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The first ascr 5-specific receptors were identified by McGrath et al. Both strains do not form dauer larvae in response to dauer pheromone obtained from wild-type N2 worms or synthetic samples of four main components of the dauer pheromone, ascr 2, ascr 3, ascr 5, and icas 9. By using recombinant inbred lines between a dauer defective strain and N2 worms for quantitative trait locus mapping, McGrath et al. Notably, srg and srg were found to be disrupted in both ascr 5-resistant strains.

Introgression of the genomic region containing the srg and srg deletion into the N2 background conferred resistance to ascr 5, but did not significantly affect sensitivity to other ascarosides, indicating that srg and srg are specifically required for perception of ascr 5. Complementing ascr 5-resistant strains with either srg and srg cDNAs restored sensitivity to ascr 5, indicating that the srg and srg genes are at least partially redundant.

Both srg and srg are strongly expressed in the ASI neurons where they localize to the sensory cilia, consistent with a function as dauer pheromone receptors. McGrath et al. Two additional ascaroside receptors, daf and daf , were identified by Park et al. In contrast, daf mutants are partially defective in responses to several different ascarosides, including ascr 2, ascr 3, and ascr 5. Photo-affinity labeling studies showed that DAFdependent activity of ascr 2 results from direct binding of the ascaroside to this GPCR, representing the first demonstration of direct molecular interactions between an ascaroside and a GPCR.

The great number of dauer pheromone components and the presence of receptors with redundant and overlapping functions indicates a highly sophisticated signaling system. The results of Kim et al. Whether srbc and srbc or srg and srg are also involved in mediating behavioral responses to ascarosides has not been studied in detail; however the observation that expression of srg cDNA or srg cDNA in the ASH neurons resulted in worms that respond strongly in an acute-avoidance assay suggests such a role for the srg genes McGrath et al.

Shortly after the original description of the dauer pheromone in , Golden and Riddle described a mutation, daf , that abolished dauer pheromone production Golden and Riddle, Metabolite extracts derived from daf cultures failed to inhibit dauer recovery and were found to have little or no dauer inducing activity. Following the chemical identification of the dauer pheromone, it was shown that daf worms do not produce the dauer inducing and male-attracting ascarosides ascr 2 and ascr 3 Srinivasan et al.

These results confirmed that ascaroside pheromones are worm-derived and not the result of bacterial metabolism, and also suggested a possible entry point for investigating ascaroside pheromone biosynthesis. In , Mak et al. A subsequent study showed that a group of four of the identified fat storage mutants mapped to the same ORF as the canonical allele of daf Butcher et al.

These results suggested that in C. Notably, transgenic intestinal DAF expression is sufficient to restore dauer inducing activity of daf mutants, implicating the intestine as a major source of ascaroside pheromones Butcher et al.

The precise roles of DHS , DAF and other peroxisomal enzymes in the biosynthesis of the ascaroside side chains was characterized in detail using mass spectrometry-based comparative metabolomics von Reuss et al. Instead large quantities of ascr 10, the saturated derivative of ascr 3 and a homologous series of longer-chained saturated ascarosides was observed von Reuss et al. Ascaroside side-chain biosynthesis.

Adapted with permission from von Reuss et al. Copyright American Chemical Society. Because biosynthesis of short and medium-chained ascarosides is not completely abolished in acox-1 loss-of-function mutants, it is assumed that other, yet unidentified acyl-CoA oxidases participate in ascaroside biosynthesis Joo et al.

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In contrast to acox-1 mutants, biosynthesis of short-chain ascarosides dominant in wild-type worms is completely abolished in maoc-1 worms von Reuss et al. Similarly, wild-type ascarosides are completely absent from the dhs and daf metabolomes Butcher et al. Some of these long-chain ascarosides have been shown to have weak dauer inducing activity and may account for the small amount of dauer-inducing activity occasionally present in dhs and daf metabolite extracts Butcher et al. These very long-chain ascarosides may represent the ultimate precursors of all or some of the ascarosides described in this section.

Reprinted with permission from von Reuss et al.

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Male ascaroside profiles are dominated by ascr 10, whereas hermaphrodites produce large amounts of ascr 3, distinguished from ascr 10 solely by the incorporation of a double bond, instead. Short-chain indole ascarosides are absent from the maoc-1 , dhs , and daf mutant metabolomes, indicating that biosynthesis of the side chains of indole ascarosides and non-indole ascarosides proceeds via the same pathway von Reuss et al.

