Pathogenic shifts in endogenous microbiota impede tissue regeneration via distinct activation of TAK1/MKK/p38

Arnold, Carrie; Merryman, M Shane; Harris-Arnold, Aleishia; McKinney, Sean A.; Seidel, Chris; Loethen, Sydney; Proctor, Kylie N; Guo, Longhua; Alvarado, Alejandro Sánchez

doi:10.7554/elife.16793

Cited by 93 publications

(101 citation statements)

References 75 publications

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“…Recent work with the planarian S. mediterranea found similar bacterial types as we detected in D. japonica, and blooms of Proteobacteria in the S. mediterranea microbiome were associated with tissue degeneration, while high abundances of Bacteroidetes, including Chryseobacterium and Pedobacter, were associated with healthy animals (Arnold et al, 2016). Work is ongoing to analyze the functional significance of the D. japonica microbiome, but we predict that shifts in the ratio of Proteobacteria and Bacteroidetes may also impact D. japonica growth and development.…”

Section: Ta B L Esupporting

confidence: 80%

Planarian regeneration in space: Persistent anatomical, behavioral, and bacteriological changes induced by space travel

et al. 2017

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Regeneration is regulated not only by chemical signals but also by physical processes, such as bioelectric gradients. How these may change in the absence of the normal gravitational and geomagnetic fields is largely unknown. Planarian flatworms were moved to the International Space Station for 5 weeks, immediately after removing their heads and tails. A control group in spring water remained on Earth. No manipulation of the planaria occurred while they were in orbit, and space‐exposed worms were returned to our laboratory for analysis. One animal out of 15 regenerated into a double‐headed phenotype—normally an extremely rare event. Remarkably, amputating this double‐headed worm again, in plain water, resulted again in the double‐headed phenotype. Moreover, even when tested 20 months after return to Earth, the space‐exposed worms displayed significant quantitative differences in behavior and microbiome composition. These observations may have implications for human and animal space travelers, but could also elucidate how microgravity and hypomagnetic environments could be used to trigger desired morphological, neurological, physiological, and bacteriomic changes for various regenerative and bioengineering applications.

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Section: Ta B L Esupporting

confidence: 80%

Planarian regeneration in space: Persistent anatomical, behavioral, and bacteriological changes induced by space travel

et al. 2017

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“…After animal dissociation, cells associated with mCherry/mScarlet-labelled E. coli or with bioparticles had similar complex cytoplasmic appearances, with numerous intracellular bodies observable by Nomarski microscopy (Figure S7H-L). Using an endogenous bacterial-level assay [30], foxF-1 RNAi animals had significantly more bacteria than controls (Figure S7M). This could reflect intestinal and/or cathepsin + cell dysfunction.…”

Section: Resultsmentioning

confidence: 99%

“…Three or four animals were pooled and homogenized in 100 μl of deionized water. 25 μl was then plated on LB agar without any antibiotics and incubated in the dark at room temperature [30]. A water control was also plated, but no bacterial colonies grew on those plates at the time of bacterial colony counting.…”

Section: Star Methodsmentioning

confidence: 99%

foxF-1 Controls Specification of Non-body Wall Muscle and Phagocytic Cells in Planarians

et al. 2018

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Summary Planarians are flatworms capable of regenerating any missing body part in a process requiring stem cells and positional information. Muscle is a major source of planarian positional information and consists of several types of fibers with distinct regulatory roles in regeneration. The transcriptional regulatory programs used to specify different muscle fibers are poorly characterized. Using single-cell RNA sequencing, we define the transcriptomes of planarian dorsal-ventral muscle (DVM), intestinal muscle (IM), and pharynx muscle. This analysis identifies foxF-1, which encodes a broadly conserved Fox-family transcription factor, as a master transcriptional regulator of all non-body wall muscle. The transcription factor genes nk4 and gata4/5/6–2 specify two different subsets of DVM, lateral and medial, respectively, whereas gata4/5/6–3 specifies IM. These muscle types all express planarian patterning genes. Both lateral and medial DVM are required for medial-lateral patterning in regeneration whereas medial DVM and IM have a role in maintaining and regenerating intestine morphology. In addition to the role in muscle, foxF-1 is required for the specification of multiple cell types with transcriptome similarities, including high expression levels of cathepsin genes. These cells include pigment cells, glia, and several other cells with unknown function. cathepsin+ cells phagocytose E. coli, suggesting these are phagocytic cells. In conclusion, we describe a regulatory program for planarian muscle cell subsets and phagocytic cells both driven by foxF-1. FoxF proteins specify different mesoderm-derived tissues in other organisms, suggesting that FoxF regulates formation of an ancient and broadly conserved subset of mesoderm derivatives in the Bilateria.

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“…These studies revealed that gut microbiota can have remote benefits on the wound healing process. Arnold et al () used a planarium ( Schmidtea mediterranea ) as a model organism in order to study the relationship between gut microbiota and tissue regeneration. Schmidtea mediterranea can regenerate and replace any of its either damaged or lost tissues.…”

Section: The Remote Effect Of the Gut Microbiota On Tissue Healing Anmentioning

confidence: 99%

The role of microbiota in tissue repair and regeneration

Shavandi

Saeedi

Gérard

et al. 2020

J Tissue Eng Regen Med

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A comprehensive understanding of the human body endogenous microbiota is essential for acquiring an insight into the involvement of microbiota in tissue healing and regeneration process in order to enable development of biomaterials with a better integration with human body environment. Biomaterials used for biomedical applications are normally germ‐free, and the human body as the host of the biomaterials is not germ‐free. The complexity and role of the body microbiota in tissue healing/regeneration have been underestimated historically. Traditionally, studies aiming at the development of novel biomaterials had focused on the effects of environment within the target tissue, neglecting the signals generated from the microbiota and their impact on tissue regeneration. The significance of the human body microbiota in relation to metabolism, immune system, and consequently tissue regeneration has been recently realised and is a growing research field. This review summarises recent findings on the role of microbiota and mechanisms involved in tissue healing and regeneration, in particular skin, liver, bone, and nervous system regrowth and regeneration highlighting the potential new roles of microbiota for development of a new generation of biomaterials.

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Pathogenic shifts in endogenous microbiota impede tissue regeneration via distinct activation of TAK1/MKK/p38

Cited by 93 publications

References 75 publications

Planarian regeneration in space: Persistent anatomical, behavioral, and bacteriological changes induced by space travel

Planarian regeneration in space: Persistent anatomical, behavioral, and bacteriological changes induced by space travel

foxF-1 Controls Specification of Non-body Wall Muscle and Phagocytic Cells in Planarians

The role of microbiota in tissue repair and regeneration

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