Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche

Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour 1 , 2 . The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The...

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Veröffentlicht in:Nature (London) 2018-06, Vol.558 (7710), p.445-448
Hauptverfasser: Kapp, Friedrich G., Perlin, Julie R., Hagedorn, Elliott J., Gansner, John M., Schwarz, Daniel E., O’Connell, Lauren A., Johnson, Nicholas S., Amemiya, Chris, Fisher, David E., Wölfle, Ute, Trompouki, Eirini, Niemeyer, Charlotte M., Driever, Wolfgang, Zon, Leonard I.
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container_issue 7710
container_start_page 445
container_title Nature (London)
container_volume 558
creator Kapp, Friedrich G.
Perlin, Julie R.
Hagedorn, Elliott J.
Gansner, John M.
Schwarz, Daniel E.
O’Connell, Lauren A.
Johnson, Nicholas S.
Amemiya, Chris
Fisher, David E.
Wölfle, Ute
Trompouki, Eirini
Niemeyer, Charlotte M.
Driever, Wolfgang
Zon, Leonard I.
description Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour 1 , 2 . The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The niche is located in the bone marrow in adult mammals, whereas it is found in other locations in non-mammalian vertebrates, for example, in the kidney marrow in teleost fish. Here we show that a melanocyte umbrella above the kidney marrow protects HSPCs against ultraviolet light in zebrafish. Because mutants that lack melanocytes have normal steady-state haematopoiesis under standard laboratory conditions, we hypothesized that melanocytes above the stem cell niche protect HSPCs against ultraviolet-light-induced DNA damage. Indeed, after ultraviolet-light irradiation, unpigmented larvae show higher levels of DNA damage in HSPCs, as indicated by staining of cyclobutane pyrimidine dimers and have reduced numbers of HSPCs, as shown by cmyb (also known as myb ) expression. The umbrella of melanocytes associated with the haematopoietic niche is highly evolutionarily conserved in aquatic animals, including the sea lamprey, a basal vertebrate. During the transition from an aquatic to a terrestrial environment, HSPCs relocated into the bone marrow, which is protected from ultraviolet light by the cortical bone around the marrow. Our studies reveal that melanocytes above the haematopoietic niche protect HSPCs from ultraviolet-light-induced DNA damage in aquatic vertebrates and suggest that during the transition to terrestrial life, ultraviolet light was an evolutionary pressure affecting the location of the haematopoietic niche. Melanocytes above the haematopoietic niche protect haematopoietic stem cells from ultraviolet-light-induced DNA damage in aquatic vertebrates throughout evolution; this niche moved to the bone marrow during the transition to terrestrial life.
doi_str_mv 10.1038/s41586-018-0213-0
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The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The niche is located in the bone marrow in adult mammals, whereas it is found in other locations in non-mammalian vertebrates, for example, in the kidney marrow in teleost fish. Here we show that a melanocyte umbrella above the kidney marrow protects HSPCs against ultraviolet light in zebrafish. Because mutants that lack melanocytes have normal steady-state haematopoiesis under standard laboratory conditions, we hypothesized that melanocytes above the stem cell niche protect HSPCs against ultraviolet-light-induced DNA damage. Indeed, after ultraviolet-light irradiation, unpigmented larvae show higher levels of DNA damage in HSPCs, as indicated by staining of cyclobutane pyrimidine dimers and have reduced numbers of HSPCs, as shown by cmyb (also known as myb ) expression. The umbrella of melanocytes associated with the haematopoietic niche is highly evolutionarily conserved in aquatic animals, including the sea lamprey, a basal vertebrate. During the transition from an aquatic to a terrestrial environment, HSPCs relocated into the bone marrow, which is protected from ultraviolet light by the cortical bone around the marrow. Our studies reveal that melanocytes above the haematopoietic niche protect HSPCs from ultraviolet-light-induced DNA damage in aquatic vertebrates and suggest that during the transition to terrestrial life, ultraviolet light was an evolutionary pressure affecting the location of the haematopoietic niche. 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The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The niche is located in the bone marrow in adult mammals, whereas it is found in other locations in non-mammalian vertebrates, for example, in the kidney marrow in teleost fish. Here we show that a melanocyte umbrella above the kidney marrow protects HSPCs against ultraviolet light in zebrafish. Because mutants that lack melanocytes have normal steady-state haematopoiesis under standard laboratory conditions, we hypothesized that melanocytes above the stem cell niche protect HSPCs against ultraviolet-light-induced DNA damage. Indeed, after ultraviolet-light irradiation, unpigmented larvae show higher levels of DNA damage in HSPCs, as indicated by staining of cyclobutane pyrimidine dimers and have reduced numbers of HSPCs, as shown by cmyb (also known as myb ) expression. The umbrella of melanocytes associated with the haematopoietic niche is highly evolutionarily conserved in aquatic animals, including the sea lamprey, a basal vertebrate. During the transition from an aquatic to a terrestrial environment, HSPCs relocated into the bone marrow, which is protected from ultraviolet light by the cortical bone around the marrow. Our studies reveal that melanocytes above the haematopoietic niche protect HSPCs from ultraviolet-light-induced DNA damage in aquatic vertebrates and suggest that during the transition to terrestrial life, ultraviolet light was an evolutionary pressure affecting the location of the haematopoietic niche. 