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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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 |
format | Article |
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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.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-018-0213-0</identifier><identifier>PMID: 29899448</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>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 ; 64/116 ; 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</subject><ispartof>Nature (London), 2018-06, Vol.558 (7710), p.445-448</ispartof><rights>Macmillan Publishers Ltd., part of Springer Nature 2018</rights><rights>COPYRIGHT 2018 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jun 21, 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c684t-96466d5415d2a5ad8f903797510bd3e8c6f213951f38e48f864040557ec190423</citedby><cites>FETCH-LOGICAL-c684t-96466d5415d2a5ad8f903797510bd3e8c6f213951f38e48f864040557ec190423</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-018-0213-0$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-018-0213-0$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29899448$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kapp, Friedrich G.</creatorcontrib><creatorcontrib>Perlin, Julie R.</creatorcontrib><creatorcontrib>Hagedorn, Elliott J.</creatorcontrib><creatorcontrib>Gansner, John M.</creatorcontrib><creatorcontrib>Schwarz, Daniel E.</creatorcontrib><creatorcontrib>O’Connell, Lauren A.</creatorcontrib><creatorcontrib>Johnson, Nicholas S.</creatorcontrib><creatorcontrib>Amemiya, Chris</creatorcontrib><creatorcontrib>Fisher, David E.</creatorcontrib><creatorcontrib>Wölfle, Ute</creatorcontrib><creatorcontrib>Trompouki, Eirini</creatorcontrib><creatorcontrib>Niemeyer, Charlotte M.</creatorcontrib><creatorcontrib>Driever, Wolfgang</creatorcontrib><creatorcontrib>Zon, Leonard I.</creatorcontrib><title>Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><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.</description><subject>13/51</subject><subject>14</subject><subject>14/19</subject><subject>14/35</subject><subject>14/63</subject><subject>631/136/232</subject><subject>631/136/334/1874/763</subject><subject>631/136/532/1542</subject><subject>631/181/2806</subject><subject>631/532/2139</subject><subject>64/116</subject><subject>Animals</subject><subject>Aquatic animals</subject><subject>Aquatic environment</subject><subject>Aquatic Organisms - classification</subject><subject>Biodiversity conservation</subject><subject>Biological Evolution</subject><subject>Bone marrow</subject><subject>Brain</subject><subject>Cells (biology)</subject><subject>Cortical bone</subject><subject>Cyclobutane</subject><subject>Cyclobutane pyrimidine 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effects</subject><subject>Methods</subject><subject>Microenvironments</subject><subject>multidisciplinary</subject><subject>Mutation</subject><subject>Niches</subject><subject>Petromyzon - classification</subject><subject>Phylogeny</subject><subject>Progenitor cells</subject><subject>Pyrimidine Dimers - radiation effects</subject><subject>Pyrimidines</subject><subject>Radiation damage</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Siblings</subject><subject>Stem Cell Niche - physiology</subject><subject>Stem Cell Niche - radiation effects</subject><subject>Stem cells</subject><subject>Terrestrial ecosystems</subject><subject>Terrestrial environments</subject><subject>Transcription factors</subject><subject>Ultraviolet radiation</subject><subject>Ultraviolet Rays - adverse effects</subject><subject>Vertebrates</subject><subject>Wildlife conservation</subject><subject>Zebrafish</subject><subject>Zebrafish - 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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> |
fulltext | fulltext |
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 64/116 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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