Skin single-cell transcriptomics reveals a core of sebaceous gland-relevant genes shared by mice and humans.

Bioinformatics Sebaceous gland Single-cell transcriptomics Skin

Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
03 Feb 2024
Historique:
received: 18 10 2023
accepted: 11 01 2024
medline: 4 2 2024
pubmed: 4 2 2024
entrez: 3 2 2024
Statut: epublish

Résumé

Single-cell RNA sequencing (scRNA-seq) has been widely applied to dissect cellular heterogeneity in normal and diseased skin. Sebaceous glands, essential skin components with established functions in maintaining skin integrity and emerging roles in systemic energy metabolism, have been largely neglected in scRNA-seq studies. Departing from mouse and human skin scRNA-seq datasets, we identified gene sets expressed especially in sebaceous glands with the open-source R-package oposSOM. The identified gene sets included sebaceous gland-typical genes as Scd3, Mgst1, Cidea, Awat2 and KRT7. Surprisingly, however, there was not a single overlap among the 100 highest, exclusively in sebaceous glands expressed transcripts in mouse and human samples. Notably, both species share a common core of only 25 transcripts, including mitochondrial and peroxisomal genes involved in fatty acid, amino acid, and glucose processing, thus highlighting the intense metabolic rate of this gland. This study highlights intrinsic differences in sebaceous lipid synthesis between mice and humans, and indicates an important role for peroxisomal processes in this context. Our data also provides attractive starting points for experimentally addressing novel candidates regulating sebaceous gland homeostasis.

Sections du résumé

BACKGROUND BACKGROUND
Single-cell RNA sequencing (scRNA-seq) has been widely applied to dissect cellular heterogeneity in normal and diseased skin. Sebaceous glands, essential skin components with established functions in maintaining skin integrity and emerging roles in systemic energy metabolism, have been largely neglected in scRNA-seq studies.
METHODS METHODS
Departing from mouse and human skin scRNA-seq datasets, we identified gene sets expressed especially in sebaceous glands with the open-source R-package oposSOM.
RESULTS RESULTS
The identified gene sets included sebaceous gland-typical genes as Scd3, Mgst1, Cidea, Awat2 and KRT7. Surprisingly, however, there was not a single overlap among the 100 highest, exclusively in sebaceous glands expressed transcripts in mouse and human samples. Notably, both species share a common core of only 25 transcripts, including mitochondrial and peroxisomal genes involved in fatty acid, amino acid, and glucose processing, thus highlighting the intense metabolic rate of this gland.
CONCLUSIONS CONCLUSIONS
This study highlights intrinsic differences in sebaceous lipid synthesis between mice and humans, and indicates an important role for peroxisomal processes in this context. Our data also provides attractive starting points for experimentally addressing novel candidates regulating sebaceous gland homeostasis.

Identifiants

pubmed: 38310227
doi: 10.1186/s12864-024-10008-8
pii: 10.1186/s12864-024-10008-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

137

Informations de copyright

© 2024. The Author(s).

