Limits...
Regulation of lifespan by chemosensory and thermosensory systems: findings in invertebrates and their implications in mammalian aging.

Jeong DE, Artan M, Seo K, Lee SJ - Front Genet (2012)

Bottom Line: Several studies have shown that chemosensory and thermosensory neurons affect the lifespan of invertebrate model animals, including Caenorhabditis elegans and Drosophila melanogaster.Although the mechanisms by which these sensory systems modulate lifespan are incompletely understood, hormonal signaling pathways have been implicated in sensory system-mediated lifespan regulation.In this review, we describe findings regarding how sensory nervous system components elicit physiological changes to regulate lifespan in invertebrate models, and discuss their implications in mammalian aging.

View Article: PubMed Central - PubMed

Affiliation: Division of Molecular and Life Science, Pohang University of Science and Technology Pohang, South Korea.

ABSTRACT
Many environmental factors that dynamically change in nature influence various aspects of animal physiology. Animals are equipped with sensory neuronal systems that help them properly sense and respond to environmental factors. Several studies have shown that chemosensory and thermosensory neurons affect the lifespan of invertebrate model animals, including Caenorhabditis elegans and Drosophila melanogaster. Although the mechanisms by which these sensory systems modulate lifespan are incompletely understood, hormonal signaling pathways have been implicated in sensory system-mediated lifespan regulation. In this review, we describe findings regarding how sensory nervous system components elicit physiological changes to regulate lifespan in invertebrate models, and discuss their implications in mammalian aging.

No MeSH data available.


Related in: MedlinePlus

Model of C. elegans lifespan control by thermosensory AFD neurons. Increased ambient temperature is perceived by AFD thermosensory neurons. Although the exact mechanism for thermal cue perception is not understood, upon sensing temperature elevation, G protein signaling promotes cyclic GMP production and facilitates the influx of Ca2+ and Na+ cations by opening cyclic nucleotide-gated channels (CNGs). The signal perceived by the thermosensory neurons is transmitted to downstream effectors, such as DAF-12/NHR and heat shock factor 1 (HSF-1), via intercellular (cell-nonautonomous) signaling. Impairment of AFD thermosensory neurons reduces DAF-9/CYP levels, which in turn decreases the level of sterol hormones, dafachronic acids (DA). This leads to altered DAF-12/NHR activity, which accelerates aging at high temperature. In addition, AFD neurons and HSF-1 regulate each other in a cell-nonautonomous manner to affect physiological processes of whole worms. Defects in thermosensory neurons decrease the activity of HSF-1 in non-neuronal tissues, while impairment of hsf-1 in non-neuronal tissues decreases thermosensory neural function. It has also been shown that inhibiting HSF-1 speeds up aging.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3475297&req=5

Figure 4: Model of C. elegans lifespan control by thermosensory AFD neurons. Increased ambient temperature is perceived by AFD thermosensory neurons. Although the exact mechanism for thermal cue perception is not understood, upon sensing temperature elevation, G protein signaling promotes cyclic GMP production and facilitates the influx of Ca2+ and Na+ cations by opening cyclic nucleotide-gated channels (CNGs). The signal perceived by the thermosensory neurons is transmitted to downstream effectors, such as DAF-12/NHR and heat shock factor 1 (HSF-1), via intercellular (cell-nonautonomous) signaling. Impairment of AFD thermosensory neurons reduces DAF-9/CYP levels, which in turn decreases the level of sterol hormones, dafachronic acids (DA). This leads to altered DAF-12/NHR activity, which accelerates aging at high temperature. In addition, AFD neurons and HSF-1 regulate each other in a cell-nonautonomous manner to affect physiological processes of whole worms. Defects in thermosensory neurons decrease the activity of HSF-1 in non-neuronal tissues, while impairment of hsf-1 in non-neuronal tissues decreases thermosensory neural function. It has also been shown that inhibiting HSF-1 speeds up aging.

