Integrated Proteomic and Metabolomic Analysis of Larval Brain Associated with Diapause Induction and Preparation in the Cotton Bollworm, <i>Helicoverpa armigera</i>

Zhang, Qi; Lu, Yuxuan; Xu, Wei‐Hua

doi:10.1021/pr200796a

Cited by 48 publications

(53 citation statements)

References 58 publications

(89 reference statements)

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“…Thirty brains of each sample were extracted and derivatized as described (22). In brief, each sample was homogenized in a 600 μL methanol-chloroform mixture (2:1) and sonicated for 15 min.…”

Section: Methodsmentioning

confidence: 99%

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Cross-talk between the fat body and brain regulates insect developmental arrest

Denlinger

2012

Proc. Natl. Acad. Sci. U.S.A.

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108

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Developmental arrest, a critical component of the life cycle in animals as diverse as nematodes (dauer state), insects (diapause), and vertebrates (hibernation), results in dramatic depression of the metabolic rate and a profound extension in longevity. Although many details of the hormonal systems controlling developmental arrest are well-known, we know little about the interactions between metabolic events and the hormones controlling the arrested state. Here, we show that diapause is regulated by an interplay between blood-borne metabolites and regulatory centers within the brain. Gene expression in the fat body, the insect equivalent of the liver, is strongly suppressed during diapause, resulting in low levels of tricarboxylic acid (TCA) intermediates circulating within the blood, and at diapause termination, the fat body becomes activated, releasing an abundance of TCA intermediates that act on the brain to stimulate synthesis of regulatory peptides that prompt production of the insect growth hormone ecdysone. This model is supported by our success in breaking diapause by injecting a mixture of TCA intermediates and upstream metabolites. The results underscore the importance of cross-talk between the brain and fat body as a regulator of diapause and suggest that the TCA cycle may be a checkpoint for regulating different forms of animal dormancy.prothoracicotropic hormone | glucose | pyruvate A s days shorten in late summer and temperatures drop, many insects respond by entering an overwintering diapause, a form of developmental arrest characterized by metabolic depression. The major endocrine events that regulate diapause are fairly well-understood. In larvae and pupae, the arrest is usually a consequence of the brain's failure to produce or release prothoracicotropic hormone (PTTH), a neuropeptide needed to stimulate the prothoracic gland to synthesize the steroid hormones ecdysteroids (20-hydroxyecdysone is the most active form and will be referred to hereafter as ecdysone) (1). Without ecdysone, the insect remains locked in a developmental arrest that persists as long as ecdysone is absent.Specific patterns of gene expression and unique metabolic profiles characterize diapause (2-4), but the interactions between genes, metabolites, and the major endocrine centers are poorly known. One of the most conspicuous metabolic patterns during diapause in insects and dormancy in other animals (5-7) is a shift to anaerobic metabolism favoring glycolysis and gluconeogenesis. Although it is usually assumed that changes in abundance of specific metabolites are downstream responses to the diapause program, the demonstration that elevated sorbitol is the cause, rather than the consequence, of developmental arrest in embryos of the silk moth (8) suggests the possibility that the metabolite profile itself may influence the diapause decision. This possibility is tested here by monitoring changes in metabolite abundance in association with diapause and then showing that artificially boosting the abundance of nondiapause met...

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Section: Methodsmentioning

confidence: 99%

“…The GC-MS analysis program was described (22) and slightly modified. The 1 μL derivatization sample was autoinjected using a 1:10 split ratio to a Trace GC Ultra-DSQ II GC-MS (Thermo), with the injector temperature held at 280°C.…”

Section: Gc-ms Analysis For Metabolitesmentioning

confidence: 99%

Cross-talk between the fat body and brain regulates insect developmental arrest

Denlinger

2012

Proc. Natl. Acad. Sci. U.S.A.

