Regional and Functional Differentiation in the Insect Fat Body

Haunerland, Norbert H.

doi:10.1146/annurev.ento.40.1.121

Cited by 54 publications

(68 citation statements)

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“…Although COX activity and ATP content are lower during diapause in both the brain and fat body, suppression during diapause is much more pronounced in the fat body. The fat body, which functions much like the mammalian liver, is the key site of intermediary metabolism (10,11), and thus, the pronounced shutdown of this organ is likely responsible for the major metabolic shifts noted in association with diapause (2,3,12). The fact that gene expression in the fat body rapidly responds to an injection of ecdysone (Fig.…”

Section: Resultsmentioning

confidence: 99%

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

Denlinger

2012

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

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: Resultsmentioning

confidence: 99%

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

Denlinger

2012

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

108

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“…The functional signi¢cance of the clear regional and structural di¡erentiation within the fat body, the main storage and metabolic organ in insects, has been little explored (Haunerland & Shirk 1995). In addition, the mobilization of other tissues, notably muscles, for egg production and maintenance is a well-known phenomenon in insects (Usherwood 1975;Stjernholm & Karlsson 2000).…”

Section: Discussionmentioning

confidence: 99%

Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect

Rivero

Giron

Casas

2001

Proc. R. Soc. Lond. B

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In holometabolous insects reproductive success is strongly determined by the nutritional resources available to the females. In addition to nutrients derived from adult feeding, resources for egg production may come from the limited reserves accumulated during the larval stages. The pattern of allocation of these larval reserves to egg production is expected to be strongly linked to the nutritional ecology of the adult. We investigate the temporal pattern of allocation of larval reserves to reproduction in a hostfeeding parasitoid wasp. As predicted by the dynamics of allocation of an adult meal, larval reserves are the main source of nutrients for four or ¢ve days after emergence. However, despite the high frequency of host feeding and the high nutrient content of a haemolymph meal, which we predicted would lead to larval reserves being conserved in the event of host deprivation, larval reserves contribute to egg production throughout the lifetime of the female. We propose several mechanistic and adaptive explanations for our results, including the possible existence of a limiting or key nutrient for egg production of exclusively larval origin. We make further predictions concerning the pattern of allocation of larval resources in parasitoids with di¡erent adult nutritional requirements.

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“…Fat body nutrient content correlates with survival capability in insects (Haunerland and Shirk, 1995;Hahn and Denlinger, 2007). Honeybee fat body also influences worker lifespan by acting as the synthesis organ of vitellogenin, a glyco-lipoprotein (Seehuus et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera)

Smedal

Brynem

Kreibich

et al. 2009

Journal of Experimental Biology

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SUMMARYHoneybee (Apis mellifera) society is characterized by a helper caste of essentially sterile female bees called workers. Workers show striking changes in lifespan that correlate with changes in colony demography. When rearing sibling sisters (brood), workers survive for 3-6 weeks. When brood rearing declines, worker lifespan is 20 weeks or longer. Insects can survive unfavorable periods on endogenous stores of protein and lipid. The glyco-lipoprotein vitellogenin extends worker bee lifespan by functioning in free radical defense, immunity and behavioral control. Workers use vitellogenin in brood food synthesis, and the metabolic cost of brood rearing (nurse load) may consume vitellogenin stores and reduce worker longevity. Yet, in addition to consuming resources, brood secretes a primer pheromone that affects worker physiology and behavior. Odors and odor perception can influence invertebrate longevity but it is unknown whether brood pheromone modulates vitellogenin stores and survival. We address this question with a 2-factorial experiment where 12 colonies are exposed to combinations of absence vs presence of brood and brood pheromone. Over an age-course of 24 days, we monitor the amount of vitellogenin stored in workers' fat body (adipose tissue). Thereafter, we track colony survival for 200 days. We demonstrate that brood rearing reduces worker vitellogenin stores and colony long-term survival. Yet also, we establish that the effects can result solely from exposure to brood pheromone. These findings indicate that molecular systems of extreme lifespan regulation are integrated with the sensory system of honeybees to respond to variation in a primer pheromone secreted from larvae. Supplementary material available online at

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Regional and Functional Differentiation in the Insect Fat Body

Cited by 54 publications

References 0 publications

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

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

Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect

Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera)

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