Damage-induced reactive oxygen species enable zebrafish tail regeneration by repositioning of Hedgehog expressing cells

Roehl, Henry; Romero, Montserrat Garcia; McCathie, Gareth; Jankun, Philip

doi:10.1101/380378

Cited by 13 publications

(25 citation statements)

References 51 publications

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“…A reduction in H 2 O 2 levels impairs axonal projections by retinal ganglion cells, and this phenotype can be rescued by activation of the Hedgehog pathway [ 120 ]. Also during adult regeneration, axonal growth is controlled by the interplay between H 2 O 2 and Hedgehog [ 121 , 122 ]. Experimental evidence in different animal models shows that a rapid concentration gradient of H 2 O 2 is generated upon injury [ 112 , 123 ], and that H 2 O 2 is a powerful chemoattractant for leukocytes [ 112 , 124 , 125 ].…”

Section: The Injury Response In the Pns: Intrinsic And Extrinsic Cmentioning

confidence: 99%

Signals Orchestrating Peripheral Nerve Repair

Rigoni

Negro

2020

Cells

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The peripheral nervous system has retained through evolution the capacity to repair and regenerate after assault from a variety of physical, chemical, or biological pathogens. Regeneration relies on the intrinsic abilities of peripheral neurons and on a permissive environment, and it is driven by an intense interplay among neurons, the glia, muscles, the basal lamina, and the immune system. Indeed, extrinsic signals from the milieu of the injury site superimpose on genetic and epigenetic mechanisms to modulate cell intrinsic programs. Here, we will review the main intrinsic and extrinsic mechanisms allowing severed peripheral axons to re-grow, and discuss some alarm mediators and pro-regenerative molecules and pathways involved in the process, highlighting the role of Schwann cells as central hubs coordinating multiple signals. A particular focus will be provided on regeneration at the neuromuscular junction, an ideal model system whose manipulation can contribute to the identification of crucial mediators of nerve re-growth. A brief overview on regeneration at sensory terminals is also included.

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Section: The Injury Response In the Pns: Intrinsic And Extrinsic Cmentioning

confidence: 99%

Signals Orchestrating Peripheral Nerve Repair

Rigoni

Negro

2020

Cells

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“…Given the importance of MAPK signaling in regeneration, we next set out to determine how MAPKs are activated in response to injury. We considered reactive oxygen species (ROS) because recent work in zebrafish and Drosophila showed the importance of ROS for regeneration, probably by either activating or modulating different signaling pathways such as JNK or Hedgehog signaling (Gauron et al, 2013;Romero et al, 2018). To test whether ROS is produced at the site of injury, animals were incubated with CellRox, a ROS sensitive dye, prior to amputation (Fig.…”

Section: Mapk Activation Depends On Ros Signalingmentioning

confidence: 99%

“…Injured epithelia show increased activation of inflammatory signals, RTK and Wnt signaling to initiate healing by stem cell activation, proliferation, and ECM remodeling, so do cancer initiating cells to promote tumorigenesis (Arwert et al, 2012;Sundaram et al, 2017). Thus, our work on the elucidation how the injury response culminates into Wnt driven patterning may contribute to both the field of regenerative biology and cancer research (Gorlach et al, 2015;Romero et al, 2018).…”

Section: Atf/creb Mediated Transcriptional Activation Of Wntsmentioning

confidence: 99%

MAPK signaling links the injury response to Wnt-regulated patterning inHydraregeneration

Tursch

Bartsch

2020

Preprint

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AbstractHydra has a long history as an informative model to study pattern formation and regeneration. Wnt signaling is a critical component of Hydra patterning that must be activated during regeneration, but it is largely unknown how the injury stimulus ultimately leads to this activation. In a proteomic screen we previously identified mitogen protein kinases (MAPKs) among the earliest injury response factors in Hydra regeneration, making them attractive candidates to transmit injury-response signals to the initial steps of patterning, which in Hydra includes Wnt signaling. Our data demonstrate that three MAPKs, p38, c-Jun N-terminal kinases (JNKs), and extracellular signal-regulated kinases (ERK), are essential to initiate regeneration in Hydra. This activation occurs in response to an injury signal, which consists of calcium and reactive oxygen species (ROS) signaling. Phosphorylated MAPKs exhibit cross-talk with a mutual antagonism between the ERK1/2 pathway and the stress induced MAPKs. The activation of these MAPK pathways, as well as the induction of apoptosis, occurs in all injuries regardless of the position of the wound. MAPK phosphorylation is required for the transcriptional activation of position independent Wnt3 and Wnt9/10c ligands. In summary, our data show that the activation of MAPKs is an essential component of the wound response which transmits the injury signal to induce the transcriptional activation of Wnt ligands, which are essential for patterning the regenerating tissue. Given the high level of evolutionary conservation of MAPKs and Wnts in the injury response, this likely represents a deeply conserved pathway in animals.

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“…3 J ). Previous reports suggest this region of cells act as a required wound-signaling center that orchestrates regeneration ( Rojas-Muñoz et al, 2009 ; Romero et al, 2018 ). Importantly, this population of cells with citrullinated histones was associated with the blastema reporter, Tg(lepb:EGFP) ( Fig.…”

Section: Resultsmentioning

confidence: 93%

Citrullination regulates wound responses and tissue regeneration in zebrafish

Golenberg

Squirrell

Bennin

et al. 2020

Journal of Cell Biology

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Calcium is an important early signal in wound healing, yet how these early signals promote regeneration remains unclear. Peptidylarginine deiminases (PADs), a family of calcium-dependent enzymes, catalyze citrullination, a post-translational modification that alters protein function and has been implicated in autoimmune diseases. We generated a mutation in the single zebrafish ancestral pad gene, padi2, that results in a loss of detectable calcium-dependent citrullination. The mutants exhibit impaired resolution of inflammation and regeneration after caudal fin transection. We identified a new subpopulation of cells displaying citrullinated histones within the notochord bead following tissue injury. Citrullination of histones in this region was absent, and wound-induced proliferation was perturbed in Padi2-deficient larvae. Taken together, our results show that Padi2 is required for the citrullination of histones within a group of cells in the notochord bead and for promoting wound-induced proliferation required for efficient regeneration. These findings identify Padi2 as a potential intermediary between early calcium signaling and subsequent tissue regeneration.

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Damage-induced reactive oxygen species enable zebrafish tail regeneration by repositioning of Hedgehog expressing cells

Cited by 13 publications

References 51 publications

Signals Orchestrating Peripheral Nerve Repair

Signals Orchestrating Peripheral Nerve Repair

MAPK signaling links the injury response to Wnt-regulated patterning inHydraregeneration

Citrullination regulates wound responses and tissue regeneration in zebrafish

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