Stem cell dynamics during growth, feeding, and starvation in the basal flatworm <i>Macrostomum</i> sp. (Platyhelminthes)

Nimeth, K.; Mahlknecht, Monika; Mezzanato, Andrea; Peter, Roland; Rieger, Reinhard M.; Ladurner, Peter

doi:10.1002/dvdy.20035

Cited by 48 publications

(69 citation statements)

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“…(Nimeth et al 2004). Worms that were fed after 30 days of starvation showed a 24-fold increase in the number of S-phase cells after just 2 h of feeding.…”

Section: Discussionmentioning

confidence: 97%

Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp.

Schärer

Ladurner

Rieger

2004

Behav Ecol Sociobiol

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“…(Nimeth et al 2004). Worms that were fed after 30 days of starvation showed a 24-fold increase in the number of S-phase cells after just 2 h of feeding.…”

Section: Discussionmentioning

confidence: 97%

Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp.

Schärer

Ladurner

Rieger

2004

Behav Ecol Sociobiol

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“…1 D and E), in contrast to most vertebrate somatic stem cells, are plentiful, making up about ∼6.5% of all cells (15), and have a very high proliferation rate (16,17). Of M. lignano neoblasts, 89% enter S-phase every 24 h (18).…”

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confidence: 99%

Genome and transcriptome of the regeneration-competent flatworm, Macrostomum lignano

Wasik

Gurtowski

Zhou

et al. 2015

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

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The free-living flatworm, Macrostomum lignano has an impressive regenerative capacity. Following injury, it can regenerate almost an entirely new organism because of the presence of an abundant somatic stem cell population, the neoblasts. This set of unique properties makes many flatworms attractive organisms for studying the evolution of pathways involved in tissue self-renewal, cellfate specification, and regeneration. The use of these organisms as models, however, is hampered by the lack of a well-assembled and annotated genome sequences, fundamental to modern genetic and molecular studies. Here we report the genomic sequence of M. lignano and an accompanying characterization of its transcriptome. The genome structure of M. lignano is remarkably complex, with ∼75% of its sequence being comprised of simple repeats and transposon sequences. This has made high-quality assembly from Illumina reads alone impossible (N50 = 222 bp). We therefore generated 130× coverage by long sequencing reads from the Pacific Biosciences platform to create a substantially improved assembly with an N50 of 64 Kbp. We complemented the reference genome with an assembled and annotated transcriptome, and used both of these datasets in combination to probe gene-expression patterns during regeneration, examining pathways important to stem cell function.F latworms belong to the superphylum Lophotrochozoa, a vast assembly of protostome invertebrates (1, 2) (Fig. 1A). The evolutionary relationships within this clade are poorly resolved and the specific position of flatworms is currently debated (3, 4). Flatworms have attracted scientific attention for centuries because of their astonishing regenerative capabilities (5, 6), as well as their ability to "degrow" in a controlled way when starved (7). As far back as the early 1900s, Thomas Morgan recognized the potential of flatworms and conducted a number of fascinating regeneration experiments on planarian flatworms before his focus shifted to Drosophila genetics (8).Macrostomum lignano is (Fig. 1B), a free-living, regenerating flatworm isolated from the coast of the Mediterranean Sea. M. lignano is an obligatorily cross-fertilizing simultaneous hermaphrodite (9) that belongs to Macrostomorpha, whereas the other often-studied freeliving flatworms and human parasitic flatworms all belong to clades that are potentially more derived (less ancestral) in comparison with Macrostomorpha (2) (Fig. 1C).Many flatworms can regenerate nearly their entire body or amputated organs. This regenerative capacity is thought to be attributable to the presence of somatic stem cells, termed neoblasts (10, 11). In Schmidtea mediterranea (planarian flatworm), even a single transplanted neoblast has the ability to rescue, regenerate, and change the genotype of a fatally irradiated worm (12). M. lignano can regenerate every tissue, with the exception of the head region containing the brain (13,14).Neoblasts in M. lignano ( Fig. 1 D and E), in contrast to most vertebrate somatic stem cells, are plentiful, making up about ...

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“…5.2B) and mitotic neoblasts (Fig. 5.2C) identified by immunohistochemistry (Nimeth et al, 2004(Nimeth et al, , 2007Egger et al, 2006;Bode et al, 2006;Peter et al, 2001;Ladurner et al, 2000), ultrastructure (Bode et al, 2006;Rieger et al, 1999), by interference contrast (Fig. 5.2D), by histological staining (Fig.…”

Section: Distribution and Number Of Neoblastsmentioning

confidence: 98%

“…Under the epidermal layer and a thin extracellular matrix a complex muscle system consisting of circular, diagonal, and longitudinal muscle cells is present (Ladurner et al, 2005a;Salvenmoser et al, 2001). The bilaterally symmetrical nervous system consists of a brain with a neuropile surrounded by perikarya, two main lateral nerve cords connected by a postpharyngeal commissure and a caudal loop, and two additional dorsal and ventral nerve cords Bode et al, 2006;Nimeth et al, 2004). Peripherally, a nerve-net like plexus covers the animals and contains sensory nerve cells.…”

Section: Morphologymentioning

confidence: 99%

“…In recent years 5'-bromo-2'-deoxyuridine (BrdU) labeling has been adapted to label and trace the S-phase subpopulation of neoblasts in M. lignano using whole mount immunocytochemistry, histological sections, and immunogold staining (Nimeth et al, 2002(Nimeth et al, , 2004(Nimeth et al, , 2007Egger et al, 2006;Bode et al, 2006;Peter et al, 2001;Ladurner et al, 2000). Moreover, the mitotic subset of neoblasts can be visualized by applying a polyclonal antibody against phosphorylated Histone H3 (Nimeth et al, 2004(Nimeth et al, , 2007Bode et al, 2006;Ladurner et al, 2000). A number of conserved genes known to play a role in stem cell maintenance or proliferation have been isolated from M. lignano (Pfister et al, 2007) and can be used to identify neoblasts (see below).…”

Section: Identification Of Neoblastsmentioning

confidence: 99%

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The Stem Cell System of the Basal Flatworm Macrostomum lignano

et al. 2008

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The scope of this review is to introduce the free-living flatworm Macrostomum lignano as an excellent model organism to address questions of platyhelminth stem cell biology. First, we sketch the historical origin of flatworm stem cell research. Second, we introduce M. lignano, and summarize the main advantages that we think it has over the classical planarian model. Third, we give a short summary of the simple culture techniques. Fourth, we give a detailed overview over its morphology and embryology as far as it is relevant for stem cell biology. Fifth, we summarize our main findings on stem cell biology, with respect to the identification of neoblasts, their distribution and number. We describe the ultrastructure of neoblasts, their dynamics and gene expression. Sixth, we outline ways to study sex allocation by means of stem cell labeling and manipulation. Last, we highlight the regeneration capacity of this species and link it to the stem cell system. We conclude that M. lignano is a highly suitable model organism to gain knowledge about flatworm stem cells and to provide insight into stem cell systems of higher organisms, including humans.

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Stem cell dynamics during growth, feeding, and starvation in the basal flatworm Macrostomum sp. (Platyhelminthes)

Cited by 48 publications

References 43 publications

Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp.

Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp.

Genome and transcriptome of the regeneration-competent flatworm, Macrostomum lignano

The Stem Cell System of the Basal Flatworm Macrostomum lignano

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