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Edition</collection><collection>ProQuest One Psychology</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>ProQuest Central Basic</collection><collection>University of Michigan</collection><collection>Genetics Abstracts</collection><collection>SIRS Editorial</collection><collection>Environment Abstracts</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kapp, Friedrich G.</au><au>Perlin, Julie R.</au><au>Hagedorn, Elliott J.</au><au>Gansner, John M.</au><au>Schwarz, Daniel E.</au><au>O’Connell, Lauren A.</au><au>Johnson, Nicholas S.</au><au>Amemiya, Chris</au><au>Fisher, David E.</au><au>Wölfle, Ute</au><au>Trompouki, Eirini</au><au>Niemeyer, Charlotte M.</au><au>Driever, Wolfgang</au><au>Zon, Leonard I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2018-06</date><risdate>2018</risdate><volume>558</volume><issue>7710</issue><spage>445</spage><epage>448</epage><pages>445-448</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><abstract>Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour 1 , 2 . The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The niche is located in the bone marrow in adult mammals, whereas it is found in other locations in non-mammalian vertebrates, for example, in the kidney marrow in teleost fish. Here we show that a melanocyte umbrella above the kidney marrow protects HSPCs against ultraviolet light in zebrafish. Because mutants that lack melanocytes have normal steady-state haematopoiesis under standard laboratory conditions, we hypothesized that melanocytes above the stem cell niche protect HSPCs against ultraviolet-light-induced DNA damage. Indeed, after ultraviolet-light irradiation, unpigmented larvae show higher levels of DNA damage in HSPCs, as indicated by staining of cyclobutane pyrimidine dimers and have reduced numbers of HSPCs, as shown by cmyb (also known as myb ) expression. The umbrella of melanocytes associated with the haematopoietic niche is highly evolutionarily conserved in aquatic animals, including the sea lamprey, a basal vertebrate. During the transition from an aquatic to a terrestrial environment, HSPCs relocated into the bone marrow, which is protected from ultraviolet light by the cortical bone around the marrow. Our studies reveal that melanocytes above the haematopoietic niche protect HSPCs from ultraviolet-light-induced DNA damage in aquatic vertebrates and suggest that during the transition to terrestrial life, ultraviolet light was an evolutionary pressure affecting the location of the haematopoietic niche. Melanocytes above the haematopoietic niche protect haematopoietic stem cells from ultraviolet-light-induced DNA damage in aquatic vertebrates throughout evolution; this niche moved to the bone marrow during the transition to terrestrial life.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29899448</pmid><doi>10.1038/s41586-018-0213-0</doi><tpages>4</tpages><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0028-0836
ispartof Nature (London), 2018-06, Vol.558 (7710), p.445-448
issn 0028-0836
1476-4687
language eng
recordid cdi_proquest_journals_2067321692
source MEDLINE; Springer Nature - Complete Springer Journals; Nature
subjects 13/51
14
14/19
14/35
14/63
631/136/232
631/136/334/1874/763
631/136/532/1542
631/181/2806
631/532/2139
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Animals
Aquatic animals
Aquatic environment
Aquatic Organisms - classification
Biodiversity conservation
Biological Evolution
Bone marrow
Brain
Cells (biology)
Cortical bone
Cyclobutane
Cyclobutane pyrimidine dimers
Cytoprotection - radiation effects
Danio rerio
Deoxyribonucleic acid
Dimers
DNA
DNA damage
DNA Damage - radiation effects
Environmental aspects
Evolution
Gene expression
Hematopoietic stem cells
Hematopoietic Stem Cells - cytology
Hematopoietic Stem Cells - radiation effects
Humanities and Social Sciences
Irradiation
Kidney
Kidneys
Laboratories
Larvae
Letter
Light
Light irradiation
Mammals
Melanocytes
Melanocytes - cytology
Melanocytes - radiation effects
Methods
Microenvironments
multidisciplinary
Mutation
Niches
Petromyzon - classification
Phylogeny
Progenitor cells
Pyrimidine Dimers - radiation effects
Pyrimidines
Radiation damage
Science
Science (multidisciplinary)
Siblings
Stem Cell Niche - physiology
Stem Cell Niche - radiation effects
Stem cells
Terrestrial ecosystems
Terrestrial environments
Transcription factors
Ultraviolet radiation
Ultraviolet Rays - adverse effects
Vertebrates
Wildlife conservation
Zebrafish
Zebrafish - classification
Zebrafish - genetics
title Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche
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