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Intestinal label-retaining cells are secretory precursors expressing Lgr5
Abstract
The rapid cell turnover of the intestinal epithelium is achieved from small numbers of stem cells located in the base of glandular crypts. These stem cells have been variously described as rapidly cycling or quiescent. A functional arrangement of stem cells that reconciles both of these behaviours has so far been difficult to obtain. Alternative explanations for quiescent cells have been that they act as a parallel or reserve population that replace rapidly cycling stem cells periodically or after injury; their exact nature remains unknown. Here we show mouse intestinal quiescent cells to be precursors that are committed to mature into differentiated secretory cells of the Paneth and enteroendocrine lineage. However, crucially we find that after intestinal injury they are capable of extensive proliferation and can give rise to clones comprising the main epithelial cell types. Thus, quiescent cells can be recalled to the stem-cell state. These findings establish quiescent cells as an effective clonogenic reserve and provide a motivation for investigating their role in pathologies such as colorectal cancers and intestinal inflammation.
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“interconversion of reserve and active intestinal stem cell (ISC) populations has also been observed previously25,28–30.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [25]
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Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,893
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 12,082
Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J., et al. (2009) · Nature · doi:10.1038/nature07935 · Cited by 7,204
limma: Linear Models for Microarray Data
Smyth, G. K. (2005) · Statistics for Biology and Health · doi:10.1007/0-387-29362-0_23 · Cited by 5,796
Identification of stem cells in small intestine and colon by marker gene Lgr5
Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J., et al. (2007) · Nature · doi:10.1038/nature06196 · Cited by 5,687
Summaries of Affymetrix GeneChip probe level data
Irizarry, R. A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gng015 · Cited by 4,837
Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Gentleman, R. C., Carey, V. J., Huber, W. K., Irizarry, R. A., & Dudoit, S. (2005) · Statistics in the health sciences · doi:10.1007/0-387-29362-0 · Cited by 3,470
Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts
Sato, T., van Es, J. H., Snippert, H. J., Stange, D. E., Vries, R. G., van den Born, M., Barker, N., Shroyer, N. F., van de Wetering, M., & Clevers, H. (2011) · Nature · doi:10.1038/nature09637 · Cited by 2,510
Snippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A. M., van Rheenen, J., Simons, B. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.09.016 · Cited by 1,951
Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt
Potten, C. S., & Loeffler, M. (1990) · Development · doi:10.1242/dev.110.4.1001 · Cited by 1,793
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An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control
Clevers, H. C., Loh, K. M., & Nusse, R. (2014) · Science · doi:10.1126/science.1248012 · Cited by 1,386
Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration
Barker, N. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3721 · Cited by 1,424
Extracellular matrix: A dynamic microenvironment for stem cell niche
Gattazzo, F., Urciuolo, A., & Bonaldo, P. (2014) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2014.01.010 · Cited by 1,365
Single-cell messenger RNA sequencing reveals rare intestinal cell types
Grün, D., Lyubimova, A., Kester, L., Wiebrands, K., Basak, O., Sasaki, N., Clevers, H., & van Oudenaarden, A. (2015) · Nature · doi:10.1038/nature14966 · Cited by 1,234
The intestinal crypt, a prototype stem cell compartment
Clevers, H. (2013) · Cell · doi:10.1016/j.cell.2013.07.004 · Cited by 1,223
Molecular regulation of stem cell quiescence
Cheung, T. H., & Rando, T. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3591 · Cited by 1,148
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Sato, T., & Clevers, H. (2013) · Science · doi:10.1126/science.1234852 · Cited by 1,170
Tales from the crypt: new insights into intestinal stem cells
