Characterization of 3D organotypic epithelial tissues reveals tonsil-specific differences in tonic interferon signaling.
Journal
PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081
Informations de publication
Date de publication:
2023
2023
Historique:
received:
27
06
2023
accepted:
18
09
2023
medline:
1
11
2023
pubmed:
4
10
2023
entrez:
4
10
2023
Statut:
epublish
Résumé
Three-dimensional (3D) culturing techniques can recapitulate the stratified nature of multicellular epithelial tissues. Organotypic 3D epithelial tissue culture methods have several applications, including the study of tissue development and function, drug discovery and toxicity testing, host-pathogen interactions, and the development of tissue-engineered constructs for use in regenerative medicine. We grew 3D organotypic epithelial tissues from foreskin, cervix, and tonsil-derived primary cells and characterized the transcriptome of these in vitro tissue equivalents. Using the same 3D culturing method, all three tissues yielded stratified squamous epithelium, validated histologically using basal and superficial epithelial cell markers. The goal of this study was to use RNA-seq to compare gene expression patterns in these three types of epithelial tissues to gain a better understanding of the molecular mechanisms underlying their function and identify potential therapeutic targets for various diseases. Functional profiling by over-representation and gene set enrichment analysis revealed tissue-specific differences: i.e., cutaneous homeostasis and lipid metabolism in foreskin, extracellular matrix remodeling in cervix, and baseline innate immune differences in tonsil. Specifically, tonsillar epithelia may play an active role in shaping the immune microenvironment of the tonsil balancing inflammation and immune responses in the face of constant exposure to microbial insults. Overall, these data serve as a resource, with gene sets made available for the research community to explore, and as a foundation for understanding the epithelial heterogeneity and how it may impact their in vitro use. An online resource is available to investigate these data (https://viz.datascience.arizona.edu/3DEpiEx/).
Identifiants
pubmed: 37792852
doi: 10.1371/journal.pone.0292368
pii: PONE-D-23-19376
pmc: PMC10550192
doi:
Substances chimiques
Interferons
9008-11-1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0292368Subventions
Organisme : NIDCR NIH HHS
ID : R03 DE030211
Pays : United States
Commentaires et corrections
Type : UpdateOf
Informations de copyright
Copyright: © 2023 Jackson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Biol Reprod. 2020 Aug 21;103(3):497-507
pubmed: 32401296
J Virol. 2017 Nov 30;91(24):
pubmed: 29021401
F1000Res. 2020 Jul 15;9:
pubmed: 33564394
Diabetes. 2003 Sep;52(9):2296-303
pubmed: 12941769
Acta Anat (Basel). 1961;46:244-76
pubmed: 13891432
BMC Bioinformatics. 2017 May 3;18(1):234
pubmed: 28468606
Science. 2015 Jan 23;347(6220):1260419
pubmed: 25613900
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Am J Physiol Lung Cell Mol Physiol. 2010 Jan;298(1):L15-22
pubmed: 19783639
Toxicol Appl Pharmacol. 2015 Aug 15;287(1):35-42
pubmed: 26028481
Mol Med. 2018 May 16;24(1):23
pubmed: 30134802
Differentiation. 2017 Sep - Oct;97:9-22
pubmed: 28918284
Innovation (Camb). 2021 Jul 01;2(3):100141
pubmed: 34557778
