BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration

Reddien, Peter W.; Bermange, Adam L.; Kicza, Adrienne M.; Alvarado, Alejandro Sánchez

doi:10.1242/dev.007138

Cited by 164 publications

(200 citation statements)

References 36 publications

(59 reference statements)

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“…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%

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

Baguñà¹

2012

Int. J. Dev. Biol.

134

111

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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...

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

confidence: 99%

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

Baguñà¹

2012

Int. J. Dev. Biol.

134

111

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“…Whole-mount in situ hybridization was performed essentially as previously described (Reddien et al, 2007;Palakodeti et al, 2008). Hybridization was performed at 50°C for 36 h with DIG-conjugated riboprobes in hybridization solution.…”

Section: Whole-mount In Situ Hybridizationmentioning

confidence: 99%

Molecular cloning and expression pattern of the DjStag gene in the planarian Dugesia japonica during embryonic development

2014

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ABSTRACT. We examined STAG-related gene (DjStag) expression in the planarian Dugesia japonica. This species is common in Far Eastern countries. The DjStag cDNA includes 1362 bp and contains a 489-bp open reading frame corresponding to a deduced protein of 162 amino acids, with a 170-bp 5'-UTR and a 703-bp 3'-UTR. Phylogenetic analysis showed that DjStag is an STAG/STAG-like member. We examined the expression pattern of DjStag in this planarian during embryonic development by whole-mount in situ hybridization. DjStag was detected in embryonic cells in the germ band at early embryo stages. The number of DjStag-positive embryonic cells increased in stage 5. Later, it was mainly expressed in lateral region parenchyma. In juveniles, extensive expression of DjStag was observed not only in the head and tail regions, but also in the parenchyma between the epidermis and the gastrodermis. We conclude that DjStag is expressed in the cellular subset that will become the neoblast cells of the adult flatworm. DjStag may play an essential role in spatial and temporal regulation during planarian embryonic development.

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“…BMP/Dpp Against the Source: Lessons From Planarians, Spiders, Crustaceans, and Beetles Recent analysis of BMPs and its modulators in planarians (Lophotrochozoan), echinoderms (basal deuterostome), spiders, crustaceans, and beetles (arthropods) have broadened our understanding of the role of this pathway during embryogenesis (Akiyama-Oda and Oda, 2006;Duboc et al, 2004;Fritsch et al, 2010;Gavino and Reddien, 2011;Lapraz et al, 2009;Molina et al, 2011;Nunes da Fonseca et al, 2010;Park et al, 2010;Reddien et al, 2007;Saina et al, 2009;van der Zee et al, 2006). In all these studies not only dpp expression was analyzed, but also the activity of Dpp signaling using antibodies against pMad was visualized.…”

Section: Presence or Absence: Different Genomes Have Different Bmp Momentioning

confidence: 99%

“…Interestingly, Dpp activity is detected far from its site of mRNA expression in all animals investigated so far. At least in spiders, beetles and echinoderms (Akiyama-Oda and Oda, 2006;Fritsch et al, 2010;Lapraz et al, 2009;Molina et al, 2007;Nunes da Fonseca et al, 2010;Reddien et al, 2007;van der Zee et al, 2006) the transport of Dpp is dependent on Sog/Chd orthologs, similar to what has been described in flies (Decotto and Ferguson, 2001;Eldar et al, 2002;Shimmi and O'Connor, 2003;Wang and Ferguson, 2005) and Xenopus (Ben-Zvi et al, 2008). It is possible that additional kernel elements (tsg and tld) are also involved in Dpp transport in other animals as we have shown in the beetle Tribolium castaneum (Nunes da Fonseca et al, 2010).…”

Section: Presence or Absence: Different Genomes Have Different Bmp Momentioning

confidence: 99%

Position matters: Variability in the spatial pattern of BMP modulators generates functional diversity

Araujo

Fontenele

Fonseca

2011

Genesis

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Summary: Bone morphogenetic proteins (BMPs) perform a variety of functions during development. Considering a single BMP, what enables its multiple roles in tissues of varied sizes and shapes? What regulates the spatial distribution and activity patterns of the BMP in these different developmental contexts? Some BMP functions require controlling spread of the BMP morphogen, while others require formation of localized, high concentration peaks of BMP activity. Here we review work in Drosophila that describes spatial regulation of the BMP encoded by decapentaplegic (dpp) in different developmental contexts. We concentrate on extracellular modulation of BMP function and discuss the mechanisms that generate concentrated peaks of Dpp activity, subdivide territories of different activity levels or regulate spread of the Dpp morphogen from a point source. We compare these findings with data from vertebrates and non-model organisms to discuss how changes in the regulation of Dpp distribution by extracellular modulators may lead to variability in dpp function in different species. genesis 49:698-718, 2011. V V C 2011 Wiley-Liss, Inc.

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BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration

Cited by 164 publications

References 36 publications

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

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

Molecular cloning and expression pattern of the DjStag gene in the planarian Dugesia japonica during embryonic development

Position matters: Variability in the spatial pattern of BMP modulators generates functional diversity

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