Références

Watt FM. Mammalian skin cell biology: at the interface between laboratory and clinic. Science. 2014;346:937–40. https://doi.org/10.1126/science.1253734 .
doi: 10.1126/science.1253734 pubmed: 25414300
Hsu Y-C, Fuchs E. Building and Maintaining the Skin. Cold Spring Harb Perspect Biol. 2022. https://doi.org/10.1101/cshperspect.a040840 .
doi: 10.1101/cshperspect.a040840 pubmed: 34607830
Rognoni E, Watt FM. Skin Cell Heterogeneity in Development, Wound Healing, and Cancer. Trends Cell Biol. 2018;28:709–22. https://doi.org/10.1016/j.tcb.2018.05.002 .
doi: 10.1016/j.tcb.2018.05.002 pubmed: 29807713 pmcid: 6098245
Joost S, Annusver K, Jacob T, Sun X, Dalessandri T, Sivan U, et al. The Molecular Anatomy of Mouse Skin during Hair Growth and Rest. Cell Stem Cell. 2020;26:441-457.e7. https://doi.org/10.1016/j.stem.2020.01.012 .
doi: 10.1016/j.stem.2020.01.012 pubmed: 32109378
Jovic D, Liang X, Zeng H, Lin L, Xu F, Luo Y. Single-cell RNA sequencing technologies and applications: A brief overview. Clin Transl Med. 2022;12: e694. https://doi.org/10.1002/ctm2.694 .
doi: 10.1002/ctm2.694 pubmed: 35352511 pmcid: 8964935
Theocharidis G, Tekkela S, Veves A, McGrath JA, Onoufriadis A. Single-cell transcriptomics in human skin research: available technologies, technical considerations and disease applications. Exp Dermatol. 2022;31:655–73. https://doi.org/10.1111/exd.14547 .
doi: 10.1111/exd.14547 pubmed: 35196402 pmcid: 9311140
Negri VA, Watt FM. Understanding Human Epidermal Stem Cells at Single-Cell Resolution. J Invest Dermatol. 2022;142:2061–7. https://doi.org/10.1016/j.jid.2022.04.003 .
doi: 10.1016/j.jid.2022.04.003 pubmed: 35570025 pmcid: 9826868
Srivastava A, Bencomo T, Das I, Lee CS. Unravelling the landscape of skin cancer through single-cell transcriptomics. Transl Oncol. 2023;27: 101557. https://doi.org/10.1016/j.tranon.2022.101557 .
doi: 10.1016/j.tranon.2022.101557 pubmed: 36257209
Joost S, Zeisel A, Jacob T, Sun X, La Manno G, Lönnerberg P, et al. Single-Cell Transcriptomics Reveals that Differentiation and Spatial Signatures Shape Epidermal and Hair Follicle Heterogeneity. Cell Syst. 2016;3:221-237.e9. https://doi.org/10.1016/j.cels.2016.08.010 .
doi: 10.1016/j.cels.2016.08.010 pubmed: 27641957 pmcid: 5052454
Haensel D, Jin S, Sun P, Cinco R, Dragan M, Nguyen Q, et al. Defining Epidermal Basal Cell States during Skin Homeostasis and Wound Healing Using Single-Cell Transcriptomics. Cell Rep. 2020;30:3932-3947.e6. https://doi.org/10.1016/j.celrep.2020.02.091 .
doi: 10.1016/j.celrep.2020.02.091 pubmed: 32187560 pmcid: 7218802
Lin Z, Jin S, Chen J, Li Z, Lin Z, Tang L, et al. Murine interfollicular epidermal differentiation is gradualistic with GRHL3 controlling progression from stem to transition cell states. Nat Commun. 2020;11:5434. https://doi.org/10.1038/s41467-020-19234-6 .
doi: 10.1038/s41467-020-19234-6 pubmed: 33116143 pmcid: 7595230
Dahlhoff M, Camera E, Schafer M, Emrich D, Riethmacher D, Foster A, et al. Sebaceous lipids are essential for water repulsion, protection against UVB-induced apoptosis and ocular integrity in mice. Development. 2016;143:1823–31. https://doi.org/10.1242/dev.132753 .
doi: 10.1242/dev.132753 pubmed: 26989175
Schneider MR, Paus R. Sebocytes, multifaceted epithelial cells: lipid production and holocrine secretion. Int J Biochem Cell Biol. 2010;42:181–5.
