Nervous system development and regeneration in freshwater planarians

Ross, Kelly; Currie, Ko W.; Pearson, Bret J.; Zayas, Ricardo M.

doi:10.1002/wdev.266

Cited by 76 publications

(63 citation statements)

References 175 publications

(540 reference statements)

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“…One of the most astonishing regenerative abilities of freshwater planarians is their ability to regrow a complete functional central nervous system (CNS) de novo from a tiny portion of the organism (Ross et al, 2017). The planarian CNS consists of an anterior bilobed brain or cephalic ganglia connected by a transverse commissure, lying on top of two ventral nerve cords that extend throughout the length of the animal (Agata et al, 1998;Cebrià et al, 2002b).…”

Section: Central Nervous Systemmentioning

confidence: 99%

“…The planarian CNS consists of an anterior bilobed brain or cephalic ganglia connected by a transverse commissure, lying on top of two ventral nerve cords that extend throughout the length of the animal (Agata et al, 1998;Cebrià et al, 2002b). In contrast to its apparent morphological simplicity, the planarian CNS displays a high degree of molecular sub-compartmentalization and complexity (Umesono et al, 1999;Cebrià et al, 2002c), and a wide range of neuronal types (reviewed in Cebrià, 2007;Ross et al, 2017). These include cholinergic (Nishimura et al, 2010), GABAergic (Nishimura et al, 2008a), dopaminergic (Nishimura et al, 2007a), octopaminergic (Nishimura et al, 2008b), serotonergic (Nishimura et al, 2007b;Cebrià, 2008), and neuropeptide F-and GYRFamide-positive (Cebrià, 2008) neurons, as well as several other subpopulations characterized by the expression of specific neuropeptides (Collins et al, 2010).…”

Section: Central Nervous Systemmentioning

confidence: 99%

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Rebuilding a planarian: from early signaling to final shape

Cebrià¹,

Adell²,

Saló³

2018

Int. J. Dev. Biol.

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Why some animals can regenerate and others not has fascinated biologists since the first examples of regeneration were reported. Although many animal phyla include species with some regenerative ability, mainly restricted to particular cell types or tissues, there are some other species capable of regenerating complex structures, such as the vertebrate limb and heart. More remarkably, there are some examples of animals that can regenerate the whole body from a tiny piece of them. Understanding how regeneration is triggered and achieved in these animals is fundamental not only to understand this fascinating primary biological question, but also because of its implications for the field of regenerative medicine. Here, we discuss one of the models with higher regenerative capabilities: the freshwater planarians. Two key features make planarians an attractive model to study regeneration: the presence of adult pluripotent stem cells and the permanent activation of the morphogenetic mechanisms that instruct cell fate. Here, we revise our current knowledge of key events that lead to successful regeneration including: how heterogeneous is the stem cell population; what are the immediate changes at the gene level after amputation and what triggers the regenerative response; how is axial polarity re-established; how do the different cell types differentiate from lineage-committed progenitors and how is size and organ proportionality controlled. Finally, we point out some open questions that the field needs to address in the near future.

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Section: Central Nervous Systemmentioning

confidence: 99%

Section: Central Nervous Systemmentioning

confidence: 99%

Rebuilding a planarian: from early signaling to final shape

Cebrià¹,

Adell²,

Saló³

2018

Int. J. Dev. Biol.

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“…In fact, high levels of adult neurogenesis and neural regeneration have been found in cnidarians, invertebrates, and vertebrates alike, suggesting that the ancestral state was that of significant neural plasticity (Holstein et al, 2003; Reddien and Sánchez Alvarado, 2004; Tanaka and Reddien, 2011; Kizil et al, 2012; Ross et al, 2017). Highly-regenerative organisms that can replace much of their nervous system offer a unique opportunity to study the cellular and molecular underpinnings of adult neurogenesis in an unrestricted context.…”

Section: Introductionmentioning

confidence: 99%

A Brain Unfixed: Unlimited Neurogenesis and Regeneration of the Adult Planarian Nervous System

Brown

Pearson

2017

Front. Neurosci.

