Keratinocytes of the Upper Epidermis and Isthmus of Hair Follicles Express Hemoglobin mRNA and Protein

The epidermis, the keratinized stratified squamous epithelium surrounding the body surface, offers a valuable framework to investigate how terrestrial animals overcome environmental stresses. However, the mechanisms underlying epidermal barrier function remain nebulous. In this study, we examined ge...

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Published inJournal of investigative dermatology Vol. 143; no. 12; pp. 2346 - 2355.e10
Main Authors Tahara, Umi, Matsui, Takeshi, Atsugi, Toru, Fukuda, Keitaro, Terooatea, Tommy W, Minoda, Aki, Kubo, Akiharu, Amagai, Masayuki
Format Journal Article
LanguageEnglish
Published United States 01.12.2023
Subjects
Animals
Carcinoma, Squamous Cell
Epidermis
Female
Hair Follicle
Hemoglobins
Humans
Keratinocytes
Mice
RNA, Messenger - genetics
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Abstract The epidermis, the keratinized stratified squamous epithelium surrounding the body surface, offers a valuable framework to investigate how terrestrial animals overcome environmental stresses. However, the mechanisms underlying epidermal barrier function remain nebulous. In this study, we examined genes highly expressed in the human and mouse upper epidermis, the outer frontier that induces various barrier-related genes. Transcriptome analysis revealed that the messenger RNA level of hemoglobin α (HBA), an oxygen carrier in erythroid cells, was enriched in the upper epidermis compared with that in the whole epidermis. Immunostaining analysis confirmed HBA protein expression in human and mouse keratinocytes (KCs) of the stratum spinosum and stratum granulosum. HBA was also expressed in hair follicle KCs in the isthmus region; its expression levels were more prominent than those in interfollicular KCs. HBA expression was not observed in noncutaneous keratinized stratified squamous epithelia of mice, for example, the vagina, esophagus, and forestomach. HBA expression was upregulated in human epidermal KC cultures after UV irradiation, a major cause of skin-specific oxidative stress. Furthermore, HBA knockdown increased UV-induced production of ROS in primary KCs. Our findings suggest that epidermal HBA expression is induced by oxidative stress and acts as an antioxidant, contributing to skin barrier function.
AbstractList The epidermis, the keratinized stratified squamous epithelium surrounding the body surface, offers a valuable framework to investigate how terrestrial animals overcome environmental stresses. However, the mechanisms underlying epidermal barrier function remain nebulous. In this study, we examined genes highly expressed in the human and mouse upper epidermis, the outer frontier that induces various barrier-related genes. Transcriptome analysis revealed that the messenger RNA level of hemoglobin α (HBA), an oxygen carrier in erythroid cells, was enriched in the upper epidermis compared with that in the whole epidermis. Immunostaining analysis confirmed HBA protein expression in human and mouse keratinocytes (KCs) of the stratum spinosum and stratum granulosum. HBA was also expressed in hair follicle KCs in the isthmus region; its expression levels were more prominent than those in interfollicular KCs. HBA expression was not observed in noncutaneous keratinized stratified squamous epithelia of mice, for example, the vagina, esophagus, and forestomach. HBA expression was upregulated in human epidermal KC cultures after UV irradiation, a major cause of skin-specific oxidative stress. Furthermore, HBA knockdown increased UV-induced production of ROS in primary KCs. Our findings suggest that epidermal HBA expression is induced by oxidative stress and acts as an antioxidant, contributing to skin barrier function.
