids are processed in the olfactory bulb. (A) 3D rendering of reactive volumes in the MOB (left hand side) and AOB (right hand side) upon mucosal application of E and P mix (E mix-responsive areas, blue; P mix-responsive areas, red). Active regions always contained both cell somata and glomerular structures. Schematics of the olfactory bulb in the upper part show the approximate location of the responsive regions. (B) Calcium responses of the glomerular regions indicated by an arrow and green color in A (MOB, green traces; AOB, magenta traces). Amino acid mixture (AA, 100 μM) was applied as a positive control for activation of the MOB. (C) Representative calcium responses of mitral/tufted cells in the MOB (green) and AOB (magenta) upon mucosal application of sulfated steroids (E mix and P mix, 200 μM) and amino acids (AA, 100 μM). In both main and accessory olfactory bulb, mitral/tufted cells were activated by either E or P steroids, or both stimuli. Amino acids only elicited calcium responses in mitral/tufted cells of the MOB. Similar results were obtained in 4 MOBs and 3 AOBs.
Mentions: To gain information about the processing of sulfated steroids in the first relay center of the system, we recorded odorant-induced calcium responses in whole mounts of the olfactory system. Nasal application of P and E mix sulfated steroids elicited transient increases in intracellular Ca2+ concentration in the main and accessory olfactory bulb. We detected responses in glomerular tufts and in somata of mitral/tufted cells (Figures 4A–C). Glomerular responses to the E mix were strongly overlapping with the P mix-responsive areas, but we also found regions reacting individually to each mixture (Figure 4A). Amino acid-evoked response patterns in the main olfactory bulb were also in part overlapping with the steroid-reactive areas (Figure 4B). Amino acids did not evoke any activity in the accessory olfactory bulb (Figures 4B,C). Signals detected in individual cell somata of the olfactory bulb showed various reactivity patterns to the different odorant stimuli (Figure 4C). Transection of the olfactory nerve abolished all olfactory bulb responses to odorant stimulation (data not shown).

Bottom Line: Chemical communication is widespread in amphibians, but if compared to later diverging tetrapods the available functional data is limited.Furthermore, we found that larval and adult animals excrete multiple sulfated compounds with physical properties consistent with sulfated steroids.Breeding tadpole and frog water including these compounds activated a large subset of sensory neurons that also responded to synthetic steroids, showing that sulfated steroids are likely to convey intraspecific information.

View Article: PubMed Central - PubMed

Affiliation: Institute of Neurophysiology and Cellular Biophysics, University of Göttingen Göttingen, Germany ; Center for Nanoscale Microscopy and Molecular Physiology of the Brain Göttingen, Germany.

ABSTRACT
Chemical communication is widespread in amphibians, but if compared to later diverging tetrapods the available functional data is limited. The existing information on the vomeronasal system of anurans is particularly sparse. Amphibians represent a transitional stage in the evolution of the olfactory system. Most species have anatomically separated main and vomeronasal systems, but recent studies have shown that in anurans their molecular separation is still underway. Sulfated steroids function as migratory pheromones in lamprey and have recently been identified as natural vomeronasal stimuli in rodents. Here we identified sulfated steroids as the first known class of vomeronasal stimuli in the amphibian Xenopus laevis. We show that sulfated steroids are detected and concurrently processed by the two distinct olfactory subsystems of larval Xenopus laevis, the main olfactory system and the vomeronasal system. Our data revealed a similar but partially different processing of steroid-induced responses in the two systems. Differences of detection thresholds suggest that the two information channels are not just redundant, but rather signal different information. Furthermore, we found that larval and adult animals excrete multiple sulfated compounds with physical properties consistent with sulfated steroids. Breeding tadpole and frog water including these compounds activated a large subset of sensory neurons that also responded to synthetic steroids, showing that sulfated steroids are likely to convey intraspecific information. Our findings indicate that sulfated steroids are conserved vomeronasal stimuli functioning in phylogenetically distant classes of tetrapods living in aquatic and terrestrial habitats.

No MeSH data available.


Related in: MedlinePlus