The Cellular and Molecular Basis for Planarian Regeneration

Reddien, Peter W.

doi:10.1016/j.cell.2018.09.021

Cited by 264 publications

(307 citation statements)

References 126 publications

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“…In C. elegans, axons of select neurons can regenerate after being severed [7] ; however, growth trajectories are error-prone [8] even when identical neurons across animals are subjected to similar injury protocols [9]. Exceptional neural plasticity can be found in planarians, which can reform entire organisms [10] from small fragments of tissue, but these animals lack a suite of transgenic tools similar to that of Drosophila and C. elegans [11].…”

Section: Introductionmentioning

confidence: 99%

Stable behavioral and neural responses to thermal stimulation despite large changes in theHydra vulgarisnervous system

Tzouanas

et al. 2019

Preprint

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Nervous systems are remarkable for supporting stable animal behavior despite dramatic changes to neurons' number and connectivity. An ideal model organism to study this phenomenon would have: 1) dynamic neural architecture 2) transgenic reporters of neural activity, 3) a small, transparent body, and 4) well-defined sensory-motor behaviors. While Hydra vulgaris possesses the first three advantages, it currently lacks well-characterized sensory-motor responses. Here, we show the first quantitative measurements of Hydra's behavioral responses to thermal stimulation and associated neural activity.Specifically, we find that Hydra elongate and then contract when heated. This behavior is accompanied by synchronous, periodic activity of neurons in the animal's peduncle. We find that the frequency of these neural oscillations is nearly the same even if the number of neurons change by a factor of two.These observations suggest that Hydra provides a rich model for studying how animals maintain stable sensory-motor responses within dynamic neural circuit architectures.One sentence summary: Here we show that Hydra have a group of thermally responsive neurons that encodes the absolute temperature of a thermal stimulus and that this encoding is independent of the number of neurons in the animal.

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Section: Introductionmentioning

confidence: 99%

Stable behavioral and neural responses to thermal stimulation despite large changes in theHydra vulgarisnervous system

Tzouanas

et al. 2019

Preprint

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“…Driven by the recent application of genomic and molecular methods, the planarian flatworm Schmidtea mediterranea has become a powerful model in which to address the molecular and cellular underpinnings of organ regeneration (9–13). In response to nearly any type of surgical amputation injury, pluripotent stem cells called neoblasts proliferate and differentiate, regenerating brain, intestine, and other tissues lost to injury (14, 15).…”

Section: Introductionmentioning

confidence: 99%

Cell-type diversity and regionalized gene expression in the planarian intestine revealed by laser-capture microdissection transcriptome profiling

Forsthoefel

Cejda

Khan

et al. 2019

Preprint

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Organ regeneration requires precise coordination of new cell differentiation and remodeling of uninjured tissue to faithfully re-establish organ morphology and function. An atlas of gene expression and cell types in the uninjured state is therefore an essential pre-requisite for understanding how damage is repaired. Here, we use laser-capture microdissection (LCM) and RNA-Seq to define the transcriptome of the intestine of Schmidtea mediterranea, a planarian flatworm with exceptional regenerative capacity. Bioinformatic analysis of 1,844 intestine-enriched transcripts suggests extensive conservation of digestive physiology with other animals, including humans. Comparison of the intestinal transcriptome to purified absorptive intestinal cell (phagocyte) and published single-cell expression profiles confirms the identities of known intestinal cell types, and also identifies hundreds of additional transcripts with previously undetected intestinal enrichment. Furthermore, by assessing the expression patterns of 143 transcripts in situ, we discover unappreciated mediolateral regionalization of gene expression and cell-type diversity, especially among goblet cells. Demonstrating the utility of the intestinal transcriptome, we identify 22 intestine-enriched transcription factors, and find that several have distinct functional roles in the regeneration and maintenance of goblet cells. Furthermore, depletion of goblet cells inhibits planarian feeding and reduces viability. Altogether, our results show that LCM is a viable approach for assessing tissue-specific gene expression in planarians, and provide a new resource for further investigation of digestive tract regeneration, the physiological roles of intestinal cell types, and axial polarity.

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“…Regeneration is a biological process that enables organ remodeling and repair in a number of 24 organisms, most prominent among them planarian flatworms with their ubiquitous ability to regenerate 25 all tissues in their body. While the regenerative process in planarians is well described (Reddien, 2018), 26 we address here two key knowledge gaps. First, it is not known how directional and positional 27 informational cues interact during regeneration -specifically, how tissue-level polarity adapts to changes 28 in organism-level polarity.…”

Section: Introduction 15mentioning

confidence: 98%

Nervous System and Tissue Polarity Dynamically Adapt to New Morphologies in Planaria

Bischof

Miller

LaPalme

et al. 2019

Preprint

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1The coordination of tissue-level polarity with organism-level polarity is crucial in development, 2 disease, and regeneration. Exploiting the flexibility of the body plan in regenerating planarians, we used 3 mirror duplication of the primary axis to show how established tissue-level polarity adapts to new 4 organism-level polarity. Tracking of cilia-driven flow to characterize planar cell polarity of the epithelium 5 revealed a remarkable reorientation of tissue polarity in double-headed planarians. This reorientation is 6 driven by signals produced by the intact brain and is not hampered by radiation-induced removal of stem 7 cells. The nervous system itself adapts its polarity to match the new organismal anatomy in these animals 8 as revealed by distinct regenerative outcomes driven by polarized nerve transport. Thus, signals from the 9 central nervous system can dynamically control and re-orient tissue-level polarity to match the organism-10 level anatomical configuration, illustrating a novel role of the nervous system in the regulation of 11 patterning. 12 13 14 6 130 Figure 1: Flow driven by the multiciliated epithelium can be tracked and epithelial polarity dynamically remodels 131 in DH animals. A) (i) Morphological differences in head development in DHs can be observed at Day 7 (days after 132 amputation -dpa), revealing that the primary head (ii) is more developed than the secondary head (iii). (iv) In DHs 133 at Day 49 both heads (v, vi) are equally developed. Scale bars 1 mm. B) Cilia of the multiciliated ventral surface 134 epithelium stained with antibody against acetylated-tubulin at (i) low and (ii) high magnification. Scale bar 100 μm 135 in (i) and 25 μm in (ii). C) Flow driven by cilia beat can be visualized with carmine powder and tracked with particle 136 image velocimetry (PIV) in a single-headed animal (red arrows). D) Opposing flow directions in DH animals lead to 137 the accumulation of particles at the point where the opposing flow fields meet. This "collision zone" (asterisk) 138 repositions towards the middle of the animal from Day 7 until Day 49. E) Plot of position of the collision zone as 139

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The Cellular and Molecular Basis for Planarian Regeneration

Cited by 264 publications

References 126 publications

Stable behavioral and neural responses to thermal stimulation despite large changes in theHydra vulgarisnervous system

Stable behavioral and neural responses to thermal stimulation despite large changes in theHydra vulgarisnervous system

Cell-type diversity and regionalized gene expression in the planarian intestine revealed by laser-capture microdissection transcriptome profiling

Nervous System and Tissue Polarity Dynamically Adapt to New Morphologies in Planaria

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