Midkine-a functions as a universal regulator of proliferation during epimorphic regeneration in adult zebrafish
Zebrafish have the ability to regenerate damaged cells and tissues by activating quiescent stem and progenitor cells or reprogramming differentiated cells into regeneration-competent precursors. Proliferation among the cells that will functionally restore injured tissues is a fundamental biological...
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| creator | Ang, Nicholas B Saera-Vila, Alfonso Walsh, Caroline Hitchcock, Peter F Kahana, Alon Thummel, Ryan Nagashima, Mikiko |
| description | Zebrafish have the ability to regenerate damaged cells and tissues by activating quiescent stem and progenitor cells or reprogramming differentiated cells into regeneration-competent precursors. Proliferation among the cells that will functionally restore injured tissues is a fundamental biological process underlying regeneration. Midkine-a is a cytokine growth factor, whose expression is strongly induced by injury in a variety of tissues across a range of vertebrate classes. Using a zebrafish Midkine-a loss of function mutant, we evaluated regeneration of caudal fin, extraocular muscle and retinal neurons to investigate the function of Midkine-a during epimorphic regeneration. In wildtype zebrafish, injury among these tissues induces robust proliferation and rapid regeneration. In Midkine-a mutants, the initial proliferation in each of these tissues is significantly diminished or absent. Regeneration of the caudal fin and extraocular muscle is delayed; regeneration of the retina is nearly completely absent. These data demonstrate that Midkine-a is universally required in the signaling pathways that convert tissue injury into the initial burst of cell proliferation. Further, these data highlight differences in the molecular mechanisms that regulate epimorphic regeneration in zebrafish. |
| doi_str_mv | 10.1371/journal.pone.0232308 |
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Proliferation among the cells that will functionally restore injured tissues is a fundamental biological process underlying regeneration. Midkine-a is a cytokine growth factor, whose expression is strongly induced by injury in a variety of tissues across a range of vertebrate classes. Using a zebrafish Midkine-a loss of function mutant, we evaluated regeneration of caudal fin, extraocular muscle and retinal neurons to investigate the function of Midkine-a during epimorphic regeneration. In wildtype zebrafish, injury among these tissues induces robust proliferation and rapid regeneration. In Midkine-a mutants, the initial proliferation in each of these tissues is significantly diminished or absent. Regeneration of the caudal fin and extraocular muscle is delayed; regeneration of the retina is nearly completely absent. These data demonstrate that Midkine-a is universally required in the signaling pathways that convert tissue injury into the initial burst of cell proliferation. Further, these data highlight differences in the molecular mechanisms that regulate epimorphic regeneration in zebrafish.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0232308</identifier><identifier>PMID: 32530962</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Ablation ; Amputation ; Analysis ; Animal Fins - physiology ; Animals ; Animals, Genetically Modified - metabolism ; Apoptosis ; Biological activity ; Biology and Life Sciences ; Cell cycle ; Cell Differentiation ; Cell Proliferation ; Cell regulation ; Cells (biology) ; Cytokines ; Danio rerio ; Growth factors ; Injuries ; Medicine and Health Sciences ; Midkine ; Midkine - genetics ; Midkine - metabolism ; Molecular modelling ; Muscles ; Mutagenesis ; Mutants ; Nervous system ; Neuroglia - cytology ; Neuroglia - metabolism ; Oculomotor Muscles - physiology ; Photoreceptors ; Physiological aspects ; Progenitor cells ; Regeneration ; Regeneration (Biology) ; Regeneration - physiology ; Research and Analysis Methods ; Retina ; Retinal Neurons - physiology ; Social Sciences ; Stem cells ; Tissues ; Vertebrates ; Zebrafish ; Zebrafish - metabolism ; Zebrafish Proteins - genetics ; Zebrafish Proteins - metabolism</subject><ispartof>PloS one, 2020-06, Vol.15 (6), p.e0232308</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Ang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Proliferation among the cells that will