Smooth Muscle Tension Induces Invasive Remodeling of the Zebrafish Intestine

Seiler, Christoph; Davuluri, Gangarao; Abrams, Joshua; Byfield, Fitzroy J.; Janmey, Paul A.; Pack, Michael

doi:10.1371/journal.pbio.1001386

Cited by 52 publications

(76 citation statements)

References 83 publications

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“…For instance, the ingestive function depends also on paramecia availability (Fig. 4B), hunting success rate, and food preference among others, and the digestive function results from the synergistic action of gastric acid and pancreatic digestive enzyme secretion, peristaltic intestinal muscle contractions, epithelial nutrient absorption, and microbiota nutrient breakdown (14,27,32,41). As larval zebrafish share these features with higher vertebrates, the simultaneous experimental readout of these metrics and integration into the model represents abundant ground for future efforts.…”

Section: Discussionmentioning

confidence: 99%

A high-throughput assay for quantifying appetite and digestive dynamics

Jordi

Guggiana-Nilo

Soucy

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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Jordi J, Guggiana-Nilo D, Soucy E, Song EY, Wee CL, Engert F. A high-throughput assay for quantifying appetite and digestive dynamics. Am J Physiol Regul Integr Comp Physiol 309: R345-R357, 2015. First published June 24, 2015 doi:10.1152/ajpregu.00225.2015.-Food intake and digestion are vital functions, and their dysregulation is fundamental for many human diseases. Current methods do not support their dynamic quantification on large scales in unrestrained vertebrates. Here, we combine an infrared macroscope with fluorescently labeled food to quantify feeding behavior and intestinal nutrient metabolism with high temporal resolution, sensitivity, and throughput in naturally behaving zebrafish larvae. Using this method and rate-based modeling, we demonstrate that zebrafish larvae match nutrient intake to their bodily demand and that larvae adjust their digestion rate, according to the ingested meal size. Such adaptive feedback mechanisms make this model system amenable to identify potential chemical modulators. As proof of concept, we demonstrate that nicotine, L-lysine, ghrelin, and insulin have analogous impact on food intake as in mammals. Consequently, the method presented here will promote large-scale translational research of food intake and digestive function in a naturally behaving vertebrate.appetite; hunger; satiation; satiety; DiR' dye FOOD INTAKE AND DIGESTION are key physiological processes that provide nutrients to drive all bodily functions. Nutrient intake is matched to nutritional needs by the brain-a process termed nutrient homeostasis-using an intertwined organism-wide array of extrinsic and intrinsic cues coding food availability and demand (2, 42). Dysfunction of feeding and digestive behavior is at the root of global health problems, such as obesity, malnutrition, and Type 2 diabetes, among many others, and, therefore, a deeper understanding of feeding and digestive behavior is of high importance (25).Drugs or genetic manipulations that alter food intake or digestion are highly desirable remedies for food-related disorders. To screen for genes or small molecules with clinically desirable impact, the technology of choice needs to support the analyses of hundreds to thousands of individual animals. Until now, large-scale studies of feeding behavior have solely been feasible in small invertebrates such as Drosophila, but were constrained to 20 -50 conditions in vertebrates, thereby making large-scale screens elusive (12,17,35). Technically, even more demanding than measuring food intake is the quantification of nutrient digestion, as there is no direct optical access to the gastrointestinal tract in most species. More specialized technologies, such as bioluminescence, MRI, or computed tomography, have been valuable to generate insights into in vivo dynamics of digestive function (10,18,19,31). However, all of these methods require immobilization of the experimental subject to reduce motion artifacts, thereby making concurrent behavioral observations impossible. Consequently, quantifying the dy...

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Section: Discussionmentioning

confidence: 99%

A high-throughput assay for quantifying appetite and digestive dynamics

Jordi

Guggiana-Nilo

Soucy

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Using time-lapse imaging, the authors showed that epithelial cells have actin-rich protrusions that are enriched in cortactin and Tks5. They also observed a weak expression of MT1-MMP at the basal area of the cell (Seiler et al, 2012). Thus, cells can successfully cross the basement membrane, most likely through a combination of a proteolytic activity and mechanical forces.…”

Section: Invadosome Plasticitymentioning

confidence: 99%

“…For instance, one study has investigated the epithelial cell invasion within the developing intestine of zebrafish with a mutation in the myosin heavy chain 11 (mlt), which constitutively activates this protein, leading to a disrupted intestinal architecture (Seiler et al, 2012). Using time-lapse imaging, the authors showed that epithelial cells have actin-rich protrusions that are enriched in cortactin and Tks5.…”

Section: Invadosome Plasticitymentioning

confidence: 99%

The microenvironment controls invadosome plasticity

Martino

Henriet

Ezzoukhry

et al. 2016

Journal of Cell Science

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Invadosomes are actin-based structures involved in extracellular matrix degradation. Invadosomes is a term that includes podosomes and invadopodia, which decorate normal and tumour cells, respectively. They are mainly organised into dots or rosettes, and podosomes and invadopodia are often compared and contrasted. Various internal or external stimuli have been shown to induce their formation and/or activity. In this Commentary, we address the impact of the microenvironment and the role of matrix receptors on the formation, and dynamic and degradative activities of invadosomes. In particular, we highlight recent findings regarding the role of type I collagen fibrils in inducing the formation of a new linear organisation of invadosomes. We will also discuss invadosome plasticity more generally and emphasise its physio-pathological relevance.

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“…60 Other studies, performed in the zebrafish, showed that intestinal epithelial cells also form invadopodia-like protrusions and invade the stroma in response to a physical signal arising from smooth muscle contractility in the larval intestine. 61 Thus, invadopodia-like protrusions are conserved subcellular structures used for BM breaching during development. Using chick embryo as a model system to study epithelial-tomesenchymal transition (EMT) in gastrulation, Nakaya and colleagues showed that destabilization of microtubules at the epiblast's basal cell cortex weaken the interactions between epiblasts and BMs, which leads to BM breakdown.…”

Section: Breaching the Bm During Developmentmentioning

confidence: 99%