Gehart, H., & Clevers, H. C. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0081-y · Cited by 1,046
Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites
Gerbe, F., Sidot, E., Smyth, D. J., Ohmoto, M., Matsumoto, I., Dardalhon, V., Cesses, P., Garnier, L., Pouzolles, M., Brulin, B., et al. (2016) · Nature · doi:10.1038/nature16527 · Cited by 1,002
Unravelling cancer stem cell potential
Beck, B., & Blanpain, C. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3597 · Cited by 915
Cancer Stem Cells: Basic Concepts and Therapeutic Implications
Nassar, D., & Blanpain, C. (2016) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044438 · Cited by 904
Structural Remodeling of the Human Colonic Mesenchyme in Inflammatory Bowel Disease
Kinchen, J., Chen, H. H., Parikh, K., Antanaviciute, A., Jagielowicz, M., Fawkner-Corbett, D., Ashley, N., Cubitt, L., Mellado-Gomez, E., Attar, M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.067 · Cited by 745
Reparative inflammation takes charge of tissue regeneration
Karin, M., & Clevers, H. (2016) · Nature · doi:10.1038/nature17039 · Cited by 767
Visualization and targeting of LGR5+ human colon cancer stem cells
Shimokawa, M., Ohta, Y., Nishikori, S., Matano, M., Takano, A., Fujii, M., Date, S., Sugimoto, S., Kanai, T., & Sato, T. (2017) · Nature · doi:10.1038/nature22081 · Cited by 728
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Beumer, J., & Clevers, H. C. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0278-0 · Cited by 703
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Grün, D., Muraro, M. J., Boisset, J.-C., Wiebrands, K., Lyubimova, A., Dharmadhikari, G., van den Born, M., van Es, J., Jansen, E., Clevers, H., et al. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.05.010 · Cited by 586
Yu, Z., Pestell, T. G., Lisanti, M. P., & Pestell, R. G. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.08.022 · Cited by 678
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de Lau, W., Peng, W. C., Gros, P., & Clevers, H. (2014) · Genes & Development · doi:10.1101/gad.235473.113 · Cited by 656
Lgr5 stem cells are indispensable for radiation-induced intestinal regeneration
Metcalfe, C., Kljavin, N. M., Ybarra, R., & de Sauvage, F. J. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2013.11.008 · Cited by 575
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Biton, M., Haber, A. L., Rogel, N., Burgin, G., Beyaz, S., Schnell, A., Ashenberg, O., Su, C., Smillie, C. S., Shekhar, K., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.008 · Cited by 597
Single-cell transcriptomes of the regenerating intestine reveal a revival stem cell
Ayyaz, A., Kumar, S., Sangiorgi, B., Ghoshal, B., Gosio, J., Ouladan, S., Fink, M., Barutcu, S., Trcka, D., Shen, J., et al. (2019) · Nature · doi:10.1038/s41586-019-1154-y · Cited by 593
Plasticity of epithelial stem cells in tissue regeneration
Blanpain, C., & Fuchs, E. (2014) · Science · doi:10.1126/science.1242281 · Cited by 589
Tetteh, P. W., Basak, O., Farin, H. F., Wiebrands, K., Kretzschmar, K., Begthel, H., van den Born, M., Korving, J., de Sauvage, F., van Es, J. H., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.01.001 · Cited by 575
Modeling mouse and human development using organoid cultures
Huch, M., & Koo, B. (2015) · Development · doi:10.1242/dev.118570 · Cited by 578
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Lambert, A. W., & Weinberg, R. A. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-021-00332-6 · Cited by 548
Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging
Ritsma, L., Ellenbroek, S. I. J., Zomer, A., Snippert, H. J. G., de Sauvage, F. J., Simons, B. D., Clevers, H. C., & van Rheenen, J. (2014) · Nature · doi:10.1038/nature12972 · Cited by 501
Organoids: Modeling Development and the Stem Cell Niche in a Dish
Kretzschmar, K., & Clevers, H. C. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.014 · Cited by 496
Mihaylova, M. M., Cheng, C.-W., Cao, A. Q., Tripathi, S., Mana, M. D., Bauer-Rowe, K. E., Abu-Remaileh, M., Clavain, L., Erdemir, A., Lewis, C. A., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.04.001 · Cited by 428
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Dekoninck, S., & Blanpain, C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0237-6 · Cited by 404
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Rompolas, P., Mesa, K. R., & Greco, V. (2013) · Nature · doi:10.1038/nature12602 · Cited by 409
