BRCA1 deficiency in skin epidermis leads to selective loss of hair follicle stem cells and their progeny
Open accessAbstract
The accurate maintenance of genomic integrity is essential for tissue homeostasis. Deregulation of this process leads to cancer and aging. BRCA1 is a critical mediator of this process. Here, we performed conditional deletion of Brca1 during epidermal development and found that BRCA1 is specifically required for hair follicle (HF) formation and for development of adult HF stem cells (SCs). Mice deficient for Brca1 in the epidermis are hairless and display a reduced number of HFs that degenerate progressively. Surprisingly, the interfollicular epidermis and the sebaceous glands remain unaffected by Brca1 deletion. Interestingly, HF matrix transient amplifying progenitors present increased DNA damage, p53 stabilization, and caspase-dependent apoptosis compared with the interfollicular and sebaceous progenitors, leading to hyperproliferation, apoptosis, and subsequent depletion of the prospective adult HF SCs. Concomitant deletion of p53 and Brca1 rescues the defect of HF morphogenesis and loss of HF SCs. During adult homeostasis, BRCA1 is dispensable for quiescent bulge SCs, but upon their activation during HF regeneration, Brca1 deletion causes apoptosis and depletion of Brca1-deficient bulge SCs. Our data reveal a major difference in the requirement of BRCA1 between different types of epidermal SCs and progenitors and during the different activation stages of adult HF SCs.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Deficiency of BRCA1 in epidermis is associated with increased DNA damage, genome instability, loss of hair follicle stem cells, and hair follicles.
“Deficiency of BRCA1, a central protein in single-stranded and double-stranded DNA repair in epidermis is associated with increased DNA damage, genome instability, loss of hair follicle stem cells (HFSCs), and hair follicles.”
From Ultraviolet Radiation‐Induced Skin Aging: The Role of DNA Damage and Oxidative Stress in Epidermal Stem Cell Damage Mediated Skin Aging (2016) · cites this paper as [78]
Defects from BRCA1 deficiency appeared to be the result of activated p53, since deletion of p53 offset the effects of BRCA1 loss.
“Defects appeared to be the result of activated p53, since deletion of p53 offset the effects of BRCA1 loss [78].”
From Ultraviolet Radiation‐Induced Skin Aging: The Role of DNA Damage and Oxidative Stress in Epidermal Stem Cell Damage Mediated Skin Aging (2016) · cites this paper as [78]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Genome maintenance mechanisms for preventing cancer
Hoeijmakers, J. H. J. (2001) · Nature · doi:10.1038/35077232 · Cited by 3,939 · see citing works
Molecular Mechanisms of Mammalian DNA Repair and the DNA Damage Checkpoints
Sancar, A., Lindsey-Boltz, L. A., Ünsal-Kaçmaz, K., & Linn, S. (2004) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.73.011303.073723 · Cited by 3,317 · see citing works
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M., & Costantini, F. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-4 · Cited by 3,121 · see citing works
Hoeijmakers, J. H. J. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804615 · Cited by 2,239 · see citing works
Defining the Epithelial Stem Cell Niche in Skin
Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., & Fuchs, E. (2004) · Science · doi:10.1126/science.1092436 · Cited by 2,031 · see citing works
Self-citationTranscriptional control of human p53-regulated genes
Riley, T., Sontag, E., Chen, P., & Levine, A. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2395 · Cited by 1,921 · see citing works