Author Fukuda, Keitaro
Kubo, Akiharu
Matsui, Takeshi
Minoda, Aki
Terooatea, Tommy W
Tahara, Umi
Atsugi, Toru
Amagai, Masayuki
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  givenname: Masayuki
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  email: masayuki.amagai@riken.jp
  organization: Laboratory for Skin Homeostasis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan; Department of Dermatology, Keio University School of Medicine, Tokyo, Japan. Electronic address: masayuki.amagai@riken.jp
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Cites_doi 10.1016/j.freeradbiomed.2011.11.019
10.1016/j.celrep.2020.02.091
10.1016/j.stemcr.2015.09.013
10.1046/j.1365-2184.35.s1.1.x
10.1016/j.redox.2020.101687
10.1016/j.cell.2021.04.048
10.1034/j.1600-0625.2000.009006431.x
10.1034/j.1600-0781.2003.00036.x
10.1038/81385
10.1111/j.1365-2141.2004.05257.x
10.1111/j.1365-2133.1983.tb01056.x
10.1073/pnas.2020722118
10.1016/j.immuni.2021.09.001
10.1093/intimm/dxv013
10.1177/1176934319862246
10.1038/ncb3359
10.1016/j.cell.2020.03.015
10.1038/nature11626
10.1006/bbrc.2002.6362
10.1093/humrep/dem430
10.1242/jcs.111.21.3179
10.1242/jeb.02007
10.1046/j.1440-0960.2002.00615.x
10.1152/physrev.1997.77.2.397
10.1038/s41467-022-29747-x
10.1016/j.celrep.2020.01.003
10.1002/jez.b.24
10.1002/bies.201700029
10.1016/j.jid.2021.07.176
10.1093/nar/gkv007
10.1126/science.1690453
10.1007/978-4-431-55855-2_13
10.1111/aji.12645
10.1038/s41467-019-09234-6
10.1016/j.peptides.2004.06.015
10.1093/molbev/msz279
10.7554/eLife.19593
10.1016/S1011-1344(00)00149-4
10.1167/iovs.07-1372
10.1111/j.1432-0436.1993.tb01585.x
10.1371/journal.pone.0171084
10.1083/jcb.65.1.180
10.1016/j.stemcr.2013.04.001
10.1016/j.cels.2016.08.010
10.1038/s41586-020-2292-y
10.1177/1358863X17722211
10.1111/jdv.13250
10.1016/j.jphotobiol.2008.07.010
10.1172/JCI99933
10.1038/ncomms14344
10.1038/nature00803
10.1007/s00403-012-1215-7
10.1007/BF00221757
10.1186/1465-9921-11-123
10.1016/S1046-2023(02)00204-9
10.1016/j.celrep.2018.09.006
10.1016/S1095-6433(01)00508-6
10.1038/jid.2011.119
10.1046/j.1432-0436.1994.5630143.x
10.1073/pnas.0813216106
10.3390/antiox10101608
10.1016/j.nbd.2004.08.014
10.1093/nar/gks1193
10.1021/ja00793a065
10.1016/j.jdermsci.2019.04.006
10.1111/j.1600-0625.2008.00786.x
10.1038/nmeth.2089
10.1007/978-1-62703-989-5_11
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References Biagioli (10.1016/j.jid.2023.08.008_bib6) 2009; 106
Kabir (10.1016/j.jid.2023.08.008_bib24) 2022; 13
Saha (10.1016/j.jid.2023.08.008_bib49) 2017; 12
Hao (10.1016/j.jid.2023.08.008_bib70) 2021; 184
Keppner (10.1016/j.jid.2023.08.008_bib26) 2020; 37
Barbosa (10.1016/j.jid.2023.08.008_bib4) 2021; 288
Kawamoto (10.1016/j.jid.2023.08.008_bib25) 2014; 1130
Gomez (10.1016/j.jid.2023.08.008_bib19) 2013; 1
Zheng (10.1016/j.jid.2023.08.008_bib66) 2017; 8
Amagai (10.1016/j.jid.2023.08.008_bib3) 2000; 6
Gimenez-Conti (10.1016/j.jid.2023.08.008_bib18) 1994; 56
Barrett (10.1016/j.jid.2023.08.008_bib5) 2013; 41
Li (10.1016/j.jid.2023.08.008_bib32) 2000; 9
10.1016/j.jid.2023.08.008_bib42
Pillai (10.1016/j.jid.2023.08.008_bib45) 2020; 581
Ritchie (10.1016/j.jid.2023.08.008_bib72) 2015; 43
Newman (10.1016/j.jid.2023.08.008_bib41) 1990; 247
Swalwell (10.1016/j.jid.2023.08.008_bib58) 2012; 52
Eckhart (10.1016/j.jid.2023.08.008_bib14) 2019; 15
Cheng (10.1016/j.jid.2023.08.008_bib9) 2005; 128
Usui (10.1016/j.jid.2023.08.008_bib73) 2019; 94
Potten (10.1016/j.jid.2023.08.008_bib46) 2002; 35
Jadkauskaite (10.1016/j.jid.2023.08.008_bib22) 2017; 39
Zhou (10.1016/j.jid.2023.08.008_bib67) 2019; 10
Hohl (10.1016/j.jid.2023.08.008_bib20) 1993; 54
Dassen (10.1016/j.jid.2023.08.008_bib10) 2008; 23
Kihm (10.1016/j.jid.2023.08.008_bib27) 2002; 417
Tini (10.1016/j.jid.2023.08.008_bib60) 2002; 131
