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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Published inNature (London) Vol. 558; no. 7710; pp. 445 - 448
Main Authors 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.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.06.2018
Nature Publishing Group
Subjects
Online AccessGet full text
ISSN0028-0836
1476-4687
1476-4687
DOI10.1038/s41586-018-0213-0

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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.
AbstractList Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour . 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.
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour.sup.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.
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour1,2. 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.Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour1,2. 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.
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour.sup.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.
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour1,2. 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-lightinduced 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.
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.
Audience Academic
Author Kapp, Friedrich G.
Zon, Leonard I.
Niemeyer, Charlotte M.
Schwarz, Daniel E.
Amemiya, Chris
Johnson, Nicholas S.
Driever, Wolfgang
Perlin, Julie R.
Gansner, John M.
Fisher, David E.
Wölfle, Ute
Hagedorn, Elliott J.
O’Connell, Lauren A.
Trompouki, Eirini
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  surname: Kapp
  fullname: Kapp, Friedrich G.
  organization: Department of Stem Cell and Regenerative Biology and Harvard Stem Cell Institute, Harvard University, Stem Cell Program and Division of Hematology/Oncology, Boston Children’s Hospital and Dana Farber Cancer Institute, Howard Hughes Medical Institute, Harvard Stem Cell Institute, Harvard Medical School, Department of Pediatric Hematology and Oncology, Center for Pediatrics, Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg
– sequence: 2
  givenname: Julie R.
  surname: Perlin
  fullname: Perlin, Julie R.
  organization: Department of Stem Cell and Regenerative Biology and Harvard Stem Cell Institute, Harvard University, Stem Cell Program and Division of Hematology/Oncology, Boston Children’s Hospital and Dana Farber Cancer Institute, Howard Hughes Medical Institute, Harvard Stem Cell Institute, Harvard Medical School
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  givenname: Elliott J.
  surname: Hagedorn
  fullname: Hagedorn, Elliott J.
  organization: Department of Stem Cell and Regenerative Biology and Harvard Stem Cell Institute, Harvard University, Stem Cell Program and Division of Hematology/Oncology, Boston Children’s Hospital and Dana Farber Cancer Institute, Howard Hughes Medical Institute, Harvard Stem Cell Institute, Harvard Medical School
– sequence: 4
  givenname: John M.
  surname: Gansner
  fullname: Gansner, John M.
  organization: Division of Hematology, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School
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  givenname: Daniel E.
  surname: Schwarz
  fullname: Schwarz, Daniel E.
  organization: US Fish and Wildlife Service, Private John Allen National Fish Hatchery
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  surname: O’Connell
  fullname: O’Connell, Lauren A.
  organization: Department of Biology, Stanford University
– sequence: 7
  givenname: Nicholas S.
  surname: Johnson
  fullname: Johnson, Nicholas S.
  organization: US Geological Survey, Great Lakes Science Center, Hammond Bay Biological Station
– sequence: 8
  givenname: Chris
  surname: Amemiya
  fullname: Amemiya, Chris
  organization: Molecular Cell Biology, University of California
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  givenname: David E.
  surname: Fisher
  fullname: Fisher, David E.
  organization: Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School
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  givenname: Ute
  surname: Wölfle
  fullname: Wölfle, Ute
  organization: Department of Dermatology, Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg
– sequence: 11
  givenname: Eirini
  surname: Trompouki
  fullname: Trompouki, Eirini
  organization: Department of Cellular and Molecular Immunology, Max Planck Institute of Immunobiology and Epigenetics
– sequence: 12
  givenname: Charlotte M.
  surname: Niemeyer
  fullname: Niemeyer, Charlotte M.
  organization: Department of Pediatric Hematology and Oncology, Center for Pediatrics, Medical Center–University of Freiburg, Faculty of Medicine, University of Freiburg
– sequence: 13
  givenname: Wolfgang
  surname: Driever
  fullname: Driever, Wolfgang
  organization: Developmental Biology, Faculty of Biology, Centre for Biological Signalling Studies (BIOSS), Albert-Ludwigs-University of Freiburg
– sequence: 14
  givenname: Leonard I.
  surname: Zon
  fullname: Zon, Leonard I.
  email: zon@enders.tch.harvard.edu
  organization: Department of Stem Cell and Regenerative Biology and Harvard Stem Cell Institute, Harvard University, Stem Cell Program and Division of Hematology/Oncology, Boston Children’s Hospital and Dana Farber Cancer Institute, Howard Hughes Medical Institute, Harvard Stem Cell Institute, Harvard Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29899448$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Macmillan Publishers Ltd., part of Springer Nature 2018
COPYRIGHT 2018 Nature Publishing Group
Copyright Nature Publishing Group Jun 21, 2018
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Snippet Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour 1 , 2 . The...
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour . The location...
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour.sup.1,2. The...
Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour1,2. The location...
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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
URI https://link.springer.com/article/10.1038/s41586-018-0213-0
https://www.ncbi.nlm.nih.gov/pubmed/29899448
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Volume 558
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