The DNA Damage Response: Ten Years After
Harper, J. W., & Elledge, S. J. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.11.015 · Cited by 1,705 · see citing works
53BP1 Inhibits Homologous Recombination in Brca1-Deficient Cells by Blocking Resection of DNA Breaks
Bunting, S. F., Callén, E., Wong, N., Chen, H.-T., Polato, F., Gunn, A., Bothmer, A., Feldhahn, N., Fernandez-Capetillo, O., Cao, L., et al. (2010) · Cell · doi:10.1016/j.cell.2010.03.012 · Cited by 1,671 · see citing works
Bonner, W. M., Redon, C. E., Dickey, J. S., Nakamura, A. J., Sedelnikova, O. A., Solier, S., & Pommier, Y. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2523 · Cited by 1,623 · see citing works
Double-Strand Break End Resection and Repair Pathway Choice
Symington, L. S., & Gautier, J. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132435 · Cited by 1,482 · see citing works
BRCA1 and BRCA2: different roles in a common pathway of genome protection
Roy, R., Chun, J., & Powell, S. N. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3181 · Cited by 1,479 · see citing works
Blanpain, C., Lowry, W. E., Geoghegan, A., Polak, L., & Fuchs, E. (2004) · Cell · doi:10.1016/j.cell.2004.08.012 · Cited by 1,428 · see citing works
Self-citationEpidermal homeostasis: a balancing act of stem cells in the skin
Blanpain, C., & Fuchs, E. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2636 · Cited by 1,270 · see citing works
Self-citationJonkers, J., Meuwissen, R. L. J., van der Gulden, H. M. L., Peterse, H. L., van der Valk, M., & Berns, A. J. M. (2001) · Nature Genetics · doi:10.1038/ng747 · Cited by 1,053 · see citing works
Self-citationBouwman, P., Aly, A., Escandell, J. M., Pieterse, M., Bartkova, J., van der Gulden, H., Hiddingh, S., Thanasoula, M., Kulkarni, A., Yang, Q., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1831 · Cited by 1,001 · see citing works
Self-citationDNA Repair, Genome Stability, and Aging
Lombard, D. B., Chua, K. F., Mostoslavsky, R., Franco, S., Gostissa, M., & Alt, F. W. (2005) · Cell · doi:10.1016/j.cell.2005.01.028 · Cited by 944 · see citing works
Schultz, L. B., Chehab, N. H., Malikzay, A., & Halazonetis, T. D. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.7.1381 · Cited by 897 · see citing works
A single type of progenitor cell maintains normal epidermis
Clayton, E., Doupé, D. P., Klein, A. M., Winton, D. J., Simons, B. D., & Jones, P. H. (2007) · Nature · doi:10.1038/nature05574 · Cited by 853 · see citing works
Epidermal Stem Cells of the Skin
Blanpain, C., & Fuchs, E. V. (2006) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.22.010305.104357 · Cited by 845 · see citing works
Self-citationXu, X., Ohler, Z. W., Linke, S. P., Li, C., Gotay, J., Wang, X. W., Harris, C. C., Ried, T., & Deng, C. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80466-9 · Cited by 819 · see citing works
<i>Lgr6</i> Marks Stem Cells in the Hair Follicle That Generate All Cell Lineages of the Skin
Snippert, H. J., Haegebarth, A., Kasper, M., Jaks, V., van Es, J. H., Barker, N., van de Wetering, M., van den Born, M., Begthel, H., Vries, R. G., et al. (2010) · Science · doi:10.1126/science.1184733 · Cited by 751 · see citing works
Vasioukhin, V., Degenstein, L., Wise, B., & Fuchs, E. (1999) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.96.15.8551 · Cited by 691 · see citing works
Hematopoietic Stem Cell Quiescence Promotes Error-Prone DNA Repair and Mutagenesis
Mohrin, M., Bourke, E., Alexander, D., Warr, M. R., Barry-Holson, K., Le Beau, M. M., Morrison, C. G., & Passegué, E. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.06.014 · Cited by 599 · see citing works
