Functional analysis of a pancreatic secretory trypsin inhibitor-like protein in insects: Silencing effects resemble the human pancreatic autodigestion phenotype

Hoef, Vincent van; Breugelmans, Bert; Spit, Jornt; Simonet, Gert; Zels, Sven; Billen, Johan; Broeck, Jozef Vanden

doi:10.1016/j.ibmb.2011.04.012

Cited by 17 publications

(13 citation statements)

References 25 publications

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“…Serine protease inhibitors (Serpins) in which kazal domains are found are involved in protection against autophagy in metazoan digestive systems (Chera et al 2006). Although homologs have been found in insects they appear to be highly specialized and in some cases structurally diverse (Nirmala et al 2001; van Hoef et al 2011). …”

Section: Resultsmentioning

confidence: 99%

New Tricks for “Old” Domains: How Novel Architectures and Promiscuous Hubs Contributed to the Organization and Evolution of the ECM

Cromar

Wong

Loughran

et al. 2014

Genome Biology and Evolution

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The extracellular matrix (ECM) is a defining characteristic of metazoans and consists of a meshwork of self-assembling, fibrous proteins, and their functionally related neighbours. Previous studies, focusing on a limited number of gene families, suggest that vertebrate complexity predominantly arose through the duplication and subsequent modification of retained, preexisting ECM genes. These genes provided the structural underpinnings to support a variety of specialized tissues, as well as a platform for the organization of spatio-temporal signaling and cell migration. However, the relative contributions of ancient versus novel domains to ECM evolution have not been quantified across the full range of ECM proteins. Here, utilizing a high quality list comprising 324 ECM genes, we reveal general and clade-specific domain combinations, identifying domains of eukaryotic and metazoan origin recruited into new roles in approximately two-third of the ECM proteins in humans representing novel vertebrate proteins. We show that, rather than acquiring new domains, sampling of new domain combinations has been key to the innovation of paralogous ECM genes during vertebrate evolution. Applying a novel framework for identifying potentially important, noncontiguous, conserved arrangements of domains, we find that the distinct biological characteristics of the ECM have arisen through unique evolutionary processes. These include the preferential recruitment of novel domains to existing architectures and the utilization of high promiscuity domains in organizing the ECM network around a connected array of structural hubs. Our focus on ECM proteins reveals that distinct types of proteins and/or the biological systems in which they operate have influenced the types of evolutionary forces that drive protein innovation. This emphasizes the need for rigorously defined systems to address questions of evolution that focus on specific systems of interacting proteins.

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Section: Resultsmentioning

confidence: 99%

New Tricks for “Old” Domains: How Novel Architectures and Promiscuous Hubs Contributed to the Organization and Evolution of the ECM

Cromar

Wong

Loughran

et al. 2014

Genome Biology and Evolution

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“…Therefore, locusts are attractive organisms for loss of function analyses, as already demonstrated in several studies (Badisco et al, 2011;He et al, 2006;Marchal et al, 2012;Ott et al, 2012;van Hoef et al, 2011;Van Wielendaele et al, 2012Wang et al, 2013;Zhao et al, 2013).…”

Section: Sensitive Sysrnai Responses Of Locustsmentioning

confidence: 88%

Biological Mechanisms Determining the Success of RNA Interference in Insects

Wynant

Santos

Broeck

2014

International Review of Cell and Molecular Biology

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“…We do not know whether this process of gradual accrual of enzymes in the bursal lumen presents a liability for older unmated females as a result of autodigestion. Intestinal tissues and other digestive organs exhibit preservative or inhibitory mechanisms that reduce the risk of autophagy, such as storing enzymes in inactive forms or secreting specialized inhibitor-like proteins (Hirota et al, 2006;van Hoef et al, 2011). Whether such mechanisms are also present in the bursa is not known, but could present a fruitful avenue for further study.…”

Section: Discussionmentioning

confidence: 99%

“…However, female responses to social cues remain largely unknown. Because digestive enzymes can present a physiological liability at high concentrations (Hirota et al, 2006;van Hoef et al, 2011), we expected that exposure to courting males might stimulate females to increase protease production in anticipation of imminent mating. However, if males are constantly present in a virgin female's environment or females rarely have the opportunity to realize a benefit from such phenotypic plasticity, we would expect little to no effect of male exposure on bursal physiology.…”

Section: Introductionmentioning

confidence: 99%

Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly

Plakke

Deutsch

Meslin

et al. 2015

Journal of Experimental Biology

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Reproductive traits experience high levels of selection because of their direct ties to fitness, often resulting in rapid adaptive evolution. Much of the work in this area has focused on male reproductive traits. However, a more comprehensive understanding of female reproductive adaptations and their relationship to male characters is crucial to uncover the relative roles of sexual cooperation and conflict in driving co-evolutionary dynamics between the sexes. We focus on the physiology of a complex female reproductive adaptation in butterflies and moths: a stomach-like organ in the female reproductive tract called the bursa copulatrix that digests the male ejaculate (spermatophore). Little is known about how the bursa digests the spermatophore. We characterized bursa proteolytic capacity in relation to female state in the polyandrous butterfly Pieris rapae. We found that the virgin bursa exhibits extremely high levels of proteolytic activity. Furthermore, in virgin females, bursal proteolytic capacity increases with time since eclosion and ambient temperature, but is not sensitive to the pre-mating social environment. Post copulation, bursal proteolytic activity decreases rapidly before rebounding toward the end of a mating cycle, suggesting active female regulation of proteolysis and/or potential quenching of proteolysis by male ejaculate constituents. Using transcriptomic and proteomic approaches, we report identities for nine proteases actively transcribed by bursal tissue and/or expressed in the bursal lumen that may contribute to observed bursal proteolysis. We discuss how these dynamic physiological characteristics may function as female adaptations resulting from sexual conflict over female remating rate in this polyandrous butterfly.

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Functional analysis of a pancreatic secretory trypsin inhibitor-like protein in insects: Silencing effects resemble the human pancreatic autodigestion phenotype

Cited by 17 publications

References 25 publications

New Tricks for “Old” Domains: How Novel Architectures and Promiscuous Hubs Contributed to the Organization and Evolution of the ECM

New Tricks for “Old” Domains: How Novel Architectures and Promiscuous Hubs Contributed to the Organization and Evolution of the ECM

Biological Mechanisms Determining the Success of RNA Interference in Insects

Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly

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