functionally restore injured tissues is a fundamental biological process underlying regeneration. Midkine-a is a cytokine growth factor, whose expression is strongly induced by injury in a variety of tissues across a range of vertebrate classes. Using a zebrafish Midkine-a loss of function mutant, we evaluated regeneration of caudal fin, extraocular muscle and retinal neurons to investigate the function of Midkine-a during epimorphic regeneration. In wildtype zebrafish, injury among these tissues induces robust proliferation and rapid regeneration. In Midkine-a mutants, the initial proliferation in each of these tissues is significantly diminished or absent. Regeneration of the caudal fin and extraocular muscle is delayed; regeneration of the retina is nearly completely absent. These data demonstrate that Midkine-a is universally required in the signaling pathways that convert tissue injury into the initial burst of cell proliferation. Further, these data highlight differences in the molecular mechanisms that regulate epimorphic regeneration in zebrafish.</description><subject>Ablation</subject><subject>Amputation</subject><subject>Analysis</subject><subject>Animal Fins - physiology</subject><subject>Animals</subject><subject>Animals, Genetically Modified - metabolism</subject><subject>Apoptosis</subject><subject>Biological activity</subject><subject>Biology and Life Sciences</subject><subject>Cell cycle</subject><subject>Cell Differentiation</subject><subject>Cell Proliferation</subject><subject>Cell regulation</subject><subject>Cells (biology)</subject><subject>Cytokines</subject><subject>Danio rerio</subject><subject>Growth factors</subject><subject>Injuries</subject><subject>Medicine and Health Sciences</subject><subject>Midkine</subject><subject>Midkine - genetics</subject><subject>Midkine - metabolism</subject><subject>Molecular modelling</subject><subject>Muscles</subject><subject>Mutagenesis</subject><subject>Mutants</subject><subject>Nervous system</subject><subject>Neuroglia - 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Proliferation among the cells that will functionally restore injured tissues is a fundamental biological process underlying regeneration. Midkine-a is a cytokine growth factor, whose expression is strongly induced by injury in a variety of tissues across a range of vertebrate classes. Using a zebrafish Midkine-a loss of function mutant, we evaluated regeneration of caudal fin, extraocular muscle and retinal neurons to investigate the function of Midkine-a during epimorphic regeneration. In wildtype zebrafish, injury among these tissues induces robust proliferation and rapid regeneration. In Midkine-a mutants, the initial proliferation in each of these tissues is significantly diminished or absent. Regeneration of the caudal fin and extraocular muscle is delayed; regeneration of the retina is nearly completely absent. These data demonstrate that Midkine-a is universally required in the signaling pathways that convert tissue injury into the initial burst of cell proliferation. Further, these data highlight differences in the molecular mechanisms that regulate epimorphic regeneration in zebrafish.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32530962</pmid><doi>10.1371/journal.pone.0232308</doi><tpages>e0232308</tpages><orcidid>https://orcid.org/0000-0003-0993-0012</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Ablation Amputation Analysis Animal Fins - physiology Animals Animals, Genetically Modified - metabolism Apoptosis Biological activity Biology and Life Sciences Cell cycle Cell Differentiation Cell Proliferation Cell regulation Cells (biology) Cytokines Danio rerio Growth factors Injuries Medicine and Health Sciences Midkine Midkine - genetics Midkine - metabolism Molecular modelling Muscles Mutagenesis Mutants Nervous system Neuroglia - cytology Neuroglia - metabolism Oculomotor Muscles - physiology Photoreceptors Physiological aspects Progenitor cells Regeneration Regeneration (Biology) Regeneration - physiology Research and Analysis Methods Retina Retinal Neurons - physiology Social Sciences Stem cells Tissues Vertebrates Zebrafish Zebrafish - metabolism Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
| title | Midkine-a functions as a universal regulator of proliferation during epimorphic regeneration in adult zebrafish |
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