The regulation of expression of insect cuticle protein genes

Charles, Jean-Philippe

doi:10.1016/j.ibmb.2009.12.005

Cited by 150 publications

(111 citation statements)

References 110 publications

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“…Even within the same insect, they are selectively switched on or off at different developmental stages as well as in cuticles with different physical properties. Therefore, the chitin-binding cuticular proteins involved in modeling and maintaining body shape differ in identity and function according to the insect and developmental stage (Soares et al 2007;Okamoto et al 2008;Togawa et al 2008;Charles 2010), and our results show that mutation of the BmorCPR2 gene alters the overall morphology of larvae, validating its role in body-shape determination in silkworm. These findings suggest that the number, expression patterns, and functional diversification of chitin-binding cuticular proteins represent key factors in understanding the diversity of insect body shape and provide a reference to analyze the molecular basis for other body-shape mutants in silkworm.…”

Section: Resultssupporting

confidence: 60%

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Mutation of a Cuticular Protein,BmorCPR2, Alters Larval Body Shape and Adaptability in Silkworm,Bombyx mori

et al. 2014

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Cuticular proteins (CPs) are crucial components of the insect cuticle. Although numerous genes encoding cuticular proteins have been identified in known insect genomes to date, their functions in maintaining insect body shape and adaptability remain largely unknown. In the current study, positional cloning led to the identification of a gene encoding an RR1-type cuticular protein, BmorCPR2, highly expressed in larval chitin-rich tissues and at the mulberry leaf-eating stages, which is responsible for the silkworm stony mutant. In the Dazao-stony strain, the BmorCPR2 allele is a deletion mutation with significantly lower expression, compared to the wild-type Dazao strain. Dysfunctional BmorCPR2 in the stony mutant lost chitin binding ability, leading to reduced chitin content in larval cuticle, limitation of cuticle extension, abatement of cuticle tensile properties, and aberrant ratio between internodes and intersegmental folds. These variations induce a significant decrease in cuticle capacity to hold the growing internal organs in the larval development process, resulting in whole-body stiffness, tightness, and hardness, bulging intersegmental folds, and serious defects in larval adaptability. To our knowledge, this is the first study to report the corresponding phenotype of stony in insects caused by mutation of RR1-type cuticular protein. Our findings collectively shed light on the specific role of cuticular proteins in maintaining normal larval body shape and will aid in the development of pest control strategies for the management of Lepidoptera.T HE cuticle covering the entire body surface of insects not only participates in defense against pathogens and adverse environmental factors, but is also indispensable for constructing and maintaining external morphological characteristics and locomotion during the entire developmental process (Wigglesworth 1957;Delon and Payre 2004;Moussian et al. 2005). Therefore, the cuticle greatly enhances survival ability and adaptability of insects, ensuring its continued existence as one of the most successful life forms in the animal kingdom.The cuticle is a complex composite material mainly comprising chitin fibers and proteins (Andersen et al. 1995;Moussian 2010). Chitin is the polymer of b-1,4-linked N-acetyl-D-glucosamine (Gilbert 2011, Chap. 7). In procuticles, chitin fibers are arranged in laminae in an antiparallel manner and superimpose each other, forming sheets of fibrils that are stacked in a helicoidal fashion, maintaining cuticle structure, elasticity, and stability (Bouligand 1965;Neville and Luke 1969;Moussian 2010). In terrestrial insects, the chitin content is positively correlated with body size, suggesting a close relationship with cuticle extension and expansion (Merzendorfer and Zimoch 2003;Lease and Wolf 2010).Cuticular proteins (CPs), the principal structural constituents of cuticle, are encoded by more than 100 genes in known insect genomes (Andersen et al. 1995 The soft, flexible cuticle of Lepidoptera larvae not only bears pressure from ...

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Section: Resultssupporting

confidence: 60%

“…5). Chitin-binding cuticular proteins are widely distributed at different development stages and play roles in the physical properties of the cuticle ( Rebers and Riddiford 1988;Guan et al 2006;Soares et al 2007;Okamoto et al 2008;Togawa et al 2008;Charles 2010;Gilbert 2011, Chap. 5;Arakane et al 2012;Jasrapuria et al 2012).…”