Mancebo (10.1016/j.jid.2023.08.008_bib38) 2015; 29
Proksch (10.1016/j.jid.2023.08.008_bib47) 2008; 17
Alibardi (10.1016/j.jid.2023.08.008_bib2) 2003; 298
Kitano (10.1016/j.jid.2023.08.008_bib28) 1983; 108
Liu (10.1016/j.jid.2023.08.008_bib35) 2011; 6
Lee (10.1016/j.jid.2023.08.008_bib30) 2002; 43
Schweizer (10.1016/j.jid.2023.08.008_bib55) 1988; 253
Lillywhite (10.1016/j.jid.2023.08.008_bib34) 2006; 209
Wang (10.1016/j.jid.2023.08.008_bib61) 2021; 10
Stynes (10.1016/j.jid.2023.08.008_bib57) 1973; 95
Mak (10.1016/j.jid.2023.08.008_bib37) 2004; 25
Saha (10.1016/j.jid.2023.08.008_bib50) 2017; 77
Ali (10.1016/j.jid.2023.08.008_bib1) 2020; 30
Piao (10.1016/j.jid.2023.08.008_bib44) 2012; 304
Haensel (10.1016/j.jid.2023.08.008_bib69) 2020; 30
Ishikawa (10.1016/j.jid.2023.08.008_bib21) 2010; 11
Lechauve (10.1016/j.jid.2023.08.008_bib29) 2018; 128
Sada (10.1016/j.jid.2023.08.008_bib48) 2016; 18
Yokouchi (10.1016/j.jid.2023.08.008_bib65) 2016; 5
Li (10.1016/j.jid.2023.08.008_bib31) 2022; 142
Sangwung (10.1016/j.jid.2023.08.008_bib52) 2017; 22
Terooatea (10.1016/j.jid.2023.08.008_bib80) 2023
Elias (10.1016/j.jid.2023.08.008_bib16) 1975; 65
Dekoninck (10.1016/j.jid.2023.08.008_bib11) 2020; 181
Petersen (10.1016/j.jid.2023.08.008_bib43) 2000; 59
Tahara (10.1016/j.jid.2023.08.008_bib79) 2023
Diffey (10.1016/j.jid.2023.08.008_bib12) 2002; 28
Schäfer (10.1016/j.jid.2023.08.008_bib53) 2011; 131
Lyle (10.1016/j.jid.2023.08.008_bib36) 1998; 111
Straub (10.1016/j.jid.2023.08.008_bib56) 2012; 491
Cheng (10.1016/j.jid.2023.08.008_bib8) 2018; 25
Joost (10.1016/j.jid.2023.08.008_bib23) 2016; 3
Matsui (10.1016/j.jid.2023.08.008_bib40) 2021; 118
Yamaguchi (10.1016/j.jid.2023.08.008_bib64) 2002; 290
Füllgrabe (10.1016/j.jid.2023.08.008_bib17) 2015; 5
Matsui (10.1016/j.jid.2023.08.008_bib39) 2015; 27
Sakamoto (10.1016/j.jid.2023.08.008_bib51) 2021; 54
Schneider (10.1016/j.jid.2023.08.008_bib54) 2012; 9
Ehrlich (10.1016/j.jid.2023.08.008_bib15) 2020; 37
Tezel (10.1016/j.jid.2023.08.008_bib59) 2009; 50
Balogh (10.1016/j.jid.2023.08.008_bib68) 2008; 93
Eckert (10.1016/j.jid.2023.08.008_bib13) 1997; 77
Li (10.1016/j.jid.2023.08.008_bib33) 2013; 8
Wu (10.1016/j.jid.2023.08.008_bib63) 2004; 17
Joost (10.1016/j.jid.2023.08.008_bib71) 2016; 3
Wride (10.1016/j.jid.2023.08.008_bib62) 2003; 9
Calzavara Pinton (10.1016/j.jid.2023.08.008_bib7) 2003; 19
References_xml – volume: 52
  start-page: 626
  year: 2012
  ident: 10.1016/j.jid.2023.08.008_bib58
  article-title: Investigating the role of melanin in UVA/UVB- and hydrogen peroxide-induced cellular and mitochondrial ROS production and mitochondrial DNA damage in human melanoma cells
  publication-title: Free Radic Biol Med
  doi: 10.1016/j.freeradbiomed.2011.11.019
  contributor:
    fullname: Swalwell
– volume: 9
  start-page: 360
  year: 2003
  ident: 10.1016/j.jid.2023.08.008_bib62
  article-title: Expression profiling and gene discovery in the mouse lens
  publication-title: Mol Vis
  contributor:
    fullname: Wride
– volume: 30
  start-page: 3932
  year: 2020
  ident: 10.1016/j.jid.2023.08.008_bib69
  article-title: Defining epidermal basal cell states during skin homeostasis and wound healing using single-cell transcriptomics
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2020.02.091
  contributor:
    fullname: Haensel
– volume: 5
  start-page: 843
  year: 2015
  ident: 10.1016/j.jid.2023.08.008_bib17
  article-title: Dynamics of Lgr6+ progenitor cells in the hair follicle, sebaceous gland, and interfollicular epidermis
  publication-title: Stem Cell Rep
  doi: 10.1016/j.stemcr.2015.09.013
  contributor:
    fullname: Füllgrabe
– volume: 35
  start-page: 1
  issue: Suppl 1
  year: 2002
  ident: 10.1016/j.jid.2023.08.008_bib46
  article-title: Cell kinetic studies in the murine ventral tongue epithelium: thymidine metabolism studies and circadian rhythm determination