doi: 10.1016/j.biocel.2009.11.017 pubmed: 19944183
Zouboulis CC, Picardo M, Ju Q, Kurokawa I, Torocsik D, Biro T, Schneider MR. Beyond acne: Current aspects of sebaceous gland biology and function. Rev Endocr Metab Disord. 2016;17:319–34. https://doi.org/10.1007/s11154-016-9389-5 .
doi: 10.1007/s11154-016-9389-5 pubmed: 27726049
Schneider MR. Lipid droplets and associated proteins in sebocytes. Exp Cell Res. 2016;340:205–8.
doi: 10.1016/j.yexcr.2015.11.008 pubmed: 26571075
Smith KR, Thiboutot DM. Thematic review series: skin lipids Sebaceous gland lipids friend or foe? J Lipid Res. 2008;49:271–81.
doi: 10.1194/jlr.R700015-JLR200 pubmed: 17975220
Stewart ME. Sebaceous gland lipids. Semin Dermatol. 1992;11:100–5.
pubmed: 1498012
Pappas A. Epidermal surface lipids. Dermatoendocrinol. 2009;1:72–6.
doi: 10.4161/derm.1.2.7811 pubmed: 20224687 pmcid: 2835894
Nicolaides N. Skin lipids: their biochemical uniqueness. Science. 1974;186:19–26.
doi: 10.1126/science.186.4158.19 pubmed: 4607408
Zouboulis CC, Coenye T, He L, Kabashima K, Kobayashi T, Niemann C, et al. Sebaceous immunobiology - skin homeostasis, pathophysiology, coordination of innate immunity and inflammatory response and disease associations. Front Immunol. 2022;13:1029818. https://doi.org/10.3389/fimmu.2022.1029818 .
doi: 10.3389/fimmu.2022.1029818 pubmed: 36439142 pmcid: 9686445
Güell M, Schneider MR. In preprints: progress in sebaceous gland homeostasis, regeneration and immunomodulatory functions. Development. 2023. https://doi.org/10.1242/dev.202177 .
doi: 10.1242/dev.202177 pubmed: 37522362
Clayton RW, Langan EA, Ansell DM, de Vos I, Gobel K, Schneider MR, et al. Neuroendocrinology and neurobiology of sebaceous glands. Biol Rev Camb Philos Soc. 2020;95:592–624. https://doi.org/10.1111/brv.12579 .
doi: 10.1111/brv.12579 pubmed: 31970855
Vietri Rudan M, Mishra A, Klose C, Eggert US, Watt FM. Human epidermal stem cell differentiation is modulated by specific lipid subspecies. Proc Natl Acad Sci U S A. 2020;117:22173–82. https://doi.org/10.1073/pnas.2011310117 .
doi: 10.1073/pnas.2011310117 pubmed: 32843345 pmcid: 7486749
Inoue T, Kuwano T, Uehara Y, Yano M, Oya N, Takada N, et al. Non-invasive human skin transcriptome analysis using mRNA in skin surface lipids. Commun Biol. 2022;5:215. https://doi.org/10.1038/s42003-022-03154-w .
doi: 10.1038/s42003-022-03154-w pubmed: 35264722 pmcid: 8907185
Harris JC, Prouty SM, Nelson MA, Sung DC, Nelson AM, Seykora JT, et al. Laser Capture Microdissection-based RNAseq for Profiling Mouse and Human Sebaceous Gland Transcriptomes. J Invest Dermatol. 2023. https://doi.org/10.1016/j.jid.2023.10.017 .
doi: 10.1016/j.jid.2023.10.017 pubmed: 37979774
Veniaminova NA, Jia Y, Hartigan AM, Huyge TJ, Tsai S-Y, Grachtchouk M, et al. Distinct mechanisms for sebaceous gland self-renewal and regeneration provide durability in response to injury. bioRxiv 2023. doi: https://doi.org/10.1101/2023.05.05.539454 .
Han X, Wang R, Zhou Y, Fei L, Sun H, Lai S, et al. Mapping the Mouse Cell Atlas by Microwell-Seq. Cell. 2018;172:1091-1107.e17. https://doi.org/10.1016/j.cell.2018.02.001 .
doi: 10.1016/j.cell.2018.02.001 pubmed: 29474909