Mentions: Despite relatively well-defined thermosensory system structures and functions for the perception of ambient temperature, the effects of these systems on the regulation of animal physiology, including aging, remain poorly understood. Lee and Kenyon demonstrated that AFD thermosensory neurons regulate worm lifespan through a sterol endocrine signaling pathway at high temperatures (Lee and Kenyon, 2009) (Figure 4). Impairment of AFD neurons by either laser ablation or mutations causes a significant lifespan decrease at high temperature (25°C) but have no effect at low temperatures (20 and 15°C). Perturbation of AFD neurons reduces the expression of daf-9, which encodes a cytochrome P450 (CYP) that is responsible for producing the sterol hormones known as dafachronic acids. This subsequently influences the activity of DAF-12, a nuclear hormone receptor (NHR) whose activity is regulated by dafachronic acids. They proposed a model in which AFD neurons stimulate daf-9/CYP expression, which in turn regulates DAF-12/NHR activity and leads to altered lifespan at high temperature. Another noteworthy study suggested that AFD thermosensory neurons regulate the transient heat shock response of whole worms upon perception of acute high temperature (Prahlad et al., 2008). When mutant worms that have defects in AFD thermosensory neurons are exposed to transient heat shock, the expression of heat-shock responsive chaperone genes in neurons and other tissues are reduced. In addition, these animals are less tolerant to heat shock than wild-type worms. A subsequent study showed that regulation of chaperone gene expression by AFD neurons also influences protein aggregation in a neurodegenerative disease model (Prahlad and Morimoto, 2011). Therefore, signaling from thermosensory neurons to other tissues appears to mediate the proper heat shock response of whole worms. The induction of heat-shock responsive genes by AFD neurons is solely dependent on the heat shock factor-1 (HSF-1), which is a leucine-zipper transcription factor crucial for various biological functions, including heat-shock response, lifespan regulation, and organismal development (Neef et al., 2011). The interplay between the thermosensory neural system and HSF-1 was further demonstrated by Sugi et al. who found that HSF-1 is required for the thermotactic behavior of worms towards a preferred cultivation temperature (Sugi et al., 2011). Non-neuronal expression of hsf-1 is sufficient to rescue thermotactic defects and does so by regulating AFD neurons through estrogen signaling. Thus, regulation of HSF-1 activity in non-neuronal cells, as well as AFD neurons in C. elegans appears to act as thermosensors. Interestingly, both AFD thermosensory neurons and the HSF-1 transcription factor are required for maintaining normal worm lifespan at high temperatures (Lee and Kenyon, 2009). It is tempting to speculate that AFD neuronal signaling and HSF-1 activity regulation in the non-neuronal cells of ectothermic animals, such as C. elegans, operate together to properly tune physiological processes, including aging (Figure 4).


Regulation of lifespan by chemosensory and thermosensory systems: findings in invertebrates and their implications in mammalian aging.

Jeong DE, Artan M, Seo K, Lee SJ - Front Genet (2012)

Model of C. elegans lifespan control by thermosensory AFD neurons. Increased ambient temperature is perceived by AFD thermosensory neurons. Although the exact mechanism for thermal cue perception is not understood, upon sensing temperature elevation, G protein signaling promotes cyclic GMP production and facilitates the influx of Ca2+ and Na+ cations by opening cyclic nucleotide-gated channels (CNGs). The signal perceived by the thermosensory neurons is transmitted to downstream effectors, such as DAF-12/NHR and heat shock factor 1 (HSF-1), via intercellular (cell-nonautonomous) signaling. Impairment of AFD thermosensory neurons reduces DAF-9/CYP levels, which in turn decreases the level of sterol hormones, dafachronic acids (DA). This leads to altered DAF-12/NHR activity, which accelerates aging at high temperature. In addition, AFD neurons and HSF-1 regulate each other in a cell-nonautonomous manner to affect physiological processes of whole worms. Defects in thermosensory neurons decrease the activity of HSF-1 in non-neuronal tissues, while impairment of hsf-1 in non-neuronal tissues decreases thermosensory neural function. It has also been shown that inhibiting HSF-1 speeds up aging.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3475297&req=5