Using worms grown in axenic cultures, the indole carboxy moiety in wild-type indole ascarosides was shown to be derived from tryptophan Srinivasan et al. Similarly, p -hydroxybenzoyl ascarosides e. Comparison of the relative amounts of indole and non-indole ascarosides in wild-type worms indicates that indole attachment is tightly regulated. For example, ascr 9 is much less abundant than ascr 3, whereas the corresponding indole ascarosides icas 9 and icas 3 are of roughly equal abundance von Reuss et al. Given that conversion of ascarosides into their indole carboxy derivatives is associated with a dramatic change in biological activity see Section 2.

However, enzymes catalyzing attachment of the indole carboxy moiety have not been identified. Whereas the biosynthesis of dideoxysugar L-ascarylose in bacteria is well understood Thorson et al. Detection of ascarosides in axenic C. Similarly, enzymes involved in hydroxylation and glycosylation of the VLCFA precursors of the ascaroside side-chains remain to be identified.

Taken together, current knowledge allows proposing a preliminary model for ascaroside biosynthesis Figure Model for ascaroside biogenesis. Chain elongation of fatty acids by putative elongase homologs elo-1—9 Agbaga et al. Production of ascaroside pheromones by C. Total amounts of ascarosides excreted increases throughout development from L1 to adult worms. Excretion of the two main components of the male-attracting signal, ascr 3 and ascr 8, peaks at the young adult stage Kaplan et al.

Under dauer-inducing conditions, excretion of the strongly dauer-inducing ascr 2 peaks right before entry into the dauer stage. Dauer worms do not appear to excrete ascarosides, but contain small amounts of ascr 1 and ascr 3 Kaplan et al. Temperature affects the ratio of ascr 1 and ascr 3 production Joo et al. Comparison of the ascaroside profiles of well-fed and starved C.

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Increasingly sensitive analytical techniques will enable more detailed studies of ascaroside production of different life stages under different environmental conditions. Comparison of the ascaroside profiles of liquid culture supernatant extracts worm excretome and worm body extracts showed that ascaroside are differentially released Kaplan et al.

In addition, worm bodies contain large quantities of ascaroside O-glycoside esters, for example the ascr 10 glucoside glas 10, which are absent from media supernatant samples von Reuss et al. As discussed in Section 2, ascaroside-based small-molecule signals regulate a stunningly diverse range of phenotypes, including dauer arrest, mate attraction, aggregation, and olfactory plasticity, and it is likely that ascarosides affect additional aspects of C.

This wide variety of biological functions is mediated by a corresponding diversity of ascaroside structures, which are generated via modular assembly of building blocks from carbohydrate, lipid, short-chain fatty acid, amino acid, and folate metabolism. Therefore, it appears that ascaroside biosynthesis integrates input from several major metabolic pathways to encode and communicate comprehensive information about reproductive and nutritional state von Reuss et al.

More detailed investigation of ascaroside biosynthetic pathways and their regulation may provide insight into how information about metabolic and reproductive state as well as environmental parameters is transduced by ascaroside signaling. Additional levels of complexity in ascaroside signaling arise from 1 the functioning of individual ascarosides in more than one pathway e.

As evident from the complicated history of the dauer pheromone identification, the reconstitution of biological activity using synthetic compounds faces considerable challenges, not only because a large number of different compounds have to be synthesized, but also because the exact composition of chemical signals may often depend on many variables, including environmental conditions and the history of the pheromone-perceiving worms.

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Given the number of ascarosides identified so far and the great variety of phenotypes downstream of ascaroside signaling, elucidation of the mechanisms of ascaroside perception and signal integration remains a formidable task. Synergistic blends of specific ascaroside combinations and concentrations elicit different phenotypes via activation of GPCR's in chemosensory neurons. The structures of most ascaroside receptors and their modes of action are not known.

Ascaroside signaling appears to be widely conserved among both free-living and parasitic nematode species Choe et al. In screening for the more than different ascarosides so far identified, 15 out of 18 tested nematode species were found to produce ascarosides known from C. Curiously, the three tested species in which none of the C.

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Nonetheless, it is possible that A. More detailed analysis of C. The authors thank Jagan Srinivasan Worchester Polytechnic Institute for a critical reading of the manuscript. Agbaga, M.