Distinct contribution of stem and progenitor cells to epidermal maintenance
Mascré, G., Dekoninck, S., Drogat, B., Youssef, K. K., Brohée, S., Sotiropoulou, P. A., Simons, B. D., & Blanpain, C. (2012) · Nature · doi:10.1038/nature11393 · Cited by 567 · see citing works
Self-citationMorris, R. J., Bortner, C. D., Cotsarelis, G., Reece, J. M., Trempus, C. S., Faircloth, R. S., & Tennant, R. W. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12088.x · Cited by 567 · see citing works
Hair follicle stem cells are specified and function in early skin morphogenesis
Nowak, J. A., Polak, L., Pasolli, H. A., & Fuchs, E. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.05.009 · Cited by 554 · see citing works
DNA‐damage repair; the good, the bad, and the ugly
Hakem, R. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.15 · Cited by 547 · see citing works
Lrig1 Expression Defines a Distinct Multipotent Stem Cell Population in Mammalian Epidermis
Jensen, K. B., Collins, C. A., Nascimento, E. M., Tan, D. W., Frye, M., Itami, S., & Watt, F. M. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.04.014 · Cited by 523 · see citing works
BRCA1 and its toolbox for the maintenance of genome integrity
Huen, M. S. Y., Sy, S. M.-H., & Chen, J. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2831 · Cited by 495 · see citing works
BRCA1 tumour suppression occurs via heterochromatin-mediated silencing
Zhu, Q., Pao, G. M., Huynh, A. M., Suh, H., Tonnu, N. U., Nederlof, P. M., Gage, F. H., & Verma, I. M. (2011) · Nature · doi:10.1038/nature10371 · Cited by 486 · see citing works
Liu, X., Holstege, H. H., van der Gulden, H. M. L., Treur-Mulder, M., Zevenhoven, J., Velds, A., Kerkhoven, R. M., van Vliet, M. H., Wessels, L. F. A., Peterse, J. L., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702969104 · Cited by 474 · see citing works
Self-citationLichti, U. F., Anders, J., & Yuspa, S. H. (2008) · Nature Protocols · doi:10.1038/nprot.2008.50 · Cited by 442 · see citing works
Hyperproliferation and Defects in Epithelial Polarity upon Conditional Ablation of α-Catenin in Skin
Vasioukhin, V., Bauer, C., Degenstein, L., Wise, B., & Fuchs, E. (2001) · Cell · doi:10.1016/s0092-8674(01)00246-x · Cited by 435 · see citing works
NFATc1 Balances Quiescence and Proliferation of Skin Stem Cells
Horsley, V., Aliprantis, A. O., Polak, L., Glimcher, L. H., & Fuchs, E. (2008) · Cell · doi:10.1016/j.cell.2007.11.047 · Cited by 424 · see citing works
DNA damage and ageing: new-age ideas for an age-old problem
Garinis, G. A., van der Horst, G. T. J., Vijg, J., & H.J. Hoeijmakers, J. (2008) · Nature Cell Biology · doi:10.1038/ncb1108-1241 · Cited by 366 · see citing works
DNA-Damage Response in Tissue-Specific and Cancer Stem Cells
Blanpain, C., Mohrin, M., Sotiropoulou, P. A., & Passegue, E. A. (2011) · Cell stem cell · doi:10.1016/j.stem.2010.12.012 · Cited by 350 · see citing works
Self-citationLhx2 Maintains Stem Cell Character in Hair Follicles
Rhee, H. H., Polak, L., & Fuchs, E. V. (2006) · Science · doi:10.1126/science.1128004 · Cited by 345 · see citing works
BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair
Chapman, J. R., Sossick, A. J., Boulton, S. J., & Jackson, S. P. (2012) · Journal of Cell Science · doi:10.1242/jcs.105353 · Cited by 327 · see citing works
The Basement Membrane of Hair Follicle Stem Cells Is a Muscle Cell Niche
Fujiwara, H., Ferreira, M. M., Donati, G., Marciano, D. K., Linton, J. M., Sato, Y., Hartner, A., Sekiguchi, K., Reichardt, L. F., & Watt, F. M. (2011) · Cell · doi:10.1016/j.cell.2011.01.014 · Cited by 317 · see citing works