BMC Bioinformatics. 2018 Nov 6;19(1):404
pubmed: 30400809
Adv Anat Embryol Cell Biol. 2012;212:v, vii, 1-115
pubmed: 22894052
Semin Cell Dev Biol. 2010 May;21(3):325-32
pubmed: 20144910
BMC Res Notes. 2018 Oct 25;11(1):763
pubmed: 30359291
Gen Pharmacol. 1996 Jul;27(5):761-71
pubmed: 8842677
J Immunol. 2019 Apr 1;202(7):2069-2081
pubmed: 30760619
Cell. 2016 Jan 28;164(3):564-78
pubmed: 26824662
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2610-5
pubmed: 12604793
Differentiation. 1992 Mar;49(2):101-7
pubmed: 1597255
J Invest Dermatol. 1983 Jul;81(1 Suppl):2s-10s
pubmed: 6306115
In Vitro Cell Dev Biol Anim. 2021 Feb;57(2):160-173
pubmed: 33237403
Mech Dev. 1998 Jan;70(1-2):133-45
pubmed: 9510030
Exp Biol Med (Maywood). 2011 Jul;236(7):832-43
pubmed: 21676921
J Invest Dermatol. 2005 May;124(5):990-7
pubmed: 15854041
J Vis Exp. 2012 Feb 22;(60):
pubmed: 22395296
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Viruses. 2015 Jul 16;7(7):3863-90
pubmed: 26193301
Genome Biol. 2014;15(12):550
pubmed: 25516281
Curr Protoc Microbiol. 2014 May 01;33:14B.2.1-13
pubmed: 24789595
Bioinformatics. 2014 Feb 01;30(3):301-4
pubmed: 24319002
J Virol. 2019 Aug 13;93(17):
pubmed: 31189705
Discov Med. 2013 Sep;16(87):123-31
pubmed: 23998448
Fertil Steril. 1973 Mar;24(3):198-201
pubmed: 4691362
Cell Rep. 2018 Oct 23;25(4):871-883
pubmed: 30355494
Biol Reprod. 1997 Apr;56(4):999-1011
pubmed: 9096884
J Dent. 2022 Oct;125:104251
pubmed: 35961474
Inflamm Regen. 2018 Dec 7;38:31
pubmed: 30546811
Nucleic Acids Res. 2019 Jul 2;47(W1):W191-W198
pubmed: 31066453
PLoS One. 2019 Jan 9;14(1):e0207898
pubmed: 30625134
Virology. 1999 Sep 30;262(2):344-54
pubmed: 10502513
Acta Otorhinolaryngol Belg. 2000;54(3):237-41
pubmed: 11082757
J Clin Oncol. 2011 Nov 10;29(32):4294-301
pubmed: 21969503
Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3062-7
pubmed: 8610168
Methods Enzymol. 2016;569:287-308
pubmed: 26778564
Gene. 1993 Dec 15;135(1-2):215-21
pubmed: 7903947
J Invest Dermatol. 1992 Mar;98(3):279-89
pubmed: 1545137
Antiviral Res. 2010 Mar;85(3):431-49
pubmed: 19883696
J Cell Mol Med. 2019 Feb;23(2):1375-1385
pubmed: 30565387
NPJ Biofilms Microbiomes. 2021 Dec 13;7(1):88
pubmed: 34903740
Immunity. 2012 Feb 24;36(2):166-74
pubmed: 22365663
Cell Death Dis. 2022 Oct 22;13(10):894
pubmed: 36272970
J Gen Virol. 2018 Aug;99(8):989-990
pubmed: 29927370
Am J Respir Cell Mol Biol. 2003 Feb;28(2):142-9
pubmed: 12540481
Cell. 1975 Nov;6(3):331-43
pubmed: 1052771
Proc Natl Acad Sci U S A. 2005 Oct 11;102(41):14611-6
pubmed: 16195385
Genome Res. 2014 May;24(5):869-84
pubmed: 24515121
Clin Microbiol Rev. 1995 Apr;8(2):240-59
pubmed: 7621400
Science. 1981 Mar 6;211(4486):1052-4
pubmed: 7008197
Acta Derm Venereol. 2002;82(2):118-20
pubmed: 12125939
Nat Rev Microbiol. 2018 Apr;16(4):226-240
pubmed: 29430011
Exp Dermatol. 1996 Feb;5(1):1-11
pubmed: 8624605
Immunology. 2020 Jun;160(2):171-182
pubmed: 32196653
Histochem Cell Biol. 2000 Oct;114(4):311-21
pubmed: 11131096
Curr Opin Cell Biol. 2016 Dec;43:22-29
pubmed: 27474805
J Exp Med. 2016 May 2;213(5):733-50
pubmed: 27069113
Nat Genet. 2013 Jun;45(6):580-5
pubmed: 23715323
Front Immunol. 2017 Feb 03;8:45
pubmed: 28217126
PLoS One. 2020 Mar 18;15(3):e0229778
pubmed: 32187186
Genome Res. 2008 Sep;18(9):1509-17
pubmed: 18550803
Proc Natl Acad Sci U S A. 1979 Mar;76(3):1274-8
pubmed: 286310