Wang S, Drummond ML, Guerrero-Juarez CF, Tarapore E, MacLean AL, Stabell AR, et al. Single cell transcriptomics of human epidermis identifies basal stem cell transition states. Nat Commun. 2020;11:4239. https://doi.org/10.1038/s41467-020-18075-7 .
doi: 10.1038/s41467-020-18075-7 pubmed: 32843640 pmcid: 7447770
Solé-Boldo L, Raddatz G, Schütz S, Mallm J-P, Rippe K, Lonsdorf AS, et al. Single-cell transcriptomes of the human skin reveal age-related loss of fibroblast priming. Commun Biol. 2020;3:188. https://doi.org/10.1038/s42003-020-0922-4 .
doi: 10.1038/s42003-020-0922-4 pubmed: 32327715 pmcid: 7181753
Cheng JB, Sedgewick AJ, Finnegan AI, Harirchian P, Lee J, Kwon S, et al. Transcriptional Programming of Normal and Inflamed Human Epidermis at Single-Cell Resolution. Cell Rep. 2018;25:871–83. https://doi.org/10.1016/j.celrep.2018.09.006 .
doi: 10.1016/j.celrep.2018.09.006 pubmed: 30355494 pmcid: 6367716
R Core Team. R: A Language and Environment for Statistical Computing. 2016. https://www.r-project.org/ .
Durinck S, Spellman PT, Birney E, Huber W. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat Protoc. 2009;4:1184–91. https://doi.org/10.1038/nprot.2009.97 .
doi: 10.1038/nprot.2009.97 pubmed: 19617889 pmcid: 3159387
Löffler-Wirth H, Kalcher M, Binder H. oposSOM: R-package for high-dimensional portraying of genome-wide expression landscapes on bioconductor. Bioinformatics. 2015;31:3225–7. https://doi.org/10.1093/bioinformatics/btv342 .
doi: 10.1093/bioinformatics/btv342 pubmed: 26063839
Wickham H. ggplot2: Elegant Graphics for Data Analysis. New York: Springer Verlag; 2016.
doi: 10.1007/978-3-319-24277-4
Klemm F, Maas RR, Bowman RL, Kornete M, Soukup K, Nassiri S, et al. Interrogation of the Microenvironmental Landscape in Brain Tumors Reveals Disease-Specific Alterations of Immune Cells. Cell. 2020;181:1643-1660.e17. https://doi.org/10.1016/j.cell.2020.05.007 .
doi: 10.1016/j.cell.2020.05.007 pubmed: 32470396 pmcid: 8558904
Herberg M, Siebert S, Quaas M, Thalheim T, Rother K, Hussong M, et al. Loss of Msh2 and a single-radiation hit induce common, genome-wide, and persistent epigenetic changes in the intestine. Clin Epigenetics. 2019;11:65. https://doi.org/10.1186/s13148-019-0639-8 .
doi: 10.1186/s13148-019-0639-8 pubmed: 31029155 pmcid: 6486978
Ma K-Y, Schonnesen AA, Brock A, van den Berg C, Eckhardt SG, Liu Z, Jiang N. Single-cell RNA sequencing of lung adenocarcinoma reveals heterogeneity of immune response-related genes. JCI Insight. 2019. https://doi.org/10.1172/jci.insight.121387 .
doi: 10.1172/jci.insight.121387 pubmed: 31723057 pmcid: 6948870
Schmidt M, Mortensen LS, Loeffler-Wirth H, Kosnopfel C, Krohn K, Binder H, Kunz M. Single-cell trajectories of melanoma cell resistance to targeted treatment. Cancer Biol Med. 2021;19:56–73. https://doi.org/10.20892/j.issn.2095-3941.2021.0267 .
doi: 10.20892/j.issn.2095-3941.2021.0267 pubmed: 34591417 pmcid: 8763000
Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics Tissue-based map of the human proteome. Science. 2015;347:1260419.
doi: 10.1126/science.1260419 pubmed: 25613900
Sipilä K, Rognoni E, Jokinen J, Tewary M, Vietri Rudan M, Talvi S, et al. Embigin is a fibronectin receptor that affects sebaceous gland differentiation and metabolism. Dev Cell. 2022;57:1453-1465.e7. https://doi.org/10.1016/j.devcel.2022.05.011 .