  publication-title: Cell Prolif
  doi: 10.1046/j.1365-2184.35.s1.1.x
  contributor:
    fullname: Potten
– volume: 37
  year: 2020
  ident: 10.1016/j.jid.2023.08.008_bib26
  article-title: Lessons from the post-genomic era: globin diversity beyond oxygen binding and transport
  publication-title: Redox Biol
  doi: 10.1016/j.redox.2020.101687
  contributor:
    fullname: Keppner
– volume: 184
  start-page: 3573
  year: 2021
  ident: 10.1016/j.jid.2023.08.008_bib70
  article-title: Integrated analysis of multimodal single-cell data
  publication-title: Cell
  doi: 10.1016/j.cell.2021.04.048
  contributor:
    fullname: Hao
– volume: 9
  start-page: 431
  year: 2000
  ident: 10.1016/j.jid.2023.08.008_bib32
  article-title: Expression of involucrin in normal, hyperproliferative and neoplastic mouse keratinocytes
  publication-title: Exp Dermatol
  doi: 10.1034/j.1600-0625.2000.009006431.x
  contributor:
    fullname: Li
– volume: 19
  start-page: 157
  year: 2003
  ident: 10.1016/j.jid.2023.08.008_bib7
  article-title: Photosensitive erythema multiforme and erythema multiforme-like polymorphous light eruption
  publication-title: Photodermatol Photoimmunol Photomed
  doi: 10.1034/j.1600-0781.2003.00036.x
  contributor:
    fullname: Calzavara Pinton
– volume: 6
  start-page: 1275
  year: 2000
  ident: 10.1016/j.jid.2023.08.008_bib3
  article-title: Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1
  publication-title: Nat Med
  doi: 10.1038/81385
  contributor:
    fullname: Amagai
– volume: 128
  start-page: 119
  year: 2005
  ident: 10.1016/j.jid.2023.08.008_bib9
  article-title: Antioxidant deficit and enhanced susceptibility to oxidative damage in individuals with different forms of alpha-thalassaemia
  publication-title: Br J Haematol
  doi: 10.1111/j.1365-2141.2004.05257.x
  contributor:
    fullname: Cheng
– volume: 108
  start-page: 555
  year: 1983
  ident: 10.1016/j.jid.2023.08.008_bib28
  article-title: Separation of the epidermal sheet by dispase
  publication-title: Br J Dermatol
  doi: 10.1111/j.1365-2133.1983.tb01056.x
  contributor:
    fullname: Kitano
– volume: 118
  year: 2021
  ident: 10.1016/j.jid.2023.08.008_bib40
  article-title: A unique mode of keratinocyte death requires intracellular acidification
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.2020722118
  contributor:
    fullname: Matsui
– volume: 54
  start-page: 2321
  year: 2021
  ident: 10.1016/j.jid.2023.08.008_bib51
  article-title: Disruption of the endopeptidase ADAM10-Notch signaling axis leads to skin dysbiosis and innate lymphoid cell-mediated hair follicle destruction
  publication-title: Immunity
  doi: 10.1016/j.immuni.2021.09.001
  contributor:
    fullname: Sakamoto
– volume: 27
  start-page: 269
  year: 2015
  ident: 10.1016/j.jid.2023.08.008_bib39
  article-title: Dissecting the formation, structure and barrier function of the stratum corneum [published correction appears in Int Immunol 2017;29:243–4]
  publication-title: Int Immunol
  doi: 10.1093/intimm/dxv013
  contributor:
    fullname: Matsui
– volume: 15
  year: 2019
  ident: 10.1016/j.jid.2023.08.008_bib14
  article-title: A stress response program at the origin of evolutionary innovation in the skin
  publication-title: Evol Bioinform Online
  doi: 10.1177/1176934319862246
  contributor:
    fullname: Eckhart
– volume: 8
  year: 2013
  ident: 10.1016/j.jid.2023.08.008_bib33
  article-title: Characterization of adult α- and β-globin elevated by hydrogen peroxide in cervical cancer cells that play a cytoprotective role against oxidative insults
  publication-title: PLoS One
  contributor:
    fullname: Li
– volume: 18
  start-page: 619
  year: 2016
  ident: 10.1016/j.jid.2023.08.008_bib48