Immunity. 2012 Jul 27;37(1):158-70
pubmed: 22705104
Curr Protoc Microbiol. 2014 Aug 01;34:14B.3.1-18
pubmed: 25082004
Genome Res. 1998 Mar;8(3):186-94
pubmed: 9521922
Blood. 2000 Apr 15;95(8):2691-8
pubmed: 10753852
J Natl Cancer Inst Monogr. 2001;(29):7-15
pubmed: 11694559
Genes Dev. 1992 Jul;6(7):1131-42
pubmed: 1321068
Nat Commun. 2019 Jul 2;10(1):2921
pubmed: 31266943
J Invest Dermatol. 1983 Jul;81(1 Suppl):189s-94s
pubmed: 6863990
Nat Rev Immunol. 2009 Oct;9(10):679-91
pubmed: 19763149
Best Pract Res Clin Obstet Gynaecol. 2014 Oct;28(7):1098-110
pubmed: 25153069
Arthritis Rheum. 2005 May;52(5):1491-503
pubmed: 15880830
Database (Oxford). 2013 Jul 09;2013:bat054
pubmed: 23842463
Am J Physiol Gastrointest Liver Physiol. 2010 Jun;298(6):G807-19
pubmed: 20299599
Cold Spring Harb Perspect Med. 2012 Jun;2(6):a009563
pubmed: 22675668
Adv Drug Deliv Rev. 1998 Dec 1;34(2-3):135-154
pubmed: 10837675
BMC Bioinformatics. 2019 Jun 13;20(1):331
pubmed: 31195976
Philos Trans R Soc Lond B Biol Sci. 2019 May 27;374(1773):20180289
pubmed: 30955493
Nat Rev Endocrinol. 2015 Jan;11(1):29-42
pubmed: 25350068
Annu Rev Virol. 2019 Sep 29;6(1):567-584
pubmed: 31283436
Nat Rev Immunol. 2015 Feb;15(2):87-103
pubmed: 25614319
Dev Biol. 1997 Feb 1;182(1):5-20
pubmed: 9073437
Mol Vis. 2014 Nov 04;20:1491-517
pubmed: 25489224
Nucleic Acids Res. 2021 Jan 8;49(D1):D939-D946
pubmed: 33152070
Stem Cell Res Ther. 2014 Apr 28;5(2):60
pubmed: 24774536
Nucleic Acids Res. 2015 Jul 1;43(W1):W589-98
pubmed: 25897122
Nat Methods. 2015 Apr;12(4):357-60
pubmed: 25751142
Int J Pediatr Otorhinolaryngol. 1983 Sep;6(1):61-75
pubmed: 6607904
Exp Mol Pathol. 2020 Aug;115:104441
pubmed: 32289285
Nucleic Acids Res. 2020 Nov 4;48(19):e113
pubmed: 32997146
Curr Protoc. 2022 Sep;2(9):e536
pubmed: 36165649
Nucleic Acids Res. 2022 Jan 7;50(D1):D988-D995
pubmed: 34791404
PLoS Biol. 2010 Apr 27;8(4):e1000361
pubmed: 20436908
Viruses. 2020 Dec 01;12(12):
pubmed: 33271909
Viruses. 2021 Jan 06;13(1):
pubmed: 33418959
J Clin Invest. 2010 Jul;120(7):2619-26
pubmed: 20516646
Curr Protoc Microbiol. 2020 Dec;59(1):e129
pubmed: 33232584
J Anat. 1994 Aug;185 ( Pt 1):111-27
pubmed: 7559106
J Immunol. 2002 Sep 1;169(5):2381-9
pubmed: 12193705
Carbohydr Polym. 2015 Mar 15;118:9-15
pubmed: 25542100
Curr Top Dev Biol. 2018;128:237-266
pubmed: 29477165
Biol Reprod. 2010 Mar;82(3):617-27
pubmed: 20007410
PLoS One. 2008 Jun 04;3(6):e2308
pubmed: 18523637
J Invest Dermatol. 2001 Jun;116(6):905-9
pubmed: 11407979
J Pathol. 2009 Nov;219(3):383-91
pubmed: 19718710
J Infect Dis. 2014 Jun 15;209(12):1989-99
pubmed: 24403560
Biol Reprod. 1997 Dec;57(6):1338-45
pubmed: 9408238
Histopathology. 2001 Oct;39(4):386-9
pubmed: 11683939
Science. 1992 Aug 14;257(5072):971-3
pubmed: 1323879
J Histochem Cytochem. 2004 Dec;52(12):1627-38
pubmed: 15557217
Am J Pathol. 1991 Mar;138(3):673-85
pubmed: 1848042
Cell. 1975 Nov;6(3):317-30
pubmed: 1052770
Eur J Immunol. 2013 May;43(5):1264-73
pubmed: 23436642
Virology. 2002 Sep 30;301(2):247-54
pubmed: 12359427
Proc Natl Acad Sci U S A. 2003 Sep 30;100 Suppl 1:11830-5
pubmed: 12913119
J Invest Dermatol. 2002 Apr;118(4):678-85
pubmed: 11918716
Genome Biol. 2016 Aug 23;17(1):177
pubmed: 27552985
J Exp Med. 2003 Mar 17;197(6):711-23
pubmed: 12642603
Genes Dev. 1998 Sep 1;12(17):2735-47
pubmed: 9732271
Biomol Ther (Seoul). 2017 May 1;25(3):296-307
pubmed: 28365978