doi: 10.1016/j.devcel.2022.05.011 pubmed: 35671757 pmcid: 9616737
Kobayashi T, Voisin B, Kim DY, Kennedy EA, Jo J-H, Shih H-Y, et al. Homeostatic Control of Sebaceous Glands by Innate Lymphoid Cells Regulates Commensal Bacteria Equilibrium. Cell. 2019;176:982-997.e16. https://doi.org/10.1016/j.cell.2018.12.031 .
doi: 10.1016/j.cell.2018.12.031 pubmed: 30712873 pmcid: 6532063
Schneider MR, Zhang S, Li P. Lipid droplets and associated proteins in the skin: Basic research and clinical perspectives. Arch Dermatol Res. 2016;308:1–6.
Turkish AR, Henneberry AL, Cromley D, Padamsee M, Oelkers P, Bazzi H, et al. Identification of two novel human acyl-CoA wax alcohol acyltransferases: members of the diacylglycerol acyltransferase 2 (DGAT2) gene superfamily. J Biol Chem. 2005;280:14755–64. https://doi.org/10.1074/jbc.M500025200 .
doi: 10.1074/jbc.M500025200 pubmed: 15671038
Hinde E, Haslam IS, Schneider MR, Langan EA, Kloepper JE, Schramm C, et al. A practical guide for the study of human and murine sebaceous glands in situ. Exp Dermatol. 2013;22:631–7. https://doi.org/10.1111/exd.12207 .
doi: 10.1111/exd.12207 pubmed: 24079731
Mathieu C, La Li de Sierra-Gallay I, Duval R, Xu X, Cocaign A, Léger T, et al Insights into Brain Glycogen Metabolism: THE STRUCTURE OF HUMAN BRAIN GLYCOGEN PHOSPHORYLASE 2016;291:18072–83. doi: https://doi.org/10.1074/jbc.M116.738898 .
Montagna W, CHASE HB, HAMILTON JB. The distribution of glycogen and lipids in human skin. J Invest Dermatol. 1951;17:147–57. https://doi.org/10.1038/jid.1951.75 .
doi: 10.1038/jid.1951.75 pubmed: 14880730
Downie MM, Kealey T. Lipogenesis in the human sebaceous gland: glycogen and glycerophosphate are substrates for the synthesis of sebum lipids. J Invest Dermatol. 1998;111:199–205. https://doi.org/10.1046/j.1523-1747.1998.00264.x .
doi: 10.1046/j.1523-1747.1998.00264.x pubmed: 9699717
Figlak K, Williams G, Bertolini M, Paus R, Philpott MP. Human hair follicles operate an internal Cori cycle and modulate their growth via glycogen phosphorylase. Sci Rep. 2021;11:20761. https://doi.org/10.1038/s41598-021-99652-8 .
doi: 10.1038/s41598-021-99652-8 pubmed: 34675331 pmcid: 8531296
Reichenbach B, Classon J, Aida T, Tanaka K, Genander M, Göritz C. Glutamate transporter Slc1a3 mediates inter-niche stem cell activation during skin growth. EMBO J. 2018. https://doi.org/10.15252/embj.201798280 .
doi: 10.15252/embj.201798280 pubmed: 29615452 pmcid: 5920238
Okumoto K, Tamura S, Honsho M, Fujiki Y. Peroxisome: Metabolic Functions and Biogenesis. Adv Exp Med Biol. 2020;1299:3–17. https://doi.org/10.1007/978-3-030-60204-8_1 .
doi: 10.1007/978-3-030-60204-8_1 pubmed: 33417203
Gorgas K, Völkl A. Peroxisomes in sebaceous glands. IV. Aggregates of tubular peroxisomes in the mouse Meibomian gland. Histochem J. 1984;16:1079–98. doi: https://doi.org/10.1007/BF01002896 .
Zhang F, Zhang Y, Deng Z, Xu P, Zhang X, Jin T, Liu Q. Genetic variants in the acylphosphatase 2 gene and the risk of breast cancer in a Han Chinese population. Oncotarget. 2016;7:86704–12. https://doi.org/10.18632/oncotarget.13495 .
doi: 10.18632/oncotarget.13495 pubmed: 27894080 pmcid: 5349947
Albrektsen T, Richter HE, Clausen JT, Fleckner J. Identification of a novel integral plasma membrane protein induced during adipocyte differentiation. Biochem J. 2001;359:393–402. https://doi.org/10.1042/0264-6021:3590393 .