  article-title: Defining the cellular lineage hierarchy in the interfollicular epidermis of adult skin
  publication-title: Nat Cell Biol
  doi: 10.1038/ncb3359
  contributor:
    fullname: Sada
– volume: 181
  start-page: 604
  year: 2020
  ident: 10.1016/j.jid.2023.08.008_bib11
  article-title: Defining the design principles of skin epidermis postnatal growth
  publication-title: Cell
  doi: 10.1016/j.cell.2020.03.015
  contributor:
    fullname: Dekoninck
– volume: 491
  start-page: 473
  year: 2012
  ident: 10.1016/j.jid.2023.08.008_bib56
  article-title: Endothelial cell expression of haemoglobin α regulates nitric oxide signalling
  publication-title: Nature
  doi: 10.1038/nature11626
  contributor:
    fullname: Straub
– volume: 290
  start-page: 1382
  year: 2002
  ident: 10.1016/j.jid.2023.08.008_bib64
  article-title: Hemoglobin equilibrium analysis by the multiangle laser light-scattering method
  publication-title: Biochem Biophys Res Commun
  doi: 10.1006/bbrc.2002.6362
  contributor:
    fullname: Yamaguchi
– volume: 23
  start-page: 635
  year: 2008
  ident: 10.1016/j.jid.2023.08.008_bib10
  article-title: Haemoglobin expression in human endometrium
  publication-title: Hum Reprod
  doi: 10.1093/humrep/dem430
  contributor:
    fullname: Dassen
– volume: 111
  start-page: 3179
  year: 1998
  ident: 10.1016/j.jid.2023.08.008_bib36
  article-title: The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells
  publication-title: J Cell Sci
  doi: 10.1242/jcs.111.21.3179
  contributor:
    fullname: Lyle
– volume: 209
  start-page: 202
  year: 2006
  ident: 10.1016/j.jid.2023.08.008_bib34
  article-title: Water relations of tetrapod integument
  publication-title: J Exp Biol
  doi: 10.1242/jeb.02007
  contributor:
    fullname: Lillywhite
– volume: 43
  start-page: 289
  year: 2002
  ident: 10.1016/j.jid.2023.08.008_bib30
  article-title: Photosensitivity: the 9-year experience at a Sydney contact dermatitis clinic [published correction appears in Australas J Dermatol 2003;44:158]
  publication-title: Australas J Dermatol
  doi: 10.1046/j.1440-0960.2002.00615.x
  contributor:
    fullname: Lee
– volume: 77
  start-page: 397
  year: 1997
  ident: 10.1016/j.jid.2023.08.008_bib13
  article-title: The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation
  publication-title: Physiol Rev
  doi: 10.1152/physrev.1997.77.2.397
  contributor:
    fullname: Eckert
– volume: 13
  start-page: 2167
  year: 2022
  ident: 10.1016/j.jid.2023.08.008_bib24
  article-title: Single cell transcriptomic analysis reveals cellular diversity of murine esophageal epithelium
  publication-title: Nat Commun
  doi: 10.1038/s41467-022-29747-x
  contributor:
    fullname: Kabir
– volume: 30
  start-page: 1463
  year: 2020
  ident: 10.1016/j.jid.2023.08.008_bib1
  article-title: Cell lineage tracing identifies hormone-regulated and wnt-responsive vaginal epithelial stem cells
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2020.01.003
  contributor:
    fullname: Ali
– volume: 6
  year: 2011
  ident: 10.1016/j.jid.2023.08.008_bib35
  article-title: Upregulation of hemoglobin expression by oxidative stress in hepatocytes and its implication in nonalcoholic steatohepatitis
  publication-title: PLoS One
  contributor:
    fullname: Liu
– volume: 298
  start-page: 12
  year: 2003
  ident: 10.1016/j.jid.2023.08.008_bib2
  article-title: Adaptation to the land: the skin of reptiles in comparison to that of amphibians and endotherm amniotes
  publication-title: J Exp Zool B Mol Dev Evol
  doi: 10.1002/jez.b.24
  contributor:
    fullname: Alibardi
– volume: 39
  year: 2017
  ident: 10.1016/j.jid.2023.08.008_bib22
  article-title: Oxidative stress management in the hair follicle: could targeting NRF2 counter age-related hair disorders and beyond?