Self-citationRottenberg, S., Nygren, A. O. H., Pajic, M., van Leeuwen, F. W. B., van der Heijden, I., van de Wetering, K., Liu, X., de Visser, K. E., Gilhuijs, K. G. A., van Tellingen, O., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702955104 · Cited by 303 · see citing works
Self-citationBRCA1-Dependent Ubiquitination of γ-Tubulin Regulates Centrosome Number
Starita, L. M., Machida, Y., Sankaran, S., Elias, J. E., Griffin, K., Schlegel, B. P., Gygi, S. P., & Parvin, J. D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.19.8457-8466.2004 · Cited by 302 · see citing works
Cao, L., Li, W., Kim, S., Brodie, S. G., & Deng, C.-X. (2003) · Genes & Development · doi:10.1101/gad.1050003 · Cited by 293 · see citing works
The BRCA1/BARD1 Heterodimer Modulates Ran-Dependent Mitotic Spindle Assembly
Joukov, V., Groen, A. C., Prokhorova, T. A., Gerson, R. S., White, E. R., Rodriguez, A., Walter, J. C., & Livingston, D. M. (2006) · Cell · doi:10.1016/j.cell.2006.08.053 · Cited by 280 · see citing works
THE ELECTRON MICROSCOPY OF THE HUMAN HAIR FOLLICLE
Birbeck, M. S. C., & Mercer, E. H. (1957) · The Journal of Cell Biology · doi:10.1083/jcb.3.2.203 · Cited by 280 · see citing works
Milyavsky, M., Gan, O. I., Trottier, M., Komosa, M., Tabach, O., Notta, F., Lechman, E. R., Hermans, K. G., Eppert, K., Konovalova, Z., et al. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.05.016 · Cited by 280 · see citing works
Sotiropoulou, P. A., Candi, A., Mascré, G., Clercq, S. D., Youssef, K. K., Lapouge, G., Dahl, E., Semeraro, C., Denecker, G., Marine, J., et al. (2010) · Nature Cell Biology · doi:10.1038/ncb2059 · Cited by 245 · see citing works
Self-citationDiamond, I., Owolabi, T., Marco, M., Lam, C. W. K., & Glick, A. (2000) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2000.00144.x · Cited by 238 · see citing works
The multiple nuclear functions of BRCA1: transcription, ubiquitination and DNA repair
Starita, L. M. (2003) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(03)00042-5 · Cited by 234 · see citing works
Nijhof, J. G. W., Braun, K. M., Giangreco, A., van Pelt, C., Kawamoto, H., Boyd, R. L., Willemze, R., Mullenders, L. H. F., Watt, F. M., de Gruijl, F. R., et al. (2006) · Development · doi:10.1242/dev.02443 · Cited by 211 · see citing works
Linking the Cellular Functions ofBRCAGenes to Cancer Pathogenesis and Treatment
Venkitaraman, A. R. (2008) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev.pathol.3.121806.151422 · Cited by 199 · see citing works
Martin, R. W., Orelli, B. J., Yamazoe, M., Minn, A. J., Takeda, S., & Bishop, D. K. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0290 · Cited by 177 · see citing works
THE ELECTRON MICROSCOPY OF THE HUMAN HAIR FOLLICLE
Birbeck, M. S. C., & Mercer, E. H. (1957) · The Journal of Cell Biology · doi:10.1083/jcb.3.2.223 · Cited by 114 · see citing works
O’Guin, W. M., Sun, T., & Manabe, M. (1992) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12494172 · Cited by 114 · see citing works
Luna‐Vargas, M. P. A., Christodoulou, E., Alfieri, A., van Dijk, W. J., Stadnik, M., Hibbert, R. G., Sahtoe, D. D., Clerici, M., Marco, V. D., Littler, D. R., et al. (2011) · Journal of Structural Biology · doi:10.1016/j.jsb.2011.03.017 · Cited by 110 · see citing works
Development and Homeostasis of the Skin EpidermisPreprint
Sotiropoulou, P., & Blanpain, C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008383 · Cited by 103 · see citing works
Self-citationPulvers, J. N., & Huttner, W. Β. (2009) · Development · doi:10.1242/dev.033498 · Cited by 77 · see citing works
Molecular Basis of the Recognition of Nephronectin by Integrin α8β1
