Monoclonal Antibodies Reveal Dynamic Plasticity Between Lgr5- and Bmi1-Expressing Intestinal Cell Populations

Nicholas R. Smith1, John R. Swain1, Paige S. Davies1, Alexandra C. Gallagher1, Michael S. Parappilly1, Catherine Z. Beach1, Philip R. Streeter2,3, Ian A. Williamson4, Scott T. Magness4, Melissa H. Wong1,3
1Department of Cell, Developmental and Cancer Biology, Oregon Health & Science University, Portland, Oregon
2Department of Pediatrics, Oregon Health & Science University, Portland, Oregon
3Oregon Health & Science University Stem Cell Center, Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon
4Department of Biomedical Engineering, Department of Medicine, Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina

Tài liệu tham khảo

Sato, 2011, Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts, Nature, 469, 415, 10.1038/nature09637 Farin, 2012, Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells, Gastroenterology, 143, 1518, 10.1053/j.gastro.2012.08.031 Aoki, 2016, Foxl1-expressing mesenchymal cells constitute the intestinal stem cell niche, Cell Mol Gastroenterol Hepatol, 2, 175, 10.1016/j.jcmgh.2015.12.004 Barker, 2007, Identification of stem cells in small intestine and colon by marker gene Lgr5, Nature, 449, 1003, 10.1038/nature06196 Montgomery, 2011, Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells, Proc Natl Acad Sci U S A, 108, 179, 10.1073/pnas.1013004108 Powell, 2012, The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor, Cell, 149, 146, 10.1016/j.cell.2012.02.042 Sangiorgi, 2008, Bmi1 is expressed in vivo in intestinal stem cells, Nat Genet, 40, 915, 10.1038/ng.165 Takeda, 2011, Interconversion between intestinal stem cell populations in distinct niches, Science, 334, 1420, 10.1126/science.1213214 Basak, 2014, Mapping early fate determination in Lgr5+ crypt stem cells using a novel Ki67-RFP allele, EMBO J, 33, 2057, 10.15252/embj.201488017 Cheng, 1974, Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types, Am J Anat, 141, 537, 10.1002/aja.1001410407 Potten, 1974, Continuous labelling studies on mouse skin and intestine, Cell Tissue Kinet, 7, 271 Li, 2010, Coexistence of quiescent and active adult stem cells in mammals, Science, 327, 542, 10.1126/science.1180794 Kondo, 2003, Biology of hematopoietic stem cells and progenitors: implications for clinical application, Annu Rev Immunol, 21, 759, 10.1146/annurev.immunol.21.120601.141007 Li, 2014, Single-cell analysis of proxy reporter allele-marked epithelial cells establishes intestinal stem cell hierarchy, Stem Cell Rep, 3, 876, 10.1016/j.stemcr.2014.09.011 Jadhav, 2017, Dynamic reorganization of chromatin accessibility signatures during dedifferentiation of secretory precursors into Lgr5+ intestinal stem cells, Cell Stem Cell, 21, 65, 10.1016/j.stem.2017.05.001 Tian, 2011, A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable, Nature, 478, 255, 10.1038/nature10408 Yan, 2012, The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations, Proc Natl Acad Sci U S A, 109, 466, 10.1073/pnas.1118857109 Smith, 2016, Defining a stem cell hierarchy in the intestine: markers, caveats and controversies, J Physiol, 594, 4781, 10.1113/JP271651 Buczacki, 2013, Intestinal label-retaining cells are secretory precursors expressing Lgr5, Nature, 495, 65, 10.1038/nature11965 Tetteh, 2016, Replacement of lost Lgr5-positive stem cells through plasticity of their enterocyte-lineage daughters, Cell Stem Cell, 18, 203, 10.1016/j.stem.2016.01.001 van Es, 2012, Dll1+ secretory progenitor cells revert to stem cells upon crypt damage, Nat Cell Biol, 14, 1099, 