  publication-title: Bioessays
  doi: 10.1002/bies.201700029
  contributor:
    fullname: Jadkauskaite
– volume: 142
  start-page: 705
  year: 2022
  ident: 10.1016/j.jid.2023.08.008_bib31
  article-title: Single-cell analysis reveals major histocompatibility complex II‒expressing keratinocytes in pressure ulcers with worse healing outcomes
  publication-title: J Invest Dermatol
  doi: 10.1016/j.jid.2021.07.176
  contributor:
    fullname: Li
– volume: 43
  start-page: e47
  year: 2015
  ident: 10.1016/j.jid.2023.08.008_bib72
  article-title: limma powers differential expression analyses for RNA-sequencing and microarray studies
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkv007
  contributor:
    fullname: Ritchie
– volume: 247
  start-page: 1219
  year: 1990
  ident: 10.1016/j.jid.2023.08.008_bib41
  article-title: PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily
  publication-title: Science
  doi: 10.1126/science.1690453
  contributor:
    fullname: Newman
– ident: 10.1016/j.jid.2023.08.008_bib42
  doi: 10.1007/978-4-431-55855-2_13
– volume: 77
  year: 2017
  ident: 10.1016/j.jid.2023.08.008_bib50
  article-title: Transcriptional regulation of Hb-α and Hb-β through nuclear factor E2-related factor-2 (Nrf2) activation in human vaginal cells: A novel mechanism of cellular adaptability to oxidative stress
  publication-title: Am J Reprod Immunol
  doi: 10.1111/aji.12645
  contributor:
    fullname: Saha
– volume: 10
  start-page: 1523
  year: 2019
  ident: 10.1016/j.jid.2023.08.008_bib67
  article-title: Metascape provides a biologist-oriented resource for the analysis of systems-level datasets
  publication-title: Nat Commun
  doi: 10.1038/s41467-019-09234-6
  contributor:
    fullname: Zhou
– volume: 25
  start-page: 1839
  year: 2004
  ident: 10.1016/j.jid.2023.08.008_bib37
  article-title: Antibacterial hemoglobin peptides in human menstrual blood
  publication-title: Peptides
  doi: 10.1016/j.peptides.2004.06.015
  contributor:
    fullname: Mak
– volume: 37
  start-page: 982
  year: 2020
  ident: 10.1016/j.jid.2023.08.008_bib15
  article-title: Convergent evolution of cysteine-rich keratins in hard skin appendages of terrestrial vertebrates
  publication-title: Mol Biol Evol
  doi: 10.1093/molbev/msz279
  contributor:
    fullname: Ehrlich
– volume: 5
  year: 2016
  ident: 10.1016/j.jid.2023.08.008_bib65
  article-title: Epidermal cell turnover across tight junctions based on Kelvin’s tetrakaidecahedron cell shape
  publication-title: Elife
  doi: 10.7554/eLife.19593
  contributor:
    fullname: Yokouchi
– volume: 59
  start-page: 123
  year: 2000
  ident: 10.1016/j.jid.2023.08.008_bib43
  article-title: Hydrogen peroxide is responsible for UVA-induced DNA damage measured by alkaline comet assay in HaCaT keratinocytes
  publication-title: J Photochem Photobiol B
  doi: 10.1016/S1011-1344(00)00149-4
  contributor:
    fullname: Petersen
– volume: 50
  start-page: 1911
  year: 2009
  ident: 10.1016/j.jid.2023.08.008_bib59
  article-title: Synthesis and secretion of hemoglobin by retinal pigment epithelium
  publication-title: Invest Ophthalmol Vis Sci
  doi: 10.1167/iovs.07-1372
  contributor:
    fullname: Tezel
– volume: 54
  start-page: 25
  year: 1993
  ident: 10.1016/j.jid.2023.08.008_bib20
  article-title: Expression patterns of loricrin in various species and tissues
  publication-title: Differentiation
  doi: 10.1111/j.1432-0436.1993.tb01585.x
  contributor:
    fullname: Hohl
– volume: 12
  year: 2017
  ident: 10.1016/j.jid.2023.08.008_bib49
  article-title: Expression of hemoglobin-α and β subunits in human vaginal epithelial cells and their functional significance
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0171084
  contributor:
    fullname: Saha
– volume: 65
  start-page: 180
  year: 1975
  ident: 10.1016/j.jid.2023.08.008_bib16
  article-title: The permeability barrier in mammalian epidermis
  publication-title: J Cell Biol
  doi: 10.1083/jcb.65.1.180
  contributor:
    fullname: Elias
– volume: 1
  start-page: 19
  year: 2013
  ident: 10.1016/j.jid.2023.08.008_bib19
  article-title: The interfollicular epidermis of adult mouse tail comprises two distinct cell lineages that are differentially regulated by Wnt, Edaradd, and Lrig1
  publication-title: Stem Cell Rep
  doi: 10.1016/j.stemcr.2013.04.001
  contributor:
    fullname: Gomez