Sato, Y., Uemura, T., Morimitsu, K., Nishiuchi, R., Manabe, R., Takagi, J., Yamada, M., & Sekiguchi, K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m900200200 · Cited by 71 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Panich, U., Sittithumcharee, G., Rathviboon, N., & Jirawatnotai, S. (2016) · Stem Cells International · doi:10.1155/2016/7370642 · Cited by 374 · see citing works
Vitale, I., Manic, G., De Maria, R., Kroemer, G., & Galluzzi, L. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.04.006 · Cited by 361 · see citing works
Transient PLK4 overexpression accelerates tumorigenesis in p53-deficient epidermis
Serçin, Ö., Larsimont, J., Karambelas, A. E., Marthiens, V., Moers, V., Boeckx, B., Mercier, M. L., Lambrechts, D., Basto, R., & Blanpain, C. (2015) · Nature Cell Biology · doi:10.1038/ncb3270 · Cited by 164 · see citing works
Self-citationRegenerating the skin: a task for the heterogeneous stem cell pool and surrounding niche
Solanas, G., & Benitah, S. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3675 · Cited by 152 · see citing works
BRCA1185delAG tumors may acquire therapy resistance through expression of RING-less BRCA1
Drost, R., Dhillon, K. K., van der Gulden, H. M. L., van der Heijden, I., Brandsma, I., Cruz, C., Chondronasiou, D., Castroviejo‐Bermejo, M., Boon, U., Schut, E., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci70196 · Cited by 140 · see citing works
Self-citationp53/p63/p73 in the Epidermis in Health and DiseasePreprint
Botchkarev, V. A., & Flores, E. R. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a015248 · Cited by 111 · see citing works
Regulation of Recombination and Genomic MaintenancePreprint
Heyer, W. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016501 · Cited by 94 · see citing works
A matter of life and death: stem cell survival in tissue regeneration and tumour formation
Soteriou, D., & Fuchs, Y. (2018) · Nature Reviews Cancer · doi:10.1038/nrc.2017.122 · Cited by 87 · see citing works
DNA damage in aging, the stem cell perspective
McNeely, T., Leone, M., Yanai, H., & Beerman, I. (2020) · Human Genetics · doi:10.1007/s00439-019-02047-z · Cited by 52 · see citing works
Emerging roles of transit‐amplifying cells in tissue regeneration and cancer
Zhang, B., & Hsu, Y. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.282 · Cited by 44 · see citing works
Epithelial Stem Cells in Adult Skin
Tadeu, A. M. B., & Horsley, V. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00004-4 · Cited by 44 · see citing works
Ribonucleotide Excision Repair Is Essential to Prevent Squamous Cell Carcinoma of the Skin
Hiller, B., Hoppe, A., Haase, C., Hiller, C., Schubert, N., Müller, W., Reijns, M. A. M., Jackson, A. P., Kunkel, T. A., Wenzel, J., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-1099 · Cited by 42 · see citing works
Gata6 promotes hair follicle progenitor cell renewal by genome maintenance during proliferation
Wang, A. B., Zhang, Y. V., & Tumbar, T. (2016) · The EMBO Journal · doi:10.15252/embj.201694572 · Cited by 38 · see citing works
Pickholtz, I., Saadyan, S., Keshet, G. I., Wang, V. S., Cohen, R., Bouwman, P., Jonkers, J., Byers, S. W., Papa, M. Z., & Yarden, R. I. (2014) · Oncotarget · doi:10.18632/oncotarget.2582 · Cited by 28 · see citing works
Self-citationGong, G., Fan, Y., Zhang, Y., Yan, X., Li, W., Yan, X., He, L., Wang, N., Chen, O., He, D., et al. (2022) · Journal of Animal Science · doi:10.1093/jas/skac292 · Cited by 24 · see citing works
Sun, P., Watanabe, K., Fallahi, M., Lee, B., Afetian, M. E., Rhéaume, C., Wu, D., Horsley, V., & Dai, X. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311395111 · Cited by 24 · see citing works
Its written all over your face: The molecular and physiological consequences of aging skin