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Vermeulen, L., Morrissey, E. R., van der Heijden, M., Nicholson, A. M., Sottoriva, A., Buczacki, S. J. A., Kemp, R., Tavaré, S., & Winton, D. J. (2013) · Science · doi:10.1126/science.1243148 · Cited by 404
Self-citationMyant, K., Cammareri, P., McGhee, E. J., Ridgway, R. A., Huels, D. J., Cordero, J. B., Schwitalla, S., Kalna, G., Ogg, E.-L., Athineos, D., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.04.006 · Cited by 391
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Westphalen, C. B., Asfaha, S., Hayakawa, Y., Takemoto, Y., Lukin, D. J., Nuber, A. H., Brandtner, A. K., Setlik, W., Remotti, H. E., Muley, A., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73434 · Cited by 400
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Hsu, Y., Li, L., & Fuchs, E. V. (2014) · Cell · doi:10.1016/j.cell.2014.02.057 · Cited by 382
Testa, U., Pelosi, E., & Castelli, G. (2018) · Medical Sciences · doi:10.3390/medsci6020031 · Cited by 401
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Merrell, A. J., & Stanger, B. Z. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.24 · Cited by 369
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Krausová, M., & Kořínek, V. (2013) · Cellular Signalling · doi:10.1016/j.cellsig.2013.11.032 · Cited by 380
Başak, O., Beumer, J., Wiebrands, K., Seno, H., van Oudenaarden, A., & Clevers, H. C. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.11.001 · Cited by 365
Parasitic helminths induce fetal-like reversion in the intestinal stem cell niche
Nusse, Y. M., Savage, A. K., Marangoni, P., Huber, A. R., Landman, T. A., de Sauvage, F. J., Locksley, R. M., & Klein, O. D. (2018) · Nature · doi:10.1038/s41586-018-0257-1 · Cited by 339
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Kabiri, Z., Greicius, G., Madan, B., Biechele, S., Zhong, Z. A., Zaribafzadeh, H., Edison, Aliyev, J., Wu, Y., Bunte, R. M., et al. (2014) · Development · doi:10.1242/dev.104976 · Cited by 351
Chen, B., Scurrah, C. R., McKinley, E. T., Simmons, A. J., Ramirez-Solano, M. A., Zhu, X., Markham, N. O., Heiser, C. N., Vega, P. N., Rolong, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.11.031 · Cited by 339
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Qi, Z., Li, Y., Zhao, B., Xu, C., Liu, Y., Li, H., Zhang, B., Wang, X., Yang, X., Xie, W., et al. (2017) · Nature Communications · doi:10.1038/ncomms13824 · Cited by 320
Mustata, R. C., Vasile, G., Vallone, V. B. F., Strollo, S., Lefort, A., Libert, F., Monteyne, D., Pérez-Morga, D. L., Vassart, G., & Garcia, M. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.09.005 · Cited by 292
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Saha, S., Aranda, E., Hayakawa, Y., Bhanja, P., Atay, S., Brodin, N. P., Li, J., Asfaha, S., Liu, L., Tailor, Y. H., et al. (2016) · Nature Communications · doi:10.1038/ncomms13096 · Cited by 284
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Stem cell dynamics in homeostasis and cancer of the intestine
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Murata, K., Jadhav, U., Madha, S., van Es, J., Dean, J., Cavazza, A., Wucherpfennig, K., Michor, F., Clevers, H., & Shivdasani, R. A. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2019.12.011 · Cited by 264
Zeng, K. X., & Hou, X. S. (2015) · Development · doi:10.1242/dev.113357 · Cited by 232
Schmitt, M., Schewe, M., Sacchetti, A., Feijtel, D., van de Geer, W. S., Teeuwssen, M., Sleddens, H. F. B. M., Joosten, R., van Royen, M. E., van de Werken, H. J. G., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.085 · Cited by 251
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Westphalen, C. B., Takemoto, Y., Tanaka, T., Macchini, M., Jiang, Z., Renz, B. W., Chen, X., Ormanns, S., Nagar, K. K., Tailor, Y. H., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.03.016 · Cited by 227
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Tian, H., Biehs, B., Chiu, C., Siebel, C. W., Wu, Y., Costa, M., de Sauvage, F. J., & Klein, O. D. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.007 · Cited by 214
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Barriga, F. M., Montagni, E., Mana, M., Méndez-Lago, M., Hernando‐Momblona, X., Sevillano, M., Guillaumet-Adkins, A., Rodríguez-Esteban, G., Buczacki, S. J. A., Gut, M., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.02.007 · Cited by 213
