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  • 1
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    Regeneration in the era of functional genomics and gene network analysis (2011)
    Marine Biological Laboratory
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    Publication Date: 2022-05-25
    Description: Author Posting. © Marine Biological Laboratory, 2011. This article is posted here by permission of Marine Biological Laboratory for personal use, not for redistribution. The definitive version was published in Biological Bulletin 221 (2011): 18-34.
    Description: What gives an organism the ability to regrow tissues and to recover function where another organism fails is the central problem of regenerative biology. The challenge is to describe the mechanisms of regeneration at the molecular level, delivering detailed insights into the many components that are cross-regulated. In other words, a broad, yet deep dissection of the system-wide network of molecular interactions is needed. Functional genomics has been used to elucidate gene regulatory networks (GRNs) in developing tissues, which, like regeneration, are complex systems. Therefore, we reason that the GRN approach, aided by next generation technologies, can also be applied to study the molecular mechanisms underlying the complex functions of regeneration. We ask what characteristics a model system must have to support a GRN analysis. Our discussion focuses on regeneration in the central nervous system, where loss of function has particularly devastating consequences for an organism. We examine a cohort of cells conserved across all vertebrates, the reticulospinal (RS) neurons, which lend themselves well to experimental manipulations. In the lamprey, a jawless vertebrate, there are giant RS neurons whose large size and ability to regenerate make them particularly suited for a GRN analysis. Adding to their value, a distinct subset of lamprey RS neurons reproducibly fail to regenerate, presenting an opportunity for side-by-side comparison of gene networks that promote or inhibit regeneration. Thus, determining the GRN for regeneration in RS neurons will provide a mechanistic understanding of the fundamental cues that lead to success or failure to regenerate.
    Description: The authors gratefully acknowledge support from The Marine Biological Laboratory, The Charles Evans Foundation (OB, JDB, JRM), AG005138 (JDB), and G. Harold and Leila Y. Mathers Research Professorship of Geriatrics and Adult Development (JDB); University of Texas, Austin start-up funds (JM), the Paralyzed Veterans of America Research Grant #2586 (JM) and the Morton Cure Paralysis Fund (JM); The Feinstein Institute for Medical Research (OB); The Essel Foundation (SJZ) and The Howard Hughes Medical Institute (Williams College).
    Repository Name: Woods Hole Open Access Server
    Type: Article
    Format: application/pdf
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  • 2
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    Activating transcription factor 3 (ATF3) is a highly conserved pro-regenerative transcription factor in the vertebrate nervous system (2022)
    Frontiers Media
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    Publication Date: 2022-10-27
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Katz, H. R., Arcese, A. A., Bloom, O., & Morgan, J. R. Activating transcription factor 3 (ATF3) is a highly conserved pro-regenerative transcription factor in the vertebrate nervous system. Frontiers in Cell and Developmental Biology, 10, (2022): 824036, https://doi.org/10.3389/fcell.2022.824036.
    Description: The vertebrate nervous system exhibits dramatic variability in regenerative capacity across species and neuronal populations. For example, while the mammalian central nervous system (CNS) is limited in its regenerative capacity, the CNS of many other vertebrates readily regenerates after injury, as does the peripheral nervous system (PNS) of mammals. Comparing molecular responses across species and tissues can therefore provide valuable insights into both conserved and distinct mechanisms of successful regeneration. One gene that is emerging as a conserved pro-regenerative factor across vertebrates is activating transcription factor 3 (ATF3), which has long been associated with tissue trauma. A growing number of studies indicate that ATF3 may actively promote neuronal axon regrowth and regeneration in species ranging from lampreys to mammals. Here, we review data on the structural and functional conservation of ATF3 protein across species. Comparing RNA expression data across species that exhibit different abilities to regenerate their nervous system following traumatic nerve injury reveals that ATF3 is consistently induced in neurons within the first few days after injury. Genetic deletion or knockdown of ATF3 expression has been shown in mouse and zebrafish, respectively, to reduce axon regeneration, while inducing ATF3 promotes axon sprouting, regrowth, or regeneration. Thus, we propose that ATF3 may be an evolutionarily conserved regulator of neuronal regeneration. Identifying downstream effectors of ATF3 will be a critical next step in understanding the molecular basis of vertebrate CNS regeneration.
    Description: This work was supported by: a Morton Cure Paralysis Fund Research Grant (to HK); a NIH/NINDS R03 Research Grant (No. 1R03NS078519) and the New York State Spinal Cord Injury Research Board (to OB); and the Marine Biological Laboratory Eugene Bell Center Endowment, Rowe Endowment for Regenerative Biology, and Charles Evans Research Development award (to JM).
    Keywords: Regeneration ; Spinal cord injury ; Zebrafish ; Lamprey ; Dorsal root ganglia (DRG) neurons
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 3
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    Highly conserved molecular pathways, including Wnt signaling, promote functional recovery from spinal cord injury in lampreys (2018)
    Nature Publishing Group
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Scientific Reports 8 (2018): 742, doi:10.1038/s41598-017-18757-1.
    Description: In mammals, spinal cord injury (SCI) leads to dramatic losses in neurons and synaptic connections, and consequently function. Unlike mammals, lampreys are vertebrates that undergo spontaneous regeneration and achieve functional recovery after SCI. Therefore our goal was to determine the complete transcriptional responses that occur after SCI in lampreys and to identify deeply conserved pathways that promote regeneration. We performed RNA-Seq on lamprey spinal cord and brain throughout the course of functional recovery. We describe complex transcriptional responses in the injured spinal cord, and somewhat surprisingly, also in the brain. Transcriptional responses to SCI in lampreys included transcription factor networks that promote peripheral nerve regeneration in mammals such as Atf3 and Jun. Furthermore, a number of highly conserved axon guidance, extracellular matrix, and proliferation genes were also differentially expressed after SCI in lampreys. Strikingly, ~3% of differentially expressed transcripts belonged to the Wnt pathways. These included members of the Wnt and Frizzled gene families, and genes involved in downstream signaling. Pharmacological inhibition of Wnt signaling inhibited functional recovery, confirming a critical role for this pathway. These data indicate that molecular signals present in mammals are also involved in regeneration in lampreys, supporting translational relevance of the model.
    Description: We gratefully acknowledge support from the National Institutes of Health (R03NS078519 to OB; R01GM104123 to JJS; R01NS078165 to JRM), The Feinstein Institute for Medical Research and The Marine Biological Laboratory, including the Charles Evans Foundation Research Award, the Albert and Ellen Grass Foundation Faculty Research Award, and The Eugene and Millicent Bell Fellowship Fund in Tissue Engineering.
    Keywords: Computational biology and bioinformatics ; Gene expression ; Spinal cord injury
    Repository Name: Woods Hole Open Access Server
    Type: Article
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