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108

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“…Answers to this question will only come from more detailed investigations to characterise downstream (effector) and upstream (regulatory) mechanisms. This has begun to some extent with investigations of diapause induction, initiation and termination in the cotton bollworm, Helicoverpa armigera, and a key role for metabolic change has been identified in regulating the diapause programme Zhang et al, 2012). Thus, while it is apparent that compatible solutes such as sugars, free fatty acids and polyols can protect cells both osmotically (Kostál et al, 2001) and by stabilising membranes and macromolecules even at low physiological concentrations, we still lack a detailed understanding of the precise functional role(s) that most cold-responsive metabolites play, or the stress response regulatory cascades that induce them.…”

Section: Reviewmentioning

confidence: 99%

“…This clearly masks any subtleties arising from tissue-specific responses and frustrates further any understanding of regulatory mechanisms controlling metabolite responses to cold. In this respect, investigations of diapause are again at the vanguard, and tissue-specific metabolomic studies have identified clear differences in fat body, brain and haemolymph profiles (Zhang et al, 2012). A more interesting issue is the extent to which metabolite responses are initiated centrally but implemented in peripheral tissues.…”

Section: Reviewmentioning

confidence: 99%

“…These include studies on mild chilling and developmental acclimation (Colinet et al, 2012b;Foray et al, 2013), stress-selected lines (Malmendal et al, 2013), RCH (Michaud and Denlinger, 2007;Teets et al, 2012), as well as freeze resistance (Hawes et al, 2008;Kostál et al, 2011;Michaud and Denlinger, 2007). Overwintering diapause has also been studied in some detail (Colinet et al, 2012b;Michaud and Denlinger, 2007;Zhang et al, 2012), and, while not necessarily representing a direct response to low temperature, often displays a similar metabolic 'fingerprint' to the cold stress response. Distinguishing unique metabolic characteristics of freezing versus chilling versus diapause is not yet possible, as the very few studies conducted to date fail to disentangle stress-specific from species-specific responses.…”

Section: Reviewmentioning

confidence: 99%

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Molecular basis of chill resistance adaptations in poikilothermic animals

Hayward

Manso

Cossins

2014

Journal of Experimental Biology

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Chill and freeze represent very different components of low temperature stress. Whilst the principal mechanisms of tissue damage and of acquired protection from freeze-induced effects are reasonably well established, those for chill damage and protection are not. Non-freeze cold exposure (i.e. chill) can lead to serious disruption to normal life processes, including disruption to energy metabolism, loss of membrane perm-selectivity and collapse of ion gradients, as well as loss of neuromuscular coordination. If the primary lesions are not relieved then the progressive functional debilitation can lead to death. Thus, identifying the underpinning molecular lesions can point to the means of building resistance to subsequent chill exposures. Researchers have focused on four specific lesions: (i) failure of neuromuscular coordination, (ii) perturbation of bio-membrane structure and adaptations due to altered lipid composition, (iii) protein unfolding, which might be mitigated by the induced expression of compatible osmolytes acting as 'chemical chaperones ', (iv) or the induced expression of protein chaperones along with the suppression of general protein synthesis. Progress in all these potential mechanisms has been ongoing but not substantial, due in part to an over-reliance on straightforward correlative approaches. Also, few studies have intervened by adoption of single gene ablation, which provides much more direct and compelling evidence for the role of specific genes, and thus processes, in adaptive phenotypes. Another difficulty is the existence of multiple mechanisms, which often act together, thus resulting in compensatory responses to gene manipulations, which may potentially mask disruptive effects on the chill tolerance phenotype. Consequently, there is little direct evidence of the underpinning regulatory mechanisms leading to induced resistance to chill injury. Here, we review recent advances mainly in lower vertebrates and in arthropods, but increasingly in genetic model species from a broader range of taxa. KEY WORDS: Membrane fluidity, Proteostasis, Compatible solutes, Gene ablation IntroductionEnvironmental cold poses multiple problems for all living organisms, especially poikilotherms (Cossins and Bowler, 1987). The effects of low temperature on performance are largely determined by the extent to which cooling reduces the rate of biochemical reactions -thus slowing down any rate-dependent processes (Hochachka and Somero, 2002). The impact on survival, however, is determined by the disruptive effects of extreme cold on *Author for correspondence (cossins@liverpool.ac.uk) the molecular processes underpinning normal cellular function, such as protein and membrane integrity, which in turn are closely associated with such fundamental cellular properties such as ion homeostasis and continued activity of excitable cells (Lee, 2010). Thus, at some point during both declining temperatures and diminishing performance, cold becomes stressful, and chilling injuries then accumulate over time, leading...

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