Hedgehog signaling regulates gene expression in planarian glia

There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

Abstract

Hedgehog signaling is critical for vertebrate central nervous system (CNS) development, but its role in CNS biology in other organisms is poorly characterized. In the planarian Schmidtea mediterranea, hedgehog (hh) is expressed in medial cephalic ganglia neurons, suggesting a possible role in CNS maintenance or regeneration. We performed RNA sequencing of planarian brain tissue following RNAi of hh and patched (ptc), which encodes the Hh receptor. Two misregulated genes, intermediate filament-1 (if-1) and calamari (cali), were expressed in a previously unidentified non-neural CNS cell type. These cells expressed orthologs of astrocyte-associated genes involved in neurotransmitter uptake and metabolism, and extended processes enveloping regions of high synapse concentration. We propose that these cells are planarian glia. Planarian glia were distributed broadly, but only expressed if-1 and cali in the neuropil near hh ⁺ neurons. Planarian glia and their regulation by Hedgehog signaling present a novel tractable system for dissection of glia biology.

DOI: http://dx.doi.org/10.7554/eLife.16996.001

Related collections

Most cited references 91

Record: found
Abstract: found
Article: not found

Astrocyte glutamate transport: review of properties, regulation, and physiological functions.

C Anderson, R A Swanson (2000)

Rapid removal of glutamate from the extracellular space is required for the survival and normal function of neurons. Although glutamate transporters are expressed by all CNS cell types, astrocytes are the cell type primarily responsible for glutamate uptake. Astrocyte glutamate uptake also plays a role in regulating the activity of glutamatergic synapses. Lastly, release of glutamate from astrocytes, via transporter reversal and other routes, can contribute to glutamate receptor activation. This review examines the mechanisms of astrocyte glutamate uptake and release, with particular focus on high-affinity Na(+)-dependent transporters. Transporter regulation, energetics, and physiological roles are discussed.

0 comments Cited 255 times – based on 0 reviews      Review now

Record: found
Abstract: found
Article: not found

Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration.

Daniel E Wagner, Irving Wang, Peter W. Reddien (2011)

Pluripotent cells in the embryo can generate all cell types, but lineage-restricted cells are generally thought to replenish adult tissues. Planarians are flatworms and regenerate from tiny body fragments, a process requiring a population of proliferating cells (neoblasts). Whether regeneration is accomplished by pluripotent cells or by the collective activity of multiple lineage-restricted cell types is unknown. We used ionizing radiation and single-cell transplantation to identify neoblasts that can form large descendant-cell colonies in vivo. These clonogenic neoblasts (cNeoblasts) produce cells that differentiate into neuronal, intestinal, and other known postmitotic cell types and are distributed throughout the body. Single transplanted cNeoblasts restored regeneration in lethally irradiated hosts. We conclude that broadly distributed, adult pluripotent stem cells underlie the remarkable regenerative abilities of planarians.

0 comments Cited 229 times – based on 0 reviews      Review now

Record: found
Abstract: found
Article: not found

Fundamentals of planarian regeneration.

Peter W. Reddien, Alejandro Sánchez Alvarado (2004)

The principles underlying regeneration in planarians have been explored for over 100 years through surgical manipulations and cellular observations. Planarian regeneration involves the generation of new tissue at the wound site via cell proliferation (blastema formation), and the remodeling of pre-existing tissues to restore symmetry and proportion (morphallaxis). Because blastemas do not replace all tissues following most types of injuries, both blastema formation and morphallaxis are needed for complete regeneration. Here we discuss a proliferative cell population, the neoblasts, that is central to the regenerative capacities of planarians. Neoblasts may be a totipotent stem-cell population capable of generating essentially every cell type in the adult animal, including themselves. The population properties of the neoblasts and their descendants still await careful elucidation. We identify the types of structures produced by blastemas on a variety of wound surfaces, the principles guiding the reorganization of pre-existing tissues, and the manner in which scale and cell number proportions between body regions are restored during regeneration.

0 comments Cited 220 times – based on 0 reviews      Review now

All references

Author and article information

Contributors

Alejandro Sánchez Alvarado: Role: Reviewing editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (hwp): eLife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 09 September 2016

Publication date Collection: 2016

Volume: 5

Electronic Location Identifier: e16996

Affiliations

[1 ]deptDepartment of Biology , Massachusetts Institute of Technology , Cambridge, United States

[2 ]deptHoward Hughes Medical Institute , Massachusetts Institute of Technology , Cambridge, United States

[3 ]deptWhitehead Institute , Massachusetts Institute of Technology , Cambridge, United States

[4 ]deptDepartment of Neurobiology , Stanford University , Stanford, United States

[5]Stowers Institute for Medical Research , United States

[6]Stowers Institute for Medical Research , United States

Author notes

reddien@ 123456wi.mit.edu

[†]

These authors contributed equally to this work.

Author information

Thomas R Clandinin http://orcid.org/0000-0001-6277-6849

Peter W Reddien http://orcid.org/0000-0002-5569-333X

Article

Publisher ID: 16996

DOI: 10.7554/eLife.16996

PMC ID: 5055395

PubMed ID: 27612382

SO-VID: 742274c5-2ebe-4c40-a84d-6221984ddd1b

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 16 April 2016

Date accepted : 02 September 2016

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;

Award Recipient : Peter W Reddien

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: R01GM080639

Award Recipient : Peter W Reddien

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Custom metadata

elife-xml-version 2.5

Author impact statement Hedgehog signaling plays a role in regulating glia gene expression in planarians, pointing to a candidate ancestral and broadly used role for the Hedgehog pathway.

ScienceOpen disciplines: Life sciences

Keywords: planaria,glia,astrocytes,hedgehog signaling,regeneration,schmidtea mediterranea,other

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: planaria, glia, astrocytes, hedgehog signaling, regeneration, schmidtea mediterranea, other

Hedgehog signaling regulates gene expression in planarian glia

Read this article at

Abstract

Related collections

Resource Identification