doi: 10.1042/0264-6021:3590393 pubmed: 11583587 pmcid: 1222159
Eguchi J, Wada J, Hida K, Zhang H, Matsuoka T, Baba M, et al. Identification of adipocyte adhesion molecule (ACAM), a novel CTX gene family, implicated in adipocyte maturation and development of obesity. Biochem J. 2005;387:343–53. https://doi.org/10.1042/BJ20041709 .
doi: 10.1042/BJ20041709 pubmed: 15563274 pmcid: 1134962
Bai N, Lu X, Jin L, Alimujiang M, Ma J, Hu F, et al. CLSTN3 gene variant associates with obesity risk and contributes to dysfunction in white adipose tissue. Mol Metab. 2022;63: 101531. https://doi.org/10.1016/j.molmet.2022.101531 .
doi: 10.1016/j.molmet.2022.101531 pubmed: 35753632 pmcid: 9254126
Leonard AE, Bobik EG, Dorado J, Kroeger PE, Chuang LT, Thurmond JM, et al. Cloning of a human cDNA encoding a novel enzyme involved in the elongation of long-chain polyunsaturated fatty acids. Biochem J. 2000;350(Pt 3):765–70.
doi: 10.1042/bj3500765 pubmed: 10970790 pmcid: 1221308
Jääskeläinen T, Makkonen H, Palvimo JJ. Steroid up-regulation of FKBP51 and its role in hormone signaling. Curr Opin Pharmacol. 2011;11:326–31. https://doi.org/10.1016/j.coph.2011.04.006 .
doi: 10.1016/j.coph.2011.04.006 pubmed: 21531172
Wanders RJA, Duran M, Loupatty FJ. Enzymology of the branched-chain amino acid oxidation disorders: the valine pathway. J Inherit Metab Dis. 2012;35:5–12. https://doi.org/10.1007/s10545-010-9236-x .
doi: 10.1007/s10545-010-9236-x pubmed: 21104317
Wirnsberger G, Zwolanek F, Stadlmann J, Tortola L, Liu SW, Perlot T, et al. Jagunal homolog 1 is a critical regulator of neutrophil function in fungal host defense. Nat Genet. 2014;46:1028–33. https://doi.org/10.1038/ng.3070 .
doi: 10.1038/ng.3070 pubmed: 25129145 pmcid: 6245568
Lagrost L, Masson D. The expanding role of lyso-phosphatidylcholine acyltransferase-3 (LPCAT3), a phospholipid remodeling enzyme, in health and disease. Curr Opin Lipidol. 2022;33:193–8. https://doi.org/10.1097/MOL.0000000000000820 .
doi: 10.1097/MOL.0000000000000820 pubmed: 35165232
Chu C-H, Cheng D. Expression, purification, characterization of human 3-methylcrotonyl-CoA carboxylase (MCCC). Protein Expr Purif. 2007;53:421–7. https://doi.org/10.1016/j.pep.2007.01.012 .
doi: 10.1016/j.pep.2007.01.012 pubmed: 17360195
Chen Y-Y, Zhang X-N, Xu C-Z, Zhou D-H, Chen J, Liu Z-X, et al. MCCC2 promotes HCC development by supporting leucine oncogenic function. Cancer Cell Int. 2021;21:22. https://doi.org/10.1186/s12935-020-01722-w .
doi: 10.1186/s12935-020-01722-w pubmed: 33407468 pmcid: 7788835
Kara M, Axton RA, Jackson M, Ghaffari S, Buerger K, Watt AJ, et al. A Role for MOSPD1 in Mesenchymal Stem Cell Proliferation and Differentiation. Stem Cells. 2015;33:3077–86. https://doi.org/10.1002/stem.2102 .
doi: 10.1002/stem.2102 pubmed: 26175344
Koch J, Pranjic K, Huber A, Ellinger A, Hartig A, Kragler F, Brocard C. PEX11 family members are membrane elongation factors that coordinate peroxisome proliferation and maintenance. J Cell Sci. 2010;123:3389–400. https://doi.org/10.1242/jcs.064907 .
doi: 10.1242/jcs.064907 pubmed: 20826455
Kim PK, Mullen RT, Schumann U, Lippincott-Schwartz J. The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER. J Cell Biol. 2006;173:521–32. https://doi.org/10.1083/jcb.200601036 .
