Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration

Oviedo, Néstor J.; Morokuma, Junji; Walentek, Peter; Kema, Ido P.; Gu, Man Bock; Ahn, Joo Myung; Hwang, Jung Shan; Gojobori, Takashi; Levin, Michael

doi:10.1016/j.ydbio.2009.12.012

Cited by 189 publications

(244 citation statements)

References 62 publications

Supporting

Mentioning

236

Contrasting

Order By: Relevance

“…Patterning and size control during development and regeneration are also regulated by bioelectric signaling (52,(71)(72)(73)(74)(75)(76)(77)(78). Mutations in two strains of zebrafish with fin size phenotypes map to genes involved in bioelectric signaling (41,79).…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

Rabinowitz

Robitaille

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Regeneration requires cells to regulate proliferation and patterning according to their spatial position. Positional memory is a property that enables regenerating cells to recall spatial information from the uninjured tissue. Positional memory is hypothesized to rely on gradients of molecules, few of which have been identified. Here, we quantified the global abundance of transcripts, proteins, and metabolites along the proximodistal axis of caudal fins of uninjured and regenerating adult zebrafish. Using this approach, we uncovered complex overlapping expression patterns for hundreds of molecules involved in diverse cellular functions, including development, bioelectric signaling, and amino acid and lipid metabolism. Moreover, 32 genes differentially expressed at the RNA level had concomitant differential expression of the encoded proteins. Thus, the identification of proximodistal differences in levels of RNAs, proteins, and metabolites will facilitate future functional studies of positional memory during appendage regeneration.regeneration | positional memory | growth control | zebrafish | caudal fin

show abstract

Section: Discussionmentioning

confidence: 99%

Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

Rabinowitz

Robitaille

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…However, such results are now made more plausible by modern discoveries such as epigenetic modification, which occurs in many cell types, not just the CNS (Arshavsky, 2006;Day and Sweatt, 2010;Ginsburg and Jablonka, 2009;Levenson and Sweatt, 2005;Zovkic et al, 2013) and RNAi (Smalheiser et al, 2001). It is likely that brain remodeling (plasticity during learning) and regeneration are both regulated via epigenetic pathways that determine patterns of self-organization of neural (Arendt, 2005;Davies, 2012;Kennedy and Dehay, 2012;Saetzler et al, 2011) and non-neural but electrically communicating cells (Levin, 2012;Mondia et al, 2011;Oviedo et al, 2010;Tseng and Levin, 2013).…”

Section: Discussionmentioning

confidence: 99%

An automated training paradigm reveals long-term memory in planaria and its persistence through head regeneration

Shomrat

Levin

2013

Journal of Experimental Biology

Self Cite

102

View full text Add to dashboard Cite

SUMMARYPlanarian flatworms are a popular system for research into the molecular mechanisms that enable these complex organisms to regenerate their entire body, including the brain. Classical data suggest that they may also be capable of long-term memory. Thus, the planarian system may offer the unique opportunity to study brain regeneration and memory in the same animal. To establish a system for the investigation of the dynamics of memory in a regenerating brain, we developed a computerized training and testing paradigm that avoided the many issues that confounded previous, manual attempts to train planarians. We then used this new system to train flatworms in an environmental familiarization protocol. We show that worms exhibit environmental familiarization, and that this memory persists for at least 14days -long enough for the brain to regenerate. We further show that trained, decapitated planarians exhibit evidence of memory retrieval in a savings paradigm after regenerating a new head. Our work establishes a foundation for objective, high-throughput assays in this molecularly tractable model system that will shed light on the fundamental interface between body patterning and stored memories. We propose planarians as key emerging model species for mechanistic investigations of the encoding of specific memories in biological tissues. Moreover, this system is likely to have important implications for the biomedicine of stem-cell-derived treatments of degenerative brain disorders in human adults. Supplementary material available online at

show abstract

“…He strove at it doing all sorts of cutting experiments trying to deduce some general rules. Despite his work is nowadays considered the first 'classic' of planarian regeneration, he actually failed to answer the main questions posed regarding axial poplarity, as we still fail today to understand it completely despite the enormous progress reported in the last 5 years (Reddien et al, 2007;Gurley et al, 2007;Iglesias et al, 2008;Oviedo et al, 2010;Molina et al, 2011). Morgan's main conclusion was that "something" (meaning some factor or factors) in the structure or composition of the old tissue determined totipotent cells to regenerate the missing parts, with an antero-posterior and/or posterior-anterior qualitative gradation of such "factors" determining axial polarity (Morgan, 1905).…”

