Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut

Agrawal, Sinu; Kelkenberg, Marco; Begum, Khurshida; Steinfeld, Lea; Williams, Clay; Kramer, Karl J.; Beeman, Richard W.; Park, Yoonseong; Muthukrishnan, Subbaratnam; Merzendorfer, Hans

doi:10.1016/j.ibmb.2014.03.009

Cited by 85 publications

(76 citation statements)

References 44 publications

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“…The variations in the number and sequence of CBDs in PMPs may also be an adaptive evolution of this family of proteins to food preferences, which differs from one insect species to another. The fact that only a limited number of PMPs have been shown to be essential for normal PM functional integrity and insect survival (Agrawal et al, 2014) supports the notion that a more recent expansion of the PMP family allowed adaptation of insects to diverse hosts. Additional genome sequence information from more insect species and more studies on CBPs functions are needed to better understand the roles of PMPs in insects.…”

Section: Origin and Evolution Of Cbds In Cpaps And Pmps E Descriptionmentioning

confidence: 68%

“…In a recent study, knocking down 2 of the 11 PMP genes from T. castaneum by RNAi (TcPMP3 and TcPMP5-B) caused abnormal larval growth and molting, and eventually death (Agrawal et al, 2014). Inhibition of the other 9 PMP genes did not show any noticeable abnormal phenotype, suggesting that they may have redundant functions and that they are not mandatory for insect development and survival.…”

Section: Phylogenetic Analysis Of Pmpsmentioning

confidence: 98%

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Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects

Tetreau

Dittmer

Cao

et al. 2015

Insect Biochemistry and Molecular Biology

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In insects, chitin is a major structural component of the cuticle and the peritrophic membrane (PM). In nature, chitin is always associated with proteins among which chitin-binding proteins (CBPs) are the most important for forming, maintaining and regulating the functions of these extracellular structures. In this study, a genome-wide search for genes encoding proteins with ChtBD2-type (peritrophin A-type) chitin-binding domains (CBDs) was conducted. A total of 53 genes encoding 56 CBPs were identified, including 15 CPAP1s (cuticular proteins analogous to peritrophins with 1 CBD), 11 CPAP3s (CPAPs with 3 CBDs) and 17 PMPs (PM proteins) with a variable number of CBDs, which are structural components of cuticle or of the PM. CBDs were also identified in enzymes of chitin metabolism including 6 chitinases and 7 chitin deacetylases encoded by 6 and 5 genes, respectively. RNA-seq analysis confirmed that PMP and CPAP genes have differential spatial expression patterns. The expression of PMP genes is midgut-specific, while CPAP genes are widely expressed in different cuticle forming tissues. Phylogenetic analysis of CBDs of proteins in insects belonging to different orders revealed that CPAP1s from different species constitute a separate family with 16 different groups, including 6 new groups identified in this study. The CPAP3s are clustered into a separate family of 7 groups present in all insect orders. Altogether, they reveal that duplication events of CBDs in CPAP1s and CPAP3s occurred prior to the evolutionary radiation of insect species. In contrast to the CPAPs, all CBDs from individual PMPs are generally clustered and distinct from other PMPs in the same species in phylogenetic analyses, indicating that the duplication of CBDs in each of these PMPs occurred after divergence of insect species. Phylogenetic analysis of these three CBP families showed that the CBDs in CPAP1s form a clearly separate family, while those found in PMPs and CPAP3s were clustered together in the phylogenetic tree. For chitinases and chitin deacetylases, most of phylogenetic analysis performed with the CBD sequences resulted in similar clustering to the one obtained by using catalytic domain sequences alone, suggesting that CBDs were incorporated into these enzymes and evolved in tandem with the catalytic domains before the diversification of different insect orders. Based on these results, the evolution of CBDs in insect CBPs is discussed to provide a new insight into the CBD sequence structure and diversity, and their evolution and expression in insects.

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Section: Origin and Evolution Of Cbds In Cpaps And Pmps E Descriptionmentioning

confidence: 68%

Section: Phylogenetic Analysis Of Pmpsmentioning

confidence: 98%

Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects

Tetreau

Dittmer

Cao

et al. 2015

Insect Biochemistry and Molecular Biology

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“…B). As a result, the best strategy for applying oral RNAi using liposome encapsulation systems for pest control should be based on targeting the genes expressed in the digestive system, many of which are vital, as shown by a number of studies . Another strategy that has been explored is to increase insecticide susceptibility by depleting detoxification genes, which might be other suitable targets for implementing RNAi pest control .…”

Section: Discussionmentioning

confidence: 99%

Oral delivery of dsRNA lipoplexes to German cockroach protects dsRNA from degradation and induces RNAi response

Lin

Huang

Liu

et al. 2016

Pest Management Science

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“…The peritrophic matrix (PM) is a thin acellular sheath that lines the midgut epithelium of most insects and envelops the midgut lumen content . The PM consists of a network of chitin fibrils associated with different classes of proteins, glycoproteins and proteoglycans, which confer strength and elasticity to this structure and influence its permeability properties . The sieving properties of the PM are related to the size and charge of the aqueous channels that cross this gel‐like structure and discriminate the passage of molecules .…”

Section: Introductionmentioning

confidence: 99%

“…affecting chitin, proteins or both. Recently, research efforts have also focused on the RNA interference approach to impair PM and insect performance …”

Section: Introductionmentioning

confidence: 99%

Effects of Trichoderma viride chitinases on the peritrophic matrix of Lepidoptera

Berini

Caccia

Franzetti

et al. 2015

Pest Management Science

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Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut

Cited by 85 publications

References 44 publications

Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects

Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects

Oral delivery of dsRNA lipoplexes to German cockroach protects dsRNA from degradation and induces RNAi response

Effects of Trichoderma viride chitinases on the peritrophic matrix of Lepidoptera

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