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confidence: 99%

Mutation of a Cuticular Protein,BmorCPR2, Alters Larval Body Shape and Adaptability in Silkworm,Bombyx mori

et al. 2014

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“…CPR proteins with the RR-3 motif have been identified only in a few species (Andersen, 2000;Futahashi et al, 2008;Willis, 2010). Transcriptional regulation of CP gene expression appears to be regulated by developmental and hormonal cues (Ali et al, 2013;Charles, 2010). Togawa et al (2008) analyzed the temporal expression patterns of 152 CPR genes in A. gambiae by using real-time PCR.…”

Section: Introductionmentioning

confidence: 99%

Two major cuticular proteins are required for assembly of horizontal laminae and vertical pore canals in rigid cuticle of Tribolium castaneum

Noh

Kramer

Muthukrishnan

et al. 2014

Insect Biochemistry and Molecular Biology

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“…The 20E effects observed in the present study (recorded 3days after hormone injection) were obviously long-term effects, suggesting some possible control(s) on gene expression. Ecdysteroids are indeed able to trigger a cascade of events, involving a complex interplay of nuclear receptors, that allow coordinated and time-delayed expression of numerous proteins, as illustrated by the control of dopa-decarboxylase gene expression (reviewed in Hiruma and Riddiford, 2009), cuticular protein secretion (Charles, 2010) or neuroendocrine cascade regulating ecdysis (reviewed in Žitňan et al, 2007). Importantly, similar long-term effects of ecdysteroids on identified ion channels have been described in insects (see Grünewald and Levine, 1998;Börner et al, 2006;Garrison and Witten, 2010).…”

Section: Mode Of Action Of 20e On Neuronsmentioning

confidence: 99%

“…Indeed, hormonal titers fluctuate and reach a large peak during premolt, declining before ecdysis. These fluctuations, during the rising as well as the falling phases of the peak, are able to orchestrate the whole cascade of events leading not only to the synthesis of a new cuticle (reviewed in Charles, 2010), but also to many other related changes, including changes in behavior. For example, in insects, it has been demonstrated that a precocious ecdysteroid rise is involved in the initiation of wandering behavior before metamorphosis (Riddiford, 1976), whereas the drop of ecdysteroid concentrations after the hormonal peak is generally associated with an arrest of locomotion and the onset of a stereotyped behavioral sequence leading rapidly to ecdysis (reviewed in Truman, 2005;Žitňan et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Control of motor activity, via motoneuron excitability and sensory-motor integration, by the steroid hormone 20-hydroxyecdysone in crayfish

Bacqué-Cazenave

Bouvet

Fossat

et al. 2013

Journal of Experimental Biology

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SUMMARYWe studied the effects of the molting hormone 20-hydroxyecdysone (20E) on leg sensory-motor networks of the red swamp crayfish, Procambarus clarkii. The hormone was injected in isolated crayfish and network activity was analyzed 3days after injection using electrophysiology on an in vitro preparation of the leg locomotor network. This 20E treatment deeply reduced motor activity, by affecting both intrinsic motoneuron (MN) properties and sensory-motor integration. Indeed, we noticed a general decrease in motor nerve tonic activities, principally in depressor and promotor nerves. Moreover, intracellular recordings of depressor MNs confirmed a decrease of MN excitability due to a drop in input resistance. In parallel, sensory inputs originating from a proprioceptor, which codes joint movements controlled by these MNs, were also reduced. The shape of excitatory postsynaptic potentials (PSPs) triggered in MNs by sensory activity of this proprioceptor showed a reduction of polysynaptic components, whereas inhibitory PSPs were suppressed, demonstrating that 20E acted also on interneurons relaying sensory to motor inputs. Consequently, 20E injection modified the whole sensory-motor loop, as demonstrated by the alteration of the resistance reflex amplitude. These locomotor network changes induced by 20E were consistent with the decrease of locomotion observed in a behavioral test. In summary, 20E controls locomotion during crayfish premolt by acting on both MN excitability and sensory-motor integration. Among these cooperative effects, the drop of input resistance of MNs seems to be mostly responsible for the reduction of motor activity.

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The regulation of expression of insect cuticle protein genes

Cited by 150 publications

References 110 publications

Mutation of a Cuticular Protein,BmorCPR2, Alters Larval Body Shape and Adaptability in Silkworm,Bombyx mori

Mutation of a Cuticular Protein,BmorCPR2, Alters Larval Body Shape and Adaptability in Silkworm,Bombyx mori

Two major cuticular proteins are required for assembly of horizontal laminae and vertical pore canals in rigid cuticle of Tribolium castaneum

Control of motor activity, via motoneuron excitability and sensory-motor integration, by the steroid hormone 20-hydroxyecdysone in crayfish

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