– volume: 3
  start-page: 221
  year: 2016
  ident: 10.1016/j.jid.2023.08.008_bib71
  article-title: Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2016.08.010
  contributor:
    fullname: Joost
– year: 2023
  ident: 10.1016/j.jid.2023.08.008_bib79
  contributor:
    fullname: Tahara
– volume: 581
  start-page: 480
  year: 2020
  ident: 10.1016/j.jid.2023.08.008_bib45
  article-title: Origin of complexity in haemoglobin evolution [published correction appears in Nature 2020;583:E26]
  publication-title: Nature
  doi: 10.1038/s41586-020-2292-y
  contributor:
    fullname: Pillai
– volume: 22
  start-page: 363
  year: 2017
  ident: 10.1016/j.jid.2023.08.008_bib52
  article-title: Regulation of endothelial hemoglobin alpha expression by Kruppel-like factors
  publication-title: Vasc Med
  doi: 10.1177/1358863X17722211
  contributor:
    fullname: Sangwung
– volume: 29
  start-page: 2326
  year: 2015
  ident: 10.1016/j.jid.2023.08.008_bib38
  article-title: Recognizing the impact of ambient air pollution on skin health
  publication-title: J Eur Acad Dermatol Venereol
  doi: 10.1111/jdv.13250
  contributor:
    fullname: Mancebo
– volume: 93
  start-page: 133
  year: 2008
  ident: 10.1016/j.jid.2023.08.008_bib68
  article-title: Reference genes for quantitative real time PCR in UVB irradiated keratinocytes
  publication-title: J Photochem Photobiol B
  doi: 10.1016/j.jphotobiol.2008.07.010
  contributor:
    fullname: Balogh
– volume: 128
  start-page: 5073
  year: 2018
  ident: 10.1016/j.jid.2023.08.008_bib29
  article-title: Endothelial cell α-globin and its molecular chaperone α-hemoglobin-stabilizing protein regulate arteriolar contractility
  publication-title: J Clin Invest
  doi: 10.1172/JCI99933
  contributor:
    fullname: Lechauve
– year: 2023
  ident: 10.1016/j.jid.2023.08.008_bib80
  contributor:
    fullname: Terooatea
– volume: 3
  start-page: 221
  year: 2016
  ident: 10.1016/j.jid.2023.08.008_bib23
  article-title: Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2016.08.010
  contributor:
    fullname: Joost
– volume: 8
  year: 2017
  ident: 10.1016/j.jid.2023.08.008_bib66
  article-title: Expression of β-globin by cancer cells promotes cell survival during blood-borne dissemination
  publication-title: Nat Commun
  doi: 10.1038/ncomms14344
  contributor:
    fullname: Zheng
– volume: 417
  start-page: 758
  year: 2002
  ident: 10.1016/j.jid.2023.08.008_bib27
  article-title: An abundant erythroid protein that stabilizes free alpha-haemoglobin
  publication-title: Nature
  doi: 10.1038/nature00803
  contributor:
    fullname: Kihm
– volume: 304
  start-page: 387
  year: 2012
  ident: 10.1016/j.jid.2023.08.008_bib44
  article-title: Nrf2-dependent and Nrf2-independent induction of phase 2 detoxifying and antioxidant enzymes during keratinocyte differentiation
  publication-title: Arch Dermatol Res
  doi: 10.1007/s00403-012-1215-7
  contributor:
    fullname: Piao
– volume: 253
  start-page: 221
  year: 1988
  ident: 10.1016/j.jid.2023.08.008_bib55
  article-title: The intermediate filament system of the keratinizing mouse forestomach epithelium: coexpression of keratins of internal squamous epithelia and of epidermal keratins in differentiating cells
  publication-title: Cell Tissue Res
  doi: 10.1007/BF00221757
  contributor:
    fullname: Schweizer
– volume: 11
  start-page: 123
  year: 2010
  ident: 10.1016/j.jid.2023.08.008_bib21
  article-title: Hemoglobin α and β are ubiquitous in the human lung, decline in idiopathic pulmonary fibrosis but not in COPD
  publication-title: Respir Res
  doi: 10.1186/1465-9921-11-123
  contributor:
    fullname: Ishikawa
– volume: 28
  start-page: 4
  year: 2002
  ident: 10.1016/j.jid.2023.08.008_bib12
  article-title: Sources and measurement of ultraviolet radiation
  publication-title: Methods
  doi: 10.1016/S1046-2023(02)00204-9
  contributor:
    fullname: Diffey
– volume: 25
  start-page: 871
  year: 2018
  ident: 10.1016/j.jid.2023.08.008_bib8
  article-title: Transcriptional programming of normal and inflamed human epidermis at single-cell resolution
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2018.09.006
  contributor:
    fullname: Cheng
– volume: 131
  start-page: 569
  year: 2002
  ident: 10.1016/j.jid.2023.08.008_bib60
  article-title: Generation and application of chicken egg-yolk antibodies