Lowry, W. E. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111315 · Cited by 21 · see citing works
Pulver, E. M., Mukherjee, C., van de Kamp, G., Roobol, S. J., Rother, M. B., van der Gulden, H. M. L., de Bruijn, R., Lattanzio, M. V., van der Burg, E., Drenth, A. P., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-1415 · Cited by 20 · see citing works
Self-citationRothwell, D. G., Li, Y., Ayub, M., Tate, C., Newton, G., Hey, Y., Carter, L., Faulkner, S., Moro, M., Pepper, S. D. V., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1129 · Cited by 19 · see citing works
In vivo reduction of RAD51‐mediated homologous recombination triggers aging but impairs oncogenesis
Matos-Rodrigues, G. E., Barroca, V., Muhammad, A., Dardillac, E., Allouch, A., Koundrioukoff, S., Lewandowski, D., Despras, E., Guirouilh‐Barbat, J., Frappart, L., et al. (2023) · The EMBO Journal · doi:10.15252/embj.2022110844 · Cited by 16 · see citing works
The Epithelial Stem Cell Niche in Skin
Guasch, G. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802734-9.00009-3 · Cited by 16 · see citing works
Liu, Y., Yang, S., Zeng, Y., Tang, Z., Zong, X., Li, X., Yang, C., Liu, L., Tong, X., Zhou, L., et al. (2022) · Experimental Dermatology · doi:10.1111/exd.14600 · Cited by 13 · see citing works
Waizenegger, J., Lenze, D., Luckert, C., Seidel, A., Lampen, A., & Hessel‐Pras, S. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400764 · Cited by 13 · see citing works
Markiewicz, E., & Idowu, O. C. (2022) · Clinical Cosmetic and Investigational Dermatology · doi:10.2147/ccid.s383790 · Cited by 12 · see citing works
Network-based analysis identifies key regulatory transcription factors involved in skin aging
Wang, X., Ming, K., Wang, S., Wang, J., Li, P., Tian, R., Liu, S.-Y., Cheng, X., Chen, Y., Shi, W., et al. (2023) · Experimental Gerontology · doi:10.1016/j.exger.2023.112202 · Cited by 9 · see citing works
Loss of Rad51c accelerates tumourigenesis in sebaceous glands of Trp53‐mutant mice
Tumiati, M., Hemmes, A., Uusivirta, S., Koopal, S., Kankainen, M., Lehtonen, E., & Kuznetsov, S. G. (2014) · The Journal of Pathology · doi:10.1002/path.4455 · Cited by 9 · see citing works
IRX5 promotes DNA damage repair and activation of hair follicle stem cells
Chen, J. K., Wiedemann, J., Nguyen, L. T. H., Lin, Z., Tahir, M., Hui, C., Plikus, M. V., & D, B. A. M. (2023) · Stem Cell Reports · doi:10.1016/j.stemcr.2023.03.013 · Cited by 7 · see citing works
Joint research towards a better radiation protection—highlights of the Fifth MELODI Workshop
Aerts, A., Impens, N. R. E. N., Baatout, S., Benotmane, M. A., Camps, J., Dabin, J., Derradji, H., Grosche, B., Horemans, N., Jourdain, J.-R., et al. (2014) · Journal of Radiological Protection · doi:10.1088/0952-4746/34/4/931 · Cited by 6 · see citing works
Deep Hair Phenomics: Implications in Endocrinology, Development, and Aging
Makkar, J., Flores, J., Matich, M., Duong, T. T., Thompson, S. M., Du, Y., Busch, I., Phan, Q. M., Wáng, Q., Delevich, K. M., et al. (2024) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2024.08.014 · Cited by 6 · see citing works
Genome Maintenance in Mammalian Stem Cells
Schimenti, J. C., Huang, R., Li, L., & James, R. C. (2022) · Annual Review of Genetics · doi:10.1146/annurev-genet-072920-022154 · Cited by 5 · see citing works
Epidermal Nbn deletion causes premature hair loss and a phenotype resembling psoriasiform dermatitis
Seidel, P., Remus, M., Delacher, M., Grigaravičius, P., Reuß, D., Frappart, L., von Deimling, A., Feuerer, M., Abdollahi, A., & Frappart, P. (2016) · Oncotarget · doi:10.18632/oncotarget.8470 · Cited by 5 · see citing works