Self-citationMini-Gut Organoids: Reconstitution of the Stem Cell Niche
Date, S., & Sato, T. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125218 · Cited by 222
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Varga, J., & Greten, F. R. (2017) · Nature Cell Biology · doi:10.1038/ncb3611 · Cited by 209
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Willet, S. G., Lewis, M. A., Miao, Z., Liu, D., Radyk, M. D., Cunningham, R. L., Burclaff, J., Sibbel, G., Lo, H. G., Blanc, V., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201798311 · Cited by 203
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Wang, Y., Chiang, I.-L., Ohara, T. E., Fujii, S., Cheng, J., Muegge, B. D., Heul, A. V., Han, N. D., Lu, Q., Xiong, S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.10.015 · Cited by 200
Signaling in the stem cell niche: regulating cell fate, function and plasticity
Chacón‐Martínez, C. A., Koester, J., & Wickström, S. A. (2018) · Development · doi:10.1242/dev.165399 · Cited by 197
Sancho, R., Cremona, C. A., & Behrens, A. (2015) · EMBO Reports · doi:10.15252/embr.201540188 · Cited by 210
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Sugimoto, S., Ohta, Y., Fujii, M., Matano, M., Shimokawa, M., Nanki, K., Date, S., Nishikori, S., Nakazato, Y., Nakamura, T., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2017.11.012 · Cited by 196
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Imajo, M., Ebisuya, M., & Nishida, E. (2014) · Nature Cell Biology · doi:10.1038/ncb3084 · Cited by 201
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Sada, A., Jacob, F., Leung, E. Y., Wang, S. S., White, B. S., Shalloway, D. I., & Tumbar, T. (2016) · Nature Cell Biology · doi:10.1038/ncb3359 · Cited by 197
Reserve Stem Cells in Intestinal Homeostasis and Injury
Bankaitis, E. D., Ha, A., Kuo, C. J., & Magness, S. T. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.08.016 · Cited by 193
Wnt signaling in cancer stem cells and colon cancer metastasis
Basu, S., Haase, G., & Ben‐Ze'ev, A. (2016) · F1000Research · doi:10.12688/f1000research.7579.1 · Cited by 189
Herring, C. A., Banerjee, A., McKinley, E. T., Simmons, A. J., Ping, J., Roland, J. T., Franklin, J. L., Liu, Q., Gerdes, M. J., Coffey, R. J., et al. (2017) · Cell Systems · doi:10.1016/j.cels.2017.10.012 · Cited by 181
Human enteroids as an ex-vivo model of host–pathogen interactions in the gastrointestinal tract
Foulke-Abel, J., In, J., Kovbasnjuk, O., Zachos, N. C., Ettayebi, K., Blutt, S. E., Hyser, J. M., Zeng, X.-L., Crawford, S. E., Broughman, J. R., et al. (2014) · Experimental Biology and Medicine · doi:10.1177/1535370214529398 · Cited by 179
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Melo, F. D. S. E., & de Sauvage, F. J. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.11.019 · Cited by 184
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Metadata
- Authors
- Buczacki, S. J. A., Zecchini, H. I., Nicholson, A. M., Russell, R., Vermeulen, L., Kemp, R., & Winton, D. J.
- Affiliations
- Cancer Research UK (GB)
- Corresponding author
- Winton, Douglas J.
- Venue
- Nature
- Published
- 2013-02-27
- Volume
- 495
- Issue
- 7439
- Pages
- 65-69
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2119059014
- Semantic Scholar
- 9cc05a3e71ae9af40d9b1e9b30a463e557747415
- Cited by
- 761
- References
- 39
- Citations by year
- 2026: 20 · 2025: 39 · 2024: 35 · 2023: 34 · 2022: 42 · 2021: 65 · 2020: 65 · 2019: 41 · 2018: 85 · 2017: 68 · 2016: 67 · 2015: 73 · 2014: 76 · 2013: 49
- FWCI
- 58.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Funders
- Cancer Research UK (17044, 22310)
- Topics
- Health Sciences › Medicine › Gastroenterology › Digestive system and related health
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Keywords
- label-retaining cells, Lgr5, Paneth cells, enteroendocrine cells, intestinal epithelial regeneration, intestinal injury, stem cell niche, lineage tracing, intestinal crypts, colorectal cancer, intestinal inflammation
- MeSH terms
- Animals, Cell Differentiation, Cell Division, Cell Separation, Clone Cells, Intestinal Neoplasms, Intestines, Regeneration, Staining and Labeling, Biomarkers, Cell Lineage, Paneth Cells, Multipotent Stem Cells, Receptors, G-Protein-Coupled, Mice, Stem Cell Niche
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