  publication-title: Comp Biochem Physiol A Mol Integr Physiol
  doi: 10.1016/S1095-6433(01)00508-6
  contributor:
    fullname: Tini
– volume: 131
  start-page: 1409
  year: 2011
  ident: 10.1016/j.jid.2023.08.008_bib53
  article-title: The cornified envelope: a first line of defense against reactive oxygen species
  publication-title: J Invest Dermatol
  doi: 10.1038/jid.2011.119
  contributor:
    fullname: Schäfer
– volume: 56
  start-page: 143
  year: 1994
  ident: 10.1016/j.jid.2023.08.008_bib18
  article-title: Expression of keratins in mouse vaginal epithelium
  publication-title: Differentiation
  doi: 10.1046/j.1432-0436.1994.5630143.x
  contributor:
    fullname: Gimenez-Conti
– volume: 288
  year: 2021
  ident: 10.1016/j.jid.2023.08.008_bib4
  article-title: The peptide secreted at the water to land transition in a model amphibian has antioxidant effects
  publication-title: Proc Biol Sci
  contributor:
    fullname: Barbosa
– volume: 106
  start-page: 15454
  year: 2009
  ident: 10.1016/j.jid.2023.08.008_bib6
  article-title: Unexpected expression of alpha- and beta-globin in mesencephalic dopaminergic neurons and glial cells
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.0813216106
  contributor:
    fullname: Biagioli
– volume: 10
  start-page: 1608
  year: 2021
  ident: 10.1016/j.jid.2023.08.008_bib61
  article-title: The role of RBC oxidative stress in sickle cell disease: from the molecular basis to pathologic implications
  publication-title: Antioxidants (Basel)
  doi: 10.3390/antiox10101608
  contributor:
    fullname: Wang
– volume: 17
  start-page: 367
  year: 2004
  ident: 10.1016/j.jid.2023.08.008_bib63
  article-title: Hemoglobin promotes Abeta oligomer formation and localizes in neurons and amyloid deposits
  publication-title: Neurobiol Dis
  doi: 10.1016/j.nbd.2004.08.014
  contributor:
    fullname: Wu
– volume: 41
  start-page: D991
  year: 2013
  ident: 10.1016/j.jid.2023.08.008_bib5
  article-title: NCBI GEO: archive for functional genomics data sets--update
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gks1193
  contributor:
    fullname: Barrett
– volume: 95
  start-page: 4087
  year: 1973
  ident: 10.1016/j.jid.2023.08.008_bib57
  article-title: Reversible binding of nitric oxide and carbon monoxide to iron porphyrins. Assessment of the role of the protein in hemoglobin
  publication-title: J Am Chem Soc
  doi: 10.1021/ja00793a065
  contributor:
    fullname: Stynes
– volume: 94
  start-page: 346
  year: 2019
  ident: 10.1016/j.jid.2023.08.008_bib73
  article-title: 3D in vivo imaging of the keratin filament network in the mouse stratum granulosum reveals profilaggrin-dependent regulation of keratin bundling
  publication-title: J Dermatol Sci
  doi: 10.1016/j.jdermsci.2019.04.006
  contributor:
    fullname: Usui
– volume: 17
  start-page: 1063
  year: 2008
  ident: 10.1016/j.jid.2023.08.008_bib47
  article-title: The skin: an indispensable barrier
  publication-title: Exp Dermatol
  doi: 10.1111/j.1600-0625.2008.00786.x
  contributor:
    fullname: Proksch
– volume: 9
  start-page: 671
  year: 2012
  ident: 10.1016/j.jid.2023.08.008_bib54
  article-title: NIH Image to ImageJ: 25 years of image analysis
  publication-title: Nat Methods
  doi: 10.1038/nmeth.2089
  contributor:
    fullname: Schneider
– volume: 1130
  start-page: 149
  year: 2014
  ident: 10.1016/j.jid.2023.08.008_bib25
  article-title: Preparation of thin frozen sections from nonfixed and undecalcified hard tissues using Kawamot’s film method (2012)
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-62703-989-5_11
  contributor:
    fullname: Kawamoto
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Snippet The epidermis, the keratinized stratified squamous epithelium surrounding the body surface, offers a valuable framework to investigate how terrestrial animals...
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pubmed
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StartPage 2346
SubjectTerms Animals
Carcinoma, Squamous Cell
Epidermis
Female
Hair Follicle
Hemoglobins
Humans
Keratinocytes
Mice
RNA, Messenger - genetics
Title Keratinocytes of the Upper Epidermis and Isthmus of Hair Follicles Express Hemoglobin mRNA and Protein
URI https://www.ncbi.nlm.nih.gov/pubmed/37981423
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