Organization and Regeneration Ability of Spontaneous Supernumerary Eyes in Planarians —Eye Regeneration Field and Pathway Selection by Optic Nerves—

Sakai, Fumie; Agata, Kiyokazu; Orii, Hidefumi; Watanabe, Kenji

doi:10.2108/jsz.17.375

Cited by 50 publications

(51 citation statements)

References 16 publications

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“…6B). Supernumerary eyes can rarely appear spontaneously during errors in asexual planarian reproduction, and consistent with the above data, these supernumerary eyes do not regenerate following removal (32). …”

Section: A Broad Targetable Zone Enables Maintenance Of Anatomy In Insupporting

confidence: 75%

Self-organization and progenitor targeting generate stable patterns in planarian regeneration

Atabay

LoCascio

Hoog

et al. 2018

Science

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During animal regeneration cells must organize into discrete and functional systems. We show that self-organization, along with patterning cues, govern progenitor behavior in planarian regeneration. Surgical paradigms allowed manipulation of planarian eye regeneration in predictable locations and numbers, generating alternative stable neuroanatomical states for wild-type animals with multiple functional ectopic eyes. We utilized animals with multiple ectopic eyes and eye transplantation to demonstrate that broad progenitor specification, combined with self-organization, allows anatomy maintenance during regeneration. We propose a model for regenerative progenitors involving (i) migratory targeting cues, (ii) self-organization into existing or regenerating eyes, and (iii) a broad zone, associated with coarse progenitor specification, in which eyes can be targeted by progenitors. These three properties help explain how tissues can be organized during regeneration.

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Section: A Broad Targetable Zone Enables Maintenance Of Anatomy In Insupporting

confidence: 75%

Self-organization and progenitor targeting generate stable patterns in planarian regeneration

Atabay

LoCascio

Hoog

et al. 2018

Science

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“…Similarly, head fragments failed to regenerate medial and posterior structures, including pharynx and tail (Figure 1A). Analysis of the pattern of several differentiated structures, such as brain branches ( gpas +) [26], anterior chemoreceptors ( cintillo +) [27] and the visual system ( ovo + and VC1+) [28], [29], revealed aberrant regeneration in the anterior blastema of JNK(RNAi) planarians (Figure 1B). We next investigated whether this inability to regenerate was associated with a prior defect in polarity determination.…”

Section: Resultsmentioning

confidence: 99%

“…The decrease in neoblast progeny observed in JNK(RNAi) animals was less pronounced than that seen in starved control animals (Figure 6D-S9F). Quantification of the number of visual system cells (VC1+, opsin +) [29], [43], specific neuronal cell types (GABAergic, gad + [44]; octopaminergic, tbh + [45] and serotoninergic, tph + [46]) and epithelial cells, revealed an increase in the density of all differentiated cell types tested in degrowing JNK(RNAi) animals (Figure 6E-6F-6G-S9G). Moreover, analysis of the population of cintillo + cells during starvation revealed a decreasing number of this anterior-specific cell type in degrowing control animals but not in degrowing JNK(RNAi) animals (Figure 6H-S9H).…”

Section: Resultsmentioning

confidence: 99%

JNK Controls the Onset of Mitosis in Planarian Stem Cells and Triggers Apoptotic Cell Death Required for Regeneration and Remodeling

et al. 2014

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Regeneration of lost tissues depends on the precise interpretation of molecular signals that control and coordinate the onset of proliferation, cellular differentiation and cell death. However, the nature of those molecular signals and the mechanisms that integrate the cellular responses remain largely unknown. The planarian flatworm is a unique model in which regeneration and tissue renewal can be comprehensively studied in vivo. The presence of a population of adult pluripotent stem cells combined with the ability to decode signaling after wounding enable planarians to regenerate a complete, correctly proportioned animal within a few days after any kind of amputation, and to adapt their size to nutritional changes without compromising functionality. Here, we demonstrate that the stress-activated c-jun–NH2–kinase (JNK) links wound-induced apoptosis to the stem cell response during planarian regeneration. We show that JNK modulates the expression of wound-related genes, triggers apoptosis and attenuates the onset of mitosis in stem cells specifically after tissue loss. Furthermore, in pre-existing body regions, JNK activity is required to establish a positive balance between cell death and stem cell proliferation to enable tissue renewal, remodeling and the maintenance of proportionality. During homeostatic degrowth, JNK RNAi blocks apoptosis, resulting in impaired organ remodeling and rescaling. Our findings indicate that JNK-dependent apoptotic cell death is crucial to coordinate tissue renewal and remodeling required to regenerate and to maintain a correctly proportioned animal. Hence, JNK might act as a hub, translating wound signals into apoptotic cell death, controlled stem cell proliferation and differentiation, all of which are required to coordinate regeneration and tissue renewal.

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“…Furthermore, the early and late progeny compartments had also higher proportional volumes than controls (Figure 2D; P<0.01), with the highest volume being at the most anterior region of the animal in front of the eyes (P<0.001) (Figure 2E5, E6, E11, E12, Figure S6). By using a panel of markers of differentiated cells [22], [24]–[28] we observed anterior blastemas with differentiation defects, especially the region that should contain the dorsal-most part of the brain ganglia and the eyes (Figure 2A, 2E13–E18, 2F and Figure S8A). This correlated with the accumulation of neoblasts and progeny in the same areas.…”

Section: Resultsmentioning

confidence: 99%

SMG-1 and mTORC1 Act Antagonistically to Regulate Response to Injury and Growth in Planarians

Gonzalez-Estevez

Felix²,

Smith³

et al. 2012

PLoS Genet

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Planarian flatworms are able to both regenerate their whole bodies and continuously adapt their size to nutrient status. Tight control of stem cell proliferation and differentiation during these processes is the key feature of planarian biology. Here we show that the planarian homolog of the phosphoinositide 3-kinase-related kinase (PIKK) family member SMG-1 and mTOR complex 1 components are required for this tight control. Loss of smg-1 results in a hyper-responsiveness to injury and growth and the formation of regenerative blastemas that remain undifferentiated and that lead to lethal ectopic outgrowths. Invasive stem cell hyper-proliferation, hyperplasia, hypertrophy, and differentiation defects are hallmarks of this uncontrolled growth. These data imply a previously unappreciated and novel physiological function for this PIKK family member. In contrast we found that planarian members of the mTOR complex 1, tor and raptor, are required for the initial response to injury and blastema formation. Double smg-1 RNAi experiments with tor or raptor show that abnormal growth requires mTOR signalling. We also found that the macrolide rapamycin, a natural compound inhibitor of mTORC1, is able to increase the survival rate of smg-1 RNAi animals by decreasing cell proliferation. Our findings support a model where Smg-1 acts as a novel regulator of both the response to injury and growth control mechanisms. Our data suggest the possibility that this may be by suppressing mTOR signalling. Characterisation of both the planarian mTORC1 signalling components and another PIKK family member as key regulators of regeneration and growth will influence future work on regeneration, growth control, and the development of anti-cancer therapies that target mTOR signalling.

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Organization and Regeneration Ability of Spontaneous Supernumerary Eyes in Planarians —Eye Regeneration Field and Pathway Selection by Optic Nerves—

Cited by 50 publications

References 16 publications

Self-organization and progenitor targeting generate stable patterns in planarian regeneration

Self-organization and progenitor targeting generate stable patterns in planarian regeneration

JNK Controls the Onset of Mitosis in Planarian Stem Cells and Triggers Apoptotic Cell Death Required for Regeneration and Remodeling

SMG-1 and mTORC1 Act Antagonistically to Regulate Response to Injury and Growth in Planarians

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