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      TRAF-like Proteins Regulate Cellular Survival in the Planarian Schmidtea mediterranea

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          Summary

          Tissue homeostasis relies on the timely renewal of cells that have been damaged or have surpassed their biological age. Nonetheless, the underlying molecular mechanism coordinating tissue renewal is unknown. The planarian Schmidtea mediterranea harbors a large population of stem cells that continuously divide to support the restoration of tissues throughout the body. Here, we identify that TNF Receptor Associated Factors (TRAFs) play critical roles in cellular survival during tissue repair in S. mediterranea. Disruption with RNA-interference of TRAF signaling results in rapid morphological defects and lethality within 2 weeks. The TRAF phenotype is accompanied by an increased number of mitoses and cell death. Our results also reveal TRAF signaling is required for proper regeneration of the nervous system. Taken together, we find functional conservation of TRAF-like proteins in S. mediterranea as they act as crucial regulators of cellular survival during tissue homeostasis and regeneration.

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          Highlights

          • •

            The expression of Smed-TRAF-1/2, - 2A/B is enriched in the digestive system

          • •

            Planarian TRAF-like proteins regulate the systemic cellular turnover

          • •

            Loss of Smed-TRAF-1/2, - 2A/B leads to impaired tissue regeneration

          Abstract

          Biological Sciences; Cell Biology; Developmental Biology

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          Most cited references55

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          IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors.

          Kenya Honda, Tadatsugu Taniguchi (2006)
          The interferon-regulatory factor (IRF) family of transcription factors was initially found to be involved in the induction of genes that encode type I interferons. IRFs have now been shown to have functionally diverse roles in the regulation of the immune system. Recently, the crucial involvement of IRFs in innate and adaptive immune responses has been gaining much attention, particularly with the discovery of their role in immunoregulation by Toll-like receptors and other pattern-recognition receptors.
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            AP-1 function and regulation.

            Michael Karin, Zheng-gang Liu, Ebrahim Zandi (1997)
            AP-1 (activating protein-1) is a collective term referring to dimeric transcription factors composed of Jun, Fos or ATF (activating transcription factor) subunits that bind to a common DNA site, the AP-1-binding site. As the complexity of our knowledge of AP-1 factors has increased, our understanding of their physiological function has decreased. This trend, however, is beginning to be reversed due to the recent studies of gene-knockout mice and cell lines deficient in specific AP-1 components. Such studies suggest that different AP-1 factors may regulate different target genes and thus execute distinct biological functions. Also, the involvement of AP-1 factors in functions such as cell proliferation and survival has been made somewhat clearer as a result of such studies. In addition, there has been considerable progress in understanding some of the mechanisms and signaling pathways involved in the regulation of AP-1 activity. In addition to regulation by heterodimerization between Jun, Fos and ATF proteins, AP-1 activity is regulated through interactions with specific protein kinases and a variety of transcriptional coactivators.
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              RING domain E3 ubiquitin ligases.

              Raymond J Deshaies, Claudio A. P. Joazeiro (2009)
              E3 ligases confer specificity to ubiquitination by recognizing target substrates and mediating transfer of ubiquitin from an E2 ubiquitin-conjugating enzyme to substrate. The activity of most E3s is specified by a RING domain, which binds to an E2 approximately ubiquitin thioester and activates discharge of its ubiquitin cargo. E2-E3 complexes can either monoubiquitinate a substrate lysine or synthesize polyubiquitin chains assembled via different lysine residues of ubiquitin. These modifications can have diverse effects on the substrate, ranging from proteasome-dependent proteolysis to modulation of protein function, structure, assembly, and/or localization. Not surprisingly, RING E3-mediated ubiquitination can be regulated in a number of ways. RING-based E3s are specified by over 600 human genes, surpassing the 518 protein kinase genes. Accordingly, RING E3s have been linked to the control of many cellular processes and to multiple human diseases. Despite their critical importance, our knowledge of the physiological partners, biological functions, substrates, and mechanism of action for most RING E3s remains at a rudimentary stage.
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                Author and article information

                Contributors
                Néstor J. Oviedo
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 09 October 2020
                Publication date Collection: 20 November 2020
                Publication date (Electronic): 09 October 2020
                Volume: 23
                Issue: 11
                Electronic Location Identifier: 101665
                Affiliations
                [1 ]Department of Molecular and Cell Biology, University of California, Merced, CA 95343, USA
                [2 ]Quantitative and Systems Biology Graduate Program, University of California, Merced, CA 95343, USA
                [3 ]Health Sciences Research Institute, University of California, Merced, CA 95343, USA
                Author notes
                [∗ ]Corresponding author noviedo2@ 123456ucmerced.edu
                [4]

                These authors contributed equally

                [5]

                Lead Contact

                Article
                Publisher Item ID: S2589-0042(20)30857-9 Publisher ID: 101665
                DOI: 10.1016/j.isci.2020.101665
                PMC ID: 7586133
                SO-VID: eecf0fae-ff4e-4b27-aab6-18db019483b8
                Copyright © © 2020 The Author(s)
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 16 May 2020
                Date revision received : 31 July 2020
                Date accepted : 7 October 2020
                Categories
                Subject: Article

                Keywords: biological sciences,cell biology,developmental biology
                Data availability:
                Keywords: biological sciences, cell biology, developmental biology

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