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Powerful genetic tools in classical laboratory models have been fundamental to our understanding of how stem cells give rise to complex neural tissues during embryonic development. In contrast, adult neurogenesis in our model systems, if present, is typically constrained to one or a few zones of the adult brain to produce a limited subset of neurons leading to the dogma that the brain is primarily fixed post-development. The freshwater planarian (flatworm) is an invertebrate model system that challenges this dogma. The planarian possesses a brain containing several thousand neurons with very high rates of cell turnover (homeostasis), which can also be fully regenerated de novo from injury in just 7 days. Both homeostasis and regeneration depend on the activity of a large population of adult stem cells, called neoblasts, throughout the planarian body. Thus, much effort has been put forth to understand how the flatworm can continually give rise to the diversity of cell types found in the adult brain. Here we focus on work using single-cell genomics and functional analyses to unravel the cellular hierarchies from stem cell to neuron. In addition, we will review what is known about how planarians utilize developmental signaling to maintain proper tissue patterning, homeostasis, and cell-type diversity in their brains. Together, planarians are a powerful emerging model system to study the dynamics of adult neurogenesis and regeneration.

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“…The key advantage of the planarian system is its sufficiently 70 complex behavioral repertoire which enables distinct behaviors to be used as a multifaceted 71 quantitative readout of neuronal function (Hagstrom et al, 2019;Zhang et al, 2019aZhang et al, , 2019b. The 72 planarian nervous system is of medium size (~10,000 neurons), possessing >95% gene homology 73 and sharing most of the same neurotransmitters and neuronal cell types as the mammalian brain 74 (Buttarelli et al, 2008;Mineta et al, 2003;Ross et al, 2017). Thus, the planarian system allows 75 for mechanistic insights into how different cells and pathways control specific behaviors (Birkholz 76 and…”

mentioning

confidence: 99%

Dugesia japonica is the best suited of three planarian species for high-throughput toxicology screening

Ireland

Bochenek

Chaiken

et al. 2020

Preprint

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AbstractHigh-throughput screening (HTS) using new approach methods is revolutionizing toxicology. Asexual freshwater planarians are a promising invertebrate model for neurotoxicity HTS because their diverse behaviors can be used as quantitative readouts of neuronal function. Currently, three planarian species are commonly used in toxicology research: Dugesia japonica, Schmidtea mediterranea, and Girardia tigrina. However, only D. japonica has been demonstrated to be suitable for HTS. Here, we assess the two other species for HTS suitability by direct comparison with D. japonica. Through quantitative assessments of morphology and multiple behaviors, we assayed the effects of 4 common solvents (DMSO, ethanol, methanol, ethyl acetate) and a negative control (sorbitol) on neurodevelopment. Each chemical was screened blind at 5 concentrations at two time points over a twelve-day period. We obtained two main results: First, G. tigrina and S. mediterranea planarians showed significantly reduced movement compared to D. japonica under HTS conditions, due to decreased health over time and lack of movement under red lighting, respectively. This made it difficult to obtain meaningful readouts from these species. Second, we observed species differences in sensitivity to the solvents, suggesting that care must be taken when extrapolating chemical effects across planarian species. Overall, our data show that D. japonica is best suited for behavioral HTS given the limitations of the other species. Standardizing which planarian species is used in neurotoxicity screening will facilitate data comparisons across research groups and accelerate the application of this promising invertebrate system for first-tier chemical HTS, helping streamline toxicology testing.

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Nervous system development and regeneration in freshwater planarians

Cited by 76 publications

References 175 publications

Rebuilding a planarian: from early signaling to final shape

Rebuilding a planarian: from early signaling to final shape

A Brain Unfixed: Unlimited Neurogenesis and Regeneration of the Adult Planarian Nervous System

Dugesia japonica is the best suited of three planarian species for high-throughput toxicology screening

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