Section: The Early Stage (1890-1940): Neoblasts As Undifferentiated Wmentioning

confidence: 99%

“…A third, more physiological approach, is to look for systemic signals that mediate short-range and long-range cues involved to control from axial polarity to neoblast homeostasis. The recent finding of gap junction proteins (innexins) specific for neoblasts and for nerve cells (Oviedo and Levin, 2007), together with the importance of nervous system integrity to transmit inhibitory signals from anterior to posterior regions to avoid duplication of existing structures, highlights the importance of those signals, whatever they turn out to be, to regulate stem cell behaviour in adult organisms (Oviedo et al, 2010). Last but not least, the known effects of several ions, the role of ion channel proteins (Nogi et al, 2009), the plethora of neuropeptides and their agonists and antagonists on neoblast proliferation (Saló and Baguñà, 1986; reviewed in Baguñà et al, 1990), and of several signalling pathways (Wnt, BMP, Notch,..) acting on neoblast determination to specify axial polarity and regional identities (Gurley and Sanchez Alvarado, 2008;Reddien, 2011), also deserve further analyses.…”

Section: The Logic Of Neoblast Lineage and Its Proliferative Controlmentioning

confidence: 99%

The planarian neoblast: the rambling history of its origin and some current black boxes

Baguñà¹

2012

Int. J. Dev. Biol.

145

111

View full text Add to dashboard Cite

First described by Randolph in 1897, the nature and main features of planarian neoblasts have a long rambling history. While their morphologically undifferentiated features have long been recognized, their origin and actual role during regeneration have been highly debated. Here I summarize the main stages of this rambling history: 1) undifferentiated, wandering cells of uncertain origin with a main, albeit undefined, role in regeneration (1890-1940s); 2) quiescent, undifferentiated cells whose main function is to build the blastema during regeneration, an idea which culminated in the 'neoblast theory' of the French School (1940-1960); 3) neoblasts as temporal, undifferentiated cells arising by dedifferentiation from differentiated cells (the 'cell dedifferentiation theory'; 1960-1980s); 4) a new paradigm, starting in the late 1970s-early 1980s, that brought together the role of neoblasts as the main cell for regeneration, with its more important role as somatic stem cells for the daily wear and tear of tissues and as the source of germ cells; and 5) more recent developments that culminate in the report of rescuing lethally irradiated planarians by injection of single neoblasts, which makes of neoblasts an unrivaled toti-, pluripotent somatic stem cell system in the Animal Kingdom. I finally discuss some "black boxes" regarding neoblasts which still baffle us, namely their phylogenetic and ontogenetic origins, their role in body size control, how their pool is regulated during growth and degrowth, the logic of their proliferative control, and some 'old' long-sought missing tools. KEY WORDS: planarian, neoblast, totipotency, dedifferentiation, stem cell A general overview of cell potency during developmentThe developmental potential of cells within embryos, and by extension in adult organisms has been one of the biggest riddles in Developmental Biology. A large amount of observations and experiments soon made clear that egg cells and early blastomeres in most phyla are totipotent cells (cells able to give rise to all cell types including germ cells). It also became evident that as development goes on, such potentialities, however ample, become restricted. After the morula stage in mammals, cells of the inner cell mass and from the outer trophoblasts are no longer totipotent but pluripotent (able to give rise to cell types of all three germ layers or to the placenta, respectively). Later, embryonic germ layers segregate. Embryonic outer cells (ectoderm), give rise to several epidermal derivatives together with central nervous system and neural crest cell types but not to any embryonic inner cells, or endoderm derivatives, and vice versa. Such cells are considered multipotent (able to give rise to several cell types). The final stage, the adult Int. J. Dev. Biol. 56: [19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37] doi: 10.1387/ijdb.113463jb organism, is formed of thousands, millions, billions, or trillions of cells of different types (over 200-300 in complex vertebrates) patter...

show abstract

Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration

Cited by 189 publications

References 62 publications

Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

An automated training paradigm reveals long-term memory in planaria and its persistence through head regeneration

The planarian neoblast: the rambling history of its origin and some current black boxes

Contact Info

Product

Resources

About