Figure 4: Model of C. elegans lifespan control by thermosensory AFD neurons. Increased ambient temperature is perceived by AFD thermosensory neurons. Although the exact mechanism for thermal cue perception is not understood, upon sensing temperature elevation, G protein signaling promotes cyclic GMP production and facilitates the influx of Ca2+ and Na+ cations by opening cyclic nucleotide-gated channels (CNGs). The signal perceived by the thermosensory neurons is transmitted to downstream effectors, such as DAF-12/NHR and heat shock factor 1 (HSF-1), via intercellular (cell-nonautonomous) signaling. Impairment of AFD thermosensory neurons reduces DAF-9/CYP levels, which in turn decreases the level of sterol hormones, dafachronic acids (DA). This leads to altered DAF-12/NHR activity, which accelerates aging at high temperature. In addition, AFD neurons and HSF-1 regulate each other in a cell-nonautonomous manner to affect physiological processes of whole worms. Defects in thermosensory neurons decrease the activity of HSF-1 in non-neuronal tissues, while impairment of hsf-1 in non-neuronal tissues decreases thermosensory neural function. It has also been shown that inhibiting HSF-1 speeds up aging.
Mentions: Despite relatively well-defined thermosensory system structures and functions for the perception of ambient temperature, the effects of these systems on the regulation of animal physiology, including aging, remain poorly understood. Lee and Kenyon demonstrated that AFD thermosensory neurons regulate worm lifespan through a sterol endocrine signaling pathway at high temperatures (Lee and Kenyon, 2009) (Figure 4). Impairment of AFD neurons by either laser ablation or mutations causes a significant lifespan decrease at high temperature (25°C) but have no effect at low temperatures (20 and 15°C). Perturbation of AFD neurons reduces the expression of daf-9, which encodes a cytochrome P450 (CYP) that is responsible for producing the sterol hormones known as dafachronic acids. This subsequently influences the activity of DAF-12, a nuclear hormone receptor (NHR) whose activity is regulated by dafachronic acids. They proposed a model in which AFD neurons stimulate daf-9/CYP expression, which in turn regulates DAF-12/NHR activity and leads to altered lifespan at high temperature. Another noteworthy study suggested that AFD thermosensory neurons regulate the transient heat shock response of whole worms upon perception of acute high temperature (Prahlad et al., 2008). When mutant worms that have defects in AFD thermosensory neurons are exposed to transient heat shock, the expression of heat-shock responsive chaperone genes in neurons and other tissues are reduced. In addition, these animals are less tolerant to heat shock than wild-type worms. A subsequent study showed that regulation of chaperone gene expression by AFD neurons also influences protein aggregation in a neurodegenerative disease model (Prahlad and Morimoto, 2011). Therefore, signaling from thermosensory neurons to other tissues appears to mediate the proper heat shock response of whole worms. The induction of heat-shock responsive genes by AFD neurons is solely dependent on the heat shock factor-1 (HSF-1), which is a leucine-zipper transcription factor crucial for various biological functions, including heat-shock response, lifespan regulation, and organismal development (Neef et al., 2011). The interplay between the thermosensory neural system and HSF-1 was further demonstrated by Sugi et al. who found that HSF-1 is required for the thermotactic behavior of worms towards a preferred cultivation temperature (Sugi et al., 2011). Non-neuronal expression of hsf-1 is sufficient to rescue thermotactic defects and does so by regulating AFD neurons through estrogen signaling. Thus, regulation of HSF-1 activity in non-neuronal cells, as well as AFD neurons in C. elegans appears to act as thermosensors. Interestingly, both AFD thermosensory neurons and the HSF-1 transcription factor are required for maintaining normal worm lifespan at high temperatures (Lee and Kenyon, 2009). It is tempting to speculate that AFD neuronal signaling and HSF-1 activity regulation in the non-neuronal cells of ectothermic animals, such as C. elegans, operate together to properly tune physiological processes, including aging (Figure 4).

Bottom Line: Several studies have shown that chemosensory and thermosensory neurons affect the lifespan of invertebrate model animals, including Caenorhabditis elegans and Drosophila melanogaster.Although the mechanisms by which these sensory systems modulate lifespan are incompletely understood, hormonal signaling pathways have been implicated in sensory system-mediated lifespan regulation.In this review, we describe findings regarding how sensory nervous system components elicit physiological changes to regulate lifespan in invertebrate models, and discuss their implications in mammalian aging.

View Article: PubMed Central - PubMed

Affiliation: Division of Molecular and Life Science, Pohang University of Science and Technology Pohang, South Korea.

ABSTRACT
Many environmental factors that dynamically change in nature influence various aspects of animal physiology. Animals are equipped with sensory neuronal systems that help them properly sense and respond to environmental factors. Several studies have shown that chemosensory and thermosensory neurons affect the lifespan of invertebrate model animals, including Caenorhabditis elegans and Drosophila melanogaster. Although the mechanisms by which these sensory systems modulate lifespan are incompletely understood, hormonal signaling pathways have been implicated in sensory system-mediated lifespan regulation. In this review, we describe findings regarding how sensory nervous system components elicit physiological changes to regulate lifespan in invertebrate models, and discuss their implications in mammalian aging.

No MeSH data available.


Related in: MedlinePlus