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Sequential onset of presynaptic molecules during olfactory sensory neuron maturation.

ABSTRACT: Differentiated olfactory sensory neurons express specific presynaptic proteins, including enzymes involved in neurotransmitter transport and proteins involved in the trafficking and release of synaptic vesicles. Studying the regulation of these presynaptic proteins will help to elucidate the presynaptic differentiation process that ultimately leads to synapse formation. It has been postulated that the formation of a synapse between the axons of the sensory neurons and the dendrites of second order neurons in the olfactory bulb is a critical step in the processes of sensory neuron maturation. One approach to study the relationship between synaptogenesis and sensory neuron maturation is to examine the expression patterns of synaptic molecules through the olfactory neuron lineage. To this end we designed specific in situ hybridization probes to target messengers for proteins involved in presynaptic vesicle release. Our findings show that, as they mature, mouse olfactory neurons sequentially express specific presynaptic genes. Furthermore, the different patterns of expression of these presynaptic genes suggest the existence of discrete steps in presynaptic development: genes encoding proteins involved in scaffolding show an early onset of expression, whereas expression of genes encoding proteins involved in the regulation of vesicle release starts later. In particular, the signature molecule for glutamatergic neurons vesicle glutamate transporter 2 shows the latest onset of expression. In addition, contact with the targets in the olfactory bulb is not controlling presynaptic protein gene expression, suggesting that olfactory sensory neurons follow an intrinsic program of development.

SUBMITTER: Marcucci F

PROVIDER: S-EPMC4313887 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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Sequential onset of presynaptic molecules during olfactory sensory neuron maturation.

Marcucci Florencia F Zou Dong-Jing DJ Firestein Stuart S

The Journal of comparative neurology 20090901 3

Differentiated olfactory sensory neurons express specific presynaptic proteins, including enzymes involved in neurotransmitter transport and proteins involved in the trafficking and release of synaptic vesicles. Studying the regulation of these presynaptic proteins will help to elucidate the presynaptic differentiation process that ultimately leads to synapse formation. It has been postulated that the formation of a synapse between the axons of the sensory neurons and the dendrites of second ord ...[more]

PMID: 19598283

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Project description:Arsenic is a contaminant of food and drinking water. Epidemiological studies have reported correlations between arsenic exposure and neurodevelopmental abnormalities, such as reduced sensory functioning, while in vitro studies have shown that arsenic reduces neurogenesis and alters stem cell differentiation. The goal of this study was assess whether arsenic exposure during embryogenesis reduced olfactory stem cell function and/or numbers, and if so, whether those changes persist into adulthood. Killifish (Fundulus heteroclitus) embryos were exposed to 0, 10, 50 or 200 ppb arsenite (AsIII) until hatching, and juvenile fish were raised in clean water. At 0, 2, 4, 8, 16, 28 and 40 weeks of age, odorant response tests were performed to assess specific olfactory sensory neuron (OSN) function. Olfactory epithelia were then collected for immunohistochemical analysis of stem cell (Sox2) and proliferating cell numbers (PCNA), as well as the number and expression of ciliated (calretinin) and microvillus OSNs (Gαi3) at 0, 4, 16 and 28 weeks. Odorant tests indicated that arsenic exposure during embryogenesis increased the start time of killifish responding to pheromones, and this altered start time persisted to 40 weeks post-exposure. Response to the odorant taurocholic acid (TCA) was also reduced through week 28, while responses to amino acids were not consistently altered. Immunohistochemistry was used to determine whether changes in odorant responses were correlated to altered cell numbers in the olfactory epithelium, using markers of proliferating cells, progenitor cells, and specific OSNs. Comparisons between response to pheromones and PCNA + cells indicated that, at week 0, both parameters in exposed fish were significantly reduced from the control group. At week 28, all exposure are still significantly different than control fish, but now with higher PCNA expression coupled with reduced pheromone responses. A similar trend was seen in the comparisons between Sox2-expressing progenitor cells and response to pheromones, although Sox2 expression in the 28 week-old fish only recovers back to the level of control fish rather than being significantly higher. Comparisons between calretinin expression (ciliated OSNs) and response to TCA demonstrated that both parameters were reduced in the 200 ppb arsenic-exposed fish in at weeks 4, 16, and 28. Correlations between TCA response and the number of PCNA + cells revealed that, at 28 weeks of age, all arsenic exposure groups had reductions in response to TCA, but higher PCNA expression, similar to that seen with the pheromones. Few changes in Gαi3 (microvillus OSNs) were seen. Thus, it appears that embryonic-only exposure to arsenic has long-term reductions in proliferation and differentiation of olfactory sensory neurons, leading to persistent effects in their function.

Dataset Information

Sequential onset of presynaptic molecules during olfactory sensory neuron maturation.

Publications

Sequential onset of presynaptic molecules during olfactory sensory neuron maturation.

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