doi: 10.1083/jcb.200601036 pubmed: 16717127 pmcid: 2063862
Gakh O, Cavadini P, Isaya G. Mitochondrial processing peptidases. Biochim Biophys Acta. 2002;1592:63–77. https://doi.org/10.1016/s0167-4889(02)00265-3 .
doi: 10.1016/s0167-4889(02)00265-3 pubmed: 12191769
Shivalingappa PKM, Sharma V, Shiras A, Bapat SA. RNA binding motif 47 (RBM47): emerging roles in vertebrate development, RNA editing and cancer. Mol Cell Biochem. 2021;476:4493–505. https://doi.org/10.1007/s11010-021-04256-5 .
doi: 10.1007/s11010-021-04256-5 pubmed: 34499322
Didier C, Broday L, Bhoumik A, Israeli S, Takahashi S, Nakayama K, et al. RNF5, a RING finger protein that regulates cell motility by targeting paxillin ubiquitination and altered localization. Mol Cell Biol. 2003;23:5331–45. https://doi.org/10.1128/MCB.23.15.5331-5345.2003 .
doi: 10.1128/MCB.23.15.5331-5345.2003 pubmed: 12861019 pmcid: 165736
Ott C, Ross K, Straub S, Thiede B, Götz M, Goosmann C, et al. Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. Mol Cell Biol. 2012;32:1173–88. https://doi.org/10.1128/MCB.06388-11 .
doi: 10.1128/MCB.06388-11 pubmed: 22252321 pmcid: 3295012
Torriglia A, Martin E, Jaadane I. The hidden side of SERPINB1/Leukocyte Elastase Inhibitor. Semin Cell Dev Biol. 2017;62:178–86. https://doi.org/10.1016/j.semcdb.2016.07.010 .
doi: 10.1016/j.semcdb.2016.07.010 pubmed: 27422329
Krycer JR, Fazakerley DJ, Cater RJ, CThomas K, Naghiloo S, Burchfield JG, et al. The amino acid transporter, SLC1A3, is plasma membrane-localised in adipocytes and its activity is insensitive to insulin. FEBS Lett. 2017;591:322–30. https://doi.org/10.1002/1873-3468.12549 .
doi: 10.1002/1873-3468.12549 pubmed: 28032905
Navarro-Imaz H, Ochoa B, García-Arcos I, Martínez MJ, Chico Y, Fresnedo O, Rueda Y. Molecular and cellular insights into the role of SND1 in lipid metabolism. Biochim Biophys Acta Mol Cell Biol Lipids. 2020;1865:158589. https://doi.org/10.1016/j.bbalip.2019.158589 .
doi: 10.1016/j.bbalip.2019.158589 pubmed: 31978555
Hwang SO, Boswell SA, Seo J-S, Lee SW. Novel oxidative stress-responsive gene ERS25 functions as a regulator of the heat-shock and cell death response. J Biol Chem. 2008;283:13063–9. https://doi.org/10.1074/jbc.M709656200 .
doi: 10.1074/jbc.M709656200 pubmed: 18326488 pmcid: 2442354
Alon A, Schmidt HR, Wood MD, Sahn JJ, Martin SF, Kruse AC. Identification of the gene that codes for the σ2 receptor. Proc Natl Acad Sci U S A. 2017;114:7160–5. https://doi.org/10.1073/pnas.1705154114 .
doi: 10.1073/pnas.1705154114 pubmed: 28559337 pmcid: 5502638
Antonicka H, Choquet K, Lin Z-Y, Gingras A-C, Kleinman CL, Shoubridge EA. A pseudouridine synthase module is essential for mitochondrial protein synthesis and cell viability. EMBO Rep. 2017;18:28–38. https://doi.org/10.15252/embr.201643391 .
doi: 10.15252/embr.201643391 pubmed: 27974379

Auteurs

Torsten Thalheim (T)

Interdisciplinary Institute for Bioinformatics (IZBI), University of Leipzig, Härtelstr. 16-18, 04107, Leipzig, Germany.
Present Address: Deutsches Biomasseforschungszentrum gGmbH, Torgauer Str. 116, 04347, Leipzig, Germany.

Marlon R Schneider (MR)

Institute of Veterinary Physiology, University of Leipzig, An den Tierkliniken 7, Leipzig, 04103, Germany. marlon.schneider@vetmed.uni-leipzig.de.

Classifications MeSH