Lin, Y., Tang, W., Huang, P., Wang, Z., Duan, L., Jia, C., Sun, R., Liu, L., & Shen, J. (2023) · Developmental Dynamics · doi:10.1002/dvdy.682 · Cited by 4 · see citing works
BRCA1 preserves genome integrity during the formation of undifferentiated spermatogonia
Li, P., Song, L., Ma, L., Han, C., Li, L., Lu, L., & Liu, Y. (2025) · EMBO Reports · doi:10.1038/s44319-025-00487-5 · Cited by 3 · see citing works
Stewart, R. M., King, M. C., & Horsley, V. (2018) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-319-16769-5_11 · Cited by 1 · see citing works
Matos-Rodrigues, G. E., Barroca, V., Muhammad, A., Allouch, A., Koundrioukoff, S., Lewandowski, D., Despras, E., Guirouilh‐Barbat, J., Frappart, L., Kannouche, P. L., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.17.476609 · Cited by 1 · see citing works
RAD51C IS A TUMOR SUPPRESSOR IN MAMMARY AND SEBACEOUS GLANDS
Tumiati, M. (2015) · Työväentutkimus Vuosikirja
Pulver, E. M., Mukherjee, C., van de Kamp, G., Roobol, S. J., Rother, M. B., van der Gulden, H. M. L., de Bruijn, R., Lattanzio, M. V., van der Burg, E., Drenth, A. P., et al. (2023) · doi:10.1158/0008-5472.c.6513568.v1
Self-citationDiscussion on Targeted Regulation Strategy of Scalp Sub-Health
梁, 嘉. (2024) · Advances in Clinical Medicine · doi:10.12677/acm.2024.14112929
Ferdousi, L. V. (2014) · theses.fr (ABES) · doi:10.70675/9d73199ez7949z4602zadcfz6763e4bdd1b0
Implication of DNA damage and repair in viability and differentiation of muscle stem cells
Sutcu, H. H. (2018) · theses.fr (ABES) · doi:10.70675/16d90ec5z5de0z495fzb8c9zc61a837a276b
Régulation des étapes précoces de la recombinaison homologue humaine par BRCA2 et RAD52
Muhammad, A. (2021) · theses.fr (ABES) · doi:10.70675/2a4e3f69zfa80z4fbcz832fzafaf38393628
RhoA WT allele loss unleashes the cancer driver function of RhoA E40Q
Noujarède, J., Wang, Q., Kokkinogenis, E., Luo, Y., Cudina, I., Willaume, S., Mooser, C., Nguyen, L. P., Poulsen, M. F., Heijmerikx, S., et al. (2026) · Journal of Clinical Investigation · doi:10.1172/jci201975
- Authors
- Sotiropoulou, P. A., Karambelas, A. E., Debaugnies, M., Candi, A., Bouwman, P., Moers, V., Revenco, T., Rocha, A. S., Sekiguchi, K., Jonkers, J., & Blanpain, C.
- Affiliations
- Université Libre de Bruxelles (BE)
- The Netherlands Cancer Institute (NL)
- The University of Osaka (JP)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2012-12-27
- Volume
- 27
- Issue
- 1
- Pages
- 39-51
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC3553282
- OpenAlex
- W2124543958
- Cited by
- 42
- References
- 57
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 5 · 2022: 5 · 2021: 2 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 4 · 2014: 8 · 2013: 1
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- OUKA (Osaka University Knowledge Archive) (Osaka University) (submittedVersion)
- Funders
- Fonds De La Recherche Scientifique - FNRS
- Walloon excellence in life sciences and biotechnology
- Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture
- Topics
- Health Sciences › Medicine › Urology › Hair Growth and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › dental development and anomalies
- Keywords
- BRCA1, hair follicle stem cells, epidermis, conditional gene deletion, hair follicle morphogenesis, DNA damage, p53, caspase-dependent apoptosis, bulge stem cells, hair follicle regeneration, genome stability, skin homeostasis
- MeSH terms
- Epidermal Cells, Animals, DNA Damage, Epidermis, Stem Cells, Tumor Suppressor Protein p53, Apoptosis, Gene Deletion, Mice, Knockout, Hair Follicle, BRCA1 Protein, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