10.1038/ncb2581 Yan, 2017, Intestinal enteroendocrine lineage cells possess homeostatic and injury-inducible stem cell activity, Cell Stem Cell, 21, 78, 10.1016/j.stem.2017.06.014 Sato, 2009, Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche, Nature, 459, 262, 10.1038/nature07935 Smith, 2017, Cell adhesion molecule CD166/ALCAM functions within the crypt to orchestrate murine intestinal stem cell homeostasis, Cell Mol Gastroenterol Hepatol, 3, 389, 10.1016/j.jcmgh.2016.12.010 Hosen, 2007, Bmi-1-green fluorescent protein-knock-in mice reveal the dynamic regulation of bmi-1 expression in normal and leukemic hematopoietic cells, Stem Cells, 25, 1635, 10.1634/stemcells.2006-0229 Madisen, 2010, A robust and high-throughput Cre reporting and characterization system for the whole mouse brain, Nat Neurosci, 13, 133, 10.1038/nn.2467 Dorrell, 2011, Isolation of mouse pancreatic alpha, beta, duct and acinar populations with cell surface markers, Mol Cell Endocrinol, 339, 144, 10.1016/j.mce.2011.04.008 Williams, 1992, Subtractive immunization techniques for the production of monoclonal antibodies to rare antigens, Biotechniques, 12, 842 Levin, 2010, Characterization of the intestinal cancer stem cell marker CD166 in the human and mouse gastrointestinal tract, Gastroenterology, 139, 2072, 10.1053/j.gastro.2010.08.053 Magness, 2013, A multicenter study to standardize reporting and analyses of fluorescence-activated cell-sorted murine intestinal epithelial cells, Am J Physiol Gastrointest Liver Physiol, 305, G542, 10.1152/ajpgi.00481.2012 von Furstenberg, 2011, Sorting mouse jejunal epithelial cells with CD24 yields a population with characteristics of intestinal stem cells, Am J Physiol Gastrointest Liver Physiol, 300, G409, 10.1152/ajpgi.00453.2010 Mahe, 2013, Establishment of gastrointestinal epithelial organoids, Curr Protoc Mouse Biol, 3, 217, 10.1002/9780470942390.mo130179 Gracz, 2015, A high-throughput platform for stem cell niche co-cultures and downstream gene expression analysis, Nat Cell Biol, 17, 340, 10.1038/ncb3104 Wang, 2013, Isolation and characterization of intestinal stem cells based on surface marker combinations and colony-formation assay, Gastroenterology, 145, 383, 10.1053/j.gastro.2013.04.050 Stelzner, 2012, A nomenclature for intestinal in vitro cultures, Am J Physiol Gastrointest Liver Physiol, 302, G1359, 10.1152/ajpgi.00493.2011 Binnerts, 2007, R-Spondin1 regulates Wnt signaling by inhibiting internalization of LRP6, Proc Natl Acad Sci U S A, 104, 14700, 10.1073/pnas.0702305104 de Lau, 2011, Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling, Nature, 476, 293, 10.1038/nature10337 Kim, 2005, Mitogenic influence of human R-spondin1 on the intestinal epithelium, Science, 309, 1256, 10.1126/science.1112521 Itzkovitz, 2011, Single-molecule transcript counting of stem-cell markers in the mouse intestine, Nat Cell Biol, 14, 106, 10.1038/ncb2384 Munoz, 2012, The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4' cell markers, EMBO J, 31, 3079, 10.1038/emboj.2012.166 Gregorieff, 2015, Yap-dependent reprogramming of Lgr5(+) stem cells drives intestinal regeneration and cancer, Nature, 526, 715, 10.1038/nature15382 Fordham, 2013, Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury, Cell Stem Cell, 13, 734, 10.1016/j.stem.2013.09.015 Mustata, 2013, Identification of Lgr5-independent spheroid-generating progenitors of the mouse fetal intestinal epithelium, Cell Rep, 5, 421, 10.1016/j.celrep.2013.09.005 Gjorevski, 2016, Designer matrices for intestinal stem cell and organoid culture, Nature, 539, 560, 10.1038/nature20168